genetic variation in wild plants and animals in sweden · genetic variation in wild plants and ......

Genetic variation in wild plants and

animals in SwedenA review of case studies from the

perspective of conservation genetics

REPORT 5786 • JAN 2008

Chromosome Copy of the chromosome

Cell

Cell nucleus

Mitochondria

Nuclear DNA

Mitochondrial DNA

Supportive proteins

Base pairs

Genetic variation in wild plantsand animals in Sweden

A review of case studies from the perspective of conservation genetics

Anna-Carin LundqvistDepartment of Evolution Genomics and Systematics

Evolutionary Functional GenomicsUppsala University

Stefan AnderssonDepartment of Ecology

Plant Ecology and Systematics Lund University

Mikael LönnSchool of Life Sciences

Molecular EcologySödertörn University College

SWEDISH ENVIRONMENTAL PROTECTION AGENCY

OrdersPhone: + 46 (0)8-505 933 40

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The Swedish Environmental Protection AgencyPhone: + 46 (0)8-698 10 00, Fax: + 46 (0)8-20 29 25

E-mail: [email protected]: Naturvårdsverket, SE-106 48 Stockholm, Sweden

Internet: www.naturvardsverket.se

ISBN 978-91-620-5786-2.pdfISSN 0282-7298

© Naturvårdsverket 2007

Tryck: CM Digitaltryck AB, Bromma 2008Layout: Naturvårdsverket and Press Art

Cover photos: Chromosome, illustration: Anna-Carin Lundqvist.

Wolf (Canis lupus) photo: Myra bildbyrå. Field fleawort (Tephroseris integrifolia) photo: Björn Widén

Permission to publish Figure 2 is given by Wiley-Blackwell(Oxford, UK) and for the remaining photos from the

respective photographer or company.

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SWEDISH ENVIRONMENTAL PROTECTION AGENCYReport 5786 • Genetic variation in natural populations of animals and plants in Sweden

Preface

This overview was initiated to get an updated report on what is known aboutthe genetic variation of wild populations of plants and animals in Sweden.The project was part of a government commission to the Swedish Environ-mental Protection Agency to suggest an action programme for conservationof genetic variation in wild plants and animals in Sweden. This is part of thework to achieve the national environmental quality objective A rich diversityof plant and animal life (http://miljomal.nu/english/english.php) which wasadopted by the Swedish Parliament in 2005. The overview has been writtenby Dr Anna-Carin Lundqvist (Department of Evolution, Genomics and Syste-matics, Uppsala University), and Associated Professors Stefan Andersson(Dept. of Plant Ecology and Systematics, Lund University) and Mikael Lönn(School of Life Sciences, Södertörn University College, Stockholm), with Seni-or Adviser Per Sjögren-Gulve (The Wildlife Management Unit of the SwedishEPA) as project leader and managing editor. The views presented in thisreport are those of the authors and should not be taken as those of the Swe-dish EPA.

The overview is written for managers and decision-makers working withnatural resources, nature- and species-conservation, and sustainable develop-ment, at central and local government agencies, ministries, in municipalitiesand in non-governmental organizations. Chapter 1 explains the focus of thereport and gives a brief background relating to basic population genetics.Chapter 2 describes positive outcomes associated with conserving geneticvariation. Chapters 3-7 review patterns in the genetic variation of wild plantsand animals in Sweden, and relevant underlying processes, on the basis ofselected themes with particular relevance to biodiversity conservation. Eachchapter starts with a summary, followed by a general review of the internatio-nal literature in the area and by illustrative examples, primarily using Swedishcase studies. Chapter 8 then discusses important principles and analyses thatneed to be considered in a genetic monitoring programme, and chapter 9 pre-sents the conclusions from the overview.

The overview has been peer reviewed by senior scientists and a draft wasdiscussed and reviewed by scientists and managers in a reference group and ata seminar. The Swedish EPA thanks all who have contributed in the processand hopes that the report will provide useful insights and examples for thework with conservation of ecosystems, species, populations and genetic varia-tion, in Europe and other parts of the world.

Stockholm, December 2007

Björn RisingerHead of the Dept. of Natural Resources

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Contents

PREFACE 3

CONTENTS 4

SUMMARY 7

1. BACKGROUND 121.1 The aim and focus of the report 131.2 Basic theory of population genetics 15

2. BENEFITS OF GENETIC DIVERSITY 172.1 Why should we conserve genetic variation? 172.2 The positive effects of genetic variation at the population, community and ecosystem levels 19

3. LOSS OF GENETIC DIVERSITY IN SMALL POPULATIONS 233.1 Loss of genetic variation on the individual level 24

3.1.1 Studies of natural populations 263.2 Effects on fertility and viability 29

3.2.1 The effects on fertility and viability in natural populations 303.3 The effects of loss of genetic variation on the long term ability to adapt 32

3.3.1 Studies investigating the effects on long term adaptive abilities in naturalpopulations 33

4. GENETIC DIVERSITY AFTER GENE FLOW AND HYBRIDISATION 354.1 Hybridisation and gene flow in theory 364.2 Hybridisation and gene flow in natural populations 37

4.2.1 Hybrid fitness 374.2.2 Gene flow and hybridisation after environmental disturbance 384.2.3 Genetic contamination by introduced species or genotypes 384.2.4 Outbreeding depression and genetic assimilation 424.2.5 Transgenes and heterosis effects 44

4.3 Importance for the formation of species and conservation values 444.4 Genetic aspects of restoration and supplementation projects 45

5. GENETIC EFFECTS OF HARVESTING 48

6. GENETIC DIVERSITY AND CHANGE OF HABITAT AND CLIMATE 526.1 Local adaptation 52

6.1.1 Transplantation experiments 536.1.2 Genetic differences between environments – molecular genetic markers 546.1.3 Genetic differentiation between environments – quantitative characters 56

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6.1.4 The possibility of future adaptations 586.2 Local adaptation in association with changes of distribution and climate 596.3 Marginal and central populations 61

7. GENETICALLY DISTINCT POPULATIONS IN SWEDEN 637.1 Genetic or taxonomic variation? 647.2 The conservation value of Scandinavian populations 66

7.2.1 Endemism in Scandinavian vascular plants 687.2.2 Genetic studies of terrestrial plants and animals 687.2.3 Genetic studies of aquatic plants and animals 72

7.3 Research progress and continued lack of knowledge 72

8. GENETIC MONITORING 758.1 Which taxa are in need of genetic monitoring? 768.2 Genetic monitoring – theory and practice 79

8.2.1 General principles of a genetic monitoring programme 798.2.2 Identifying populations showing negative population trends 808.2.3 Genetic monitoring in practice 80

9. CONCLUSIONS 83

10. ACKNOWLEDGEMENTS 87

11. REFERENCES 88

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Summary

By ratifying the Convention of Biological Diversity, Sweden has agreed toconserve the biological diversity at the ecosystem, species and genetic levels.One common assumption is that the conservation of ecosystems and habitatsalso conserves species, and that the conservation of species also conservesgenetic diversity. However, there is a growing realization that the conserva-tion of species does not necessarily conserve the genetic diversity within speci-es. Until now, the conservation of genetic resources has attracted relativelylittle attention in practical nature conservation.

In recent years several scientists have argued that the conservation of bio-logical diversity should focus on preventing the disappearance of geneticallydistinct populations rather than to solely prevent the extinction of species. Toconserve genetically distinct populations could be a better way of conservingthe evolutionarily potential of species. This will also reduce the risk that spe-cies go extinct, even in a longer time perspective.

In 2006, The Swedish Environmental Protection Agency received agovernment commission to develop a national action plan for the conserva-tion of genetic diversity in wild plants and animals, in consultation with theSwedish Board of Agriculture, the Swedish Forest Agency, the Swedish Boardof Fisheries and the Swedish University of Agricultural Sciences. This reportconstitutes a part of this work and is the internationally adapted version ofthe original report in Swedish, published in 2007 (Andersson et al. 2007).The objective of the report is to characterize the genetic variation in Swedishpopulations of wild plant and animals from the perspective of several themes.These themes were chosen to illustrate general issues currently identified inthe international research field of conservation genetics, exemplified withrelevant genetic studies of Swedish organisms.

The aim of this report is not to summarize all studies of genetic variationof wild animals and plants performed in Sweden. Studies performed before1997 have been reviewed in two earlier reports, one about genetic monitoring(Laikre & Ryman 1997) and the other about genetically distinct populationsin Sweden (Lönn et al. 1998). These reports are still of immediate importan-ce. Because of the amount of genetic research performed in Sweden and othercountries, the present report is not an exhaustive review of all recent progressin the field. Instead it focuses on illustrative examples and on relevant proces-ses that may change the genetic diversity of wild populations in Sweden.

Benefits of genetic variation. The genetic differentiation between individu-als is the basis of evolution and adaptation. If all individuals of a species wereidentical, the species could not adapt genetically to a changing environmente.g. climate change anticipated due to anthropogenic emissions of greenhousegases. To measure genetic variation and relate it to evolutionary change andecological function in wild populations is challenging. Recently, some studieshave revealed direct effects associated with the genetic variation of a popula-tion. A review summarising the results from several plant-studies shows a

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positive correlation between population size, genetic variation and differentmeasures of viability and fertility. Experiments with artificial plant communi-ties having different levels of genetic diversity have also produced evidence.Eelgrass stands consisting of many genotypes were less sensitive to environ-mental change, grew denser, and had larger numbers of small animals associ-ated with them than stands with low levels of genetic diversity.

Human activities may have negative consequences for the genetic diversi-ty, and consequently for the adaptive potential, of wild populations. Regard-less of whether the genetic variation is useful or not in the present-day popu-lations, we cannot anticipate which traits will be essential for survival in arapidly changing environment.

Loss of genetic diversity in small populations. Decreasing population sizeis a problem for many animals and plants that inhabit areas affected byhuman activities. Small isolated populations are expected to lose geneticdiversity through local random processes (genetic drift). Loss of genetic diver-sity may ultimately have effects on the ability to cope with environmentalchanges (evolutionary potential). Studies show that many populations are sosmall and isolated that they will be affected by the loss of genetic diversity.Furthermore, populations with low genetic diversity may have reduced fertili-ty and viability either as a result of inbreeding, or because valuable alleleshave been lost. Several studies suggest that a few immigrants are sufficient toeliminate or reduce the negative effects of inbreeding. However, so far it isdifficult to draw general conclusions about how the loss of genetic diversityaffects the long-term evolutionary potential of populations.

Genetic diversity after gene flow and hybridisation. Although anthropo-genic habitat fragmentation usually causes negative isolation effects, humanactivities may also result in increased gene flow between natural populationsof animals or plants. A too extensive or too distant gene flow can have nega-tive effects on the recipient populations. Occasionally, human activities haveincreased the gene flow by creating zones or ”hybrid environments” wheregenetically dissimilar populations or closely related species can meet andexchange genes. In several species it is known that genes from introduced ordomesticated species have spread to Swedish populations, as in the cases ofthe mountain hare (genes from the brown hare) and two subspecies of theplant lucerne (genes from the cultivated Medicago sativa spp. sativa to thewild relative sickle medick M. sativa spp. falcata). There is only sporadicknowledge about gene flow that occurs when alien populations of trees, birdsand fish are released into the wild and come into contact with indigenouspopulations, or when foreign grass seeds are sown on road verges. Studies ofsalmon show that gene flow can be harmful by creating hybrids with lowlevels of viability and fertility (i.e. outbreeding depression). In other casesgene flow has been so intense that the genetic integrity of species is threatenedas in the case of the low-density populations of the plant Viola alba on theisland of Öland, a species that easily hybridises with other related species.Sometimes populations with the capability to invade natural ecosystems havebeen created due to human-mediated hybridisation between closely relatedspecies. Potentially negative effects of gene flow must also be taken into con-

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sideration in conservation biology, e.g. when populations are supplementedwith individuals raised in captivity or with individuals from distant popula-tions.

Genetic effects of harvesting. Many Swedish animal and plant species areexposed to regular harvesting, such as fishing, hunting and forestry. Harves-ting is expected to increase the random loss of genetic variation by decreasingthe effective population size. In a study of cod (Gadus morhua), local harves-ting led to increased migration of individuals (and genes) from nearby popu-lations, which also resulted in a change of the large-scale pattern of geneticvariation. There are many examples of harvested animal populations thathave undergone directional evolution as a result of selective harvesting. Inseveral cases this change has decreased the ability for the population to reco-ver after a period of intense harvesting.

Genetic diversity and change of habitat and climate. Local adaptationoccurs when populations become genetically adapted to different environ-ments. Generally, the ability to adapt is larger the more genetic variation ispresent in a population. There are many examples of species in Sweden withlocally adapted populations in certain environments, e.g. the rough periwink-le (Littorina saxatilis), the common mussel (Mytilus edulis), herring (Clupeaharengus), three-spined stickle-back (Gasterosteus aculeatus), Scots pine(Pinus sylvestris) and white clover (Trifolium repens). Local adaptation impli-es that individuals from different populations are not interchangeable –locally adapted populations have a conservation value of their own. For thisreason, local adaptation is an important issue in e.g. reintroduction and sup-plementation strategies. For each type of adaptation, specific genetic varia-tion is needed. How this variation is distributed and exchanged betweenpopulations through gene flow is largely unknown.

Genetically distinct populations in Sweden. There are few endemic taxa atthe species level in Sweden, and those that exist have arisen relatively recentlythrough local processes such as hybridisation and polyploidisation. At thesame time there are many genetically distinct populations in Sweden. Popula-tions are different due to different origins and colonisation routes or becausethey are adapted to their local environments. Taxonomic units as species,varieties and forms, together with informal genetic entities such as evolutio-nary significant units and management units reflect genetic differentiationthat has arisen within or outside the borders of Sweden. Genetically differen-tiated groups can be difficult to distinguish morphologically (they are cryp-tic), but molecular genetic studies have provided strong evidence for ”hid-den” genetic structure in Swedish taxa. Lönn et al. (1998) called attention tothe fact that populations with their main distribution in Sweden are not mar-ginal populations from a genetic perspective. In contrast, species that aremainly distributed in southern areas and are represented by marginal popula-tions in Sweden are less genetically variable in this region. In many cases,Swedish populations are as genetically diverse as the populations in areas thatwere not covered with ice during the last glaciation. This pattern is also con-firmed by more recent studies. Furthermore, recent investigations also verifythat populations from the islands Öland and Gotland, the Baltic Sea with the

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surrounding coastal areas, the mountain areas and some traditionally mana-ged landscapes, are genetically distinct. Each population that is lost meansloss of genetic variation and consequently loss of adaptive potential. For thepurpose of conserving genetic resources, populations or groups of popula-tions are the natural conservation units, because genetic variation occurs bothwithin and between populations.

Genetic monitoring. The need for a genetic monitoring programme inSweden was the main conclusion by Laikre & Ryman (1997). We concur thata centrally organised genetic monitoring programme is still needed. Our sug-gestion is largely based on the proposal made in 1997 and is meant as anupdated starting point for more detailed discussions of programme design.We propose that the monitoring programme should focus on six differenttypes of taxa (species or groups of populations within species), for exampletaxa with negative population trends and taxa that are harvested by humans.One of the most important issues for the monitoring programme is toestablish procedures for collecting and storing different types of biologicalmaterial, e.g. tissue samples, which can be used in genetic investigations. It isvery important that the storing of the biological material does not in any waylimit which methods that can be used in future investigations. We suggest theestablishment of a common database for biological material stored in diffe-rent museums, and we also suggest a formalised system where researchers canreport when collected biological material no longer can be stored locally andtherefore could be offered to the museums.

Lack of knowledge and suggestion for research areas. In spite of the factthat many genetic studies have been performed within the focal research fieldof this report, we have identified several issues with significant knowledgegaps. We would like to see more genetic research regarding the followinggeneral questions:

(i) Global warming is likely to result in large changes for Swedish popula-tions and ecosystems. Processes like gene flow and local adaptation will beimportant for Swedish populations in order to meet these changes. We needmore knowledge to address questions such as: What role may geneticallydistinct populations in Sweden play to enable species to meet large-scale cli-matic and environmental changes? Is there sufficient genetic variation in rele-vant ecological traits to enable species to adapt to rapidly changing environ-ments? Which populations are most valuable in this respect – central popula-tions or those at the periphery of the distribution? Is there a risk that geneti-cally distinct populations will disappear in those habitats that supposedly willbe most affected by global warming? Which genetic methods are most rele-vant for assessing evolutionary potential? How will genetic variation of keyspecies in important Swedish ecosystems affect the function, species composi-tion and stability of these ecosystems?

(ii) It is important to understand how the human-mediated gene flowaffects the gene pool of the genetically distinct populations present in Sweden.What genetic effect does the release of alien populations that takes place ine.g. the forestry and fisheries have? How will grass-species of natural grass-lands be affected by the gene flow from foreign provenances sown on road

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verges? When is it appropriate to supplement small or inbred populations, orpopulations that are poorly adapted to a changing environment? When willsuch measures be harmful? From which populations should the individualsused in the supplementation be taken?

(iii) There are several scientific questions that are in need of answers whendeveloping a genetic monitoring programme. One of the most central ques-tions is: How can we differentiate natural changes in genetic diversity fromthe un-natural, which might constitute a threat to the genetic diversity?

What should the national action plan include? The national action planfor conserving genetic diversity in wild plants and animals in Sweden shouldfirst and foremost include a genetic monitoring programme and also prioriti-se the suggested research areas. Furthermore we suggest that the action planproposes guidelines for how to deal with genetic problems in monitoredpopulations and in the supplementation of wild populations, an action alrea-dy suggested in several of the recovery and action plans for red-listed speciesin Sweden. The national action plan should also aim to develop guidelinesand effective systems for the registration of the release of alien populationsthat take place e.g. in forestry, fish management and in road management.

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1. Background

Conservation and sustainable use of biological diversity is presently a politi-cal objective for many countries in the world. The International Union for theConservation of Nature and Natural Resources (IUCN) identifies three levelsof biological diversity that are equally important to conserve: ecosystem, spe-cies and genetic diversity (McNeely et al. 1990). The UN Convention of Bio-logical Diversity (CBD) makes a similar classification. Until now, the conser-vation of genetic resources has attracted relatively little attention in practicalnature conservation. One common assumption is that the conservation ofecosystems and habitats also conserves species, and that the conservation ofspecies also conserves genetic diversity. However, there is a growing realiza-tion that the conservation of species does not necessarily conserve the geneticdiversity within them. Within the CBD there is an agreement to work fromthe general perspective of the ecosystem level. They suggest that the biologicaldiversity should be viewed from the landscape perspective, which also inclu-des socio-economic factors, but emphasize that this does not contradictactions directed to conserve biological diversity on either the species or thegenetic levels.

Genetic differences between individuals are the basis of evolution andadaptation. If all individuals of a species were identical the evolution wouldbe disabled, all individuals would for example be equally sensitive to a certaindisease or would react to an environmental change in the same way. As a con-sequence the species could not adapt genetically to a changing environmente.g. climate change due to anthropogenic emissions of greenhouse gases. Inspite of the limited attention the conservation of genetic diversity has receivedwithin practical conservation biology, knowledge of the importance of gene-tic variation for the survival of species is far from new. Already Darwin(1896) understood the importance of genetic variation when he pointed outthat the reason why deer in British parks were in bad condition was becausethey were kept in small isolated populations (see also Allendorf & Luikart2007). However, it was not until after 70 years the actual debate about theconservation of genetic resources started with a paper in the journal “Gene-tics” (1974) by Otto Frankel, an agricultural plant geneticist. Frankle (1974)argued that because we cannot anticipate what the future world will looklike, we cannot predict which traits the organisms will need to survive there.For this reason it is vital that the level of genetic variation within species isconserved so evolution may continue (Frankel 1974; see also Allendorf &Luikart 2007).

In a society with limited economical resources, conservation actions oftenare weighted against each other and against other interest of society. Whichspecies should we conserve? Should the economic resources be used to con-serve natural habitats instead of species? In recent years several scientists haveargued that the conservation of biological diversity should focus on preven-ting the disappearance of genetically distinct populations rather than to solely

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prevent the extinction of species (Hughes et al. 1997; Hobbs & Mooney1998). To conserve genetically distinct populations could be a better way ofconserving the evolutionarily potential of species. This will also reduce therisk that species go extinct, even in a longer time perspective (Allendorf &Luikart 2007).

A population focus in conservation biology suggests that Sweden togetherwith the other Nordic countries share a common responsibility to conservethe populations in this area. Many species also present in continental Europeare in Sweden represented by so-called marginal populations – populations atthe edge of their distributions. These populations are often genetically distinctand are therefore essential to protect if we aim to conserve the evolutionarypotential of a particular species.

The importance of conserving genetic diversity is emphasised in one of theSwedish environmental objectives “A Rich Diversity of Plant and AnimalLife”, which was adopted by the Swedish parliament in November 2005. In2006, the Swedish Environmental Protection Agency received a governmentcommission to develop a national action plan for the conservation of geneticdiversity in wild plants and animals, in consultation with the Swedish Boardof Agriculture, the Swedish Forest Agency, the Swedish Board of Fisheriesand the Swedish University of Agricultural Sciences. This report constitutes apart of this work and is the internationally adapted version of the originalreport in Swedish, published in 2007 (Andersson et al. 2007).

1.1 The aim and focus of the reportThe objective of this report is to characterize the genetic variation in Swedishpopulations of wild plant and animals from the perspective of several themes.These themes were chosen to illustrate general issues currently identified inthe international research field of conservation genetics, exemplified withrelevant genetic studies of Swedish organisms. In this section we describe thebackground and aim of this report in more detail.

Even if the genetic aspect of practical conservation biology has not alwaysbeen prioritised, the question has attracted some attention in the SwedishEnvironmental Protection Agency since the late 1990s. At that time tworeports were published that reviewed the genetic variation of natural plantsand animals in Sweden from two, slightly different, perspectives.

The first report discusses the monitoring of biodiversity at the gene level(Laikre & Ryman 1997), and suggests an action plan and a research pro-gramme to ensure that the genetic diversity of Swedish organisms is conser-ved. The authors emphasise the need for long-term studies of natural fluctua-tions of genetic variation to be able to differentiate between natural and un-natural changes of genetic diversity. The report also lists practically allmolecular genetic studies of natural plants and animals in Sweden, performeduntil November 1996. The list was created in part through literature searchesin databases of scientific studies and in part by a questionnaire sent directly tovarious research institutes, and identifies 316 studies. Although many studies

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of genetic variation of Swedish organisms exist, Laikre & Ryman (1997)emphasise that these studies are not necessarily useful when for exampleassessing the conservation status of a species from a genetic perspective.

The second report discusses the genetic distinctness of Swedish popula-tions of natural plants and animals in relation to populations in other Euro-pean areas (Lönn et al. 1998). This report reviews mainly molecular, but alsosome quantitative genetic studies, and presents many studies illustrating thatSwedish populations are genetically distinct. Lönn et al. (1998) describe seve-ral geographic areas in Sweden that contain many genetically distinct (mostlyplant) populations: the mountain areas, the Baltic Sea with the surroundingcoastal areas, the Baltic sea islands Öland and Gotland and some traditio-nally managed landscapes. Because taxonomic and genetic variation does notalways coincide, the authors stress the importance of performing genetic stu-dies in order to discover genetic distinctness.

These two reports refer to a large number of genetic studies of naturalplant and animal populations in Sweden, and together they provide an exhau-stive review of the genetic studies published before 1997. Both reports arestill of immediate importance, because much of the information in them hasnot significantly changed over time.

Since 1997 a large number of genetic studies of wild organisms in Swedenhas been published. Previous to writing the present report, a literature searchin three different databases of scientific studies (Biological Abstacts, ISI Webof Knowledge, CSA Illumina) was performed for the years 1996 to November2006, using the same key words as in Laikre & Ryman (1997). The searchresulted in the identification of 844 studies of genetic variation of Swedishorganisms. However, the aim of the present report is not to summarize all stu-dies of genetic variation of wild animals and plants performed in Sweden sin-ce 1997. For some organism groups, or specific questions, reviews of thiskind are already published. For example a report of genetic research of com-mercially exploited fish species in the Nordic countries was published recent-ly by the Nordic Council of Ministers (Olsson et al. 2007). Other reportsdiscuss the problem of release of genetically alien populations in Sweden(Laikre & Palmé 2005; Laikre et al. 2006) and research concerning ecologicaleffects of genetically modified organisms (Palm & Ryman 2006). The presentreport is instead a complement to these more detailed reports, and focus onthe processes that modify the genetic variation of natural populations descri-bed from a Swedish perspective. Genetic variation of Swedish natural popula-tions of plants and animals is described from the perspective of several the-mes, chosen to demonstrate what problems and general threats to their gene-tic diversity that natural populations presently are facing. Each chapter corre-sponds to a theme, and opens with a short summary followed by someinformation about the theoretical background and results from internationalresearch, after which examples are provided of Swedish research relevant tothe issue at hand. Some of the questions addressed in this report, and discus-sed from the perspective of Swedish genetic studies, are:• Why do species need genetic variation?• What is the effect of small population size on genetic diversity?

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• What are the negative consequences of gene flow and hybridisation?• Can harvesting of natural populations, for example by fishing and hun-

ting, have genetic consequences• How will the ongoing climate changes affect natural populations in Swe-

den?• What should the national action plan for the conservation of genetic

diversity in wild plants and animals in Sweden include?

1.2 Basic theory of population geneticsThe present report is the English adaptation of a report previously publishedin Swedish by the Swedish Environmental Protection Agency (Andersson etal. 2007). In addition to the objective of describing problems and generalthreats to the genetic diversity of Swedish plants and animals, the originalreport also had a second equally important aim – to give a presentation (inSwedish) of relevant parts of the basic theory of population genetics for peo-ple who are less familiar with the subject, or those who wished to renew theirtheoretical knowledge (Figure 1). The Swedish version of this report alsoincluded an appendix where the most common molecular genetic methodswere described, summarising the advantages and drawbacks of currentmolecular methods. The reason for not including these parts in the internatio-nally adapted version of the report is that there are several excellent books inEnglish, describing basic population genetic theory, evolutionary processesand current molecular methods. If you are interested in this subject or wantto renew your theoretical background we recommend you to read for examp-le “Conservation and the Genetic of Populations” (Allendorf & Luikart2007) or “Introduction to Conservation Genetics” (Frankham et al. 2005), orsome other textbook of the subject.

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Chromosome Copy of the chromosome

Cell

Cell nucleus

Mitochondria

Nuclear DNA

Mitochondrial DNA

Supportive proteins

Base pairs

Figure 1. In an animal cell DNA is found in the nucleus of the cell and in the mitochondria (the“power plants” of all eukaryotic cells). In a plant cell DNA can also be found in the chloroplasts.Nuclear DNA is accumulated in chromososomes, which consist of a extremely long DNA moleculeswrapped around different types of proteins. During most of the cell cycle, the chromosomes aregenerally loosly packed, and are streched out in long threadlike formations in the cell nucleus.Before cell division, the DNA is replicated to create identical copies of all the chromososmes. Afterthe replication all chromosomes condense, i.e. they are tightly packed around the supportive prote-ins. At this time the chromosome can be stained and studied using a microscope. Becaue the origi-nal chromosome and its identical copy are attached to each other, the condensed chromosomeoften has a characteristic X-shape.Mitochondrial DNA (mtDNA) is a circular molecule that exists in several copies inside eachmitochondrion. The organisation of mtDNA is not as well known as nuclear DNA. A study of humanmitochondria demonstrated that one or probably several mtDNA molecules are loosely organisedtogether with (unknown) proteins into loosely packed structures (Garrido et al. 2003).Illustration: A-C Lundqvist. The illustration is rewritten and modified from an illustration on thehomepage, www.genome.gov (The National Human Genome Research Institute, NHGRI, Educatio-nal resources, Talking glossary)

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2. Benefits of genetic diversity

2.1 Why should we conserve genetic variation?Genetic differentiation between individuals is the basis for the evolutionarychange of species, populations and lineages. In which way a population orspecies will change is determined by natural selection – individuals with cer-tain traits will survive to a greater degree and/or will produce more offspring.This evolution will result in a slightly altered genetic composition of the spe-cies or population. A species or population may also evolve genetically due toa random process, genetic drift. Random genetic drift changes the frequencyof alleles (alternative forms of a gene) between generations; some alleles willdecrease in frequency while other will become more common, only dependingon random effects during the formation of gametes (e.g. egg or sperm cells).However, random genetic drift generally is a weak force and evolutionthrough this process will not modify a population to any great extent. Thiswill require a directed force such as natural selection.

Evolutionary change requires modification of genes or gene combina-tions. The functions of existing alleles are changed through mutation orrecombination. Favourable mutations may enable the organisms to better uti-lise the existing environment – predators may develop the ability for morerapid attacks, whereas prey might develop a more acute sense for detectingthe predators.

If the environment changes, for example if a predator invades a new habi-tat or if the climate suddenly changes, yet another situation can arise. Allelesthat previously were neutral or had a small effect on the reproductive successof the individuals suddenly can become important. Alleles controlling frosttolerance will be of no importance in an environment that never experiencestemperatures below zero, but can rapidly become important if the climate

Summary:The genetic differentiation between individuals is the basis of evolu-tion and adaptation. To measure genetic variation and relate it to evo-lutionary change and ecological function in wild populations is chal-lenging. Recently, some studies have revealed direct effects associatedwith the genetic variation of a population. A review summarising theresults from several plant-studies shows a positive correlation betweenpopulation size, genetic variation and different measures of viabilityand fertility. Experiments with artificial plant communities with diffe-rent levels of genetic diversity have also produced evidence. Eelgrassstands consisting of many genotypes were less sensitive to environ-mental change, grew denser, and had larger numbers of small animalsassociated with them than stands with low levels of genetic diversity.

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suddenly turns colder. Nevertheless, obtaining useful genetic variationthrough mutation is a very slow process. Consequently, the probability that apopulation will survive a forthcoming environmental change will increase themore alleles that are present in the population because some of the allelesmight be useful just by chance.

It is impossible to anticipate which alleles will be needed for a species tosurvive in the future. Obviously, the probability that a population or specieshas the required allele increases with the amount of genetic variation that ispresent in the population. For a specific population to survive, at least oneindividual (but preferably many individuals) must possess the allele. In thesame way, for a species the allele has to be present in at least one of the popu-lations. If only one or a few populations possess the necessary allele, otherpopulations can receive it through gene flow or because a population disap-pears and is replaced by individuals from another more viable populationpossessing the allele. However, the more populations that have the requiredallele the better – the distance between populations can some times be consi-derable and for many organisms dispersal is limited to small distances (10-1000 meters; see Edenhamn et al. 1999). It is essential to possess many alleles(high allelic richness), but it is also important that the different alleles are rea-sonably common (high levels of allele diversity), because that decreases theprobability that alleles are lost through random processes.

To measure genetic variation and relate it to evolutionary change and eco-logical function in wild populations is challenging. First, the genotypes of theindividuals in the populations under study must be known. Second, an envi-ronmental change affecting the success of the studied alleles must occur(because it is not possible to study all alleles at all loci in a population). Afterthat the relative success of the different populations or lineages can be evalua-ted based on their genetic variation previous to the environmental change.

Genetic variation present in a population today may not be entirely bene-ficial in the current environment. A few alleles may be directly harmful forthe individuals carrying the alleles under the present circumstances. Severalexamples of this have been recorded in natural populations, when organismshave adapted rapidly to "unexpected" environmental changes, as for exampledeposits of toxic heavy metals or other pollutants. Frankham & Kingsolver(2004) review a number of scientific studies demonstrating this phenomenonin natural populations. One classical example is colour adaptation in the pep-pered moth (Biston betularia), a species that resides on the trunks of light-coloured trees in Britain. During the industrial revolution pollution discolou-red the trees, and the dark colour of the trunks was reflected in an increasedproportion dark-coloured moths. The dark, melanistic, variants of the mothwere disadvantaged when the tree trunks were pale, but natural selectionmade the alleles causing the melanistic form much more common because theenvironment had changed. Years later, when the pollution was less pronoun-ced the light-coloured moths became more common once more, at the expen-se of the darker variant.

Several examples from other groups of organisms also show this pheno-menon. In many cases, plants that grow in localities where mining residues

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are deposited will adapt to the high levels of heavy metals and become resi-stant to them. Also, Swedish populations of the moor frog (Rana arvalis)have rapidly adapted to the acidified environment caused by atmospheric pol-lution (Räsänen et al. 2003). However, this is not true for all species andpopulations, because some of them lack the alleles that enable adaptation tothe novel environment (Davies 1993).

In general, natural populations show high levels of genetic variation whi-ch can be expressed if the selection pressures changes. Plant and animal bree-ding are based on this genetic variation. By artificially altering the selectionpressure (this corresponds to an environmental change) populations rapidlygain traits because some of the alleles are “favoured”. One experiment usingfruit flies (Drosophila melanogaster) showed that populations kept in anunpredictable environment were more successful when they were exposed toan environmental change compared with populations that had been kept in astable environment (Reed et. al. 2003). The authors suggest that populationskept in a variable environment have the possibility to maintain higher levelsof genetic diversity and will consequently have the capacity to face unknownenvironmental changes.

2.2 The positive effects of genetic variation at the population, community and ecosystemlevelsBenefits of genetic variation can be shown for example by the ability of diffe-rent populations to adapt to their local environment; this will be discussed ina different section (Chapter 6). The main focus of the present section is studi-es examining the level of genetic variability within species or populations (i.e.genetic diversity of populations).

If we assume that the levels of genetic variation shown by molecular mar-kers reflect the variation of the entire genome, the benefits of genetic varia-tion can be studied indirectly using molecular markers. A meta-analysis (asummarising analysis of the results of several scientific studies) showed thatpopulation size, genetic variability and different fitness related traits (fertilityand viability) all were positively correlated with each other. Thus, in this stu-dy the benefit of genetic variation was demonstrated by its positive associa-tion with fitness. The authors stress that because population size and geneticvariability also are positively correlated, habitat fragmentation may pose arisk to the genetic diversity of populations, as a consequence of the reducedpopulations size and limited gene flow between the subpopulations (Leimu etal. 2006).

Recently, a newly emerged research field termed “community genetics”has received some scientific attention. Community genetics is the study ofhow the genetic variability of one species in a community or ecosystem,affects other species or ecosystem functions. To investigate if the genetic vari-ation of the eelgrass (Zostera marina), a dominant plant in shallow waters,

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would have an effect on the function of the entire ecosystem, Reusch et al.(2005) performed a manipulative field experiment in the Baltic Sea. Eelgrasswas planted in three different groups either consisting of one, three or six eel-grass genotypes. During the experiment, a natural period of extremely high(for the eelgrass close to lethal) water temperatures occurred. Thus, the expe-riment also reflected the resistance to environmental stress of the manipulatedeelgrass communities. The results showed that eelgrass in communities consi-sting of several different genotypes grew at a higher density and producedmore biomass than those with lower diversity. Genetically variable communi-ties performed better, either because the different genotypes facilitated theirmutual growth or because the different genotypes utilised the environment inslightly different ways. Genetically more variable eelgrass communities werealso associated with a greater number of small animals, which are a valuablefood source for larger animals in the ecologically important eelgrass eco-systems. This study shows that genetic variation of a species can have far-reaching consequences both for other species and for the entire ecosystem.

For individual organisms, the importance of genetic variation can bedemonstrated by the fact that different genotypes do not have identical fitnessin different environments – this is the basis of natural selection. At the popu-lation level, the importance of genetic variation can be shown by demonstra-ting that the success of a population depends on the genetic variability withinthe population. In a study of the fastigiate gypsophila (Gypsophila fastigiata),a rare plant in the genus baby’s breath on the Baltic island of Öland, the gene-tic variation was compared between different subpopulations from differentareas in the regional population (Lönn & Prentice 2002). After correcting sta-tistically for geographic position of the subpopulations, it was shown thatgenetically more variable subpopulations displayed a higher frequency ofyoung individuals, but did not show an elevated number of dead individuals,which indicates that these populations are expanding at the expense of othersubpopulations. This can be explained by the fact that in the genetically morevariable populations, each individual displays higher levels of genetic varia-tion (are heterozygous at a large number of loci), which in turn enables eachindividual to survive in areas showing a wide span of environmental varia-tion. Another explanation could be that each genetically variable populationcan generate many different genotypes, which together can utilise the envi-ronment throughout the entire distribution area in a more effective way.

In a manipulative field experiment performed on an English grassland,genetic variation was found to be an important issue for plant communitydiversity (Booth & Grime 2003). In this experiment, the ten most commonspecies were used to construct artificial plant communities with three levels ofgenetic diversity. Each species was represented either by a number of geneti-cally identical individuals (1 genotype) or by a number of individuals of 4 dif-ferent genotypes, or by individuals with unique genotypes (16 different geno-types). The results demonstrated that the genetically variable artificial plantcommunities were able to recreate plant communities resembling the naturalgrassland. In contrast, the artificial plant communities where each speciesconsisted of genetically identical individuals were very different from each

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other, and from the original grassland, even after a long time period (Figure2). These results indicate that different genotypes may have a different func-tion in the interaction between species, and the authors suggest that a matureplant society not only has a certain species composition, but also a specificcomposition of genotypes.

Furthermore, the species diversity declined much more slowly in the gene-tically variable artificial plant communities, which might be due to decreasedcompetition between the different species or an elevated resistance to disease.

Figure 2. Ordination of the species composition over 5 years in 36 artificial plant communities.Each diagram shows a principal component analysis. An ordination arranges object according tolikeness. The closer the dots are to each other the more the species composition in the differentcommunities resembles each other. White triangles = communities where each species is represen-ted by 16 genotypes; grey squares = 4 genotypes; black diamonds = 1 genotype. From: Booth, R. E.& Grime J. P. (2003): Effects of genetic impoverishment on plant community diversity. Journal ofEcology 91: 721-730. Copyright and permission to publish: Wiley-Blackwell, Oxford.

Prentice et al. (2006) observed a related process at the species level, study-ing the quaking-grass (Briza media) on the Baltic island of Öland (Figure 3).The study area is a grassland with a continuity of up to 300 years. Popula-tions of quaking-grass were found to be genetically more similar (measuredwith allozymes) the longer the grassland continuity at the specific localitywas. The authors suggest that the environment and the species compositionbecome more homogenous in areas with long grassland continuity, and thatspecific genotypes might be better adapted to that plant community (i.e.directional selection may favour optimal genotypes over time).

One of the main conclusions both from Booth & Grime (2003) and Pren-tice et al. (2006) is that it seems to matter which genotypes represent a speciesin a community. Therefore, it is important to consider the genotypes of indivi-duals in conservation actions such as habitat restorations, or when predictingchanges in the distribution of species or in studies of community and eco-system processes.

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Figure 3. Quaking-grass (Briza media) is a characteristic grass species in pastures in Sweden.(Photo: Myra bildbyrå)

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3. Loss of genetic diversity insmall populations

Most natural populations have at least moderate levels of genetic diversity – abasic condition to enable species and populations to adapt to the present andfuture changes of the environment. Since the 1980s conservation biologyoften has focused on the loss of genetic variation that is expected in small iso-lated populations or populations experiencing "bottlenecks" – time periodswhen the size of the population is very small. Loss of genetic diversity haslong been considered as a problem mostly concerning rare plants and ani-mals, but this loss can also – and sometimes to a greater degree – have aneffect on common species with large populations, especially species affectedby the ongoing fragmentation of the landscape (Ellstrand & Elam 1993;Frankham 1995a; Young et al. 1996). In addition, low levels of genetic diver-sity can often be observed in populations inhabiting areas that were recoloni-sed only after the latest ice age (Hewitt 1996).

Populations can show low levels of genetic diversity or be geneticallyimpoverished in different ways: (1) many alleles may have become rare or areabsent from the gene pool because of genetic drift; (2) the proportion ofhomozygotes may have increased at the expense of the heterozygotes due to

Summary:Decreasing population size is a problem for many animals and plantsthat inhabit areas affected by human activities. In this chapter wediscuss the effect of loss of genetic diversity in small isolated popula-tions due to local random processes (genetic drift). In the beginning ofthe chapter we consider the loss of genetic diversity at the individuallevel, which can be studied using different molecular methods. Then wediscuss how loss of genetic diversity in a population may ultimatelyhave effects on its viability, fertility and ability to cope with environ-mental changes (evolutionary potential). Each section starts with ashort theroetical backgroud followed by examples from empirical stu-dies, focusing on studies of Swedish plant and animals.

Studies show that many populations are so small and isolated thatthey will be affected by the loss of genetic diversity. Furthermore,populations with low genetic diversity may have reduced fertility andviability either as a result of inbreeding, or because valuable alleleshave been lost. Several studies suggest that a few immigrants are suffi-cient to eliminate or reduce the negative effects of inbreeding. Howe-ver, so far it is difficult to draw general conclusions about how the lossof genetic diversity affects the long-term evolutionary potential ofpopulations.

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inbreeding in the population; (3) the gene pool may be fixed for alleles thatdecrease the viability and fertility of the individuals or the population.

3.1 Loss of genetic variation on the individual level Many populations are so small that a random process, genetic drift, has a sig-nificant impact on the number of alleles that are passed on to the next genera-tion. Genetic drift has two major consequences: the frequencies of the diffe-rent alleles will fluctuate between generations, and the population will loosegenetic variation. Initially, the rare alleles will be lost, and with time the ave-rage heterozygosity (the allele diversity) will decrease. Genetic diversity willdecrease within the populations while the genetic differences between thepopulations may increase or decrease, depending on whether the randomgenetic drift acts in the same or opposite directions in different populations.The genetic diversity (both the loss of rare alleles and the average heterozygo-sity) within the populations will decrease at a rate inversely proportional tothe effective population size (Ne). The average heterozygosity within thepopulation is expected to decrease at rate of 1/2Ne per generation (Box 1).This loss will continue until the gene pool is fixed for one allele or until anequilibrium arises between the loss of genetic variation and creation of gene-tic variation through mutations (Wright 1931; Kimura 1968).

The effect of genetic drift is easiest to illustrate with an example of apopulation that has gone through a short period of small population size. If alarge population decreased to an effective size of Ne = 20 individuals, andmaintained this size for five generations, the population is expected to have88 % of the allele diversity (expected heterozygosity) present before the sizereduction. If the population instead decreased to an effective size of one indi-vidual (Ne = 1), and that individual establishes a new population throughself-fertilization, this population is expected to retain only half of the originalallele diversity of the first generation of the bottleneck. An extreme bottle-neck, like the latter example, will also drastically reduce the number of alle-les, because one diploid individual can only pass on at most two differentalleles at each locus to the next generation. In general, it is the rare alleles thatwill be lost in bottlenecks (Nei et al. 1975).

Only a small amount of gene flow (gametes, pollen, migrating individuals)is needed to counteract the loss of genetic diversity in a population. In agroup of populations exchanging genes between each other from time to timean equilibrium is expected to arise, where the effects of genetic drift arebalanced by mutations and gene flow. This equilibrium is expected to arisequickly for the various estimates of genetic differentiation between popula-tions (GST, FST), but more slowly for estimates of genetic diversity withinpopulations (allele diversity). As a consequence, estimates of allele diversityof populations in a recently fragmented landscape will indicate their larger“historical” population sizes and the estimates of allele diversity will decrease


further, before an equilibrium between gene flow and mutations will bereached (Wright 1931; Varvio et al. 1986).

Box 1: Loss of genetic variationIn all finite populations, genetic drift is expected to decrease the geneticvariation in a population every generation. According to populationgenetic theory it is possible to show that a finite population will loose acertain proportion of the average heterozygosity (allele diversity), becau-se the proportion of homozygotes in the population will increase due toinbreeding. The increased inbreeding, or the increase of the inbreedingcoefficient (F), can be expressed as:

where Ne is the effective size of the population. Inbreeding increases the proportion of homozygotes, because mating

between closely related individuals increases the frequency of homozy-gous loci in each offspring compared with mating between non-relatedindividuals. The homozygotes (or homozygous loci) generated byinbreeding will consequently have two identical alleles that can be tra-ced back to the same individual – the alleles are identical by descent. Ifwe consider the total gene pool of a population of N diploid individuals,the probability to "pick" the same allele twice is 1/2N for any allele inthe gene pool. This can be explained as a process in two steps: first onespecific allele is randomly picked from the gene pool and in the secondstep the exact same allele is picked a second time. Because the frequencyof this specific allele is 1/2N in the gene pool (the allele only exists in onesingle copy), the probability to pick this specific allele in the second stepis 1/2N.

If the frequency of homozygotes increases with a factor 1/2Ne theexpected frequency of heterozygotes (allele diversity) will at the sametime decrease with the same factor. A population of 10 individuals willeach generation loose 1/(2x10) = 0.05 = 5 % of its heterozygosity.

Conservation geneticists have tried to define population sizes thatare large enough to retain sufficient genetic variation (1) to avoid loss ofreproductive fitness or (2) to enable the population to evolve in responseto environmental changes. Soulé (1980) and Franklin (1980) arguedthat an effective population size of Ne = 50 (1% of genetic variation islost each generation) is sufficient to retain reproductive fitness, and Ne = 500 is sufficient to retain evolutionary potential because 0.1% ofgenetic variation is lost each generation, and this loss will be compensated by new genetic variation created by mutation. However,this approach is under much debate, and there is no consensus amongconservation geneticists which population sizes that are “safe” from agenetic perspective.

eNF

2

1=Δ

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3.1.1 Studies of natural populations A meta-analysis including published studies of 102 species (of which mostwere animals), showed that estimations of the effective population size (Ne)on average is about 10 % of the census size (N), and that many populationsare so small that they might be affected by genetic drift and/or bottlenecks(Frankham 1995b). In a meta-analysis of 46 enzyme and DNA-studies of 41plant species, Leimu et al. (2006) demonstrated that small populations gene-rally have lower frequencies of variable genes, fewer alleles per locus andlower levels of allele diversity compared with larger populations. Thisexplains why rare or threatened species – which often occur in small isolatedpopulations – frequently have less genetic variation than common species,both in relation to the “average” population and the entire species (Cole2003; Spielman et al. 2004). Molecular markers also confirm that loss ofgenetic variation leads to an increased random differentiation between popu-lations (Cole 2003).

The hazel (Corylus avellana) demonstrates apparent signs of genetic drift,despite the fact that pollen from this bush is wind dispersed over large distan-ces (Figure 4). Populations in Sweden lack many of the chloroplast-DNAhaplotypes that can be observed in southern and central parts of Europe, as aconsequence of bottlenecks occurring during the early and rapid recolonisa-tion of Scandinavia after the most recent ice-age (Palmé & Vendramin 2002).There are also results indicating random effects at a later date occurringlocally: small isolated populations of hazel growing on south facing hillsidesin north Sweden have fewer variable genes, fewer alleles per locus and lowerlevels of allele diversity (heterozygosity) than the larger continuous popula-tions in southern parts of Sweden (Persson et al. 2004).

Figure 4. Hazel (Corylus avellana) has been studied genetically to investigate the effects of isola-tion and colonization history. To a large extent, Swedish populations of hazel lack the genetic varia-tion of chloroplast DNA that can be observed in southern and central parts of Europe. The decrea-sed level of variation is likely an effect of bottlenecks during the rapid recolonisation of Scandinaviaafter the most recent ice age. A more recent loss of genetic variation in the small isolated popula-tions of hazel in northern Sweden has also been observed. (Photo: Myra bildbyrå)

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The loss of genetic variation observed in populations of the flower prolife-rous pink (Petrorhagia prolifera) in southern Sweden is much more pronoun-ced that the moderate loss of genetic variation observed in hazel. The prolife-rous pink is an annual self-reproducing plant that demonstrates a mosaic pat-tern of genetic variation geographically – separate populations have been fix-ed for different allozyme alleles. Almost all genetic variation (>90 %) is foundamong populations (Lönn & Prentice 1990), whereas the corresponding esti-mate in hazel is 8 % (Persson et al. 2004). The pattern of genetic variation isprobably created by bottleneck effects as a consequence of the reproductivesystem, which enables the proliferous pink to establish a novel populationonly from a few individuals. Furthermore, there are only slight possibilitiesthat gene flow between populations will compensate for the loss of geneticdiversity and counteract the population divergence, because the seeds have nodispersal adaptations and most pollen grains fail to leave the small flowers.

Some species seems to be very resistant to the loss of genetic diversity. Oneof these, the spring pea (Lathyrus vernus) is a boreal, insect-pollinated plant,lacking specialised adaptations for seed dispersal. The genetic variation atseveral loci show that marginal populations in north Sweden display the samelevels of allele diversity as populations in Central Europe, which are closer tothe supposed glacial refuge. In addition, the estimates of allele diversity aresimilar both in “small” (<150 ind.) and “large” (>500 ind.) populations. Thehigh levels of genetic diversity in small marginal populations of the spring peacan be contrasted with the loss of genetic variation that is observed in popula-tions of hazel growing in similar geographic areas, a phenomenon that mightbe explained by a slower recolonisation (lack of bottlenecks) in the spring pea(Schiemann et al. 2000).

In recent times, studies of the loss of genetic variation have largely beenfocused on natural populations of animal and plant species that previouslyhad large continuous distributions but where the present populations aresmall and isolated due to the ongoing fragmentation of natural habitats (Jac-quemyn et al. 2004; Keyghobadi et al. 2005; Honnay et al. 2006; Prentice etal. 2006). Because the fragmentation often is recent, there are often maps oraerial photos available which can be used to show how the different frag-ments were connected and how large the fragments were originally. Thisinformation can be combined with data from molecular genetic markers, todemonstrate how fast the loss of genetic variation affects natural populations.Several of the species suffering from fragmentation show apparent signs ofloss of genetic variation, whereas the genetic variation in other species arestill typical of the larger population sizes that existed in the previous continu-ous landscape (Keyghobadi et al. 2005). In contrast, other studies indicatethat the fragmentation of habitat occasionally may counteract the loss ofgenetic variation because gene flow from very distant populations may incre-ase, introducing novel genetic variation in the gene pools (Young et al. 1996;White et al. 2002).

Recently bottlenecked populations often show low levels of genetic varia-tion in molecular markers. This can be seen for example in animals and plantsthat have recovered from near extinction e.g. the northern elephant seal

(Mirounga angustirostris; Hoelzel et al. 1993), Mauritius kestrel (Falco puncta-tus; Groombridge et al. 2000) and the Swedish beaver and wolf populations(Castor fiber, Canis lupus; Ellegren et al. 1993, 1996). In several cases, (e.g.Mauritius kestrel), the level of genetic variation are in agreement with what canbe expected from the bottleneck period. In other species, e.g. the northern elep-hant seal, the level of genetic variation is too low to be explained only by thebottleneck. In this particular case, the extremely low levels of genetic variationcan be explained by the fact that predators (as a group) often have low levels ofgenetic variation in molecular markers (Amos & Balmford 2001). This examp-le demonstrates the importance of comparing results to relevant reference mate-rial, e.g. large populations of the same species (Ellegren 1993, Leimu et al.2006), or a common species within the same genus (Cole 2003; Spielman et al.2004), when evaluating the effects of bottlenecks and variation losses.

Figure 5. The current population of wolves (Canis lupus) in Scandinavia was established from alimited number of individuals arriving in the 1980s and 1990s. The population has since expan-ded, but shows apparent signs of both inbreeding effects and low levels of genetic variation. (Pho-to: Myra bildbyrå)

Some bottlenecks are followed by a rapid recovery of genetic variation,most likely caused by a small number of immigrants arriving after the bottle-neck (Keller et al. 2001). An illustrative example of this phenomenon is theScandinavian population of wolves (Figure 5). This species had been absentfrom Sweden for a couple of decades, but in 1983 a pack of wolves was obser-ved in southern Scandinavia, more than 900 km from the neighbouring popula-tions in Finland and Russia. The pack consisted of about 10 animals for a num-ber of years, and evidence of loss of genetic variation and inbreeding could beseen in molecular markers (Ellegren et al. 1996). Suddenly, the populationexpanded and started to disperse to other geographic regions in the 1990s. Stu-dies using microsatellites showed that the expansion begun with an increase ofthe genetic variation (increased levels of heterozygosity, several new alleles).The increase of the genetic variation was most likely caused by the arrival of asingle male to the Scandinavian population (Vilá et al. 2002). Furthermore,

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recent microsatellite data show that it is more common that individuals withhigh levels of genetic variation breed, which could reduce the negative effects ofinbreeding among the wolves in Scandinavia (Bensch et al. 2006).

3.2 Effects on fertility and viabilityRandom processes such as genetic drift affect all parts of the genome uni-formly, not only neutral loci often used in studies of genetic variation, butalso the genes affecting the fertility and viability of individuals (fitness). Con-sequently, loss of variation in molecular markers could indicate that geneticvariation in ecologically important traits also has been lost. In this context itis important to keep in mind that “essential” alleles are expected to be pre-sent at high frequencies because they are favoured by selection, and thus theywill most likely be present even in small gene pools (Nei et al. 1975). Advan-tageous alleles that are only needed infrequently (e.g. during a disease outbre-ak), will be lost at a much higher rate, because no selective force operates tokeep them in the population between these events (Amos & Balmford 2001).

The risk for “serious” allele losses is also large in the so-called S-locus,genes that control self-incompatibility in plants and fungi (Box 2). In general,this system favours rare S-alleles; these will seldom encounter a copy of them-selves and as a result they will have a high probability of being passed on tothe next generation.

A population in equilibrium will consequently have a large number of S-alleles present at low frequencies. Therefore, the gene pool of a population atequilibrium will be at great risk to loose alleles if the number of individualssuddenly declines, because random genetic drift is greater in smaller popula-tions. Because of the random loss of S-alleles, many individuals will haveidentical S-allele genotypes which mean that fewer individuals will be able tomate with each other, thus affecting the reproductive success of the entirepopulation. Computer simulations demonstrate that populations with lessthan 25 individuals will not be able to keep sufficient S-alleles to maintain ahigh level of reproductive success (Byers & Meagher 1992).

Box 2: Self-incompatibility locus (S-locus)The self-incompatibility locus in some plants and fungi is a locus underfrequency-dependent selection. The function of this locus is to preventself-fertilization and breeding between closely related individuals. Gene-tic variation in this locus is a necessity for breeding, because pollen (orspores) with a certain genotype at the S-locus will only be able to fertili-ze individuals that possess at least one different allele at the same locus.A novel S-allele, introduced into the population by migration or muta-tion, will be at a selective advantage because the individual that possessthis allele will be able to fertilize all individuals in the population exceptitself. As a result, the frequency of the novel allele will increase until itreaches the same level as the other S-alleles.

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On top of loosing genetic variation as a consequence of genetic drift,small isolated populations are also expected to become inbred because eachgeneration the individuals are continuously getting more related to eachother. The inbreeding is entirely an effect of the reduced population size, andwill increase with 1/2Ne each generation, i.e. at the same rate as the decreaseof heterozygosity and additive quantitative genetic variation (Box 1). Inbree-ding will increase the homozygosity and the proportion of alleles that areidentical by descent. Eventually, the proportion of homozygotes will be solarge that the population might suffer from inbreeding depression, similar towhat occurs after self-fertilisation or breeding between siblings (Charles-worth & Charlesworth 1987).

With increased inbreeding, the recessive deleterious alleles that cause theinbreeding depression are expected to be removed from the population oneafter another; especially those that have large negative effects on fertility andviability. As a result, a severe inbreeding event is expected to be more seriousfor species with large out-crossing populations, compared with species thathave a long term history of inbreeding, as for example a self-fertilising plantwhich previously has undergone a"purging-process" as described above(Lande & Schemske 1985).

Population geneticists have observed that populations may experiencereduced fertility and viability if deleterious mutations are accumulated in thegene pool, especially alleles that individually have small deleterious effects.These mutations will never reach high frequencies in large populations withsexual reproduction, where selection will prevent the deleterious alleles frombecoming common. However, in small isolated populations where geneticdrift may be a stronger force than natural selection, these deleterious allelescould increase in frequency and might even be fixed by chance. The fixationof deleterious alleles in small populations may ultimately affect the survival ofthese populations, in spite of the fact that each allele individually only has asmall effect on population growth. Every fixation of a deleterious mutationwill decrease the population size, which in turn enables the fixation of otherdeleterious mutations – the population has been trapped in a downward spi-ral. In theory, the onset of such a "mutational meltdown" potentially canoccur in relatively large populations (Ne > 1000), in which case the extinctionwill take place after many thousands of generations (Lande 1995).

The risk that different populations will be fixed for exactly the same dele-terious mutations is minute. As a consequence, migrants from different popu-lations will often pass on alleles that lead to higher fitness compared with thedeleterious mutations that happen to be fixed in the local gene pool. These“foreign” alleles will be favoured by natural selection, and will increase infrequency in the local gene pool. As a result, this will restore the viability andfertility of the receiving population, a phenomenon termed the "geneticrescue effect" (Ingvarsson 2001; Keller & Waller 2002).

3.2.1 The effects on fertility and viability in natural populationsThere are numerous studies investigating if populations with low levels ofgenetic variation suffer from the loss of genetic variation, inbreeding or

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because deleterious mutations have become fixed in the gene pool. Reed &Frankham (2003) performed a meta-analysis of 34 animal and plant studies,aiming to investigate the correlations between genetic variation, populationsize and the average of different fitness related traits (growth, fertility andsurvival). All correlations were found to be significantly positive: individualsin large or genetically variable populations demonstrated a tendency forhaving higher fitness compared with individuals in small populations. Up to20 % of the variation in “average fitness” between populations was explai-ned by population size or the level of genetic variation. These results wereconfirmed in a meta-analysis of plant studies using common garden experi-ments (Leimu et al. 2006), where these associations remained. Consequently,the reason why small populations or populations with low levels of geneticvariation have reduced fertility or viability must be genetic and cannot onlybe caused by a deteriorating environment. Furthermore, several studies indi-cate that the decrease of fitness is greatest when individuals or populationsare subject to different forms of stress (Keller & Waller 2002; Armbruster &Reed 2005; Frankham 2005a).

Evidence from a number of studies show that reduced fertility and viabili-ty are caused by inbreeding or because the gene pool has been fixed for dele-terious mutations (van Treuren et al. 1993; Keller & Waller 2002; Paland &Schmid 2003). Other studies have tried to find associations between lowlevels of fitness and the loss of specific alleles. Researchers argued that thedecline of the cheetah (Acinonyx jubatus) and other mammals can be explai-ned by the loss of variation in genes controlling the immune system, theMajor Histocompatibility Complex (MHC) (O'Brien et al. 1985). However,this interpretation is controversial and recent evidence suggests that environ-mental factors, especially loss of habitat, primarily caused the decline of thecheetah (Amos & Balmford 2001). However, associations between low levelsof fitness and loss of specific alleles in various S-loci have been demonstratedfor several plant species (DeMauro 1993; Byers 1995). Lack of S-alleles mightexplain why small isolated populations of the mountain arnica (Arnica mon-tana) in Holland and the field fleawort (Tephroseris integrifolia) in Swedenhave lower levels of seed-set than large populations (Widén 1993; Luijten etal. 2000). In the case of creeping spearwort (Ranunculus reptans), smallpopulations appear to suffer from inbreeding depression, fixed deleteriousmutations as well as lack of S-alleles (Willi et al. 2005).

Both experimental studies and studies using molecular markers have con-firmed that loss of genetic diversity can increase the extinction risks of natu-ral populations (Keller & Waller 2002; Frankham 2005b). In Finnish popula-tions of the butterfly Glanville fritillary (Melitaea cinxia) on the Baltic islandÅland, the decrease of heterozygosity in molecular markers was associatedwith increased extinction risk (Saccheri et al. 1998). In experimental popula-tions of the meadow plant field gentian (Gentianella campestris), researchersfound a clear correlation between habitat fragmentation, reduced seed setand increased mortality of seedlings for the variant of the field gentian thathas to be insect pollinated (Lennartsson 2002). The association was strongand even affected the life expectancy of the populations if the loss of habitat

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was as large as 40-50 %. The reduced fitness was in part caused by the lackof pollinators in the fragmented landscape and in part by the increasedinbreeding depression in the few seeds that were produced.

It has been suggested that natural selection will eliminate (purge) thedetrimental alleles causing the inbreeding depression in populations with dec-reasing sizes. Although many experiments and several meta-analyses havebeen performed aiming to corroborate this statement, e.g. Byers & Waller(1999) and Crnokrak & Barrett (2002), there is no conclusive evidence thatthis occurs in natural populations. However, several studies indicate thatpopulation with low levels of genetic diversity can regain fertility and viabili-ty, through gene flow from other populations (Keller & Waller 2002). Thiscan be a natural process, as in the case of the Swedish wolf population (Viláet al. 2002), or as a result of conservation actions such as supplementation. InScania, a province in southern Sweden, a decreasing European adder popula-tion (Vipera berus) suffering from escalating inbreeding, started to grow insize after 20 males from another locality were released into the population.The most likely reason for the population expansion is that more snakes sur-vived to adult age in the restored population (Madsen et al. 1999).

Several species have recovered from extreme bottlenecks without a contri-bution of alleles from other populations, e.g. the northern elephant seal andthe Swedish beaver population (Hoelzel et al. 1993; Ellegren et al. 1993).Often these examples are put forward as arguments in opposition to the viewthat loss of genetic variation is a problem for natural populations. However,it is important to remember that these few examples of “successful” bottle-necks only constitute an extremely small proportion of all the bottlenecksthat have occurred. Species or populations that do not successfully recoverfrom a bottleneck, and thus are extirpated for genetic or other causes, arerarely observed because they disappear without being noticed. Furthermore,the negative effects of a bottleneck may not be visible until after a long timeperiod, or after an unusual event that challenges the adaptive abilities of apopulation, e.g. outbreak of a disease (Frankham et al. 1999).

3.3 The effects of loss of genetic variation onthe long term ability to adapt

Adaptation can be a rapid process, and sometimes only involves a single gene.If the positive selection is strong, the “best” allele will quickly be fixed in alocus and the adaptive process will come to an end, unless a new still “better”allele is created through mutation or is introduced into the population bygene flow. This limitation does not apply to the traits that are affected bymany genes. Quantitative traits can maintain high levels of genetic diversityeven when they are subject to selection. Firstly, the level of genetic variation ishigh because there are many genes that might mutate and recombine, at thesame time as the selection at each locus is very weak. Secondly, the type ofselection for these traits can often be of a kind that maintains genetic diversity

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rather than eliminates it (Johnson & Barton 2005). Together, these two fac-tors enable the selection process to go on for a very long time, assuming thatthe gene pool is large enough not to be strongly affected by genetic drift orbottlenecks.

Decreasing population size can have negative effects on a population’sability to adapt to environmental change. The additive genetic variation (thegenetic variation available to selection) is expected to decrease with 1/2Neeach generation, i.e. at the same rate as the expected heterozygosity is lost ata single locus (Box 1). As before, this decline will continue until an equilibri-um arises, where the loss of “old” genetic variation is balanced by the newvariation created by mutations. The total amount of additive genetic varia-tion that can be maintained at the equilibrium will increase with larger effec-tive population size Ne, and the variation pattern also depends on the type ofselection that act on the trait (Willi et al. 2006). To maintain “normal” levelsof genetic variation in traits that influence a population’s long term ability toadapt, the Ne of the population must be at least 500 or 5000 depending onthe assumptions made for the mutations that introduce novel variation. Thelower estimate is calculated taking both the favourable and deleterious muta-tions into account, whereas the higher estimate is calculated only from thefavourable mutations (Franklin 1980; Lande 1995).

The occurrence of non-additive genetic variation (genetic variation of alle-les that affect the phenotype by having an effect on other alleles in the sameor other loci, e.g. dominant alleles masking the effects of recessive alleles)complicates the picture, especially when populations are undergoing extremebottlenecks. In such cases the genetic variation available to selection maysometimes increase or be at a constant level, even if the effective populationsize decreases. One possible explanation is that rare recessive alleles, nor-mally not expressed in the phenotype, will reach high frequencies by chancewith the result that individuals homozygous for the previously rare allele areformed. Thus, more genetic variation is available for selection to act onbecause of the increased frequency of phenotypes that previously were extre-mely rare in the population.

3.3.1 Studies investigating the effects on long term adaptive abilities innatural populations Only a few studies that compare the additive variation between small and lar-ge populations exist, and these studies do not show any clear differences (Wil-li et al. 2006). Quantitative genetic analysis of the two red listed meadow flo-wers Tephroseris integrifolia (field fleawort) (Figure 6) and Scabiosa cane-scens in Sweden both fail to show loss of genetic diversity in ecologicallyimportant traits, in spite of a 10-fold (T. integrifolia) or 200-fold (S. cane-scens) size difference between the smallest and largest populations. The heri-tability (how large the proportion of the variation that is available to selec-tion, the additive variation, is of the total variation) varied for the differentcharacters, but was well within the range usually observed in plants, both forthe small and large populations (Widén & Andersson 1993; Waldmann &Andersson 1998; Waldmann 2001). Furthermore, there is no obvious correla-

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tion between additive variation in phenotypic characters and allele diversityof molecular markers in populations of different sizes, despite the expectationthat genetic drift should affect both these estimates in the same way (Wald-mann & Andersson 1998; Reed & Frankham 2001). The processes thatmaintain high levels of genetic variation in natural populations seem to bestrong enough to counteract the loss of genetic variation in ecological impor-tant characters, at least in the populations that have been investigated so far.

Lately, experiments manipulating the population size have been perfor-med to study how a decrease in population size affects the additive geneticvariation and thus the population’s ability to adapt (evolutionary potential).In several cases, the genetic variation decreased, just as predicted in theory,but in other cases the decrease was much less than expected. In some casesthe variation increased, especially in fitness related characters (fertility, viabi-lity etc.) and particularly if the populations had undergone extreme bottle-necks (Willi et al. 2006). However, many researchers have questioned if thishas any positive effects for evolutionary potential, because the increase ingenetic variation is often followed by increased inbreeding (Willis & Orr1993; Barton & Turelli 2004). In any case, it is difficult to draw general con-clusions about how the loss of genetic diversity affects the long-term evolutio-nary potential of populations, from the data that are available at present.

Figure 6. The field fleawort (Tephroseris integrifolia) is one of the few plants in Swedenthat has been subject to studies of quantitative genetic characters. The result from this,and other studies of threatened Swedish species, do not show any signs of loweredlevels of genetic variation in ecologically important characters, regardless of populationsize. (Photo: Björn Widén)

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4. Genetic diversity after geneflow and hybridisation

The genetic characteristics of populations are primarily determined byevolutionary processes acting on the local gene pool (natural selection, gene-tic drift, mutations, and recombination), but they are also affected by theexchange of genes between other populations, through gametes, spores, pol-len, seeds or migrating individuals that are able to reproduce. This gene flowis often a positive factor, because connections between populations will incre-ase their effective population size, and consequently oppose the loss of geneticvariation caused by genetic drift and bottlenecks. However, the gene flow can

Summary:Gene flow between populations is often a positive process and decrea-ses the risk of local extinction and loss of genetic variation. Althoughanthropogenic habitat fragmentation usually causes negative isolationeffects, human activities may also result in increased gene flow betweennatural populations of animals or plants. In this chapter we describehow a too extensive or too distant gene flow can have negative effectson the recipient population.

Occasionally, human activities have increased the gene flow by cre-ating zones or ”hybrid environments” where genetically dissimilarpopulations or closely related species can meet and exchange genes. Itis known that genes from introduced or domesticated species havespread to Swedish populations of several species – as for example themountain hare (genes from the brown hare) and two subspecies of theplant lucerne (genes from the cultivated Medicago falcata spp. sativa tothe wild M. falcata spp. falcata).

There is only sporadic knowledge about gene flow that occurswhen alien populations of trees, birds and fish are released into thewild and come into contact with indigenous populations, or whenforeign grass seeds are sown on road verges. Studies of salmon showthat gene flow can be harmful by creating hybrids with low levels ofviability and fertility (i.e. outbreeding depression). In other cases geneflow has been so intense that the genetic integrity of species is threate-ned, as in the case of the low-density populations of the plant Violaalba on the island of Öland, a species that easily hybridises with otherrelated species. Sometimes populations with the capability to invadenatural ecosystems have been created due to human-mediated hybridi-sation between closely related species. At the end of this chapter, wediscuss the conservation value of hybrids and the potentially negativeeffects of gene flow, e.g. when populations are supplemented with indi-viduals raised in captivity or with individuals from too distant popula-tions.

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sometimes be too extensive or from populations too far apart, resulting inharmful effects on the recipient population, causing populations to looseimportant local adaptations or decreasing their production of viable and fer-tile offspring (outbreeding depression). An extreme variation of gene flow ishybridisation, i.e. crossings between individuals so different that they areclassified as different species or subspecies (Ellstrand & Elam 1993; Levin etal. 1996).

Gene flow and hybridization are processes that can be affected by humanactivities in different ways. Although anthropogenic habitat fragmentationusually causes negative isolation effects, human activities may also result inincreased gene flow between natural populations of animals or plants. Occa-sionally, human activities have increased the gene flow by creating zones or”hybrid environments” where genetically dissimilar populations or closelyrelated species can meet and exchange genes. Human activities have also faci-litated gene flow between taxa through intentional or unintentional release ofalien species or genotypes that later on reproduced with related local taxa. InSweden, alien species or genotypes are presently used e.g. in agriculture, inforestry, in the fish industry, and as plants sown to stabilize road verges.

In practical conservation biology gene flow can cause problems, especiallywhen supplementation and reintroduction techniques are used to boost localpopulations with individuals from distant localities, or when dispersal betwe-en localities is facilitated in other ways.

4.1 Hybridisation and gene flow in theory An inflow of alien genes can have several negative effects on the gene pool.Gene flow from too distant populations can cause outbreeding depression,i.e. the offspring suffer from lowered vitality or fertility compared with off-spring from cross-fertilisations within the population. Outbreeding depres-sion can be elusive, because it is often not observable until the second genera-tion (F2) after the hybridisation, because the adaptive gene complexes inheri-ted from the parental generation will not start to break down until then. Ifthe gene flow comes from a species or population with a different karyotype,e.g. higher chromosome number, the hybrids may become sterile because ofdisruptions in meiosis (Grant 1981). Outbreeding depression and hybrid ste-rility will not pose a major problem when the level of alien gene flow is low,because natural selection will have time to eliminate the unfit individuals.Large levels of gene flow on the other hand, as for example when a smallpopulation comes into contact with a large one, may have a substantial nega-tive effect on the reproduction and viability of the smaller population (Levinet al. 1996).

Even if the alien genes have positive effects on fertility and viability, thegene flow may cause problems for the recipient population. If the genes givethe individuals large and immediate competitive advantages, the foreign geneswill replace the original genes, which might be needed for long term adapta-tion. As a consequence, the original locus (and linked loci) will loose valuable

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genetic variation. If the increase in fitness is substantial, the entire populationmay be at an advantage, hence becoming a threat to other species and popu-lations. This is a relevant scenario for the transgenes or other types of modifi-ed genes that might spread from genetically modified organisms (GMO) totheir relatives in the wild (Ellstrand et al. 1999), but also for the genes thatwill increase the viability of individuals through heterosis. Heterosis effectsare most apparent in the first generation hybrids (F1), before the onset of theoutbreeding depression. The inflow of alien genes may be so large that thepopulation loses its genetic distinctness and is “assimilated” into a larger genepool, which might be a potential threat to populations of rare species thatsuddenly come in contact with more common relatives (Ellstrand & Elam1993; Levin et al. 1996).

4.2 Hybridisation and gene flow in natural populations

4.2.1 Hybrid fitnessThe possibility for alien genes to establish themselves in natural populationswill largely be determined by the fitness of the hybrids and their offspring.Many studies where the fitness of hybrids is compared with their parentalpopulations have been performed, both in controlled environments and infield experiments under natural conditions (Hufford & Mazer 2003). It isfairly common that the F1-hybrids from crossings within species show hetero-sis, whereas the second and third hybrid generation demonstrate signs of out-breeding depression when the parental genes start to recombine to a largerextent. In several cases an “optimal crossing distance” has been determined;where too short distances (e.g. between close relatives) leads to inbreedingdepression, while too large distances instead lead to outbreeding depression.There are also situations where the heterosis effects overshadow the effects ofthe outbreeding depression or vice versa, or where the dominating factor isdependent on which fitness measure is considered (Hufford & Mazer 2003).

Studies of hybridisation between species demonstrate similar variation:hybrids between species may have higher, unaltered or lower viability and fer-tility compared with their parents. Results are influenced by which specieshybridised, which species was “mother” or “father”, which populationsrepresented the parental species and in which environment the hybrids havebeen raised (Arnold 1997). Many hybrids seem to cope extraordinary wellwith novel or disturbed environments (Levin et al. 1996), and there is eviden-ce that natural selection can restore the average fertility of a hybrid popula-tion by removing the genotypes suffering from outbreeding depression (Cam-pbell et al. 2006). Presently, it seems to be difficult to draw general conclu-sions about the potential of alien genes to spread to natural populations,because the experiments conducted so far only include one or a few crossings,few hybrid generations, and a limited number of cultivation environments.

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4.2.2 Gene flow and hybridisation after environmental disturbanceNumerous examples exist of situations where human activities have brokendown the various reproductive barriers between species and populations.Sometimes, only a small disturbance or an environmental change can be suffi-cient to enable species or populations to make contact and start to exchangegenes. According to an Australian study, two species of Banksia with overlap-ping flowering time have a greater possibility to form hybrids when growingtogether in a disturbed environment along road verges, compared with whenthey grow in solitude in their natural habitat (Lamont et al. 2003). Manyhybrids between European plants are also more common in certain habitats,as for example hybrids formed between water avens (Geum rivale) and itsshade-loving relative wood avens (G. urbanum) (Briggs & Walters 1997). ASwedish example of disturbance-induced hybridisation is that between theweed Silene vulgaris (the bladder campion) and the closely related S. uniflorassp. petraea, a subspecies endemic to the southern parts of the Baltic area.The narrow hybrid zone between these two taxa extends along an old railwayembankment in the east-west direction over the Baltic island of Öland. Allo-zyme data demonstrate that there is extensive gene flow between the twotaxa, and the morphology of 14 % of the individuals in this area also suggeststhat they are hybrids (Runyeon-Lager & Prentice 2000).

Hybridisation between fish species also exist in Swedish waters, especiallyafter disturbance. Natural hybridisation between the Atlantic salmon (Salmosalar) and the brown trout (S. trutta) is less than 1 %, but in disturbed habitatmore than 25 % of the individuals are hybrids (Jansson et al. 1991). An inter-national example of hybridisation induced by disturbance is the increasedhybridisation resulting in decreased species and subspecies diversity of certaincichlid fish genera, as a consequence of the increased eutrophication of LakeVictoria in Africa. The eutrophicatied water is so muddy that males andfemales of the same species no longer can recognize each other, and hence thefrequency of matings between species is increasing (Seehausen et al. 1997).

4.2.3 Genetic contamination by introduced species or genotypesThe effect of human mediated gene flow and hybridisation is especiallyobvious when introduced species or genotypes come in contact with wildrelatives in a habitat. Recently, attention has been given to the gene flow thatmay occur when southerly provenances of forest trees (mostly Scots pine,Pinus sylvestris; Norway spruce, Picea abies; and silver birch, Betulapendula) are planted to increase the production of timber, when birds rearedin captivity (mostly mallard, Anas platyrhynchos; grey quail, Perdix perdix;and common pheasant, Phasianus colchicus) are released for hunting purpo-ses, or when accidentally or intentionally released fish (mostly brown trout,Salmo trutta; Atlantic salmon, Salmo salar; arctic char, Salvelinus alpinus;common whitefish, Coregonus lavaretus; and grayling, Thymallus thymallus)with an alien genetic background come in contact with the indigenous fishpopulations (Laikre & Palmé 2005; Laikre et al. 2006). All these situationsinvolve a possibility for gene exchange, because the introduced individualsare only domesticated to a small degree, but often have excellent dispersal

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abilities both regarding themselves and their genes, and also have a greatopportunity to come in contact with natural populations. The extent of thistype of gene flow is uncertain, because an effective system where these intro-ductions can be registered is lacking in Sweden at present, but it is likely thatmillions of forest trees, birds and fish are released each year (Laikre & Palmé2005; Laikre et al. 2006).

In Sweden, much of the cultivation material of Norway spruce (Picea abi-es) (Figure 7) comes from eastern parts of Europe, predominantly Belorussia.In this part of Europe the spruce has lower levels of genetic variation compa-red with Scandinavian populations (Lagerkrantz & Ryman 1990), which ulti-mately may affect the genetic variation in natural forests neighbouring thespruce plantations (Laikre & Ryman 1996). For the Atlantic salmon (Salmosalar) (Figure 8), a species with distinctive philopatric instincts, there is anobvious risk that alien genes might confuse the fish and cause them to returnto breed in the wrong rivers if cultivated salmon are used for supplementationof local salmon populations. Genetic studies show that up to 25 % of the sal-mon breeding in the river Vindelälven might be fish released in other Swedishriver systems (Ångermanälven, Luleälven, Ljusnan) (Vasemägi et al. 2005).Furthermore, there is evidence that hybridisation between natural salmonpopulations and salmon that have escaped from cultivation rapidly changesthe genetic diversity of the natural salmon populations (Crozier 1993; Fle-ming et al. 2000).

Figure 7. The pollen of Norway spruce (Picea abies) is wind dispersed over great distances. Apartfrom this natural gene flow, many Swedish spruce populations are affected by gene flow fromforeign provenances, planted to improve timber production. The extent and consequence of thisgene flow is not fully known. (Photo: Myra bildbyrå)

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The possibilities of alien gene flow are most likely large between grass ofunknown genetic origin, sown on newly established road verges, and theirSwedish conspecifics. Several new grass species have been established in theSwedish flora as a result of intentional release of grass seeds of non-nativespecies (Aronsson 1997; Mossberg & Stenberg 2003). Introduction of aliengenotypes of native species has almost certainly also occurred in the sameway; the seed mixtures used largely consist of common meadow species asred fescue (Festuca rubra), smooth meadow-grass (Poa pratensis), commonbent (Agrostis capillaris) and timothy (Phleum pratense ssp. serotinum). Themajority of the seed mixtures come from Europe but some are of Americanorigin (Aronsson 1997). The extent of this gene flow is unknown, and has asfar as we know not been subject to any scientific investigations.

It is known that about 50 of the cultivated crop species, including 12 ofthe 13 most important crops, spontaneously form hybrids with one or severalof their wild relatives (Ellstrand et al. 1999; Ellstrand 2003). Among thecrops cultivated in Sweden that can form hybrids with native species or popu-lations are: oilseed rape (Brassica napus; hybridises with wild turnip, B. rapaand wild radish, Raphanus raphanistrum); sugar beet (Beta vulgaris ssp. vul-garis; hybridises with sea beet, B. vulgaris ssp. maritima); appel (Malus xdomestica; hybridises with crab apple, M. sylvestris); lucern (Medicago sativassp. sativa); hybridises with, sickle medick, (M. sativa ssp. falcata); and thegrass creeping bent (Agrostis stolonifera), often grown on golf courses. Furt-hermore, two of these wild species, the wild radish and the sea beet have (orhave until recently been) red listed in Sweden (Gärdenfors 2005).

Genetic studies have demonstrated that genes from cultivated crop speciesare already present in wild plants (Ellstrand 2003), and there are at least two

Figure 8. Atlantic salmon (Salmo salar) is a species that often appears in conservation genetic pro-jects. Swedish research has focused on the genetic changes in wild salmon populations that occurwhen cultivated salmon are released to supplement the local populations. (Photo: Myra bildbyrå)

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examples showing that genes from genetically modified plants successfullyhave spread to natural populations (oilseed rape, Warwick et al. 2003; cree-ping bentgrass, Reichman et al. 2006). In both cases it is genes coding for her-bicide resistance that can be found in natural populations several kilometresfrom the cultivations, but only to a limited extent. In Denmark, an extensivegene flow from oilseed rape (not genetically modified) to wild turnip has beenobserved, when the latter is growing as a weed in organically managed farms(Hansen et al. 2003; Jørgensen et al. 2004). Sometimes, the gene flow can bebidirectional, as in the case of sugar beet (Beta vulgaris ssp. vulgaris). Insouth-western Europe, where sugar beet is grown to produce the seeds usedin beet cultivations, gene flow from natural populations of an annual beetrelative to the sugar beet has been observed. The hybridisation produces“weed beets” that flower prematurely instead of storing sugar in the rosettes(Viard et al. 2002). In some areas where sugar beets are grown to producesugar, gene flow in the opposite direction, from the sugar beet to naturalpopulations of the sea beet, has been observed (Bartsch et al. 1999). Howe-ver, gene flow between these two sub-species has not yet been documented inSweden.

One of the most obvious examples of gene flow between cultivated andnatural populations in Sweden is the hybrid sand lucerne (Medicago sativassp. varia), which is a result of a crossing between the native sickle medick(M. sativa ssp. falcate) and the cultivated lucern (Medicago sativa ssp. sativa).The hybrids constitute a “hybrid swarm”, common on road verges and inother disturbed areas, and are distinguished by an enormous variation in flo-wer colour (from light blue to green or almost black flowers) (Mossberg &Stenberg 2003).

Figure 9. The artic fox (Alopex lagopus) is a threatened species found in the Scandinavian alpinelandscape. Recently, another threat to this species has been identified: hybridisation with foxesescaped from fur farms. (Photo: Myra bildbyrå)

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There are many examples of hybridisation – and potential gene flow –between domestic animals and their natural relatives, e.g. in the genus Canis(dogs and wolves, Vilà & Wayne 1999). In Scandinavia, zoologists haverecently showed that wild arctic foxes (Alopex lagopus) (Figure 9) hybridisewith foxes escaping from fur farms, which might pose a serious threat to thealready endangered species (Norén et al. 2005).

Recent studies have also demonstrated hybridisation between native andnon-domesticated species intentionally released into the wild. The brownhare (Lepus europeus) was introduced to Sweden in the late 19th century forhunting purposes, and has since then produced fertile hybrids with the nativemountain hare (L. timidus) (Figure 10). Evidence from studies ofmitochondrial DNA show that most hybrids are a result of breeding betweenfemale mountain hares and male brown hares (Thulin et al. 1997), but thereverse hybridisation (female brown hare and male mountain hare) has alsobeen documented on rare occasions (Thulin et al. 2006).

Lately, an increased production of hybrid falcons used in hunting (falcon-ry), has increased the risk of hybridisation with native peregrine falcons (Fal-co peregrinus) in Sweden. At least one such case has been observed in sout-hern parts of Sweden, where a domesticated hunting falcon male nested witha native peregrine falcon female (Lindberg & Nejse 2002).

4.2.4 Outbreeding depression and genetic assimilationOccasionally gene flow can be so severe that it can be harmful for the recipi-ent population. This is the case for the wild Atlantic salmon (Salmo salar),which easily breeds with the much faster growing cultivated salmon that

Figure 10. The native mountain hare (Lepus timidus) produces fertile hybrid offspring with theintroduced brown hare (L. europeus), and hybridisation in the wild has been going on since theintroductions were made in the late 19th century. In general the female mountain hares hybridisewith male brown hares, which can be traced studying mitochondrial DNA, an organelle only inheri-ted maternally. (Photo: Myra bildbyrå)

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often escapes from captivity or sometimes even are intentionally released. Thehybrids have lower vitality compared to wild salmon, and there are indica-tions that this outbreeding depression contributed to the extinction of manylocal salmon populations (McGinnity et al. 2003).

In other cases, the genetic distinction of species or populations may disap-pear because of gene flow. Hybridisation with stray dogs (Canis familiaris) isa serious threat for one of the most endangered canids in the world – the Ethi-opian wolf (C. simensis). In one population as many as 8-17 % of the wolveshad a genotype or morphology suggesting that they were hybrids (Gottelli etal. 1994). A classical example of genetic assimilation is the Catalina mahoga-ny tree (Cercocarpus traskiae), an extremely rare species, the total populationof which is about 10 individuals on a small island near California. This speci-es can hybridise with a common relative, the Mountain mahogany (C. betulo-ides), and genetic data show that several trees thought to be Catalina maho-gany are hybrids between the two species. There is an obvious risk that theCatalina mahogany might become extinct because of this hybridisation (Rie-seberg & Gerber 1995). Likewise, the red listed Parma violet (Viola alba)(Figure 11), in Sweden only found on the Baltic island of Öland, hybridisesboth with the hairy violet (V. hirta) and sweet violet (V. odorata), both ofwhich are much more common (Gärdenfors 2005). Genetic assimilation alsoseems to be a problem for the Norwegian populations of boreal Jacobs-ladder(Polemonium boreale), which hybridise with the Jacobs ladder (P. caerule-um), a plant that is introduced to this area (Alm et al. 1995).

Figure 11. One of the threats to the populations of Parma violet (Viola alba) on the Baltic island ofÖland, is that it hybridises with more common species e.g. sweet violet (V. odorata), at the expenseof the rare Parma violet. The hybridisation is largely caused by humans, who facilitated the spreadof the Sweet violet, and consequently increased the possibility for contact between the two species.(Photo: Myra bildbyrå)

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4.2.5 Transgenes and heterosis effectsIt is still uncertain if transgenes, or genes modified in other ways, can beexpected to spread and affect the fertility and viability of natural populationsof Swedish species. In Sweden, especially three groups of organisms mightsoon be at risk of being affected by large scale introductions of geneticallymodified organisms: oilseed rape (Brassica napus), forest trees and fish (Palm& Ryman 2006). Knowledge about gene transfer from genetically modifiedorganisms to natural populations is limited, only a few studies have beencompleted, and these display ambiguous results concerning the possibility ofgene flow from genetically modified organisms (Palm & Ryman 2006).Transgenic oilseed rape with higher tolerance to insects or herbicides does notseem to have any advantages under natural conditions, and transgenic hybridaspen (Populus tremula x P. tremuloides) with altered hormone or ligninlevels does not seem to have any advantages, at least in green house experi-ments. Empirical studies under natural conditions are lacking both for foresttrees and fish. Altogether, knowledge of the dispersal abilities of genes fromgenetically modified organisms, and the ecological effects thereof, are unsatis-factorily (Palm & Ryman 2006).

Several weed species have arisen, or have become more invasive, afterhybridisation events between a native species and a domesticated relative(Barrett 1983; Ellstrand et al. 1999, Ellstrand 2003). In several cases, hybridswith the ability to invade and have an impact on natural ecosystems havebeen formed (Ellstrand & Schierenbeck 2000). This is true for the commoncordgrass (Spartina anglica), a tetraploid hybrid between the small cordgrass(S. maritima) which is native to Europe, and smooth cordgrass (S.alternifolia), a species introduced from North America. The common cord-grass has spread along the Atlantic coast in Europe, and has drastically alte-red the vegetation in several coastal areas (Thomson 1991). Further examplescan be found within the genus water milfoil (Myriophyllum), where severalspecies have developed into aggressive aquatic pests in parts of North Ameri-ca after hybridising with local species. In this case, the increased invasive abi-lity seems to rely on a heterosis effect, maintained through effectively vegeta-tive propagation (Moody & Les 2002).

4.3 Importance for the formation of speciesand conservation valuesMany botanists, and recently also zoologists, have developed a renewedinterest in hybridisation and gene flow as natural evolutionary forces. Hybri-disation between species is relatively common, especially between vascularplants (angiosperms, ferns etc.), but also among animals (butterflies, grouse,anseriform birds, cyprinid fishes). There are also several mechanisms, forexample polyploidisation, that may “stabilise” the hybrids so that they nolonger can backcross to the parental species. In contrast, a hybridisationevent followed by backcrossing to the parental species may lead to a restric-ted gene flow between species, without merging of the gene pools. This type

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of gene flow or introgression enables advantageous traits to spread betweenspecies (Rieseberg 1995; Arnold 1997; Mallet 2005).

The occurrence of natural hybrids can have an influence on how hybridi-sation and gene flow “problems” are regarded within the field of conserva-tion biology. Hybridisation followed by polyploidisation has created severaldistinct and endemic species in the Scandinavian flora, e.g. in the genus Sor-bus (whitebeam, rowan) and the orchid genus Dactylorhiza. Some of theseallopolyploids have high conservation value, as for example the annual Sax-ifraga osloensis, a tetraploid species formed from the diploid hybrid betweenS. tridactylites and S. adscendens (Gärdenfors 2005). In a species complexwith many “young” allopolyploids it may be appropriate to also give a highconservation value to the diploid parental species to enable species evolutionin the future (Hedrén 2001).

4.4 Genetic aspects of restoration and supplementation projectsIt is very important to consider all the different aspects of gene flow whenindividuals from distant populations are used to supplement native popula-tions or to establish new populations in areas where the species existed earli-er. According to Hufford & Mazer (2003), who based their conclusions onpublished hybrid studies and transplantation experiments, the relocated indi-viduals should come from populations as geographically close to the recipientpopulation as possible, and/or from an environment that closely resemblesthe restored environment. Thus, the negative effects of outbreeding depres-sion and of local adaptation to other environmental types can be avoided.The authors also recommend maximising the genetic variation among therelocated individuals to minimise the risk of genetic bottlenecks.

Demographic studies of experimental plant populations have on the who-le confirmed the conclusions of Hufford & Mazer (2003). Among otherthings, it seems to be an advantage to use offspring of cross-fertilisations(Luijten et al. 2002; Kephart 2004; Vergeer et al. 2004), and to maximise thegenetic variation among the transplanted individuals (Procaccini & Piazzi2001; Ahlroth et al. 2003; Vergeer et al. 2005). Ongoing transplantation stu-dies of the plant field fleawort (Tephroseris integrifolia) demonstrate that off-spring from sibling matings flower less and have lower survival rates compa-red with offspring from cross pollinations, both between and within popula-tions (B. Widén, pers. comm.). Evidence from several other plant species, e.g.the mountain arnica (Arnica montana) and the Devil's-bit scabious (Succisapratensis), show that pollination from other populations results in better off-spring – and consequently a more effective restoration – compared with localcross-fertilisations within populations, at least in the geographic areas inclu-ded in this study (Luijten et al. 2002; Vergeer et al. 2004). In contrast, othercases show that the use of foreign gene material can have negative effects.This is true for e.g. the corncockle (Agrostemma githago) and the commonpoppy (Papaver rhoeas), two plants that often are included in many commer-

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cial meadow seed mixes. A Swiss study of these two species showed cleareffects of outbreeding depression when local genotypes were crossed withplants of German origin, but the negative effects were not apparent until theformation of second generation hybrids (F2) (Keller et al. 2000).

In 2005, McKay et al. complemented the recommendations given in Huf-ford & Mazer (2003), with the advice that the introduced individuals shouldhave the same karyotype as the recipient population in order to prevent steri-lity of the possible hybrids. They also suggest actions to avoid the effects ofselection that may affect animals and plants reared in captivity, which mightcause problems when these individuals are used in e.g. supplementation orreintroduction projects. Captive conditions often are very different from thenatural environment and there is an apparent risk that these populationsbecome adapted to the captive environment (Sundström et al. 2004), whichmight cause the reintroduction to be less successful (Lynch & O'Hely 2001;Woodworth et al. 2002). These problems can be counteracted by minimisingthe number of generations in captivity or by continually using individualscaptured in the wild as breeding stock. Genetic studies of Atlantic salmonreared in captivity (Ståhl 1983; Kallio-Nyberg & Koljonen 1997), and of thelarge Nordic carnivores kept in zoological institutions (Laikre 1999), clearlydemonstrate the need for minimising the loss of genetic diversity and theinbreeding problems that might arise in captive populations. The release offish from genetically impoverished breeding stock is a likely cause of the lossof genetic variation observed in certain populations of brown trout (Salmotrutta) and grayling (Thymallus thymallus) (Hansen et al. 2000; Koskinen etal. 2002; see also Ryman 1981). However, under certain conditions a success-ful breeding program may increase the genetic diversity of a population(Ryman et al. 1995; Wang & Ryman 2001).

Several researchers have used molecular markers to follow up the resultsof supplementation or reintroduction projects, estimating for example theeffective population size (Ne), and the impact on the genetic variation of thepopulation. A restored population of the shrub Corrigin grevillea (Grevilleascapigera), one of Australia’s (and the worlds) most endangered species, con-sisted in 1996-1998 of ten micro bred genotypes identified by AFLP-markers.In 1999, only eight genotypes remained, and the genetic diversity was verylow because a majority of the surviving individuals had the same genotype.The extremely low estimate of effective population size (Ne≈2)was the reasonwhy particular conservation actions were recommended to prevent future lossof genetic diversity (Krauss et al. 2002). Another example is the repatriatedpopulation of giant Galápagos tortoises (Geochelone hoodensis) that can befound on one of the islands (Espanóla). Until 2002, this population had beensupplemented with 1200 individuals, all offspring from a breeding programof twelve females and three males. Milinkovitch et al. (2004) estimated theeffective population size of the population as about 6, using microsatellitedata to identify the parents of 132 of the reintroduced animals. The low esti-mate indicates a risk for future variation losses unless the breeding program ismodified. There are also examples of re-established populations that haveretained genetic variation (Ramp et al. 2006), or where the introduced indivi-

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duals have contributed new genetic material to the gene pool without increa-sing the total amount of genetic variation. The latter is true for one of twoSwedish populations of otter (Lutra lutra) supplemented with animals fromNorway (Arrendal et al. 2004).

Genetic aspects have played an important role in two reintroduction pro-jects in Sweden, involving two bird species: the lesser white-fronted goose(Anser erythropus) and the white stork (Ciconia ciconia). The lesser white-fronted goose is the most threatened goose species in Scandinavia, and in theyear 2000, after the discovery that the breeding population was contaminatedwith genes from greater white-fronted goose (A. albifrons) and greylag goose(A. anser), all reintroductions were stopped. As much as 36 % of the breedingpopulation might have hybrid ancestors according to analyses ofmitochondrial and nuclear (microsatellite) DNA (Ruokonen et al. 2007). Atthe moment, investigations of how the project can be reinstated, and whichlesser white-fronted geese can be used for future reintroduction projects, areunder way. The stork project aimed to reintroduce a self-sustaining popula-tion of the white stork to the Swedish province Scania and has so far succee-ded, to the point that released storks regularly are roosting in the area. Unfor-tunately, most storks remain in Scania during winter, and as a consequencethey have to be fed during long periods of cold weather. The reason behindthe lack of migration instinct is most likely that the introduced birds descendfrom North African birds lacking this behaviour. To counteract this problem,the original breeding stock has been replaced with storks from Poland, whichhopefully will represent the more northern migrating stork type.

5. Genetic effects of harvesting

Human activities such as fishing, hunting and forestry mainly rely on natu-rally reproducing populations, but also include activities that enhance theproduction in these populations (subsidiary feeding, fertilizing) and activitiesthat aim to replace individuals removed from the populations (supplementa-tion with captive reared or relocated individuals). These actions can haveboth direct and indirect effects on the genetic diversity of natural populations.Harvested populations can become so small that they lose genetic variationthrough genetic drift and bottlenecks. Similar losses can occur in the animaland plant populations used in the different supplementation regimes, and atthe same time there is a risk of introgression when introduced individualscome from genetically distant populations (Chapters 3 and 4).

Genetic studies of harvested, and therefore economically important, speci-es have contributed much of the information in this report. In spite of this,only relatively few studies examining the genetic consequences of the harves-ting in itself exist (Laikre & Ryman 1996; Ashley et al. 2003; Olsson et al.2007). In a theoretical paper, Ryman et al. (1981) describe how the geneticeffective population size (Ne) – and thus the risk of losing genetic variation –will be affected by different hunting regimes in the Swedish moose population(Alces alces). Microsatellite variation in populations of North Sea cod (Gadusmorhua) demonstrate that the harvesting can increase the inflow of individu-als – and genes – from other populations, which may affect the large scalepattern of genetic variation (Hutchinson et al. 2003). In the case of Atlanticherring (Clupea harengus), microsatellite data show that the population is infact three genetically different populations, one in the North Sea, one in theSkagerrak and one in the Kattegat/Baltic Sea (Ruzzante et al. 2006). How-ever, the harvesting is expected to affect these three populations simultane-ously, because modern fishing often occurs in the mixed populations that ari-

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Summary:Many Swedish animal and plant species are exposed to regular harves-ting, such as fishing, hunting and forestry. In this chapter we give anoverview of the relatively few studies investigating the genetic effects ofharvesting.

Harvesting is expected to increase the random loss of genetic varia-tion by decreasing the effective population size. In a study of cod(Gadus morhua), local harvesting led to increased migration of indivi-duals (and genes) from nearby populations, also resulting in a changeof the large-scale pattern of genetic variation. There are many examp-les of harvested animal populations that have undergone directionalevolution as a result of selective harvesting. In several cases this changehas decreased the ability of the population to recover after a period ofintense harvesting.

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se when individuals from different populations migrate to the same area tofeed.

Harvesting can also be selective in a way that will affect the variation andproductivity of natural populations (Law 2000; Ashley et al. 2003; Gård-mark et al. 2003). For example harvesting of adult individuals will favourindividuals that reach sexual maturity at an early stage (Roff 1992). Thisselection pressure can also be combined with a selection regime favouringsmall individuals if the harvesting is focused on large individuals, which iscommon in the case with fishing (Conover & Munch 2002; Olsson et al.2007). An evolutionary change towards early maturity and/or small individu-als will decrease a population’s ability to reproduce and will consequentlyreduce the capability to recover after a period of intense harvesting (Law2000; Conover & Munch 2002).

The recent decline of the cod populations in the North Atlantic is mainlycaused by too intense harvesting (Figure 12) (Myers et al. 1997). Over-fishingof this population also had genetic consequences, at least for the populationoutside the Eastern coast of Canada. This population collapsed in the late1980s and the early 1990s, and the population has not recovered, in spite ofthe fact that all fishing has been prohibited since 1992. According to Olsen etal. (2004), the collapse was preceded by a time period when the cod started toreproduce at still younger age and smaller sizes. Most likely this shift wascaused by the fact that genotypes that matured late were caught before theywere able to reproduce, resulting in an increased frequency of genotypesmaturing early. The authors suggest that such an increase might be a warning

Figure 12. The cod (Gadus morhua) has been subject to intense over-fishing in many areas. Recentstudies suggest that the harvesting of certain cod populations has been selective in a way that dec-reases the population growth and the ability to recover after a period of small population sizes.Under periods of intense fishing, individuals maturing late will risk being caught before they repro-duce. The effect of this selection scheme will be that the average cod will start to reproduce atyounger and younger age, which will have a negative effect on population growth. (Photo: Myra bild-byrå)

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that a collapse of a harvested fish population is imminent.Several studies suggest that selective fishing has caused a change towards

earlier onset of reproduction and/or smaller size of fish populations in Euro-pe. This has been observed in e.g. the Baltic cod (Gadus morhua) (Cardinale& Modin 1999), grayling (Thymallus thymallus) in Alpine lakes in Norway(Haugen & Vollestad 2001), North Sea plaice (Pleuronectes platessa) (Grift etal. 2003), and spring-spawning herring (Clupea harengus) off the Norwegiancoast (Engelhard & Heino 2004).

Hunting may change natural animal populations if the removal of indivi-duals is based on phenotypic traits with high heritability. Selective hunting ofthis type has probably contributed to the fact that males in a Canadian popu-lation of bighorn sheep (Ovis canadensis) currently produce smaller hornsthan they used to, because hunters mainly have focused on hunting animalswith large trophies. In 1996 hunting restrictions were introduced, limitinghunting only to animals with fully developed horns. These restrictions aimedto protect juveniles, i.e. individuals who whose entire reproduction was infront of them. Coltman et al. (2003) demonstrated in a quantitative geneticstudy that the horn size, or more correctly the ability to produce large hornsearly, has high heritability (≈70 %). During the 30 years of this study, the ave-rage horn size decreased by one fourth in this population. As a side effect ofthe decreased horn size, the average body size also decreased during the sametime period. Furthermore, the risk that the decreased horn size also may havean effect on the reproductive success of the bighorn sheep cannot be elimina-ted, because horn size is an important character for the males when compe-ting for females during mating season (Coltman et al. 2003).

In a recent study, Mooney & McGraw (2007) investigated how selectiveharvesting affects natural populations of American ginseng (Panax quinque-folius). The roots of this perennial plant are harvested and exported to Asia,where they are used as treatment in indigenous medicine. The harvesting isdestructive (the plants die) and is focused on individuals with the largestroots, because these are easiest to find and are the most valuable. Presently,the harvesting of individuals falling below a specific minimum size is prohibi-ted. To study the effects of the harvesting, a number of experienced ginsengharvesters were contracted to find and indicate which ginseng individualsthey would have harvested in a geographic area previously unknown to them.All plants were determined as to size after survival and reproduction in theforthcoming year; a fitness value was calculated for each plant. In a scenariowithout harvesting (all plants were included in the study) fitness increasedwith plant size, i.e. natural selection favoured large plants. In the scenariowith harvesting (harvested plants excluded), the association was weak ornon-existent, as a consequence of most large plants having been “harvested”,i.e. given the fitness value 0. Evidently, natural selection for largeness decrea-sed in the harvested population. The question as to whether the altered selec-tion pressures will have any genetic effects is still unanswered, but harvestedpopulations seem to have a different variation pattern in molecular markerscompared with protected populations (Cruse-Sanders & Hamrick 2004).

A common way to harvest natural plant communities is either to take

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away a part of the biomass and give it to milk or meat producing animals ashay or green fodder, or to let the animals consume the biomass on location(using the land as pasture). The two different regimes, haymaking andpasturing, can be selective in a way that leads to increased adaptation (Snay-don 1987), which is obvious from all the different pasture and haymakingplant ecotypes developed in the Swedish flora (Chapter 7). Sometimes theharvest of biomass may decrease the genetic variation. In a Swiss study, popu-lations of the grass meadow fescue (Festuca pratensis) were compared betwe-en meadows mowed two or three times each year during a period of elevenyears. According to a RAPD marker analysis, individuals in the populationsgrowing on meadows mowed more intensely had more similar genotypescompared with individuals in populations on meadows mowed less frequent-ly (Kölliker et al. 1998).

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6. Genetic diversity andchange of habitat and climate

6.1 Local adaptation

A species can have general adaptations to survive in water, manage droughtor to use specific food items as e.g. thick coated seeds. In contrast, local adaptation is when the different populations of a species are geneticallyadapted to different environments, and this is expressed in morphology, phy-siology and/or behaviour. Local adaptation requires that genetic variation ispresent in the populations.

Local adaptation can be studied by moving individuals from a population

Summary: Local adaptation occurs when populations become genetically adaptedto different environments. Generally, the ability to adapt is larger themore genetic variation that is present in a population.

Local adaptation can be studied by moving individuals betweenpopulations and observing how these individuals survive in their newenvironment compared with the individuals that exist there naturally.Local adaptation can also be studied by observing the associationbetween the environment and the occurrence of a specific allele or aphenotypic trait. There are many examples of species in Sweden withlocally adapted populations in certain environments, e.g. the roughperiwinkle (Littorina saxatilis), the common mussel (Mytilus edulis),herring (Clupea harengus), three-spined stickleback (Gasterosteus acu-leatus), Scots pine (Pinus sylvestris) and white clover (Trifoliumrepens).

Local adaptation implies that individuals from different popula-tions are not interchangeable – locally adapted populations have a con-servation value of their own. For this reason, local adaptation is animportant issue in e.g. reintroduction and supplementation strategies.

In the future populations will have to adapt to their local environ-ments and forthcoming climate changes. The evolutionary potential ofa population is larger the more genetic variation that is present in apopulation. In many cases, Swedish populations are as genetically vari-able as populations from areas not affected by the last ice-age. Howe-ver, for each type of adaptation, specific genetic variation is needed.How this variation is distributed and exchanged between populationsthrough gene flow is largely unknown.

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to other environments and observing how they manage in their new surroun-dings. Individuals can also be moved in both directions, between two or morepopulations (reciprocal translocation). Another way to study local adaptationis to move individuals from different populations to a common location tocompare survival of individuals from diverse environments – a common gar-den experiment. In these ways it is possible to study how large a part of thephenotypic variation between individuals is based on genetic differences.Consequently, local adaptation is the genetic variation that enables success inthe familiar environment in contrast to other environments.

Apart from the genetically based local adaptation, individuals also havepossibilities for various physiological adaptations within certain limits. Localadaptation will allow populations to utilise new environments, and accor-dingly move the boundaries that restrict the physiological adaptations of apopulation. Another phenomenon causing variation among individuals andpopulations is phenotypic plasticity, which allows organisms to adjust theirphenotype according to the surrounding environment during their develop-ment. For example, fish dwelling in coastal waters often have a different bodyshape and diet compared with their conspecifics in open water.

Local adaptation is important from a conservationist’s point of view,because it will determine how far a population can follow an environmentalchange in an evolutionary perspective.

6.1.1 Transplantation experimentsA pioneer in the scientific field of local adaptation studies is the Swedishresearcher Göte Turesson (1922), who conducted transplantation experiments,moving plants of the same species from different habitat types to a commongrowth place (common garden experiment), to investigate how the plants hadadapted to their respective environments. Turesson coined the term ecotype todescribe populations of a species that are adapted to a specific habitat type.Olsson & Ågren (2002) performed a similar common garden experiment,sowing seeds of purple-loosestrife (Lythrum salicaria) from different Swedishpopulations in Umeå in northern Sweden. Several characters (growth and flo-wering period, resource allocation for winter buds and time to reproductiveage) differed between the populations in a systematic way depending on thelatitude of the original population. Other characters, as for example flowershape, varied between the populations in a more mosaic pattern.

A reciprocal translocation experiment, performed on natural grass landswith different soil types in central Sweden, recently demonstrated that popu-lations of the Carline thistle (Carlina vulgaris) were locally adapted (Jakobs-son & Dinnetz 2005). The juvenile survival of the Carline thistles was alwayshigher in the original population compared with the populations the indivi-duals were transplanted into. A common garden experiment showed thatseveral other characters also differed between the populations. Local adapta-tion was greatest in large isolated populations, and the authors suggest thatthis is because the gene flow from other populations (with other adaptations)is lower, causing the local adaptation to proceed further and more rapidly(Jakobsson & Dinnetz 2005).

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Transplantation experiments are common practise in forestry research. Atransplantation study of Norway spruces (Picea abies) from Sweden and Ger-many showed that the diameter of the resin channels varied according to theenvironment of the original population – drier environment resulted in thin-ner channels (Rosner & Hannrup 2004). Seasonal variation in starch turno-ver, associated to geographic origin, can be observed in the Scots pine (Pinussylvestris) from northern and southern parts of Europe. In a common gardenexperiment, pines from northern areas were more effective in retracting nutri-ents (nitrogen, phosphorous), from needles before they were dropped (Olek-syn 2003).

In another variant of transplantation experiments, populations with iden-tical genotypes are grown in different environments after which the potentialgenetic changes are studied after a number of generations. In one such experi-ment, a cultivated form of white clover (Trifolium repens) was planted inthree different locations: Sweden, Germany and Switzerland (Collins et al.2002). After two or three years these populations were compared with theoriginal population. The Swedish and German populations demonstrated agreater ability for adjusting leaf growth according to temperature (increasedphenotypic plasticity), and were also able to re-grow from terminal buds afterfreezing temperatures to a greater degree than the original population. Thefrequencies of favourable alleles and allele combinations had increased in the-se two populations due to natural selection, which resulted in higher levels ofsurvival.

6.1.2 Genetic differences between environments– molecular genetic markersLocal adaptation can also be studied using molecular genetic markers. If aspecific marker allele is more common in a particular environment this maysuggest that the allele is favoured by selection, either directly or indirectly (thecommon allele is linked to the gene favoured by selection). However, the stu-dy of local adaptation using this method demands several independent obser-vations, e.g. an environmental factor that varies in a mosaic pattern in a land-scape.

The above method has nevertheless enabled researchers to demonstratelocal adaptation in an environment that varies over short distances, in severalSwedish plants. For example, in the plant soft-brome (Bromus hordeaceus)(Figure 13), the frequency of specific alleles of a metabolic enzyme differedbetween subpopulations growing in an environment where water levels andsoil depth varies. The frequency differences exist although the distance betwe-en the subpopulations is short, 10-100 meters (Lönn 1993). A similar associa-tion between enzyme variation and different environmental conditions can beobserved in the grass sheep's-fescue (Festuca ovina), at the scale of 100meters (Prentice et al. 1995). These results were corroborated in a field expe-riment where nutrient and water availability was managed and varied betwe-en subpopulations (Prentice et al. 2000). In a study of the fastigiate gypsophi-la (Gypsophila fastigiata), a perennial plant in the genus baby's-breath, enzy-me alleles were associated with lichen coverage at a scale of about 50 meters

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(Lönn et al. 1996). The authors suggest that the pattern arose because of localadaptation – high lichen coverage indicates dry and warm local climate – andthe reproduction of individuals carrying the “correct” allele is superior in the“correct” environment. A similar study, using AFLP-markers instead of allo-zymes, showed that the leaf shape of thistles differs between individualsgrowing as weeds on organic farms, conventional farms, along roadsides andin natural populations. This may be due to local adaptation to the cultivatedlandscape because the shape differentiation is consistent between the popula-tions (Mikael Lönn, pers. com.). Unpublished studies of the rare plant Viciapisiformis in south Sweden show an association between AFLP-markers andthe amount of solar radiation that reaches the population (Magnus Johans-son, pers. com.).

In the brackish water of the Baltic Sea the distribution of organisms areprimarily dependent on the saline gradient. The main gradient is in the north-south direction, which might constitute a methodological problem when stu-dying local adaptation to the saline content, because it is difficult to disting-uish between saline gradient and geographic location. Several studies showthat different organisms are genetically differentiated along the saline gradi-ent, and consequently most likely locally adapted to the saline conditions ofthe Baltic Sea (reviewed in Lönn et al. 1998). A number of recent studies alsoconfirm that populations in the Baltic Sea are locally adapted (Bekkevold etal. 2005; Riginos & Cunningham 2005). Microsatellite studies of herringpopulations (Clupea harengus) from the Atlantic to the Baltic Sea, show thatfish spawning at locations that differ in saline content also are genetically dif-ferentiated (Bekkevold et al. 2005).

In the Baltic Sea, the common mussel is considered by some researchers tobe two separate species, Mytilus trossulus, widespread in the Baltic Sea and

Figure 13. The soft-brome (Bromus hordeaceus) among white stonecrop (Sedum album) on thinsoil on the heaths of Öland (Ölands alvar). (Photo: Mikael Lönn)

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M. edulis (the common mussel), mostly found towards the Atlantic Ocean.The two species of mussel hybridise with each other, and the “Atlantic” mus-sel has more “Baltic” mussel alleles the farther into the Baltic Sea the “Atlan-tic” mussels are sampled (Riginos & Cunningham 2005). M. trossulus showapparent adaptations to the saline gradient. Alleles from two enzyme loci areparticularly associated with the saline gradient, either because their functionsare directly connected to the saline content or because the alleles are linked toloci having a function relating to adaptation to saline content.

Also Baltic Sea populations of herring (Clupea harengus) display signs oflocal adaptation. A genetic difference in one microsatellite locus can be obser-ved between herring populations in the Atlantic and the Baltic Sea, but becau-se other microsatellite loci show no signs of differentiation, the genetic diffe-rence is likely due to selection on a locus linked to the microsatellite locus(Larsson et al. 2007).

6.1.3 Genetic differentiation between environments – quantitative charactersNumerous genetic studies of quantitative characters confirm that populationsof various organisms are locally adapted. A study of the Glanville fritillary(Melitaea cinxia) on the Baltic Sea island Åland, showed that groups of thebutterfly are genetically adapted to utilise only one of the possible hostplants, either ribwort plantain (Plantago lanceolata) or spiked speedwell(Veronica spicata), and that this genetic pattern coincided with the distribu-tion patterns of each plant (Kuussaari et al. (2000).

Rough periwinkles (Littorina saxatilis) can form two different variants(ecotypes) over very short distances (about 10 meters) either adapted to rockyshores (thick shells and large openings) or exposed cliffs (thin shells and smallopenings). The two variants are formed in situ (Panova et al. 2006), and thefrequency of specific enzyme alleles differs between the periwinkle ecotypes,in a way that can be expected from the functions of the different enzymes(Panova & Johannesson 2004). The periwinkle ecotypes develop in parallelin areas where these environmental contrasts are repeated in a regular way(Johannesson 2003).

Three-spined stickleback (Gasterosteus aculeatus) (Figure 14) can befound both in the Baltic Sea and in fresh water lakes. The body shapes ofsticklebacks in populations from different part of Fennoscandia were compa-red in a study by Leinonen et al. (2006). They observed apparent differencesin body shapes between populations in the Baltic Sea and fresh water lakes,and also among populations from different fresh water lakes, which suggestlocal adaptation. In contrast, no difference in molecular genetic markers wasfound between three-spined sticklebacks in the Baltic Sea and in fresh waterlakes, though small but clear differences were found between geographicalregions (Mäkinen et al. 2006).

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The winter moth (Operophtera brumata) can use several tree species ashost plants. Two of them, bird cherry (Prunus padus) and common oak(Quercus robur), differs considerably in time of leaf burst. In one study Tik-kanen et al. (2002) showed that there was a strong genetic component in hat-ching date of the moths, corresponding to the date of leaf burst of the hostplant from which the moths were collected. The moths clearly were locallyadapted to the leaf burst of their hosts.

Arabidopsis lyrata is an annual plant growing along the shores of the Bot-hnian Bay. The genetic pattern in neutral molecular markers between thepopulations is different from the pattern in leaf trichome production betweenlocalities. High levels of leaf trichome production are a successful strategyonly in certain localities – thus A. lyrata has adapted to the local environmen-tal conditions (Kärkkäinen et al. 2004).

The A. lyrata study compared the genetic differentiation (estimated as FST)between localities both for neutral molecular markers and for the gene codingfor leaf trichome production. Because the level of differentiation observed forthe gene coding for leaf trichome production was much higher (higher FST

values), the authors conclude that natural selection has acted in differentdirections in the different environments for this particular gene. Recently,similar studies comparing the levels of differentiation between neutralmolecular markers (FST) and quantitative traits (QST) have been performed instudies of Swedish populations of for example common frogs and moor frogs(Rana temporaria, R. arvalis; Palo et al. 2003; Cano et al. 2004; Knopp et al.2007), Scots pine (Pinus sylvestris; Waldmann et al. 2005), small scabiousand fragrant scabious (Scabiosa columbaria, S. canescens; Waldmann &Andersson 1998). In general, the results from these studies and studies ofother species (Merilä & Crnokrak 2001) reveal higher levels of differentia-tion in phenotypic characters compared to the differentiation observed in

Figure 14. Three-spined stickleback (Gasterosteus aculeatus). (Photo: Myra Bildbyrå)

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neutral molecular markers (i.e. QST > FST). This pattern is completely consi-stent with the frequent evidence of local adaptation, repeatedly documentedin transplantation experiments and ecotype studies.

6.1.4 The possibility of future adaptationsNumerous populations show apparent signs of local adaptation and conse-quently these populations evidently have sufficient genetic variation torespond to various selection pressures. In this context, it is interesting toknow if sufficient genetic variation exists to enable these populations torespond to future environmental changes as well. Long-term adaptive abilitiesare often measured by estimating the genetic variation expressed in phenoty-pic traits because this genetic variation is available to natural selection.However, to estimate the parameters affecting the adaptive abilities of popu-lations (genetic variance, genetic co-variance and heritability) large amount ofdata from individuals with known pedigrees are required. It has become moreand more common for researchers to use quantitative genetic methods whenstudying natural populations of plants and animals.

Birds have often been subject to quantitative genetic studies, because it isrelatively easy to follow many individuals and their mutual relations in natu-ral populations of these organisms. Over a period of 20 years, Swedishresearchers have demonstrated significant estimates of heritability for a num-ber of fitness related traits in for example the collared flycatcher (Ficedulaalbicollis; Gustafsson 1986; Merilä & Sheldon 2000), the European starling(Sturnus vulgaris; Smith & Wettermark 1995), the willow tit (Parus monta-nus; Thessing & Ekman 1994), and the great reed warbler (Acrocephalusarundinaceus; Åkesson et al. 2007). Several studies of how the expression ofgenetic variation differs between environments have also been performed(Larsson 1993; Merilä 1997; Merilä & Fry 1998; Kunz & Ekman 2000;Brommer et al. 2005).

In other organisms it has been possible to estimate genetic variationthrough experimental crossings and cultivation experiments. Studies of thecommon frog (Rana temporaria) and the moor frog (R. arvalis) have demon-strated significant estimates of heritability both for size and growth parame-ters (Laurila et al. 2002; Pakkasmaa et al. 2003; Cano et al. 2004; Merilä etal. 2004; Knopp et al. 2007), and also showed that genetic variances and co-variances can differ among populations of the same species (Cano et al. 2004;Knopp et al. 2007). In a Swedish population of the comma butterfly (Polygo-nia c-album) the females’ choice of host plants for the larvae had a geneticbackground (Nylin et al. 2005).

Many plant species have also been subject to quantitative genetic studies,especially the tree species used in Swedish forestry (Scots pine, Pinussylvestris; Norway spruce, Picea abies; and silver birch, Betula pendula etc.).Naturally, these studies often focused on the genetic variation in traits affec-ting growth and biomass production, but this variation is likely also to beimportant for the adaptation and differentiation occurring in natural popula-tions. Several Swedish studies have revealed genetic variation in ecologicallyimportant characters such as growth rate, survival, drought resistance and

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resistance to fungal diseases, in Scots pine (Pinus sylvestris; Olsson & Erics-son 2002; Andersson et al. 2003; Persson & Andersson 2003), Norway spru-ce (Picea abies; Swedjemark et al. 1998; Hannerz et al. 1999; Sonesson &Eriksson 2003) and birches (Betula sp.; Elamo et al. 2000; Stener & Heden-berg 2003).

An increasing number of quantitative genetic studies have also been per-formed in natural populations of various plant species. A study of a Swedishpopulation of narrowleaf hawksbeard (Crepis tectorum) demonstrated thatthis population contained significant genetic variation in all characters distin-guishing the different ecotypes in this species, e.g. leaf shape, plant height,flowering time and seed size (Andersson 1991). In recent times, researchershave performed quantitative genetic studies of several threatened or red listedplant species in Sweden, e.g. field fleawort (Tephroseris integrifolia; Widén &Andersson 1993), and the perennial Scabiosa canescens (Waldmann &Andersson 1998; Waldmann 2001). Other studies compared marginal popu-lations in Sweden with central populations in East and Central Europe, e.g.with the European white elm (Ulmus laevis), which also is red listed in Swe-den (Whiteley 2004; Black-Samuelsson 2006). Neither of these studies sho-wed any signs that the populations suffer from low levels of genetic variationin ecologically important traits, in spite of the fact that some of the popula-tions are far from the central distribution of the species.

Altogether, genetic variation in quantitative traits seem to be abundant inSwedish animal and plant populations, which suggests that these populationswill have the opportunity to adapt to present or future environmentalchanges. However, for individual species or populations these generalizationsare not necessarily true, and consequently most species and populationsdemand specific case studies.

6.2 Local adaptation in association withchanges of distribution and climate

The climate continuously changes and throughout time the distribution ofspecies adjusts accordingly. However, there is a huge difference between thehistoric and present situation, because today the landscape is strongly frag-mented due to human activities and furthermore there is evidence suggestingthat future climate changes may be rapid (Jump & Penuelas 2005).

Let us assume that a population inhabits a specific area when a rapidchange in climate occurs. If the individuals are unable to move away to anot-her more hospitable area, the population quickly must adapt to the new cli-mate. To be able to adapt to the new environmental conditions, sufficientlevels of genetic variation must already be present in the population. But ifthe climate change is too fast or too drastic, the survival of the populationmight depend on introduction of novel genetic variation, either by mutationsor by gene flow from other populations. However, habitat fragmentation willlimit the possibility for gene flow or dispersal, and as a consequence the

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population may be trapped without the possibilities for further adaptation.An alternative strategy for the population could be to move together with theclimate change, but habitat fragmentation will again be a problem, and sui-table habitats may lie outside the dispersal range of the species. Jump &Penuelas (2005) suggest that the combined effect of rapid climate change andhabitat fragmentation may prevent local adaptation over the entire distribu-tion area of a species, which will lead to extinction. These risks will of coursebe greatest for species with limited dispersal ranges and fragmented distribu-tions, e.g. plants and small animals (Figure 15) (see Edenhamn et al. 1999).

Joshi et al. (2001) performed an experiment investigating the local adap-tation to different climates for a number of plant species. Three commonplant species, the cocksfoot (Dactylis glomerata), ribwort plantain (Plantagolanceolata) and red clover (Trifolium pratense) were moved reciprocallybetween eight localities in Europe, of which one was in Sweden. The resultswere clear for all three species: transplanted individuals originating in geo-graphically adjacent populations managed much better compared with indivi-duals that originated in distant populations. Joshi et al. (2001) attempted toquantify a “climatic distance” between locations by calculating differences inaverage temperatures in January and July and average annual precipitation.However, these “climatic distances” had no significant effect on the success ofthe populations, while geographic distance had a clear effect. We suggest thatgeographical distance nevertheless might reflect climatic differences, becauseclimatic differences are the main factor that varies systematically with geo-graphic distance. One interesting result was that several cocksfoot and redclover populations did not survive at all in the marginal populations of theexperimental area (Sweden and Portugal), which demonstrated that not allpopulations have the genetic variants needed for local adaptation. In this

Figure 15. Dispersal ranges for different organism groups, data from Edenhamn et al. (1999). Compiled by Per Sjögren-Gulve.

Distance

Num

ber o

f spe

cies

Mammals

Birds

Reptiles

Amphibians

Terrestrial arthropods

Terrestrial molluscs

Earthworms, 3 years

Trees & bushes

Other vascular plants

Cryptogams

Lichens

Marine mammals

Fishes

Marine invertebrates

Multicellular algae

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experiment, the populations that were able to adapt to their new environmenthad previously adapted to similar conditions.

A genetic study of European beech (Fagus sylvatica) in south-westernEurope showed that a molecular marker (AFLP) was associated with presentand historical temperature adaptations in this species. The two alleles associ-ated with high and low temperatures are both found in most populations,which mean that these populations should have the ability to adapt to a chan-ging climate. However, there is a limit to how far the populations can adapt,lowland populations adapted to a warm climate have recently disappeared,and the European beech has successively spread to higher, colder, altitudes.The authors suggest that the European beech might disappear from warmerparts of the distribution area, because the genetic variation that enables theEuropean beech to cope with yet warmer climate are lacking.

A study of Scots pine (Pinus sylvestris) in Finland reveals that high levelsgenetic diversity associated with climate adaptation exist in these populations(Savolainen et al. 2004). A model based on knowledge of the genetic varia-tion in these populations in relation to the climate today shows that the gene-tic adaptation will likely fall behind the climate change. This is mainly causedby the longevity of the Scots pine, which forces genetic change in a localpopulation to move slowly. The authors suggest that one possible strategy toenable cultivated species to cope with climate change is to plant individualshaving the particular genes needed for the expected climate change in diffe-rent locations. However, they continue to emphasise that the slow adaptationwill cause major problems for wild plants, especially for species with frag-mented distributions that also have limited dispersal ranges. To what extenthumans should manipulate populations, particularly natural populations, is acontroversial issue.

6.3 Marginal and central populationsTraditionally, distribution changes due to altered climate are believed to be aresult of the movement and extinction of populations. However, in a recentpaper Davis et al. (2005) argues that evolutionary processes also are animportant component in distribution changes, because some populations thatadapt to the new environment are able to expand their distribution due to anincreased growth rate. In some cases, marginal populations may lead a colo-nisation front, but if the environmental gradient is too sharp these popula-tions might be negatively affected by gene flow either from adjacent or morecentral populations. Because a moderately fragmented landscape will decrea-se gene flow, and many populations in Sweden are at the margin of the speci-es distribution, some of these populations may play an important role in thefuture adaptation of the species.

Many marine species have a distribution limit somewhere in the BalticSea, because of the steep saline gradient in this region (Johannesson & André2006). These peripheral populations are under a strong selection pressurebecause of the environmental factors. Baltic Sea populations of several species

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generally have lower levels of genetic variability, and also show a clear geneticdistinction from populations in the Atlantic. Johannesson & André (2006)caution against using e.g. cod (Gadus morhua) from Atlantic populations tosupplement Baltic Sea populations of cod, because the Atlantic populationsare not locally adapted to the Baltic Sea and the mixing of populations mightdestroy the adaptations of the local populations.

A study of sago pondweed (Potamogeton pectinatus) showed complexresults – populations of this species display signs of local adaptation at thesame time as they demonstrate low levels of genetic variation (Santamaria etal. 2003). Sago pondweeds were sampled from several European populations(including some Swedish ones), after which they were transplanted in threedifferent localities within the sampling area. Individuals from Central Euro-pean populations managed best in all localities, which the authors explain bythe loss of genetic variation and inbreeding in southern and northern popula-tions, living in the periphery of the distribution area. However, these popula-tions are adapted to local environmental conditions, as the northern popula-tions have a time-reduced life cycle whereas southern populations are peren-nial. The authors suggest that this is a result of a combination of random andadaptive patterns. Loss of genetic variation through genetic drift and inbree-ding has made the marginal population less successful, at least when only thegeneral fitness measure “growth” is considered. However, the marginal popu-lations are also locally adapted to the seasonal variation. These results sug-gest that general fitness measures (such as growth) do not necessarily reflectthe functionality of organisms in their natural habitat.

In a genetic study of a perennial outcrossing plant, the fastigiate gypsophi-la (Gypsophila fastigiata), on the Baltic island of Öland, populations with dif-ferent levels of genetic variation (in allozyme markers) and different geograp-hic position (central/peripheral) were compared (Lönn & Prentice 2002).Results showed that peripheral populations were genetically different fromeach other, and had lower levels of genetic diversity compared with centralpopulations. Additionally, the peripheral populations had a more rapiddemographic turnover. Lönn & Prentice (2002) suggest that this pattern aro-se because peripheral populations inhabit habitats that are marginal in tworespects, firstly because they reside at the geographic limits of the species andsecondly because these populations might also be relatively short-lived (Lönn& Prentice 2002). The results from this study suggest that marginal popula-tions are dynamic, have rapid turnover and are genetically divergent fromeach other.

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7. Genetically distinct populations in Sweden

Summary:In Sweden there are few endemic taxa at the species level and those thatexist arose relatively recently through local processes such as hybridisa-tion and polyploidisation. At the same time there are many geneticallydistinct populations in Sweden. Populations are different because theyhave different origins, colonisation routes or because they are adapted totheir local environments. Taxonomic units as species, varieties andforms, together with informal genetic entities such as evolutionary signi-ficant units and management units reflect genetic differentiation that hasarisen within or outside the borders of Sweden. Genetically differentiatedgroups can be difficult to distinguish morphologically (they are cryptic),but molecular genetic studies have provided strong evidence for ”hid-den” genetic structure in Swedish taxa.

Lönn et al. (1998) called attention to the fact that species having theirmain distribution in Sweden are not necessarily marginal populationsfrom a genetic perspective. In contrast, species mainly distributed insouthern areas are represented by marginal populations in Sweden andhave lower level of genetic diversity. Recent studies confirm that in manycases Swedish populations are as genetically diverse as populations inareas not covered with ice during the last glaciation. Furthermore, recentinvestigations also verify that populations from the islands Öland andGotland, the Baltic Sea with the surrounding coastal areas, the mountainareas and some traditionally managed landscapes, are often geneticallydistinct. Each population that is lost means loss of genetic variation andconsequently loss of adaptive potential. For the purpose of conservinggenetic resources, populations or groups of populations are the naturalconservation units, because genetic variation occurs both within andbetween populations.

In this chapter we also formulate research questions for the future:On what level can genetically functional units be found in different speci-es? Some studies exist but several organism groups, e.g. insects, moss andlichens, are underrepresented in this respect. What role may geneticallydistinct populations in Sweden play to enable species to meet large-scaleclimatic and environmental changes? Is there sufficient genetic variationin relevant ecological traits to enable species to adapt to rapidly changingenvironments? Which populations are most valuable in this respect –central populations or those at the periphery of the distribution? Is therea risk that genetically distinct populations will disappear in those habi-

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7.1 Genetic or taxonomic variation? How to define what constitutes a species is under a continuous debate amongresearchers, because no unambiguous definition exists in nature. One defini-tion that works well in most cases is the biological species definition – a speci-es consists of individuals that produce fertile offspring under natural condi-tions. However, under certain circumstances the biological species definitioncan be problematic, for example if we consider a species with vast distribu-tion, where populations far apart are clearly different and can not reproducewith each other. The biological species definition can also be problematic fororganisms such as bacteria and viruses, which reproduce and exchange gene-tic material in a different way from species with two sexes. Naturally, thereare also genetic differences between species, but in conservation genetics thegenetic variation within species is the main concern. Traditionally variationwithin species is studied in the field of systematics, where researchers disting-uish groups due to morphological characters that differ between them. Thus,within a species there may exist: subspecies, sections (asexually formed speci-es within certain species complexes where several morphologically distinctclones can be distinguished, e.g. in dandelions, Taraxacum), races (geograp-hic groups), varieties and forms.

Evolutionary ecologists primarily describe genetic variation within speciesin association with environmental variation. Groups within a species that areadapted to specific environments e.g. dry habitats, sea shores or lime-richland are termed ecotypes. If the adaptation is local and temporary the groupis called an epitype.

With molecular genetic methods it is possible to trace which populationsshare an evolutionary history. In systematics these groups are called cladesand some researchers suggest that these clades should be the criteria for defi-ning species – a cladistic species definition.

From the perspective of conservation biology, historically separatedgroups within a species are called evolutionary significant units, ESUs(Moritz 1994). An ESU can consist of many individuals and populations. Inconservation projects, it is useful to know which parts of an ESU act as sepa-rate biological units and therefore should be managed separately. This can beevaluated by investigating how demographically independent the groups are,i.e. if it is events within the group (births and deaths) that determine the sizeof the group, or if for example immigration from other groups are a moreimportant factor. Groups with an independent demography are distinguishedas management units, MUs. Generally, it is difficult to observe if an individu-

tats that supposedly will be most affected by global warming? Whichgenetic methods are most relevant for assessing evolutionary potential?How will genetic variation of key species in important Swedish eco-systems affect the function, species composition and stability of theseecosystems?

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al is born in a population or if it has reached the population through migra-tion, hence genetic methods are often used to identify management units. In arecent paper, Palsbøll et al. (2007) discuss what distinguish a MU in geneticterms. The authors point out that even if two groups are significantly diffe-rent genetically they are not necessarily two separate management units, andsuggest that the boundaries are set also using demographic data. They propo-se that groups with less than 10 % immigration per generation can be consi-dered as separate management units, but the boundaries should of course bedifferent for different species, geographic areas and management actions.

Moritz (1994) defines evolutionary significant units on the basis of theirevolutionary history, which mainly is equivalent to a species in the cladisticspecies definition. A different way to define an evolutionary significant unit isto state that they should neither be exchangeable ecologically (they shouldhave different adaptations) nor genetically (the gene flow should be limited)(Crandall et al. 2000). The latter way of defining an ESU is closer to the biolo-gical species concept – and to the definition of management units – where unitsare recognized because of function instead of evolutionary history. The defini-tion of evolutionary significant and managements units will continue to beunder debate. Laikre et al. (2005b) point out that because different types ofpopulation genetic structure exist in natural populations (distinct, continuousand unstructured), obvious units are difficult to distinguish in many cases.

In a study of the northern pike (Esox lucius) in the Baltic Sea, manage-ment units are defined for the benefit of commercial fishing (Laikre et al.2005a). Based on the association between genetic distance (using microsatelli-tes) and geographic distance, the authors found that the populations weregenetically differentiated at a distance of 100-150 kilometres, which they sug-gested is the size of management units.

From the perspective of the conservation of genetic variation, all groupswithin a species are important regardless of how they are distinguished – allgenetically differentiated groups are important to conserve because they holda part of the total genetic variation of a species. Therefore, the conservationof species must also include the conservation of the genetic variation within aspecies. A species can be regarded as the sum of all genetic variation found inall its populations, without this variation the species can not continue to evol-ve and adapt. An example of this viewpoint is the conservation of the white-tailed eagle (Haliaetus albicilla), where local conservation projects in nort-hern Europe have succeeded in preserving a larger part of the genetic varia-tion of this species than the original plans to only protect the large and viablepopulation in Norway would have managed (Hailer et al. 2006).

Studying the genetic variation within species may enable the discovery ofdifferences that are not apparent in the morphology of a species. Within thecommon variety of the fragrant orchid (Gymnadenia conopsea var. conopsea)– a morphologically congruent group – two strongly genetically differentiatedgroups can be distinguished: an early and a late flowering group. Furthermolecular studies showed that the late flowering conopsea group was geneti-cally different from another late flowering G. conopsea variety named densif-lora. The level of differentiation corresponded to what normally is expected

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between two different species. In contrast, the early flowering conopseaplants were genetically more similar to another species of orchid G. odoratis-sima, but differentiated from their late flowering conspecifics (var. densiflo-ra). To treat the fragrant orchid as one species in conservation context isincorrect because the differentiation is between the early and late floweringgroups (Gustavsson & Lönn 2003).

Within the rusty peat moss (Sphagnum fuscum) two genetically differenti-ated groups can be distinguished within the same bog. The genetically diffe-rentiated groups are associated with variation in the environment, which dif-fers in pH and ground water level (Gunnarsson et al. 2007). It is likely thatgenetic studies within other species also will give similar results.

7.2 The conservation value of Scandinavianpopulations

All terrestrial species presently in Scandinavia arrived in this region after thelatest ice age (Lönn et al. 1998). Taxonomic groups that only exist in Scandi-navia are either on a lower taxonomic level than species or are recently crea-ted species, so called micro-endemes. Thus, the genetic distinctiveness ofScandinavian taxa was mainly created by in situ evolutionary processes. Noknown species exist in Sweden without occurring elsewhere, which is not sur-prising because similar environments also exist in the neighbouring geograp-hic areas.

Occasionally people argue that Swedish populations have low conserva-tion value, because the next ice age will eliminate all Swedish populations asthey will not have time to spread to glacial refugia situated in southern partsof Europe. However, there is no scientific evidence for this argument – alllocally adapted populations, varieties, ecotypes and micro-endemes that arosein Scandinavia may well be essential parts of the regional biodiversity duringor after the next ice age.

Species favoured by a warm climate often survived the last glacial maxi-mum in refugia in Southern Europe, which might be difficult for Swedish spe-cies to reach. Recent studies, however, show that some plant species, mainlydistributed in areas with cold climates, survived in glacial refugia at muchhigher latitudes than previously thought (Palmé 2003a, 2003b). The same isalso true for larger animals because of their ability to move.

Apart from the ice-age perspective there are of course many other reasonsto conserve biodiversity. One common motive for conserving species is thateach species has a value of its own. Species conservation can also be motiva-ted because the species has, or under other circumstances may have, animportant function in a process, e.g. it may be important for the function ofan ecosystem or for regulating the population size of a harmful organism.The conservation of genes and alleles can be motivated in a similar way. Forexample, genetically distinct populations in Sweden, as populations from theBaltic islands of Öland and Gotland, the Baltic Sea with surrounding coastal

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areas, the mountain areas and some traditionally managed landscapes areimportant to conserve because they have a value of their own (Lönn et al.1998). Part of their distinctness has arisen through isolation, or because thepopulations have adapted to novel environments. From a functionalistic per-spective, alleles are important because of their present functions, because theymight enable adaptation to a changing environment and because they mightbe a starting point for species formation. In addition, alleles can affect thedemography of populations and the relationship between species in an eco-system (Chapter 2). Also populations can be valuable from different perspec-tives: those that are already adapting to a specific environment are importantif the environment continues to change in the same direction, while popula-tions that at the moment are slightly maladapted might be starting points forecological species formation, because these populations have the possibility toinvade novel environments (Levin 2003).

The genetic variation within species that are common in Sweden shouldbe considered a valuable resource – it might be among these that we find thepopulations that are adapted to specific environments, or the populationsthat have the genetic variation needed to meet future environmental and cli-mate change (see for example Gustavsson 2001; Palmé et al. 2003 a, 2003b;Garkava-Gustavsson 2005; in the next section). In a longer time perspective,these populations might be the survivors of the next glacial maximum. Forarctic species such as lemmings (Lemmus) (Figure 16), the ice age refugia aresituated close to the ice edge, and Swedish populations of these species are animportant genetic resource for their conservation in a very long time perspec-tive (Fedorov et al. 2003).

Figure 16. The lemmings (Lemmus) have a northern distribution and the Swedish populations arean important part of the world population. (Photo: Myra Bildbyrå)

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7.2.1 Endemism in Scandinavian vascular plantsA complete review of the endemic vascular plant taxa (species or taxa at alower level only present within a certain geographic area) in the Nordiccountries can be found in the “Flora Nordica” (Jonsell 2004). The authorreports 127 endemic taxa (46 species, 45 subspecies and 32 varieties) in theNordic countries. Of these, 77 taxa are present in Sweden, most occurring inthe mountain areas, in the Baltic seas and the surrounding costal areas, on theislands Öland and Gotland, and on some traditionally managed landscapes(for a overview see also Lönn et al. 1998). The endemic taxa in Sweden wereformed after the last ice age, and many of them are not dissimilar enoughfrom others to be considered species. New plant species are generally formedby polyploidisation after hybridisation (allopolyploidisation), asexual repro-duction (sections) and ecotype formation. In Scandinavia, ecotype formationis more common than the creation of species through geographic isolationfollowed by differentiation; an apparent example of ecotype formation is thesmall annual eyebright species Euphrasia bottnica.

Two of the varieties referred to as Swedish endemes in Jonsell (2004),were part of a genetic study of five morphological eyebright varieties (Euph-rasia) on the Baltic island Gotland (Kolseth & Lönn 2005). One of the varie-ties E. stricta var. suecica also was genetically distinct; while in contrast oneother variety E. stricta var. gotlandica appeared to be a local adaptation, for-med on location by populations of E. stricta var. stricta. The relationshipbetween the two former varieties is under further investigation.

A rare variety of the grass-species Arctophila fulva var. pendulina is ende-mic to the Bothnian Bay. Genetic studies (AFLP) demonstrated small geneticdifferentiation between populations, but strong demographic dynamics –populations move around in the landscape (Kreivi et al. 2005). The authorssuggest that in this particular case it is more important to conserve the habi-tats rather than the individual populations.

7.2.2 Genetic studies of terrestrial plants and animalsIn the two following sections, we give a few examples of genetic studies thathave been performed after the publication of the review “Genetic differentia-tion of Swedish populations of plants and animals” (Lönn et al. 1998), whichare not discussed elsewhere in this report.

The genetic variation of spring peas (Lathyrus vernus) from populationsin the Czech Republic, southern and central parts of Sweden was investigatedusing allozymes. The level of genetic variation did not differ between popula-tions, and was also independent of the population sizes (Schiemann et al.2000).

In Sweden the rare orchid Gymnadenia odoratissima can be found in twoprovinces in south Sweden (Östergötland, Västergötland) and on the Balticisland Gotland. The island populations show higher levels of genetic variabi-lity and also exchange alleles to a larger extent, compared with the mainlandpopulations (Gustafsson & Sjögren-Gulve 2002).

A recurrent theme in genetic studies is the question as to whether Scandi-navian populations are more or less variable compared with populations in

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Central Europe. There is no unambiguous answer to this question, but thereare tendencies that populations on the margin of their distribution often showlower levels of genetic variation (Lönn et al. 1998). Contrasting results can befound in genetic studies of the grass bearded couch (Elymus caninus) (Diaz etal. 1999). Allozyme variation in 54 bearded grass populations in Eurasia wasinvestigated, and the most variable populations were found in the Nordiccountries. The genetic variation of a related grass species, E. alaskanus, witha northern distribution was generally low – no genetic variation was observedwithin the populations in Sweden, Russia and Iceland. However, geneticallyvariable populations were found in Norway.

A genetic study of the lingonberry (Vaccinium vitis-idaea) showed thatNorwegian populations are genetically differentiated from Swedish and Fin-nish populations (Garkava-Gustavsson et al. 2005). If an artificial “popula-tion” of lingonberry had to be created for conservation purposes, with theaim to preserve as much genetic variation as possible, the researchers wouldhave to include individuals from all countries included in the study (Sweden,Finland, Norway, Estonia and Russia). The lingonberry mainly has a nort-hern distribution and valuable genetic variation in different characters suchas size, height and berry production was scattered over the entire distributionarea and furthermore the genetic variation was often associated with the lati-tude of the population (Gustavsson 2001). In contrast, there are examples ofother Swedish boreal plants that neither have a clear genetic structure norshow any signs of decreased genetic diversity towards the margins of the dis-tribution, e.g. wood millet (Milium effusum), fingered sedge (Carex digitata)and mountain melick (Melica nutans) (Tyler 2002; Tyler et al. 2002).

Chloroplast DNA variation in the silver birch (Betula pendula) revealedthat the birches are most genetically variable towards the northern part oftheir distribution (Palmé et al. 2003a). Silver birches are adapted to cold cli-mates and according to the study, the Scandinavian birch populations are notderived from the glacial refugia in Southern Europe, (as are oak and beech,which are adapted to warmer climate), but likely recolonised Scandinaviafrom glacial refugia situated further north. Also sallow (Salix caprea) is sug-gested to have survived the last glacial maximum in glacial refugia in CentralEurope (Palmé et al. 2003b).

The hazel (Corylus avellana), which is adapted to a warm climate, showsa pattern where marginal populations (in central Sweden) are less variableand more differentiated from each other compared with central populationsin continental Europe (Persson et al. 2004). The hazel is suggested to haverecolonised Scandinavia from glacial refuges in Southern Europe.

An epiphytic bryophyte Leucodon sciuroides, showed lower levels ofgenetic variation in Sweden compared with populations in southern parts ofEurope (Cronberg 2000).

Many species recolonised Scandinavia both from the south-west and fromnorth-east after the latest ice-age. The two colonising fronts met in a hybridzone in north Sweden. This genetic pattern can be observed in for examplethe mountainous plant alpine mouse-ear (Cerastium alpinum; Berglund &Westerbergh 2001); the plant Nottingham catchfly (Silene nutans; van Ros-

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sum & Prentice 2004), and the field vole (Microtus agrestis; Jaarola & Searle2002) (for a review see Lönn et al. 1998).

Genetic variation of the European lynx (Lynx lynx), was comparedamong populations in Sweden, Norway, Estonia and Latvia (Hellborg et al.2002). Both mitochondrial DNA and nuclear microsatellites showed that theSwedish and Norwegian populations were less variable than populations inFinland and the Baltic states. The authors suggest that the lynxes recolonisedScandinavia from the east, and argue that two separate colonisation routesare a less likely scenario for this species. The recolonisation process resultedin a loss of genetic variation for the Scandinavian lynx populations. Presently,the Scandinavian populations are so genetically different from the neigh-bouring populations that they should be regarded as separate managementunits.

Another large predator, the wolverine (Gulo gulo), is genetically lessstructured in Scandinavia than elsewhere, due to high levels of gene flowamong the populations (Walker et al. 2001).

The arctic fox (Alopex lagopus) has decreased drastically in Sweden(Dalén et al. 2006). Using microsatellite variation, four populations can bedistinguished among arctic foxes in Scandinavia. Furthermore, these popula-tions are genetically differentiated from the geographically adjacent Russianpopulations. Presently, the gene flow between Scandinavian and Russianpopulations is very small and from a conservation aspect they are demograp-hically separated and should be treated as separate management units.

A genetic study of the white-backed woodpecker (Dendrocopos leucotos)compared populations from Sweden, Norway, Poland and Latvia (Ellegren etal. 1999). The Swedish populations only showed marginally lower levels ofgenetic variation compared with the other populations, despite the fact thatthe white-backed woodpecker almost has disappeared from Sweden. Theonly populations that were clearly genetically differentiated from each otherwere the Polish and the Swedish populations. The aim with this study was toevaluate if it was possible to supplement Swedish populations of white-back-ed woodpeckers with individuals from northern Europe, and the investigationdid not reveal any facts that suggest that this should not be done. However, itis important to keep in mind that the populations still might have differentecological adaptations because these differences might not be detectable onlyusing molecular markers.

The capercaillie (Tetrao urogallus) is a large grouse species whose centralpopulations are situated in Sweden. Microsatellite variation shows that thesepopulations have high levels of genetic variation compared with the small iso-lated populations in the Pyrenees and Central Europe (Segelbacher et al.2003).

Variation of the Major Histocompatibility Complex (MHC), a genefamily involved in the immune system in most vertebrates, is often the objectof genetic studies. Genetic variation at one MHC-locus in the great snipe(Gallinago media), showed that individuals from populations in Scandinaviaand the Baltic states were clearly differentiated (Ekblom et al. 2007). Becausethe differentiation at the MHC-locus is much higher compared with differen-

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tiation at neutral microsatellite loci, the authors suggest that natural selectioncreated the differences in MHC-loci between the geographic regions. Anothergenetic study of the same populations showed that the differentiation inquantitative characters such as tarsus length and plumage ornamentation ismuch larger than the differentiation at neutral molecular marker loci, whichindicates that the great snipe populations is locally adapted at the regionallevel (Sæther et al. 2007).

A study of microsatellite variation among Swedish populations of thecommon frog (Rana temporaria) revealed genetic differentiation at all studiedgeographic distances (the smallest distances varied from 5 to 20 km) (Johans-son et al. 2006). Furthermore, the level of genetic variation was lower amongpopulations at the northern edges of the distribution area, and the authorssuggest that this is because the population sizes decrease towards the northand genetic variation has been lost due to the random genetic drift.

Genetic differentiation between populations of pool frogs (Rana lessonae)from Sweden, Russia, Latvia and Poland was investigated using three diffe-rent molecular markers – allozymes, mini- and microsatellites (Tegelström &Sjögren-Gulve 2004). The study revealed that the Polish pool frogs had thehighest levels of heterozygosity, and that the marginal populations in Swedenand Russia had the lowest heterozygosity levels. The genetic differentiationwas however largest between the Swedish and Russian populations, both ofwhich had alleles not found among Polish pool frogs.

A study of twelve banded demoiselle (Calopteryx splendens) populationsfrom south Sweden revealed clear differences both in morphological charac-ters and in molecular markers (AFLP) among the populations (Svensson et al.(2004). The results demonstrated that the longer the geographical distancebetween populations, the greater were the genetic differences, which showthat dispersal abilities can be limited even in winged insects (Figure 17).

Figure 17. Banded demoiselle (Calopteryx splendens). (Photo: Myra Bildbyrå)

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7.2.3 Genetic studies of aquatic plants and animalsBladder wrack (Fucus vesiculosus) is an important component in the eco-system of the Baltic Sea. In northern parts of the Baltic Sea a dwarf form of thealgae exists, which has special adaptations for asexual reproduction enablingsurvival even in this region, which has the lowest salinity levels in the distribu-tion of the bladder wrack (Tatarenkov et al. 2005). Recently, this dwarf formhas been recognised as a separate species F. radicans (Bergström et al. 2005).

Results from a microsatellite study of the herring (Clupea harengus) hasenabled researchers to split the total Baltic Sea population into three clearlyseparated populations with only small amount of gene flow between them.The borders between the three populations coincide both with the steep salinegradient in the south-west and the boundary between the Baltic Sea and theBothnian Sea (Jørgensen et al. 2005).

The mussel Baltic telling (Macoma balthica) occurs in many of the world’soceans. Luttikhuizen et al. (2003) demonstrated that genotypes found in theBaltic Sea also can be found in Alaska, but have not been observed in betwe-en. Consequently, the Baltic tellings from the Baltic Sea belong to an evolutio-nary linage colonising this region long before the latest ice age, and are notderived from evolutionary lineages in the east Atlantic.

7.3 Research progress and continued lack of knowledge

In 1998, the review “Genetic differentiation of Swedish populations of plantsand animals” was published (Lönn et al. 1998). This report focused on gene-tic variation that was distinct for Swedish populations, and also on geneticdifferences among populations within Sweden. The present report has aslightly different angle and instead focuses on the conservation of geneticvariation. Naturally the two subjects overlap to some extent – it is of courseimportant to know if genetic variation shows any signs of distinctness or iftwo populations are genetically different even from the perspective of conser-vation genetics. However, there are aspects that separate the two angles. If theobjective is to conserve the genetic diversity within a species, we must preser-ve not only genetically distinct populations but also populations with highlevels of genetic variation. There may sometimes be a contradictory relation-ship between populations that are genetically distinct and populations thatshows high levels of genetic variation.

Lönn et al. (1998) called attention to the need for identifying evolutionarysignificant units and management units for Swedish populations, but alsooutlined some general conclusions about the genetic distinctness of Swedishpopulations. Since then genetic studies have confirmed many of the patternsindicated in this report (Lönn et al.1998). For example, several more Swedishspecies can be separated into two different evolutionary lineages that respecti-vely recolonised Scandinavia both from the northeast and the south-west.Furthermore, for many species these two evolutionary lineages meet in nort-

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hern or central Sweden. In addition it has been confirmed that some speciesof mussel are part of very old glacial dynamics in the Baltic Sea, and belong tovery old evolutionary lineages that recolonised the Baltic Sea long before thelast ice age. Also, several studies confirm that populations on the Baltic Seaislands Öland and Gotland often are genetically distinct.

Management units have been identified in some fish species, because thesepopulations are strongly affected by harvesting. How to define managementunits under natural conditions is still under debate – when should a populationbe considered demographically independent? Most likely no general answersexist, but different species and environments demand specific definitions.

Lönn et al. (1998) also concluded that there was a need for genetic studiesof forest trees. In recent years several studies have demonstrated that there isa difference between tree species adapted to a warmer climate – in Swedenrepresented by populations toward the northern limits of their distribution –and tree species adapted to colder climate. Generally, tree species adapted towarm climate have recolonised Scandinavia from glacial refugia situated inSouthern Europe, and often have low levels of genetic variation compared topopulations in Central Europe. In contrast, tree species adapted to colder cli-mate are as genetically variable as trees in surrounding geographic areas, andlikely survived the last glacial maximum in refugia closer to the ice edge.

In other studies, researchers have shown that several forest dwellingplants demonstrate high levels of genetic variation that does not seem to dec-rease, despite these plants existing at the edge of their distribution. Also, theforest dwelling capercaille shows high levels of genetic variation comparedwith populations in Southern Europe.

Information about the genetic variation in mosses, lichens and fungi is,with a few exceptions, still very limited.

Several recent studies also show that many Baltic Sea populations of diffe-rent organisms are genetically distinct compared with Atlantic populations ofthe same species, thus confirming the conclusions of Lönn et al. (1998).

In their report, Lönn et al. (1998) requested studies investigating the rela-tionship between habitat variation and the genetic distinctness of popula-tions. There are many populations in Sweden that are locally adapted compa-red with other populations, both in Sweden and in Europe. However, infor-mation on the existing adaptations to environmental types especially com-mon in Sweden is still missing. Even though organisms in the Baltic Sea arefairly well studied in comparison with most habitats, this sea is both impor-tant and exceptional and there is still a need for much more information.There is also a lack of studies of populations in the coastal areas surroundingthe Baltic Sea. Furthermore, information is lacking about the mechanismsthat enable local adaptation or the mechanisms that cause some populationsnever to adapt to their local environment.

There is a deficiency of general studies of the importance of marginal popu-lations in adaptation to future environmental changes, as well as studies of theassociation between local adaptation and dispersal in marginal populations.

Increased knowledge about the genetic variation behind ecological charac-ters and evolutionarily important traits is especially important, but studies

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answering these questions are few (Vasemägi & Primmer 2005). The authorssuggest nine research strategies that can be used to identify loci with ecologicalfunction. In one type of strategy the genetic variation of many loci is studied todetect if some loci deviate from the genetic structure shown by neutral molecu-lar markers. Other methods study RNA – (the products of DNA) and proteins(the products of RNA) to identify which genes are active in different environ-ments. A third group of methods studies the variation of a large number ofmolecular markers to find out which are associated with a particular phenoty-pic trait or associated with individuals living in a particular environment. Thefirst methods show which parts of the DNA sequence are under selection pres-sure, but fail to identify which environmental characteristics induce this selec-tion pressure. In contrast, the last group of strategies reveals which environ-mental factors cause selection to vary between the different DNA variants, butthe association with the DNA sequence variation underlying these effects isweak. None of the nine strategies is optimal on its own, and which strategy orcombination of strategies to use depends on the question being asked. Howe-ver, it is important to note that all the methods suggested by Vasemägi & Prim-mer (2005) mainly show ongoing or historical effects of selection and do notnecessarily point to variation that might be needed in the future.We would like to see more genetic research regarding the following generalquestions:1. At which spatial levels do genetically functional units exist? The units in

question can be evolutionary significant units, management units, regio-nal or local populations, ecotypes etc. What differences exist between spe-cies and groups of species?

2. What types of genetic variation is unique from a Swedish /European/world perspective? It may be adaptations to particular habitat types asfor example coastal areas, land rising from the sea after the last glaciation,or adaptations to the brackish waters of the Baltic Sea. Do unique evolu-tionary lineages exist on the Baltic Sea islands, in the agricultural landsca-pe and in the mountain region? Endemic species or varieties? Some studiesalready exist, but many organism groups are still underrepresented(insects, moss, lichens, fungi), and also common species whose popula-tions may be genetically distinct.

3. What is the association between local adaptation, evolutionary potential,habitat fragmentation and gene flow? This is especially important for spe-cies that presently are suffering from habitat fragmentation and for margi-nal populations that are undergoing distribution changes due to environ-mental changes, as for example the ongoing climate change.

4. How can we effectively measure genetic variation to mirror the functionalaspects of genetic variation, as local adaptation, evolutionary potential,inbreeding depression and hybridisation? How do molecular markers,gene functions, quantitative and morphological variation connect to eachother and to different evolutionary processes? Which methods should beused in a genetic monitoring programme?

5. How does the genetic composition of the key species in important Swe-dish ecosystems affect the function, species composition and stability ofthese ecosystems?

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8. Genetic monitoring

All countries agreeing to conserve and sustainably use biological diversity, accor-ding to the Convention of Biological Diversity, have the responsibility to conser-ve biological diversity at all levels recognised by the convention: the ecosystem,species and genetic levels. To be able to conserve the genetic variation of wildplant and animals we must know where to find the genetic variation that is espe-cially important to conserve. In 2006, The Swedish Environmental ProtectionAgency received a government commission to develop a national action plan forthe conservation of genetic diversity in wild plants and animals, in consultationwith the Swedish Board of Agriculture, the Swedish Forest Agency, the SwedishBoard of Fisheries and the Swedish University of Agricultural Sciences. Thisnational action plan should (among other things) include routines for a geneticmonitoring programme, in order to discover “unnatural” genetic changes andalso to be able to follow up the effects of different conservation actions.

Ten years ago Laikre & Ryman (1997) wrote a report where they emphasizedthat general knowledge about the genetic diversity of Swedish species was limited

Summary: The immediate need for a genetic monitoring programme in Swedenwas the main conclusion in a report by Laikre & Ryman (1997),published by the Swedish Environmental Protection Agency. There isstill a need for a centrally organised genetic monitoring programme.Our suggestion is largely based on the proposal made in 1997, and isintended as an updated starting point for more detailed discussions ofprogramme design.

We propose that the monitoring programme should focus on sixdifferent types of taxa (species or groups of populations within species),for example taxa with negative population trends, and taxa that areharvested by humans. One of the most important issues for the moni-toring programme is to establish procedures for collecting and storingdifferent types of biological material, e.g. tissue samples, which can beused in genetic investigations. It is very important that the storing ofthe biological material does not in any way limit which methods can beused in future investigations. The types of molecular methods thatshould be used in the genetic monitoring must be chosen according tothe species and the question that needs to be answered. Quantitativegenetic methods may also be used in genetic monitoring.

We suggest the establishment of a common database for biologicalmaterial stored in different museums, and we also suggest a formalisedsystem where researchers can report when collected biological materialno longer can be stored locally and therefore could be offered to themuseums.

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and that there was a need to monitor the genetic diversity of certain species. Alt-hough many genetic studies of Swedish organisms exist, most scientific studiesmay not necessarily be useful in the context of genetic monitoring, because manystudies do not reveal the genetic population structure over as large geographicareas as demanded by a genetic monitoring programme. In 1997, when the reportwas published, no general genetic monitoring programmes existed in the world(Laikre & Ryman 1997). As far as we know, no centrally organised general gene-tic monitoring programmes exists even today, although centrally organised gene-tic studies are performed in many countries, sometimes even regularly.

In Sweden, regular investigations of the genetic variation in populations ofsome fish species are performed (e.g. salmon, Salmo salar; brown trout, Salmotrutta; wels catfish, Silurus glanis) (Torbjörn Järvi, pers. com.). Also, specificcod (Gadus morhua) populations have been sampled to investigate geneticstructure (Mattias Sköld, pers. com.). Apart from these minor projects, themost extensive long-term scientific study of genetic variation in the world iscurrently performed in Sweden. The objective of the project is to monitor thechanges in genetic variation over time in natural and introduced populations ofbrown trout (Salmo trutta) (see e.g. Jorde & Ryman 1996; Laikre et al. 1998;Palm et al. 2003). This study has been going on since 1979; samples have beentaken each season and are stored at -70°C. The project is headed by a researchgroup at Stockholm University, and even though the project has been financedfrom time to time by the Environmental Protection Agency, no permanent fun-ding exists. As a consequence no guarantees exist that the project or the tissuecollection will remain in the future.

We believe that a general genetic monitoring programme for Swedish taxa isstill of immediate importance. In this section we present some ideas about how amonitoring programme might be designed. Our suggestions are neither exhau-stive nor worked out in detail, but may act as a basis for further discussions.

8.1 Which taxa are in need of genetic monitoring?

We believe that some Swedish taxa must be monitored genetically within the fra-mework of national action plan. It is important to try to define which taxa ofwild plants and animals are in need of a systematic genetic monitoring program-me. In this chapter we will use the term taxon/taxa to emphasize that the moni-toring programme in many cases must be limited to populations (or groups ofpopulations) that do not have a taxonomic status (subspecies or variety). Howwill we identify the taxa that specifically need genetic monitoring? In some casesthere are scientific studies that indicate that the genetic variation of a populationis especially important to conserve. Some populations may have specific traitse.g. ability to survive in environments where other populations of the same speci-es have difficulties to survive. In other cases the populations may be importantbecause they contain a large part of the genetic variation of a species. However,for most organisms the genetic variation is unknown for the main part of the dis-

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tribution area, and it may not be feasible to perform genetic studies for all speci-es in a country, within reasonable time (Laikre & Ryman 1997).

Laikre & Ryman (1997) outlined a genetic monitoring programme sugges-ting regular genetic "inventories" of certain species and also emphasized theneed for long-term studies of genetic variation in natural populations. Theirproposal is still of immediate importance, and is the basis of the list of specieswe recommend should be the focus of a genetic monitoring programme, presen-ted below. Some items on this list (1-4, 6) are fully or in part based on the pro-posal of Laikre & Ryman (1997).

We suggest that the monitoring program first and foremost should focus oncollecting samples of the taxa in question, to be stored centrally. This will enab-le a genetic investigation, either immediately or in the future when a genetic stu-dy for some reason or another becomes desirable. We recommend that a selec-tion of the following taxa should be part of a genetic monitoring programme:

1) Swedish taxa with negative population trends. This includes populationsor species where a long-term decrease in population size or number withinthe natural distribution area can be observed. Even if another populationreplaces a population that disappears, this might (most likely) mean thatgenetic variation is lost.

The key to monitoring populations within this group is of course to iden-tify a long-term negative population trend. We will return to this in section 8where we will present some suggestions.

2) Swedish taxa with small population sizes. Two types of species are in thiscategory; species with a small total population size (about 1000 individualsor fewer; Laikre & Ryman 1997), and species that may have large total cen-sus size, but where the population distribution is so fragmented that the geneflow is strongly reduced. Laikre & Ryman (1997) emphasize that the speciesin this category should not be the object of genetic "inventories", becausesmall population sizes inevitable result in loss of genetic variation. The moni-toring should instead be a basis for future conservation actions, e.g. if thepopulations become so small or inbred that it might be desirable to supple-ment them with individuals from other, genetically similar, populations.

3) Swedish taxa risking unwanted gene flow or hybridisation with other spe-cies or populations, due to human influence. Species that are influenced bygene flow because humans actively introduce or move individuals betweengeographic regions belong to this category (Laikre & Ryman 1997; Laikre &Palmé 2005). Wild species that are at risk of coming into contact with dome-sticated populations, including genetically modified organisms (GMO; Palm& Ryman 2006), also belong to this category, as well as species risking hybri-disation because of human mediated distribution changes.

4) Swedish taxa that are harvested. This category includes species where theharvest in itself may have an effect on the genetic diversity of the species orpopulation, and involve species that are hunted, fished and logged (Laikre &Ryman 1997).

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5) Swedish taxa where the genetic diversity might be affected by other humanactivities. According to Swedish law, Environmental Impact Assessmentsmust be carried out when human activities that might have an impact on thebiological diversity are planned, e.g. when constructing a road. This assess-ment should present what effects the activity is expected to have on the biolo-gical diversity, of which the genetic diversity is a part. However, it is likelythat the Environmental Impact Assessments investigators in most cases disre-gard the fact that the genetic diversity of populations must also be taken intoaccount.

It is especially important to consider the genetic variation of populationsin cases where the variation might be particularly important for a species, e.g.when populations are genetically distinct or when populations contain a largepart of the genetic diversity of a species in the area under investigation.

6) Swedish taxa that are subject to different types of conservation actions.This category includes populations that are supplemented with individualsfrom other populations, or species or populations that are reintroduced intoareas where they previously used to exist (Laikre & Ryman 1997). Speciesthat may be in need of genetic variation to be able to cope with future climatechange also belong to this category.

Apart from identifying species that may be in need of genetic monitoring,we believe that the programme also would benefit by identifying species whichare in no immediate need of genetic monitoring. A central expression within theinternational conservation community is favourable conservation status. Theexpression applies both to habitat and species, and originally comes from theHabitat Directive (EC Directive 92/43/EEG). Simplified, favourable conserva-tion status is defined to ensure that the species (or habitat) will persist in thelong-term (population trend, natural distribution area and potential environ-ment for the species are stable or increasing). However, for several reasons thisexpression does not guarantee that the genetic diversity of the species also isconserved according to the definition given in Swedish law (Miljöbalken;Förordning 1998:1252, 16§). Even if the population trend of a species is increa-sing (the population sizes and the number of populations are constant or incre-asing), there might be situations where important genetic variation may be lost.For example, the original size of the populations may be so small that geneticvariation will be lost due to the random genetic drift. Also, if the geographicdistribution is so fragmented that gene flow is decreased or absent, genetic vari-ation will be lost through drift. Another example is if genetically distinct popu-lations or populations with high levels of genetic variation disappear or arereplaced by population with lower levels or more trivial genetic variation. Wethink that the genetic monitoring programme would benefit if a conservationconcept that included the conservation of genetic resources was defined.

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8.2 Genetic monitoring – theory and practice8.2.1 General principles of a genetic monitoring programmeWe propose that a genetic monitoring programme is developed in Sweden. Theprogramme should have a central organisation.

One of the most essential tasks for the programme will be to establish pro-cedures for collecting and storing different types of biological material, whichcan be used in genetic investigations of the monitored taxa. For many taxa thegenetic investigation must be performed immediately, whereas for other taxa itmay be possible to wait. It is vital that that the storage methods enable storageover very long time periods without degrading DNA or in other ways limitingwhich types of molecular methods can be used. Because the number of sampleswill quickly increase, the method must allow storage of very small sampleamounts. We suggest that available storage methods, both for DNA and diffe-rent types of tissue samples, are evaluated. It is important that the investigationpresents answers as to how the samples can be stored for long periods of timeas well as what economic resources this storage requires.

There are many Swedish museums with large collections of biological mate-rial, of various ages. In many cases, these collections can be used for genetic stu-dies without damaging the collections to a great extent. The collections are anexcellent reference material that can be used to compare the present and thehistorical genetic variation in a species, which enables researchers to draw con-clusions about the genetic status of populations. From this perspective it isimportant to digitalise the documentation of the collections, and for mostmuseums this work is already in progress. Collections with several individualsper population should be prioritised, but also samples consisting of one indivi-dual per population can be of interest, because combining samples from severalmuseums might create population samples. A joint database over all biologicalcollections in Swedish museums would simplify the procedure and would likelyallow the material to be used to a greater extent.

Research departments also store biological material that could be used asreference material in genetic monitoring projects. However, research collectionscannot be stored indefinitely, because most departments both lack space and/orfunding. We suggest the establishment of a system that enables researchers tooffer biological collections that they have no possibilities to keep to a museum,in order to save material for future monitoring projects.

There are a large number of scientific studies investigating the genetic varia-tion of wild plant and animals in Sweden. Laikre & Ryman (1997) compiled alist of 316 Swedish studies of genetic variation. The list was based on a literatu-re search in a number of databases and a questionnaire that was sent to resear-ch departments in Sweden, and encompassed studies available to databases inNovember 1996. A similar literature search using exactly the same key wordswas performed in three databases (Biological Abstracts, ISI Web of Knowledge,CSA Illumina) from 1996 to October 2006, before the writing the presentreport and resulted in 844 additional studies. Even if many of these studiesmight not be useful from the perspective of genetic monitoring, it would bevaluable to compile a database on which species have been the subject of gene-

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tic studies in Sweden. Also a list of the genetically distinct populations in Swe-den might simplify the work of those involved in both research and in practicalconservation.

8.2.2 Identifying populations showing negative population trendsEarlier we stressed that species and populations demonstrating negative longterm population trends risk losing genetic variation and should therefore bemonitored genetically. An essential question in this context is how we can iden-tify negative population trends. We believe that to answer this question acentral organisation is needed; both to collect information about the populationtrends of species and to recommend the onset of a monitoring programme. Along-term negative population trend will most likely not be the same for allorganisms, depending on longevity, dispersal abilities, distribution patterns andbreeding systems of the different species.

Information about population trends can be gathered in several ways: fromdirected population surveys, from the county boards (gathering informationfrom the municipalities) or from non-profit environmental organisations. Infor-mation from the Species Gateway (Artportalen.se) might also be used as anindication of negative population trends. The Species Gateway is an indepen-dent site for collecting sightings of species and is a part of the Swedish SpeciesInformation Centre. This internet site accumulates information from observa-tions from non-profit environmental organizations and county boards but alsofrom individual persons with different levels of knowledge, and the informationmight have to be scientifically evaluated in some way before being used as indi-cations of population trends.

8.2.3 Genetic monitoring in practiceGenetic monitoring is a process of several steps, and in this section we brieflydescribe a few aspects that might be important to consider when starting amonitoring project.

The first step is to search for earlier studies of the genetic variation of the spe-cies in need of genetic monitoring. Both studies using molecular genetic markersand quantitative genetic analyses of phenotypic characters can be of interest. Ifno studies of the genetic variation of the species in question can be found, eitherin Sweden or in other countries, the search should be widened to also includeclosely related species. All genetic studies (even of closely related species in othercountries) can offer valuable information that may greatly simplify a geneticmonitoring programme. Such studies offer information about, for example, whi-ch levels of genetic variation can be expected for a particular species, how thevariation is distributed among populations in general or which molecular mar-kers have been used and are well-functioning for this species group.

The second step involves collection of material for the genetic monitoringproject. What type of material (e.g. faeces, hair, blood, leaves), the sample size(see Sjögren & Wyöni 1994) and from which geographic areas, depend on whi-ch species and the type of genetic study. For a quantitative traits study, this stepmight involve collection of measurements from individuals in their naturalhabitat or collecting a representative sample of individuals to be used in cultiva-

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tion or crossing experiments to estimate heritabilities etc. Which genetic met-hod to use both depends on the objective of the monitoring project and on thespecies. If no genetic studies have been performed on the species in question, itis wise to perform an initial study investigating the genetic structure across thedistribution area, using a genetic method generating a large amount of informa-tion without large development costs. A multi-locus method such as AFLPcould be an alternative in these cases. However, multi-locus methods sufferfrom some negative traits (e.g. dominance, sensitivity to poor DNA quality), soit might be sensible to switch to other types of markers after the initial survey,especially if the initial study indicates that the species should be monitored for alonger time period. In these cases markers that generate co-dominant data, areinsensitive to poor DNA quality and produce data which do not have to becontinually compared with earlier results to guarantee correct conclusions, areneeded (e.g. microsatellites). It might be necessary to switch method even if themarkers have to be developed from the start.

If genetic studies of the organism exist, it is appropriate to use the samemolecular markers as in these studies in the initial phase, because the results ofboth studies will then be entirely comparable. Of course, it might be necessaryto switch molecular marker system also in these cases.

Using reference materials from old museum samples in the genetic moni-toring will require a genetic method that can be used even if the DNA qualityis poor.

Certain types of genetic monitoring involve specific problems with precisequestions. It may for example be required to investigate the level of inbreeding,the effects of natural selection or hybridization between species, and the mar-kers should of course be chosen accordingly. If the level of inbreeding in apopulation is under question, the molecular marker must be co-dominant (e.g.microsatellites or allozymes) so that deviations from Hardy-Weinberg propor-tions can be calculated. If the genetic monitoring aim is to follow the variationin phenotypic characters involved in natural selection, the markers mustdemonstrate a strong association to these characters (in some plants and coldblooded animals, certain allozyme alleles are associated with certain environ-mental parameters). If the character has high heritability, the phenotypic varia-tion in itself may indicate how the genetic variation may change over time. Infavourable cases, e.g. in species easily cultivated and crossed, it may be possibleto perform a series of quantitative genetic studies to follow changes in the varia-tion directly accessible to natural selection. To be able to discover and followhybridisation between two species it is necessary to use markers that reflect thegenetic variation in as large part of the genome as possible. In the search fordiagnostic molecular markers to discriminate two species, a multi-locus markersuch as AFLP is an excellent alternative.

New molecular methods are frequently developed. We emphasize that it isvery important that a genetic monitoring project does not commit itself to aspecific method, but instead focuses on collecting and storing samples that willalso enable genetic studies with future methods.

We stressed earlier that Swedish museums have large collections of plantsand animals from past times. However, today the museums seldom acquire new

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samples, mainly because the museums often lack the economical resources toreceive and store biological material even if they are offered them. Collectionsof biological material instead are scattered among different departments at vari-ous universities all over Sweden. There is an imminent risk that these collectionsare lost to future genetic studies.

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9. Conclusions

By ratifying the Convention of Biological Diversity, Sweden together withabout 180 other countries, has agreed to conserve biological diversity at theecosystem, species and genetic levels. One common assumption is that theconservation of ecosystems and habitats also conserves species, and that theconservation of species also conserves genetic diversity. However, there is agrowing realization that the conservation of species does not necessarily con-serve the genetic diversity within them.

The genetic diversity within cultivated and domesticated species is oftenstudied to a greater extent and there are several programs that aim to conser-ve this diversity (gene banks, breeding programmes). In these cases, the gene-tic diversity has direct benefits for humans – the genetic diversity can be usedin breeding programs to produce organisms with specific characteristics, sui-table for new situations, new diseases or environments. In the same way,natural populations need genetic diversity to adapt to new situations, forexample the global climate change, but it is virtually unknown how this natu-ral genetic variation is structured among and within populations.

The objective of this report is to identify different threats to the geneticdiversity of Swedish populations, and also to suggest areas where moreresearch is needed in order to develop a national action plan for the conserva-tion of genetic diversity in wild plants and animals.

Numerous studies show that there are genetic differences among popula-tions of Swedish species, as well as among populations in Sweden and othercountries. Populations are different because they have different historical ori-gins, different recolonisation routes or because they are adapted to their localenvironment. Because genetic diversity is found within or among populations,populations or groups of populations are the natural unit to consider whenconserving genetic diversity.

Current research on Swedish populations shows that genetic diversity hasdirect effects on populations and species as well as ecosystems, and also thatgenetic diversity connects processes at the population, species and ecosystemlevels. Genetic diversity within populations has (e.g.) been shown to affect theviability and fertility of individual organisms (the soft-brome, Bromus hor-deaceus; the sheep’s-fescue, Festuca ovina), the demographic development ofpopulations (Gypsophila fastigiata) and the function and species compositionof the local ecosystem or community (eelgrass, Zostera marina; quaking-grass, Briza media). Genetic diversity enabled populations to adapt to localenvironmental conditions in Sweden (e.g. the rough periwinkle, Littorina sax-atilis; the common mussel, Mytilus edulis; herring, Clupea harengus; three-spined stickle-back, Gasterosteus aculeatus; Scots pine, Pinus sylvestri; whiteclover, Trifolium repens).

A species can be viewed as the sum of all genetic variation within it. Gene-tic diversity is needed for the species to evolve and to have the possibility toadapt to future climate change. Regardless if the genetic variation is useful for

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the population at the moment, it is impossible to know which characteristicsare going to be essential in a new environment. All disappearing populationswill result in lost genetic variation, especially if the populations are geneti-cally distinct or locally adapted.

Few endemic species exist in Sweden, and most of them are a result ofrecent local processes such as hybridisation and polyploidisation. At the sametime there are many genetically distinct populations in Sweden, those that aredistinguished taxonomically and ecologically (e.g. subspecies, ecotypes), andthose that can only be distinguished using molecular genetic methods. Geneti-cally distinct populations can be found on the Baltic islands Öland and Got-land, in the Baltic Sea with the surrounding coastal areas, in the mountainareas and in some traditionally managed landscapes. This diversity has arisenas a result of populations being isolated or adapted to unique environments.It may be those populations that have the local adaptations needed for adap-ting to a large-scale environmental change such as global warming.

Human activities may have negative consequences for the genetic diversityof a species, and will as a consequence also affect the adaptive abilities of thespecies. Among the problems affecting natural populations of plant and ani-mals in Sweden, we especially call attention to the following;(i) Every lost population might result in loss of valuable genetic variation

which ultimately results in loss of the adaptive abilities of a species. Thisthreat can gradually increase due to future climate change, e.g. globalwarming might decrease the distribution of alpine species to the extentthat many genetically distinct populations are lost in this area.

(ii) Many Swedish species that previously had large and cohesive distribu-tions presently form small isolated populations where processes such asrandom genetic drift and inbreeding can have large effects. This threatnot only affects rare species (e.g. wolf), but can ultimately affect speciesthat presently are relatively common in the agricultural and silviculturallandscape. On the other hand, several studies suggest that only a smallnumber of immigrants or introduced individuals may be sufficient toreduce the negative effects of inbreeding.

(iii) A potential risk to the genetic diversity of Swedish populations is thegene flow that occurs when provenances of trees from southern parts ofEurope are planted to increase the timber production, when birds andfish bred in captivity are released for hunting and fishing purposes, orwhen foreign provenances of grass seeds are sown on road verges.Because these activities are not always registered, it is difficult to estima-te the extent of the gene flow and the possible negative effects for thegene pools of the native species. The negative effects of gene flow mustalso be considered in conservation projects that aim to supplementpopulations with captive bred individuals or individuals from distantpopulations.

Based on the present report and the threats to genetic diversity we identifyhere, we would like to see more research regarding the following generalquestions:

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Genetic variation and environmental change. Global warming will invol-ve fundamental change for Swedish populations and ecosystems, and geneticprocesses such as gene flow and adaptation will play major roles in meetingthese changes. We lack knowledge to address the following questions:

What role may genetically distinct populations in Sweden play to enablespecies to meet large-scale climatic and environmental changes? Is there suffi-cient genetic variation in relevant ecological traits to enable species to adaptto rapidly changing environments? Which populations are most valuable inthis respect – central populations or those at the periphery of the distribu-tion? Is there a risk that genetically distinct populations will disappear in thehabitats that supposedly will be most affected by global warming? Whichgenetic methods are most relevant for assessing evolutionary potential? Howwill genetic variation of key species in important Swedish ecosystems affectthe function, species composition and stability of these ecosystems?

Genetic diversity after gene flow and hybridisation. Several Swedishpopulations are subject to an extensive gene flow from distant populations asa consequence of human actions. It is important to understand how thehuman-mediated gene flow affects the gene pool of the genetically distinctpopulations present in Sweden. What are the genetic effects of the release ofalien populations that take place in e.g. the forestry and fisheries? How willgrass-species of natural grasslands be affected by the gene flow from foreignprovenances sown on road verges? When is it appropriate to supplementsmall or inbred populations, or populations that are poorly adapted to achanging environment? When will such measures be harmful? From whichpopulations should the individuals used in the supplementation be taken?

In the present report we also suggest that a genetic monitoring program-me should be developed. We propose that the programme focuses on speciesor populations having negative population trends and/or populations that areat risk of being affected by habitat fragmentation, a large inflow of aliengenes or intense harvesting.

One of the most essential issues for the monitoring programme is toestablish procedures for repeated collection and storing of different types ofbiological material, e.g. tissue samples, which can be used in genetic investi-gations to examine long-term genetic trends. It is very important that thestoring of the biological material does not in any way limit which methodscan be used in future investigations. The types of molecular methods thatshould be used in the genetic monitoring must be chosen according to the spe-cies and the question that needs to be answered.

Plant and animal materials kept in museums are excellent sources of refe-rence material for genetic monitoring programmes, and we suggest that acentral organisation responsible for the collection and storage of samples isdeveloped, to guarantee a continuation of genetic monitoring programmes.This organisation could also be responsible for developing a formalisedsystem for taking care of terminated research collections.

There are several scientific questions that are in need of answers whendeveloping a genetic monitoring programme. One of the most central ques-tions is: How can we differentiate natural changes in genetic diversity from

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the un-natural, which might constitute a threat to the genetic diversity?What should the national action plan include? The national action plan

for conserving genetic diversity in wild plants and animals in Sweden shouldfirst and foremost include a genetic monitoring programme and also prioriti-se the suggested research areas. Furthermore we suggest that the action planproposes guidelines for how to deal with genetic problems in monitoredpopulations and in the supplementation of wild populations, an action alrea-dy suggested in several of the recovery and action plans for red-listed speciesin Sweden. The national action plan should also aim to develop guidelinesand effective systems for the registration of the release of alien populationsthat takes place e.g. in forestry, fish management and in road management.

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10. Acknowledgements

We are indebted to Professor Trevor Beebee for reviewing the translation ofthis report to English. We are also very grateful to all who read and commen-ted on earlier drafts, and to those who in other ways contributed to thisreport:Björn WidénCarl AndréGabrielle RosquistHåkan MarklundJacob HöglundJan-Åke LundénJenny LonnstadJohan DannewitzJohanna ArrendalLars BergLennart AckzellLinda LaikreMaria Hall-DiemerMats GrahnMelanie JosefssonMette SvejgaardMikael SvenssonNils RymanPekka PamiloPer Sjögren-GulvePeter LindbergSofia GyljeSusanna PakkasmaaTorbjörn Ebenhardand other members of the government commission’s Reference group and Steering group.

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Genetic differentiation between individuals – the genetic variation –

is the basis of all evolution and adaptation to changes in the envi-

ronment and climate. Sweden has agreed to conserve the biological

diversity, which includes genetic diversity, but until now, the conser-

vation of genetic resources has attracted relatively little attention of

its own in practical nature conservation.

In 2006, the Swedish Environmental Protection Agency was com-

missioned to develop and suggest a national action programme for

the conservation of genetic diversity in wild plants and animals.

This report constitutes part of this work and is an internationally

adapted version of the original report in Swedish. The report is

intended for persons working in government agencies, municipaliti-

es, and non-governmental organizations with natural-resources

management, nature conservation and sustainable development.

In this overview the genetic variation in Swedish populations of

wild plants and animals is characterized on the basis of selected

themes. These themes were chosen to illustrate general issues in the

international research field of conservation genetics, and are

exemplified using relevant genetic studies primarily of Swedish

organisms. Can important genetic variation be found among

Swedish populations? What are the genetic consequences of

decreasing population sizes in Sweden? Starting with the identified

threats to genetic diversity, areas with lack of essential information

are also identified.

Swedish Environmental Protection Agency SE-106 48 Stockholm. Tel: +46 8-698 10 00, fax: +46 8-20 29 25, e-mail: [email protected] Internet: www.naturvardsverket.se Orders Telephone orders: +46 8-505 933 40, fax orders: +46 8-505 933 99, e-mail: [email protected] Postal address: CM-Gruppen, Box 110 93, 161 11 Bromma. Internet: www.naturvardsverket.se/bokhandeln

Genetic variation in wild plants and animals in SwedenA review of case studies from the perspective of conservation genetics

SWEDISH ENVIRONMENTAL

PROTECTION AGENCY

ISBN: 978-91-620-5786-2

ISSN: 0282-7298

REPORT 5786

genetic variation in wild plants and animals in sweden · genetic variation in wild plants and ......

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