seed dispersal and crop domestication - ucl

Annual Plant Reviews (2009) 38, 238–295 www.interscience.wiley.comdoi: 10.1002/9781444314557.ch7

Chapter 7

SEED DISPERSAL AND CROPDOMESTICATION:SHATTERING, GERMINATIONAND SEASONALITY INEVOLUTION UNDERCULTIVATIONDorian Q. Fuller1 and Robin Allaby2

1 Institute of Archaeology, University College London, London, UK2 Warwick, HRI, University of Warwick, Wellesbourne, Warwick, UK

‘The Angiosperm seed had a double significance. It not only gave command of dryland to plant life, but it provided the means by which mankind has been able toobtain an ample and assured food supply. To the Angiosperm seed, perhaps morethan to any other structure, the economic evolution of the human race is due.’

Oakes Ames (1939, p. 5)

Abstract: The transition between wild plant forms and domesticated species canbe considered an evolutionary adaptation by plants in response to a human drivenecology. Evidence from archaeobotany and genetics is providing deeper insightinto this evolutionary process in terms of its scale, mechanism and parallelismbetween species. The evidence indicates that the timescale of this evolution wasconsiderably longer than previously supposed, raising questions about the modeof human mediated selection pressure and increasing the importance of the role ofpre-domestication cultivation. Different selection pressures were chronologicallyseparated into at least three stages, each important at different points of the evolu-tionary process affecting different traits. Early selection pressures were ultimatelydriven by the pre-domestication sowing activities affecting the polygenically con-trolled germination and seed size traits. Later, in the second stage, release of natu-ral selection pressures of dispersal requirements led to modification of architecturesuch as awns loss of awns and increase in dispersal unit size. The loss of disper-sal requirement combined with positive pressure through harvesting practice led

238 Fruit Development and Seed Dispersal Edited by Lars Østergaard© 2010 Blackwell Publishing Ltd. ISBN: 978-1-405-18946-0

Seed Dispersal and Crop Domestication � 239

to the typically monogenically controlled non-shattering phenotypes. At the ter-tiary stage new selection pressures were imposed with changing climate caused bymovement of the crops into different latitudes, resulting in typically monogenicallycontrolled aseasonal phenotypes. The genetic evidence shows in most cases thatgenetically similar mechanisms have been affected in different plant species im-plying an evolutionary convergence in response to adaptation to human ecology.These adaptations can be considered various types of heterochrony; a mechanismof major importance generally in plant evolution.

Keywords: archaeology; genetics; cereals; legumes; convergent evolution;dehiscence; dormancy

7.1 Introduction

In the long-term view of human history, the beginnings of agriculture wasone of the great turning points, and a central part of this turning point wasthe evolution of new plant forms, domesticated crops. Anthropologists andbotanists alike have argued about how precisely to demarcate ‘domestica-tion’ from non-domesticated wild species (e.g. Higgs and Jarman, 1969, 1972;Harris, 1996, 2008; Zeder, 2006). But, in general, all agree that domesticationimplies an increased interdependence between human cultivators and theplants they cultivate, and that this can be considered a case of symbioticcoevolution (Higgs and Jarman, 1969; Reed, 1977; Rindos, 1980). It is cer-tainly true that different kinds of crops have experienced different selectivepressures and show different adaptations for domestication; thus fruit treesand vines differ fundamentally from tuber crops or seed crops. In the presentcontribution, we will focus on seed crops and review the role of changesin seed dispersal, broadly interpreted, and how these have been essentialaspects of the domestication process. By seed crops, we mean those specieswhich are cultivated primarily for their harvested seeds or fruits and whichare plants grown from seed. As such, this category not only includes all ce-reals, pulses (grain legumes) and oilseeds, but also some fibre crops. We willassess examples of changes in dispersal traits and how their evolution canbe studied through archaeological plant remains (archaeobotany) as well asthrough genetics. While we will not attempt to provide a comprehensive listof seed crops and domestication traits, we will draw from a selection of exam-ples from across different regions of origin, taxonomic families and degreesof current knowledge.

Domestication, as we use it here, is a quality of plants in which mor-phological (and genetic) changes are found amongst cultivated popula-tions by comparison to free-growing wild populations. These changes rep-resent adaptations to systems of cultivation and human harvesting, and assuch evolved by frequency changes of key alleles in the genomes of culti-vated populations. These changes would have first appeared during a pe-riod of pre-domestication cultivation when human behaviours modified the

240 � Fruit Development and Seed Dispersal

environments and reproductive cycles of plants, especially by human inter-vention in the dispersal of seeds (Harris, 1989; Hillman and Davies, 1990,1999; Fuller, 2007a). One of the key changes often regarded as the charac-teristic of domesticated grain crops was a shift from natural seed dispersalthrough shattering mechanisms (pod dehiscence, or spikelet shedding ofgrass ears/panicles) to obligate dispersal by people (Zohary, 1969; Harlanet al., 1973; Hillman and Davies, 1990, 1999). Populations can be regarded asfully domesticated when they are dominated by such non-dispersing geno-types, and the term ‘semi-domesticated’ has been proposed for populationswhich show other changes associated with domestication prior to fixation ofthe non-shattering traits (Fuller, 2007a). Some of these other changes includeloss of wild-type germination inhibition and changes in seed size, which arealso linked to successful early growth of seeds planted in cultivated fields(Harlan et al., 1973; Harlan, 1992: Ch. 6; Smith, 2006a; Fuller, 2007a). All ofthese changes were essential to the success of domesticated plants, and ar-chaeobotanical studies are providing increased evidence for the process andtiming of their evolution. Another important set of changes in many crops,which is broadly related to dispersal, is seasonality control, through processesof photoperiodicity and vernalization. Changes in the control of seasonalityof growth and flowering played an important role in the dispersal of somedomesticated plants by farmers into new geographical zones, which differedin climate or environment. The genetic dissection of these traits is providingnew insights into the history of this process. In the sections that follow, wewill review these traits and their study, drawing selected examples from thosespecies that have been best documented.

7.2 Loss of natural seed dispersal in wheat and barley:archaeobotanical evidence

‘. . . wild wheats and barley have fragile spikes, and their ears disarticulate im-mediately upon maturity. The fragility of the spike is, in fact, the main diagnosticcharacter that serves for distinction of wild cereals from their cultivated counter-parts. But what is less emphasized is that brittleness is only the most conspicuousreflection of one of the major adaptations of these wild cereals to their wild envi-ronment: their specialization in seed dispersal.’

Daniel Zohary (1969, pp. 57–58)

This is often regarded as the single most important domestication trait(‘domestication’ sensu stricto) because it makes a species dependent uponthe human farmer for seed dispersal. In cereals, this occurs by the loss ofabscission at the abscission scars, such as the rachis attachment points inwheat or barley ears or the rachilla to spikelet base attachment in panicledcereals (rice and millets). The result is that instead of shedding seeds whenthey are mature, a plant retains them, and they are then usually separated


(a)

(b)

Figure 7.1 Comparisons between wild and domesticated plants in terms of seeddispersal. (a) Comparison between a wild shattering wheat ear (left) and domestic wheatear with a tough rachis, which requires pounding to break apart (right). The form ofrachis segments that can be recovered archaeologically is shown in the middle. (b)Generalized wild bean with pod that twists and opens, dispersing seeds (left) comparedwith a domestic pod that remains closed (middle) and must be split open by humanforce (right).

by the addition of human labour (threshing and winnowing) (Fig. 7.1). Forfarmers, this increased the efficiency of harvest and thus yields. Higher yieldscan be produced because the farmer could wait until all, or most, of thegrains on a plant have matured, whereas earlier harvesting would have hadto balance loss of grain through shedding, as they matured, with reducedyields through grains harvested immature (i.e. before spikelets have filledentirely). This would have been a particular problem with cereals such as


wild rice which has a long period of grain maturation, and which may havegrown in wetland environments in which shed grains were lost (Fuller et al.,2007a; Fuller and Qin, 2008).

The evolution of non-shattering would have occurred as a result of partic-ular methods of harvesting that favoured non-shattering (tough rachis) mu-tants in harvested populations which were then sown (Hillman and Davies,1990, 1999). Archaeologists have long attributed this to the use of sickles forharvesting (e.g. Wilke et al., 1972; Hillman and Davies, 1990, 1999; Bar-Yosef,1998; Willcox, 1999), although recently Fuller (2007a) has questioned thison the grounds that non-shattering cereals appear to have evolved slowerthan what sickle harvesting models have predicted; in some regions such asthe Near East, sickles precede domestication by many thousands of years,while in other regions such as the Yangtze valley of China, sickles or stoneharvesting knives were introduced to artefact toolkits after rice was alreadydomesticated. This is currently an area of debate and discussion amongstarchaeobotanists (see Balter, 2007). What is clear is that other methods ofharvesting might not have selected for this domestication trait. Ethnograph-ically gatherers of wild seeds have often used paddle and basket harvestingmethods (Harris, 1984; Harlan, 1989, 1992) and some harvest by uprooting im-mature grasses (Allen, 1974). It has been suggested that early hunter–gatherergroups in the Near East could have gathered wild wheat and barley spikeletsfrom the ground after shedding, which is also one method that would notbe expected to select for domestication traits (Kislev et al., 2004). The meth-ods of harvesting, together with their timing in relation to spikelet maturity,created some level of selection for non-shattering domestic-type mutants.While archaeologists may continue to debate what those human behaviourswere, archaeobotanical studies are beginning to provide hard evidence, atleast for a few species, for the proportions of wild (shattering) and domes-ticated (non-shattering) morphotypes in populations at particular times andplaces and thus we are able to document that rate at which domesticationevolved.

Wheat and barley have the best documented record of domestication whichtook place in the Near East (Fig. 7.2). In these cereals, the distinction betweenshattering and non-shattering forms is clearly manifest in the attachmentscars on the rachis segments, which are part of the spikelet base in wheats.Therefore, a clear distinction between wild and domesticated plants, anddocumenting the transition between them, should involve a study of rachisremains. While this was already clear to Helbaek (1959), data were limited,mainly to a few impressions in mud-brick. Early flotation in the Near Eastdid recover rachis remains but large assemblages in which wild and domesti-cated morphtypes were distinguished did not begin to be published until themid-1980s, with Van Zeist’s study of the barley rachis from Tell Aswad (VanZeist and Bakker-Heeres, 1985). It is only in the past few years that studieshave directly examined the time gap between the beginnings of cultivation,and the initial appearance of non-shattering cereal ears, and the end of the


Figure 7.2 Map of Southwest Asia, showing the locations of sites witharchaeobotanical evidence that contribute to understanding the origins and spread ofagriculture (after Fuller, 2007a). Sites are differentiated on the basis of whether theyprovide evidence for pre-domestication cultivation, enlarged grains, mixed orpredominantly domestic-type rachis data. Note that these sites represent a range ofperiods, and many sites have multiple phases of use, in which case the earliest phase withsignificant archaeobotanical data is represented. Shaded areas indicate the generaldistribution of wild progenitors (based on Zohary and Hopf, 2000 with some refinementsfrom Willcox, 2005). It should be noted that wild emmer (Triticum diococcoides) occursover a subset of the wild barley zone, and mainly in the western part of the crescent.

domestication process marked by the predominance or fixation of domestic-type non-shattering cereals (Tanno and Willcox, 2006; Fuller, 2007a). Althoughtheoretically it could have happened very quickly, as demonstrated underideal experimental conditions (Hillman and Davies, 1990, 1999; see also Zo-hary, 2004), this no longer appears to be the case.

As already indicated, there is now growing recognition of a long period ofpre-domestication cultivation. In a compilation of data from five representa-tive sites, three with einkorn wheat and two with barley, Tanno and Willcox(2006) suggested that cereal domestication might take millennia, perhaps aslong as 3000 years, while Weiss et al. (2006) accepted at least a 1000-year pe-riod. A comprehensive compilation of nearly 5000 barley rachises (Hordeumspontaneum/vulgare) and 1800 einkorn wheat (Triticum boeitucm/monococcum)spikelet bases (Fuller, 2007a) similarly indicated slow domestication with anestimated 1500–2000 years for the transition to predominantly non-shatteringmorphotypes, starting from ca. 9500 BC (Fig. 7.3). But if weed flora evidencefor pre-domestication cultivation is accepted for Abu Hureyra and Murey-bit (Colledge, 1998; Hillman et al., 2001; Willcox et al., 2008) and assumedto be continuous with later cultivation and domestication, then it should be


Figure 7.3 Domesticate rates in barley and einkorn wheat modelled fromarchaeobotanical data (after Fuller, 2007a). Proportion of domesticated type for each siteis plotted by a box against a median estimate of site age. A margin of error is indicated bythe line which connects the sum of domesticated and uncertain types (indicated by across or x). Trend lines are shown based on the lower estimate. (a) Barley domesticationrate model, on which period averages are also plotted for the PPNA, Early PPNB and LatePPNB, in which the diamond indicates the proportion of domesticated types and thecircle the sum of domesticated and uncertain types. (b) Einkorn domestication ratemodel; trend line does not consider the much later Kosak Shamali.

assumed that cultivation began a further 1000–1500 years earlier, bringing theestimate to 3000–3500 years. The recognition of pre-domestication cultivationtogether with a slow domestication process reopens the question as to justhow early some cultivation might have begun. It also dissociates the begin-nings of cultivation from subsequent domestication leaving an open question


as to how many centres of origin there were for cultivation and whether allof these were equally involved in selection for domesticated plants. Mostarchaeologists now assume that there were multiple independent centres ofearly cultivation and eventual domestication in the Near East (Nesbitt, 2004;Willcox, 2005; Weiss et al., 2006; Fuller, 2007a; Zeder, 2008) but further researchis still needed to delineate these.

The overall regional pattern is the replacement of entirely/predominantlymorphologically wild barley with predominantly domesticated barley by theend of the Pre-Pottery Neolithic periods. How we explain this long domestica-tion period, however, remains uncertain. Willcox et al. (2008) have suggestedthat continued collecting from wild stands to replenish stores would slowdown the rate at which domesticated types were selected, and harvestingof ears somewhat immature would also act against strong selection for do-mesticated types (as already noted by Hillman and Davies, 1990, 1999; seealso Fuller, 2007a; and parallel issues with Asian rice, Fuller et al., 2007a).Certainly, even in the late Pre-Pottery Neolithic B (PPNB) period of the NearEast, there is intersite variability in the proportion of wild barley rachis, whichmay relate to different degrees of continued reliance on gathering from wildstands. As suggested by Ladizinsky (2008), local bottlenecks may have beencaused by drought or disease and forced cultivation of additional stock fromwild populations. Another alternative is to reconsider the presumption thathunter–gatherers would have sickle-harvested wild cereals, which has longbeen the basis for our models of the evolution of non-shattering domesticates,but which should have led to rapid domestication (Hillman and Davies, 1990,1999). It can be suggested that the sickle was transferred to harvesting cropsafter non-shattering ears were a significant component of crops (Fuller, 2007a).Sickle harvesting of crops was an exaptation as sickles were developed ear-lier as a technology for cutting basketry or building materials (Sauer, 1958;Sherratt, 1997; Kislev et al., 2004; and note the cut wild straw as beddingmaterial at 23 000 bp Ohalo II: Nadel et al., 2004). Hillman and Davies (1999)had discussed how harvesting by cultivators would be expected to maximizeyield per unit area (cultivated plots) rather than unit of time, as expected forhunter–gatherers (also Bar-Yosef, 1998). Fuller (2007a) proposes that multipleharvests over time of a single crop, which would increase total yields froma crop that matured unevenly, would lead to the latest harvests favouringdomesticates, even if sickles were not used. Variation between households interms of whether first or last harvests were stored for sowing could createvery weak selection at the community level for domestic morphotypes fromthose late harvests.

Another emerging issue is whether full cereal domestication (fixation oftough-eared mutants) took place first outside the area of the wild progenitorsand earliest cultivation. While the predominance of domesticated type barleyon most Near Eastern sites may have waited until ca. 7500–7000 BC, by thisperiod crops had dispersed towards Europe, reaching mainland Greece andCrete by ca. 7000 BC (see Colledge et al., 2004, 2005), where fully domesticated


forms dominate. Even earlier by 8000 BC, cereals had been transferred toCyprus, where domesticated chaff remains also dominate (although assem-blages are very small) (Colledge, 2004). This may suggest that local bottleneckeffects when crops were carried away from their centres of origin sped up do-mestication within the translocated population. The recent genetic diversitystudy of einkorn wheat indicates that early domestics retained high levels ofgenetic diversity (Kilian et al., 2007), and this is to be expected where prox-imity allowed continued introgression between cultivated and free-growingpopulations, especially since the domestication that differentiated them wasslow to evolve. By contrast, major genetic diversity bottlenecks can be ex-pected with dispersal events beyond the wild range when farming spread tonew regions, such as Cyprus or Europe.

It must also be kept in mind that in centres of origin, because there re-mained wild populations, natural selection for wild-type adaptations con-tinued alongside artificial selection amongst cultivars. The invasion of cropfields of weedy, wild-types, as well as the abandonment of old fields, wouldhave provided contexts that favoured persistence of the wild, shattering mor-photype. This could have been further reinforced by cross-pollination withwild populations. All of this would have bolstered the wild-adapted ge-netic diversity amongst early crops, which may have provided degrees ofresistance to the ‘artificial’ selection of cultivated populations (Allaby, 2008;Allaby et al., 2008). Those crops which were dispersed in small foundingpopulations to Cyprus, Crete and Greece would have been removed fromconflicting selection for wild-type adaptations.

7.3 Non-shattering in other cereals: rice, pearlmillet and maize

No other cereals are as well documented archaeologically as einkorn wheatand barley, although there are growing data sets for rice (Oryza sativa), pearlmillet (Pennisetum glaucum) and maize (Zea mays). For most crops early ar-chaeobotanical evidence documents use. Meanwhile, domestication is in-ferred by other traits, such as grain size (see below) or else from associatedarchaeological context or changes in distribution that suggest dispersal out-side of the wild habitat. For example in Sorghum bicolor, early Holocene findsin the Western Desert of Egypt at Nabta Playa indicate that wild-type shatter-ing spikelets were harvested together with other wild grasses by ca. 7500 BC(Wasylikowa et al., 1995, 1997, 2001), as also in central Sudan by ca. 4000 BC(Magid, 1989, 2003; Stemler, 1990). A single possible non-shattering specimenis reported from the Sudan (Stemler, 1990). Subsequent evidence for sorghumcomes from grains that appear domesticated in size and shape that had beentranslocated from Africa to India around 2000 BC (Fuller, 2003). But thereremains no data from which to infer when selection for the domesticated


forms began or ended. Some have hypothesized that domesticated formsfirst appeared outside Africa in South Asia aided by the separation from wildpopulations (Haaland, 1999), although the archaeobotanical record in easternAfrica remains so depauperate during the period between 4000 BC and 1000BC that this hypothesis cannot yet be tested.

Rice shattering is controlled by abscission layers where the spikelet at-taches to the rachilla (Li et al., 2006) and this can be studied archaeologicallyfrom the spikelet base which preserves the scar (Thompson, 1996, 1997; Zhenget al., 2007; Fuller and Qin, 2008). These spikelet bases are very small and untilrecent changes in how archaeological sites were sampled for plant remains,they were not recovered from early sites in either China or India where ricedomestication events have been postulated. It is now clear that these can pre-serve in quantity, and current research programmes in the Yangtze valley arequantifying the proportions of wild, domesticated and potentially immatureharvested spikelet base types (Fig. 7.4). Work by the author and others will

Figure 7.4 Archaeological remains of rice spikelet bases that allow the distinctionbetween wild and domesticated types. At left are the drawings of three spikelet basetypes from the archaeological sites of Caoxieshan, Jiangsu, China ca. 4000 bc (after Fullerand Qin, 2008), showing domesticated, non-shattering scar (top), smooth scar ofshattering wild mature type (middle), and protruding scar of probable immature type(bottom). At right are the scanning electron micrographs of archaeological spikelet basesfrom Neolithic Tian Luo Shan, ca. 4700 bc, Zhejiang Province China (see Fuller et al.,2009): at top right is domesticated type and at lower right is wild-type. Reproduced withpermission from Antiquity Publications Ltd.


Figure 7.5 Diagram of differences between a domesticated (top) and wild (bottom)spike of pearl millet (Pennisetum glaucum). In domesticated type, non-shatteringinvolucres are born on a stalk, and often include more than one grain, whereas in wildpearl millet sessile spikelets, normally one-grained, are shed by dehiscence (based onPoncet et al., 2000; Fuller et al., 2007b). Images provided by University of Groningen,Groningen Institute of Archaeology.

soon provide some quantitative results from which to estimate how quicklynon-shattering rice evolved and when domestication was completed, but cur-rent estimates suggest this process began sometime before 6000 BC and wascompleted by ca. 4000 BC (cf. Zheng et al., 2007; Fuller et al., 2007a; Fuller andQin, 2008; Fuller et al., 2009).

Pennisetum glaucum, pearl millet, is the only African cereal for which exist-ing archaeobotanical evidence provides some indicators of the domesticationprocess, but this is still limited and hampered by an absence of data sets ofancient wild-type pearl millet prior to the start of domestication. The involu-cres, which contain spikelets and bristles, change from being sessile and shedwhen mature to being non-shedding and stalked in the domesticated form(Fig. 7.5; also, Brunken et al., 1977; Poncet et al., 2000; D’Andrea et al., 2001;Zach and Klee, 2003; Fuller et al., 2007b). Evidence for the early occurrenceof domesticated, stalked involucres comes from impressions in ceramics ofpearl millet chaff that had been mixed with clay during pottery production(Amblard and Pernes, 1989; MacDonald et al., 2003; Klee et al., 2004; Fulleret al., 2007b). These impressions can preserve the threshed involucre stalks(Fig. 7.6), of which the earliest are now from 2500 BC to 2200 BC atKarkarichinkat (unpublished data of Fuller and K. Manning; cf. Finucane


Figure 7.6 Examples of archaeological pearl millet remains of domesticated type. Atleft is a cast (in polyvinylsiloxane) of an impression of pearl millet chaff used to temperpottery from Neolithic Djiganyai Mauretania (1500–1700 bc) (after MacDonald et al.,2003; Fuller et al., 2007b); at right is an image of charred macro-remains of pearl milletinvolcure from Cubalel, Senegal (ca. ad 500) (after Murray et al., 2007). Images providedby University of Groningen, Groningen Institute of Archaeology.

et al., 2008). Chaff can also sometimes be preserved carbonized although westill lack very early assemblages (Fig. 7.6; cf. Murray et al., 2007).

The most important cereal domesticate in the New World was maize whichalso differs from its wild progenitor in terms of being non-shattering. Whilethe small alternating involucres of wild teosinte ears (Zea mexicana) shatterat maturity, the cobs of maize do not and grains must be forcibly removedfrom their cupules (Iltis, 2000). The presence of this trait is apparent fromthe earliest preserved maize cobs from dry caves in southern Mexico thatdate back about 6200–6300 years (Benz, 2001; Long and Fritz, 2001; Pipernoand Flannery, 2001; Smith, 2001). However, the beginnings of cultivation isinferred to be much earlier based on evidence from phytoliths and starchgrains, including evidence that maize had dispersed already towards SouthAmerica before this time, ca. 7000 BC (Dickau et al., 2007). The beginningsof cultivation remain obscure and there is no significant early archaeologicalrecord for wild teosinte use, or how quickly this was transformed into thesmall non-shattering cobs of maize.

7.4 The genetics of non-shattering cereals

Breeding experiments have long shown that the genetic control of seed shat-tering is simple in that the trait is usually governed by a single locus asevidenced by simple Mendelian inheritance ratios of brittle and tough rachisphenotypes. The tough rachis alleles have been found to be loss of function


genes that are recessive. The synteny of the grass genomes and initial quan-titative trait loci analyses led to the initial supposition that the same genesmight be responsible in the different grass lineages in a neat example ofevolutionary convergence (Paterson et al., 1995). While this was a reasonablehypothesis given the evidence at the time, the picture has subsequently de-veloped into something more complex. It now appears to be the case thatdifferent grass lineages have had different genes modified to produce theloss of seed shattering (Li and Gill, 2006). The number of genes responsiblethat have been characterized by DNA sequence still remains low, with riceleading the way.

Two different genes have been identified in rice, qSH1 (Konishi et al., 2006)and sh4 (Li et al., 2006), which carry mutations leading to the non-shatteringphenotype. The qSH1 gene codes for a homeodomain protein highly similarto REPLUMLESS (RPL) in Arabidopsis that is responsible for down-regulatingtwo other homeodomain proteins (SHP1 and SHP2) involved in developinga dehiscent zone in silique maturation (Roeder et al., 2003). It seems likelythat the qSH1 is also involved in an interaction between MADS-box home-odomain genes in dehiscence regulation, although it should be noted that thedehiscence zones between the two plants are not homologous and the SHPsof Arabidopsis have no known orthologues in rice. In this case, the changeof function at the qSH1 gene is associated with just one single nucleotidepolymorphism (SNP), although the mechanism of action is as yet unclear.The second gene identified in rice to produce a non-shattering phenotypesh4 is different to qSH1 and has only low levels of similarity to genes foundin Arabidopsis, or elsewhere in the rice genome. It has a Myb3 DNA bind-ing domain, which suggests it is a transcription factor. Again a single SNP,leading to a single conserved amino acid change, results in the change infunction, which appears to result in either the incomplete formation of theabscission zone (Li et al., 2006), or the failure to initiate cell degradation (Linet al., 2007). In this case, these two studies have found allelic variations ofthe sh4 gene, suggesting an allele of some antiquity and perhaps with in-teresting phylogeography. In the case of rice then, two independent geneticpathways to non-shattering have occurred. Haplotype analysis including oneof these, qSH1, suggests that the non-shattering phenotype came after othermutations associated with an increase in grain size and the waxy phenotype(Shomura et al., 2008), supporting the idea that the mutation arose in the ‘do-mesticated’ population of rice. Interestingly, although the sh4 non-shatteringgenotype was found in the wild progenitor Oryza nivara, this was thoughtto be due to an introgression from domesticated rice, as the alleles that weremost closely related to the non-shattering type in the wild were found inO. rufipogon rather than O. nivara. Since O. rufipogon is generally regarded asthe ancestor of domesticated japonica rices in East Asia, while O. nivara hascloser affinities in general with indica cultivars (Cheng et al., 2003; Fuller, 2006;cf. Sweeney and McCouch, 2007; Vaughan et al., 2008), this evidence impliesthat sh4 evolved during japonica rice domestication, and entered indica rice


through a more complex process involving hybridization between lineages(Sang and Ge, 2007). Two alternative hypotheses exist: either there were highlevels of introgression from wild South Asian rices as domesticates spreadfrom a single origin in the Yangtze valley, the ‘snowball model’ (Sang andGe, 2007; Vaughan et al., 2008), or else there were separate origins of culti-vation and subsequent hybridization of cultivars, the ‘combination model’(Sang and Ge, 2007; preferred by Kovach et al., 2007; and consistent with thearchaeobotany of South Asia, cf. Fuller, 2006). Similarly the mutation for awhite pericarp evolved once in early japonica and was introgressed into SouthAsian rices (Kovach et al., 2007; Sweeney and McCouch, 2007; Sweeney et al.,2007; Vaughan et al., 2008).

In barley, two closely linked loci btr1 and btr2 have long been implicated intough rachis formation on two independent occasions in the evolution of do-mesticated varieties (Takahashi, 1955). While these two genes have yet to havetheir sequences characterized, sequence analysis of closely linked biomark-ers found through amplified fragment length polymorphism (AFLP) havesupported this suggestion strongly by clearly showing two clades of brittlerachis origin for the two respective loci (Azhaguvel and Komatsuda, 2007).Based on mapping positions, it seems unlikely that the two Btr loci in barleyare orthologous to the Br1 locus responsible for tough rachis in lower wheats(Li and Gill, 2006). Two loci have been identified in wheat to confer toughrachis formation in different types of disarticulation, W (wedge type) and B(barrel type), respectively. The W-type disarticulation occurs in the A, B, S, Gand T genomes and is governed by Br1 located on the short arm of chromo-some 3. Einkorn, emmer and Iranian spelt wheats have this disarticulationtype, for instance. The B-type shattering originates from A. tauschii and isfound on the long arm of chromosome 3D, and gives rise to the shatteringfound in European spelt. Comparison with QTLs derived from maize alsosuggests that these loci are not orthologous between maize, rice and wheat(Li and Gill, 2006). It should be noted that a number of other loci have beenidentified to be involved with rachis fragility (Janatasuriyarat et al., 2004),through the pleiotropic action of glume tenacity (Tg) on chromosome 2D,and the free threshing gene Q on chromosome 5A. Interestingly, the Q genehas been characterized by sequence, and found to be similar to APETALA 2(AP2) of Arabidopsis, an important transcription factor in floral development(Simons et al., 2006). What makes the Q gene especially interesting is thatthe free threshing allele, q, is a gain of function mutation. A single aminoacid change from Q to q has resulted in the ability of the protein to formhomodimers, which has had consequences on its transcription regulationactivity.

There is little information on the remaining principal panicoid grassesmaize, sorghum and Pennisetum. A discrete shattering locus was identifiedthrough QTL in sorghum (Paterson et al., 1995), which was syntenic to a highscoring region for the trait in maize, which also had further seven regionsassociated with shattering. Pennisetum is thought to have oligenic control of


shattering in a tightly linked cluster (Poncet et al., 1998, 2000), but furthercharacterization has not yet been published.

Finally, another crop in which tough rachis loci have been identified isbuckwheat (Matsui et al., 2003, 2004). In this case, two independent loci havebeen identified (Sht1 and Sht2), which are not closely linked but both canconfer the non-brittle phenotype independently. The sht1 allele that confersthe first non-brittle phenotype is fixed within the cultivated population, butthe sht2 is not. On this basis, the authors argue that the sht2 mutant may haveoccurred after the crop was domesticated and has not been subject to strongselection. Further phylogeographic evidence will help to elucidate this story.

7.5 Reduction in seed dispersal aids

Accompanying the loss of natural seed dispersal was the reduction of ap-pendages that aid dispersal. De Candolle (1885, p. 460) summarized this aschanges in the ‘form, size, or pubescence of the floral organs which persistround the fruits or seeds.’ Plants, and especially grasses, have a range ofstructures that aid seed dispersal, including hairs, barbs, awns and even thegeneral shape of the spikelet in grasses. Thus, domesticated wheat spikeletsare less hairy, have shorter or no awns and are plump, whereas in the wild,they are heavily haired, barbed and aerodynamic in shape. All of these tendto be greatly reduced in the domesticated form. While this is connected tothe loss of shattering, we expect it to have evolved by a different process(Fuller, 2007a). Instead of being positively selected for by human activities,as the tough rachis was, this probably came about by the removal of natu-ral selection for effective dispersal. The recent study by Elbaum et al. (2007),demonstrated how the awns in wild wheat function mechanically to help thespikelet work its way into the soil by daily cycles of humidity. Dispersal bywind and by sticking to animal fur may be co-selected (see Schurr et al., thisvolume), and the wild progenitors of several cereals include bristly diasporeunits for such dispersal, such as in Setaria spp. and Pennisetum glaucum. Oncenatural selection was removed to maintain such dispersal aids, smaller andfewer appendages may have developed by genetic drift, in which case wewould expect to find a great deal of diversity in early cultivars. Certainly, thereremains a great deal of variation in this regard: some cultivated rices haveawns while others do not; there are ‘bearded’ and ‘unbearded’ wheats. How-ever, it may also be the case that selection operated by reducing metabolic‘expenditure’ creating a parallel trend towards less barbed and hairy cerealspikelets, which can be observed across species.

Unfortunately, there is little archaeological evidence on this evolutionarytrend, as hairs and awns survive poorly in the archaeological record. Someremains of early rice from China have been examined in this regard (e.g.Sato, 2002; Tang et al., 1996), and the reduction of the number of spikeletswith awns, the density of hairs on the awns, and the length of those hairs can


Figure 7.7 Comparison of awn hair (bristle) density and bristle length on wild anddomesticated rice awns, together with a few archaeological specimens from Hemudu,Zhejiang Province China, ca. 4800 bc (after Tang et al., 1996).

potentially be studied (Fig. 7.7). Evidence for variation in both the numberof unicellular trichomes (bristles) on awns and the length of these trichomessuggests that shorter trichomes are typical of domesticated rices that haveawns at all (Fig. 7.7), and indeed many domesticated rices have lost their awnsaltogether. Evidences from four archaeological rice awns examined from thesite of Hemudu (5000–4500 BC) place these amongst the wild scatter (Tanget al., 1996), a situation in agreement with arguments from grain size datafrom the region (Fuller et al., 2007a), and more recent evidences from spikeletbases (Zheng et al., 2007; Fuller and Qin, 2008; Fuller et al., 2009) that indicatepopulations of rice from the Lower Yangtze of that period were dominatedwith wild-type morphological adaptations. To date, too few samples of ar-chaeological rice awns have been studied for any temporal trends in suchevidence; nor has comparable data from other taxa been examined.

A related trait is the shift from single-grained wild dispersal units to themultiplication of grains under domestication. The best studied example isthat of barley, in which wild Hordeum spp. normally have a single grain withtwo lateral sterile florets that contribute to an overall aerodynamic shape ofthe diaspore. In domesticated barley, six-row varieties have evolved by the


removal of inhibition of lateral florets. This not only led to production ofmore grains (by ca. 150%) per year, but it also created difficult-to-dispersegrouped triplets of spikelets (Harlan, 1992, p. 120; Zohary and Hopf, 2000,p. 60). Genetic studies indicate that the six-row condition evolved three times,by three distinct mutations, across different parts of Eurasia (Komatsuda et al.,2007). Archaeobotanically, this trait can be inferred from the form of grains aswell as the form of well-preserved rachis segments. Such evidence indicatesthat this trait evolved very early indeed. Asymmetrical grains, typical ofsix-row forms, and rachis segments with widened apices are reported in theNear East from the Early PPNB (8800–8000 BC) (Zohary and Hopf, 2000, p. 68),prior even to the fixation of non-shattering rachises (see discussion above).Similarly, the earliest barley remains from Pakistan at Mehrgarh, ca. 7000BC, include evidence for six-row forms (Costantini, 1983). Possible paralleltrends are indicated for the New World little barley (Hordeum pussilum),for which some twisted grains, and possible naked–grained varities havebeen reported, but remains debated (cf. Bohrer, 1984; Asch and Asch, 1985,p. 194; Hunter, 1992). This species has long been argued to be an indigenouscultivar in prehistoric North America on the basis of finds of large quantities,mainly from the First Millennia BC and AD (Asch and Asch, 1985, pp. 191–195;Dunne and Green, 1998). Such evidences require confirmation and furtherdocumentation, but it would imply domestication in terms of being releasedfrom the need to maintain wild dispersal aids.

A similar development occurred with the domestication of pearl millet(Pennisetum glaucum). Wild Pannisetum, normally has a single grain in eachbristly involcure, while domesticated forms often have multiples grains.The study by Godbole (1925) of Indian peal millet suggests ∼70% of in-volucres include two spikelets (each with a grain), while ∼20% are singlegrained. The other ∼10% includes more than two grains, with as many asnine grains reported from a single involucre. Archaeologically, early impres-sions of pearl millet preserved in pottery, indicate not only the presence ofthe non-shattering stalked forms, but also the presence of paired spikeletsindicating that this trait had evolved in cultivated populations certainly byca. 1700 BC (see Fuller et al., 2007b).

7.6 Non-cereal alternative: appendage hypermorphyin fibre crops

In the case of at least a few fibre crops, selection under cultivation has favouredincreases in appendage size, as human selection has worked on what wereadaptations for dispersals and caused exaptation for fibre production. This ismost clear in the cases of cottons, in which four domesticated species are cul-tivated for seed coat hairs, which are extensions of testa cells. In the wild, suchhairs may aid dispersal by wind or attachment to animal fur (see Ridley, 1930,


p. 158; Fryxell, 1979, pp. 142–143; Hovav et al., 2008), but in wild tetraploidcottons domesticated in the New World, lint seems to have been exapted todispersal by water to littoral habitats (Fryxell, 1979, pp. 143–147, 164–165),and oceanic drift is hypothesized to have brought A-genome cotton fromAfrica to America (Phillips, 1976). In domesticated cottons, however, hairshave become so heavy, long and tangled as to preclude such dispersal meth-ods. In addition, domesticates have lost the hard impermeable seed coatswhich allowed survival in salt water. Early cultivators seem to have chosenthose wild Gossypium species with the longest hairs, but it is also true thatall cultivated cottons have significantly longer hairs than their wild relativesindicating selection. Hutchinson (1970, p. 271) reported an apparently spon-taneous single gene mutation controlling this in wild G. barbadense. Fryxell(1979, p. 173) argues that selection for increased lint probably preceded se-lection for increased fruit size, at least in domesticated G. hirsutum. Unlikethe loss of wild-type seed dispersal which is regarded as having evolvedfrom unconscious selection on the part of farmers, we might expect hair en-largement to have been intentional. As such, conscious selection might beexpected to exert a stronger selection pressure on genes involved in seed coathair formation than that typical of most domestication traits.

Another example comes from the Devil’s claw (Proboscidea parviflora), whichhas also been cultivated for its fibres in the American Southwest since prehis-toric times (Nabhan et al., 1981; Bretting, 1982, 1986; Nabhan and Rea, 1987).The claws of this species represent extensions of seed capsule apices (rostra).These apical claws bend such that they can serve as hooks to cling to animalhair for long-distance dispersal. Human use of this species involves softeningand pounding of capsules to separate the fibres that make up the capsule.These are used to make cords and basketry type products. It is suggestedthat it has only been cultivated in recent centuries, and the earliest finds areca. AD 1150 (Nabhan and Rea, 1987, pp. 59–60). The enlarged capsules andmuch longer claws of domesticated forms provide for more extensive fibres.This is therefore also likely to have been a product of conscious selection. Inaddition, domesticated devil’s claw has evolved white seeds, rather than theblack seeds of the wild form, probably indicative of typical domesticate-typeloss of germination inhibition (see below).

7.7 Loss of natural seed dispersal in pulsesand other crops

Other seed crops have also evolved non-dispersing fruit types with domesti-cation, although these remain largely undocumented archaeologically. Mem-bers of the Fabaceae have been domesticated in parallel in most world regionswhich had early cereal domestications (Harris, 1981, 2004; Smartt, 1990).Natural seed dispersal in wild legumes, including the wild progenitors of


domesticated pulses, is normally by pod dehiscence. That is, seeds are phys-ically shed by pods that twisted and split as they dried after maturity. Indomesticated species, this is removed or delayed (see Fig. 7.1), although vari-ous observations suggest that the degrees of reduction in this trait vary acrosstaxa (e.g. Fuller and Harvey, 2006, p. 223, for South Asian species). In contextswhere pulse pods are preserved, such as by desert conditions, it may be pos-sible to determine the presence of this domestication trait by examination ofthe pod layering: the inner layer that causes dehiscence should be reduced.Pods of Phaeseolus lunatus and P. vulgaris from Guitarerro Cave in Peru showthat this non-shattering trait was present (Kaplan et al., 1973), although thesemay be intrusive finds in deposits attributed to ca. 8000 BC (cf. Lynch et al.,1985), since direct dates on P. lunatus and P. vulgaris seeds go back to 3500and 2300 years ago, respectively (Fritz, 1994, p. 307; Kaplan, 2000). Withinsome pulses, genetic loci involved in non-deshicent pod formation have beenidentified, such as Dpo1 and Dpo2 in Pisum (Weeden et al., 2002; Weeden,2007), and the different loci v and p were selected in common bean, Phaseolusvulgaris (Koinange et al., 1996). Interestingly, by contrast to non-shattering incereals, this trait appears to be controlled by more than one locus in some ofthe above studied Fabaceae domesticates (Phaseolus spp., Pisum). This pre-sumably accounts for the degrees of pod dehiscence reported from somespecies and may suggest that this was a less central part of the early do-mestication syndrome in many pulses than it was in cereals. Nevertheless, inother pulse species, there appears to be one key gene mutation involved innon-shattering. Such evidence comes from Lens (Ladizinsky, 1979), and fromazuki bean, Vigna angularis (Kaga et al., 2008). In these species, this trait isthus comparable to the cereal rachis in that respect, especially with regards toprocesses of selection on a population level. As argued by Ladizinsky (1987,1993), pulse domestication may be fundamentally different from cereal do-mestication, contradicting Zohary and Hopf (1973; Zohary, 1989), in that lossof germination inhibition may have been the key and prerequisite trait thatmade early cultivation efficient.

Some other seed crops show parallel trends towards non-dehiscent mor-phologies, such as flax (Linum usitatissimum) which has non-shattering cap-sules in the domesticated state (Zohary and Hopf, 2000, p. 123). Early evi-dence suggesting domesticated flax comes from the Near East from fragmentsof probable capsules at Pre-Pottery Neolithic Jericho (8400–7500 BC) andlarger than wild seeds at Tell Ramad (7500–6500 BC) (Zohary and Hopf, 2000,p. 130). On the other hand, a few crop species appear to not have evolvedthis, perhaps due to differences in the genetic architecture of this trait. Thus,in sesame (Sesamum indicum), for example, capsules still dehisce in most do-mesticated forms, and this constitutes a persistent issue for plant breeders(Day, 2000; Fuller, 2003). In this case, non-dehiscent forms produce muchlower yields and are unattractive. Because pods and capsules tend to belight, and are therefore unlikely to survive contact with fire, they are exceed-ingly rare in archaeological contexts. It is therefore the case that we have little


direct archaeological evidence on the evolution of these traits in pulses oroilseeds.

7.8 Germination traits in domestication: the importanceof loss of dormancy

In the wild, many seeds will only germinate after certain conditions havepassed, such as conditions of day length, temperature, or after the seed coatis physically damaged. Crops tend to germinate as soon as they are wet andplanted. This is selected for simply by cultivation, and sowing from harvestedyield, as those seeds that do not readily germinate will not contribute to theharvest. As such, the selective forces and mechanisms involved are expectedto differ from those involved in the loss of wild-type seed dispersal.

Germination differences between crops and their wild progenitors comein a range of severity. The study of changes in dormancy with domesticationis complicated in many crops; this is due to limited morphological visibilityof dormancy-related traits, and limited knowledge of the factors that governdormancy.

Dormancy and germination are traits that are controlled in a highly com-plex manner involving one or a combination of morphology, physiology andphysical structures (Baskin and Baskin, 2001; Finch-Savage and Leubner-Metzger, 2006). Not least of the complications of dormancy is its definition.Dormancy can be described as a block to germination, which is to say thata non-germinating seed may not be dormant, but merely awaiting inductionof germination. Finch-Savage and Leubner-Metzger (2006) define dormancyclasses by distinguishing morphological, physiological deep, physiologicalnon-deep and physical dormancy. Morphological dormancy refers to seedsthat have an underdeveloped embryo and require time to grow and germi-nate. Physiological dormancy, the most prevalent form of dormancy, appearsto broadly involve abscissic acid (ABA) and gibberellins (GA) metabolism.Physical dormancy (coat dormancy) involves the development of a water-impermeable seed coat, and is typically broken by scarification. Such physi-cal dormancy is typical of the wild progenitors of cultivated legumes, and isone of the key traits that has been modified with domestication (Zoharyand Hopf, 1973, 2000, p. 93; Ladizinsky, 1987; Plitman and Kislev, 1989;Kaplan, 2000). It is interesting to note that morphological dormancy is moretypical of the less-derived flowering plants; physiological dormancy is foundthroughout flowering plants (and gymnosperms), while physical dormancyoccurs amongst the most derived families, most notably the Fabaceae (seeFinch-Savage and Leubner-Metzger, 2006).

In crops from several dicotyledonous families, dormancy traits can be seenin the seed coat. In particular, wild-type seeds tend to have thicker seed coats,often of a different colour (black or dark brown, or mottled) and often with


Figure 7.8 Comparisons between wild and domesticated seeds, showing seed coatcolour, surface texture and thickness differences with domestication. At left are wild anddomesticated Sesamum indicum, wild above and domesticated below; at right are wildand domesticated Chenopodium album, wild above and domesticated below. Seeds fromInstitute of Archaeology, UCL collections: Seasmum malabaricum from coastal sanddune,Sindhudurg district, Maharashtra, India (coll. D Fuller 9/2004); Domesticated S, indicumblack variety from Pune (8/2000); white S. indicum from India PI164384 01 SD;Chenopodium album, wild from European seed reference collection, Institute ofArchaeology, UCL; Chenopodium album, domesticated, collected by E. Takei from theRukai tribe, Taiwan (5/2007) (sample in UCL, courtesy of E. Takei).

additional surface ornamentations. Domestication has resulted in the thin-ning of seed coats, the lightening of seed coat colour and the loss of rugae orpapillae. Such traits have evolved in parallel across families and genera, andworld regions. For illustration, examples of modern wild and domesticatedseed pairs are shown from Sesamum indicum and Chenopodium album (Fig. 7.8).Pigmented seed coats (or pericarps), which have long been associated withfunctional dormancy in wheats (Flintham and Humphry, 1993), may also belinked to dormancy in wild rice, which has evolved white pericarps onlyonce after domestication (Sweeney et al., 2006, 2007). Nevertheless, it is alsothe case that physical changes are not always evident from visible morphol-ogy. Morphological indicators of pericarp colour change are not detectablein the charred grains recovered by archaeologists. Even in other families,this may prove difficult to document archaeologically. In Near Eastern pulsecrops, for example Butler (1989, 1990) was able to document clear morpho-logical differences in the seed coats of wild and domesticated peas, but notof lentils, chickpeas or Vicia spp., where morphological variation falls alonga spectrum from thicker (and sometimes ornamented) seed coats in wildpopulations and some cultivars, to thinner, smooth forms in other cultivars.This physical spectrum may relate to a functional spectrum in germination


inhibition. Weeden (2007), for example, has documented a spectrum of varia-tion in germination between wild Pisum sativum subsp. elatius, with virtuallyno immediate germination within 1 year of seed formation, Pisum abyssinicum(the Ethiopian pea), which shows partial breakdown of germination inhibi-tion (seeds germinate in 3–12 months), and modern Pisum sativum subsp.sativum which readily germinates (cf. Weeden, 2007). A wide range of germi-nation rates is reported from Lablab purpureus, but with significantly higherproportions of faster germination in cultivated populations (Maass, 2005). Awide range of variation is especially noted amongst wild accessions of Lablab,which may suggest that domestication drew upon existing genetic variationin this species.

Ladizinsky (1987) argued that the very low germination rates in wildpulses, in particular Lens, would have precluded successful cultivation onthe basis of very low yields from planted seeds. He therefore suggested thathunter–gatherers must have recognized favourable wild mutants with readygermination from which to begin cultivation, that is there was a form of‘pre-cultivation domestication’. This hypothesis, however, received critiques(Zohary, 1989; Blumler, 1991). Ladizinsky’s (1987) argument for Lens cultiva-tion contrasts to cereal cultivation in that he reasons that the domesticationsyndrome phenotype of a lack of dormancy would have to arise in the wildrather than the cultivated gene pool because cultivator pressures would nothave been sufficient to break dormancy. Ladizinsky argued that this is alsosupported by genetic diversity data based on isozymes, which show differentcultivated groups of Lens appear to be most closely related to different wildgroups of Lens, indicating a multiple domesticated origin, despite a singlemutation responsible for dormancy breaking (Ladizinsky, 1987, 1993). He ar-gued that the most parsimonious explanation is that such a mutant may havebeen persisting in the wild. The ‘comparable’ tough rachis mutant in cerealsis postulated to have arisen in the cultivated population rather than the wildwhere it has been believed that the tough rachis mutant would not persist.Zohary (1989) argues that the lack-of-dormancy mutant also would not sur-vive in the wild. More recently, Kerem et al. (2007) have suggested that evenlow yields from wild-type pulses (in particular chickpea, Cicer arietinum) mayhave been favoured because the presence of particular micronutrients (theamino acid tryptophan) were the target of early pulse consumption ratherthan overall protein or carbohydrate (also Abbo et al., 2007, on Pisum). Theextent to which any of these hypotheses might apply across pulse domes-tications from difference subfamilies and different regions is unclear. Moreresearch is needed. So far, archaeobotanical evidence has contributed little tothe documentation of the earliest processes of pulse domestication and theevolution of these domestication traits.

Evidence for the loss of germination inhibition may be preserved archaeo-logically, although detailed studies are only available for a few species. Onechallenge is preservational: seed coats are often not preserved on charredpulses. This is clearly the case with Indian Vigna spp., for example (Fuller


and Harvey, 2006). Those species which have been best documented areNew World Chenopodium domesticates (e.g. Smith, 1989, 1992, 2006bb; Brunoand Whitehead, 2003; Bruno, 2006). In a classic case of the fossil record (ar-chaeobotany) identifying an extinct crop, Smith (1989, 1992, 2006b) trackeda marked decrease in seed coat thickness in Chenopodium berlanderii seedsfrom sites in the Eastern Woodlands of the United States between ca. 2500BC and 1500 BC. In addition to thinning seed coats, presumably linked to lossof wild-type germination inhibition, seeds tended to change shape and size,although wild-type forms persisted as weeds alongside the Chenopodium crop(Gremillion, 1993). Bruno (2006) has developed a similar approach to study-ing South American Chenopodium domestication, although variation in seedcoat thickness amongst wild species makes this more difficult requiring theuse of additional size and shape characters. Although modern material sug-gests a similar change has occurred in Old World Chenopodium album, at leastamongst East Asian domesticated populations (see Fig. 7.8), archaeobotani-cal evidence tracking such changes has not been gathered. Given suggestionsthat Chenopodium was formerly a crop of Iron Age Europe (Helbaek, 1954; cf.Henriksen and Robinson, 1996, pp. 9–19; Stokes and Rowley-Conwy, 2002)or of Bronze Age Gujarat, India (‘intential collection’ inferred by Weber, 1991,p. 121), studies along these lines are warranted.

7.9 The genetic basis for dormancy and germination

A large number of genes may be directly or indirectly involved with dor-mancy. For instance, developmental genes can be expected to be involvedin morphological and physical dormancy, while abscissic acid (ABA) andgiberellic acid (GA) make up two of the most common plant hormones,which are expected to involve numerous loci across the genome.

Some progress is being made with understanding the molecular basis ofdormancy with regards to non-deep physiological dormancy, typical of thecereals. Physiological dormancy is largely governed by the ratio of ABA toGA. When this ratio is high, dormancy prevails, and when GA levels becomehigh enough relative to ABA, then germination is initiated (White et al.,2000; Kucera et al., 2005). Two other hormones also known to have roles areethylene and the brassinosteroids, both of which act similar to GA to promotegermination and counter the effects of ABA (Kucera et al., 2005).

Dormancy is a necessary part of seed development during which ABApromotes maturation pathways that govern storage compound depositionand dessication of the grain. GA synthesis is actively inhibited in maizeduring this time (White and Rivin, 2000). It is thought that dormancy releaseis due to ABA breakdown and this is the primary hormone. After breakdown,the presence of GA in sufficient concentrations relative to ABA can promotegermination. This is supported by work with Avena fatua, which demonstratesthat GA is involved in dormancy loss (although it can be used to break


dormancy in this case), but is involved in initiating germination (Fennimoreand Foley, 1998).

In cereals, QTL studies have been used to try and track down importantloci for dormancy. One gene of great significance is VP1 (McCarty et al., 1991).VP1 is a transcription factor that promotes dormancy in the presence of ABA(Cao et al., 2007). Mutations in this gene lead to a loss of function that resultsin vivipary where seeds will germinate while still on the plant (also knownas preharvest sprouting). This gene has been identified in sorghum, wheat,rice, barley and oats (Hattori et al., 1994; Jones et al., 1997; Bailey et al., 1999;Carrari et al., 2003; Osa et al., 2003). In wheat, the incorrect assemblage ofexons (mis-splicing) of VP1 messenger RNAs is responsible for the non-functional types leading to vivipary (McKibbin et al., 2002). Interestingly,these mutants in hexaploid wheat appeared to have been inherited fromtheir tetraploid ancestors, thus implying that they were established early onin the development of agriculture. The VP1 gene is up-regulated by ABA,and has the function of promoting dormancy (Cao et al., 2007). The functionalVP1 gene also activates an anthocyanin pathway resulting in pigmented seedcoats, which have long been associated with functional dormancy in wheats(Flintham and Humphry, 1993). The VP1 and seed coat colour (R) genesare loosely linked which may also partly explain the correlative effect to dor-mancy – efforts are being made to increase dormancy of white-grained wheats(Kottearachchi et al., 2006). There are several other genomic regions, whichare important in dormancy, which have been identified by QTL analysis, butthese genes’ loci have yet to be identified (e.g. Wan et al., 2005; Vanhala andStam, 2006; Hori et al., 2007; Gao et al., 2008).

The physical dormancy imposed by seed coats is thought to be largely as-sociated by �-1,3-glucans (callose) which are deposited in cell walls (the neckregions of plasmodesmata) during maturation (Finch-Savage and Leubner-Metzger, 2006). Increased callose deposition is associated with increased dor-mancy in a number of species. The �-1,3-glucanases which break the callosedown are associated with the dormancy release. It is likely that mutationsin genes associated with these pathways are involved in the domesticationprocesses that are associated with weaker dormancy by seed coat thinning asseen in pulses. This may also be true in other families of domesticates such asAmaranthaceae, Chenopodiaceae and Pedaliaceae/Martyniaceae (Sesamum,Proboscidea). In the case of lentil, a single dominant gene is reported to be re-lated to the hard seed coat in non-germinating wild-types (Ladizinsky, 1985).

7.10 Germination and seedling competition: changesin seed size

‘. . . we must conclude that man cultivated the cereals at an enormously remoteperiod, and that he formerly practiced some degree of selection, which in itselfis not improbable. We may, perhaps, further believe that, when wheat was first


cultivated the ears and grains increased quickly in size, in the same manner as theroots of the wild carrot and parsnip are known to increase quickly in bulk undercultivation.’

Charles Darwin (1883, p. 338)

Changes in size are one of the most widely commented on and obviousdifferences between domesticated and wild varities (e.g. Darwin, 1883; DeCandolle, 1885, p. 460; Helbaek, 1960). While this is one trait that might besuggested to be under conscious and intentional selection on the part of hu-mans, what Darwin termed ‘methodical selection’, there remains no clearevidence that this was the case in prehistory when seed sizes changed undercultivation. Heiser (1990, p. 199) concluded that it is ‘more likely that largeseeds result from unconscious selection over a period of time,’ because itwas unlikely to be easy to select for as it is thought to be the product of theinteraction of many genes. In a recent comparative review, it was shown thatchanges in seed size did not happen at a consistent rate or timing in relationto the beginnings of cultivation or other domestication traits (Fuller, 2007a).This suggests in turn that certain factors in cultivation regimes interact withthe inherent variability and genetic architecture of seed size traits within par-ticular taxa in ways that are not uniform across taxa. Changes in size are notqualitative traits of domesticates, like non-shattering is, or to a certain extentthat even ease of germination tends to be. Thus, it has been suggested thatthe trait be regarded as ‘semi-domestication’ as it is a quantitative populationlevel trait that is selected at some stage during human cultivation but notnecessarily linked directly to key domestication traits. Seed size and othersuch traits constitute a kind of soft selection in relation to the cultivated en-vironment and probably a high degree of population variability built on amulti-genic basis. In this regard, it is of interest to document the extent towhich grain-size increases precede hard-selected domestication traits, likenon-shattering or loss of germination inhibition, as seems to be the case inwheat, barley and possibly rice; or whether size increase is later as appearsto be the case in pulses and Pennisetum glaucum (Fuller, 2007a). These dif-ferences may point towards the underlying selective pressures in the soilenvironment.

The arable field has been called a ‘botanical battleground’ (Jones, 1988), andthis is true not only between crops, farmers and weeds but also within speciesin the form of seedling competition. Well-tilled and cleared fields offer nutri-ents, abundant sunlight and normally plenty of water, and thus competitionshould be expected to favour seeds that not only germinate rapidly but alsoestablish rapidly and even overtop competition. This tilled field competition,including factors of both general disturbance and depth of burial, can be ex-pected to select for larger seed size (Harlan et al., 1973; Harlan, 1992, p. 122;Fuller, 2007a). As studies of weed seed ecology have shown, there is a vari-ation between species in terms of ideal and tolerable depths of germination(King, 1966, pp. 138–140), and this means that weed communities have been


heavily influenced by human tillage practices that have established differ-ing average depths of burial. This is indicated by studies within species andbetween species that suggest a correlation between larger seeds and largerseedlings (Krishnasamy and Seshu, 1989; Harlan, 1992, p. 122; Baskin andBaskin, 2001, p. 214). Comparative ecology indicates that larger seeds gen-erally have competitive advantages over smaller seeds under certain kindsof competition including deeper burial (Maranon and Grubb, 1993; Westobyet al., 1996; but there are some apparent exceptions amongst grasses (Baskinand Baskin, 2001, pp. 212–213). Oka and Morishima (1971) showed in exper-imental cultivation of wild rice that some increase in average grain weightcould be measured within just five generations, in the cultivation of wildperennial rice (O. rufipogon). An old agronomic rule of thumb is that seedsgerminate best at depths up to four times the diameter of the seed (King, 1966,p. 140). Since archaeology mainly recovers the seeds of crops, archaeobotan-ical evidence lends itself to studies of variation and changes in sizes throughtime. Nevertheless, caution is warranted in interpreting such evidence as do-mesticated crops often include a much greater range of grain size variationthan is found in wild species (Harlan et al., 1973; Vaughan et al., 2008).

While study of seed size is the most readily available domestication trait inarchaeological evidence, it is complicated by some confounding factors. Pre-served seed size may be affected by the state of archaeological preservation:most archaeological seeds are preserved carbonized, by exposure to fire, andthis has been shown to distort seed shape but especially to lead to shrink-age (e.g. Helbaek, 1970; Van Zeist and Bakker-Heeres, 1985; Lone et al., 1993;Braadbaart et al., 2004). Nevertheless, if it is assumed that most archaeologicalseeds have been affected in a similar manner, then real trends can be inferredfrom the data. Experiments provide some general guidance on the probablerange of correction factors for comparing modern seeds, although the usual10–20% shrinkage that is suggested is by no means a given. Another potentialproblem is that past crops may have been harvested before all seeds were ma-ture and immature seeds may resemble smaller versions of the more matureseeds. For example, on the basis of growing experiments with a number ofpulses, Butler (1990) concluded that seed size could be misleading:

‘If harvesting is confined to one episode, the seeds constituting the crop are not allin the same state of maturity. This may be reflected in their size; smaller, slightlyimmature seeds may be present together with the full-sized ripe ones. Commonly,it seems, the number of fruiting nodes per branch is two, which bear seeds at twostages of maturity at any one time. If these are harvested together, the impressionmay be formed that the seeds have been derived from two different populations oreven different taxa. This could lead to erroneous identifications such as the seedsof a cultigen occurring together with those of its wild relative.’

E. A. Butler (1990, p. 350)

Similar concerns over the likelihood of immature harvesting of wild riceand early rice crops were discussed by Fuller et al. (2007a; also Fuller, 2007a).


While such concerns make it dubious to identify single archaeological grainsas domestic or wild only on the basis of size, it nevertheless still appearsuseful to examine the metrical traits of populations (site assemblages andassemblages from across a region), as these appear to show real evolutiontrends over time.

There is a growing morphometric database for wheat and barley fromthe Near East (Colledge, 2001, 2004; Peltenberg et al., 2001; Willcox, 2004).This indicates that wheat and barley grains increased in size starting in thePre-Pottery Neolithic A (PPNA) and earliest PPNB. This is before clear andwidespread evidence for tough rachises and loss of natural seed dispersal.It is well known that wild and domesticated cereal grains differ in size andthis has been used to infer the domesticated status of cereals, already in thePPNA and the earliest PPNB, including sites from the Jordan Valley, the upperEuphrates in Syria, and the first settlements on Cyprus (Colledge, 2001, 2004).This evolutionary shift can be illustrated from evidence from individual sitesequences, such as at Jerf el Ahmar (Willcox, 2004), in which a contrast is seenbetween the barley grains from the early phase at Jerf el Ahmar (9500–8800BC) and the later phase at Jerf el Ahmar, ca. 8500 BC (Fig. 7.9). The grains ofthe later phase are comparable to those from the Chalcolithic Kosak Shimali(ca. 5500 BC). If such data are plotted as means and standard deviationsagainst time, the long-term trend is clear (Fig. 7.10): an early increase in grainthickness and breadth followed by a remarkable stable grain size from 6000BC onwards.

Nevertheless, an explanation of these data remains controversial. We takethis to indicate evolution towards larger grain size during the occupa-tion of this site (Fuller, 2007a; also, Nesbitt, 2004, p. 39), whereas Willcox(2004), by contrast, queries whether this is not just a product of bettertended cultivars or the introduction of larger grained varieties from else-where (see also Willcox et al., 2008). This early change is indicated in seedwidth and thickness, but not in seed length. While Willcox (2004) arguesthat this does not fit with evolution of larger grains under cultivation, wethink that a comparative perspective indicates quite the opposite. As washypothesized by Harlan et al. (1973), grain size should increase as a prod-uct of soil disturbance and deeper burial with cultivation, and this has anestablished observational and experimental basis in seed ecological stud-ies (e.g. Krishnasamy and Seshu, 1989; Maranon and Grubb, 1993; Baskinand Baskin, 2001, p. 214; see also experimental cultivation by Oka andMorishima, 1971). However, rather than seeing this as a single directionalprocess, we must consider the likelihood that there were differing selec-tive thresholds that acted on grain size (and multiple contributing geneticloci) at different times. This is suggested by comparative examples, suchas West African pearl millet in which an initial grain thickening occurred,but increase in grain size (mainly in length and, allometrically, in width)only happened much later, in regions and periods with more intensiveagriculture.


Figure 7.9 Scatter plots of archaeological grain measurements showing the increase ingrain size under early pre-domestication cultivation (after Willcox, 2004). (a) Barley grainmeasurements, comparing early Pre-Pottery Neolithic A Jerf el Ahmar with the much laterdomesticated material from Kosak Shimali. (b) Comparing early and late Jerf el Ahmar,indicating that shift towards larger grain size had already occurred. (c) Similar comparisonof einkorn grains (probably including some rye grains) at early Jerf el Ahmar and KosakShimali. (d) Trend towards larger grain sizes over the course of Jerf el Ahmar occupation.

In the case of pearl millet, we have some metrical data from West Africafrom which to examine grain size change during and after domestication,with some comparative data from ancient India (Figs. 7.11 and 7.12). Datasets for looking at morphometric traits of past African populations of pearlmillet have only been published recently, since 2000. As already noted, pearlmillet domestication is evident from ceramic impressions of pearl millet chaffthat include the stalk, which are present by ca. 2500 BC in northeast Mali (un-published data), and 1700–1500 BC in Mauretania (Amblard and Pernes, 1989;MacDonald et al., 2003; Fuller et al., 2007a), and slightly later in Nigeria (Kleeet al., 2000, 2004). Early grain assemblages of similar date show the sub-tle change in grain shape, becoming apically thicker and more club-shaped


Figure 7.10 Time series of archaeobotanical metrical data on charred barley grains.Data plotted on the basis of a median age estimate for each site in calibrated radiocarbonyears. Lines indicate standard deviation and minimum and maximum outliers are alsoindicated. Sites (in chronological order): Jerf Early, ZAD 2, Jerf Late, Djade, Ganj Dareh(no thickness data), Ramad, Bouqras, Erbaba, Kosak Shamali, Selenkhiye, Hadidi, RoshHiyat. Where standard deviations were not provided in published sources, these havebeen estimated after the normal distribution following Pearson and Hartley (1976).

(D’Andrea et al., 2001; Zach and Klee, 2003). However, a major increase inseed size appears delayed (D’Andrea et al., 2001, p. 346; Fuller, 2007a). Of noteis that early West African populations, from the second and first millenniaBC, have their averages firmly in the wild size range, although there are longtails of variation that extend into the larger size range (e.g. at Birimi, Ghana).


Figure 7.11 A map of archaeobotanical sites with important pearl millet data in Africain relation to probable West African domestication zones. Later ‘historical’ sites post-date100 bc, and represent only a selection with metrical data used in Fig. 7.12 (Indian sitesnot shown). Site numbers are as follows: 1. Dhar Tichitt sites; 2. Dhar Oualata sites; 3.Djiganyai; 4. Winde Koroji; 5. Karkarichinkat; 6. Ti-n-Akof; 7. Oursi; 8. Birimi; 9.Ganjigana; 10. Kursakata. Historical sites with pearl millet metrical data: 11. Arondo; 12.Jarma; 13. Qasr Ibrim. (Primary data sources compiled in Fuller, 2007a.)

One of the earliest finds of pearl millet from India comes from Surkotada,Gujarat, ca. 1700 BC, which can be seen to fall with these early domesti-cated African populations. By contrast, rather later seeds of a North Indian(Gangetic) population from Narhan are markedly larger, suggesting selectionfor larger grained pearl millet. On basis of Vigna pulse size increase in thesame horizon, it was suggested that selection for larger grains may be drivenby deeper seed burial through the use of ard tillage (Fuller and Harvey, 2006;Fuller, 2007a). However, the continued small-grained populations in EarlyHistoric South India (Nevasa) suggests that there may be factors that workagainst gigantism in pearl millet, and in the absence, reinforcing selectionpopulations may retain or even revert to smaller size ranges. In Africa, largergrained populations appear only in the First Millennium AD, represented byfinds from Nubia and Libya, as well as Medieval Senegal.

This raises questions about the selection pressures involved in large-grained Pennisetum, and in seed crops generally. While initial cultivation


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may have selected for non-shattering, and slight changes in grain weight andshape (the club shape), serious gigantism may have required a stronger selec-tion pressure and therefore evolved later: a millennium or more later in India,and two millennia later in Africa. As both Libya and South India lack wildpopulations, this cannot be attributed to cross-pollination with wild-types.There may be some constraints particular to this crop, as one experimentindicates that optimal germination occurred under higher temperatures thatresult in lower average grain weights (Mohamed et al., 1985). In addition,pearl millet involucres are polymorphic in grain count with the vast majorityproducing two grains, a large minority with one larger grain, and a fur-ther minority producing three to nine grains, which are necessarily smaller(Godbole, 1925). Thus selection for higher grain counts, and more reliablegermination, might conflict with selection for larger seed sizes. Nevertheless,as a working hypothesis, it is proposed that there is a deeper burial thresholdthat selected for gigantism in pearl millet in some times and places (Fuller,2007a). If so, then large-grained varieties evolved under plough systems andthen dispersed back to West Africa at a later date. In that regard, it mightbe noted that the larger grain populations in Libya and Nubia, like that inGangetic India, are associated with more intensive plough cultures. This sug-gests separate events of grain enlargement in India and northeastern Africa.Beyond informing us about pearl millet, this case provides useful compar-ison to other cases of plant domestication, including that in the Near East.It suggests that we need to consider different aspects of the domesticationsyndrome separately, even different aspects of grain shape and size change.

A lag between domestication and any appreciable seed size increaseappears to be the case in several tropical pulses, including Indian Vigna(Fuller and Harvey, 2006; Fuller, 2007a), and West African Vigna unguiculata(D’Andrea et al., 2007). This may suggest that a higher selective pressure wasneeded to cross the threshold into big-seeded pulses; a threshold inferredby Fuller and Harvey (2006) to be ploughing (ard tillage). Perhaps, a similareffect created a lag time between initial grain thickening in cereals, associ-ated with the earliest cultivation, and more marked grain size increase in alldimensions, including length.

In Near Eastern lentils, size change appears to have been much slowerand more gradual than in the cereals, without a clear levelling off after theNeolithic (Fig. 7.13). This may suggest an initially weaker selection, but mayalso indicate that seed size is more plastic in pulses. The genetics of seed/grainsize is still poorly understood, but it is presumed to be under polygeniccontrol. This has been documented in Lens (Abbo et al., 1991) and Pisum(Weeden, 2007).

In the case of rice domestication, the utility of grain measurements is hotlydebated (Thompson, 1996; Crawford and Shen, 1998; Fuller et al., 2007a; Liuet al., 2007). As modern comparative data indicate, there is a vast range of met-rical variation in domesticated rice (Fuller et al., 2007a; Vaughan et al., 2008),and some of this variation seems to be correlated with climatic conditions


Figure 7.13 Time series of archaeobotanical metric data on charred lentil seeds. Dataplotted on the basis of a median age estimate for each site in calibrated radiocarbonyears. Lines indicate standard deviation and minimum and maximum outliers are alsoindicated. Where standard deviations were not provided in published sources, these havebeen estimated after the normal distribution following Pearson and Hartley (1976).(Compiled from a large number of primary archaeobotanical reports by Jupe, 2003: Fromleft to right, sites include Qermez Dere, Murreybit, Jericho, Aswad, Jericho, Ganj Dareh,Yiftah’el, Aswad, Ain Ghazel, Basta, Ramad, Ali Kosh, Ras Shamra, Jericho, Tepi Sabz, BethShean, Jericho, Lachish, Arad, Tell Bazmosian, Jericho, Hadidi (some sites occur more thanonce representing different phases))

such as altitude or latitude (Oka, 1988; Kitano et al., 1993): more northerlytemperate japonica landraces are short grained, while tropical varieties (thejavanica race rices) are massively long; in East Asia, upland rices tend to belonger grained versus shorter grained lowland forms (Nitsuma, 1993). Suchproblems are further compounded by variation in grain measurements thatmay relate to maturity, especially as wild rice and early cultivars are likelyto have been harvested somewhat immature to increase total harvests andbecause of uneven ripening (Fuller, 2007a; Fuller et al., 2007a). For this rea-son, it is probably safest to focus on changes through time within a fairlyrestricted region, or even within individual stratigraphic sequences (Fulleret al., 2008). On the left hand side of Fig. 7.14 is a time series of grain width datafrom the Lower Yangtze region (Chinese provinces of Zhejiang and Jiangsu),whereas on the left hand side later are the data from the Yellow River valleyfurther north where climatic conditions may have both selected for smallerrice and reduced the reliability of harvests and yields (thus causing the incor-poration of more immature or poorly formed grains). While the metrical datavary between regions, within a particular region (the Lower Yangtze), oftenpostulated as a probable centre of domestication and trajectory of increasinggrain size is visible.

Changes in grain size have played an important role in documenting pastdomestications in oilseed crops as well, including an extinct species formNorth America. Achene size is an important domestication trait of the sun-flower (Helianthus annus) and archaeological documentation of this indicatesdomestication taking place by ca. 2000–1500 BC in North America (Asch andAsch, 1985; Smith, 2006b; cf. Heiser, 2008). The most extensively documented


Figure 7.14 Time series of archaeobotanical metrical data on charred rice grains. Dataplotted on the basis of a median age estimate for each site in calibrated radiocarbonyears. Lines indicate standard deviation and minimum and maximum outliers are alsoindicated. Grey arrows indicate suggested selection trends with domestication; over thesame period, selection for non-shattering is indicated by spikelet base data. (Huang andZhang, 2000; Tang, 2003; Zheng et al., 2004; Liu et al., 2007; Tian Luo Shan: D. Fuller,unpublished.)

increase in seed/fruit size in North America is that associated with marshel-dar, Iva annua. Although this species is not known to have been cultivatedwithin historically documented periods, it was a major domesticate of theeastern North America from ca. 2000 BC, alongside the native Chenopodium,Hordeum pussilum and Helianthus annus. Indeed, it is the documentation ofpotential morphological indicators of domestication traits related to germina-tion that has allowed the reconstruction of indigenous cultivation in EasternNorth America (Smith, 1989, 1992, 2006b).

7.11 The genetics of seed size

The quality of seed size is a trait that is affected by many factors, and so can bethought of as polygenically controlled. Moreover, the regulatory networks in-volved with governing seed size, either directly or indirectly, are not at all wellknown. This is borne out by the many QTL analyses that have been carriedout which have shown seed size to be associated with many loci of varyingeffect (Gupta et al., 2006). Again, it is rice that is leading the way to elucidationof what these loci might be doing. At the time of writing, three genes derivedfrom principal QTLs have been identified in rice that directly influence grainsize (Fan et al., 2005; Song et al., 2007; Shomura et al., 2008). All three are lossof function mutations. Two result in an increase in the number glume cells,thereby giving the grain milk a larger cavity to fill, resulting in larger grainswhich are wider (Song et al., 2007; Shomura et al., 2008). The first of these, GW2,


occurs on chromosome 2 and encodes an ubiquitin ligase that may possiblybe involved with negative regulation of the cell cycle. The larger grained phe-notype is associated with an allele that has a mutation causing a prematurestop codon resulting in a non-functional truncated protein, which may resultin an inability to down-regulate cell division in the glume. The second, qSW5,occurs on chromosome 5. In this case, the large grain phenotype is associatedwith a large deletion in the gene, again resulting in more cells in the glume.It remains to be seen whether these two loci are actually interacting with thesame process of grain development, probably at different stages. The thirdlocus, GS3, affects grain length and size rather than width (on which it hasa small effect). This gene occurs on chromosome 3 and encodes a transmem-brane protein of unknown function. The protein normally has four domains:a PEBP-like (phosphatidylethanolamine-binding protein) domain, a trans-membrane region, TNFR/NGFR (tumour necrosis factor receptor/nervegrowth factor receptor), cysteine-rich domain and a VWFC (von Willerbrandefactor C) domain. The PEBP-like domain is partially deleted in proteins asso-ciated with longer and heavier grains. The authors assert that the gene couldbe involved with regulating grain growth, which is to say they suppose thismight be a direct influence rather than the more indirect consequences ongrain size that glume cell number has in the previous two loci. These earlyglimpses into grain size regulation confirm the expectations that grain size isinfluenced by many factors that may only be indirectly concerned with grainsize itself, and part of as yet uncharacterized networks of interaction.

In the case of barley, which has QTLs affecting grain mass across all sevenchromosomes, the largest effect is linked to the Vrs-1 locus, which determinesthe row architecture (Marquez-Cedillo et al., 2001; Komatsuda et al., 2007).In this case, the genetic control of grain size is quite indirect. The grainsof two-row barley are fatter than those of six-row, most likely because theyhave more space in which to develop. Similarly, wheat and maize have QTLsassociated with increasing grain mass on all chromosomes (Gupta et al., 2006),and pleiotropic effects of loci being involved with both grain weight andplant height are evident from recent studies (Maccaferri et al., 2008; Roderet al., 2008). Undoubtedly, many of these will be tracked down to genes in thecoming years. Gupta et al. (2006) cite only one gene in wheat, three in barleyand two in maize to be involved with grain size. As with the elucidationof rice outlined above, these are both directly and indirectly involved withgrain development. Examples of directly involved genes include the crinkly4(Becraft et al., 1996) and mn1 (Carlson et al., 2000) in maize. The pseudo-response regulator ppd1 in both wheat and barley is also associated withgrain size, but is likely to be an indirect effect through day-length sensitivityaltering the developmental time of grain maturation. The number of locigoverning seed size appears to be equally large in legumes as with cerealswith as many as ten QTLs governing the trait in peas (Blair et al., 2006), andbetween three and nine QTLs in azuki bean (Kaga et al., 2008). Only four


such QTLs were identified in chickpea (Cho et al., 2002), but very small-seededness has been shown to result from interaction of two recessive genes(Upadhyaya et al., 2006). Again, very little is currently known about whichgenes are responsible.

7.12 Seasonality controls: photoperiodicity andvernalization

Another set of key changes with domestication are the controls over the sea-sonality of crop harvests and planting: photoperiodicity and vernalization.In many plant species, the seasonality of flowering and hence of seed set iscontrolled by environmental cues such as day length, thus species can bedivided into long-day and short-day plants. As discussed by Willcox (1992),there tends to be an important difference between the crops domesticated inthe Near East and those of the Old World tropics, such as those of India orthe African savannas. The tropical crops tend to be grown in summer andadapted to monsoon rainfall, flowering as days shorten after summer. Bycontrast, those of the Near East were originally tied to winter rains. The im-portance of seasonality of cultivation and the changes in seasonality betweendifferent regions has been a focus of much discussion in archaeological cir-cles, since differences in seasonal potential of different regions might serveto create environmental frontiers that limited the spread of certain cropsinto certain regions (e.g. Sherratt, 1980; Halstead, 1989; Bogaard, 2004, pp.160–164; Kreuz et al., 2005; Fuller, 2007b, p. 405; Conolly et al., 2008). Onmorphological grounds, there is no basis for distinguishing the seasonalityof archaeological crop remains, although archaeobotanists have made someprogress in inferring seasonality from associated non-crop weed remains.Nevertheless, there remain debates, for example as to whether or not theearliest agriculture in central Europe was autumn sown, and grown over thewinter, or spring sown and grown in the summer (e.g. Jacomet and Behre,1991, p. 86; Bogaard, 2004, pp. 160–164; Kreuz et al., 2005). As crops spreadnorthward into new latitudinal bands, with longer and colder winters, cul-tivation may have become increasingly difficult over the traditional winterseason. Wetter and cooler summers may also have precluded certain species,as appears to be the case with lentils and chickpeas (Conolly et al., 2008). Asa result, crops either had to evolve adaptations to surviving cold winters,such as through vernalization in which autumn sown crops have a pausein growth during the frost months and then resume growth in the warmingof spring; or else their original seasonality of flowering had to be switchedoff, allowing them to be planted in spring and grown through the summer,thus flowering during shortening days rather than long days. Recent yearshave seen substantial developments in understanding the genetic basis ofvernalization and photoperiod sensitivity in cereals.


Figure 7.15 Diagrammatic representations comparing the regulatory gene networksinvolved in vernalization and photoperiodicity, as inferred for wheat/barley, rice andArabidopsis. For sources, see text.

The emergent picture of the genetics of seasonality in various plant groupsgives a fascinating insight into regulatory network evolution. This exampleshows how fluidly regulatory networks change over time often retaining corecomponents, but not necessarily with the same functionality. The scientificcommunity has been of the opinion for some time that the vernalizationresponse evolved in parallel in grasses and in eudicots as exemplified by Ara-bidopsis thaliana. This opinion is borne out by phylogenetics which supportsthe idea that the ancestral grass type was more like the panicoid group whichis adapted to tropical conditions being short-day plants with no vernalizationresponse (Kellogg, 1998). However, recent identification of the major compo-nents of the vernalization response in grasses shows that much of the samemolecular apparatus is utilized between the groups (Fig. 7.15).

In wheat and barley, three principal components to the vernalization sys-tem have been discovered, named VRN1, VRN2 and VRN3 (Yan et al., 2003,2004a, 2004b, 2006). In an unfortunate clash of nomenclature, it should benoted that these are not directly comparable components to the similarlynamed VRN1 and VRN2 in A. thaliana. While the latter two work in synergyat a different point in the vernalization pathway, VRN1 and VRN2 in cere-als work antagonistically. All these genes have been named so because oftheir direct effects on phenotype through which they were originally discov-ered. As with many of the relationships shown in the network diagrams of


Fig. 7.15, the interactions have been correlatively determined between genesin the cereals; consequently, they may be either direct or indirect throughother as yet undetermined factors. That some of these interactions at leastare likely to be indirect, or an incomplete description of the regulation due toother factors, is evident from some inconsistencies in the network relative toobservations that will be pointed out below.

In barley and wheat, VRN2 represses VRN3 and VRN1. VRN3 acts to pro-mote VRN1, which in turn promotes flowering and further down-regulatesVRN2 that would otherwise resume action in the absence of short days orcold temperatures. Short days or cold temperatures inhibit the action of VRN2(Dubcovsky et al., 2006). It is not likely that VRN2 is involved directly in sens-ing such environmental cues. The inhibition of VRN2 is not in itself enough tocause up-regulation of VRN3 and subsequently VRN1. After VRN2 inhibition,VRN3 up-regulation is induced by long days, through the action of a fourthimportant intermediary Ppd1. Through this set of interactions, temperate ce-reals have evolved a system in which they must experience either short daysor cold followed by longer days before flowering so ensuring that floweringis delayed through the winter and initiated in the spring. This winter habitis the ancestral condition, and suited to the climate of biogeographical rangeof the wild progenitors. The spring habit has evolved several times and inseveral ways from this regulatory network involving degenerative mutationsat each of the three main loci.

The action of VRN2 is to repress VRN1 and VRN3 through the action of aCCT domain in VRN2, a domain type found in the CO-like group of genesin A. thaliana. A mutation causing a R/W amino acid change at a conservedposition in this domain results in a lack of repression (Robson et al., 2001;Cockram et al., 2007a) causing a phenotype in which flowering is triggeredby long days without the need for vernalization. This mutation makes arecessive allele (vrn2) because in the heterozygous condition the functioningallele will still achieve repression. A similar phenotype is also caused bynaturally occurring deletions at the VRN2 locus (Dubcovsky et al., 2005).

A spring phenotype is also caused by mutations at the VRN1 locus (Yanet al., 2004b; Fu et al., 2005). There appear to be two sites at the VRN1 locusthat are involved with repression of the gene by acting as receptors to theVRN2-mediated repressors. One is in the promoter region, and the secondwithin the first intron. Deletions at either of these sites result in a lack ofrepression of VRN1 by VRN2. This time the mutant allele is dominant (Vrn1),because in the heterozygous condition, even though the wild-type responsiveallele is repressed successfully by VRN2, the receptor region deleted allelewill still initiate flowering. The resulting phenotype is similar to that ob-tained with the vrn2 allele in that vernalization is not required for long daysto initiate flowering. Interestingly, a range of large deletions have occurredin intron 1 both in barley and wheat, which indicate that both cereals haveachieved the spring phenotype independently, but through the same under-lying mechanism (Fu et al., 2005). There are now known to be a large range of


combinations of VRN1 and VRN2 alleles possible, with 17 haplotypes occur-ring in the European barley germplasm of which only one winter and twospring types dominate 79% of varieties (Cockram et al., 2007b).

The VRN3 locus also has a regulatory element in its promoter throughwhich VRN2 represses its action. In this case, a dominant mutant allele Vrn3occurs in wheat that has a retrotransposon in the promoter rendering itinsensitive to VRN2 repression, again resulting in a similar phenotype tothe mutants described above (Yan et al., 2006). Although VRN3 completes thenetwork of interaction, as described in Fig. 7.15, it is not likely to be the com-plete story. The current understanding shown in the diagram implies that theclear association between Vrn1 and spring phenotypes could not have beendiscovered unless the Vrn3 genotype was also in place. Indeed, germplasmsurveys have already indicated that wherever Vrn3 occurs Vrn1 is also found.However, Yan et al. (2006) argue that a mutation in the regulatory region ofeither gene is enough to initiate the flowering cascade.

A fourth important locus in the seasonality of temperate cereals is Ppd1,which builds on the spring phenotype produced by mutations at the ver-nalization loci. Ppd1 is responsible for initiating signal cascades in responseto long days (Turner et al., 2005). There are differing Ppd1 mutants in bar-ley and wheat, respectively. In barley, a SNP causes the ppd-H1 (recessive)mutant, which is insensitive to long days resulting in delayed flowering. Inmost of the wild biogeographical range, this phenotype is selected against,since the growing season is short followed by a hot dry summer that thelate flowering plants would find difficult to survive in. However, furthernorth, the potential growing season is much longer with wetter summers.Spring varieties grown in northern temperate latitudes benefit from the ppd-H1 mutant that has a longer vegetative phase resulting in more resourcesequestration and so in larger grain yields. This mutation appears to havearisen within the domesticated barley gene pool east of the Fertile Cres-cent as crops moved in to more northern latitudes (Jones et al., 2008). Theknown Ppd1 mutants in wheat result in a different phenotype to that of bar-ley, probably due to different underlying mutations which appear to involvelarge promoter region deletions (Beales et al., 2007). In the case of wheat, thePpd1 mutants are dominant resulting in floral initiation regardless of daylength. These early flowering types appear to do well under conditions insouthern Europe, but less well in more northerly latitudes (Worland et al.,1998).

The regulatory networks for vernalization between the temperate cerealsand Arabidopsis thaliana are remarkably similar. Orthologous components areutilized in each – VRN3 in wheat and barley is orthologous to FT, and VRN1is orthologous to AP1. Wheat and barley also have versions of the GI andCO genes which are established to act upstream of FT in A. thaliana, and arelikely to prove the same in cereals. However, there is no identifiable geneorthologous to FLC in cereals, nor is there anything like the cereal VRN2 inA. thaliana. However, these two genes act in a highly similar way in termsof the network of relationships. It seems that a similar network solution has


been converged upon in temperate cereals and the eudicot lineage repre-sented by A. thaliana. In the cereals, VRN2 appears to have evolved at leastin part from a CO-like ancestor, whereas in eudicots, FLC originated fromanother MADS-box gene (Zhao et al., 2006). However, there may be more todiscover in the cereals. A. thaliana has a second ‘FLC independent’ vernaliza-tion pathway in which VIN3 is up-regulated during cold spells and activatesAGL24 which initiates the flowering cascade (Michaels et al., 2003). VIN3 alsohas the function of repressing FLC. Curiously, a well-conserved version ofthe VIN3 gene has also been shown to be up-regulated by vernalization inwheat (Fu et al., 2007). There is also a group of genes orthologous to AGL24in wheat (Zhao et al., 2006).

Rice and the panicoid grasses such as maize do not have vernalizationadaptations. These grasses are naturally adapted to the tropics to flowerunder short days. Very little is known yet about maize, although mutationsassociated with early flowering have been identified (Chardon et al., 2005). Itis likely that the regulation of flowering time in this group of grasses is wellrepresented by rice about which a great deal has emerged in recent years.

The emergent picture of regulatory interactions that govern rice floweringshows striking similarities and differences to the cereal network. Under con-ditions of long days, both Hd1, orthologous to CO, and Ghd7 repress Hd3a,which is orthologous to FT (Yano et al., 2000; Kojima et al., 2002; Hayama et al.,2003; Xue et al., 2008). The function of Hd1 is surprising in this instance, be-cause it acts in the opposite way to its orthologous counterpart in Arabidopsis.However, it appears that Hd6, which is also known to have a repressive effecton flowering time under long days, may be acting in conjunction with theHd1 complex to repress Hd3a (Yamamoto et al., 2000; Takahashi et al., 2001;Ogiso et al., 2007). Ghd7, most closely related to VRN2 in cereals (Xue et al.,2008), also represses Ehd1 that would otherwise initiate flowering (Doi et al.,2004), resulting in a regulation reminiscent of VRN2 and FLC. Interestingly,Ghd7 also appears to have pleiotropic effects on plant size and grain number,leading to increased growth, cell proliferation and differentiation.

As days become shorter, during the monsoon season, the actions of bothHd1 and Ghd7 change. Ghd7 promotes Ehd1 (Xue et al., 2008) and Hd1 promotesHd3a (Yano et al., 2000). Possibly, this apparent return of Hd1 to a functionmore normally associated with a CO orthologue may represent a releaseof action by Hd6. Once Hd3a has been promoted, the flowering cascade isinitiated.

Photoperiod sensitive rice (and maize) crops are restricted to tropical areas,because the growing season further north is too short. Photoperiod insensitivevarieties of rice that can be grown in more temperate conditions furthernorth are associated with less or non-functioning alleles, and the earliest ricevarieties actually have Ghd7 deleted, resulting in a strong latitudinal clineof Ghd7 alleles (Xue et al., 2008). Consequently, not only is the resemblancebetween the wheat/barley and rice regulation striking, the point at whichmutations causing loss of functionality to induce seasonal insensitivity alsocoincide in VRN2 and Ghd7.


7.13 Discussion: evolution and development ofdomesticated seed traits

The domestication of crop plants represents numerous trajectories of parallelevolution, with some instances of true convergence as plants adapted to theselective pressures brought to bear by human farmers. The major selectivepressures were associated with the dispersal and establishment of the nextgeneration of seeds, from dispersal mechanism (the shift to human harvest-ing), seed germination (shifts away from dormancy and changes in seasonalcontrols on germination), and seedling establishment. In most cases, theseselective pressures were initially unconscious on the part of people, as recog-nized by Darwin and his successors (e.g. Darwin, 1883, Chapter 20; Zohary,1969; Darlington, 1973, p. 155; Harlan, 1992). Since human food production asa behaviour follows similar patterns for similar aims, the selection pressureswith domestication have often been similar. There has been some debate,and perhaps, confusion over whether to regard the similar domesticationoutcomes as products of convergence or parallelism. As clarified by the defi-nitions of Niklas (1997, pp. 303–305) and Gould (2002, pp. 81–82, 1076–1089),convergence is a case of analogy when unrelated organisms produce simi-lar morphological ends (adaptations) in different ways. By contrast, parallelevolution is when related organisms evolve similar adaptations from thesame ancestral mechanism or underlying developmental/genetic architec-ture: this represents selection working on existing developmental constraintsthat are shared across species. Parallelism like phylogenetic/historical ho-mology is a form of syngeny (generative homology) (as defined in Butlerand Saidel, 2000). Seen in these terms, there are clear cases of both paral-lelism and convergence in domestication: orthologous loci, such as some lociregulating flowering show parallel evolution (e.g. Vrn3 in Hordeae, Hd3a inrice, FT in Arabidopsis; see Fig. 7.15); by contrast, the loci involved in cerealshattering differ between wheat/barley and rice such that they have evolvedalong multiple non-orthologous genetic paths, and thus represent allogenyor generative homoplasy (as defined in Butler and Saidel, 2000). Such non-orthologous means of achieving similar adaptations are convergent in thesense used here (but note that Paterson et al., 1995 argued for ‘convergence’in the sense of parallelism as used here; a hypothesis now falsified by furtherwork: Li and Gill, 2006; and see above).

A key area of evolution under domestication involved changes in seeddispersal, taken broadly to include the timing of fruiting, the mode of dis-persal, and patterns of germination. In recent years, much scientific progresshas been made in understanding these evolutionary processes through theefforts of archaeobotany and through genetics. Archaeological plant remains(archaeobotany) can provide hard fossil evidence for the rate and extent ofevolution in those morphological traits which are prone to archaeologicalpreservation, especially in charred seeds or cereal chaff (rachises and spikeletbases). Genetics, starting from QTLs and moving onto sequencing studies,


allows the identification of the coding gene regions and the developmentalpathways involved in these domestication traits, how many different waysand times these have evolved and potentially provides a framework for infer-ring aspects of the geographical history of these traits. We expect that soon as-sociation mapping studies will provide important new insights about linkedsyndromes of genetic adaptation, as suggested by recent work in Arabidopsis(Aranzana et al., 2005), and the extent to which genetic linkage evolved dur-ing the domestication process (cf. D’Ennequin et al., 1999) or was part ofpre-existing wild variation. In both archaeology and genetics, there is muchfurther research to do. At present, there are still relatively few species whichhave been studied, and there are limited cases of potential comparisons fromwhich recurrent patterns of the evolution of domesticated seed dispersal canbe studied.

Nevertheless, there are a few aspects that can be highlighted. The fact thatavailable data point to rather slow processes of evolution towards fixation intraits such as non-shattering in cereals and grain size increase, taking placeon the order of 1000 generations or more, was unexpected by earlier the-orists. For example Harlan (1992, p. 124) concludes that ‘cultivated plantshave the capacity to evolve rapidly,’ and experimental inferences of Hillmanand Davies (1990, 1999) suggested that 20–100 generations of self-pollinatingcereals should be sufficient. As reviewed above, archaeobotanical data nowsuggest a much slower process (also Fuller, 2007a; Allaby, 2008; Allaby et al.,2008), perhaps more akin to cases of natural selection, as seed dispersal andseedling traits became adapted to human ecology. As with many cases ofnatural selection, genetic changes involved with domestication have oper-ated through changes in the regulation of seed and fruit development, withseveral known domestication genes representing mutations to regulatorytranscription factors (cf. Doebly et al., 2006; Burger et al., 2008).

It may be possible to consider these changes in an ontogenetic frameworkof heterochrony. As discussed by Niklas (1994, pp. 262–274; also Nikalas1997,pp. 101–104), there are different ways in which the timing of developmentmay change in heterochronic evolution. One that is often discussed is pae-domorphosis, in which the ancestral juvenile form shows more resemblanceto the derived mature form. A subcategory of this is neoteny, in which somevegetative traits are arrested and some ancestral juvenile character states areretained longer in relation to overall organismal development. The loss ofshattering appears to represent an example of this as formation of wild-typeadult abscission layers is arrested, that is sexual maturation is delayed. Otherdomestication traits may be regarded as peramorphosis or pre-displacementin which development is accelerated in vegetative traits and completed beforeall of the ancestral adult reproductive traits have formed: this may be appliedto germination, loss of photoperiodicity functions, or the loss of appendages.Finally, acceleration may be applied to the expanded and exaggerated traitsof domesticates, such as increases in grain size or the expanded appendagesassociated with a few fibre crops (cotton, devil’s claw), in which vegetative


growth is simply increased prior to reproductive maturity. Indeed, the pro-longed development programme of cotton testa cells involved in fibre pro-duction has been molecularly characterized (Hovav et al., 2008). Because thedomesticate often differs in shape and proportion (e.g. domesticated cerealsare wider and thicker but may not be longer), and not merely size, this is anot a simple case of gigas (gigantism), when size is increased along a fixedallometric relationship (cf. Niklas, 1994). In some cases of domesticated sizeincrease, such as in cucurbit fruits, simple gigantism may apply (see Sinnott,1936, 1939). Further research documenting when during seed developmentcertain traits, which have been modified by domestication, are expressed mayprovide further insights into the evolution of the domestication syndrome.What remains unclear is why the rates and ordering of domesticated traitshave varied across some taxa and differences between families (cf. Fuller,2007a), and an ontogenetic perspective on these traits may offer a frameworkfor understanding the nature of these parallel or convergent evolutions.

As Ames (1939) recognized the angiosperm seed has been central to humaneconomic evolution, but it is the changes to seed dispersal and establishmentthat made this possible, giving human populations sources of growing sur-pluses, and particular species in domesticated form evolved unprecedentedfitness across a range of environments. The further investigation of the evolu-tion of seed crop domestication has much to contribute to our understandingof the processes of parallel and convergent evolution and the intertwinedhistory of a limited range of plant species and Homo sapiens.

References

Abbo, S., Ladizinsky, G. and Weeden, N.F. (1991) Genetic analysis and linkage studyof seed weight in lentil. Euphytica 58, 259–266.

Abbo, S., Zezak, I., Schwartz, E., Lev-Yadun, S. and Gopher, A. (2007) Experimentalharvesting of wild pea in Israel: implications for the origins of Near Eastern farming.Journal of Archaeological Science 35, 922–929.

Allaby, R. (2008) The rise of plant domestication: life in the slow lane. Biologist 55(2),94–99.

Allaby, R.G., Fuller, D.Q. and Brown, T.A. (2008) The genetic expectations of a pro-tracted model for the origins of domesticated crops. Proceedings of the NationalAcademy of Sciences USA 105(37), 13982–13986.

Allen, H. (1974) The Bagundji of the Darling Basin: cereal gatherers in an uncertainenvironment. World Archaeology 5, 309–322.

Amblard, S. and Pernes, J. (1989) The identification of cultivated pearl millet (Pen-nisetum) amongst plant impressions on pottery from Oued Chebbi (Dhar Oualata,Mauritania). African Archaeological Review 7, 117–126.

Ames, O. (1939) Economic Annuals and Human Cultures. Botanical Museum of HarvardUniversity, Cambridge, MA.

Aranzana, M.J., Kim, S., Zhao, K., Bakker, E., Horton, M., Jakob, K., Lister, C., Molitor,J., Shindo, C., Tang, C., Toomajian, C., Traw, B., Zheng, H., Bergelson, J., Dean,C., Marjoram, P. and Nordborg, M. (2005) Genome-wide association mapping in


arabidopsis identifies previously known flowering time and pathogen resistancegenes. PLoS Genetics 1, 531–539.

Asch, D.L. and Asch, N.B. (1985) Prehistoric plant cultivation in west-central Illinois.In: Prehistoric Food Production in North America (ed. R.I. Ford). AnthropologicalPapers No. 75. Museum of Anthropology, University of Michigan, Ann Arbor, pp149–203.

Azhaguvel, P. and Komatsuda, T. (2007) A phylogenetic analysis based on nucleotidesequence of a marker linked to the brittle rachis locus indicates a diphyletic originof barley. Annals of Botany 100, 1009–1015.

Bailey, P.C., McKibbin, R.S., Lenton, J.R., Holdsworth, M.J., Flintham, J.E. and Gale,M.D. (1999) Genetic map locations for orthologous Vp1 genes in wheat and rice.Theoretical and Applied Genetics 98, 281–284.

Balter, M. (2007) Seeking agriculture’s ancient roots. Science 316, 1830–1835.Bar-Yosef, O. (1998) The Natufian culture in the Levant. Evolutionary Anthropology 6,

159–177.Baskin, C. and Baskin, J.M. (2001) Seeds: Ecology, Biogeography and Evolution of Dormancy

and Germination. Academic Press, San Diego.Beales, J., Turner, A., Griffiths, S., Snape, J.W. and Laurie, D.A. (2007) A PSEUDO-

RESPONSE REGULATOR is misexpressed in the photoperiod insensitive Ppd-D1amutant of wheat (Triticum aestivum L.). Theoretical and Applied Genetics 115, 721–733.

Becraft, P.W., Stinard, P.S. and McCarty, D.R. (1996) CRINKLY 4: a TNFR-like receptorkinase involved in maize epidermal differentiation. Science 273, 1406–1409.

Benz, B.F. (2001) Archaeological evidence of teosinte domestication from GuilaNaquitz, Oaxaca. Proceedings of the National Academy of Sciences USA 98, 2104–2106.

Blair, M.W., Iriarte, G. and Beebe, S. (2006) QTL analysis of yield traits in an advancedbackcross population derived from a cultivated Andean X wild common bean(Phaseolus vulgaris L.) cross. Theoretical and Applied Genetics 112, 1149–1163.

Blumler, M.A. (1991) Modelling the origins of legume domestication and cultivation.Economic Botany 45, 243–250.

Bogaard, A. (2004) Neolithic Farming in Central Europe: An Archaeobotanical Study ofCrop Husbandry Practices C5500–2200 BC. Routledge, London.

Bohrer, V.L. (1984) Domesticated and wild crops in the CAEP study area. In: PrehistoricCultural Development in Central Arizona: Archaeology of the Upper New River Region(eds P. Spoerl and G. Gemerman). Occasional Paper No. 5, Center for ArchaeologicalInvestigations, Southern Illinois University, Carbondale, pp 183–259.

Braadbaart, F., Boon, J.J., Veld, H., David, P. and van Bergen, P.F. (2004) Studies onthe heat treatment of peas: changes of their physical and bulk chemical properties.Journal of Archaeological Science 31, 821–833.

Bretting, P.K. (1982) Morphological differentiation of proboscidea parviflora ssp. parvi-flora (Martyniaceae) under domestication. American Journal of Botany 69, 1531–1537.

Bretting, P.K. (1986) Changes in fruit shape in proboscidea parviflora ssp. parviflora(Martyniaceae) with domestication. Economic Botany 40(2), 170–176.

Brunken, J., De Wet, J.M.J. and Harlan, J.R. (1977) The morphology and domesticationof pearl millet. Economic Botany 31, 163–174.

Bruno, M.C. (2006) A morphological approach to documenting the domesticationof chenopodium in the Andes. In: Documenting Domestication. New Genetic andArchaeological Paradigms (eds M.A. Zeder, D.G. Bradley, E. Emshwiller and B.D.Smith). Universty of California Press, Berkeley, pp 32–45.


Bruno, M. and Whitehead, W.T. (2003) Chenopodium cultivation and formative periodagriculture at Ciripa, Bolivia. Latin American Antiquity 14, 339–355.

Burger, J.C., Chapman, M.J. and Burke, J.M. (2008) Molecular insights into the evolu-tion of crop plants. American Journal of Botany 95, 113–122.

Butler, A.B. and Saidel, W.M. (2000) Defining sameness: historical, biological, andgenerative homology. BioEssays 22(9), 846–853.

Butler, E.A. (1989) Cryptic anatomical characters as evidence of early cultivation inthe grain legumes (pulses). In: Foraging and Farming (eds D.R. Harris and G.C.Hillman). Unwin and Hyman, London, pp 390–407.

Butler, E.A. (1990) Legumes in Antiquity: A Micromorphological Investigation of Seedsof the Viceae. Unpublished Ph.D. Dissertation. Institute of Archaeology, UniversityCollege, London.

Cao, X., Costa, L.M., Biderre-Petit, C., Kbhaya, B., Dey, N., Perez, P., McCarty, D.R.,Gutierrez-Marcos, J.F. and Becraft, P.W. (2007) Abscisic acid and stress signals in-duce Viviparous1 expression in seed and vegetative tissues of maize. Plant Physiol-ogy 143, 720–731.

Carlson, S.J., Shanker, S. and Chourey, P.S. (2000) A point mutation at the Miniature1seed locus reduces levels of the encoded protein but not its mRNA in maize.Molecular and General Genetics 263, 367–373.

Carrari, F., Benech-Arnold, R., Osuna-Fernandez, R., Hopp, E., Sanchez, R., Iusem, N.and Lijavetzky, D. (2003) Genetic mapping of the Sorghum bicolor vp1 gene andits relationship with preharvest sprouting resistance. Genome 46, 253–258.

Chardon, F., Hourcade, D., Combes, V. and Charcosset, A. (2005) Mapping of a spon-taneous mutation for early flowering time in maize highlights contrasting allelicseries at two-linked QTL on chromosome 8. Theoretical and Applied Genetics 112,1–11.

Cheng, C., Motohashi, R., Tchuchimoto, S., Fukuta, Y., Ohtsubo, H. and Ohtsubo, E.(2003) Polyphyletic origin of cultivated rice: based on the interspersion patterns ofSINEs. Molecular Biology and Evolution 20, 67–75.

Cho, S., Kumar, J., Anupama, K., Tefera, F. and Muehlbauer, F.J. (2002) Mappinggenes for double podding and other morphological traits in chickpea. Euphytica128, 285–292.

Cockram, J., Chiapparino, E., Tayor, S.A., Stamati, K., Donini, P., Laurie, D.A. andO’Sullivan, D. (2007b) Haplotype analysis of vernalization loci in European barleygermplasm reveals novel VNR-H1 alleles and a predominant winter VRN-H1/VRN-H2 multilocus haplotype. Theoretical and Applied Genetics 115, 93–1001.

Cockram, J., Jones, H., Leigh, F.J., O’Sullivan, D., Powell, W., Laurie, D. and Green-land, A.J. (2007a) Control of flowering time in temperate cereals: genes, domes-tication, and sustainable productivity. Journal of Experimental Botany 58, 1231–1244.

Colledge, S. (1998) Identifying pre-domestication cultivation using multivariate anal-ysis. In: The Origins of Agriculture and Crop Domestication (eds A.B. Damania, J.Valkoun, G. Willcox and C.O. Qualset). ICARDA, Aleppo, pp 121–131.

Colledge, S. (2001) Plant Exploitation on Epipalaeolithic and Early Neolithic Sites in theLevant. British Archaeological Reports, Oxford.

Colledge, S. (2004) Reappraisal of the archaeobotanical evidence for the emergenceand dispersal of the ‘founder crops’. In: Neolithic Revolution. New Perspectives onSouthwest Asia in Light of Recent Discoveries on Cyprus (eds E. Peltenberg and A.Wasse). Oxbow Books, Oxford, pp 49–60.


Colledge, S., Conolly, J. and Shennan, S. (2004) Archaeobotanical evidence for thespread of farming in the eastern Mediterranean. Current Anthropology 45, S35–S58.

Colledge, S., Conolly, J. and Shennan, S. (2005) The evolution of Neolithic farmingfrom SW Asian origins to NW European limits. European Journal of Archaeology 8,137–156.

Conolly, J., Colledge, S. and Shennan, S. (2008) Founder effect, drift, and adaptivechange in domestic crop use in early Neolithic Europe. Journal of ArchaeologicalScience 35, 2797–2804.

Costantini, L. (1983) The beginning of agriculture in the Kachi Plain: the evidence ofMehrgarh. In: South Asian Archaeology 1981 (ed. B. Allchin). Cambridge UniversityPress, Cambridge, pp 29–33.

Crawford, G.W. and Shen, C. (1998) The origins of rice agriculture: recent progress inEast Asia. Antiquity 72, 858–866.

D’Andrea, A.C., Kahlheber, S. Logan, A.L. and Watson, D.J. (2007) Early domesticatedcowpea (Vigna unguiculata) from Central Ghana. Antiquity 81, 686–698.

D’Andrea, A.C., Klee, M. and Casey, J. (2001) Archaeobotanical evidence for pearlmillet (Pennisetum glaucum) in sub-Saharan West Africa. Antiquity 75, 341–348.

Darlington, C.D. (1973) Chromosome Botany and the Origins of Cultivated Plants, 3rd edn.George Allen & Unwin, London.

Darwin, C. (1883) The Variation of Animals and Plants Under Domestication, 2nd edn. D.Appleton & Co., New York.

Day, J.S. (2000) Development and maturation of sesame seeds and capsules. FieldCrops Research 67, 1–9.

De Candolle, A. (1885) Origin of Cultivated Plants. D. Appleton & Co., New York.D’Ennequin, M. Le Thierry, Toupance, B., Robert, T., Godelle, B. and Gouton, P.H.

(1999) Plant domestication: a model for studying the selection of linkage. Journal ofEvolutionary Biology 12, 1138–1147.

Dickau, R., Ranere, A.J. and Cooke, R.G. (2007) Starch grain evidence for the prece-ramic dispersals of maize and root crops into tropical dry and humid forests ofPanama. Proceedings of the National Academy of Sciences USA 104, 3651–3656.

Doebly, J.F., Gaut, B.S. and Smith, B. D (2006) The molecular genetics of crop domes-tication. Cell 127, 1309–1321.

Doi, K., Izawa, T., Fuse, F., Yamanouchi, U., Kubo, T., Shimatini, Z., Yano, M. andYoshimura, A. (2004) Ehd1, a B-type response regulator in rice, confers short-daypromotion of flowering and controls FT-like gene expression independently of Hd1.Genes and Development 18, 926–936.

Dubcovsky, J., Chen, C. and Yan, L. (2005) Molecular characterization of the al-leleic variation at the VRN-H2 vernalization locus in barley. Molecular Breeding15, 395–407.

Dubcovsky, J., Loukoianov, A., Fu, D., Valarik, M., Sanchez, A. and Yan, L. (2006)Effect of photoperiod on the regulation of wheat vernalization genes VRN1 andVRN2. Plant Molecular Biology 60, 469–480.

Dunne, M.T. and Green, W. (1998) Terminal archaic and early woodland plant use atthe gast spring site (13LA152), southeast Iowa. Midcontinental Journal of Archaeology23(1), 45–48.

Elbaum, R., Zaltzman, L., Burgert, I. and Fratzl, P. (2007) The role of wheat awns inthe seed dispersal unit. Science 316(5826), 884–886.

Fan, C., Xing, Y., Mao, H., Lu, T., Han, B., Xu, C., Li, X. and Zhang, Q. (2005) GS3,a major QTL for grain length and weight and minor QTL for grain width and


thickness in rice, encodes a putative transmembrane protein. Theoretical and AppliedGenetics 112, 1164–1171.

Fennimore, S.A. and Foley, M.E. (1998) Genetic and physiological evidence for therole of giberrelic acid in the germination of Avena fatua seeds. Journal of ExperimentalBotany 49, 89–94.

Finch-Savage, W. and Leubner-Metzger, G. (2006) Seed dormancy and the control ofgermination. New Phytologist 171, 501–523.

Finucane, B., Manning, K. and Toure, M. (2008) Late Stone Age subsistence in theTilemsi Valley, Mali: stable isotope analysis of human and animal remains fromthe site of Karkarichinkat Nord (KN05) and Karkarichinkat Sud (KS05). Journal ofAnthropological Archaeology 27, 82–92.

Flintham, J.E. and Humphry, S.J. (1993) Red coat genes and wheat dormancy. AspectsApplied Biology 36, 135–141.

Fritz, G.J. (1994) Are the first American farmers getting younger? Current Anthropology35, 305–309.

Fryxell, P.A. (1979) The Natural History of the Cotton Tribe. Texas A & M UniversityPress, London.

Fu, D., Dunbar, M. and Dubcovsky, J. (2007) Wheat VIN3-like PHD finger genesare upregulated by vernalization. Molecular Genetics and Genomics 277, 301–313.

Fu, D., Szucs, P., Yan, L., Helguera, M., Skinner, J.S., Zitzewitz, J., Hayes, P.M. andDubcovsky, J. (2005) Large deletions within the first intron in VRN-1 are associatedwith spring growth habit in barley and wheat. Molecular Genetics and Genomics 273,54–65.

Fuller, D.Q. (2003) Further evidence on the prehistory of sesame. Asian Agri-History7(2), 127–137.

Fuller, D.Q. (2006) Agricultural origins and frontiers in South Asia: a working syn-thesis. Journal of World Prehistory 20, 1–86.

Fuller, D.Q. (2007a) Contrasting patterns in crop domestication and domesticationrates: recent archaeobotanical insights from the Old World. Annals of Botany 100(5),903–924.

Fuller, D.Q (2007b) Non-human genetics, agricultural origins and historical lin-guistics in South Asia. In: The Evolution and History of Human Populations inSouth Asia (eds M. Petraglia and B. Allchin). Springer, Netherlands, pp 393–443.

Fuller, D.Q. and Harvey, E.L. (2006) The archaeobotany of Indian Pulses: identifi-cation, processing and evidence for cultivation. Environmental Archaeology 11(2),219–246.

Fuller, D.Q., Harvey, E.L. and Qin, L. (2007a) Presumed domestication? Evidence forwild rice cultivation and domestication in the fifth millennium BC of the lowerYangtze region. Antiquity 81, 316–331.

Fuller, D.Q., Macdonald, K. and Vernet, R. (2007b) Early domesticated pearl milletin Dhar Nema (Mauritania): evidence of crop-processing waste as ceramic tem-per. In: Fields of Change. Progress in African Archaeobotany (ed. R.T.J. Cappers),Grongingen Archaeological Studies 5. Barkhuis Publishing, Groningen, pp 71–76.

Fuller, D.Q. and Qin, L. (2008) Immature rice and its archaeobotanical recognition: areply to Pan. Antiquity 82(316). On-line project gallery. Available from http: //an-tiquity.ac.uk/ProjGall/fuller2/index.html.


Fuller, D.Q., Qin, L. and Harvey, E.L. (2008) Rice archaeobotany revisited: commentson Liu et al. (2007). Antiquity 82(315). On-line project gallery. Available from http://antiquity.ac.uk/ProjGall/fuller1/index.html.

Fuller, D.Q., Qin, L., Zheng, Y., Zhao, Z., Chen, X., Hosoya, L.A. and Sun, G.P. (2009)The domestication process and domestication rate in rice: spikelet bases from theLower Yangtze. Science 323, 1607–1610.

Gao, F.Y., Ren, G.J., Lu, X.J., Sun, S.X., Li, H.J., Gao, Y.M., Luo, H., Yan, W.G. and Zhang,Y.Z. (2008) QTL analysis for resistance to preharvest sprouting in rice (Oryza sativa).Plant Breeding 127, 268–273.

Godbole, S.V. (1925) Pennisetum typhoideum. Studies on the Bajri Crop. I. The mor-phology of Pennisetum typhoideum. Memoirs of the Department of Agriculture in India(Agricultural Research Institute, Pusa) 14(8), 247–268.

Gould, S.J. (2002) The Structure of Evolutionary Theory. Harvard University Press,Cambridge, MA.

Gremillion, K.J. (1993) Crop and weed in prehistoric eastern North America: theChenopodium Example. American Antiquity 58, 496–509.

Gupta, P., Rustgi, S. and Kumar, N. (2006) Genetic and molecular basis of grain sizeand grain number and its relevance to grain productivity in higher plants. Genome49, 565.2–571.2.

Haaland, R. (1999) The puzzle of the late emergence of domesticated sorghum in theNile Valley. In: The Prehistory of Food. Appetites for Change (eds C. Gosden and J.Hather). Routledge, London, pp 397–418.

Halstead, P. (1989) Like a rising damp? An ecological approach to the spread offarming in south-east and central Europe. In: The Beginnings of Agriculture (eds A.Milles, D. Williams and N. Gardner). British Archaeological Resports, Oxford, pp23–53.

Harlan, J.R. (1989) Wild grass-seed harvesting in the Sahara and sub-Sahara of Africa.In: Foraging and Farming: The Exploitation of Plant Resources (eds D.R. Harris andG.C. Hillman). Unwin and Hyman, London, pp 79–98.

Harlan, J.R. (1992) Crops and Ancient Man, 2nd edn. American Society for Agronomy,Madison.

Harlan, J.R., De Wet, J.M.J. and Price, E.G. (1973) Comparative evolution of cereals.Evolution 27, 311–325.

Harris, D.R. (1981) The prehistory of human subsistence: a speculative outline.In: Food, Nutrition and Evolution: Food as an Environmental Factor in the Genesisof Human Variability (eds D.N. Walcher and N. Kretchmer). Masson, New York,pp 15–35.

Harris, D.R. (1984) Ethnohistorical evidence for the exploitation of wild grasses andforbes: its scope and archaeological implications. In: Plants and Ancient Man. Studiesin Paleoethnobotany (eds W. Van Zeist and W.A. Casparie). A. A. Balkema, Rotterdam,pp 63–69.

Harris, D.R. (1989) An evolutionary continuum of people-plant interaction. In: For-aging and Farming: The Evolution of Plant Exploitation (eds D.R. Harris and G.C.Hillman). Routledge, London, pp 11–26.

Harris, D.R. (1996) Introduction: themes and concepts in the study of early agriculture.In: The Origins and Spread of Agriculture and Pastoralism in Eurasia (ed. D.R. Harris).UCL Press, London, pp 1–9.

Harris, D.R. (2004) Origins and spread of agriculture. In: The Cultural History of Plants(eds M. Nesbitt and G. Prance). Routledge, London, pp 13–26.


Harris, D.R. (2008) Agriculture, cultivation and domestication: exploring the concep-tual framework of early food production. In: Rethinking Agriculture. Archaeologicaland Ethnoarchaeological Perspectives (eds T. Denham, J. Iriarte and L. Vrydaghs). LeftCoast Press, Walnut Creek, pp 16–35.

Hattori, T., Terada, T. and Hamasuna, S.T. (1994) Sequence and functional analysesof the rice gene homologous to the maize Vp1. Plant Molecular Biology 24, 805–810.

Hayama, R., Yokoi, S., Tamaki, S., Yano, M. and Shimamoto, K. (2003) Adaptation ofphotoperiodic control pathways produce short-day flowering in rice. Nature 422,719–722.

Heiser, C.B. (1990) Seed to Civilization: The Story of Food, new (3rd) edn. HarvardUniversity Press, Cambridge, MA.

Heiser, C.B. (2008) The domesticated sunflower in old Mexico? Genetic Resources andCrop Evolution 45, 447–449.

Helbaek, H. (1954) Prehistoric food plants and weeds in Denmark. A survey of ar-chaeobotanical research 1923–1954. Danmarks Geoligishe Unders, Series II 80, 250–261.

Helbaek, H. (1959) Domestication of food plants in the Old World. Science 130, 365–372.Helbaek, H. (1960) The paleoethnobotany of the Near East and Europe. In: Prehistoric

Investigations in Iraqi Kurdistan (eds R.J. Braidwood and B. Howe). University ofChicago Press, Chicago, pp 99–118.

Helbaek, H. (1970) The plant husbandry of Hacilar. In: Excavations at Hacilar (ed. J.Mellaart). Edinburgh University Press, Edinburgh, pp 189–244.

Henriksen, P.S. and Robinson, D. (1996) Early Iron Age agriculture: archaeobotani-cal evidence from an underground granary at Overbygaard in northern Jutland,Denmark. Vegetation History and Archaeobotany 5, 1–11.

Higgs, E.S. and Jarman, M.R. (1969) The origins of agriculture: a reconsideration.Antiquity 43, 31–41.

Higgs, E.S. and Jarman, M.R. (1972) The origins of animal and plant husbandry.In: Papers in Economic Prehistory (ed. E.S. Higgs). Cambridge University Press,Cambridge, pp 3–13.

Hillman, G.C. and Davies, M.S. (1990) Domestication rates in wild wheats and barleyunder primitive cultivation. Biological Journal of the Linnean Society 39, 39–78.

Hillman, G.C. and Davies, M.S. (1999) Domestication rate in wild wheats and barleyunder primitive cultivation: preliminary results and archaeological implications offield measurements of selection coefficient. In: Prehistory of Agriculture. New Experi-mental and Ethnographic Approaches (ed. P.C. Anderson), Monograph 40. Institute ofArchaeology, University of California, Los Angeles, pp 70–102.

Hillman, G.C., Hedges, R., Moore, A.M.T., Colledge, S. and Pettitt, P. (2001) Newevidence of Late Glacial cereal cultivation at Abu Hureyra on the Euphrates. TheHolocene 11, 383–393.

Hori, K, Sato, K. and Takeda, K. (2007) Detection of seed dormancy QTL in multiplemapping populations derived from crosses involving novel barley germplasm.Theoretical and Applied Genetics 115, 869–876.

Hovav, R., Udall, J.A., Chaudhart, B., Hovav, E., Flagel, L., Hu, G. and Wendel, J.F.2008. The evolution of spinnable cotton fiber entailed prolonged development anda novel metabolism. PLoS Genetics 4(2), e25.

Huang, F. and Zhang, M. (2000) Pollen and phytolith evidence for rice cultivationduring the Neolithic at Longquizhuang, eastern Jainghuai, China. Vegetation Historyand Archaeobotany 9, 161–168.


Hunter, A.A. (1992) Utilization of Hordeum pusillum (Little Barley) in the MidwestUnited States: Applying Rindos’Co-evolutionary Model of Domestication. Ph.D. Disser-tation. Department of Anthropology, University of Missouri, Columbia.

Hutchinson, J. (1970) The genetics of evolutionary change. The Indian Journal of Genetics& Plant Bredding 30(2), 269–279.

Iltis, H. (2000) Homeotic sexual translocations and the origin of maize (Zea mays,Poaceae): a new look at an old problem. Economic Botany 54, 7–42.

Jacomet, S. and Behre, K.-H. (1991) The ecological interpretation of archaeobotanicaldata. In: Progress in Old World Paleoethnobotany (eds W.A. Van Zeist, K. Wasylikowaand K.-H. Behre). A. A. Balkema, Rotterdam, pp 81–108.

Janatasuriyarat, C., Vales, M.I., Watson, C.J. and Riera-Lizarazu, W. (2004) Identifi-cation and mapping of genetic loci affecting the free-threshing habit and spikecompactness in wheat (Triticum aestivum L.) Theoretical and Applied Genetics 108,261–273.

Jones, H., Leigh, F., Mackay, I., Bower, M., Smith, L., Charles, M., Jones, G., Jones,M., Brown, T. and Powell, W. (2008) Population based re-sequencing reveals thatthe flowering time adaptation of cultivated barley originated east of the FertileCrescent. Molecular Biology and Evolution 25, 2211–2219.

Jones, H.D., Peters, N.C.B. and Holdsworth, M.J. (1997) Genotype and environmentinteract to control dormancy and differential expression of the VIVIPAROUS-1homologue in embryos of Avena fatua. Plant Journal 12(4), 911–920.

Jones, M.K. (1988) The arable field: a botanical battleground. In: Archaeology and theFlora of the British Isles—Human Influence on the Evolution of Plant Communities (ed.M.K. Jones). Oxford University Committee for Archaeology Monograph 14, Oxford,pp 86–92.

Jupe, M. (2003) The Effects of Charring on Pulses and Implications for Using Size Change toIdentify Domestication in Eurasia. Unpublished BA Dissertation. Institute of Archae-ology, University College London, London.

Kaga, A., Isemura, T., Tomooka, N. and Vaughan, D.A. (2008) The genetics of domes-tication of the Azuki bean (Vigna angularis). Genetics 178, 1013–1036.

Kaplan, L. (2000) Beas, peas and lentils. In: The Cambridge World History of Food (edsK.F. Kiple and K.C. Ornelas). Cambridge University Press, Cambridge, pp 271–281.

Kaplan, L., Lynch, T.F. and Smith, C.E., Jr. (1973) Early cultivated beans (Phaeseolusvulgaris) from an intermontane valley in Peru. Science 179, 76–77.

Kellogg, E.A. (1998) Relationships of cereal crops and other grasses. Proceedings of theNational Academy of Sciences USA 95, 2005–2010.

Kerem, Z., Gopher, A., Lev-Yadun, S., Weinberg, P. and Abbo, S. (2007) Chickpeadomestication in the Neolithic Levant through the nutritional perspective. Journalof Archaeological Science 34, 1289–1293.

Kilian, B., Ozkan, H., Walther, A., Kohl, J., Dagan, T., Salamini, F. and Martin, W.(2007) Molecular diversity at 18 loci in 321 wild and 92 domesticate lines reveal noreduction of nucleotide diversity during Triticum monococcum (Einkorn) domesti-cation: implications for the origin of agriculture. Molecular Biology and Evolution 24,2657–2668.

King, L.J. (1966) Weeds of the World, Biology and Control. Interscience Publishers, Inc.,New York.

Kislev, M.E., Weiss, E. and Hartmann, A. (2004) Impetus for sowing and the beginningof agriculture: ground collecting of wild cereals. Proceedings of the National Academyof Sciences USA 101, 2692–2695.


Kitano, H., Futsuhara, Y. and Satoh, H. (1993) Morphological variations in ricecultivars. In: Science of the Rice Plant. Volume One. Morphology (eds T. Mat-suo and K. Hoshikawa). Food and Agriculture Policy Research Center, Tokyo,pp 79–88.

Klee, M., Zach, B. and Neumann, K. (2000) Four thousand years of plant exploitationin the Chad Basin of northeast Nigeria I: the archaeobotany of Kursakata. VegetationHistory and Archaeobotany 9, 223–237.

Klee, M., Zach, B. and Stika, H.-P. (2004) Four thousand years of plant exploitationin the Lake Chad Basin (Nigeria), part III: plant impressions in potsherds from thefinal Stone Age Gajiganna Culture. Vegetation History and Archaeobotany 13, 131–142.

Koinange, E.M.K., Singh, S.P. and Gepts, P. (1996) Genetic control of the domesticationsyndrome in common bean. Crop Science 36, 1037–1045.

Kojima, S., Takahashi, Y., Kobayashi, Y., Monna, L., Sasaki, T., Araki, T. and Yano,M. (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition toflowering downstream of Hd1 under short day conditions. Plant Cell Physiology 43,1096–1105.

Komatsuda, T., Pourkheirandish, M., He, C., Azhaguvel, P., Kanamori, H., Perovic, D.,Stein, N., Graner, A., Wicker, T., Tagiri, A., Lundqvist, U., Fujimura, T., Matsuoka,M., Matsumoto, T. and Yano, M. (2007) Six-rowed barley originated from a mutationin a homeodomain-leucine zipper I-class homeobox gene. Proceedings of the NationalAcademy of Sciences USA 104, 1424–1429.

Konishi, S., Izawa, T., Lin, S.Y., Ebana, K., Fukuta, Y., Sasaki, T. and Yano, M. (2006)A SNP caused loss of seed shattering during rice domestication. Science 312,1392–1396.

Kottearachchi, N.S., Uchino, N., Kato, K. and Miura, H. (2006) Increased grain dor-mancy in white-grained wheat by introgression of preharvest sprouting toleranceQTLs. Euphytica 152, 421–428.

Kovach, M.J., Sweeney, M.T. and McCouch, S.R. (2007) New insights into the historyof rice domestication. Trends in Genetics 23, 578–587.

Kreuz, A., Marinova, E., Schafer, E. and Wiethold, J. (2005) A comparison of early Ne-olithic crop and weed assemblages from the Linearbankeramik and the BulgarianNeolithic culture: differences and similarities. Vegetation History and Archaeobotany14, 237–258.

Krishnasamy, V. and Seshu, D.V. (1989) Seed germination rate and associated charac-ters in rice. Crop Science 29, 904–908.

Kucera, B., Cohn, M.A. and Leubner-Metzger, G. (2005) Plant hormone interactionsduring seed dormancy release and germination. Seed Science Research 15, 281–307.

Ladizinsky, G. (1979) The genetics of several morphological traits in lentil. The Journalof Heredity 70, 135–137.

Ladizinsky, G. (1985) The genetics of hard seed coat in the genus Lens. Euphytica 34,539–543.

Ladizinsky, G. (1987) Pulse domestication before cultivation. Economic Botany 41,60–65.

Ladizinsky, G (1993) Lentil domestication: on the quality of evidence and arguments.Economic Botany 47, 60–64.

Ladizinsky, G. (2008) How many tough-rachis mutants gave rise to domesticatedbarley? Genetic Resources and Crop Evolution 45, 395–489.

Li, C., Zhou, A. and Sang, T. (2006) Rice domestication by reducing shattering. Science311, 1936–1939.


Li, W. and Gill, B.S. (2006) Multiple genetic pathways for seed shattering in the grasses.Functional and Integrative Genomics 6, 300–309.

Lin, Z., Griffith, M., Li, X., Zhu, Z., Tan, L., Fu, Y., Zhang, W., Wang, X., Xie, D. andSun, C. (2007) Origin of seed shattering in rice (Oryza sativa L.) Planta 226, 11–20.

Liu, L., Lee, G.-A., Jiang, L. and Zhang, J. (2007) Evidence for the early beginning (c.9000 cal. BP) of rice domestication in China: a response. The Holocene 17, 1059–1068.

Lone, F.A., Khan, M. and Buth, G.M. (1993) Palaeoethnobotany – Plants and Ancient Manin Kashmir. A. A. Balkema, Rotterdam.

Long, A. and Fritz, G.J. (2001) Validity of AMS dates on maize from the TehuacanValley: a comment on MacNeish and Eubanks. Latin American Antiquity 12(1), 87–90.

Lynch, T.F., Gillespie, R., Gowlette, J.A. and Hedges, R.M. 1985. Chronology of Gui-tarrero Cave, Peru. Science 229, 864–867.

Maass, B. (2005) Changes in seed morphology, dormancy and germination from wildto cultivated hyacinth bean germplasm (Lablab purpureus: Papilionoideae). GeneticResources and Crop Evolution 53, 1127–1135.

Maccaferri, M., Sanguineti, M.C., Corneti, S., Ortega, J.L.A., Salem, M.B., Bort, J.,DeAmbrogio, E., Fernando, L., Moral, G., Demontis, A., El-Ahmed, A., Malouff,F., Machlab, H., Martos, V., Moragues, M., Motajawi, J., Nachit, M., Nserallah, N.,Ouabbou, H., Royo, C., Slama, A., Tuberosa, R. (2008) Quantitative trait loci forgrain yield and adaptation of durum wheat (Triticum durum Desf.) across a widerange of water availability. Genetics 178, 489–511.

MacDonald, K., Vernet, R. Fuller, D. and Woodhouse, J. (2003) New light on theTichitt tradition: a preliminary report on survey and excavation at Dhar Nema. In:Researching Africa’s Past. New Contributions from British Archaeologists (eds P. Mitchell,A. Haour and J. John Hobart). Oxford Univerity School of Archaeology MonographNo. 57, Oxford, pp 73–80.

Magid, A.A. (1989) Plant Domestication in the Middle Nile Basin – An Archaeobotani-cal Case Study, Vol. 523. BAR International Series. British Archaeological Reports,Oxford.

Magid, A.A. (2003) Exploitation of food-plants in the early and middle Holocene BlueNile area, Sudan and neighbouring areas. Complutum 14, 345–372.

Maranon, T. and Grubb, P.J. (1993) Physiological basis and ecological significanceof the seed size and relative growth rate relationship in Mediterranean annuals.Functional Ecology 7, 591–599.

McKibbin, R.S., Wilkinson, M.D., Bailey, P.C., Flintham, J.E., Andrew, L.M., Lazzeri,P.A., Gale, M.D., Lenton, J.R. and Holdsworth, M.J. (2002) Transcripts of Vp-1homologues are misspliced in modern wheat and ancestral species. Proceedings ofthe National Academy of Sciences USA 99, 10203–10208.

Marquez-Cedillo, L.A., Hayes, P.M., Kleinhofs, A., Legge, W.G., Rossnagel, B.G., Sato,K., Ullrich, S.E., Wesenberg, D.M. ([The North American Barley Genome Map-ping Project]) (2001) QTL analysis of agronomic traits in barley based on the dou-bled haploid progeny of two elite North American varieties representing differentgermplasm groups. Theoretical and Applied Genetics 203, 625–637.

Matsui, K., Kiryu, Y., Komatsuda, T., Kurauchi, N., Ohtani, T. and Tetsuka, T. (2004)Identification of AFLP markers linked to non-seed shattering locus (sht1) in buck-wheat and conversion to STS markers for marker-assisted selection. Genome 47,469–474.

Matsui, K., Tetsuka, T. and Hara, T. (2003) Two independent gene loci controllingnon-brittle pedicels in buckwheat. Euphytica 134, 203–208.


McCarty, D.R., Hattori, T., Carson, C.B., Vasil, V., Lazar, M. and Vasil, I. (1991) TheVivaporous-1 developmental gene of maize encodes a novel transcriptional activator.Cell 66, 895–905.

Michaels, S.D., Ditta, G., Gustafson-Brown, C., Pelaz, S., Yanofsky, M. and Amasino,R.M. (2003) AGL24 acts a s apromoter of flowering in Arabidopsis and is positivelyregulated by vernalization. The Plant Journal 33, 867–874.

Mohamed, H.A., Clark, J.A. and Ong, C.K. (1985) The influence of temperature duringseed development on the germination characteristics of millet seeds. Plant, Cell andEnvironment 8, 361–362.

Murray, M.A., Fuller, D.Q. and Cappeza, C. (2007) Crop production on the SenegalRiver in the early first Millennium AD: preliminary archaeobotanical results fromCubalel. In: Fields of Change. Progress in African Archaeobotany (ed. R.T.J. Cappers),Grongingen Archaeological Studies 5. Barkhuis Publishing, Groningen, pp 63–70.

Nabhan, G.P. and Rea, A. (1987) Plant domestication and folk-biological change: theupper Piman/Devil’s claw example. American Anthropologist 89, 57–73.

Nabhan, G.P., Whiting, A., Dobyns, H., Hevly, R. and Euler, R. (1981) Devil’s clawdomestication: evidence from southwestern Indian fields. Journal of Ethnobiology 1,135–164.

Nadel, D., Weiss, E., Simchoni, O., Tsatskin, A. Danin, A. and Kislev, M.E. (2004)Stone age hut in Israel yields world’s oldest evidence of bedding. Proceedings of theNational Academy of Sciences USA 101, 6821–6826.

Nesbitt, M.N. (2004) Can we identify a centre, a region or a supra-region for neareastern plant domestication? Neo-lithics 1, 38–40.

Niklas, K.J. (1994) Plant Allometry: The Scaling of Form and Process. University of ChicagoPress, Chicago.

Niklas, K.J. (1997) The Evolutionary Biology of Plants. University of Chicago Press,Chicago.

Nitsuma, Y. (1993) Upland rice. In: Science of the Rice Plant. Volume One. Morphology(eds T. Matsuo and K. Hoshikawa). Food and Agriculture Policy Research Center,Tokyo, pp 70–76.

Ogiso, E., Izawa, T., Takahashi, Y., Sasaki, T. and Yano, M. (2007) Functional analysisof Hd6, a rice flowering time gene. Plant and Cell Physiology 48(Suppl.), S150.

Oka, H.-I. (1988) Origins of Cultivated Rice. Elsevier, Amsterdam.Oka, H.-I. and Morishima, H. (1971) The dynamics of plant domestication: cultivation

experiments with Oryza perennis and its hybrid with O. sativa. Evolution 25, 356–364.Osa, M., Kato, K., Mori, M., Shindo, C., Torada, A. and Miura, H. (2003) Mapping

QTLs for seed dormancy and the Vp1 homologue on chromosome 3A in wheat.Theoretical and Applied Genetics 106, 1491–1496.

Paterson, A.H., Lin, Y.-R., Li, Z., Schertz, K.F., Doebley, J.F., Pinson, S.R.M., Liu, S.-C.,Stansel, J.W. and Irvine, J.E. (1995) Convergent domestication of cereal crops byindependent mutations at corresponding genetic loci. Science 269, 1714–1718.

Pearson, E.S. and Hartley, H.O. (1976) Biometrika Tables for Statisticians, Vol. 1.Biometrika Trust, Cambridge University Press, Cambridge.

Peltenberg, E., Colledge, S., Croft, P., Jackson, A., McCartney, C. and Murray, M.A.(2001) Neolithic dispersals from the Levantine Corridor: a Mediterranean perspec-tive. Levant 33, 35–64.

Phillips, L.L. (1976) Cotton. In: The Evolution of Crop Plants (eds N.W. Simmonds).Longman, Harlow, pp 196–200.


Piperno, D.R. and Flannery, K.V. (2001) The earliest archaeological maize (Zeamays L.) from highland Mexico: new accelerator mass spectrometry dates andtheir implications. Proceedings of the National Academy of Sciences USA 98, 2101–2103.

Plitman, U. and Kislev, M.E. (1989) Reproductive changes induced by domestica-tion. In: Advances in Legume Biology (eds C.H. Stirton and J.L. Zarucchi). MissouriBotanical Garden, St. Louis, pp 487–503.

Poncet, V., Lamy, F., Devos, K., Gale, M., Sarr, A. and Robert, T. (2000) Genetic controlof domestication traits in pearl millet (Pennisetum glaucum L., Poaceae). Theoreticaland Applied Genetics 100, 147–159.

Poncet, V., Lamy, F., Enjalbert, J., Joly, H., Sarr, H. and Robert, T. (1998) Geneticanalysis of the domestication syndrome in pearl millet (Pennisetum glaucum L.,Poaceae): inheritance of the major characters. Heredity 81, 648–658.

Reed, C.A. (1977) Introduction: prologue. In: Origins of Agriculture (ed. C.A. Reed).Mouton, The Hague, pp 1–21.

Ridley, H.N. (1930) The Dispersal of Plants throughout the World. L. Reeve, London.Rindos, D. (1980) Symbiosis, instability, and the origins and spread of agriculture: a

new model. Current Anthropology 21, 751–772.Robson, F., Costa, M.M.R., Hepworth, S.R., Vizir, I., Pineiro, M., Reeves, P.H., Putterill,

J. and Coupland, G. (2001) Functional importance of conserved domains in theflowering-time gene CONSTANS demonstrated by analysis of mutant alleles andtransgenic plants. The Plant Journal 28, 619–631.

Roder, M.S., Huang, X.-Q. and Borner, A. (2008) Fine mapping of the region of wheatchromosome 7D controlling grain weight. Functional and Integrative Genomics 8,79–86.

Roeder, A.H.K., Ferrandiz, C. and Yanofsky, M.F. (2003) The role of the REPLUM-LESS homeodomain protein in patterning the Arabidopsis fruit. Current Biology 13,1630–1635.

Sang, T. and Ge, S. (2007) The puzzle of rice domestication. Journal of Integrative PlantBiology 49, 760–768.

Sato, Y.-I. (2002) Origin of rice cultivation in the Yangtze River basin. In: The Originsof Pottery and Agriculture (ed. Y. Yasuda). Lustre Press/Roli Books, New Delhi, pp143–150.

Sauer, C.O. (1958) Jericho and composite sickles. Antiquity 32, 187–189.Sherratt, A.G. (1980) Water soil and seasonality in early cereal cultivation. World

Archaeology 11, 313–330.Sherratt, A.G. (1997) Climatic cycles and behavioural revolutions: the emergence of

modern humans and the beginnings of farming. Antiquity 71, 271–287.Shomura, A., Izawa, E.K., Ebitani, T., Kanegae, H., Konishi, S. and Yano, M. (2008)

Deletion in a gene associated with grain size increased yields during rice domesti-cation. Nature Genetics 40, 1023—1028. doi: 10.1038/ng.169.

Simons, K.J., Fellers, J.P., Trick, H.N., Zhang, Z., Tai, Y.-S., Gill, B.S. and Faris, J. (2006)Molecular characterization of the major wheat domestication gene Q. Genetics 172,547–555.

Sinnott, E.W. (1936) A developmental analysis of inherited shape differences in cu-curbit fruits. American Naturalist 70, 245–254.

Sinnott, E.W. (1939) A developmental analysis of the relation between cell size andfruit size in cucurbits. American Journal of Botany 26, 179–189.

Smartt, J. (1990) Grain Legumes. Cambridge University Press, Cambridge.


Smith, B.D. (1989) Origins of agriculture in eastern North America. Science 246,1566–1571.

Smith, B.D. (1992) River of Change. Essays on Early Agriculture in Eastern North America.Smithsonian Press, Washington, D.C.

Smith, B.D. (2001) Documenting plant domestication: the consilience of biological andarchaeological approaches. Proceedings of the National Academy of Sciences USA 98,1324–1326.

Smith, B.D. (2006a) Documenting domesticated plants in the archaeological record.In: Documenting Domestication. New Genetic and Archaeological Paradigms (eds M.A.Zeder, D.G. Bradley, E. Emshwiller and B.D. Smith). University of California Press,Berkeley, pp 15–24.

Smith, B.D. (2006b) Eastern North America as an independent center of plantdomestication. Proceedings of the National Academy of Sciences USA 103, 12223–12228.

Song, X.-J., Huang, W., Shi, M., Zhu, M.-Z. and Lin, H.-X. (2007) A QTL for rice grainwidth and weight encodes a previously unknown RING-type E3 ubiquitin ligase.Nature Genetics 39, 623–630.

Stemler, A.B. (1990) A scanning electron microscopic analysis of plant impressions inpottery from the sites of Kadero, El Zakiab, Um Direiwa and el Kadada. Archeologiedu Nil Moyen 4, 87–105.

Stokes, P. and Rowley-Conwy, P. (2002) Iron Age cultigen? Experimental return ratesfor Fat Hen (Chenopodium album L.). Environmental Archaeology 7, 95–99.

Sweeney, M.T. and McCouch, S.R. (2007) The Complex History of the Domesticationof Rice. Annals of Botany 100, 951–957.

Sweeney, M.T., Thomson, M.J., Cho, Y.G., Park, Y.J., Williamson, S.H., Bustamante,C. and McCouch, S.R. (2007) Global dissemination of a single mutation conferringwhite pericarp in rice. PLoS Genetics 3(8), e133. doi: 10.1371/journal.pgen.0030133.

Sweeney, M.T., Thomson, M.J., Pfeil, B.E. and McCouch, S.R. (2006) Caught red-handed: Rc encodes a basic helix–loop–helix protein conditioning red pericarp inrice. Plant Cell 18, 283–294.

Takahashi, R (1955) The origin and evolution of cultivated barley. In: Advances inGenetics 7 (ed. M. Demerc). Academic Press, New York, pp 227–266.

Takahashi, Y., Shomura, A., Sasai, T., Yano, M. (2001) Hd6, a rice quantitativelocus involved in photoperiod sensitivity, encodes the alpha subunit of pro-tein kinase CK2. Proceedings of the National Academy of Sciences USA 98, 7922–7927.

Tang, L. (2003) The primitive rice remains from Chuodun Site. In: Chuodun ShanSite: Collected Papers, Dongnan Wenhua [Southeast Culture] 2003(special issue 1),46–49 [ in Chinese].

Tang, S., Min, S. and Sato, Y.-I. (1996) Exploration on Origin of keng rice (japonica) inChina. In: Origin and Differentiation of Chinese Cultivated Rice (eds X. Wang and C.Sun). Chinese Agricultural University Press, Beijing, pp 72–80.

Tanno, K.-I. and Willcox, G. (2006) How fast was wild wheat domesticated? Science311, 1886.

Thompson, G.B. (1996) The Excavations of Khok Phanom Di, A Prehistoric Site in CentralThailand. Volume IV. Subsistence and Environment: The Botanical Evidence. The BiologicalRemains Part III. The Society of Antiquaries of London, London.

Thompson, G.B. (1997) Archaeobotanical indicators of rice domestication – a criticalevaluation of diagnostic criteria. South-East Asian Archaeology 1992. Instituto Italianoper L’Africa e L’Orient, Rome, pp 159–174.


Turner, A., Beales, J., Faure, S., Dunford, R.P. and Laurie, D.A. (2005) The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science310, 1031–1034.

Upadhyaya, H.D., Kumar, S., Gowda, S.L.L. and Singh, S. (2006) Two major genes forseed size in chickpea (Cicer arietinum L.). Euphytica 147, 311–315.

Van Zeist, W. and Bakker-Heeres, J.H. (1985) Archaeobotanical studies in the Levant1. Neolithic sites in the Damascus Basin: Aswad, Ghoraife, Ramad. Palaeohistoria24, 165–256.

Vanhala, T.K. and Stam, P. (2006) Quantitative trait loci for seed dormancy in wildbarley (Hordeum spntaneum C. Koch). Genetic Resources and Crop Evolution 53, 1013–1019.

Vaughan, D.A., Lu, B.-R. and Tomooka, N. (2008) The evolving story of rice evolution.Plant Science 174, 394–408.

Wan, J.M., Jiang, L., Tang, J.Y., Wang, C.M., Hou, M.Y., Jing, W. and Zhang, L.X. (2005)Genetic dissection of the seed dormancy trait in cultivated rice. (Oryza sativa L.).Plant Science 170, 786–792.

Wasylikowa, K., Barakat, H.N., Boulos, L., Butler, A., Dahlberg, J.A., Hather, J. andMitka, J. (2001) Site E-75-6: vegetation and subsistence of the early neolithic at NabtaPlaya, Egypt, reconstructed from charred plant remains. In: Holocene Settlement ofthe Egyptian Sahara: Volume 1: The Archaeology of Nabta Playa (eds F. Wendorf and R.Schild). Kluwer/Plenum, New York, pp 544–591.

Wasylikowa, K., Mitka, J., Wendorf, F. and Schild, R. (1997) Exploitation of wild plantsby the early neolithic hunter–gatherers in the Western Desert of Egypt: Nabta Playaas a case-study. Antiquity 71, 932–941.

Wasylikowa, K., Schild, R., Wendorf, F., Krolik, H., Kubiak-Martens, L. and Harlan,J.R. (1995) Archaeobotany o the early neolithic site E-75–6 at Nabta Playa, WesternDesert, South Egypt (preliminary results). Acta Palaeobotanica 35, 133–155.

Weber, S.A. (1991) Plants and Harappan Subsistence. An Example of Stability and Changefrom Rojdi. Oxford and IBH, New Delhi.

Weeden, N.F. (2007) Genetic changes accompanying the domestication of Pisumsativum: Is there a common genetic basis to the ‘Domestication Syndrome’ forLegumes? Annals of Botany 100(5), 1017–1025.

Weeden, N.F., Brauner, S. and Przyborowski, J.A. (2002) Genetic analysis of poddehiscence in pea (Pisum sativum L.). Cellular and Molecular Biology Letters 7, 657–663.

Weiss, E., Kislev, M.E. and Hartmann, A. (2006) Autonomous cultivation before do-mestication. Science 312, 1608–1610.

Westoby, M., Leishman, M. and Lord, J. (1996) Comparative ecology of seed sizeand dispersal. Philosophical Transactions of the Royal Society B: Biological Sciences 351,1309–1318.

White, C., Proebsting, W.M., Hedden, P. and Rivin, C.J. (2000) Giberellins and seed de-velopment. I. Evidence that gibberellin/abscissic acid balance governs germinationversus maturation pathways. Plant Physiology 122, 1081–1088.

White, C. and Rivin, C.J. (2000) Giberellins and seed development. II. Giberellin syn-thesis inhibition enhances abscisic acid signalling in culture embryos. Plant Physi-ology 122, 1088–1097.

Wilke, P.J., Bettinger, R., King, T.F. and O’Connell, J.F. (1972) Harvest selection anddomestication in seed plants. Antiquity 46, 203–209.

Willcox, G. (1992) Some differences between crops of Near Eastern origin and thosefrom the tropics. In: South Asian Archaeology 1989 (ed. C. Jarrige). Prehistory Press,Madison, pp 291–299.


Willcox, G. (1999) Agrarian change and the beginnings of cultivation in the Near East:evidence from wild progenitors, experimental cultivation and archaeobotanicaldata. In: The Prehistory of food. Appetites for Change (eds C. Gosden and J. Hather).Routeledge, London, pp 478–500.

Willcox, G. (2004) Measuring grain size and identifying near eastern cereal domes-tication: evidence from the Euphrates valley. Journal of Archaeological Science 31,145–150.

Willcox, G. (2005) The distribution, natural habitats and availability of wild cereals inrelation to their domestication in the Near East: multiple events, multiple centres.Vegetation History and Archaeobotany 14, 534–541.

Willcox, G., Fornite, S. and Herveux, L. (2008) Early Holocene cultivation beforedomestication in northern Syria. Vegetation History and Archaeobotany 17, 313–325.

Worland, A.J., Borner, A., Korzun, V., Li, W.M., Petrvıc, S. and Sayers, E.J. (1998) Theinfluence of photoperiod genes on the adaptability of European winter wheats.Euphytica 100, 385–394.

Xue, W., Xing, Y., Weng, X., Zhao, Y., Tang, W., Wang, L., Zhou, H., Yu, S., Xu, C.,Li, X. and Zhang, Q. (2008) Natural variation in Gdh7 is an important regulator ofheading date and yield potential in rice. Nature Genetics 40, 761–767.

Yamamoto, T., Lin, H.X., Sasaki, T. and Yano, M. (2000) Identification of heading datequantitative trait locus Hd6 and characterization of its epistatic interactions withHd2 in rice using advance backcross progeny. Genetics 154, 885–891.

Yan, L., Fu, D., Li, C., Blechl, A., Tranquilli, G., Bonafede, M., Sanchez, A., Valarik,M., Yasuda, S. and Dubcovsky, J. (2006) The wheat and barley vernalization geneVRN3 is an orthologue of FT. Proceedings of the National Academy of Sciences USA103, 19581–19586.

Yan, L., Helguera, M., Kato, K., Fukuyama, S., Sherman, J. and Dubcovsky, J. (2004b)Allelic variation at the VRN-1 promoter region in polyploidy wheat. Theoretical andApplied Genetics 109, 1677–1686.

Yan, L., Loukoianov, A., Blechl, A., Tranquilli, G., Ramakrishna, W., San Miguel,P., Bennetzen, J.L., Echenique, V. and Dubcovsky, J. (2004a) The wheat VRN2gene is a flowering repressor down-regulated by vernalization. Science 303, 1640–1644.

Yan, L., Loukoianov, A., Tranquilli, G., Helguera, M., Fahima, T. and Dubcovsky, J.(2003) Positional cloning of the wheat vernalization gene VRN1. Proceedings of theNational Academy of Sciences USA 100, 6263–6268.

Yano, M., Katayose, Y., Ashikari, M., Yamanouchi, U., Monna, L., Fuse, T., Baba,T., Yamamoto, K., Umehara, Y., Nagamura, Y. and Sasaki, T. (2000) Hd1, a majorphotoperiod sensitivity quantitative trait locus in rice, is closely related to theArabidopsis flowering time gene CONSTANS. The Plant Cell 12, 2473–2483.

Zach, B. and Klee, M. (2003) Four thousand years of plant exploitation in the ChadBasin of NE Nigeria II: discussion on the morphology of caryopses of domesticatedPennisetum and complete catalogue of the fruits and seeds of Kursakata. VegetationHistory and Archaeobotany 12, 187–204.

Zeder, M. (2006) Central questions in the domestication of plants and animals. Evolu-tionary Anthropology 15, 105–117.

Zeder, M.A. (2008) Domestication and early agriculture in the Mediterranean Basin:origins, diffusion, and impact. Proceedings of the National Academy of Sciences USA105(33), 11597–11604.


Zhao, T., Ni, Z., Dai, Y., Yao, Y., Nie, X. and Sun, Q. (2006) Characterization andexpression of 42 MADS-box genes in wheat (Triticum astivum L.). Molecular Geneticsand Genomics 276, 334–350.

Zheng, Y., Jaing, L. and Zheng, J. (2004) Study on the remains of ancient rice fromKuahuqiao Aite in Zhejiang Province. Chinese Journal of Rice Science 18, 119–124 [inChinese].

Zheng, Y., Sun, G. and Chen, X. (2007) Characteristics of the short rachillae of rice fromarchaeological sites dating to 7000 years ago. Chinese Science Bulletin 52, 1654–1660.

Zohary, D. (1969) The progenitors of wheat and barley in relation to domesticationand agriculture dispersal in the Old World. In: The Domestication and Exploitationof Animals and Plants (eds P.J. Ucko and G.W. Dimbleby). Duckworth, London, pp47–66.

Zohary, D. (1989) Pulse and cereal domestication: how different are they? EconomicBotany 43(1), 31–34.

Zohary, D. (2004) Unconscious selection and the evolution of domesticated plants.Economic Botany 58(1), 5–10.

Zohary, D. and Hopf, M. (1973) Domestication of pulses in the Old World. Science 182,887–894.

Zohary, D. and Hopf, M. (2000) Domestication of Plants in the Old World, 3rd edn.Oxford University Press, Oxford.

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