macroevolutionary patterns of flowering plant speciation...

PP69CH25_Vamosi ARI 4 April 2018 8:6

Annual Review of Plant Biology

Macroevolutionary Patternsof Flowering Plant Speciationand ExtinctionJana C. Vamosi,1 Susana Magallon,2 Itay Mayrose,3

Sarah P. Otto,4 and Herve Sauquet5,6

1Department of Biological Sciences, University of Calgary, Calgary, Alberta T2N 1N4, Canada;email: [email protected] de Biologıa, Universidad Nacional Autonoma de Mexico, Ciudad de Mexico 04510,Mexico3Department of Molecular Biology and Ecology of Plants, George S. Wise Faculty of LifeSciences, Tel Aviv University, Tel Aviv 69978, Israel4Department of Zoology and the Biodiversity Research Centre, University of British Columbia,Vancouver, British Columbia V6T 1Z4, Canada5Laboratoire Ecologie, Systematique, Evolution, Universite Paris-Sud, CNRS UMR 8079,91405 Orsay, France6National Herbarium of New South Wales (NSW), Royal Botanic Gardens and Domain Trust,Sydney, NSW 2000, Australia

Annu. Rev. Plant Biol. 2018. 69:685–706

First published as a Review in Advance onFebruary 28, 2018

The Annual Review of Plant Biology is online atplant.annualreviews.org

https://doi.org/10.1146/annurev-arplant-042817-040348

Copyright c© 2018 by Annual Reviews.All rights reserved

Keywords

biome, conservation, dispersal, diversification, pollination, polyploidy,sexual system

Abstract

Species diversity is remarkably unevenly distributed among flowering plantlineages. Despite a growing toolbox of research methods, the reasons under-lying this patchy pattern have continued to perplex plant biologists for thepast two decades. In this review, we examine the present understanding oftransitions in flowering plant evolution that have been proposed to influencespeciation and extinction. In particular, ploidy changes, transitions betweentropical and nontropical biomes, and shifts in floral form have received at-tention and have offered some surprises in terms of which factors influencespeciation and extinction rates. Mating systems and dispersal characteristicsonce predominated as determining factors, yet recent evidence suggests thatthese changes are not as influential as previously thought or are importantonly when paired with range shifts. Although range extent is an important

685

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ANNUAL REVIEWS Further

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https://www.annualreviews.org/doi/full/10.1146/annurev-arplant-042817-040348


correlate of speciation, it also influences extinction and brings an applied focus to diversificationresearch. Recent studies that find that past diversification can predict present-day extinction riskopen an exciting avenue for future research to help guide conservation prioritization.

Contents

1. INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6862. KEY INNOVATIONS AND DIVERSIFICATION PATTERNS

OVER LONG TIMESCALES . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6902.1. Diversification Rate Shifts in Angiosperms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6902.2. Key Floral Innovations in Angiosperms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 691

3. GENOMIC AND GEOGRAPHICAL INFLUENCES ON ANGIOSPERMDIVERSIFICATION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6933.1. Whole-Genome Duplications in the Evolutionary History of Angiosperms . . . . 6933.2. Geographical Patterns in Angiosperm Diversification. . . . . . . . . . . . . . . . . . . . . . . . . 695

4. MECHANISMS UNDERLYING PATTERNS OF ANGIOSPERMDIVERSIFICATION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6954.1. The Context Dependence of Trait Transitions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6964.2. Constraints of Trait Evolution and Their Influence on Angiosperm

Diversification. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6965. EXTINCTION PATTERNS AND ANGIOSPERM DIVERSIFICATION . . . . . . 697

5.1. Macroevolutionary Patterns of Extinction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6975.2. The Fate of Flowering Plants in the Anthropocene . . . . . . . . . . . . . . . . . . . . . . . . . . . 698

1. INTRODUCTION

Angiosperms, or flowering plants, are a diverse group consisting of 304,000 named species—andpotentially as many as 156,000 unnamed (102)—that originated more recently than any otherclade of vascular plants, between approximately 140 and 250 Mya (37, 77, 131). Because of thiscomparatively recent origin, flowering plants have been subject to fewer major mass extinctionevents that obscure their patterns of speciation and background extinction (131). The remarkablevariation in form and habit among extant vascular plant clades has generated a proliferation ofinvestigations into macroevolutionary patterns. If we examine the time line of land plant evolutionover the entire Phanerozoic (18), paleontological approaches find that the high species diversityof angiosperms is a result of patterns of speciation outpacing extinction early in their evolutionaryhistory. Although this is similar to patterns exhibited by ferns (18, 127), some characteristics offlowering plants are unique (18).

The uneven distribution of species within the angiosperm clade was noticed early in paleobi-ological studies yet given relatively little attention (76), to some degree because species richnessvalues could be biased by differences in the quality of the fossil record between major plant clades(158). Nevertheless, the fossil record consistently produces patterns that show younger clades (i.e.,that originated in the Tertiary) contribute disproportionately to angiosperm species diversity dueto higher speciation rates and lower extinction rates (76). Phylogenetic perspectives of speciationand extinction surged after the development of sister-group tests by Slowinski & Guyer (133). Sincethen, our ability to incorporate phylogenetic evidence into diversification analyses has expanded

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rapidly (e.g., see References 107, 116, 120) (Figure 1), yet the methods differ in their assumptions,the range of models they explore, and the way they deal with incomplete and biased sampling (sum-marized in Figure 2; see also the sidebar titled Summary of Trait-Independent Methods to IdentifyShifts in Diversification Rates). Understanding the intricacies of these alternatives is critical if weare to understand when and why plants have diversified over evolutionary time (summarized inFuture Issues).

50 100 150 200Time (millions of years)

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www.annualreviews.org • Macroevolutionary Patterns of Flowering Plants 687

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Figure 1 (Figure appears on preceding page)

Disentangling speciation and extinction rates. The shape of a phylogenetic tree provides information about the relative rates ofspeciation (λ) and extinction (μ), not just the net diversification rate (r =λ – μ). Example trees were generated using diversitree in R(35), with (a) λ= 0.1 and μ= 0.075 (r = 0.025) in green; (b) λ= 0.1 and μ= 0.08 (r = 0.02) in blue; and (c) λ= 0.02 and μ= 0 (r = 0.02)in red. (d ) These differences can be detected in a plot showing lineages over time (88), here shown as the expected number of species(on a log scale) over time for those lineages that survive to the present. Early on, the slope reflects the diversification rate (r), which isthe same for blue and red clades [e.g., the number of lineages at time 100 (dashed lines)]. Near the present, recently formed taxa have notyet had time to go extinct and the slope approaches the speciation rate (λ) (116), which is the same for green and blue lineages (notethat these clades have many more younger taxa). (e) A simulated tree in which a character affecting the speciation and extinction rateswas allowed to change between green, blue, and red states at r = 0.003 (other parameters as above). Most of the youngest species are inthe states with a high speciation rate ( green or blue), whereas the overall high number of red lineages may be attributed to this statebeing ancestral. Hence, this upturn near the present primarily provides information about the effects of a trait on speciation (λ), and theoverall growth in size of a lineage provides information about the diversification rate (r).

Continuation

Speciationλ0

Extinctionμ1

Transitionq01

Figure 2Schematic of the processes considered in the Binary State Speciation and Extinction (BiSSE) model for abinary trait that can exist in two states, 0 and 1, denoted in the figure by blue and red, respectively (74). Thecore logic of BiSSE involves calculating the probability, DNi, of observing all the data (N) that descend froma particular point on the tree, given that the trait is in state i at that point. These data include both the shapeof the tree (its topology and the distribution of branch lengths) and the distribution of the character statesamong the extant species. As we move down a branch toward the root by an amount of time �t, eachpossible type of transition illustrated in the figure could occur and change DN0 with probability:μ0 �t 0︸︷︷︸

extinction

+ q01�tDN 1︸︷︷︸

transition

+ λ0�t2DN 0 E0︸︷︷︸

speciation

+ (1 − (μ0 + λ0 + q01)�t)DN 0︸︷︷︸

continuation

. In words, if extinction occurs

within this short time interval, then it is impossible to explain the data that descend from this point (hencethe 0 in the first term). If a trait transition occurs to state 1, then DN1 is the probability that we observe thedata (second term). If speciation occurs, then we have two daughter lineages, but assuming that we are on anonbifurcating branch, only one of these daughter species has descendants in the present, so one daughterlineage (either one, hence the 2) must explain the data and the other must go extinct by the present, whichoccurs with probability E0. Finally, nothing might have happened, in which case the probability of explainingthe data remains described by the variable DN0. Taking the limit as �t goes to 0 gives us a differentialequation for how DN0 changes over time, dDN0/dt. Along the way, however, we have introduced a newvariable, Ei, the probability that a single species that occurs at a particular point in the past in state i fails toleave any descendants in the present. However, we can describe the dynamics of Ei just as we did above. Thatis, E0 at a point �t closer to the root is: μ0�t1

︸︷︷︸

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. If the

lineage goes extinct in this interval, then we are done and extinction is certain (hence the 1). If there is atransition, then we have E1 as the new probability of extinction. If there is speciation, we have two lineagesthat must both go extinct by the present (E0

2, assuming they are independent). Finally, if nothing happens,then we still must explain the extinction of a lineage in state 0 with the probability E0. The above logic givesrise to four differential equations that can be traced back down through the tree: dDN0/dt, dDN1/dt, dE0/dt,dE1/dt. Nodes are traversed by setting the probability of observing the data for a node in state i to the rate ofspeciation multiplied by the probability of observing the data that descend from each daughter. Theseequations are numerically solved in the diversitree package in R (35), allowing the user to determine theparameters that give a high overall probability of observing a tree and the suite of extant traits.

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SUMMARY OF TRAIT-INDEPENDENT METHODS TO IDENTIFY SHIFTS INDIVERSIFICATION RATES

Early methods to detect changes in diversification rates in phylogenetic trees aimed to test the hypothesis that aconstant rate of diversification could explain observed differences in species richness between pairs of sister clades(e.g., 132, 133). Recently, however, it has been pointed out that sister clades are not expected to have equal numbersof species if one accounts for the waiting time until the derived character arises in one of the sisters (61).

The MEDUSA (Modeling Evolutionary Diversification Using Stepwise Akaike information criterion) approach(1) uses maximum likelihood to fit variable-rate birth-death models to a phylogenetic tree (or several trees inmultiMEDUSA). MEDUSA uses stepwise Akaike information criterion, known as AIC, to select the diversificationmodels that best fit the data. It identifies significant diversification shifts (increases or decreases) among branches ofthe tree. Each of the identified diversification regimes remains constant until a nested diversification shift is detected.It estimates the rate of diversification (r) and relative extinction (ε) for each diversification regime. Simulation studieshave shown that MEDUSA, in spite of its general utility, underestimates the number of diversification regimes in atree when rates vary through time and has a high false discovery rate, and simulations revealed little correspondencebetween actual and estimated rate parameters (80, 105). Nevertheless, it still is an attractive method owing to itsability to automatically detect diversification rate shifts rather than a priori break points in diversification rates (e.g.,Reference 87).

Bayesian analysis of macroevolutionary mixtures (BAMM) (104, 105) is related to MEDUSA. BAMM estimatesaveraged lineage rates of speciation (λ) and extinction (μ), as well as regime models that may include variablespeciation or extinction, or both, through time. Concerns have been expressed regarding BAMM’s likelihoodfunction, as it does not account for the possibility of diversification shifts along extinct branches, and about theaccuracy of the posterior distribution for the number of rate shifts (86, but see 108 for a response).

Synapomorphy:a newly evolvedcharacteristic presentin an ancestor andshared by itsdescendants

Key innovation:a novel trait thatallows the subsequentradiation and successof a taxonomic group

In this review, we reexamine several transitions in flowering plant evolution that have beenproposed to repeatedly influence speciation and extinction. Some of the transitions are marked bythe appearance of morphological traits that define lineages (synapomorphies). We do not attemptto review the potential effect on species richness of specific synapomorphies of angiosperms as awhole because most of these transitions are unique and their lack of replication is a major challengefor current macroevolutionary methods (73, 90, 143; see also Figures 1 and 2 and the sidebar titledSummary of Trait-Independent Methods to Identify Shifts in Diversification Rates). Instead, ourfocus is on transitions—such as those among ploidy levels (157), self-compatibility (42), or matingsystems (7, 44, 113)—that have recurred frequently, entailing changes to patterns of gene flow, tothe fixation rate of mutations, and to effective population size, and that may affect speciation andextinction rates.

Geography and environment are important drivers of diversification rates as well, and wesummarize recent insights into the mechanisms underlying the latitudinal biodiversity gradient.Many of these advances come from exploring how traits can spur diversification under certainenvironmental conditions yet depress diversification rates under others. This context dependencymay make many of the patterns of diversification appear idiosyncratic, with signatures of past keyinnovations that are difficult, but nevertheless exciting, to trace. Understanding the influence ofevolutionary history on biodiversity has practical applications in helping us to preserve hot spotsof speciation, as well as pinpoint areas of future conservation concern (24).

The above factors represent the environmental (extrinsic) and morphological (intrinsic) factorshypothesized to influence diversification in angiosperms (146, 147). The approaches to investi-gating these factors often diverge into two main lines of enquiry when examining diversification


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shifts in a group as large and globally distributed as the angiosperms: (a) How many shifts indiversification rates have occurred, and are these shifts clustered phylogenetically, temporally,environmentally, or geographically? (b) Are there floral and other intrinsic traits that have con-sistently influenced the diversification of flowering plants, and which of these traits represent keyinnovations that have spurred rapid radiations? We explore the present understanding of thesecomplexities below.

2. KEY INNOVATIONS AND DIVERSIFICATION PATTERNSOVER LONG TIMESCALES

2.1. Diversification Rate Shifts in Angiosperms

Evolutionary radiations can often be conceptualized as bursts of high diversification that are aconsequence of the evolution of a key morphological innovation, which might predict that shifts indiversification should closely mirror recognized clades, such as monophyletic families and orders(112). Many early studies investigated the unique features of angiosperms as possible factorsassociated with high species richness (17, 65, 139), with much of the attention focused on thepositive role of biotic pollination and dispersal, as well as herbaceous growth form, yet tools werenot available to determine overall patterns. We review here more recent studies that incorporatea model-based approach to diversification that is used to identify bursts in species richness thatresult from significant shifts in diversification along the phylogeny of flowering plants (Table 1).

Table 1 Summary of candidate traits and habitats affecting angiosperm diversification, speciation, and extinction ratesa

Trait or condition Method Proposed mechanism References

Intrinsic traits

Zygomorphy BiSSE Pollinator specialization increases speciation rate(but can also increase extinction rate)

115

Fruit and dispersal syndromes MEDUSA; BAMM Animal dispersal causes species to have larger rangesand lower extinction rates

67

Whole-genome duplication ChromEvol; BiSSE Polyploids diversify less, but polyploidization is acommon speciation mechanism available to diploids

96, 125, 144

Herbaceousness corHMM Originally, short generation time was thought toincrease divergence rate; it is now thought thatsmaller vasculature of trees allows niche expansionto colder climates

159

Extrinsic conditions

Dry habitats GeoSSE Patchy habitats (commonly found inMediterranean-like biomes) result in habitatgeneralization and decreased extinction

43

Open habitats BiSSE and QuaSSE Expansion of open, dry biomes after the Miocenespurred diversification of lineages with traitcombinations adapted for these conditions

93

Island archipelagos or island-likeregions (sky islands inmountainous regions)

GeoSSE Allopatric speciation rates increase with populationisolation

5, 15

Abbreviations: BAMM, Bayesian analysis of macroevolutionary mixtures; BiSSE, Binary State Speciation and Extinction (SSE); GeoSSE, Geographic SSE;MEDUSA, Modeling Evolutionary Diversification Using Stepwise AIC (Akaike information criterion); QuaSSE, Quantitative SSE.aThis table is not exhaustive but focuses on traits that have been examined with the current phylogenetically informed toolbox (see also the sidebar titled ASummary of Trait-Independent Methods to Identify Shifts in Diversification Rates).

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Sanderson & Donoghue (121) were among the first to evaluate the possibility that increaseddiversification rates were associated with the origin of angiosperm synapomorphies. They fittedpure birth models (no extinction) that differed in the number and placement of diversification shiftson a three-terminal phylogeny, representing the deepest split within the angiosperm clade and itsoutgroup, under different potential angiosperm rootings. The most likely models indicated thatlow ancestral diversification rates persisted through the earliest stages of angiosperm evolution,shifting later within the group. Thus, the origins of distinctive angiosperm traits—such as flow-ers, double fertilization, endosperm development, and seeds encased in fruits—do not coincidetemporally with the major expansions in angiosperm lineages. Extending this type of analysis withupdated methodologies and improved phylogenetic resolution, Magallon & Sanderson (78) cal-culated the rate of diversification of angiosperms as a whole and within a set of angiosperm cladesusing method-of-moments estimators based on a stochastic birth-death process that accounts forextinction. By comparing the observed diversity of major monophyletic groups to a null modelin which clades diversify homogeneously through time at a rate equal to that of angiosperms as awhole, they identified a number of unexpectedly species-rich clades, indicating that diversificationrates have increased independently in several groups of angiosperms. The same estimators wereapplied by Magallon & Castillo (75) to a set of angiosperm orders. Consistent with previous anal-yses, they found that early-branching angiosperm lineages displayed lower diversification rates,but higher rates were observed among several of the younger orders (e.g., Lamiales, with >23,000species, and Gentianales, with >17,000 species, both with origins dating back 77 to 102 Mya).They concluded that the extensive diversity of flowering plants is unlikely to have a single commonexplanation; rather, the appearance of various trait and ecological combinations likely spurred di-versity in different groups. Similar conclusions were reached by Davies et al. (22), who examineddiversification shifts across a supertree representing 379 angiosperm families.

Smith et al. (134) compared backbone trees including placeholders for major clades with mega-phylogenies derived from large and densely sampled alignments to detect diversification shifts inangiosperms. Backbone phylogenies were obtained for angiosperms as a whole and for six largeclades within the group. A megaphylogeny for angiosperms as a whole was assembled with molec-ular sequences for more than 55,000 species. Using a method that detects local shifts in diversifi-cation rates based on the distribution of species richness among tree terminals (62), they detectedapproximately 2,700 shifts across the full phylogeny, although only 16 remained after a highlyconservative Bonferroni correction. These shifts were broadly distributed across the tree, with atendency to be embedded within major named clades rather than at their origin (with similar re-sults obtained using the backbone phylogenies). These results reinforce the view that the trait andecological shifts driving higher rates of diversification have not generally been the synapomorphiesused by systematists to define the major clades of angiosperms. Nevertheless, the traits (in particu-lar, floral traits) that unite major clades of angiosperms have intrigued systematists, providing a longhistory of study of the candidate morphological key floral innovations described in the next section.

2.2. Key Floral Innovations in Angiosperms

We use the term key innovation in its restricted, contemporary macroevolutionary sense, definedas a trait that positively and significantly influences net diversification rates, but we acknowledgethat other definitions exist (29, 53). Because of the important functional role that flowers have inangiosperm diversification, much attention has focused on floral traits and their association withbroad-scale patterns of species richness, which we review here.

Floral bilateral symmetry, often synonymized with zygomorphy, is one of the most-studiedand most-reviewed floral traits from many perspectives, including developmental, genetic,


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morphological, and macroevolutionary (e.g., References 13, 20, 28, 47, 115). Because zygomor-phy has evolved repeatedly [more than 130 independent times according to Reyes et al. (115)] andcharacterizes some of the most species-rich clades in angiosperms, including Faboideae and Orchi-daceae, it remains one of the most-studied candidate floral key innovations. By restricting the angleat which animal pollinators can approach, possibly land, and interact with a flower, zygomorphymay have led to both increased specialization (and therefore reproductive isolation) and pollina-tion efficiency, providing a mechanistic explanation for increased speciation rates (13). However,zygomorphy may also lead to increased extinction rates in the longer term because of the risksassociated with pollinator specialization. Using sister-clade comparisons, Sargent (122) showedthat zygomorphy was associated with species-rich clades of angiosperms. Vamosi & Vamosi (147)also tested the question by using phylogenetic regressions and found that floral symmetry signif-icantly contributes to tree imbalance in angiosperms. However, the approaches taken by Sargent(122) and Vamosi & Vamosi (147) require simplifications and assumptions about character ho-mogeneity within large taxonomic units, whereas there is much more variation in floral symmetryat all taxonomic scales than was previously recognized and many reversals (at least 69) (115). Inparticular, the effect of zygomorphy was considered equivocal in a subsequent study (63), withstatistical support for higher species richness in zygomorphic taxa depending on the exact choiceof sister clade and the fuzzy categorization of trait data. As an illustration of the problems that canarise with trait definitions, the highly speciose Asteraceae family can be considered zygomorphic,as are its ray florets, or actinomorphic (i.e., radially symmetric), as are its inflorescences and discflorets. The appropriate choice depends on the functional role(s) that one assumes about a trait.

Moving beyond sister-species comparisons, the Binary State Speciation and Extinction (BiSSE)model and its derivatives (74) (see Figure 2 and the sidebar titled Summary of Trait-IndependentMethods to Identify Shifts in Diversification Rates) were developed specifically to test the impactof a binary trait on diversification rates while accounting for the full phylogeny and distributionof a trait among its tips (36, 73). This method has been applied to the family Proteaceae (approx-imately 1,700 species), which is an interesting, moderately sized model system for studying theevolution of floral symmetry because zygomorphy originated independently 10–18 times withinthe clade (14). Although zygomorphy increased both speciation and extinction rates, BiSSE failedto detect a significant impact of floral symmetry on the net diversification rate (the rate at whichspeciation exceeds extinction) (115). Additional studies are needed to confirm whether the patternshighlighted by Sargent (122) and Vamosi & Vamosi (147) can indeed be explained in other groupsof angiosperms by a generalized positive impact of zygomorphy on net diversification rates and todisentangle the effects of the trait on speciation and extinction.

Among other floral traits, fusions of parts, in particular the congenital fusion of carpels (syn-carpy) and of petals (sympetaly), have been proposed as major key innovations within angiosperms(4, 27, 32). Syncarpy is characteristic of the majority of monocots and eudicots, and it is thoughtto be advantageous over apocarpy (free carpels) by providing a common transmitting tissue forpollen tube growth, favoring pollen competition, and allowing the evolution of drupes and nuts asa result of selection from animal dispersers (4, 27, 30, 32). The phylogenetic pattern of syncarpyin angiosperms has been evaluated independently in various studies, identifying 2–17 indepen-dent transitions in angiosperms (4, 32). Sympetaly is characteristic of most of the Asteridae clade,including some of the most species-rich orders (Asterales, Gentianales, Lamiales, Solanales), butit also evolved repeatedly elsewhere in angiosperms (29, 32, 123). Sympetaly is thought to beadvantageous because it allows for increased architectural stability and, at the same time, allowsfor large variation in floral size and floral tube lengths. This variation is well documented to haveallowed for increased reproductive isolation and pollinator diversification (29). More generally,the close arrangement among floral organs of the same kind or of different kinds (e.g., between

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Pentamery:consisting of floralparts in fives; acommon trait inPentapetalae withincore eudicots

stamens and petals) has been proposed as a major innovative process in angiosperm evolution,leading to highly specialized, but efficient, pollination strategies (29–32). With the exception offloral symmetry and the recent study by O’Meara et al. (90), discussed further below in Section 4,there have been virtually no formal analyses of the impact of any of the above-described floral traitson species diversification at the scale of angiosperms as a whole and, therefore, these hypothesesremain to be broadly tested.

Other floral traits usually considered to be key innovations include perianth differentiation(into sepals and petals), nectar spurs, pentamery, polyandry (i.e., a high number of stamens), andinferior ovaries (29–32). For some of these, the hypothesis that they are key innovations arisesmerely from their high frequency among extant angiosperms (e.g., pentamery) rather than from amechanistic link to speciation or extinction, or both, which remains unclear. For others, especiallynectar spurs, the innovation is consistent but localized to a few families and, when it does evolve,it appears to be labile and readily reversible (30, 48, 63). Patterns of this sort point toward theinnovation (i.e., restricting the suite of pollinators) depending on the context (e.g., geographicalor ecological) in which it evolves (9), as we discuss in Section 4.

3. GENOMIC AND GEOGRAPHICAL INFLUENCES ON ANGIOSPERMDIVERSIFICATION

3.1. Whole-Genome Duplications in the Evolutionary History of Angiosperms

Among the traits considered thus far, polyploidy is the trait that has received the most attentionwith regard to its possible effects on diversification patterns in plants. Polyploidization events caninvolve hybridization between two species (allopolyploidy) or manifest from genome duplicationsof a single species (autopolyploidy). Over the long term, polyploidization could spur shifts in lifehistory traits, ecological tolerances, and interactions with herbivores and pollinators (69, 109,110, 130, 141). Yet early generation polyploids suffer from reduced fertility, exhibit low geneticvariability, and are faced with an initial demographic hurdle (68, 110). Polyploidy may furtherheighten extinction risk if adaptive changes are masked by multiple alleles and less able to spreaddue to selection (139). Thus, although polyploids are known to be widespread, with 30–40% offlowering plant species having polyploidized since the origin of their genus (137, 157), there hasbeen extensive debate about whether polyploidy is little more than evolutionary noise, arisingrepeatedly but often resulting in an evolutionary dead end (46, 91, 129, 138, 152). During the pasttwo decades, the emergence of sequencing technologies and the development of computationalgenomics tools have unveiled an extensive history of polyploidization in the form of ancient whole-genome duplications among seed plants (59, 60, 151), with some of these being inferred at the baseof particularly species-rich groups (135). Genomic analyses have further revealed extensive changesin genome organization following whole-genome duplication, such as changes in gene familydynamics and in the transcriptome that together could result in neo- and subfunctionalizationand, eventually, in new phenotypes (71, 95). These discoveries have resulted in polyploidy beingviewed as a key innovation that could drive evolutionary novelty and speciation (25, 135).

Importantly, neither the high prevalence of polyploids among extant taxa nor the multiplerounds of ancient whole-genome duplications detected in the ancestry of most plant genomescan support or refute the hypothesis that polyploidy contributes to evolutionary success becauseboth could be explained by high rates of polyploid formation. Indeed, using a quantitative modelfor the evolution of ploidy levels, Meyers & Levin (85) demonstrated that a high abundance ofpolyploidy is inevitable—simply because of the high frequency of polyploid formation coupledwith the slow reversal to the diploid state—and, thus, the frequency of polyploids and ancient


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whole-genome duplication events can be explained without invoking any polyploid advantage.Scarpino et al. (125) extended this model to allow for differential speciation rates of polyploid anddiploid lineages. By fitting this model to 60 angiosperm genera, the authors obtained statisticalsupport for a polyploid diversification disadvantage compared with their diploid congeners. Thus,Scarpino et al. (125) concluded that polyploids are common not because of any short- or long-termadvantage, but simply because they arise frequently through polyploidization (96, 144).

The results of Meyers & Levin (85) and Scarpino et al. (125) were obtained by fitting theirmodel’s parameters to per-genus estimates of species richness at each ploidy level while ignor-ing within-genus phylogenetic relationships. Thus, these models lacked the ability to distinguishbetween the effect of speciation and that of extinction, and they could not differentiate betweena single polyploidization event that resulted in a diverse polyploid clade and multiple indepen-dent polyploidization events, each resulting in few descendants. Nevertheless, similar conclusionswere observed by Mayrose et al. (82), who applied phylogenetic approaches to a set of 63 plantgroups (mostly genera). In that analysis, ploidy levels were first inferred using chromEvol (81),and ploidy-dependent diversification rates were inferred using the BiSSE model (Figure 2). Thismeta-analysis demonstrated a strong signal for lower diversification rates of polyploid lineages.Using an extension to the BiSSE model (79) that can differentiate between speciation events thatinvolve polyploidization and those that do not, the higher overall speciation rate of diploids wasbest explained by diploids having greater access to a mechanism of speciation via polyploidy thando neopolyploids. Although the analyses of Mayrose et al. (82) and Scarpino et al. (125) werebased on distinct methodologies and mostly on nonoverlapping data sets, they were still based ona relatively low percentage of angiosperm diversity and, thus, should be viewed with caution untilapplied more broadly (136). Future investigations will also further benefit from a more thoroughcharacterization of the context-dependent effects of polyploidy (e.g., auto- versus allopolyploidy,effects in herbaceous versus woody taxa). A recent literature survey conducted by Barker et al. (6)suggested that the formation rate of autopolyploids is expected to exceed that of allopolyploids, yetthe frequencies of these two types were inferred to be roughly the same among contemporary planttaxa. This implies that the merging of two distinct genomes may provide allopolyploids with impor-tant advantages in terms of establishment and persistence, possibly due to greater niche divergencefrom diploid progenitors and increased genetic variability. Whether these advantages extend todifferences in diversification rates over longer evolutionary time frames has yet to be explored.

Even considering that during short evolutionary timescales polyploids suffer lower evolution-ary success than related diploids, it remains possible that the potential long-term advantages ofpolyploidy would become apparent at deeper timescales. Thus, particularly fit polyploid lineagesthat overcame the initial demographic hurdle and succeeded in diverging from their progenitors ingeographical and phenotypic attributes could then radiate, potentially aided by the greater geneticvariability conferred by genome duplication. For example, Schranz et al. (128) suggested that thepositive effects of polyploidy on diversification manifest only following a lag period, thus allowinggenome stabilization through diploidization, novel key traits to evolve, and the buildup of geneticdiversity. Some anecdotal support for this hypothesis exists, still at relatively shallow evolution-ary timescales [e.g., in Veronica (84) and Brassicaceae (49)], warranting further investigation topinpoint the conditions that promote species radiations after whole-genome duplication.

Tank et al. (140) evaluated the link between whole-genome duplications in angiosperms andincreased diversification. Using a set of dated family-level trees derived from more than 1,000bootstrap replicates, they identified significant diversification shifts on phylogenetic branches,identifying the best fit model with MEDUSA (1; see also the sidebar titled Summary of Trait-Independent Methods to Identify Shifts in Diversification Rates). Diversification rate shiftswere distributed heterogeneously across the tree, showing a pattern of nested radiations. Few

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diversification increases were exactly associated with whole-genome duplications, but a significantnumber of shifts were placed up to three nodes downstream of six well-characterized whole-genome duplications, providing initial support for the radiation lag-time hypothesis (128). Yetthis association could be due to the greater availability of genomic data in species-rich clades thatallows for reliable detection of whole-genome duplications, and future studies should account fordifferences across the tree in the power to detect whole-genome duplications.

3.2. Geographical Patterns in Angiosperm Diversification

Plant diversity, like that of most other taxonomic groups, peaks in the tropics (39), where climaticconditions are seasonably stable, and declines toward the temperate and polar zones. Althoughsome studies have indicated that tropical clades experience higher diversification rates (23, 56, 57),others have argued that higher speciation rates are observed in temperate clades following a rangeshift from the tropics (64). Thus, lineages with temperate affinities are generally younger and nestedwithin older, more tropical lineages (64); this latter pattern parallels some analyses performed inbirds (154) and mammals (118). Overall, much of the latitudinal biodiversity gradient appears tostem from stable climates producing lowered extinction rates in the tropics combined with thegreater historical geographical coverage of tropical biomes (e.g., References 16, 19).

New evidence suggests that there is intercontinental variation in the diversification differencesobserved between tropical and nontropical lineages, with only the Neotropics observed as animportant engine of species formation (2). Other researchers have noticed that diversification ratesare particularly high for lineages in tropical mountain ranges (52, 66, 83, 101, 142), suggestingthat diversification rates may rise in areas with steep gradients in temperature and rapid shifts inspecies communities. Typically, analyses do not include elevational topography as well as latitudewhen examining clade diversification, and future studies should attempt to tease apart latitudinaland altitudinal biodiversity gradients in plants.

One intriguing example of the interplay among environment, geography, and gene flow dis-ruptions comes from geographical patterns of polyploidization. As noted above, genome doublingoften results in reproductive isolation between the polyploid descendant lineage and its progen-itor(s) and, thus, serves to drive the formation of new species (160). Thus, the observation ofhigher speciation rates in northern or alpine areas may be related to the observation of higherrates of polyploidization in these regions (10, 145), with polyploidy generating reproductive andecological differences that allow new species to colonize and persist in harsh new environments.

Species richness also varies with geographical aspects beyond temperature and humidity, par-ticularly aspects related to population connectivity. Adaptive radiations in angiosperms are knownin lineages that occur in island archipelagos (5) or in sky island formations in mountainous regions(15, 83). Other studies have found patterns of high speciation rates in dry Mediterranean habitats(12, 43, 114). Dry habitats may not be uniformly dry, and spatial heterogeneity in water availabilityor soil nutrients may provide the necessary impetus to elevate speciation rates (e.g., Reference 124).

4. MECHANISMS UNDERLYING PATTERNS OF ANGIOSPERMDIVERSIFICATION

One of the greatest challenges in understanding the mechanisms underlying variation in diver-sification rates is that alternative processes, not studied, may actually drive trait shifts and di-versification rates (73, 106). Although it is impossible to know whether all salient features areincluded in a macroevolutionary analysis, accounting for multiple traits makes it more likely thatkey innovations will be correctly identified. Multitrait analyses also make it possible to detect


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cases in which speciation and extinction depend on key trait combinations (93). One example isthe study by O’Meara et al. (90), who analyzed the joint effect on diversification of six floral traitsscored across a random sample of 500 species of angiosperms. They found that the combina-tion of corolla presence, zygomorphy, and low stamen number acted as a key innovation at thescale of angiosperms more than any one of these traits alone. This study is especially importantbecause botanists have long held the view that floral traits are not independent (hence the termfloral syndrome), and evolutionary correlations among floral traits have indeed been found to besignificant (e.g., References 55, 123). Although the study by O’Meara et al. (90) is a major stepin the direction of analyzing trait interactions, it required assigning the same diversification rateparameters to groups of traits, as well as further simplifications of the transition patterns betweenstates, thereby reducing the massive number of parameters that would be needed in a full model.Further, it drew conclusions from a comparatively small sample of angiosperm species. In the nextsection, we discuss the challenges that need to be addressed and some recent progress made inexamining the pluralistic triggers to angiosperm diversification.

4.1. The Context Dependence of Trait Transitions

Before considering the impact of multiple traits on diversification, we first consider studies inves-tigating the context—morphological, geographical, genomic—within which trait transitions arelikely to occur. Models examining the evolution of traits across a phylogeny have been developedto test explicitly whether traits evolve independently or in a correlated fashion, for both discrete(51, 70, 97, 99, 100, 126) and continuous (98, 126) traits. These methods have been used to examinethe correlated evolution of a wide variety of features—such as petal microstructure and pollinatortype (92), the presence of particular genes, and the ability of a pathogen to infect woody plants(89)—and between traits and geographical presence or absence in different regions (40, 159).

Although these methods cannot prove causation, the discrete-trait models can also be usedto infer how the state of a trait influences transition patterns among other traits. For example,in analyzing the correlated evolution between the environment and C3 and C4 photosyntheticpathways, Osborne & Freckleton (94) found no evidence that C4 grasses were more likely to arisein arid habitats, but C4 grasses, once evolved, were more likely to switch to arid environments,providing a novel explanation for the observed correlation between C4 grasses and dry habitats.Similarly, analyses of floral color and autumn leaf color in the euphorbia genus Dalechampia and inthe maple genus Acer not only found these traits to be correlated but also found that changes in leafcolor tended to occur first, suggesting that pigments elsewhere in the plant (e.g., leaf anthocyanins)are more directly selected and subsequently incorporated in flowers (3). Other traits linked to highdiversification rates may also act indirectly by enabling further trait or range shifts. For example,trees with small conduits (xylem vessels and tracheids) have fewer fitness costs associated withfreezing temperatures and are more likely to colonize cold environments (159). Thus, such traitsact as preadaptations that allow niche expansion (Table 1).

4.2. Constraints of Trait Evolution and Their Influence on AngiospermDiversification

Many of the morphological features thought to represent key innovations may not be the only,or even the primary, cause of diversification rate shifts among angiosperms. Instead, unstudiedtraits or trait–environment combinations may spur speciation (9). Thus, one must always accountfor the possibility that correlated traits are not causatively linked to diversification, but are indi-rectly associated through other traits (73). Trait associations with speciation and extinction are

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particularly pernicious because any process that perturbs the shape of a phylogeny but that is notmodeled could cause a trait to appear to be associated with faster or slower diversifying cladesby chance alone (35, 106). Analyzing combinations of influential forces simultaneously is compu-tationally difficult and depends on whether the traits are binary, quantitative, or geographical innature, or a combination of these, but phylogenetic approaches are becoming increasingly avail-able to tease apart multiple factors. In particular, the basic BiSSE approach (Figure 2) has beenextended to account for missing taxa (36), traits with more than two states (MuSSE) (35), multi-ple traits (MuSSE) (35), quantitative traits (QuaSSE) (34), trait changes at the time of speciation(cladogenesis or ClaSSE) (41, 79), geography as a trait (GeoSSE) (43), and unstudied or hiddencharacters that might also be influencing diversification (HiSSE) (8) (see Table 1 for examples ofstudies). The HiSSE model allows one to assess whether a focal trait of interest is able to accountfor the data, given that other processes may also be affecting diversification and assuming thatthese other processes can be adequately described by the evolution of a binary hidden character.

To overcome unjustified conclusions and to determine whether a trait has a consistent effect ondiversification, researchers should ideally perform analyses on multiple data sets, allowing conclu-sions to be drawn based on the preponderance of evidence (106). For example, in an analysis exam-ining the association between separate sexes and diversification, some clades showed strong signalsbetween dioecy and higher diversification (Dodonaea, Fragaria, Galium, and Sidalcea), but othersshowed the reverse (Pilea) (119). By examining many different clades, it became clear that dioecydoes not generally facilitate or hamper diversification. This suggests that the significant results insome clades may have been spurious or, alternatively, could be clade specific, potentially dependenton the ecological context or on the state of other traits. To investigate this possibility, Sabath et al.(119) examined a number of traits that are known to be associated with dioecy, but they were unableto identify a context in which dioecy is repeatedly associated with low (or high) diversification.

Similarly, in the study by Mayrose et al. (82), BiSSE was performed on multiple clades in an at-tempt to disentangle polyploidy from other traits and to avoid spurious correlations. Nevertheless,repeating analyses in multiple clades only helps to separate a trait, such as polyploidy, from traitsthat happen to co-occur in any one clade due to chance. However, polyploidy may be causallyassociated with other traits, which, in turn, are driving the observed diversification patterns. Forexample, polyploidy is repeatedly associated with self-fertilization and asexual reproduction (109,117), which reduce mating with related diploids (lessening the minority cytotype disadvantage) andincrease the establishment success of polyploids (111); but, on a longer timescale, these associatedtraits may be the ultimate cause of the lower diversification rates attributed to polyploidy (as seen,for example, in self-compatible plants) (42). Additionally, it is possible that the high extinction riskof recently formed polyploids is driven by ecological associations between polyploidy and extremeor disturbed environments (10, and references within).

5. EXTINCTION PATTERNS AND ANGIOSPERM DIVERSIFICATION

5.1. Macroevolutionary Patterns of Extinction

Diversification rate shifts can be caused by changes in speciation rate, extinction rate, or both.Unfortunately, there is generally less power to detect the effect of a trait on these distinct processesthan on the net diversification rate (Figure 1). In particular, there is often low power to estimateextinction rates from phylogenies (74), and extinction rate estimates tend to be more sensitive toadditional traits and processes that are not explicitly incorporated within a model (103).

Nevertheless, some traits have been associated with higher or lower extinction rates by exam-ining the placement of traits on phylogenetic trees (Figure 1). If a trait is associated with higher


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extinction rates, it will often appear only at the tips of trees (i.e., the trait will exhibit what has beencoined as tippiness) (11) because young lineages have yet to experience much extinction. UsingBiSSE, Goldberg et al. (42) traced shifts between self-compatibility and incompatibility across thenightshade family (Solanaceae) and found consistent evidence that self-incompatibility increaseddiversification rates. Moreover, this effect was not due to a lowered speciation rate (indeed, self-compatible species exhibited higher rates of speciation), but rather self-compatibility more thandoubled the rate of extinction. Other studies have found that a large range size buffers speciesfrom extinction (149) and that biotically dispersed lineages tend to have both larger ranges andlower extinction rates (67).

Beyond phylogenetic analyses, many of our insights about plant extinction come from the moreclassical toolbox of paleontology (18). For example, studies suggest that herbaceous clades wererelatively unaffected by the Cretaceous–Paleogene mass extinction (153). Some basal angiospermclades at high latitudes (156) withstood this mass extinction; yet another study suggests that highlatitude clades suffer frequent glaciation episodes and, thus, are often severely impacted by periodicextinction (58).

Interestingly, many of the ancient whole-genome duplications detected in extant plant genomesare not distributed uniformly across the angiosperm phylogeny, but rather are clustered aroundthe Cretaceous–Tertiary boundary (33, 150), a period characterized by environmental instabilityand the extinction of a substantial fraction of the Earth’s flora. This intriguing finding suggestsan adaptive advantage for duplicated genomes, endowing polyploids with the broader phenotypicplasticity needed to overcome periods of environmental upheavals. Yet as discussed by Vannesteet al. (150), this pattern might also be explained by neutral processes, such as the increased for-mation of unreduced gametes under stressful and fluctuating environmental conditions or theoverall reduction of population sizes that could mitigate the minority cytotype disadvantage facedby polyploids under normal conditions. Furthermore, Freeling (38) has argued that the overabun-dance of dated paleopolyploidy events around the Cretaceous–Tertiary boundary is a hitchhikingeffect that was driven by selection for reduced sex, which allowed polyploids to hide out duringperiods of mass extinctions. Future work examining other mass extinction events and their impactson plant trait distributions, such as polyploidy and mating systems, will shed further light on thetraits that have historically increased or decreased extinction risk.

5.2. The Fate of Flowering Plants in the Anthropocene

Historical extinction rate indicators (e.g., small range size, low dispersal) may also predict present-day extinction risk. To the extent that they do, studies that estimate past diversification and extinc-tion rates can help guide conservation prioritization (50). Climate change scenarios indicate thatentire clades could be at risk when environmental niche conservatism for traits such as floweringtime is strong (155). Extinction risk from climate change may have more to do with which plantclades occupy regions forecast to experience large differences in environmental conditions andwhether these clades are endemic to the region (45).

Although no known plant trait offers protection from extinction in all contexts, the imbalance ofthe angiosperm phylogenetic tree suggests that traits that evolved more recently (in the Tertiary)(76) are more adapted to recent environmental conditions than older lineages. This pattern likelycontributes an explanation to why estimates of species’ ages have been used as predictors of globaldecline (148), accounting for 15% of variation in extinction risk (21), with older lineages accountingfor higher extinction risk (26). Species’ age and evolutionary uniqueness are now metrics beingincorporated into conservation policies designed for mammals and birds (such as the EDGEprogram) (54), but they have not yet been applied to flowering plants.

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Although species in older clades may be subject to higher extinction risks due to traits that areadaptive for historical environmental conditions, species of recent origin in rapidly diversifyingclades may also be at risk. Many species designated as being at risk of extinction have only asmall area of occupancy (72), yet the extent to which range distribution is determined by age andhistorical contingency is just beginning to be explored (24). Instances of rapid cladogenesis havebeen detected in some fairly young lineages (in Lupinus, shifts to elevated diversification occurred2.7 to 6.5 Mya) (26). Endemism has also been associated with young lineages (less than 6 millionyears old) (83), suggesting that rapid speciation may be integral to the appearance of rare speciesthat we rank as high priority species for assessment. To our knowledge, few comparisons existof whether at-risk species (e.g., those with limited extent of occurrence) are the result of pastrapid diversification rates, but diversification research could be used to reveal habitats that elevatespeciation rate (and the frequency of rare species). Such studies will greatly add to the emergingtoolbox used for conserving the most important representatives of the remarkable evolutionaryradiations of flowering plants.

SUMMARY POINTS

1. Flowering plant evolution has involved numerous morphological transitions, yet shiftsin diversification rates do not appear to be consistently coincident with the adaptation ofthese key innovations.

2. Angiosperms have transitioned frequently in sexual system and at the ploidy level, yetthe effect of these traits is not consistent and may depend on whether the shift occurredin conjunction with shifts in other traits.

3. Dispersal to new habitats (open, dry, or alpine) appears to be important in spurringdiversification and can favor certain morphological adaptations.

4. Recent findings that extinction rates may be higher in rapidly diversifying clades relateto the amount of evolutionary history in jeopardy due to anthropogenic extinction.

FUTURE ISSUES

1. Better methods are required to detect and identify confounding factors that affect diver-sification rate heterogeneity (especially in cases in which key innovations arose once or afew times); HiSSE (the Hidden State Speciation and Extinction model) provides a goodbeginning for this endeavor, but it is not necessarily the most powerful approach.

2. Another challenge in the development of analytical tools that is particularly relevantto the analysis of plant clades is the effect of reticulated evolution on diversificationanalyses. Although some approaches consider alternative topologies and, thus, accountfor phylogenetic uncertainty, all methods are firmly grounded within a phylogeneticframework that assumes strictly bifurcating branches and, thus, ignores the possibility ofhybridization and introgression.

3. A known confounding factor that has been well discussed but has not been tackled is therelative contribution to macroevolutionary patterns of genome duplication per se andthat of hybridization. This task first necessitates distinguishing between polyploidiza-tion events that involve hybridization between two species (allopolyploidy) and genomeduplications of a single species (autopolyploidy), yet tools for this step are lacking.


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DISCLOSURE STATEMENT

The authors are not aware of any affiliations, memberships, funding, or financial holdings thatmight be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS

This work was funded by NSERC Discovery Grants to S.P.O. and J.C.V., and grants to I.M. fromNSF-BSF Environmental Biology (1655478) and the Israel Science Foundation (ISF 961/2017).

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RELATED RESOURCES

The 1KP project, https://sites.google.com/a/ualberta.ca/onekp/: With the upcoming releaseof genomic data from 1,000 species of plants, this resource will allow for a more detailedpicture of the association between traits, such as polyploidization, and diversification shifts

The IUCN Red List of Threatened Species, http://www.iucnredlist.org: The list describesflowering plant clades and, therefore, which ecosystems and which traits are at risk

State of the World’s Plants, https://stateoftheworldsplants.com: Tools are being developed topredict which species and ecosystems will be common in future environments

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https://sites.google.com/a/ualberta.ca/onekp/

http://www.iucnredlist.org

https://stateoftheworldsplants.com

PP69_FrontMatter ARI 5 April 2018 9:11

Annual Review ofPlant Biology

Volume 69, 2018

Contents

My Secret LifeMary-Dell Chilton � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Diversity of Chlorophototrophic Bacteria Revealed in the Omics EraVera Thiel, Marcus Tank, and Donald A. Bryant � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �21

Genomics-Informed Insights into Endosymbiotic Organelle Evolutionin Photosynthetic EukaryotesEva C.M. Nowack and Andreas P.M. Weber � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �51

Nitrate Transport, Signaling, and Use EfficiencyYa-Yun Wang, Yu-Hsuan Cheng, Kuo-En Chen, and Yi-Fang Tsay � � � � � � � � � � � � � � � � � � � � �85

Plant VacuolesTomoo Shimada, Junpei Takagi, Takuji Ichino, Makoto Shirakawa,

and Ikuko Hara-Nishimura � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 123

Protein Quality Control in the Endoplasmic Reticulum of PlantsRichard Strasser � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 147

Autophagy: The Master of Bulk and Selective RecyclingRichard S. Marshall and Richard D. Vierstra � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 173

Reactive Oxygen Species in Plant SignalingCezary Waszczak, Melanie Carmody, and Jaakko Kangasjarvi � � � � � � � � � � � � � � � � � � � � � � � � � � 209

Cell and Developmental Biology of Plant Mitogen-Activated ProteinKinasesGeorge Komis, Olga Samajova, Miroslav Ovecka, and Jozef Samaj � � � � � � � � � � � � � � � � � � � � � 237

Receptor-Like Cytoplasmic Kinases: Central Players in Plant ReceptorKinase–Mediated SignalingXiangxiu Liang and Jian-Min Zhou � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 267

Plant Malectin-Like Receptor Kinases: From Cell Wall Integrity toImmunity and BeyondChristina Maria Franck, Jens Westermann, and Aurelien Boisson-Dernier � � � � � � � � � � � � 301

Kinesins and Myosins: Molecular Motors that Coordinate CellularFunctions in PlantsAndreas Nebenfuhr and Ram Dixit � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 329

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The Oxylipin Pathways: Biochemistry and FunctionClaus Wasternack and Ivo Feussner � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 363

Modularity in Jasmonate Signaling for Multistress ResilienceGregg A. Howe, Ian T. Major, and Abraham J. Koo � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 387

Essential Roles of Local Auxin Biosynthesis in Plant Developmentand in Adaptation to Environmental ChangesYunde Zhao � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 417

Genetic Regulation of Shoot ArchitectureBing Wang, Steven M. Smith, and Jiayang Li � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 437

Heterogeneity and Robustness in Plant Morphogenesis: From Cellsto OrgansLilan Hong, Mathilde Dumond, Mingyuan Zhu, Satoru Tsugawa,

Chun-Biu Li, Arezki Boudaoud, Olivier Hamant, and Adrienne H.K. Roeder � � � � � � 469

Genetically Encoded Biosensors in Plants: Pathways to DiscoveryAnkit Walia, Rainer Waadt, and Alexander M. Jones � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 497

Exploring the Spatiotemporal Organization of Membrane Proteins inLiving Plant CellsLi Wang, Yiqun Xue, Jingjing Xing, Kai Song, and Jinxing Lin � � � � � � � � � � � � � � � � � � � � � � � 525

One Hundred Ways to Invent the Sexes: Theoretical and ObservedPaths to Dioecy in PlantsIsabelle M. Henry, Takashi Akagi, Ryutaro Tao, and Luca Comai � � � � � � � � � � � � � � � � � � � � � � 553

Meiotic Recombination: Mixing It Up in PlantsYingxiang Wang and Gregory P. Copenhaver � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 577

Population Genomics of Herbicide Resistance: Adaptation viaEvolutionary RescueJulia M. Kreiner, John R. Stinchcombe, and Stephen I. Wright � � � � � � � � � � � � � � � � � � � � � � � � � 611

Strategies for Enhanced Crop Resistance to Insect PestsAngela E. Douglas � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 637

Preadaptation and Naturalization of Nonnative Species: Darwin’s TwoFundamental Insights into Species InvasionMarc W. Cadotte, Sara E. Campbell, Shao-peng Li, Darwin S. Sodhi,

and Nicholas E. Mandrak � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 661

Macroevolutionary Patterns of Flowering Plant Speciationand ExtinctionJana C. Vamosi, Susana Magallon, Itay Mayrose, Sarah P. Otto,

and Herve Sauquet � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 685

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When Two Rights Make a Wrong: The Evolutionary Genetics ofPlant Hybrid IncompatibilitiesLila Fishman and Andrea L. Sweigart � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 707

The Physiological Basis of Drought Tolerance in Crop Plants:A Scenario-Dependent Probabilistic ApproachFrancois Tardieu, Thierry Simonneau, and Bertrand Muller � � � � � � � � � � � � � � � � � � � � � � � � � � � � 733

Paleobotany and Global Change: Important Lessons for Species toBiomes from Vegetation Responses to Past Global ChangeJennifer C. McElwain � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 761

Trends in Global Agricultural Land Use: Implications forEnvironmental Health and Food SecurityNavin Ramankutty, Zia Mehrabi, Katharina Waha, Larissa Jarvis,

Claire Kremen, Mario Herrero, and Loren H. Rieseberg � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 789

Errata

An online log of corrections to Annual Review of Plant Biology articles may be found athttp://www.annualreviews.org/errata/arplant

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macroevolutionary patterns of flowering plant speciation...

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