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Annual Review of Plant Biology Macroevolutionary Patterns of Flowering Plant and

Jana C. Vamosi,1 Susana Magallon,´ 2 Itay Mayrose,3 Sarah P. Otto,4 and HerveSauquet´ 5,6

1Department of Biological Sciences, University of Calgary, Calgary, Alberta T2N 1N4, Canada; email: [email protected] 2Instituto de Biologıa,´ Universidad Nacional Autonoma´ de Mexico,´ Ciudad de Mexico´ 04510, Mexico´ 3Department of Molecular Biology and Ecology of Plants, George S. Wise Faculty of Sciences, Tel Aviv University, Tel Aviv 69978, Israel 4Department of Zoology and the Research Centre, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada 5Laboratoire Ecologie,´ Systematique,´ ,´ Universite´ Paris-Sud, CNRS UMR 8079, 91405 Orsay, France 6National Herbarium of New South Wales (NSW), Royal Botanic Gardens and Domain Trust, Sydney, NSW 2000, Australia

Annu. Rev. Plant Biol. 2018. 69:685–706 Keywords First published as a Review in Advance on biome, conservation, dispersal, diversification, pollination, polyploidy, February 28, 2018 sexual system The Annual Review of Plant Biology is online at plant.annualreviews.org Abstract https://doi.org/10.1146/annurev-arplant-042817- Species diversity is remarkably unevenly distributed among flowering plant 040348 Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org lineages. Despite a growing toolbox of research methods, the reasons under- Access provided by University of British Columbia on 05/17/18. For personal use only. Copyright c 2018 by Annual Reviews. lying this patchy pattern have continued to perplex plant biologists for the All rights reserved past two decades. In this review, we examine the present understanding of transitions in flowering plant evolution that have been proposed to influence speciation and extinction. In particular, ploidy changes, transitions between ANNUAL REVIEWS Further tropical and nontropical biomes, and shifts in floral form have received at- Click here to view this article's online features: tention and have offered some surprises in terms of which factors influence • Download figures as PPT slides speciation and extinction rates. Mating systems and dispersal characteristics • Navigate linked references • Download citations once predominated as determining factors, yet recent evidence suggests that • Explore related articles • Search keywords these changes are not as influential as previously thought or are important only when paired with range shifts. Although range extent is an important

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

Contents 1. INTRODUCTION ...... 686 2. KEY INNOVATIONS AND DIVERSIFICATION PATTERNS OVERLONGTIMESCALES...... 690 2.1.DiversificationRateShiftsinAngiosperms...... 690 2.2.KeyFloralInnovationsinAngiosperms...... 691 3. GENOMIC AND GEOGRAPHICAL INFLUENCES ON ANGIOSPERM DIVERSIFICATION...... 693 3.1. Whole-Genome Duplications in the Evolutionary History of Angiosperms . . . . 693 3.2.GeographicalPatternsinAngiospermDiversification...... 695 4. MECHANISMS UNDERLYING PATTERNS OF ANGIOSPERM DIVERSIFICATION...... 695 4.1.TheContextDependenceofTraitTransitions...... 696 4.2. Constraints of Trait Evolution and Their Influence on Angiosperm Diversification...... 696 5. EXTINCTION PATTERNS AND ANGIOSPERM DIVERSIFICATION ...... 697 5.1. Macroevolutionary Patterns of Extinction...... 697 5.2. 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—and potentially as many as 156,000 unnamed (102)—that originated more recently than any other of vascular plants, between approximately 140 and 250 Mya (37, 77, 131). Because of this comparatively recent origin, flowering plants have been subject to fewer major mass extinction events that obscure their patterns of speciation and background extinction (131). The remarkable variation in form and habit among extant vascular plant has generated a proliferation of

Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org investigations into macroevolutionary patterns. If we examine the time line of land plant evolution Access provided by University of British Columbia on 05/17/18. For personal use only. over the entire (18), paleontological approaches find that the high species diversity of angiosperms is a result of patterns of speciation outpacing extinction early in their evolutionary history. Although this is similar to patterns exhibited by ferns (18, 127), some characteristics of flowering 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 richness values 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 due to higher speciation rates and lower extinction rates (76). Phylogenetic perspectives of speciation and extinction surged after the development of sister-group tests by Slowinski & Guyer (133). Since then, 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 Identify Shifts in Diversification Rates). Understanding the intricacies of these alternatives is critical if we are to understand when and why plants have diversified over evolutionary time (summarized in Future Issues).

a d Slope ≈ l

500

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10 Slope ≈ λ – μ

Number of lineages 5 b

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50 100 150 200 Time (millions of years) e

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(Caption appears on following page)

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Figure 1 (Figure appears on preceding page) Disentangling speciation and extinction rates. The shape of a provides information about the relative rates of speciation (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 is the same for blue and red clades [e.g., the number of lineages at time 100 (dashed lines)]. Near the present, recently formed taxa have not yet had time to go extinct and the slope approaches the speciation rate (λ) (116), which is the same for green and blue lineages (note that these clades have many more younger taxa). (e) A simulated tree in which a character affecting the speciation and extinction rates was allowed to change between green, blue, and red states at r = 0.003 (other parameters as above). Most of the youngest species are in the states with a high speciation rate ( green or blue), whereas the overall high number of red lineages may be attributed to this state being ancestral. Hence, this upturn near the present primarily provides information about the effects of a trait on speciation (λ), and the overall growth in size of a lineage provides information about the diversification rate (r).

Extinction μ1 Continuation

Transition q01

Speciation λ0

Figure 2 Schematic of the processes considered in the Binary State Speciation and Extinction (BiSSE) model for a binary trait that can exist in two states, 0 and 1, denoted in the figure by blue and red, respectively (74). The core logic of BiSSE involves calculating the probability, DNi, of observing all the data (N) that descend from a particular point on the tree, given that the trait is in state i at that point. These data include both the shape of the tree (its topology and the distribution of branch lengths) and the distribution of the character states among the extant species. As we move down a branch toward the root by an amount of time t, each possible type of transition illustrated in the figure could occur and change DN0 with probability: μ + + λ + − μ + λ +  0 t 0 q01 tDN 1 0 t2DN 0 E0 (1 ( 0 0 q01) t)DN 0 . In words, if extinction occurs extinction transition speciation continuation within this short time interval, then it is impossible to explain the data that descend from this point (hence the 0 in the first term). If a trait transition occurs to state 1, then DN1 is the probability that we observe the data (second term). If speciation occurs, then we have two daughter lineages, but assuming that we are on a nonbifurcating branch, only one of these daughter species has descendants in the present, so one daughter lineage (either one, hence the 2) must explain the data and the other must go extinct by the present, which occurs with probability E0. Finally, nothing might have happened, in which case the probability of explaining the data remains described by the variable D . Taking the limit as t goes to 0 gives us a differential Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org N0

Access provided by University of British Columbia on 05/17/18. For personal use only. equation for how DN0 changes over time, dDN0/dt. Along the way, however, we have introduced a new variable, Ei, the probability that a single species that occurs at a particular point in the past in state i fails to leave any descendants in the present. However, we can describe the dynamics of Ei just as we did above. That is, E at a point t closer to the root is: μ t1 + q tE + λ tE2 + (1 − (μ + λ + q )t)E .Ifthe 0  0  01  1 0  0  0 0 01 0 extinction transition speciation continuation lineage goes extinct in this interval, then we are done and extinction is certain (hence the 1). If there is a transition, then we have E1 as the new probability of extinction. If there is speciation, we have two lineages 2 that must both go extinct by the present (E0 , 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 gives rise 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 of speciation multiplied by the probability of observing the data that descend from each daughter. These equations are numerically solved in the diversitree package in R (35), allowing the user to determine the parameters 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 IN DIVERSIFICATION RATES

Early methods to detect changes in diversification rates in phylogenetic trees aimed to test the hypothesis that a constant 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 numbers of 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- models to a phylogenetic tree (or several trees in multiMEDUSA). MEDUSA uses stepwise Akaike information criterion, known as AIC, to select the diversification models that best fit the data. It identifies significant diversification shifts (increases or decreases) among branches of the 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 studies have shown that MEDUSA, in spite of its general utility, underestimates the number of diversification regimes in a tree when rates vary through time and has a high false discovery rate, and simulations revealed little correspondence between actual and estimated rate parameters (80, 105). Nevertheless, it still is an attractive method owing to its ability 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 estimates averaged lineage rates of speciation (λ) and extinction (μ), as well as regime models that may include variable speciation or extinction, or both, through time. Concerns have been expressed regarding BAMM’s likelihood , as it does not account for the possibility of diversification shifts along extinct branches, and about the accuracy of the posterior distribution for the number of rate shifts (86, but see 108 for a response).

In this review, we reexamine several transitions in flowering plant evolution that have been proposed to repeatedly influence speciation and extinction. Some of the transitions are marked by the appearance of morphological traits that define lineages (synapomorphies). We do not attempt to review the potential effect on species richness of specific synapomorphies of angiosperms as a whole because most of these transitions are unique and their lack of replication is a major challenge for current macroevolutionary methods (73, 90, 143; see also Figures 1 and 2 and the sidebar titled Summary of Trait-Independent Methods to Identify Shifts in Diversification Rates). Instead, our focus is on transitions—such as those among ploidy levels (157), self-compatibility (42), or mating systems (7, 44, 113)—that have recurred frequently, entailing changes to patterns of gene flow, to

Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org the fixation rate of , and to effective population size, and that may affect speciation and Access provided by University of British Columbia on 05/17/18. For personal use only. extinction rates. Synapomorphy: Geography and environment are important drivers of diversification rates as well, and we a newly evolved summarize recent insights into the mechanisms underlying the latitudinal biodiversity gradient. characteristic present Many of these advances come from exploring how traits can spur diversification under certain in an ancestor and environmental conditions yet depress diversification rates under others. This context dependency shared by its may make many of the patterns of diversification appear idiosyncratic, with signatures of past key descendants innovations that are difficult, but nevertheless exciting, to trace. Understanding the influence of Key innovation: evolutionary history on biodiversity has practical applications in helping us to preserve hot spots a novel trait that allows the subsequent of speciation, as well as pinpoint areas of future conservation concern (24). radiation and success The above factors represent the environmental (extrinsic) and morphological (intrinsic) factors of a taxonomic group hypothesized 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 in diversification 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 key innovations that have spurred rapid radiations? We explore the present understanding of these complexities below.

2. KEY INNOVATIONS AND DIVERSIFICATION PATTERNS OVER LONG TIMESCALES

2.1. Diversification Rate Shifts in Angiosperms Evolutionary radiations can often be conceptualized as bursts of high diversification that are a consequence of the evolution of a key morphological innovation, which might predict that shifts in diversification should closely mirror recognized clades, such as monophyletic families and orders (112). Many early studies investigated the unique features of angiosperms as possible factors associated with high species richness (17, 65, 139), with much of the attention focused on the positive role of biotic pollination and dispersal, as well as herbaceous growth form, yet tools were not available to determine overall patterns. We review here more recent studies that incorporate a model-based approach to diversification that is used to identify bursts in species richness that result 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 115 (but can also increase extinction rate) Fruit and dispersal syndromes MEDUSA; BAMM Animal dispersal causes species to have larger ranges 67 and lower extinction rates Whole-genome duplication ChromEvol; BiSSE Polyploids diversify less, but polyploidization is a 96, 125, 144 common speciation mechanism available to diploids Herbaceousness corHMM Originally, short generation time was thought to 159 increase divergence rate; it is now thought that smaller vasculature of trees allows niche expansion to colder climates Extrinsic conditions Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org

Access provided by University of British Columbia on 05/17/18. For personal use only. Dry habitats GeoSSE Patchy habitats (commonly found in 43 Mediterranean-like biomes) result in habitat generalization and decreased extinction Open habitats BiSSE and QuaSSE Expansion of open, dry biomes after the Miocene 93 spurred diversification of lineages with trait combinations adapted for these conditions Island archipelagos or island-like GeoSSE rates increase with population 5, 15 regions (sky islands in isolation mountainous regions)

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 A Summary 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 increased diversification rates were associated with the origin of angiosperm synapomorphies. They fitted pure birth models (no extinction) that differed in the number and placement of diversification shifts on a three-terminal phylogeny, representing the deepest split within the angiosperm clade and its outgroup, under different potential angiosperm rootings. The most likely models indicated that low 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 coincide temporally with the major expansions in angiosperm lineages. Extending this type of analysis with updated 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 clades using method-of-moments estimators based on a stochastic birth-death process that accounts for extinction. By comparing the observed diversity of major monophyletic groups to a null model in which clades diversify homogeneously through time at a rate equal to that of angiosperms as a whole, they identified a number of unexpectedly species-rich clades, indicating that diversification rates have increased independently in several groups of angiosperms. The same estimators were applied 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 >23,000 species, 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 common explanation; 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 examined diversification 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 in angiosperms. Backbone phylogenies were obtained for angiosperms as a whole and for six large clades 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 detected approximately 2,700 shifts across the full phylogeny, although only 16 remained after a highly conservative Bonferroni correction. These shifts were broadly distributed across the tree, with a tendency 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 and ecological shifts driving higher rates of diversification have not generally been the synapomorphies

Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org used by systematists to define the major clades of angiosperms. Nevertheless, the traits (in particu- Access provided by University of British Columbia on 05/17/18. For personal use only. lar, floral traits) that unite major clades of angiosperms have intrigued systematists, providing a long history 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, defined as a trait that positively and significantly influences net diversification rates, but we acknowledge that other definitions exist (29, 53). Because of the important functional role that flowers have in angiosperm diversification, much attention has focused on floral traits and their association with broad-scale patterns of species richness, which we review here. Floral bilateral symmetry, often synonymized with zygomorphy, is one of the most-studied and 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)] and characterizes 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 angle at which animal pollinators can approach, possibly land, and interact with a flower, zygomorphy may 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 risks associated with pollinator specialization. Using sister-clade comparisons, Sargent (122) showed that 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 symmetry at all taxonomic scales than was previously recognized and many reversals (at least 69) (115). In particular, the effect of zygomorphy was considered equivocal in a subsequent study (63), with statistical support for higher species richness in zygomorphic taxa depending on the exact choice of sister clade and the fuzzy categorization of trait data. As an illustration of the problems that can arise 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 disc florets. 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-Independent Methods to Identify Shifts in Diversification Rates) were developed specifically to test the impact of a binary trait on diversification rates while accounting for the full phylogeny and distribution of 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 the evolution of floral symmetry because zygomorphy originated independently 10–18 times within the clade (14). Although zygomorphy increased both speciation and extinction rates, BiSSE failed to detect a significant impact of floral symmetry on the net diversification rate (the rate at which speciation exceeds extinction) (115). Additional studies are needed to confirm whether the patterns highlighted by Sargent (122) and Vamosi & Vamosi (147) can indeed be explained in other groups of angiosperms by a generalized positive impact of zygomorphy on net diversification rates and to disentangle the effects of the trait on speciation and extinction. Among other floral traits, fusions of parts, in particular the congenital fusion of carpels (syn-

Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org carpy) and of petals (sympetaly), have been proposed as major key innovations within angiosperms Access provided by University of British Columbia on 05/17/18. For personal use only. (4, 27, 32). Syncarpy is characteristic of the majority of monocots and eudicots, and it is thought to be advantageous over apocarpy (free carpels) by providing a common transmitting tissue for pollen tube growth, favoring pollen competition, and allowing the evolution of drupes and nuts as a result of selection from animal dispersers (4, 27, 30, 32). The phylogenetic pattern of syncarpy in 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), but it also evolved repeatedly elsewhere in angiosperms (29, 32, 123). Sympetaly is thought to be advantageous because it allows for increased architectural stability and, at the same time, allows for large variation in floral size and floral tube lengths. This variation is well documented to have allowed 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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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 of floral symmetry and the recent study by O’Meara et al. (90), discussed further below in Section 4, Pentamery: there have been virtually no formal analyses of the impact of any of the above-described floral traits consisting of floral on species diversification at the scale of angiosperms as a whole and, therefore, these hypotheses partsinfives;a remain to be broadly tested. common trait in Other floral traits usually considered to be key innovations include perianth differentiation Pentapetalae within (into sepals and petals), nectar spurs, pentamery, polyandry (i.e., a high number of stamens), and core eudicots inferior ovaries (29–32). For some of these, the hypothesis that they are key innovations arises merely from their high frequency among extant angiosperms (e.g., pentamery) rather than from a mechanistic link to speciation or extinction, or both, which remains unclear. For others, especially nectar 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 the innovation (i.e., restricting the suite of pollinators) depending on the context (e.g., geographical or ecological) in which it evolves (9), as we discuss in Section 4.

3. GENOMIC AND GEOGRAPHICAL INFLUENCES ON ANGIOSPERM DIVERSIFICATION

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 attention with regard to its possible effects on diversification patterns in plants. Polyploidization events can involve hybridization between two species (allopolyploidy) or manifest from genome duplications of a single species (autopolyploidy). Over the long term, polyploidization could spur shifts in life history traits, ecological tolerances, and interactions with herbivores and pollinators (69, 109, 110, 130, 141). Yet early generation polyploids suffer from reduced fertility, exhibit low genetic variability, and are faced with an initial demographic hurdle (68, 110). Polyploidy may further heighten extinction risk if adaptive changes are masked by multiple alleles and less able to spread due to selection (139). Thus, although polyploids are known to be widespread, with 30–40% of flowering plant species having polyploidized since the origin of their genus (137, 157), there has been extensive debate about whether polyploidy is little more than evolutionary noise, arising repeatedly but often resulting in an evolutionary dead end (46, 91, 129, 138, 152). During the past two decades, the emergence of sequencing technologies and the development of computational genomics tools have unveiled an extensive history of polyploidization in the form of ancient whole-

Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org genome duplications among seed plants (59, 60, 151), with some of these being inferred at the base Access provided by University of British Columbia on 05/17/18. For personal use only. of particularly species-rich groups (135). Genomic analyses have further revealed extensive changes in genome organization following whole-genome duplication, such as changes in gene family dynamics and in the transcriptome that together could result in neo- and subfunctionalization and, eventually, in new (71, 95). These discoveries have resulted in polyploidy being viewed 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 multiple rounds of ancient whole-genome duplications detected in the ancestry of most plant genomes can support or refute the hypothesis that polyploidy contributes to evolutionary success because both could be explained by high rates of polyploid formation. Indeed, using a quantitative model for the evolution of ploidy levels, Meyers & Levin (85) demonstrated that a high abundance of polyploidy is inevitable—simply because of the high frequency of polyploid formation coupled with 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 and diploid lineages. By fitting this model to 60 angiosperm genera, the authors obtained statistical support 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-term advantage, 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 their model’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 distinguish between the effect of speciation and that of extinction, and they could not differentiate between a single polyploidization event that resulted in a diverse polyploid clade and multiple indepen- dent polyploidization events, each resulting in few descendants. Nevertheless, similar conclusions were observed by Mayrose et al. (82), who applied phylogenetic approaches to a set of 63 plant groups (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). This meta-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 that involve polyploidization and those that do not, the higher overall speciation rate of diploids was best explained by diploids having greater access to a mechanism of speciation via polyploidy than do neopolyploids. Although the analyses of Mayrose et al. (82) and Scarpino et al. (125) were based on distinct methodologies and mostly on nonoverlapping data sets, they were still based on a relatively low percentage of angiosperm diversity and, thus, should be viewed with caution until applied more broadly (136). Future investigations will also further benefit from a more thorough characterization 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, yet the frequencies of these two types were inferred to be roughly the same among contemporary plant taxa. 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 divergence from diploid progenitors and increased genetic variability. Whether these advantages extend to differences 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 of polyploidy would become apparent at deeper timescales. Thus, particularly fit polyploid lineages that overcame the initial demographic hurdle and succeeded in diverging from their progenitors in

Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org geographical and phenotypic attributes could then radiate, potentially aided by the greater genetic Access provided by University of British Columbia on 05/17/18. For personal use only. variability conferred by genome duplication. For example, Schranz et al. (128) suggested that the positive effects of polyploidy on diversification manifest only following a lag period, thus allowing genome stabilization through diploidization, novel key traits to evolve, and the buildup of genetic diversity. 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 to pinpoint the conditions that promote species radiations after whole-genome duplication. Tank et al. (140) evaluated the link between whole-genome duplications in angiosperms and increased diversification. Using a set of dated family-level trees derived from more than 1,000 bootstrap 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 shifts were 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 significant number 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). Yet this association could be due to the greater availability of genomic data in species-rich clades that allows for reliable detection of whole-genome duplications, and future studies should account for differences 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 climatic conditions are seasonably stable, and declines toward the temperate and polar zones. Although some 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 range shift from the tropics (64). Thus, lineages with temperate affinities are generally younger and nested within older, more tropical lineages (64); this latter pattern parallels some analyses performed in birds (154) and mammals (118). Overall, much of the latitudinal biodiversity gradient appears to stem from stable climates producing lowered extinction rates in the tropics combined with the greater historical geographical coverage of tropical biomes (e.g., References 16, 19). New evidence suggests that there is intercontinental variation in the diversification differences observed between tropical and nontropical lineages, with only the Neotropics observed as an important engine of species formation (2). Other researchers have noticed that diversification rates are particularly high for lineages in tropical mountain ranges (52, 66, 83, 101, 142), suggesting that diversification rates may rise in areas with steep gradients in temperature and rapid shifts in species communities. Typically, analyses do not include elevational topography as well as latitude when examining clade diversification, and future studies should attempt to tease apart latitudinal and 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 doubling often 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 of higher speciation rates in northern or alpine areas may be related to the observation of higher rates of polyploidization in these regions (10, 145), with polyploidy generating reproductive and ecological 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 known

Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org in lineages that occur in island archipelagos (5) or in sky island formations in mountainous regions Access provided by University of British Columbia on 05/17/18. For personal use only. (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 availability or soil nutrients may provide the necessary impetus to elevate speciation rates (e.g., Reference 124).

4. MECHANISMS UNDERLYING PATTERNS OF ANGIOSPERM DIVERSIFICATION 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 are included in a macroevolutionary analysis, accounting for multiple traits makes it more likely that key 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 is the study by O’Meara et al. (90), who analyzed the joint effect on diversification of six floral traits scored 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 the scale of angiosperms more than any one of these traits alone. This study is especially important because botanists have long held the view that floral traits are not independent (hence the term floral syndrome), and evolutionary correlations among floral traits have indeed been found to be significant (e.g., References 55, 123). Although the study by O’Meara et al. (90) is a major step in the direction of analyzing trait interactions, it required assigning the same diversification rate parameters to groups of traits, as well as further simplifications of the transition patterns between states, 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 next section, we discuss the challenges that need to be addressed and some recent progress made in examining 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 are likely to occur. Models examining the evolution of traits across a phylogeny have been developed to 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 examine the correlated evolution of a wide variety of features—such as petal microstructure and pollinator type (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 used to 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 photosynthetic pathways, Osborne & Freckleton (94) found no evidence that C4 grasses were more likely to arise

in 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 in the maple genus Acer not only found these traits to be correlated but also found that changes in leaf color 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 high

Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org diversification rates may also act indirectly by enabling further trait or range shifts. For example, Access provided by University of British Columbia on 05/17/18. For personal use only. trees with small conduits (xylem vessels and tracheids) have fewer fitness costs associated with freezing temperatures and are more likely to colonize cold environments (159). Thus, such traits act as preadaptations that allow niche expansion (Table 1).

4.2. Constraints of Trait Evolution and Their Influence on Angiosperm Diversification 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, unstudied traits or trait–environment combinations may spur speciation (9). Thus, one must always account for 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 not modeled could cause a trait to appear to be associated with faster or slower diversifying clades by 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 in nature, 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 been extended 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 ( or ClaSSE) (41, 79), geography as a trait (GeoSSE) (43), and unstudied or hidden characters that might also be influencing diversification (HiSSE) (8) (see Table 1 for examples of studies). The HiSSE model allows one to assess whether a focal trait of interest is able to account for the data, given that other processes may also be affecting diversification and assuming that these 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 on diversification, 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 signals between dioecy and higher diversification (Dodonaea, Fragaria, Galium,andSidalcea), but others showed the reverse (Pilea) (119). By examining many different clades, it became clear that dioecy does not generally facilitate or hamper diversification. This suggests that the significant results in some clades may have been spurious or, alternatively, could be clade specific, potentially dependent on 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 unable to 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 traits that happen to co-occur in any one clade due to chance. However, polyploidy may be causally associated with other traits, which, in turn, are driving the observed diversification patterns. For example, polyploidy is repeatedly associated with self-fertilization and asexual reproduction (109, 117), which reduce mating with related diploids (lessening the minority cytotype disadvantage) and increase the establishment success of polyploids (111); but, on a longer timescale, these associated traits 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 risk of recently formed polyploids is driven by ecological associations between polyploidy and extreme

Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org or disturbed environments (10, and references within). Access provided by University of British Columbia on 05/17/18. For personal use only.

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 processes than on the net diversification rate (Figure 1). In particular, there is often low power to estimate extinction rates from phylogenies (74), and extinction rate estimates tend to be more sensitive to additional 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 been coined as tippiness) (11) because young lineages have yet to experience much extinction. Using BiSSE, Goldberg et al. (42) traced shifts between self-compatibility and incompatibility across the nightshade family (Solanaceae) and found consistent evidence that self-incompatibility increased diversification 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 than doubled the rate of extinction. Other studies have found that a large range size buffers species from extinction (149) and that biotically dispersed lineages tend to have both larger ranges and lower extinction rates (67). Beyond phylogenetic analyses, many of our insights about plant extinction come from the more classical toolbox of (18). For example, studies suggest that herbaceous clades were relatively unaffected by the Cretaceous–Paleogene mass extinction (153). Some basal angiosperm clades at high latitudes (156) withstood this mass extinction; yet another study suggests that high latitude clades suffer frequent glaciation episodes and, thus, are often severely impacted by periodic extinction (58). Interestingly, many of the ancient whole-genome duplications detected in extant plant genomes are not distributed uniformly across the angiosperm phylogeny, but rather are clustered around the Cretaceous–Tertiary boundary (33, 150), a period characterized by environmental instability and the extinction of a substantial fraction of the Earth’s flora. This intriguing finding suggests an adaptive advantage for duplicated genomes, endowing polyploids with the broader needed to overcome periods of environmental upheavals. Yet as discussed by Vanneste et 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 the overall reduction of population sizes that could mitigate the minority cytotype disadvantage faced by polyploids under normal conditions. Furthermore, Freeling (38) has argued that the overabun- dance of dated paleopolyploidy events around the Cretaceous–Tertiary boundary is a hitchhiking effect that was driven by selection for reduced sex, which allowed polyploids to hide out during periods of mass . Future work examining other mass extinction events and their impacts on plant trait distributions, such as polyploidy and mating systems, will shed further light on the traits 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-

Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org tion rates can help guide conservation prioritization (50). Climate change scenarios indicate that Access provided by University of British Columbia on 05/17/18. For personal use only. entire clades could be at risk when environmental niche conservatism for traits such as flowering time is strong (155). Extinction risk from climate change may have more to do with which plant clades occupy regions forecast to experience large differences in environmental conditions and whether these clades are endemic to the region (45). Although no known plant trait offers protection from extinction in all contexts, the imbalance of the 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 likely contributes an explanation to why estimates of species’ ages have been used as predictors of global decline (148), accounting for 15% of variation in extinction risk (21), with older lineages accounting for higher extinction risk (26). Species’ age and evolutionary uniqueness are now metrics being incorporated into conservation policies designed for mammals and birds (such as the EDGE program) (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 are adaptive for historical environmental conditions, species of recent origin in rapidly diversifying clades may also be at risk. Many species designated as being at risk of extinction have only a small area of occupancy (72), yet the extent to which range distribution is determined by age and historical contingency is just beginning to be explored (24). Instances of rapid cladogenesis have been detected in some fairly young lineages (in Lupinus, shifts to elevated diversification occurred 2.7 to 6.5 Mya) (26). Endemism has also been associated with young lineages (less than 6 million years old) (83), suggesting that rapid speciation may be integral to the appearance of rare species that we rank as high priority species for assessment. To our knowledge, few comparisons exist of whether at-risk species (e.g., those with limited extent of occurrence) are the result of past rapid diversification rates, but diversification research could be used to reveal habitats that elevate speciation rate (and the frequency of rare species). Such studies will greatly add to the emerging toolbox used for conserving the most important representatives of the remarkable evolutionary radiations of flowering plants.

SUMMARY POINTS 1. Flowering plant evolution has involved numerous morphological transitions, yet shifts in diversification rates do not appear to be consistently coincident with the of these key innovations. 2. Angiosperms have transitioned frequently in sexual system and at the ploidy level, yet the effect of these traits is not consistent and may depend on whether the shift occurred in conjunction with shifts in other traits. 3. Dispersal to new habitats (open, dry, or alpine) appears to be important in spurring diversification and can favor certain morphological . 4. Recent findings that extinction rates may be higher in rapidly diversifying clades relate to 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 a few times); HiSSE (the Hidden State Speciation and Extinction model) provides a good beginning for this endeavor, but it is not necessarily the most powerful approach. Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org Access provided by University of British Columbia on 05/17/18. For personal use only. 2. Another challenge in the development of analytical tools that is particularly relevant to the analysis of plant clades is the effect of reticulated evolution on diversification analyses. Although some approaches consider alternative topologies and, thus, account for phylogenetic uncertainty, all methods are firmly grounded within a phylogenetic framework that assumes strictly bifurcating branches and, thus, ignores the possibility of hybridization and introgression. 3. A known confounding factor that has been well discussed but has not been tackled is the relative contribution to macroevolutionary patterns of genome duplication per se and that of hybridization. This task first necessitates distinguishing between polyploidiza- tion events that involve hybridization between two species (allopolyploidy) and genome duplications 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 that might 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. from NSF-BSF Environmental Biology (1655478) and the Israel Science Foundation (ISF 961/2017).

LITERATURE CITED 1. Alfaro ME, Santini F, Brock C, Alamillo H, Dornburg A, et al. 2009. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. PNAS 106:13410–14 2. Antonelli A, Zizka A, Silvestro D, Scharn R, Cascales-Minana˜ B, Bacon CD. 2015. An engine for global plant diversity: highest evolutionary turnover and emigration in the American tropics. Front. Genet. 6:130 3. Armbruster WS. 2002. Can indirect selection and genetic context contribute to trait diversification? A transition-probability study of blossom-colour evolution in two genera. J. Evol. Biol. 15:468–86 4. Armbruster WS, Debevec EM, Willson MF. 2002. Evolution of syncarpy in angiosperms: theoretical and phylogenetic analyses of the effects of carpel fusion on offspring quantity and quality. J. Evol. Biol. 15:657–72 5. Baldwin BG, Sanderson MJ. 1998. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). PNAS 95:9402–6 6. Barker MS, Arrigo N, Baniaga AE, Li Z, Levin DA. 2016. On the relative abundance of autopolyploids and allopolyploids. New Phytol. 210:391–98 7. Barrett SCH. 2013. The evolution of plant reproductive systems: How often are transitions irreversible? Proc. R. Soc. B 280:20130913 8. Beaulieu JM, O’Meara BC. 2016. Detecting hidden diversification shifts in models of trait-dependent speciation and extinction. Syst. Biol. 65:583–601 9. Bouchenak-Khelladi Y, Onstein RE, Xing Y, Schwery O, Linder HP. 2015. On the complexity of triggering evolutionary radiations. New Phytol. 207:313–26 10. Brochmann C, Brysting AK, Alsos IG, Borgen L, Grundt HH, et al. 2004. Polyploidy in Arctic plants. Biol. J. Linn. Soc. 82:521–36 11. Bromham L, Hua X, Cardillo M. 2016. Detecting macroevolutionary self-destruction from phylogenies. Syst. Biol. 65:109–27 12. Buerki S, Jose S, Yadav SR, Goldblatt P, Manning JC, Forest F. 2012. Contrasting biogeographic and diversification patterns in two Mediterranean-type ecosystems. PLOS ONE 7:e39377 13. Citerne HL, Jabbour F, Nadot S, Damerval C. 2010. The evolution of floral symmetry. Adv. Bot. Res.

Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org 54:85–137 Access provided by University of British Columbia on 05/17/18. For personal use only. 14. Citerne HL, Reyes E, Le Guilloux M, Delannoy E, Simonnet F, et al. 2017. Characterization of CYCLOIDEA-like genes in Proteaceae, a basal eudicot family with multiple shifts in floral symmetry. Ann. Bot. 119:367–78 15. Comes HP, Tribsch A, Bittkau C. 2008. Plant speciation in continental island floras as exemplified by Nigella in the Aegean Archipelago. Phil. Trans. R. Soc. B 363:3083–96 16. Crane PR, Lidgard S. 1989. Angiosperm diversification and paleolatitudinal gradients in Cretaceous floristic diversity. Science 246:675–78 17. Crepet WL. 1984. Advanced (constant) insect pollination mechanisms: pattern of evolution and impli- cations vis-a-vis angiosperm diversity. Ann. Mo. Bot. Gard. 71:607–30 18. Crepet WL, Niklas KJ. 2009. Darwin’s second “abominable mystery”: Why are there so many an- giosperm species? Am. J. Bot. 96:366–81 19. Crisp MD, Arroyo MTK, Cook LG, Gandolfo MA, Jordan GJ, et al. 2009. Phylogenetic biome conser- vatism on a global scale. Nature 458:754–56

700 Vamosi et al. PP69CH25_Vamosi ARI 4 April 2018 8:6

20. Cubas P. 2004. Floral zygomorphy, the recurring evolution of a successful trait. BioEssays 26:1175–84 21. Daru BH, Yessoufou K, Mankga LT, Davies TJ. 2013. A global trend towards the loss of evolutionarily unique species in mangrove ecosystems. PLOS ONE 8:e66686 22. Davies TJ, Barraclough TG, Chase MW, Soltis PS, Soltis DE, Savolainen V. 2004. Darwin’s abominable mystery: insights from a supertree of the angiosperms. PNAS 101:1904–9 23. Davies TJ, Barraclough TG, Savolainen V. 2004. Environmental causes for plant biodiversity gradients. Philos.Trans.R.Soc.B359:1645–56 24. Davies TJ, Smith GF, Bellstedt DU, Boatwright JS, Bytebier B, et al. 2011. Extinction risk and diversi- fication are linked in a plant biodiversity hotspot. PLOS Biol. 9:e1000620 25. De Bodt S, Maere S, Van de Peer Y. 2005. Genome duplication and the origin of angiosperms. Trends Ecol. Evol. 20:591–97 26. Drummond CS, Eastwood RJ, Miotto STS, Hughes CE. 2012. Multiple continental radiations and correlates of diversification in Lupinus (Leguminosae): testing for key innovation with incomplete sampling. Syst. Biol. 61:443–60 27. Endress PK. 1982. Syncarpy and alternative modes of escaping disadvantages of apocarpy in primitive angiosperms. Taxon 31:48–52 28. Endress PK. 2001. Evolution of floral symmetry. Curr. Opin. Plant Biol. 4:86–91 29. Endress PK. 2001. Origins of flower morphology. J. Exp. Zool. 291:105–15 30. Endress PK. 2006. Angiosperm floral evolution: morphological developmental framework. Adv. Bot. Res. 44:1–61 31. Endress PK. 2010. Flower structure and trends of evolution in eudicots and their major subclades. Ann. Mo. Bot. Gard. 97:541–83 32. Endress PK. 2011. Evolutionary diversification of the flowers in angiosperms. Am. J. Bot. 98:370–96 33. Fawcett JA, Maere S, Van de Peer Y. 2009. Plants with double genomes might have had a better chance to survive the Cretaceous–Tertiary . PNAS 106:5737–42 34. FitzJohn RG. 2010. Quantitative traits and diversification. Syst. Biol. 59:619–33 35. FitzJohn RG. 2012. Diversitree: comparative phylogenetic analyses of diversification in R. Methods Ecol. Evol. 3:1084–92 36. FitzJohn RG, Maddison WP, Otto SP. 2009. Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. Syst. Biol. 58:595–611 37. Foster CSP, Sauquet H, van der Merwe M, McPherson H, Rossetto M, Ho SYW. 2017. Evaluating the impact of genomic data and priors on Bayesian estimates of the angiosperm evolutionary timescale. Syst. Biol. 66:338–51 38. Freeling M. 2017. Picking up the ball at the K/Pg boundary: the distribution of ancient polyploidies in the plant phylogenetic tree as a spandrel of asexuality with occasional sex. Plant Cell 29:202–6 39. Gentry AH. 1988. Changes in plant community diversity and floristic composition on environmental and geographical gradients. Ann. Mo. Bot. Gard. 75:1–34 40. Givnish TJ, Barfuss MHJ, Van Ee B, Riina R, Schulte K, et al. 2014. , correlated and contingent evolution, and net species diversification in Bromeliaceae. Mol. Evol. 71:55–78 Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org 41. Goldberg EE, Igic´ B. 2012. Tempo and mode in plant breeding system evolution. Evolution 66:3701–9 Access provided by University of British Columbia on 05/17/18. For personal use only. 42. Goldberg EE, Kohn JR, Lande R, Robertson KA, Smith SA, Igic´ B. 2010. Species selection maintains self-incompatibility. Science 330:493–95 43. Goldberg EE, Lancaster LT, Ree RH. 2011. Phylogenetic inference of reciprocal effects between geo- graphic range evolution and diversification. Syst. Biol. 60:451–65 44. Goldberg EE, Otto SP, Vamosi JC, Mayrose I, Sabath N, et al. 2017. Macroevolutionary synthesis of flowering plant sexual systems. Evolution 71:898–912 45. Gonzalez-Orozco CE, Pollock LJ, Thornhill AH, Mishler BD, Knerr N, et al. 2016. Phylogenetic approaches reveal biodiversity threats under climate change. Nat. Clim. Change 6:1110–14 46. Grant V. 1981. Plant Speciation. New York: Columbia Univ. Press 47. Hileman LC. 2014. Trends in flower symmetry evolution revealed through phylogenetic and develop- mental genetic advances. Philos. Trans. R. Soc. B 369:20130348 48. Hodges SA, Arnold ML. 1995. Spurring plant diversification: Are floral nectar spurs a key innovation? Proc. R. Soc. B 262:343–48

www.annualreviews.org • Macroevolutionary Patterns of Flowering Plants 701 PP69CH25_Vamosi ARI 4 April 2018 8:6

49. Hohmann N, Wolf EM, Lysak MA, Koch MA. 2015. A time-calibrated road map of Brassicaceae species radiation and evolutionary history. Plant Cell 27:2770–84 50. Huang D, Goldberg EE, Roy K. 2015. Fossils, phylogenies, and the challenge of preserving evolutionary history in the face of anthropogenic extinctions. PNAS 112:4909–14 51. Huelsenbeck JP, Nielsen R, Bollback JP. 2003. Stochastic mapping of morphological characters. Syst. Biol. 52:131–58 52. Hughes C, Eastwood R. 2006. Island radiation on a continental scale: exceptional rates of plant diversi- fication after uplift of the Andes. PNAS 103:10334–39 53. Hunter JP. Key innovations and the ecology of . Trends Ecol. Evol. 13:31–36 54. Isaac NJB, Turvey ST, Collen B, Waterman C, Baillie JEM. 2007. Mammals on the EDGE: conservation priorities based on threat and phylogeny. PLOS ONE 3:e296 55. Jabbour F, Damerval C, Nadot S. 2008. Evolutionary trends in the flowers of Asteridae: Is polyandry an alternative to zygomorphy? Ann. Bot. 102:153–65 56. Jablonski D, Roy K, Valentine JW. 2006. Out of the tropics: evolutionary dynamics of the latitudinal diversity gradient. Science 314:102–6 57. Jansson R, Davies TJ. 2008. Global variation in diversification rates of flowering plants: energy vs. climate change. Ecol. Lett. 11:173–83 58. Jansson R, Dynesius M. 2002. The fate of clades in a world of recurrent climatic change: Milankovitch oscillations and evolution. Annu. Rev. Ecol. Evol. Syst. 33:741–77 59. Jiao Y, Leebens-Mack J, Ayyampalayam S, Bowers JE, McKain MR, et al. 2012. A genome triplication associated with early diversification of the core eudicots. Genome Biol. 13:R3 60. Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, et al. 2011. Ancestral polyploidy in seed plants and angiosperms. Nature 473:97–100 61. Kafer¨ J, de Boer HJ, Mousset S, Kool A, Dufay M, Marais GAB. 2014. Dioecy is associated with higher diversification rates in flowering plants. J. Evol. Biol. 27:1478–90 62. Kai MAC, Moore BR. 2002. Whole-tree methods for detecting differential diversification rates. Syst. Biol. 51:855–65 63. Kay KM, Voelckel C, Yang JY, Hufford KM, Kaska DD, Hodges SA. 2006. Floral characters and species diversification. In Ecology and Evolution of Flowers, ed. LD Harder, SCH Barrett, pp. 311–25. Oxford: Oxford Univ. Press 64. Kerkhoff AJ, Moriarty PE, Weiser MD. 2014. The latitudinal species richness gradient in New World woody angiosperms is consistent with the tropical conservatism hypothesis. PNAS 111:8125–30 65. Kiester AR, Lande R, Schemske DW. 1984. Models of and speciation in plants and their pollinators. Am. Nat. 124:220–43 66. Lagomarsino LP, Condamine FL, Antonelli A, Mulch A, Davis CC. 2016. The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae). New Phytol. 210:1430–42 67. Larson-Johnson K. 2016. Phylogenetic investigation of the complex evolutionary history of dispersal mode and diversification rates across living and fossil Fagales. New Phytol. 209:418–35 68. Levin DA. 1975. Minority cytotype exclusion in local plant populations. Taxon 24:35–43 Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org 69. Levin DA. 1983. Polyploidy and novelty in flowering plants. Am. Nat. 122:1–25 Access provided by University of British Columbia on 05/17/18. For personal use only. 70. Lewis PO. 2001. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 50:913–25 71. Li Z, Defoort J, Tasdighian S, Maere S, Van de Peer Y, De Smet R. 2016. Gene duplicability of core genes is highly consistent across all angiosperms. Plant Cell 28:326–44 72. Mace GM, Lande R. 1991. Assessing extinction threats: toward a reevaluation of IUCN threatened species categories. Conserv. Biol. 5:148–57 73. Maddison W, FitzJohn R. 2015. The unsolved challenge to phylogenetic correlation tests for categorical characters. Syst. Biol. 64:127–36 74. Maddison WP, Midford PE, Otto SP. 2007. Estimating a binary character’s effect on speciation and extinction. Syst. Biol. 56:701–10 75. Magallon´ S, Castillo A. 2009. Angiosperm diversification through time. Am. J. Bot. 96:349–65 76. Magallon´ S, Crane PR, Herendeen PS. 1999. Phylogenetic pattern, diversity, and diversification of eudicots. Ann. Mo. Bot. Gard. 86:297–372

702 Vamosi et al. PP69CH25_Vamosi ARI 4 April 2018 8:6

77. Magallon´ S, Gomez-Acevedo´ S, Sanchez-Reyes´ LL, Hernandez-Hern´ andez´ T. 2015. A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytol. 207:437–53 78. Magallon´ S, Sanderson MJ. 2001. Absolute diversification rates in angiosperm clades. Evolution 55:1762– 80 79. Magnuson-Ford K, Otto S. 2012. Linking the investigations of character evolution and species diversi- fication. Am. Nat. 180:225–45 80. May MR, Moore BR. 2016. How well can we detect lineage-specific diversification-rate shifts? A simu- lation study of sequential AIC methods. Syst. Biol. 65:1076–84 81. Mayrose I, Barker MS, Otto SP. 2010. Probabilistic models of number evolution and the inference of polyploidy. Syst. Biol. 59:132–44 82. Mayrose I, Zhan SH, Rothfels CJ, Magnuson-Ford K, Barker MS, et al. 2011. Recently formed polyploid plants diversify at lower rates. Science 333:1257 83. Merckx VSFT, Hendriks KP, Beentjes KK, Mennes CB, Becking LE, et al. 2015. Evolution of endemism on a young tropical mountain. Nature 524:347–50 84. Meudt HM, Rojas-Andres´ BM, Prebble JM, Low E, Garnock-Jones PJ, Albach DC. 2015. Is genome downsizing associated with diversification in polyploid lineages of Veronica? Bot. J. Linn. Soc. 178:243–66 85. Meyers LA, Levin DA. 2006. On the abundance of polyploids in flowering plants. Evolution 60:1198–206 86. Moore BR, Hohna¨ S, May MR, Rannala B, Huelsenbeck JP. 2016. Critically evaluating the theory and performance of Bayesian analysis of macroevolutionary mixtures. PNAS 113:9569–74 87. Morlon H, Parsons TL, Plotkin JB. 2011. Reconciling molecular phylogenies with the fossil record. PNAS 108:16327–32 88. Nee S, Holmes EC, May RM, Harvey PH. 1994. Extinction rates can be estimated from molecular phylogenies. Philos. Trans. R. Soc. B 344:77–82 89. Nowell RW, Laue BE, Sharp PM, Green S. 2016. Comparative genomics reveals genes significantly associated with woody hosts in the plant pathogen Pseudomonas syringae. Mol. Plant Pathol. 17:1409–24 90. O’Meara B, Smith S, Armbruster W, Harder L, Hardy C, et al. 2016. Non-equilibrium dynamics and floral trait interactions shape extant angiosperm diversity Proc.R.Soc.B283:20152304 91. Ohno S. 1970. Evolution by Gene Duplication. New York: Springer 92. Ojeda DI, Valido A, Fernandez´ de Castro AG, Ortega-Olivencia A, Fuertes-Aguilar J, et al. 2016. Pollinator shifts drive petal epidermal evolution on the Macaronesian Islands bird-flowered species. Biol. Lett. 12:20160022–24 93. Onstein RE, Jordan GJ, Sauquet H, Weston PH, Bouchenak-Khelladi Y, et al. 2016. Evolutionary radiations of Proteaceae are triggered by the interaction between traits and climates in open habitats. Glob. Ecol. Biogeogr. 25:1239–51 94. Osborne CP, Freckleton RP. 2009. pressures for C4 photosynthesis in the grasses. Proc. R. Soc. B 276:1753–60 95. Otto SP. 2007. The evolutionary consequences of polyploidy. Cell 131:452–62 96. Otto SP, Whitton J. 2000. Polyploid incidence and evolution. Annu. Rev. Genet. 34:401–37

Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org 97. Pagel M. 1994. Detecting correlated evolution on phylogenies: a general method for the comparative Access provided by University of British Columbia on 05/17/18. For personal use only. analysis of discrete characters. Proc. R. Soc. B 255:37–45 98. Pagel M. 1997. Inferring evolutionary processes from phylogenies. Zool. Scr. 26:331–48 99. Pagel M. 1999. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst. Biol. 48:612–22 100. Pagel M, Meade A. 2006. Bayesian analysis of correlated evolution of discrete characters by reversible- jump Markov chain Monte Carlo. Am. Nat. 167:808–25 101. Pennington RT, Lavin M, Sarkinen¨ T, Lewis GP, Klitgaard BB, Hughes CE. 2010. Contrasting plant diversification histories within the Andean biodiversity hotspot. PNAS 107:13783–87 102. Pimm SL, Raven PH. 2017. The fate of the world’s plants. Trends Ecol. Evol. 32:317–20 103. Rabosky DL. 2010. Extinction rates should not be estimated from molecular phylogenies. Evolution 64:1816–24 104. Rabosky DL. 2014. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLOS ONE 9:e89543

www.annualreviews.org • Macroevolutionary Patterns of Flowering Plants 703 PP69CH25_Vamosi ARI 4 April 2018 8:6

105. Rabosky DL, Donnellan SC, Grundler M, Lovette IJ. 2014. Analysis and visualization of complex macroevolutionary dynamics: an example from Australian scincid lizards. Syst. Biol. 63:610–27 106. Rabosky DL, Goldberg EE. 2015. Model inadequacy and mistaken inferences of trait-dependent speci- ation. Syst. Biol. 64:340–55 107. Rabosky DL, Lovette IJ. 2008. Explosive evolutionary radiations: decreasing speciation or increasing extinction through time? Evolution 62:1866–75 108. Rabosky DL, Mitchell JS, Chang J. 2017. Is BAMM flawed? Theoretical and practical concerns in the analysis of multi-rate diversification models. Syst. Biol. 66:477–98 109. Ramsey J, Ramsey TS. 2014. Ecological studies of polyploidy in the 100 years following its discovery. Philos. Trans. R. Soc. B 369:20130352 110. Ramsey J, Schemske DW. 2002. Neopolyploidy in flowering plants. Annu. Rev. Ecol. Syst. 33:589–639 111. Rausch JH, Morgan MT. 2005. The effect of self-fertilization, inbreeding depression, and population size on autopolyploid establishment. Evolution 59:1867–75 112. Ree RH. 2005. Detecting the historical signature of key innovations using stochastic models of character evolution and cladogenesis. Evolution 59:257–65 113. Renner SS. 2014. The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. Am. J. Bot. 101:1588–96 114. Reyes E, Morlon H, Sauquet H. 2015. Presence in Mediterranean hotspots and floral symmetry affect speciation and extinction rates in Proteaceae. New Phytol. 207:401–10 115. Reyes E, Sauquet H, Nadot S. 2016. Perianth symmetry changed at least 199 times in angiosperm evolution. Taxon 65:945–64 116. Ricklefs RE. 2007. Estimating diversification rates from phylogenetic information. Trends Ecol. Evol. 22:601–10 117. Robertson K, Goldberg EE, Igic´ B. 2011. Comparative evidence for the correlated evolution of polyploidy and self-compatibility in Solanaceae. Evolution 65:139–55 118. Rolland J, Condamine FL, Jiguet F, Morlon H. 2014. Faster speciation and reduced extinction in the tropics contribute to the mammalian latitudinal diversity gradient. PLOS Biol. 12:e1001775 119. Sabath N, Goldberg EE, Glick L, Einhorn M, Ashman T-L, et al. 2016. Dioecy does not consistently accelerate or slow lineage diversification across multiple genera of angiosperms. New Phytol. 209:1290– 300 120. Sanchez-Reyes´ LL, Morlon H, Magallon´ S. 2017. Uncovering higher-taxon diversification dynamics from clade age and species-richness data. Syst. Biol. 66:367–78 121. Sanderson MJ, Donoghue MJ. 1994. Shifts in diversification rate with the origin of angiosperms. Science 264:1590–93 122. Sargent RD. 2004. Floral symmetry affects speciation rates in angiosperms. Proc.R.Soc.B271:603–8 123. Sauquet H, von Balthazar M, Magallon´ S, Doyle J, Endress P, et al. 2017. The ancestral flower of angiosperms and its early diversification. Nature Commun. 8:16047 124. Savolainen V, Anstett M-C, Lexer C, Hutton I, Clarkson JJ, et al. 2006. in palms

Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org on an oceanic island. Nature 441:210–13 Access provided by University of British Columbia on 05/17/18. For personal use only. 125. Scarpino SV, Levin DA, Meyers LA. 2014. Polyploid formation shapes flowering plant diversity. Am. Nat. 184:456–65 126. Schluter D, Price T, Mooers AO, Ludwig D. 1997. Likelihood of ancestor states in adaptive radiation. Evolution 51:1699–711 127. Schneider H, Schuettpelz E, Pryer KM, Cranfill R, Magallon S, Lupia R. 2004. Ferns diversified in the shadow of angiosperms. Nature 428:553–57 128. Schranz ME, Mohammadin S, Edger PP. 2012. Ancient whole genome duplications, novelty and diver- sification: the WGD Radiation Lag-Time Model. Curr. Opin. Plant Biol. 15:147–53 129. Schultz RJ. 1980. Role of polyploidy in the evolution of fishes. In Polyploidy: Biological Relevance,ed.WH Lewis, pp. 313–40. New York: Plenum 130. Segraves KA. 2017. The effects of genome duplications in a community context. New Phytol. 215:57–69 131. Silvestro D, Cascales-Minana˜ B, Bacon CD, Antonelli A. 2015. Revisiting the origin and diversification of vascular plants through a comprehensive Bayesian analysis of the fossil record. New Phytol. 207:425–36

704 Vamosi et al. PP69CH25_Vamosi ARI 4 April 2018 8:6

132. Slowinski JB, Guyer C. 1989. Testing the stochasticity of patterns of organismal diversity: an improved null model. Am. Nat. 134:907–21 133. Slowinski JB, Guyer C. 1993. Testing whether certain traits have caused amplified diversification: an improved method based on a model of random speciation and extinction. Am. Nat. 142:1019–24 134. Smith SA, Beaulieu JM, Stamatakis A, Donoghue MJ. 2011. Understanding angiosperm diversification using small and large phylogenetic trees. Am. J. Bot. 98:404–14 135. Soltis DE, Albert VA, Leebens-Mack J, Bell CD, Paterson AH, et al. 2009. Polyploidy and angiosperm diversification. Am. J. Bot. 96:336–48 136. Soltis DE, Segovia-Salcedo MC, Jordon-Thaden I, Majure L, Miles NM, et al. 2014. Are polyploids re- ally evolutionary dead-ends (again)? A critical reappraisal of Mayrose et al. (2011). New Phytol. 202:1105– 17 137. Stebbins GL Jr. 1938. Cytological characteristics associated with the different growth habits in the dicotyledons. Am. J. Bot. 25:189 138. Stebbins GL Jr. 1950. Variation and Evolution in Plants. New York: Columbia Univ. Press 139. Stebbins GL Jr. 1971. Relationships between adaptive radiation, speciation and major evolutionary trends. Taxon 20:3–16 140. Tank DC, Eastman JM, Pennell MW, Soltis PS, Soltis DE, et al. 2015. Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. New Phytol. 207:454–67 141. Thompson JN, Merg KF. 2008. Evolution of polyploidy and the diversification of plant–pollinator interactions. Ecology 89:2197–206 142. Uribe-Convers S, Tank DC. 2015. Shifts in diversification rates linked to biogeographic movement into new areas: an example of a recent radiation in the Andes. Am.J.Bot.102:1854–69 143. Uyeda JC, Zenil-Ferguson R, Pennell MW. 2017. Rethinking phylogenetic comparative methods. bioRxiv 222729. https://doi.org/10.1101/222729 144. Vamosi JC, Dickinson TA. 2006. Polyploidy and diversification: a phylogenetic investigation in Rosaceae. Int. J. Plant. Sci. 167:349–58 145. Vamosi JC, McEwen JR. 2012. Origin, elevation, and evolutionary success of hybrids and polyploids in British Columbia, Canada. Botany 91:182–88 146. Vamosi JC, Vamosi SM. 2010. Key innovations within a geographical context in flowering plants: towards resolving Darwin’s abominable mystery. Ecol. Lett. 13:1270–79 147. Vamosi JC, Vamosi SM. 2011. Factors influencing diversification in angiosperms: at the crossroads of intrinsic and extrinsic traits. Am. J. Bot. 98:460–71 148. Vamosi JC, Wilson JRU. 2008. Nonrandom extinction leads to elevated loss of angiosperm evolutionary history. Ecol. Lett. 11:1047–53 149. Vamosi SM, Vamosi JC. 2012. Causes and consequences of range size variation: the influence of traits, speciation, and extinction. Front. Biogeogr. 4:167–77 150. Vanneste K, Maere S, Van de Peer Y. 2014. Tangled up in two: a burst of genome duplications at the end of the Cretaceous and the consequences for plant evolution. Philos. Trans. R. Soc. B. 369:20130353 Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org 151. Vekemans D, Proost S, Vanneste K, Coenen H, Viaene T, et al. 2012. Gamma paleohexaploidy in the Access provided by University of British Columbia on 05/17/18. For personal use only. stem lineage of core eudicots: significance for MADS-Box gene and species diversification. Mol. Biol. Evol. 29:3793–806 152. Wagner WH Jr. 1970. Biosystematics and evolutionary noise. Taxon 19:146–51 153. Wang W, Lin L, Xiang X-G, del C Ortiz R, Liu Y, et al. 2016. The rise of angiosperm-dominated herbaceous floras: insights from Ranunculaceae. Sci. Rep. 6:27259 154. Weir JT, Schluter D. 2007. The latitudinal gradient in recent speciation and extinction rates of birds and mammals. Science 315:1574–76 155. Willis CG, Ruhfel B, Primack RB, Miller-Rushing AJ, Davis CC. 2008. Phylogenetic patterns of species loss in Thoreau’s woods are driven by climate change. PNAS 105:17029–33 156. Wolfe JA, Upchurch GR. 1986. Vegetation, climatic and floral changes at the Cretaceous–Tertiary boundary. Nature 324:148–52 157. Wood TE, Takebayashi N, Barker MS, Mayrose I, Greenspoon PB, Rieseberg LH. 2009. The frequency of polyploid speciation in vascular plants. PNAS 106:13875–79

www.annualreviews.org • Macroevolutionary Patterns of Flowering Plants 705 PP69CH25_Vamosi ARI 4 April 2018 8:6

158. Xing Y, Gandolfo MA, Onstein RE, Cantrill DJ, Jacobs BF, et al. 2016. Testing the biases in the rich Cenozoic angiosperm macrofossil record. Int. J. Plant Sci. 177:371–88 159. Zanne AE, Tank DC, Cornwell WK, Eastman JM, Smith SA, et al. 2014. Three keys to the radiation of angiosperms into freezing environments. Nature 506:89–92 160. Zhan SH, Drori M, Goldberg EE, Otto SP, Mayrose I. 2016. Phylogenetic evidence for cladogenetic polyploidization in land plants. Am. J. Bot. 103:1252–58

RELATED RESOURCES The 1KP project, https://sites.google.com/a/ualberta.ca/onekp/: With the upcoming release of genomic data from 1,000 species of plants, this resource will allow for a more detailed picture of the association between traits, such as polyploidization, and diversification shifts The IUCN Red List of Threatened Species, http://www.iucnredlist.org: The list describes flowering 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 to predict which species and ecosystems will be common in future environments Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org Access provided by University of British Columbia on 05/17/18. For personal use only.

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Annual Review of Plant Biology

Volume 69, 2018 Contents

My Secret Life Mary-Dell Chilton ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp1 Diversity of Chlorophototrophic Bacteria Revealed in the Omics Era Vera Thiel, Marcus Tank, and Donald A. Bryant pppppppppppppppppppppppppppppppppppppppppp21 Genomics-Informed Insights into Endosymbiotic Organelle Evolution in Photosynthetic Eva C.M. Nowack and Andreas P.M. Weber ppppppppppppppppppppppppppppppppppppppppppppppp51 Nitrate Transport, Signaling, and Use Efficiency Ya-Yun Wang, Yu-Hsuan Cheng, Kuo-En Chen, and Yi-Fang Tsay ppppppppppppppppppppp85 Plant Vacuoles Tomoo Shimada, Junpei Takagi, Takuji Ichino, Makoto Shirakawa, and Ikuko Hara-Nishimura ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp123 Protein Quality Control in the Endoplasmic Reticulum of Plants Richard Strasser ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp147 Autophagy: The Master of Bulk and Selective Recycling Richard S. Marshall and Richard D. Vierstra ppppppppppppppppppppppppppppppppppppppppppppp173 Reactive Oxygen Species in Plant Signaling Cezary Waszczak, Melanie Carmody, and Jaakko Kangasj¨arvi pppppppppppppppppppppppppp209 Cell and Developmental Biology of Plant Mitogen-Activated Protein Kinases Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org

Access provided by University of British Columbia on 05/17/18. For personal use only. George Komis, Olga Samajov´ˇ a, Miroslav Oveˇcka, and Jozef Samajˇ ppppppppppppppppppppp237 Receptor-Like Cytoplasmic Kinases: Central Players in Plant Receptor Kinase–Mediated Signaling Xiangxiu Liang and Jian-Min Zhou pppppppppppppppppppppppppppppppppppppppppppppppppppppp267 Plant Malectin-Like Receptor Kinases: From Cell Wall Integrity to Immunity and Beyond Christina Maria Franck, Jens Westermann, and Aur´elien Boisson-Dernier pppppppppppp301 Kinesins and Myosins: Molecular Motors that Coordinate Cellular Functions in Plants Andreas Nebenf¨uhr and Ram Dixit pppppppppppppppppppppppppppppppppppppppppppppppppppppppp329

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The Oxylipin Pathways: Biochemistry and Function Claus Wasternack and Ivo Feussner pppppppppppppppppppppppppppppppppppppppppppppppppppppppp363 in Jasmonate Signaling for Multistress Resilience Gregg A. Howe, Ian T. Major, and Abraham J. Koo ppppppppppppppppppppppppppppppppppppp387 Essential Roles of Local Auxin Biosynthesis in Plant Development and in Adaptation to Environmental Changes Yunde Zhao pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp417 Genetic Regulation of Shoot Architecture Bing Wang, Steven M. Smith, and Jiayang Li ppppppppppppppppppppppppppppppppppppppppppp437 Heterogeneity and Robustness in Plant Morphogenesis: From Cells to Organs Lilan Hong, Mathilde Dumond, Mingyuan Zhu, Satoru Tsugawa, Chun-Biu Li, Arezki Boudaoud, Olivier Hamant, and Adrienne H.K. Roeder pppppp469 Genetically Encoded Biosensors in Plants: Pathways to Discovery Ankit Walia, Rainer Waadt, and Alexander M. Jones ppppppppppppppppppppppppppppppppppp497 Exploring the Spatiotemporal Organization of Membrane Proteins in Living Plant Cells Li Wang, Yiqun Xue, Jingjing Xing, Kai Song, and Jinxing Lin ppppppppppppppppppppppp525 One Hundred Ways to Invent the Sexes: Theoretical and Observed PathstoDioecyinPlants Isabelle M. Henry, Takashi Akagi, Ryutaro Tao, and Luca Comai pppppppppppppppppppppp553 Meiotic Recombination: Mixing It Up in Plants Yingxiang Wang and Gregory P. Copenhaver pppppppppppppppppppppppppppppppppppppppppppp577 Population Genomics of Herbicide Resistance: Adaptation via Evolutionary Rescue Julia M. Kreiner, John R. Stinchcombe, and Stephen I. Wright ppppppppppppppppppppppppp611 Strategies for Enhanced Crop Resistance to Insect Pests Angela E. Douglas ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp637 Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org Access provided by University of British Columbia on 05/17/18. For personal use only. Preadaptation and Naturalization of Nonnative Species: Darwin’s Two Fundamental Insights into Species Invasion Marc W. Cadotte, Sara E. Campbell, Shao-peng Li, Darwin S. Sodhi, and Nicholas E. Mandrak pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp661 Macroevolutionary Patterns of Flowering Plant Speciation and Extinction Jana C. Vamosi, Susana Magall´on, Itay Mayrose, Sarah P. Otto, and Herv´e Sauquet ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp685

vi Contents PP69_FrontMatter ARI 5 April 2018 9:11

When Two Rights Make a Wrong: The Evolutionary Genetics of Plant Incompatibilities Lila Fishman and Andrea L. Sweigart ppppppppppppppppppppppppppppppppppppppppppppppppppppp707 The Physiological Basis of Drought Tolerance in Crop Plants: A Scenario-Dependent Probabilistic Approach Fran¸cois Tardieu, Thierry Simonneau, and Bertrand Muller pppppppppppppppppppppppppppp733 Paleobotany and Global Change: Important Lessons for Species to Biomes from Vegetation Responses to Past Global Change Jennifer C. McElwain ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp761 Trends in Global Agricultural Land Use: Implications for Environmental Health and Food Security Navin Ramankutty, Zia Mehrabi, Katharina Waha, Larissa Jarvis, Claire Kremen, Mario Herrero, and Loren H. Rieseberg pppppppppppppppppppppppppppppp789

Errata

An online log of corrections to Annual Review of Plant Biology articles may be found at http://www.annualreviews.org/errata/arplant Annu. Rev. Plant Biol. 2018.69:685-706. Downloaded from www.annualreviews.org Access provided by University of British Columbia on 05/17/18. For personal use only.

Contents vii