Angiosperm flowers reached their highest morphological diversity early in their evolutionary history.

Flowers are the complex and highly diverse reproductive structures of angiosperms. Because of their role in sexual reproduction, the evolution of flowers is tightly linked to angiosperm speciation and diversification. Accordingly, the quantification of floral morphological diversity (disparity) among angiosperm subgroups and through time may give important insights into the evolutionary history of angiosperms as a whole. Based on a comprehensive dataset focusing on 30 characters describing floral structure across angiosperms, we used 1201 extant and 121 fossil flowers to measure floral disparity and explore patterns of floral evolution through time and across lineages. We found that angiosperms reached their highest floral disparity in the Early Cretaceous. However, decreasing disparity toward the present likely has not precluded the innovation of other complex traits at other morphological levels, which likely played a key role in the outstanding angiosperm species richness. Angiosperms occupy specific regions of the theoretical morphospace, indicating that only a portion of the possible floral trait combinations is observed in nature. The ANA grade, the magnoliids, and the early-eudicot grade occupy large areas of the morphospace (higher disparity), whereas nested groups occupy narrower regions (lower disparity).

Assessing digital accessible botanical knowledge and priorities for exploration and discovery of plant diversity across Mesoamerica.

Digital accessible biodiversity knowledge has the potential to greatly advance botanical research and guide conservation efforts. Evaluating its shortfalls is key to understanding its limits and prioritising regions in need of renewed survey efforts. We used the Royal Botanical Gardens Kew's World Checklist of Vascular Plants to parse publicly available occurrence data downloaded from the Global Biodiversity Information Facility and quantify the spatial distribution of spatial, phylogenetic, and temporal data shortfalls across Mesoamerica. After processing 3578 777 occurrence records for 32 522 species of vascular plants across Mesoamerica, we found evidence of poor data coverage: incomplete characterisation of species diversity, old occurrence records, and low phylogenetic representation. One-third of the region showed large gaps for at least one of these dimensions (hotspots) and < 15% had adequate data coverage across dimensions. Overall, the shortfalls we identified compromise the quality of digitally available occurrence data and hamper research on spatial phylogenetics and species dynamics under anthropogenic disturbances. Our analyses identified areas of opportunity for increased efforts in data digitisation, botanical exploration, sequencing, and biodiversity monitoring. These efforts would serve to increase and rejuvenate knowledge on the geographic distribution of vascular plants in Mesoamerica.

Plastome phylogenomics reveals an early Pliocene North- and Central America colonization by long-distance dispersal from South America of a highly diverse bromeliad lineage.

Understanding the spatial and temporal frameworks of species diversification is fundamental in evolutionary biology. Assessing the geographic origin and dispersal history of highly diverse lineages of rapid diversification can be hindered by the lack of appropriately sampled, resolved, and strongly supported phylogenetic contexts. The use of currently available cost-efficient sequencing strategies allows for the generation of a substantial amount of sequence data for dense taxonomic samplings, which together with well-curated geographic information and biogeographic models allow us to formally test the mode and tempo of dispersal events occurring in quick succession. Here, we assess the spatial and temporal frameworks for the origin and dispersal history of the expanded clade K, a highly diverse Tillandsia subgenus Tillandsia (Bromeliaceae, Poales) lineage hypothesized to have undergone a rapid radiation across the Neotropics. We assembled full plastomes from Hyb-Seq data for a dense taxon sampling of the expanded clade K plus a careful selection of outgroup species and used them to estimate a time- calibrated phylogenetic framework. This dated phylogenetic hypothesis was then used to perform biogeographic model tests and ancestral area reconstructions based on a comprehensive compilation of geographic information. The expanded clade K colonized North and Central America, specifically the Mexican transition zone and the Mesoamerican dominion, by long-distance dispersal from South America at least 4.86 Mya, when most of the Mexican highlands were already formed. Several dispersal events occurred subsequently northward to the southern Nearctic region, eastward to the Caribbean, and southward to the Pacific dominion during the last 2.8 Mya, a period characterized by pronounced climate fluctuations, derived from glacial-interglacial climate oscillations, and substantial volcanic activity, mainly in the Trans-Mexican Volcanic Belt. Our taxon sampling design allowed us to calibrate for the first time several nodes, not only within the expanded clade K focal group but also in other Tillandsioideae lineages. We expect that this dated phylogenetic framework will facilitate future macroevolutionary studies and provide reference age estimates to perform secondary calibrations for other Tillandsioideae lineages.

Integrating Fossil Flowers into the Angiosperm Phylogeny Using Molecular and Morphological Evidence.

Fossils are essential to infer past evolutionary processes. The assignment of fossils to extant clades has traditionally relied on morphological similarity and on apomorphies shared with extant taxa. The use of explicit phylogenetic analyses to establish fossil affinities has so far remained limited. In this study, we built a comprehensive framework to investigate the phylogenetic placement of 24 exceptionally preserved fossil flowers. For this, we assembled a new species-level data set of 30 floral traits for 1201 extant species that were sampled to capture the stem and crown nodes of all angiosperm families. We explored multiple analytical approaches to integrate the fossils into the phylogeny, including different phylogenetic estimation methods, topological-constrained analyses, and combining molecular and morphological data of extant and fossil species. Our results were widely consistent across approaches and showed minor differences in the support of fossils at different phylogenetic positions. The placement of some fossils agrees with previously suggested relationships, but for others, a new placement is inferred. We also identified fossils that are well supported within particular extant families, whereas others showed high phylogenetic uncertainty. Finally, we present recommendations for future analyses combining molecular and morphological evidence, regarding the selection of fossils and appropriate methodologies, and provide some perspectives on how to integrate fossils into the investigation of divergence times and the temporal evolution of morphological traits. [Angiosperms; fossil flowers; phylogenetic uncertainty; RoguePlots.].

The use of Anchored Hybrid Enrichment data to resolve higher-level phylogenetic relationships: A proof-of-concept applied to Asterales (Eudicotyledoneae; Angiosperms).

Anchored Hybrid Enrichment (AHE) is a tool for capturing orthologous regions of the nuclear genome shared in low or single copy across lineages. Despite the increasing number of studies using this method, its usefulness to estimate relationships at deeper taxonomic levels in plants has not been fully explored. Here we present a proof of concept about the performance of nuclear loci obtained with AHE to infer phylogenetic relationships and explore the use of gene sampling schemes to estimate divergence times in Asterales. We recovered low-copy nuclear loci using the AHE method from herbarium material and silica-preserved samples. Maximum likelihood, Bayesian inference, and coalescence approaches were used to reconstruct phylogenomic relationships. Dating analyses were conducted under a multispecies coalescent approach by jointly inferring species tree and divergence times with random gene sampling schemes and multiple calibrations. We recovered 403 low-copy nuclear loci for 63 species representing nine out of eleven families of Asterales. Phylogenetic hypotheses were congruent among the applied methods and previously published results. Analyses with concatenated datasets were strongly supported, but coalescence-based analyses showed low support for the phylogenetic position of families Argophyllaceae and Alseuosmiaceae. Estimated family ages were congruent among gene sampling schemes, with the mean age for Asterales around 130 Myr. Our study documents the usefulness of AHE for resolving phylogenetic relationships at deep phylogenetic levels in Asterales. Observed phylogenetic inconsistencies were possibly due to the non-inclusion of families Phellinceae and Pentaphragmataceae. Random gene sampling schemes produced consistent age estimates with coalescence and species tree relaxed clock approaches.

New plastome structural rearrangements discovered in core Tillandsioideae (Bromeliaceae) support recently adopted taxonomy.

Full plastome sequences for land plants have become readily accessible thanks to the development of Next Generation Sequencing (NGS) techniques and powerful bioinformatic tools. Despite this vast amount of genomic data, some lineages remain understudied. Full plastome sequences from the highly diverse (>1,500 spp.) subfamily Tillandsioideae (Bromeliaceae, Poales) have been published for only three (i.e., Guzmania, Tillandsia, and Vriesea) out of 22 currently recognized genera. Here, we focus on core Tillandsioideae, a clade within subfamily Tillandsioideae, and explore the contribution of individual plastid markers and data categories to inform deep divergences of a plastome phylogeny. We generated 37 high quality plastome assemblies and performed a comparative analysis in terms of plastome structure, size, gene content and order, GC content, as well as number and type of repeat motifs. Using the obtained phylogenetic context, we reconstructed the evolution of these plastome attributes and assessed if significant shifts on the evolutionary traits' rates have occurred in the evolution of the core Tillandsioideae. Our results agree with previously published phylogenetic hypotheses based on plastid data, providing stronger statistical support for some recalcitrant nodes. However, phylogenetic discordance with previously published nuclear marker-based hypotheses was found. Several plastid markers that have been consistently used to address phylogenetic relationships within Tillandsioideae were highly informative for the retrieved plastome phylogeny and further loci are here identified as promising additional markers for future studies. New lineage-specific plastome rearrangements were found to support recently adopted taxonomic groups, including large inversions, as well as expansions and contractions of the inverted repeats. Evolutionary trait rate shifts associated with changes in size and GC content of the plastome regions were found across the phylogeny of core Tillandsioideae.

Localized Phylogenetic Discordance Among Nuclear Loci Due to Incomplete Lineage Sorting and Introgression in the Family of Cotton and Cacao (Malvaceae).

The economically important cotton and cacao family (Malvaceae sensu lato) have long been recognized as a monophyletic group. However, the relationships among some subfamilies are still unclear as discordant phylogenetic hypotheses keep arising when different sources of molecular data are analyzed. Phylogenetic discordance has previously been hypothesized to be the result of both introgression and incomplete lineage sorting (ILS), but the extent and source of discordance have not yet been evaluated in the context of loci derived from massive sequencing strategies and for a wide representation of the family. Furthermore, no formal methods have been applied to evaluate if the detected phylogenetic discordance among phylogenomic datasets influences phylogenetic dating estimates of the concordant relationships. The objective of this research was to generate a phylogenetic hypothesis of Malvaceae from nuclear genes, specifically we aimed to (1) investigate the presence of major discordance among hundreds of nuclear gene histories of Malvaceae; (2) evaluate the potential source of discordance; and (3) examine whether discordance and loci heterogeneity influence on time estimates of the origin and diversification of subfamilies. Our study is based on a comprehensive dataset representing 96 genera of the nine subfamilies and 268 nuclear loci. Both concatenated and coalescence-based approaches were followed for phylogenetic inference. Using branch lengths and topology, we located the placement of introgression events to directly evaluate whether discordance is due to introgression rather than ILS. To estimate divergence times, concordance and molecular rate were considered. We filtered loci based on congruence with the species tree and then obtained the molecular rate of each locus to distribute them into three different sets corresponding to shared molecular rate ranges. Bayesian dating was performed for each of the different sets of loci with the same parameters and calibrations. Phylogenomic discordance was detected between methods, as well as gene histories. At deep coalescent times, we found discordance in the position of five subclades probably due to ILS and a relatively small proportion of introgression. Divergence time estimation with each set of loci generated overlapping clade ages, indicating that, even with different molecular rate and gene histories, calibrations generally provide a strong prior.

What is the age of flowering plants?

The origin of flowering plants (angiosperms) was one of the most transformative events in the history of our planet. Despite considerable interest from multiple research fields, numerous questions remain, including the age of the group as a whole. Recent studies have reported a perplexing range of estimates for the crown-group age of angiosperms, from ~140 million years (Ma; Early Cretaceous) to 270 Ma (Permian). Both ends of the spectrum are now supported by both macroevolutionary analyses of the fossil record and fossil-calibrated molecular dating analyses. Here, we first clarify and distinguish among the three ages of angiosperms: the age of their divergence with acrogymnosperms (stem age); the age(s) of emergence of their unique, distinctive features including flowers (morphological age); and the age of the most recent common ancestor of all their living species (crown age). We then demonstrate, based on recent studies, that fossil-calibrated molecular dating estimates of the crown-group age of angiosperms have little to do with either the amount of molecular data or the number of internal fossil calibrations included. Instead, we argue that this age is almost entirely conditioned by its own prior distribution (typically a calibration density set by the user in Bayesian analyses). Lastly, we discuss which future discoveries or novel types of analyses are most likely to bring more definitive answers. In the meantime, we propose that the age of angiosperms is best described as largely unknown (140-270 Ma) and that contrasting age estimates in the literature mostly reflect conflicting prior distributions. We also suggest that future work that depends on the time scale of flowering plant diversification be designed to integrate over this vexing uncertainty.

Role of diversification rates and evolutionary history as a driver of plant naturalization success.

Human introductions of species beyond their natural ranges and their subsequent establishment are defining features of global environmental change. However, naturalized plants are not uniformly distributed across phylogenetic lineages, with some families contributing disproportionately more to the global alien species pool than others. Additionally, lineages differ in diversification rates, and high diversification rates have been associated with characteristics that increase species naturalization success. Here, we investigate the role of diversification rates in explaining the naturalization success of angiosperm plant families. We use five global data sets that include native and alien plant species distribution, horticultural use of plants, and a time-calibrated angiosperm phylogeny. Using phylogenetic generalized linear mixed models, we analysed the effect of diversification rate, different geographical range measures, and horticultural use on the naturalization success of plant families. We show that a family's naturalization success is positively associated with its evolutionary history, native range size, and economic use. Investigating interactive effects of these predictors shows that native range size and geographic distribution additionally affect naturalization success. High diversification rates and large ranges increase naturalization success, especially of temperate families. We suggest this may result from lower ecological specialization in temperate families with large ranges, compared with tropical families with smaller ranges.

Phylogeny, Diversification Rate, and Divergence Time of Agave sensu lato (Asparagaceae), a Group of Recent Origin in the Process of Diversification.

Agave sensu lato is one of the most diverse and complex genera of Asparagaceae, with more than 250 species. The morphological, ecological, and evolutionary diversity of the group has complicated its taxonomical study. We conducted phylogenetic analyses of DNA sequence data to reconstruct the phylogenetic relationships of the Agave genus. We included 107 species of the Asparagaceae family from which 83 correspond to the Agave sensu lato clade (Agave sensu stricto + Polianthes + Manfreda and Prochnyanthes, which together represent 30% of the genus) and as outgroups the genera Dasylirion, Hesperoyucca, Chlorogalum, Camassia, Hesperaloe, Yucca, Beschorneria, and Furcraea, in order to estimate the age and propose the history of their diversification. Previous studies postulated the relevance of the Miocene in the speciation rates of the agaves, as well as the relevance of the type of inflorescence in its diversification. However, these assertions have not been well supported. The analysis of chloroplast regions resulted in low resolution, which could be the consequence of the few variable sites. On the other hand, the internal transcribed spacer (ITS) implemented in our analysis ensued in higher resolution and better support values. Our phylogenetic analyses recovered five groups; one is the Striatae group, which is the sister group to Agave sensu stricto clade. Within this clade, we found three main groups with high support; these groups are not related with previous morphological proposals. We also analyzed the dates of origin and diversification rates. A Bayesian analysis of macroevolutionary mixtures indicated two significant shifts; the first was identified at 6.18 Ma, where the speciation rate increased to 4.10 species/Mya, this shift occurred during the late Miocene period, characterized by the emergence of arid biomes in North America. The second was identified at a stem age of 2.68 Ma where the speciation rate increased to 6.04 species/Mya. Concerning the ancestral reconstruction state of the inflorescence type in the Agave sensu stricto clade, the spike inflorescence character was predominant in the early-diverging groups, whereas the late-diverging groups present panicle inflorescences as the predominant character and higher speciation rates.

Phylogenetic analysis of fossil flowers using an angiosperm-wide data set: proof-of-concept and challenges ahead.

PREMISE: Significant paleobotanical discoveries in recent decades have considerably improved our understanding of the early evolution of angiosperms and their flowers. However, our ability to test the systematic placement of fossil flowers on the basis of phylogenetic analyses has remained limited, mainly due to the lack of an adequate, angiosperm-wide morphological data set for extant taxa. Earlier attempts to place fossil flowers phylogenetically were, therefore, forced to make prior qualitative assessments of the potential systematic position of fossils and to restrict phylogenetic analyses to selected angiosperm subgroups. METHODS: We conduct angiosperm-wide molecular backbone analyses of 10 fossil flower taxa selected from the Cretaceous record. Our analyses make use of a floral trait data set built within the framework of the eFLOWER initiative. We provide an updated version of this data set containing data for 28 floral and two pollen traits for 792 extant species representing 372 angiosperm families. RESULTS: We find that some fossils are placed congruently with earlier hypotheses while others are found in positions that had not been suggested previously. A few take up equivocal positions, including the stem branches of large clades. CONCLUSIONS: Our study provides an objective approach to test for the phylogenetic position of fossil flowers across angiosperms. Such analyses may provide a complementary tool for paleobotanical studies, allowing for a more comprehensive understanding of fossil phylogenetic relationships in angiosperms. Ongoing work focused on extending the sampling of extant taxa and the number of floral traits will further improve the applicability and accuracy of our approach.

The delayed and geographically heterogeneous diversification of flowering plant families.

The Early Cretaceous (145-100 million years ago (Ma)) witnessed the rise of flowering plants (angiosperms), which ultimately lead to profound changes in terrestrial plant communities. However, palaeobotanical evidence shows that the transition to widespread angiosperm-dominated biomes was delayed until the Palaeocene (66-56 Ma). Important aspects of the timing and geographical setting of angiosperm diversification during this period, and the groups involved, remain uncertain. Here we address these aspects by constructing and dating a new and complete family-level phylogeny, which we integrate with 16 million geographic occurrence records for angiosperms on a global scale. We show substantial time lags (mean, 37-56 Myr) between the origin of families (stem age) and the diversification leading to extant species (crown ages) across the entire angiosperm tree of life. In turn, our results show that families with the shortest lags are overrepresented in temperate and arid biomes compared with tropical biomes. Our results imply that the diversification and ecological expansion of extant angiosperms was geographically heterogeneous and occurred long after most of their phylogenetic diversity originated during the Cretaceous Terrestrial Revolution.

Thirty clues to the exceptional diversification of flowering plants.

BACKGROUND AND AIMS: As angiosperms became one of the megadiverse groups of macroscopic eukaryotes, they forged modern ecosystems and promoted the evolution of extant terrestrial biota. Unequal distribution of species among lineages suggests that diversification, the process that ultimately determines species richness, acted differentially through angiosperm evolution. METHODS: We investigate how angiosperms became megadiverse by identifying the phylogenetic and temporal placement of exceptional radiations, by combining the most densely fossil-calibrated molecular clock phylogeny with a Bayesian model that identifies diversification shifts among evolutionary lineages and through time. We evaluate the effect of the prior number of expected shifts in the phylogenetic tree. KEY RESULTS: Major diversification increases took place over 100 Ma, from the Early Cretaceous to the end of the Paleogene, and are distributed across the angiosperm phylogeny. The long-term diversification trajectory of angiosperms shows moderate rate variation, but is underlain by increasing speciation and extinction, and results from temporally overlapping, independent radiations and depletions in component lineages. CONCLUSIONS: The identified deep time diversification shifts are clues to the identification of ultimate drivers of angiosperm megadiversity, which probably involve multivariate interactions among intrinsic traits and extrinsic forces. An enhanced understanding of angiosperm diversification will involve a more precise phylogenetic location of diversification shifts, and integration of fossil information.

Target Nuclear and Off-Target Plastid Hybrid Enrichment Data Inform a Range of Evolutionary Depths in the Orchid Genus Epidendrum.

Universal angiosperm enrichment probe sets designed to enrich hundreds of putatively orthologous nuclear single-copy loci are increasingly being applied to infer phylogenetic relationships of different lineages of angiosperms at a range of evolutionary depths. Studies applying such probe sets have focused on testing the universality and performance of the target nuclear loci, but they have not taken advantage of off-target data from other genome compartments generated alongside the nuclear loci. Here we do so to infer phylogenetic relationships in the orchid genus Epidendrum and closely related genera of subtribe Laeliinae. Our aims are to: 1) test the technical viability of applying the plant anchored hybrid enrichment (AHE) method (Angiosperm v.1 probe kit) to our focal group, 2) mine plastid protein coding genes from off-target reads; and 3) evaluate the performance of the target nuclear and off-target plastid loci in resolving and supporting phylogenetic relationships along a range of taxonomical depths. Phylogenetic relationships were inferred from the nuclear data set through coalescent summary and site-based methods, whereas plastid loci were analyzed in a concatenated partitioned matrix under maximum likelihood. The usefulness of target and flanking non-target nuclear regions and plastid loci was assessed through the estimation of their phylogenetic informativeness. Our study successfully applied the plant AHE probe kit to Epidendrum, supporting the universality of this kit in angiosperms. Moreover, it demonstrated the feasibility of mining plastome loci from off-target reads generated with the Angiosperm v.1 probe kit to obtain additional, uniparentally inherited sequence data at no extra sequencing cost. Our analyses detected some strongly supported incongruences between nuclear and plastid data sets at shallow divergences, an indication of potential lineage sorting, hybridization, or introgression events in the group. Lastly, we found that the per site phylogenetic informativeness of the ycf1 plastid gene surpasses that of all other plastid genes and several nuclear loci, making it an excellent candidate for assessing phylogenetic relationships at medium to low taxonomic levels in orchids.

Contemporaneous radiations of fungi and plants linked to symbiosis.

Interactions between fungi and plants, including parasitism, mutualism, and saprotrophy, have been invoked as key to their respective macroevolutionary success. Here we evaluate the origins of plant-fungal symbioses and saprotrophy using a time-calibrated phylogenetic framework that reveals linked and drastic shifts in diversification rates of each kingdom. Fungal colonization of land was associated with at least two origins of terrestrial green algae and preceded embryophytes (as evidenced by losses of fungal flagellum, ca. 720 Ma), likely facilitating terrestriality through endomycorrhizal and possibly endophytic symbioses. The largest radiation of fungi (Leotiomyceta), the origin of arbuscular mycorrhizae, and the diversification of extant embryophytes occurred ca. 480 Ma. This was followed by the origin of extant lichens. Saprotrophic mushrooms diversified in the Late Paleozoic as forests of seed plants started to dominate the landscape. The subsequent diversification and explosive radiation of Agaricomycetes, and eventually of ectomycorrhizal mushrooms, were associated with the evolution of Pinaceae in the Mesozoic, and establishment of angiosperm-dominated biomes in the Cretaceous.

Key questions and challenges in angiosperm macroevolution.

Contents Summary 1170 I. Introduction 1170 II. Six key questions 1172 III. Three key challenges 1177 IV. Conclusions 1181 Acknowledgements 1182 References 1183 SUMMARY: The origin and rapid diversification of angiosperms (flowering plants) represent one of the most intriguing topics in evolutionary biology. Despite considerable progress made in complementary fields over the last two decades (paleobotany, phylogenetics, ecology, evo-devo, genomics), many important questions remain. For instance, what has been the impact of mass extinctions on angiosperm diversification? Are the angiosperms an adaptive radiation? Has morphological evolution in angiosperms been gradual or pulsed? We propose that the recent and ongoing revolution in macroevolutionary methods provides an unprecedented opportunity to explore long-standing questions that probably hold important clues to understand present-day biodiversity. We present six key questions that explore the origin and diversification of angiosperms. We also identify three key challenges to address these questions: (1) the development of new integrative models that include diversification, multiple intrinsic and environmental traits, biogeography and the fossil record all at once, whilst accounting for sampling bias and heterogeneity of macroevolutionary processes through time and among lineages; (2) the need for large and standardized synthetic databases of morphological variation; and (3) continuous effort on sampling the fossil record, but with a revolution in current paleobotanical practice.

Recent radiation and dispersal of an ancient lineage: The case of Fouquieria (Fouquiericeae, Ericales) in North American deserts.

Arid biomes are particularly prominent in the Neotropics providing some of its most emblematic landscapes and a substantial part of its species diversity. To understand some of the evolutionary processes underlying the speciation of lineages in the Mexican Deserts, the diversification of Fouquieria is investigated, which includes eleven species, all endemic to the warm deserts and dry subtropical regions of North America. Using a phylogeny from plastid DNA sequences with samples of individuals from populations of all the species recognized in Fouquieria, we estimate divergence times, test for temporal diversification heterogeneity, test for geographical structure, and conduct ancestral area reconstruction. Fouquieria is an ancient lineage that diverged from Polemoniaceae ca. 75.54 Ma. A Mio-Pliocene diversification of Fouquieria with vicariance, associated with Neogene orogenesis underlying the early development of regional deserts is strongly supported. Test for temporal diversification heterogeneity indicates that during its evolutionary history, Fouquieria had a drastic diversification rate shift at ca.12.72 Ma, agreeing with hypotheses that some of the lineages in North American deserts diversified as early as the late Miocene to Pliocene, and not during the Pleistocene. Long-term diversification dynamics analyses suggest that extinction also played a significant role in Fouquieria's evolution, with a very high rate at the onset of the process. From the late Miocene onwards, Fouquieria underwent substantial diversification change, involving high speciation decreasing to the present and negligible extinction, which is congruent with its scant fossil record during this period. Geographic phylogenetic structure and the pattern of most sister species inhabiting different desert nucleus support that isolation by distance could be the main driver of speciation.

Macroevolutionary Patterns of Flowering Plant Speciation and Extinction.

Species diversity is remarkably unevenly distributed among flowering plant lineages. Despite a growing toolbox of research methods, the reasons underlying this patchy pattern have continued to perplex plant biologists for the 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 tropical and nontropical biomes, and shifts in floral form have received attention and have offered some surprises in terms of which factors influence speciation and extinction rates. Mating systems and dispersal characteristics once predominated as determining factors, yet recent evidence suggests that these changes are not as influential as previously thought or are important only when paired with range shifts. Although range extent is an important 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.