Estimation Of Diversification Rates Research Articles

Palaearctic origin and repeated dispersal over the world shaped the biogeographic history of the saprophytic genus Coprinopsis (Psathyrellaceae, Basidiomycota)

AbstractAimThe biogeographic history of most fungi is still poorly known, as well as the patterns and processes responsible for their diversification. Recent studies uncovered that most fungi have originated and present higher diversification rates in the temperate zone. The distributional pattern known for fungi is also different from many plants, animals and microbes. Using the most comprehensive phylogeny of the saprotrophic genus Coprinopsis, we aim to infer the biogeographic history and test evolutionary hypotheses in the genus.LocationWorldwide.TaxonFungi, Basidiomycota, Psathyrellaceae, Coprinopsis.MethodsWe used a four‐gene alignment with 100 species to estimate divergence times using two fossil calibrations within Agaricales. The chronograms were used to estimate diversification rates and geographic state‐dependent models were applied. We further reconstructed the ancestral range history of the genus.ResultsMolecular dating estimated that the genus has diverged ca. 41 Ma (Eocene) and was originated in the Palaearctic region. Diversification rates showed a decreasing pattern towards the present across Coprinopsis, especially after the Miocene (ca. 14 Ma). The diversification models dependent on distribution showed cosmopolitan lineages with a higher net‐diversification rates. When we compared temperate and tropical regions, we found that temperate lineages have higher net‐diversification rates. The biogeographic history of Coprinopsis estimated different routes of dispersal. The most common dispersal route was from Palaearctic to the Nearctic (15 times), followed by Palaearctic to the Neotropics (14 times).Main ConclusionsThe study is the first to estimate the diversification rates and the historical biogeography of the coprinoid genus Coprinopsis. The diversification dynamics estimates in Coprinopsis are in agreement with the ‘generalized diversification rates model’, where we found higher diversification rates in temperate regions compared with tropical regions. In general, the ancestral area and major dispersals routes recovered in the genus are similar to findings in other groups of fungi.

Diversifying in the mountains: spatiotemporal diversification of frogs in the Western Ghats biodiversity hotspot.

Mountain ranges are hotspots of biodiversity. However, the mechanisms that generate biodiversity patterns in different mountainous regions and taxa are not apparent. The Western Ghats (WG) escarpment in India is a globally recognized biodiversity hotspot with high species richness and endemism. Most studies have either invoked paleoclimatic conditions or climatic stability in the southern WG refugium to explain this high diversity and endemism. However, the factors driving macroevolutionary change remain unexplored for most taxa. Here, we generated the most comprehensive dated phylogeny to date for ranoid frogs in the WG and tested the role of paleoclimatic events or climatic stability in influencing frog diversification. We found that the diversity of different ranoid frog clades in the WG either accumulated at a constant rate through time or underwent a decrease in speciation rates around 3-2.5 Ma during the Pleistocene glaciation cycles. We also find no significant difference in diversification rate estimates across elevational gradients and the three broad biogeographic zones in the WG (northern, central, and southern WG). However, time-for-speciation explained regional species richness within clades, wherein older lineages have more extant species diversity. Overall, we find that global paleoclimatic events have had little impact on WG frog diversification throughout most of its early history until the Quaternary and that the WG may have been climatically stable allowing lineages to accumulate and persist over evolutionary time.

The angiosperm radiation played a dual role in the diversification of insects and insect pollinators

Interactions with angiosperms have been hypothesised to play a crucial role in driving diversification among insects, with a particular emphasis on pollinator insects. However, support for coevolutionary diversification in insect–plant interactions is weak. Macroevolutionary studies of insect and plant diversities support the hypothesis that angiosperms diversified after a peak in insect diversity in the Early Cretaceous. Here, we used the family-level fossil record of insects as a whole, and insect pollinator families in particular, to estimate diversification rates and the role of angiosperms on insect macroevolutionary history using a Bayesian process-based approach. We found that angiosperms played a dual role that changed through time, mitigating insect extinction in the Cretaceous and promoting insect origination in the Cenozoic, which is also recovered for insect pollinator families only. Although insects pollinated gymnosperms before the angiosperm radiation, a radiation of new pollinator lineages began as angiosperm lineages increased, particularly significant after 50 Ma. We also found that global temperature, increases in insect diversity, and spore plants were strongly correlated with origination and extinction rates, suggesting that multiple drivers influenced insect diversification and arguing for the investigation of different explanatory variables in further studies.

Slowing taxon cycle can explain biodiversity patterns on islands: Insights into the biogeography of the tropical South Pacific from molecular data

AbstractIslands in the tropical Pacific Ocean are renowned for high biodiversity and endemism despite having relatively small landmasses. However, our knowledge of how this biodiversity is formed remains limited. The taxon cycle, where well‐dispersed, earlier colonizers become displaced from coastal to inland habitats by new waves of colonizers, producing isolated, range‐restricted species, has been proposed to explain current biodiversity patterns. Here, we integrate the outcomes of phylogenetic studies in the region to investigate the sources, age, number of colonizations, and diversification of 16 archipelagos in the tropical and subtropical South Pacific. We then evaluate whether the results support the taxon cycle as a plausible mechanism for these observations. We find that most species in the Pacific arrived less than 5 Mya from geographically close sources, suggesting that colonization by new taxa is a frequent and ongoing process. Therefore, our findings are broadly consistent with the theory of the Taxon Cycle, which posits that ongoing colonization results in the gradual displacement of established lineages. Only the oldest archipelagos, New Caledonia and Fiji, do not conform to this trend, having proportionally less recent colonization events, suggesting that the taxon cycle may slow on older islands. This conclusion is further validated by New Caledonia having lower diversification rate estimates than younger islands. We found that diversification rates across archipelagos are negatively correlated with area and age. Therefore, a taxon cycle that slows with island age appears to be a suitable concept for understanding the dynamic nature and biodiversity patterns of the Pacific Islands.

Commonly used Bayesian diversification methods lead to biologically meaningful differences in branch-specific rates on empirical phylogenies

Abstract Identifying along which lineages shifts in diversification rates occur is a central goal of comparative phylogenetics; these shifts may coincide with key evolutionary events such as the development of novel morphological characters, the acquisition of adaptive traits, polyploidization or other structural genomic changes, or dispersal to a new habitat and subsequent increase in environmental niche space. However, while multiple methods now exist to estimate diversification rates and identify shifts using phylogenetic topologies, the appropriate use and accuracy of these methods are hotly debated. Here we test whether five Bayesian methods—Bayesian Analysis of Macroevolutionary Mixtures (BAMM), two implementations of the Lineage-Specific Birth–Death–Shift model (LSBDS and PESTO), the approximate Multi-Type Birth–Death model (MTBD; implemented in BEAST2), and the Cladogenetic Diversification Rate Shift model (ClaDS2)—produce comparable results. We apply each of these methods to a set of 65 empirical time-calibrated phylogenies and compare inferences of speciation rate, extinction rate, and net diversification rate. We find that the five methods often infer different speciation, extinction, and net-diversification rates. Consequently, these different estimates may lead to different interpretations of the macroevolutionary dynamics. The different estimates can be attributed to fundamental differences among the compared models. Therefore, the inference of shifts in diversification rates is strongly method dependent. We advise biologists to apply multiple methods to test the robustness of the conclusions or to carefully select the method based on the validity of the underlying model assumptions to their particular empirical system.

Reticulate evolution of the tertiary relict Osmanthus.

When interspecific gene flow is common, species relationships are more accurately represented by a phylogenetic network than by a bifurcating tree. This study aimed to uncover the role of introgression in the evolution of Osmanthus, the only genus of the subtribe Oleinae (Oleaceae) with its distribution center in East Asia. We built species trees, detected introgression, and constructed networks using multiple kinds of sequencing data (whole genome resequencing, transcriptome sequencing, and Sanger sequencing of nrDNA) combined with concatenation and coalescence approaches. Then, based on well-understood species relationships, historical biogeographic analyses and diversification rate estimates were employed to reveal the history of Osmanthus. Osmanthus originated in mid-Miocene Europe and dispersed to the eastern Tibetan Plateau in the late Miocene. Thereafter, it continued to spread eastwards. Phylogenetic conflict is common within the 'Core Osmanthus' clade and is seen at both early and late stages of diversification, leading to hypotheses of net-like species relationships. Incomplete lineage sorting proved ineffective in explaining phylogenetic conflicts and thus supported introgression as the main cause of conflicts. This study elucidates the diversification history of a relict genus in the subtropical regions of eastern Asia and reveals that introgression had profound effects on its evolutionary history.

Paleoenvironmental models for Australia and the impact of aridification on blindsnake diversification

AbstractAimShifts in diversification rates of Australian flora and fauna have been associated with aridification, but the relationship between diversification rates and aridity has never been quantified. We employed multiple approaches to reconstruct paleoenvironments of Australia for the first time. We used this information, and phylogenetic‐based analyses, to explore how changes in temperature and increasing aridity during the Neogene influenced the diversification of the Australian blindsnakes. We tested whether diversification rates differ between arid‐adapted and mesic‐adapted lineages.TaxonTyphlopidae, Anilios blindsnakes.LocationAustralia.Materials and MethodsWe estimated the historical biogeography of blindsnakes using BioGeoBEARS. We synthesised multiple approaches to reconstruct paleotemperature and paleoaridity of Australia during the Neogene. We fitted several birth‐death models and estimated diversification rates under paleoenvironmental conditions using RPANDA. We further compared diversification rates between arid‐adapted lineages versus mesic‐adapted lineages using ClaDS and GeoHiSSE.ResultsAncestral area estimation indicated Australian blindsnakes have tropical grassland origins. We found that Australia‐specific regional paleotemperature and paleoaridity provided a better explanation for diversification rate variation than global paleotemperature. Specifically, our best‐fitting model indicated that speciation rates of blindsnakes decreased with increasing aridity. We found no difference in diversification rates between arid‐ and mesic‐adapted lineages.Main ConclusionsSoon after dispersing to Australia, the common ancestors of Australian blindsnakes diversified rapidly in mesic habitats during the early Miocene. However, as the continent became increasingly arid, diversification rates decreased. We found that shifts in the environment led to the emergence of two major clades: one remaining in primarily mesic habitats and the other adapting to the expanding arid biome. Our results emphasise the importance of both arid and tropical biomes as sources and sinks of diversification.

Climbing mechanisms and the diversification of neotropical climbing plants across time and space.

Climbers germinate on the ground but need external support to sustain their stems, which are maintained attached to supports through modified organs, that is, climbing mechanisms. Specialized climbing mechanisms have been linked to higher diversification rates. Also, different mechanisms may have different support diameter restrictions, which might influence climbers' spatial distribution. We test these assumptions by linking climbing mechanisms to the spatiotemporal diversification of neotropical climbers. A dataset of climbing mechanisms is presented for 9071 species. WCVP was used to standardize species names, map geographical distributions, and estimate diversification rates of lineages with different mechanisms. Twiners appear concentrated in the Dry Diagonal of South America and climbers with adhesive roots in the Chocó region and Central America. However, climbing mechanisms do not significantly influence the distribution of neotropical climbers. Also, we found no strong support for correlations between specialized climbing mechanisms and higher diversification rates. Climbing mechanisms do not strongly impact the spatiotemporal diversification of neotropical climbers on a macroevolutionary scale. We argue that the climbing habit is a synnovation, meaning the spatiotemporal diversification it promotes is due to the sum effect of all the habit's traits rather than isolated traits, such as climbing mechanisms.

Deep vicariance and frequent transoceanic dispersal shape the evolutionary history of a globally distributed fern family.

The historical biogeography of ferns is typically expected to be dominated by long-distance dispersal due to their minuscule spores. However, few studies have inferred the historical biogeography of a large and widely distributed group of ferns to test this hypothesis. Our aims were to determine the extent to which long-distance dispersal vs. vicariance have shaped the history of the fern family Blechnaceae, to explore ecological correlates of dispersal and diversification, and to determine whether these patterns differ between the northern and southern hemispheres. We used sequence data for three chloroplast loci to infer a time-calibrated phylogeny for 154 of 265 species of Blechnaceae, including representatives of all genera in the family. This tree was used to conduct ancestral range reconstruction and stochastic character mapping, estimate diversification rates, and identify ecological correlates of diversification. Blechnaceae originated in Eurasia and began diversifying in the late Cretaceous. A lineage comprising most extant diversity diversified principally in the austral Pacific region around the Paleocene-Eocene Thermal Maximum. Land connections that existed near the poles during periods of warm climates likely facilitated migration of several lineages, with subsequent climate-mediated vicariance shaping current distributions. Long-distance dispersal is frequent and asymmetrical, with New Zealand/Pacific Islands, Australia, and tropical America being major source areas. Ancient vicariance and extensive long-distance dispersal have shaped the history of Blechnaceae in both the northern and southern hemispheres. The exceptional diversity in austral regions appears to reflect rapid speciation in these areas; mechanisms underlying this evolutionary success remain uncertain.

Fossils Do Not Substantially Improve, and May Even Harm, Estimates of Diversification Rate Heterogeneity.

The fossilized birth-death (FBD) model is a naturally appealing way of directly incorporating fossil information when estimating diversification rates. However, an important yet often overlooked property of the original FBD derivation is that it distinguishes between two types of sampled lineages. Here, we first discuss and demonstrate the impact of severely undersampling, and even not including fossils that represent samples of lineages that also had sampled descendants. We then explore the benefits of including fossils, generally, by implementing and then testing two types of FBD models, including one that converts a fossil set into stratigraphic ranges, in more complex likelihood-based models that assume multiple rate classes across the tree. Under various simulation scenarios, including a scenario that exists far outside the set of models we evaluated, including fossils rarely outperform analyses that exclude them altogether. At best, the inclusion of fossils improves precision but does not influence bias. Similarly, we found that converting the fossil set to stratigraphic ranges, which is one way to remedy the effects of undercounting the number of k-type fossils, results in turnover rates and extinction fraction estimates that are generally underestimated. Although fossils remain essential for understanding diversification through time, in the specific case of understanding diversification given an existing, largely modern tree, they are not especially beneficial. [Fossilized birth-death; fossils; MiSSE; state speciation extinction; stratigraphic ranges; turnover rate.].

A flexible method for estimating tip diversification rates across a range of speciation and extinction scenarios.

Estimates of diversification rates at the tips of a phylogeny provide a flexible approach for correlation analyses with multiple traits and to map diversification rates in space while also avoiding the uncertainty of deep time rate reconstructions. Available methods for tip rate estimation make different assumptions, and thus their accuracy usually depends on the characteristics of the underlying model generating the tree. Here, we introduce MiSSE, a trait-free, state-dependent speciation and extinction approach that can be used to estimate varying speciation, extinction, net diversification, turnover, and extinction fractions at the tips of the tree. We compare the accuracy of tip rates inferred by MiSSE against similar methods and demonstrate that, due to certain characteristics of the model, the error is generally low across a broad range of speciation and extinction scenarios. MiSSE can be used alongside regular phylogenetic comparative methods in trait-related diversification hypotheses, and we also describe a simple correction to avoid pseudoreplication from sister tips in analyses of independent contrasts. Finally, we demonstrate the capabilities of MiSSE, with a renewed focus on classic comparative methods, to examine the correlation between plant height and turnover rates in eucalypts, a species-rich lineage of flowering plants.

The scaling of diversification rates with age is likely explained by sampling bias.

Numerous phylogenetic studies reported the existence of a pervasive scaling relationship between the ages of extant eukaryotic clades and their estimated diversification rates. The causes of this age-rate-scaling (ARS), whether biological and/or artifactual, remain unresolved. Here we fit diversification models to thousands of eukaryotic time-calibrated phylogenies to explore multiple potential causes of the ARS including parameter non-identifiability, model inadequacy, biases in taxonomic practice, and an important and ubiquitous form of sampling bias-preferentially analyzing larger extant clades. We distinguish between two mechanism by which such sampling biases can cause an ARS: First, by favoring clades that happen to be unusually large merely by chance (i.e., due to the stochastic nature of the cladogenic process), thus leading to rate overestimation, and second, by favoring clades that have truly higher diversification rates. We find that, of the proposed explanations, only sampling biases are likely to contribute to the observed ARS. We develop methods for fully correcting for sampling bias mechanism 1, and find that despite these corrections a substantial ARS remains. We then confirm using simulations that preferring trees with truly higher rates (mechanism 2) likely explains this residual ARS. Since we do not have a completely unbiased sample of clades, including extinct ones, for phylogenetic analyses, it is difficult to demonstrate unambiguously that sampling biases are the sole cause of the ARS. Sampling biases are, however, a parsimonious and plausible explanation for this widely observed macroevolutionary pattern, and this has implications for how we interpret the distribution of diversification rate estimates in extantclades.

Reconstruction of State-Dependent Diversification: Integrating Phenotypic Traits into Molecular Phylogenies.

The relative contribution of speciation and extinction into current diversity is certainly unknown, but mathematical frameworks that use genetic information have been developed to provide estimates of these processes. To that end, it is necessary to reconstruct molecular phylogenetic trees which summarize ancestor-descendant relationships as well as the timing of evolutionary events (i.e., rates). Nevertheless, diversification models show poor fit when assuming that single rate of speciation/extinction is constant over time and across lineages: species exhibit such a great variation in features that it is unlikely they give birth and die at the same pace. The state-dependent diversification framework (SSE) reconciles the species phenotypic variation with heterogeneous rates of diversification observed in a clade. This family of models allows testing contrasting hypotheses on mode of speciation, trait evolution, and its influence on speciation/extinction regimes. Although microbial species richness outnumbers diversity in plants and animals, diversification models are underused in microbiology. Here, we introduce microbiologists to models that estimate diversification rates and provide a detailed description of SSE models. Besides theoretical principles underlying the method, we also show how SSE analysis should be set up in R. We use pH evolution in Thaumarchaeota to explain its evolutionary dynamic in the light of SSE model. We hope this chapter spurs the study of trait evolution and evolutionary outcomes in microorganisms.

Phylogeny, biogeography and diversification of the mining bee family Andrenidae

AbstractThe mining bees (Andrenidae) are a major bee family of over 3000 described species with a nearly global distribution. They are a particularly significant component of northern temperate ecosystems and are critical pollinators in natural and agricultural settings. Despite their ecological and evolutionary significance, our knowledge of the evolutionary history of Andrenidae is sparse and insufficient to characterize their spatiotemporal origin and phylogenetic relationships. This limits our ability to understand the diversification dynamics that led to the second most species‐rich genus of all bees, Andrena Fabricius, and the most species‐rich North American genus, Perdita Smith. Here, we develop a comprehensive genomic dataset of 195 species of Andrenidae, including all major lineages, to illuminate the evolutionary history of the family. Using fossil‐informed divergence time estimates, we characterize macroevolutionary dynamics, incorporate paleoclimatic information, and present our findings in the context of diversification rate estimates for all other bee tribes. We found that diversification rates of Andrenidae steeply increased over the past 15 million years, particularly in the genera Andrena and Perdita. This suggests that these two groups and the brood parasites of the genus Nomada Scopoli (Apidae), which are the primary cleptoparasitic counterparts of Andrena, are similar in age and represent the fastest diversifying lineages of all bees. Using our newly developed time frame of andrenid evolution, we estimate a late Cretaceous origin in South America for the family and reconstruct the past dispersal events that led to its present‐day distribution.

Evolutionary diversification in the hyper-diverse montane forests of the tropical Andes: radiation ofMacrocarpaea(Gentianaceae) and the possible role of range expansion

AbstractThe humid mid-elevation montane forests (MMF) of the tropical Andes harbour high levels of plant species diversity, contributing to the exceptional overall diversity of the tropical Andean biodiversity hotspot. However, little is known about the diversification dynamics of MMF plant lineages compared to lineages in other Andean biomes. Here, we use Macrocarpaea (Gentianaceae) to investigate patterns of plant diversification in the MMF, using molecular dating with fossils and secondary calibration (from a family-wide phylogenetic analysis of Gentianaceae). We sequenced 76 of 118 recognized Macrocarpaea spp. for six markers to reconstruct a time-calibrated phylogenetic tree and infer the historical biogeography of Macrocarpaea using maximum-likelihood methods implemented in BioGeoBEARS, estimating diversification rates through time and among lineages with BAMM. We document a rapid radiation of Macrocarpaea in Andean MMF coinciding with rapid colonization and range expansion across the entire distribution of the genus in the Andes starting 7.2 Mya. Our results support allopatric founder-event speciation as the dominant process contributing to geographical phylogenetic structure across the genus. We propose that establishment of the MMF in the late Miocene, when the Andes attained critical elevation to modify regional climates, provided large new areas of suitable habitat for Macrocarpaea to quickly colonize and expand through repeated founder-events. We suggest that this wave of colonization and range expansion triggered rapid diversification, and, as the MMF became progressively occupied, the diversification rate slowed. Our study also supports the idea that MMF plant radiations are older and more slowly evolving than the quickly evolving lineages in the recent Andean high-elevation grasslands.

Limited evidence for a positive relationship between hybridization and diversification across seed plant families.

Hybridization has experimental and observational ties to evolutionary processes and outcomes such as adaptation, speciation, and radiation. Although it has been hypothesized that hybridization and diversification are positively correlated, this idea remains largely untested empirically, and hybridization can also potentially reduce diversity. Here, we use a hybridization database on 170 seed plant families, life history information, and a time-calibrated phylogeny to test for phylogenetically-corrected associations between hybridization and diversification rates, while also taking into account life-history traits that may be correlated with both processes. We use three methods to estimate diversification rates and two metrics of hybridization. Although hybridization explains only a small amount of overall variation in diversification rates, we show that diversification and hybridization are sometimes positively correlated, although the effect sizes are very small. Moreover, the relationship remains detectable when incorporating the correlations between diversification and two other life history characteristics, perenniality and woodiness. We discuss potential mechanisms for this association under four different scenarios: hybridization may drive diversification, diversification may drive hybridization, both hybridization and diversification may jointly be driven by other factors, or, as an alternative, that there is in fact no relationship between the two. We suggest future studies to disentangle the causal structure.

Origin and diversification of flax and their relationship with heterostyly across the range

AbstractAimUnderstanding plant diversity and how different traits have shaped the current biodiversity setting across the world is one of the major challenges for evolutionary biology. In this sense, genus Linum have been broadly studied as a model of species showing heterostyly, but no studies have attempted to investigate possible correlations between heterostyly and diversification. Thus, in this study we aim to explore the origin and diversification of the genus Linum and to determine its centre of diversity and potential source for the colonisation of other areas. Also, we aim to study how heterostyly may have shaped diversification rates and colonisation patterns in the genus.LocationWorldwide (focused on the Western Palearctic).TaxonGenus Linum L. (Linaceae).MethodsWe analysed nuclear ITS and plastid ndhF, matK and trnL‐F DNA regions in a total of 103 samples of 93 different species of the genus Linum, as well as seven samples from other Linaceae. We performed divergence time analysis in BEAST2 under a birth‐death tree model, then used the resulting tree for an ancestral area reconstruction using the R package “BioGeoBEARS.” Finally, we estimated diversification rates using BAMM and examined the correlation between diversification rates and geographic ranges and heterostyly.ResultsLinum s.l. diverged during the late Eocene to mid Oligocene (27.2–38.29 Ma at 95% highest posterior density interval) in the Western Palearctic, where most species diversified. Within‐area speciation is the main mechanism of diversification in the genus. Most dispersal events occurred from the Western Palearctic to other regions, probably through long‐distance dispersal (LDD). No changes were found regarding diversification rates in specific clades or in relation with reproductive system (heterostyly) or geographic areas. Colonisation of new areas was achieved mostly by monomorphic lineages, whereas heterostylous species mostly remained in the ancestral Western Paleartic area.Main conclusionsThe Western Palearctic acted as a source of dispersal in seven out of nine total dispersal events but never as a sink. All species or lineages that colonised new areas after LDD were monomorphic for style length, as predicted by the theory on reproductive traits of colonising species. Thus, heterostyly is shown to affect establishment success in a new area. Neither biogeographic changes nor analysed trait changes can explain speciation nor extinction rates in Linum. Our results confirm that the evolution of heterostyly is related to the paleogeographic history and are not consistent with the idea that a key innovation or “dispersification” has shaped the diversification patterns in Linum.

Polyploidy Expands the Range of Centaurium (Gentianaceae).

The Mediterranean region is one of the most important worldwide hotspots in terms of number of species and endemism, and multiple hypotheses have been proposed to explain how diversification occurred in this area. The contribution of different traits to the diversification process has been evaluated in different groups of plants. In the case of Centaurium (Gentianaceae), a genus with a center of diversity placed in the Mediterranean region, polyploidy seems to have been an important driver of diversification as more than half of species are polyploids. Moreover, ploidy levels are strongly geographically structured across the range of the genus, with tetraploids distributed towards more temperate areas in the north and hexaploids in more arid areas towards the south. We hypothesize that the diversification processes and biodiversity patterns in Centaurium are explained by the coupled formation of polyploid lineages and the colonization of different areas. A MCC tree from BEAST2 based on three nuclear DNA regions of a total of 26 taxa (full sampling, of 18 species and 8 subspecies) was used to perform ancestral area reconstruction analysis in “BioGeoBEARS.” Chromosome evolution was analyzed in chromEvol and diversification in BAMM to estimate diversification rates. Our results suggest that two major clades diverged early from the common ancestor, one most likely in the western Mediterranean and the other in a widespread area including west and central Asia (but with high uncertainty in the exact composition of this widespread area). Most ancestral lineages in the western clade remained in or around the western Mediterranean, and dispersal to other areas (mainly northward and eastward), occurred at the tips. Contrarily, most ancestral lineages in the widespread clade had larger ancestral areas. Polyploidization events in the western clade occurred at the tips of the phylogeny (with one exception of a polyploidization event in a very shallow node) and were mainly tetraploid, while polyploidization events occurred in the widespread clade were at the tips and in an ancestral node of the phylogeny, and were mainly hexaploid. We show how ancestral diploid lineages remained in the area of origin, whereas recent and ancestral polyploidization could have facilitated colonization and establishment in other areas.

Genome-wide macroevolutionary signatures of key innovations in butterflies colonizing new host plants

The mega-diversity of herbivorous insects is attributed to their co-evolutionary associations with plants. Despite abundant studies on insect-plant interactions, we do not know whether host-plant shifts have impacted both genomic adaptation and species diversification over geological times. We show that the antagonistic insect-plant interaction between swallowtail butterflies and the highly toxic birthworts began 55 million years ago in Beringia, followed by several major ancient host-plant shifts. This evolutionary framework provides a valuable opportunity for repeated tests of genomic signatures of macroevolutionary changes and estimation of diversification rates across their phylogeny. We find that host-plant shifts in butterflies are associated with both genome-wide adaptive molecular evolution (more genes under positive selection) and repeated bursts of speciation rates, contributing to an increase in global diversification through time. Our study links ecological changes, genome-wide adaptations and macroevolutionary consequences, lending support to the importance of ecological interactions as evolutionary drivers over long time periods.

Biogeographic diversification of Mahonia (Berberidaceae): Implications for the origin and evolution of East Asian subtropical evergreen broadleaved forests

The subtropical evergreen broadleaved forests (EBLFs) inhabit large areas of East Asia and harbor rich biodiversity and high endemism. However, the origin and evolution of biodiversity of East Asian subtropical EBLFs remain poorly understood. Here, we used Mahonia (Berberidaceae), an eastern Asian-western North American disjunct evergreen genus, to obtain new insights into the historical assembly of this biome. We present the most comprehensive phylogenetic analysis of Mahonia do date based on six nuclear and plastid loci. Using the phylogenetic framework, we estimated divergence times, reconstructed ancestral ranges, inferred evolutionary shift of habitats, and estimated diversification rates. Mahonia and each of its two groups (Orientales and Occidentales) are strongly supported as monophyletic. Mahonia originated in western North America during the late Eocene (c. 40.41 Ma) and subsequently dispersed into East Asia prior to the early Oligocene (c. 32.65 Ma). The North Atlantic Land Bridge might have played an important role in population exchanges of Mahonia between East Asia and western North America. The western North American Occidentales began to diversify in summer-dry climates and open landscapes in the early Miocene, whereas the eastern Asian Orientales began to diversify in subtropical EBLFs in the early Miocene and furthermore had a rapid lineage accumulation since the late Miocene. The net diversification rate of Mahonia in eastern Asia appeared to be higher than that in western North America, which is ascribed to lower extinction rates and ecological opportunity. Our findings suggest that western North America is a source of biodiversity of East Asian subtropical EBLFs. This biome in eastern Asia began to rise in the early Miocene and further diversified in the late Miocene, driven by the intensifying East Asian summer monsoon during these two periods.