Increase In Diversification Rate Research Articles

Evolution of reproductive traits and selfing syndrome in the sub-endemic Mediterranean genus Centaurium Hill (Gentianaceae)

AbstractIn flowering plants, the shift from outcrossing to selfing is associated with a set of correlated changes in morphological and reproductive features known as the ‘selfing syndrome’. Species of the sub-endemic Mediterranean genus Centaurium Hill (Gentianaceae) exhibit a wide array of flower traits related to pollination biology and different ploidy levels. We explored if the evolutionary transitions of seven flower traits and life cycle, typically associated with the selfing syndrome, are related to polyploidy, diversification patterns, divergence times and the geological and climatic history of the Mediterranean Basin. Using 26 species of Centaurium we reconstructed a phylogenetic tree, inferred the ancestral states of the selected traits, estimated their phylogenetic signal and tested the correlative evolution among them. We found a significant increase in diversification rates during the Quaternary. Anther length, flower size, herkogamy and polyploidy undergo rapid state transitions without phylogenetic signal that could be the result of adaptation for selfing. Changes in character states do not show evidence of correlative evolution among them, as would be predicted during the evolution of selfing syndrome. The evolution of reproductive traits in Centaurium has probably relied on a more diverse array of drivers than just reproductive assurance or polyploidy events.

Pleistocene diversification in an ancient lineage: a role for glacial cycles in the evolutionary history of Dioon Lindl. (Zamiaceae).

Recent estimates of crown ages for cycad genera (Late Miocene) challenge us to consider what processes have produced the extant diversity of this ancient group in such relatively little time. Pleistocene climate change has driven major shifts in species distributions in Mexico and may have led to speciation in the genus Dioon by forcing populations to migrate up in elevation, thereby becoming separated by topography. We inferred orthologs from transcriptomes of five species and sequenced these in 42 individuals representing all Dioon species. From these data and published plastid sequences, we inferred dated species trees and lineage-specific diversification rates. Analyses of 84 newly sequenced nuclear orthologs and published plastid data confirm four major clades within Dioon, all of Pleistocene age. Gene tree analysis, divergence dates, and an increase in diversification rate support very recent and rapid divergence of extant taxa. This study confirms the Pleistocene age of Dioon species and implicates Pleistocene climate change and established topography in lineage spitting. These results add to our understanding of the cycads as evolutionarily dynamic lineages, not relicts or evolutionary dead ends. We also find that well-supported secondary calibration points can be reliable in the absence of fossils. Our hypothesis of lineage splitting mediated by habitat shifts may be applicable to other taxa that are restricted to elevation specific ecotones.

Climate and host-plant associations shaped the evolution of ceutorhynch weevils throughout the Cenozoic.

Using molecular phylogenetic data and methods we inferred divergence times and diversification patterns for the weevil subfamily Ceutorhynchinae in the context of host‐plant associations and global climate over evolutionary time. We detected four major diversification shifts that correlate with both host shifts and major climate events. Ceutorhynchinae experienced an increase in diversification rate at ∼53 Ma, during the Early Eocene Climate Optimum, coincident with a host shift to Lamiaceae. A second major diversification phase occurred at the end of the Eocene (∼34 Ma). This contrasts with the overall deterioration in climate equability at the Eocene‐Oligocene boundary, but tracks the diversification of important host plant clades in temperate (higher) latitudes, leading to increased diversification rates in the weevil clades infesting temperate hosts. A third major phase of diversification is correlated with the rising temperatures of the Late Oligocene Warming Event (∼26.5 Ma); diversification rates then declined shortly after the Middle Miocene Climate Transition (∼14.9 Ma). Our results indicate that biotic and abiotic factors together explain the evolution of Ceutorhynchinae better than each of these drivers viewed in isolation.

Augmenting Trait-Dependent Diversification Estimations with Fossil Evidence: A Case Study Using Osmoregulatory Neurovasculature

When comparative neuromorphological studies are extended into evolutionary contexts, traits of interest are often linked to diversification patterns. Features demonstrably associated with increases in diversification rates and the infiltration or occupation of novel niche spaces are often termed “key innovations.” Within the past decade, phylogenetically informed methods have been developed to test key innovation hypotheses and evaluate the influence these traits have had in shaping modern faunas. This is primarily accomplished by estimating state-dependent speciation and extinction rates. These methods have important caveats and guidelines related to both calculation and interpretation, which are necessary to understand in cases of discrete (qualitative) character analysis, as can be common when studying the evolution of neuromorphology. In such studies, inclusion of additional characters, acknowledgement of character codistribution, and addition of sister clade comparison should be explored to ensure model accuracy. Even so, phylogenies provide a survivor-only examination of character evolution, and paleontological contexts may be necessary to replicate and confirm results. Here, I review these issues in the context of selective brain cooling – a neurovascular-mediated osmoregulatory physiology that dampens hypothalamic responses to heat stress and reduces evaporative water loss in large-bodied mammals. This binary character provides an example of the interplay between sample size, evenness, and character codistribution. Moreover, it allows for an opportunity to compare phylogenetically constrained results with paleontological data, augmenting survivor-only analyses with observable extinction patterns. This trait- dependent diversification example indicates that selective brain cooling is significantly associated with the generation of modern large-mammal faunas. Importantly, paleontological data validate phylogenetic patterns and demonstrate how suites of characters worked in concert to establish the large-mammal communities of today.

Exon-Capture-Based Phylogeny and Diversification of the Venomous Gastropods (Neogastropoda, Conoidea).

Transcriptome-based exon capture methods provide an approach to recover several hundred markers from genomic DNA, allowing for robust phylogenetic estimation at deep timescales. We applied this method to a highly diverse group of venomous marine snails, Conoidea, for which published phylogenetic trees remain mostly unresolved for the deeper nodes. We targeted 850 protein coding genes (678,322 bp) in ca. 120 samples, spanning all (except one) known families of Conoidea and a broad selection of non-Conoidea neogastropods. The capture was successful for most samples, although capture efficiency decreased when DNA libraries were of insufficient quality and/or quantity (dried samples or low starting DNA concentration) and when targeting the most divergent lineages. An average of 75.4% of proteins was recovered, and the resulting tree, reconstructed using both supermatrix (IQ-tree) and supertree (Astral-II, combined with the Weighted Statistical Binning method) approaches, are almost fully supported. A reconstructed fossil-calibrated tree dates the origin of Conoidea to the Lower Cretaceous. We provide descriptions for two new families. The phylogeny revealed in this study provides a robust framework to reinterpret changes in Conoidea anatomy through time. Finally, we used the phylogeny to test the impact of the venom gland and radular type on diversification rates. Our analyses revealed that repeated losses of the venom gland had no effect on diversification rates, while families with a breadth of radula types showed increases in diversification rates, thus suggesting that trophic ecology may have an impact on the evolution of Conoidea.

Ecological opportunity may facilitate diversification in Palearctic freshwater organisms: a case study on hydrobiid gastropods

BackgroundDifferences in species richness among phylogenetic clades are attributed to clade age and/or variation in diversification rates. Access to ecological opportunity may trigger a temporary increase in diversification rates and ecomorphological variation. In addition, lower body temperatures in poikilothermic animals may result in decreasing speciation rates as proposed by the metabolic theory of ecology. For strictly freshwater organisms, environmental gradients within a river continuum, linked to elevation and temperature, might promote access to ecological opportunity and alter metabolic rates, eventually influencing speciation and extinction processes. To test these hypotheses, we investigated the influence of environmental temperature and elevation, as proxies for body temperature and ecological opportunity, respectively, on speciation rates and ecomorphological divergence. As model systems served two closely related gastropod genera with unequal species richness and habitat preferences – Pseudamnicola and Corrosella.ResultsLineage-through-time plots and Bayesian macroevolutionary modeling evidenced that Pseudamnicola species, which typically live in lower reaches of rivers, displayed significantly elevated speciation rates in comparison to the ‘headwater genus’ Corrosella. Moreover, state-dependent speciation models suggested that the speciation rate increased with decreasing elevation, supporting the ecological opportunity hypothesis. In contrast, a significant effect of environmental temperature, as proposed by the metabolic theory of ecology, could not be observed. Disparity-through-time plots, models of ecomorphological evolution, and ancestral habitat estimation showed for Pseudamnicola species rapid morphological divergence shortly after periods of elevational and habitat divergence. In contrast, Corrosella species did not deviate from null models of drift-like evolution.ConclusionOur finding that speciation rates are correlated with elevation and ecomorphological disparity but not with environmental temperatures suggests that differences in ecological opportunity may have played a key role in Corrosella and Pseudamnicola diversifications. We propose that Pseudamnicola lineages experienced higher ecological opportunity through dispersal to new locations or habitats in lowlands, which may explain the increase in speciation rates and morphological change. In contrast, the evolution of Corrosella in headwaters is likely less facilitated by the environment and more by non-ecological processes.

On geographic barriers and Pleistocene glaciations: Tracing the diversification of the Russet-crowned Warbler (Myiothlypis coronata) along the Andes.

We studied the phylogeography and plumage variation of the Russet-crowned Warbler (Myiothlypis coronata), from Venezuela to Bolivia, with focus on populations from Ecuador and northern Peru. We analyzed sequences of mitochondrial and nuclear genes, geographic distributions, as well as photographs of specimens deposited at museum collections. Phylogenetic analyses identified three major lineages formed by populations from: Venezuela and Colombia (M. c. regulus), Ecuador and northern Peru (M. elata, M. castaneiceps, M. orientalis, M. c. chapmani), and central Peru and Bolivia (M. c. coronata). We found further population structure within M. c. regulus and M. c. coronata, and population structure and complexity of plumage variation within the Ecuador-northern Peru lineage. Time-calibrated trees estimated that most intraspecific variation originated during the Pleistocene; however, this pattern may not be attributed to an increase in diversification rate during that period. We discuss these results in the context of the importance of geographic-ecological barriers in promoting lineage diversification along the Andes and put forward a preliminary taxonomic proposal for major lineages identified in this study.

Evolutionary history of Coleoptera revealed by extensive sampling of genes and species

Beetles (Coleoptera) are the most diverse and species-rich group of insects, and a robust, time-calibrated phylogeny is fundamental to understanding macroevolutionary processes that underlie their diversity. Here we infer the phylogeny and divergence times of all major lineages of Coleoptera by analyzing 95 protein-coding genes in 373 beetle species, including ~67% of the currently recognized families. The subordinal relationships are strongly supported as Polyphaga (Adephaga (Archostemata, Myxophaga)). The series and superfamilies of Polyphaga are mostly monophyletic. The species-poor Nosodendridae is robustly recovered in a novel position sister to Staphyliniformia, Bostrichiformia, and Cucujiformia. Our divergence time analyses suggest that the crown group of extant beetles occurred ~297 million years ago (Mya) and that ~64% of families originated in the Cretaceous. Most of the herbivorous families experienced a significant increase in diversification rate during the Cretaceous, thus suggesting that the rise of angiosperms in the Cretaceous may have been an ‘evolutionary impetus’ driving the hyperdiversity of herbivorous beetles.

Phylogenetic and paleobotanical evidence for late Miocene diversification of the Tertiary subtropical lineage of ivies (Hedera L., Araliaceae)

BackgroundHedera (ivies) is one of the few temperate genera of the primarily tropical Asian Palmate group of the Araliaceae, which extends its range out of Asia to Europe and the Mediterranean basin. Phylogenetic and phylogeographic results suggested Asia as the center of origin and the western Mediterranean region as one of the secondary centers of diversification. The bird-dispersed fleshy fruits of ivies suggest frequent dispersal over long distances (e.g. Macaronesian archipelagos), although reducing the impact of geographic barriers to gene flow in mainland species. Genetic isolation associated with geographic barriers and independent polyploidization events have been postulated as the main driving forces of diversification. In this study we aim to evaluate past and present diversification patterns in Hedera within a geographic and temporal framework to clarify the biogeographic history of the genus.ResultsPhylogenetic (biogeographic, time divergence and diversification) and phylogeographic (coalescence) analyses using four DNA regions (nrITS, trnH-psbA, trnT-trnL, rpl32) revealed a complex spatial pattern of lineage divergence. Scarce geographic limitation to gene flow and limited diversification are observed during the early-mid Miocene, followed by a diversification rate increase related to geographic divergence from the Tortonian/Messinian. Genetic and palaeobotanical evidence points the origin of the Hedera clade in Asia, followed by a gradual E-W Asian extinction and the progressive E-W Mediterranean colonization. The temporal framework for the E Asia - W Mediterranean westward colonization herein reported is congruent with the fossil record. Subsequent range expansion in Europe and back colonization to Asia is also inferred. Uneven diversification among geographic areas occurred from the Tortonian/Messinian onwards with limited diversification in the newly colonized European and Asian regions. Eastern and western Mediterranean regions acted as refugia for Miocene and post-Miocene lineages, with a similar role as consecutive centers of centrifugal dispersal (including islands) and speciation.ConclusionsThe Miocene Asian extinction and European survival of Hedera question the general pattern of Tertiary regional extinction of temperate angiosperms in Europe while they survived in Asia. The Tortonian/Messinian diversification increase of ivies in the Mediterranean challenges the idea that this aridity period was responsible for the extinction of the Mediterranean subtropical Tertiary flora. Differential responses of Hedera to geographic barriers throughout its evolutionary history, linked to spatial isolation related to historical geologic and climatic constraints may have shaped diversification of ivies in concert with recurrent polyploidy.

Species-level phylogeny, fruit evolution and diversification history of Geranium (Geraniaceae)

The cosmopolitan genus Geranium L. (Geraniaceae) consists of c. 350 species distributed in temperate habitats worldwide, with most of its diversity concentrated in the Mediterranean region. Unlike other genera in Geraniaceae, the species of Geranium present contrasting seed discharge syndromes, i.e. the ‘Erodium-type’ (ET), the ‘carpel-projection type’ (CP), the ‘seed-ejection type’ (SE), and the ‘inoperative type’ (IT), which have been used to delimit major groups within the genus. However, phylogenetic relationships within Geranium are unknown and so is the evolution of the different seed discharge mechanisms. Here, we used a calibrated multispecies coalescent approach to infer the species-level phylogeny and divergence times of the genus based on chloroplast (rbcL, trnL-trnF) and nuclear (ITS) DNA sequences. Our sampling represents most of the morphological variation described in the genus. We reconstruct the evolution of the seed discharge mechanism using ancestral state reconstruction (ASR) techniques on the multispecies coalescent tree, and assess the association between fruit type evolution and species diversification using stochastic birth-death and trait-dependent diversification models. Finally, we reconstruct the early biogeographic history of the genus using discrete and continuous biogeographic analyses of species distribution centroids, including fossil evidence and tip dates. Our results show that fruit type is homoplasious and that the classification based on fruit type in Geranium is artificial. The taxonomy and putative apomorphic characters for Geranium are discussed. ASR of the fruit characters suggests that ET may represent the ancestral state in Geranium and from which CP originated twice, IT presumably once, and SE twice. The independent appearance of the SE syndrome is in both cases associated with increases in diversification rates in the genus. The biogeographic analysis centers the origin and early 10Ma diversification of Geranium on the Mediterranean region. The evolution of seed discharge mechanism about 5Ma might have allowed the species of Geranium to increase in geographic range and to ultimately, diversify.

How the Aridification of Australia Structured the Biogeography and Influenced the Diversification of a Large Lineage of Australian Cicadas.

Over the last 30 million years, Australia's landscape has undergone dramatic cooling and drying due to the establishment of the Antarctic Circumpolar Current and change in global CO$_{2}$ levels. Studies have shown that many Australian organisms went extinct during these major cooling events, while others experienced adaptive radiations and increases in diversification rates as a result of exploiting new niches in the arid zone. Despite the many studies on diversification and biogeography in Australia, few have been continent-wide and none have focused on a group of organisms adapted to feeding on plants. We studied 162 species of cicadas in the Australian Pauropsalta complex, a large generic lineage within the tribe Cicadettini. We asked whether there were changes in the diversification rate of Pauropsalta over time and if so: 1) which clades were associated with the rate change? 2) did timing of rate shifts correspond to known periods of dramatic historical climate change, 3) did increases in diversification rate along select lineages correspond to adaptive radiations with movement into the arid zone? To address these questions, we estimated a molecular phylogeny of the Pauropsalta complex using ${\sim}$5300 bp of nucleotide sequence data distributed among five loci (one mtDNA locus and four nDNA loci). We found that this large group of cicadas did not diversify at a constant rate as they spread through Australia; instead the signature of decreasing diversification rate changed roughly around the time of the expansion of the east Antarctic ice sheets ${\sim}$16 Ma and the glaciation of the northern hemisphere ${\sim}$3 Ma. Unlike other Australian taxa, the Pauropsalta complex did not explosively radiate in response to an early invasion of the arid zone. Instead multiple groups invaded the arid zone and experienced rates of diversification similar to mesic-distributed taxa. We found evidence for relictual groups, located in pre-Mesozoic habitat, that have not diversified and continue to reside on mesic hosts in isolated "habitat islands". Future work should focus on groups of similar ages with similar distribution patterns to determine whether this tempo and pattern of diversification and biogeography is consistent with evidence from other phytophagous insects.

Is the switch to an ectomycorrhizal state an evolutionary key innovation in mushroom-forming fungi? A case study in the Tricholomatineae (Agaricales).

Although fungi are one of the most diverse groups of organisms, little is known about the processes that shape their high taxonomic diversity. This study focuses on evolution of ectomycorrhizal (ECM) mushroom-forming fungi, symbiotic associates of many trees and shrubs, in the suborder Tricholomatineae of the Agaricales. We used the BiSSE model and BAMM to test the hypothesis that the ECM habit represents an evolutionary key innovation that allowed the colonization of new niches followed by an increase in diversification rate. Ancestral state reconstruction (ASR) supports the ancestor of the Tricholomatineae as non-ECM. We detected two diversification rate increases in the genus Tricholoma and the Rhodopolioid clade of the genus Entoloma. However, no increases in diversification were detected in the four other ECM clades of Tricholomatineae. We suggest that diversification of Tricholoma was not only due to the evolution of the ECM lifestyle, but also to the expansion and dominance of its main hosts and ability to associate with a variety of hosts. Diversification in the Rhodopolioid clade could be due to the unique combination of spore morphology and ECM habit. The spore morphology may represent an exaptation that aided spore dispersal and colonization. This is the first study to investigate rate shifts across a phylogeny that contains both non-ECM and ECM lineages.

Explosive ice age diversification of kiwi

Molecular dating largely overturned the paradigm that global cooling during recent Pleistocene glacial cycles resulted in a burst of species diversification although some evidence exists that speciation was commonly promoted in habitats near the expanding and retracting ice sheets. Here, we used a genome-wide dataset of more than half a million base pairs of DNA to test for a glacially induced burst of diversification in kiwi, an avian family distributed within several hundred kilometers of the expanding and retracting glaciers of the Southern Alps of New Zealand. By sampling across the geographic range of the five kiwi species, we discovered many cryptic lineages, bringing the total number of kiwi taxa that currently exist to 11 and the number that existed just before human arrival to 16 or 17. We found that 80% of kiwi diversification events date to the major glacial advances of the Middle and Late Pleistocene. During this period, New Zealand was repeatedly fragmented by glaciers into a series of refugia, with the tiny geographic ranges of many kiwi lineages currently distributed in areas adjacent to these refugia. Estimates of effective population size through time show a dramatic bottleneck during the last glacial cycle in all but one kiwi lineage, as expected if kiwi were isolated in glacially induced refugia. Our results support a fivefold increase in diversification rates during key glacial periods, comparable with levels observed in classic adaptive radiations, and confirm that at least some lineages distributed near glaciated regions underwent rapid ice age diversification.

Out‐of‐Tibet: the spatio‐temporal evolution of Gentiana (Gentianaceae)

AbstractAimWe investigated the historical biogeography and diversification of Gentiana L. (Gentianaceae). Our study depicts the origin and dispersal routes of this alpine genus, and the role of the uplift of the Qinghai–Tibet Plateau (QTP) and past climate changes as triggers for its diversification.LocationTibeto‐Himalayan region and world‐wide mountain habitats.MethodsOur sampling represents more than 50% of the extant Gentiana species, including all sections across their entire geographical ranges. We investigated the evolutionary history of Gentiana using phylogenetic reconstructions (maximum likelihood and Bayesian inference) of ITS, atpB–rbcL and trnL–trnF sequences, as well as molecular dating with beast. We tested two approaches of ancestral area reconstructions (DEC, DIVA) in BioGeoBEARS and investigated diversification rates using BAMM.ResultsThe common ancestor of Gentiana and subtribe Gentianinae lived in the QTP region at around 34 (25–45) million years ago (Ma), and 40 (29–52) Ma respectively. From the surroundings of the QTP, Gentiana lineages dispersed to eastern China, Taiwan, Europe, North and South America, Australia and New Guinea, from mid‐Miocene onward (c. 15 Ma–present), with only one older dispersal event to Europe (c. 37–21 Ma). Diversification rates gradually increased over time, and two switches of diversification rates were identified in Gentianinae (c. 7 Ma, simultaneously in the Pneumonanthe/Cruciata lineage and in Tripterospermum).Main conclusionsGentiana existed in the QTP region throughout most of its uplift history following the India‐Asia collision. This region acted as the primary source area for dispersals to many areas of the world. Because steady increase in diversification rates coincides with the extension of the QTP, we argue that the museum theory rather than the explosive radiation theory prevails for gentians in this region, although rare shifts of diversification rates are associated with niche shifts across the alpine/subalpine ecotone.

Biogeography of the cosmopolitan sedges (Cyperaceae) and the area‐richness correlation in plants

AbstractAimAcross angiosperm families, the area occupied by a family is strongly correlated with its richness. We explore the causes of this area‐richness correlation using the cosmopolitan family, Cyperaceae Juss., as a model. We test the hypothesis that, despite a proposed tropical origin, temperate lineages in the family diversified at elevated rates. We test the hypothesis that the area‐richness correlation is maintained within intrafamilial clades, and that this relationship could be described as a function of niche space. We also test the hypothesis that the partitioning of geographical and ecological space, not the extent of this space, is the factor most closely associated with clade richness.LocationCosmopolitan.MethodsWe use molecular data from four genes sequenced in 384 taxa to develop a chronogram of Cyperaceae. We then develop a model of ancestral ranges and measure rates of diversification throughout the history of the family. Integrating data from over 4,800,000 digitized herbarium records, we characterize the range and niche of more than 4500 species and test for correlations of the species richness maintained within clades with range size, range partitioning, range overlap, niche, clade age and rate of diversification.ResultsCyperaceae originated in South America in the late Cretaceous and subsequently dispersed throughout the globe. Of three increases in diversification rate, two occurred in the temperate Northern Hemisphere. The variable most closely associated with clade richness is the partitioning of geographical space by species within each clade.Main conclusionsWe show that species‐rich clades in Cyperaceae are not only more widespread, occupy more niche space, and diversify more quickly, but also exhibit patterns that are consistent with the partitioning of geographical and ecological space as a major correlate to diversification.

An all-evidence species-level supertree for the palms (Arecaceae)

Several attempts have been made to generate complete species-level phylogenies for large clades, enabling comprehensive analyses of ecological or evolutionary hypotheses at the species level. No such phylogeny has, however, been generated for any major plant group yet, but here we generate such a phylogeny for the palm family (Arecaceae). We do this using a novel Bayesian approach, estimating the validity of intra-generic taxonomic groupings as topological constraints to assist in placing species without genetic or morphological data. From these we implement those that are supported by genetic or morphological data for a given genus or for related genera. The intergeneric relationships in our new phylogeny are surprisingly different from earlier phylogenies in the placement of genera within tribes, but largely identical to previous findings in the deeper branches in the phylogeny, pointing to the need for incorporating phylogenetic uncertainty in analyses based on this phylogeny. Initial analyses of the new phylogeny suggest non-constancy in diversification rates over time within genera, with an apparent increase in diversification rate over time, but no evidence for any geographic variation in the magnitude of this increase. We hope that our study will stimulate further evolutionary or ecological studies using palms as study organisms as well as discussions of the optimal way to place the many species without genetic or morphological data.

Strong effects of variation in taxonomic opinion on diversification analyses

Summary The effects of variation in taxonomic opinion between ‘splitters’ and ‘lumpers’ have been debated intensely in conservation biology and have also been discussed in macroecology. However, the impact on diversification analyses has received little attention and has largely been ignored by many end‐users of macroevolutionary analyses. Using simulated data sets, we analysed the effects of variation in taxonomic opinion on lineage diversification analysis, focusing on two measures of phylogenetic asymmetry (β and IC), a measure of the relative age composition of nodes (γ), and the MEDUSA algorithm, which searches for clades with unique diversification histories. All measures were biased by variation in taxonomic opinion, but to different degrees. The γ‐estimate and the MEDUSA algorithm were found to be especially sensitive, with error rates high enough to make it likely that false increases in diversification rates over time or clades with apparently, but not actually, unique diversification histories would be present in many published analyses. In contrast, for the two measures of phylogenetic asymmetry the biases were likely too small to substantially change conclusions in studies ignoring variation in taxonomic opinion. Our results highlight that variation in taxonomic opinion can be an important source of error in diversification analyses. We therefore suggest that all end‐users of diversification analyses should consider whether the approaches used are sensitive to this issue and, if so, whether any of their results could be a consequence of different taxonomic treatment of different lineages rather than real biological differences.

Range expansion and habitat shift triggered elevated diversification of the rice genus (Oryza, Poaceae) during the Pleistocene.

BackgroundThe rice genus (Oryza) contains many wild genetic resources that are vital to the well-being of humans. However, little is known about the process by which the genus diversified or the factors that drove its speciation. Here, we integrated the phylogenetic, molecular dating and biogeographic methods to investigate the spatial-temporal patterns of Oryza diversification, and used a series of model tests to examine whether intercontinental migrations and/or key innovations were associated with significant changes in diversification rates in the genus.ResultsOryza became differentiated in tropical Asia in the Miocene. There were two migrations from the ancestral area into Africa and Australia during the Miocene. We inferred at least 10 migration events out of tropical Asia since the Pleistocene, mainly involving the species adapting open habitat. A rapid increase in diversification rates of the whole Oryza occurred during the Pleistocene. Intercontinental migrations from tropical Asia to other tropical regions were positively correlated with shift in habitat, but not with changes in life history. A habitat preference shift from shade tolerant to open habitat predated the burst in diversification rates.ConclusionsRice species may have been pre-adapted to invade open habitat. Significant increase in diversification rates occurred during the Pleistocene and is associated with range expansion and habitat shift, but not with life history. The rice genus provides an excellent case supporting the idea that range expansion and invasion of novel habitats can drive the diversification of a group.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0459-1) contains supplementary material, which is available to authorized users.

The adaptive radiation of lichen-forming Teloschistaceae is associated with sunscreening pigments and a bark-to-rock substrate shift

Adaptive radiations play key roles in the generation of biodiversity and biological novelty, and therefore understanding the factors that drive them remains one of the most important challenges of evolutionary biology. Although both intrinsic innovations and extrinsic ecological opportunities contribute to diversification bursts, few studies have looked at the synergistic effect of such factors. Here we investigate the Teloschistales (Ascomycota), a group of >1,000 lichenized species with variation in species richness and phenotypic traits that hinted at a potential adaptive radiation. We found evidence for a dramatic increase in diversification rate for one of four families within this order--Teloschistaceae--which occurred ∼ 100 Mya (Late Cretaceous) and was associated with a switch from bark to rock and from shady to sun-exposed habitats. This adaptation to sunny habitats is likely to have been enabled by a contemporaneous key novel phenotypic innovation: the production in both vegetative structure (thallus) and fruiting body (apothecia) of anthraquinones, secondary metabolites known to protect against UV light. We found that the two ecological factors (sun exposure and rock substrate) and the phenotypic innovation (anthraquinones in the thallus) were all significant when testing for state-dependent shifts in diversification rates, and together they seem likely to be responsible for the success of the Teloschistaceae, one of the largest lichen-forming fungal lineages. Our results support the idea that adaptive radiations are driven not by a single factor or key innovation, but require a serendipitous combination of both intrinsic biotic and extrinsic abiotic and ecological factors.

Coupling of diversification and pH adaptation during the evolution of terrestrial Thaumarchaeota

The Thaumarchaeota is an abundant and ubiquitous phylum of archaea that plays a major role in the global nitrogen cycle. Previous analyses of the ammonia monooxygenase gene amoA suggest that pH is an important driver of niche specialization in these organisms. Although the ecological distribution and ecophysiology of extant Thaumarchaeota have been studied extensively, the evolutionary rise of these prokaryotes to ecological dominance in many habitats remains poorly understood. To characterize processes leading to their diversification, we investigated coevolutionary relationships between amoA, a conserved marker gene for Thaumarchaeota, and soil characteristics, by using deep sequencing and comprehensive environmental data in Bayesian comparative phylogenetics. These analyses reveal a large and rapid increase in diversification rates during early thaumarchaeotal evolution; this finding was verified by independent analyses of 16S rRNA. Our findings suggest that the entire Thaumarchaeota diversification regime was strikingly coupled to pH adaptation but less clearly correlated with several other tested environmental factors. Interestingly, the early radiation event coincided with a period of pH adaptation that enabled the terrestrial Thaumarchaeota ancestor to initially move from neutral to more acidic and alkaline conditions. In contrast to classic evolutionary models, whereby niches become rapidly filled after adaptive radiation, global diversification rates have remained stably high in Thaumarchaeota during the past 400-700 million years, suggesting an ongoing high rate of niche formation or switching for these microbes. Our study highlights the enduring importance of environmental adaptation during thaumarchaeotal evolution and, to our knowledge, is the first to link evolutionary diversification to environmental adaptation in a prokaryotic phylum.