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

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.

The diversification of Caribbean Buxus in time and space: elevated speciation rates in lineages that accumulate nickel and spreading to other islands from Cuba in non-obligate ultramafic species.

BACKGROUND AND AIMS: The genus Buxus has high levels of endemism in the Caribbean flora, with ~50 taxa. In Cuba, 82 % grow on ultramafic substrates and 59 % are nickel (Ni) accumulators or Ni hyperaccumulators. Hence it is an ideal model group to study if this diversification could be related to adaptation to ultramafic substrates and to Ni hyperaccumulation. METHODS: We generated a well-resolved molecular phylogeny, including nearly all of the Neotropical and Caribbean Buxus taxa. To obtain robust divergence times we tested for the effects of different calibration scenarios, and we reconstructed ancestral areas and ancestral character states. Phylogenetic trees were examined for trait-independent shifts in diversification rates and we used multi-state models to test for state-dependent speciation and extinction rates. Storms could have contributed to Cuba acting as a species pump and to Buxus reaching other Caribbean islands and northern South America'. KEY RESULTS: We found a Caribbean Buxus clade with Mexican ancestors, encompassing three major subclades, which started to radiate during the middle Miocene (13.25 Mya). Other Caribbean islands and northern South America were reached from ~3 Mya onwards. CONCLUSIONS: An evolutionary scenario is evident in which Buxus plants able to grow on ultramafic substrates by exaptation became ultramafic substrate endemics and evolved stepwise from Ni tolerance through Ni accumulation to Ni hyperaccumulation, which has triggered species diversification of Buxus in Cuba. Storms could have contributed to Cuba acting as a species pump and to Buxus reaching other Caribbean islands and northern South America'.

Macroevolutionary trends and diversification dynamics in Atripliceae (Amaranthaceae s.l., Chenopodioideae): a first approach.

BACKGROUND AND AIMS: Atripliceae evolved and diversified by dispersals and radiations across continents in both hemispheres, colonizing similar semi-arid, saline-alkaline environments throughout the world. Meanwhile, its species developed different life forms, photosynthetic pathways, mono- or dioecy, and different morphological features in flowers, fruiting bracteoles and seeds. In this study, we introduce a first approach to the macroevolutionary patterns and diversification dynamics of the Atripliceae to understand how time, traits, speciation, extinction and new habitats influenced the evolution of this lineage. METHODS: We performed molecular phylogenetic analyses and clade age estimation of Atripliceae to apply time-, trait- and geographic-dependent diversification analyses and ancestral state reconstructions to explore diversification patterns within the tribe. KEY RESULTS: Opposite diversification dynamics within the two major clades of Atripliceae, the Archiatriplex and Atriplex clades, could explain the unbalanced species richness between them; we found low mean speciation rates in the Archiatriplex clade and one shift to higher speciation rates placed in the branch of the Atriplex core. This acceleration in diversification seems to have started before the transition between C3 and C4 metabolism and before the arrival of Atriplex in the Americas, and matches the Mid-Miocene Climatic Optimum. Besides, the American species of Atriplex exhibit slightly higher net diversification rates than the Australian and Eurasian ones. While time seems not to be associated with diversification, traits such as life form, photosynthetic pathway and plant sex may have played roles as diversification drivers. CONCLUSIONS: Traits more than time played a key role in Atripliceae diversification, and we could speculate that climate changes could have triggered speciation. The extreme arid or saline environments where Atripliceae species prevail may explain its particular evolutionary trends and trait correlations compared with other angiosperms and highlight the importance of conservation efforts needed to preserve them as genetic resources to deal with climatic changes.

Exceptional evolutionary lability of flower-like inflorescences (pseudanthia) in Apiaceae subfamily Apioideae.

PREMISE: Pseudanthia are widespread and have long been postulated to be a key innovation responsible for some of the angiosperm radiations. The aim of our study was to analyze macroevolutionary patterns of these flower-like inflorescences and their potential correlation with diversification rates in Apiaceae subfamily Apioideae. In particular, we were interested to investigate evolvability of pseudanthia and evaluate their potential association with changes in the size of floral display. METHODS: The framework for our analyses consisted of a time-calibrated phylogeny of 1734 representatives of Apioideae and a morphological matrix of inflorescence traits encoded for 847 species. Macroevolutionary patterns in pseudanthia were inferred using Markov models of discrete character evolution and stochastic character mapping, and a principal component analysis was used to visualize correlations in inflorescence architecture. The interdependence between net diversification rates and the occurrence of pseudocorollas was analyzed with trait-independent and trait-dependent approaches. RESULTS: Pseudanthia evolved in 10 major clades of Apioideae with at least 36 independent origins and 46 reversals. The morphospace analysis recovered differences in color and compactness between floral and hyperfloral pseudanthia. A correlation between pseudocorollas and size of inflorescence was also strongly supported. Contrary to our predictions, pseudanthia are not responsible for variation in diversification rates identified in this subfamily. CONCLUSIONS: Our results suggest that pseudocorollas evolve as an answer to the trade-off between enlargement of floral display and costs associated with production of additional flowers. The high evolvability and architectural differences in apioid pseudanthia may be explained on the basis of adaptive wandering and evolutionary developmental biology.

Linking the evolution of development of stem vascular system in Nyctaginaceae and its correlation to habit and species diversification.

BACKGROUND: Alternative patterns of secondary growth in stems of Nyctaginaceae is present in all growth habits of the family and have been known for a long time. However, the interpretation of types of cambial variants have been controversial, given that different authors have given them different developmental interpretations. The different growth habits coupled with an enormous stem anatomical diversity offers the unique opportunity to investigate the evolution of complex developments, to address how these anatomies shifted within habits, and how the acquisition of novel cambial variants and habit transitions impacted the diversification of the family. METHODS: We integrated developmental data with a phylogenetic framework to investigate the diversity and evolution of stem anatomy in Nyctaginaceae using phylogenetic comparative methods, reconstructing ancestral states, and examining whether anatomical shifts correspond to species diversification rate shifts in the family. RESULTS: Two types of cambial variants, interxylary phloem and successive cambia, were recorded in Nyctaginaceae, which result from four different ontogenies. These ontogenetic trajectories depart from two distinct primary vascular structures (regular or polycyclic eustele) yet, they contain shared developmental stages which generate stem morphologies with deconstructed boundaries of morphological categories (continuum morphology). Unlike our a priori hypotheses, interxylary phloem is reconstructed as the ancestral character for the family, with three ontogenies characterized as successive cambia evolving in few taxa. Cambial variants are not contingent on habits, and their transitions are independent from species diversification. CONCLUSIONS: Our findings suggest that multiple developmental mechanisms, such as heterochrony and heterotopy, generate the transitions between interxylary phloem and successive cambia. Intermediate between these two extremes are present in Nyctaginaceae, suggesting a continuum morphology across the family as a generator of anatomical diversity.

Molecular phylogeny, classification, biogeography and diversification patterns of a diverse group of moths (Geometridae: Boarmiini).

Understanding how and why some groups have become more species-rich than others, and how past biogeography may have shaped their current distribution, are questions that evolutionary biologists have long attempted to answer. We investigated diversification patterns and historical biogeography of a hyperdiverse lineage of Lepidoptera, the geometrid moths, by studying its most species-rich tribe Boarmiini, which comprises ca. 200 genera and ca. known 3000 species. We inferred the evolutionary relationships of Boarmiini based on a dataset of 346 taxa, with up to eight genetic markers under a maximum likelihood approach. The monophyly of Boarmiini is strongly supported. However, the phylogenetic position of many taxa does not agree with current taxonomy, although the monophyly of most major genera within the tribe is supported after minor adjustments. Three genera are synonymized, one new combination is proposed, and four species are placed in incertae sedis within Boarmiini. Our results support the idea of a rapid initial diversification of Boarmiini, which also implies that no major taxonomic subdivisions of the group can currently be proposed. A time-calibrated tree and biogeographical analyses suggest that boarmiines appeared in Laurasia ca. 52 Mya, followed by dispersal events throughout the Australasian, African and Neotropical regions. Most of the transcontinental dispersal events occurred in the Eocene, a period of intense geological activity and rapid climate change. Diversification analyses showed a relatively constant diversification rate for all Boarmiini, except in one clade containing the species-rich genus Cleora. The present work represents a substantial contribution towards understanding the evolutionary origin of Boarmiini moths. Our results, inevitably biased by taxon sampling, highlight the difficulties with working on species-rich groups that have not received much attention outside of Europe. Specifically, poor knowledge of the natural history of geometrids (particularly in tropical clades) limits our ability to identify key innovations underlying the diversification of boarmiines.

Phylogeny, divergence times, and diversification in Calophyllaceae: Linking key characters and habitat changes to the evolution of Neotropical Calophylleae.

The clusioid clade comprises five monophyletic families: Bonnetiaceae, Calophyllaceae, Clusiaceae s.s., Hypericaceae, and Podostemaceae. Even though the circumscription of these families is well established, phylogenetic relationships within some families remain unresolved. This study aims to infer phylogenetic relationships within the Neotropical Calophylleae based on a broad sampling of taxa and a multilocus approach. We then use our phylogenetic framework as basis to investigate the evolution and biogeography of Calophylleae and diversification shifts in Calophyllaceae. To reconstruct the phylogeny of the Neotropical Calophylleae, we used five plastid (matK, ndhF, rbcL, psbA-trnH, and trnK), two mitochondrial (matR and rps3), and two nuclear (EMB2765 and ITS) markers, including previously published and newly generated sequences. We sampled 74 species, increasing sampling of Neotropical taxa by 500%. Our phylogenetic hypothesis for Calophyllaceae provides additional support for the monophyly of all genera and allowed us to identify four main clades: Calophyllum, Kayea, Mammea, and the Neotropical clade. The Neotropical clade includes three main lineages, a small clade composed of Clusiella and Marila, and a large HaCaKi clade (i.e., Haplocarpa, Caraipa, and Kilmeyera) that is sister to Mahurea exstipulata. The evolution of three morphological traits (i.e., fleshy fruits, anther glands, and winged seeds) were shown to be associated with changes in evolutionary dynamics in Calophyllaceae, while a biome shift was detected in Kielmeyera, affecting net diversification within this genus. Major geological and climatic events such as the Andean uplift and a gradual decrease in temperatures seem to have influenced diversification rates within the Neotropical Calophylleae.

Temporal patterns of diversification in Brassicaceae demonstrate decoupling of rate shifts and mesopolyploidization events.

BACKGROUND AND AIMS: Whole-genome duplication (WGD) events are considered important driving forces of diversification. At least 11 out of 52 Brassicaceae tribes had independent mesopolyploid WGDs followed by diploidization processes. However, the association between mesopolyploidy and subsequent diversification is equivocal. Herein we show the results from a family-wide diversification analysis on Brassicaceae, and elaborate on the hypothesis that polyploidization per se is a fundamental driver in Brassicaceae evolution. METHODS: We established a time-calibrated chronogram based on whole plastid genomes comprising representative Brassicaceae taxa and published data spanning the entire Rosidae clade. This allowed us to set multiple calibration points and anchored various Brassicaceae taxa for subsequent downstream analyses. All major splits among Brassicaceae lineages were used in BEAST analyses of 48 individually analysed tribes comprising 2101 taxa in total using the internal transcribed spacers of nuclear ribosomal DNA. Diversification patterns were investigated on these tribe-wide chronograms using BAMM and were compared with family-wide data on genome size variation and species richness. KEY RESULTS: Brassicaceae diverged 29.9 million years ago (Mya) during the Oligocene, and the majority of tribes started diversification in the Miocene with an average crown group age of about 12.5 Mya. This matches the cooling phase right after the Mid Miocene climatic optimum. Significant rate shifts were detected in 12 out of 52 tribes during the Mio- and Pliocene, decoupled from preceding mesopolyploid WGDs. Among the various factors analysed, the combined effect of tribal crown group age and net diversification rate (speciation minus extinction) is likely to explain sufficiently species richness across Brassicaceae tribes. CONCLUSIONS: The onset of the evolutionary splits among tribes took place under cooler and drier conditions. Pleistocene glacial cycles may have contributed to the maintenance of high diversification rates. Rate shifts are not consistently associated with mesopolyploid WGD. We propose, therefore, that WGDs in general serve as a constant 'pump' for continuous and high species diversification.

A multigene timescale and diversification dynamics of Ciliophora evolution.

Ciliophora is one of the most diverse lineages of unicellular eukaryotes. Nevertheless, a robust timescale including all main lineages and employing properly identified ciliate fossils as primary calibrations is lacking. Here, we inferred a time-calibrated multigene phylogeny of Ciliophora evolution, and we used this timetree to investigate the rates and patterns of lineage diversification through time. We implemented a two-step analytical approach that favored both gene and taxon sampling, reducing the uncertainty of time estimates and yielding narrower credibility intervals on the ribosomal-derived chronogram. We estimate the origin of Ciliophora at 1143 Ma, which is substantially younger than previously proposed ages, and the huge diversity explosion occurred during the Paleozoic. Among the current groups recognized as classes, Spirotrichea diverged earlier, its origin was dated at ca. 850 Ma, and Protocruziea was the younger class, with crown age estimated at 56 Ma. Macroevolutionary analysis detected a significant rate shift in diversification dynamics in the spirotrichean clade Hypotrichia + Oligotrichia + Choreotrichia, which had accelerated speciation rate ca. 570 Ma, during the Ediacaran-Cambrian transition. For all crown lineages investigated, speciation rates declined through time, whereas extinction rates remained low and relatively constant throughout the evolutionary history of ciliates.

Speciation Rate Is Independent of the Rate of Evolution of Morphological Size, Shape, and Absolute Morphological Specialization in a Large Clade of Birds.

Whether ecological differences between species evolve in parallel with lineage diversification is a fundamental issue in evolutionary biology. These processes might be connected if conditions that favor the proliferation of species, such as release from competitors, facilitate the evolution of novel ecological relationships. Despite this, phylogenetic studies do not consistently identify such a connection. Conversely, if higher diversity caused species to become increasingly specialized ecologically, then lineage diversification might become dissociated from ecological diversification. In this analysis, we ask whether the rate of lineage diversification in a large clade of birds is correlated with morphological specialization and with rates of morphological evolution. We find that morphological variation is related to species richness within clades but that rates of morphological evolution are decoupled from the rate of lineage diversification. Additionally, morphological specialization within lineages is independent of the rate at which lineages diversify, with the results apparently robust against false negative inference. This dissociation is likely a consequence of the major ecomorphological differences between avian clades arising early in their evolutionary history, with comparatively little variation added subsequently, while avian diversification has been driven predominantly by geographic isolation and sexual selection. Accordingly, biodiversity appears to be limited by the extent to which taxa can subdivide exploited regions of ecological space and not just overall ecological opportunity.

Towards a global phylogeny of freshwater mussels (Bivalvia: Unionida): Species delimitation of Chinese taxa, mitochondrial phylogenomics, and diversification patterns.

The Yangtze River Basin in China is one of the global hotspots of freshwater mussel (order Unionida) diversity with 68 nominal species. Few studies have tested the validity of these nominal species. Some taxa from the Yangtze unionid fauna have not been adequately examined using molecular data and well-positioned phylogenetically with respect to the global Unionida. We evaluated species boundaries of Chinese freshwater mussels, and disentangled their phylogenetic relationships within the context of the global freshwater mussels based on the multi-locus data and complete mitochondrial genomes. Moreover, we produced the time-calibrated phylogeny of Unionida and explored patterns of diversification. COI barcode data suggested the existence of 41 phylogenetic distinct species from our sampled 40 nominal taxa inhabiting the middle and lower reaches of the Yangtze River. Maximum likelihood and Bayesian inference analyses on three loci (COI, 16S, and 28S) and complete mitochondrial genomes showed that the subfamily Unioninae sensu stricto was paraphyletic, and the subfamily Anodontinae should be subsumed under Unioninae. In addition, we described two new tribes (Aculamprotulini tribe nov. and Lepidodesmini tribe nov.) in the subfamily Unioninae and one new genus (Parvasolenaiagen. nov.) in the subfamily Gonideinae. Molecular dating analysis suggested freshwater mussels diversified at 346.1 Mya (HPD = 286.6-409.9). The global diversification rate for Unionida was estimated to be 0.025 species/Myr. Our study found only a single well-supported rate shift in Unionida diversification, occurring at the base of the subfamily Ambleminae. The evolution of active host-attraction may have triggered the burst of speciation in Ambleminae, and the environment and geography of the Mississippi River Basin likely sustained this radiation.

What affects power to estimate speciation rate shifts?

The development of methods to estimate rates of speciation and extinction from time-calibrated phylogenies has revolutionized evolutionary biology by allowing researchers to correlate diversification rate shifts with causal factors. A growing number of researchers are interested in testing whether the evolution of a trait or a trait variant has influenced speciation rate, and three modelling methods-BiSSE, MEDUSA and BAMM-have been widely used in such studies. We simulated phylogenies with a single speciation rate shift each, and evaluated the power of the three methods to detect these shifts. We varied the degree of increase in speciation rate (speciation rate asymmetry), the number of tips, the tip-ratio bias (ratio of number of tips with each character state) and the relative age in relation to overall tree age when the rate shift occurred. All methods had good power to detect rate shifts when the rate asymmetry was strong and the sizes of the two lineages with the distinct speciation rates were large. Even when lineage size was small, power was good when rate asymmetry was high. In our simulated scenarios, small lineage sizes appear to affect BAMM most strongly. Tip-ratio influenced the accuracy of speciation rate estimation but did not have a strong effect on power to detect rate shifts. Based on our results, we provide suggestions to users of these methods.

BAMM gives misleading rate estimates in simulated and empirical datasets.

In a previous paper, we used simulations and empirical data to show that BAMM (Bayesian Analysis of Macroevolutionary Mixtures) can give misleading estimates of rates and rate shifts. In simulations, BAMM underestimated rate shifts across every tree analyzed, and assigned incorrect rates to most clades in most trees. In empirical analyses, BAMM behaved as expected from simulations, and assigned different rates to clades when clades were analyzed alone versus across the tree (i.e., with rate heterogeneity). Rabosky recently criticized our paper, focusing primarily on the idea that our comparison of BAMM to another approach (method-of-moments estimators of Magallón and Sanderson, or MS estimators) was unfair to BAMM. Here, we provide further evidence that BAMM gives misleading rate estimates in empirical studies. We then describe how Rabosky's rown method comparisons were either acknowledged as being problematic or were described inaccurately (to favor BAMM). Finally, we show that the MS estimators can perform well when rates vary over time, despite untested assertions that they require constant rates to be accurate. Many other methods are available for analyzing diversification rates: we argue that BAMM should be avoided for estimating both diversification rates and rate shifts.

Generalized morphea/eosinophilic fasciitis overlap after epoxy exposure.

Generalized morphea is associated with epoxy resin vapors and is characterized by the development of lesions shortly after exposure. Morphea presenting along with eosinophilic fasciitis (EF), or morphea/EF overlap, is rare and an indicator of poor prognosis and resistance to treatment. Here we present a case of generalized morphea/EF overlap linked to epoxy exposure. Our patient received multiple therapies-ultraviolet A1 phototherapy, prednisone, methotrexate, azathioprine, mycophenolate mofetil, cyclophosphamide, cyclosporine, and rituximab-none of which led to a significant response. The refractory nature of this disease warrants vigilance in its association with epoxy exposure.

Impact of whole-genome duplication events on diversification rates in angiosperms.

PREMISE OF THE STUDY: Polyploidy or whole-genome duplication (WGD) pervades the evolutionary history of angiosperms. Despite extensive progress in our understanding of WGD, the role of these events in promoting diversification is still not well understood. We seek to clarify the possible association between WGD and diversification rates in flowering plants. METHODS: Using a previously published phylogeny spanning all land plants (31,749 tips) and WGD events inferred from analyses of the 1000 Plants (1KP) transcriptome data, we analyzed the association of WGDs and diversification rates following numerous WGD events across the angiosperms. We used a stepwise AIC approach (MEDUSA), a Bayesian mixture model approach (BAMM), and state-dependent diversification analyses (MuSSE) to investigate patterns of diversification. Sister-clade comparisons were used to investigate species richness after WGDs. KEY RESULTS: Based on the density of 1KP taxon sampling, 106 WGDs were unambiguously placed on the angiosperm phylogeny. We identified 334-530 shifts in diversification rates. We found that 61 WGD events were tightly linked to changes in diversification rates, and state-dependent diversification analyses indicated higher speciation rates for subsequent rounds of WGD. Additionally, 70 of 99 WGD events showed an increase in species richness compared to the sister clade. CONCLUSIONS: Forty-six of the 106 WGDs analyzed appear to be closely associated with upshifts in the rate of diversification in angiosperms. Shifts in diversification do not appear more likely than random within a four-node lag phase following a WGD; however, younger WGD events are more likely to be followed by an upshift in diversification than older WGD events.

Are rates of species diversification and body size evolution coupled in the ferns?

PREMISE OF THE STUDY: Understanding the relationship between phenotypic evolution and lineage diversification is a central goal of evolutionary biology. To extend our understanding of the role morphological evolution plays in the diversification of plants, we examined the relationship between leaf size evolution and lineage diversification across ferns. METHODS: We tested for an association between body size evolution and lineage diversification using a comparative phylogenetic approach that combined a time-calibrated phylogeny and leaf size data set for 2654 fern species. Rates of leaf size change and lineage diversification were estimated using BAMM, and rate correlations were performed for rates obtained for all families and individual species. Rates and patterns of rate-rate correlation were also analyzed separately for terrestrial and epiphytic taxa. KEY RESULTS: We find no significant correlation between rates of leaf area change and lineage diversification, nor was there a difference in this pattern when growth habit is considered. Our results are consistent with the findings of an earlier study that reported decoupled rates of body size evolution and diversification in the Polypodiaceae, but conflict with a recent study that reported a positive correlation between body size evolution and lineage diversification rates in the tree fern family Cyatheaceae. CONCLUSIONS: Our findings indicate that lineage diversification in ferns is largely decoupled from shifts in body size, in contrast to several other groups of organisms. Speciation in ferns appears to be primarily driven by hybridization and isolation along elevational gradients, rather than adaptive radiations featuring prominent morphological restructuring. The exceptional diversity of leaf morphologies in ferns appears to reflect a combination of ecophysiological constraints and adaptations that are not key innovations.

Estimating diversification rates for higher taxa: BAMM can give problematic estimates of rates and rate shifts.

Estimates of diversification rates are invaluable for many macroevolutionary studies. Recently, an approach called BAMM (Bayesian Analysis of Macro-evolutionary Mixtures) has become widely used for estimating diversification rates and rate shifts. At the same time, several articles have concluded that estimates of net diversification rates from the method-of-moments (MS) estimators are inaccurate. Yet, no studies have compared the ability of these two methods to accurately estimate clade diversification rates. Here, we use simulations to compare their performance. We found that BAMM yielded relatively weak relationships between true and estimated diversification rates. This occurred because BAMM underestimated the number of rates shifts across each tree, and assigned high rates to small clades with low rates. Errors in both speciation and extinction rates contributed to these errors, showing that using BAMM to estimate only speciation rates is also problematic. In contrast, the MS estimators (particularly using stem group ages), yielded stronger relationships between true and estimated diversification rates, by roughly twofold. Furthermore, the MS approach remained relatively accurate when diversification rates were heterogeneous within clades, despite the widespread assumption that it requires constant rates within clades. Overall, we caution that BAMM may be problematic for estimating diversification rates and rate shifts.

Ecological opportunity alters the timing and shape of adaptive radiation.

The uneven distribution of diversity is a conspicuous phenomenon across the tree of life. Ecological opportunity is a prominent catalyst of adaptive radiation and therefore may alter patterns of diversification. We evaluated the distribution of shifts in diversification rates across the cichlid phylogeny and the distribution of major clades across phylogenetic space. We also tested if ecological opportunity influenced these patterns. Colonization-associated ecological opportunity altered the tempo and mode of diversification during the adaptive radiation of cichlid fishes. Clades that arose following colonization events diversified faster than other clades. Speciation rate shifts were nonrandomly distributed across the phylogeny such that they were disproportionally concentrated around nodes that corresponded with colonization events (i.e., of continents, river basins, or lakes). Young clades tend to expand faster than older clades; however, colonization-associated ecological opportunity accentuated this pattern. There was an interaction between clade age and ecological opportunity that explained the trajectory of clades through phylogenetic space over time. Our results indicate that ecological opportunities afforded by continental and ecosystem-scale colonization events explain the dramatic speciation rate heterogeneity and phylogenetic imbalance that arose during the evolutionary history of cichlid fishes.

Is BAMM Flawed? Theoretical and Practical Concerns in the Analysis of Multi-Rate Diversification Models.

Bayesian analysis of macroevolutionary mixtures (BAMM) is a statistical framework that uses reversible jump Markov chain Monte Carlo to infer complex macroevolutionary dynamics of diversification and phenotypic evolution on phylogenetic trees. A recent article by Moore et al. (MEA) reported a number of theoretical and practical concerns with BAMM. Major claims from MEA are that (i) BAMM's likelihood function is incorrect, because it does not account for unobserved rate shifts; (ii) the posterior distribution on the number of rate shifts is overly sensitive to the prior; and (iii) diversification rate estimates from BAMM are unreliable. Here, we show that these and other conclusions from MEA are generally incorrect or unjustified. We first demonstrate that MEA's numerical assessment of the BAMM likelihood is compromised by their use of an invalid likelihood function. We then show that "unobserved rate shifts" appear to be irrelevant for biologically plausible parameterizations of the diversification process. We find that the purportedly extreme prior sensitivity reported by MEA cannot be replicated with standard usage of BAMM v2.5, or with any other version when conventional Bayesian model selection is performed. Finally, we demonstrate that BAMM performs very well at estimating diversification rate variation across the ${\sim}$20% of simulated trees in MEA's data set for which it is theoretically possible to infer rate shifts with confidence. Due to ascertainment bias, the remaining 80% of their purportedly variable-rate phylogenies are statistically indistinguishable from those produced by a constant-rate birth-death process and were thus poorly suited for the summary statistics used in their performance assessment. We demonstrate that inferences about diversification rates have been accurate and consistent across all major previous releases of the BAMM software. We recognize an acute need to address the theoretical foundations of rate-shift models for phylogenetic trees, and we expect BAMM and other modeling frameworks to improve in response to mathematical and computational innovations. However, we remain optimistic that that the imperfect tools currently available to comparative biologists have provided and will continue to provide important insights into the diversification of life on Earth.

A major shift in diversification rate helps explain macroevolutionary patterns in primate species diversity.

Primates represent one of the most species rich, wide ranging, and ecologically diverse clades of mammals. What major macroevolutionary factors have driven their diversification and contributed to the modern distribution of primate species remains widely debated. We employed phylogenetic comparative methods to examine the role of clade age and evolutionary rate heterogeneity in the modern distribution of species diversity of Primates. Primate diversification has accelerated since its origin, with decreased extinction leading to a shift to even higher evolutionary rates in the most species rich family (Cercopithecidae). Older primate clades tended to be more diverse, however a shift in evolutionary rate was necessary to adequately explain the imbalance in species diversity. Species richness was also poorly explained by geographic distribution, especially once clade age and evolutionary rate shifts were accounted for, and may relate instead to other ecological factors. The global distribution of primate species diversity appears to have been strongly impacted by heterogeneity in evolutionary rates.