A time-calibrated species tree of Crocodylia reveals a recent radiation of the true crocodiles

True crocodiles (Crocodylus) are the most broadly distributed, ecologically diverse, and species-rich crocodylian genus, comprising about half of extant crocodylian diversity and exhibiting a circumtropical distribution. Crocodylus traditionally has been viewed as an ancient group of morphologically conserved species that originated in Africa prior to continental breakup. In this study, these long-held notions about the temporal and geographic origin of Crocodylus are tested using DNA sequence data of 10 loci from 76 individuals representing all 23 crocodylian species. I infer a time-calibrated species tree of all Crocodylia and estimate the spatial pattern of diversification within Crocodylus. For the first time, a fully resolved phylogenetic estimate of all Crocodylia is well-supported. The results overturn traditional views of the evolution of Crocodylus by demonstrating that the true crocodiles are not "living-fossils" that originated in Africa. Rather, Crocodylus originated from an ancestor in the tropics of the Late Miocene Indo-Pacific, and rapidly radiated and dispersed around the globe during a period marked by mass extinctions of fellow crocodylians. The findings also reveal more diversity within the genus than is recognized by current taxonomy.     

From success to persistence: Identifying an evolutionary regime shift in the diverse Paleozoic aquatic arthropod group Eurypterida,driven by the Devonian biotic crisis

Mass extinctions have altered the trajectory of evolution a number of times over the Phanerozoic. During these periods of biotic upheaval a different selective regime appears to operate, although it is still unclear whether consistent survivorship rules apply across different extinction events. We compare variations in diversity and disparity across the evolutionary history of a major Paleozoic arthropod group, the Eurypterida. Using these data, we explore the group's transition from a successful, dynamic clade to a stagnant persistent lineage, pinpointing the Devonian as the period during which this evolutionary regime shift occurred. The late Devonian biotic crisis is potentially unique among the “Big Five” mass extinctions in exhibiting a drop in speciation rates rather than an increase in extinction. Our study reveals eurypterids show depressed speciation rates throughout the Devonian but no abnormal peaks in extinction. Loss of morphospace occupation is random across all Paleozoic extinction events; however, differential origination during the Devonian results in a migration and subsequent stagnation of occupied morphospace. This shift appears linked to an ecological transition from euryhaline taxa to freshwater species with low morphological diversity alongside a decrease in endemism. These results demonstrate the importance of the Devonian biotic crisis in reshaping Paleozoic ecosystems.     

Primary controls on species richness in higher taxa

The disparity in species richness across the tree of life is one of the most striking and pervasive features of biological diversity. Some groups are exceptionally diverse, whereas many other groups are species poor. Differences in diversity among groups are frequently assumed to result from primary control by differential rates of net diversification. However, a major alternative explanation is that ecological and other factors exert primary control on clade diversity, such that apparent variation in net diversification rates is a secondary consequence of ecological limits on clade growth. Here, I consider a likelihood framework for distinguishing between these competing hypotheses. I incorporate hierarchical modeling to explicitly relax assumptions about the constancy of diversification rates across clades, and I propose several statistics for a posteriori evaluation of model adequacy. I apply the framework to a recent dated phylogeny of ants. My results reject the hypothesis that net diversification rates exert primary control on species richness in this group and demonstrate that clade diversity is better explained by total time-integrated speciation. These results further suggest that it may not possible to estimate meaningful speciation and extinction rates from higher-level phylogenies of extant taxa only.     

Dynamics of clade diversification on the morphological hypercube

Understanding the relationship between taxonomic and morphological changes is important in identifying the reasons for accelerated morphological diversification early in the history of animal phyla. Here, a simple general model describing the joint dynamics of taxonomic diversity and morphological disparity is presented and applied to the data on the diversification of blastozoans. I show that the observed patterns of deceleration in clade diversification can be explicable in terms of the geometric structure of the morphospace and the effects of extinction and speciation on morphological disparity without invoking major declines in the size of morphological transitions or taxonomic turnover rates. The model allows testing of hypotheses about patterns of diversification and estimation of rates of morphological evolution. In the case of blastozoans, I find no evidence that major changes in evolutionary rates and mechanisms are responsible for the deceleration of morphological diversification seen during the period of this clade''s expansion. At the same time, there is evidence for a moderate decline in overall rates of morphological diversification concordant with a major change (from positive to negative values) in the clade''s growth rate.     

Continental faunal exchange and the asymmetrical radiation of carnivores

Lineages arriving on islands may undergo explosive evolutionary radiations owing to the wealth of ecological opportunities. Although studies on insular taxa have improved our understanding of macroevolutionary phenomena, we know little about the macroevolutionary dynamics of continental exchanges. Here we study the evolution of eight Carnivora families that have migrated across the Northern Hemisphere to investigate if continental invasions also result in explosive diversification dynamics. We used a Bayesian approach to estimate speciation and extinction rates from a substantial dataset of fossil occurrences while accounting for the incompleteness of the fossil record. Our analyses revealed a strongly asymmetrical pattern in which North American lineages invading Eurasia underwent explosive radiations, whereas lineages invading North America maintained uniform diversification dynamics. These invasions into Eurasia were characterized by high rates of speciation and extinction. The radiation of the arriving lineages in Eurasia coincide with the decline of established lineages or phases of climate change, suggesting differences in the ecological settings between the continents may be responsible for the disparity in diversification dynamics. These results reveal long-term outcomes of biological invasions and show that the importance of explosive radiations in shaping diversity extends beyond insular systems and have significant impact at continental scales.     

Interactions within and between clades shaped the diversification of terrestrial carnivores

A longstanding debate in evolutionary biology and paleontology is whether ecological interactions such as competition impose diversity dependence on speciation and extinction rates. Here, we analyze the fossil record of terrestrial mammalian carnivores in North America and Eurasia using a Bayesian framework to assess whether their diversity dynamics were affected by diversity dependence within and between families (12 in Eurasia, 10 in North America). We found eight instances of within‐clade diversity dependence suppressing speciation rates and detected between‐clade effects increasing extinction rates in six instances. Diversity dependence often involved lineages that migrated between continents and we found that speciation was more responsive to diversity changes within the clade, whereas extinction responded to diversity of taxa in other clades. The analysis of the fossil record of Carnivora suggests that interactions within and between clades are associated with different speciation and extinction regimes, opening room for a broader theory of diversity dependence.     

Extinction, ecological opportunity, and the origins of global snake diversity

Snake diversity varies by at least two orders of magnitude among extant lineages, with numerous groups containing only one or two species, and several young clades exhibiting exceptional richness (>700 taxa). With a phylogeny containing all known families and subfamilies, we find that these patterns cannot be explained by background rates of speciation and extinction. The majority of diversity appears to derive from a radiation within the superfamily Colubroidea, potentially stemming from the colonization of new areas and the evolution of advanced venom-delivery systems. In contrast, negative relationships between clade age, clade size, and diversification rate suggest the potential for possible bias in estimated diversification rates, interpreted by some recent authors as support for ecologically mediated limits on diversity. However, evidence from the fossil record indicates that numerous lineages were far more diverse in the past, and that extinction has had an important impact on extant diversity patterns. Thus, failure to adequately account for extinction appears to prevent both rate- and diversity-limited models from fully characterizing richness dynamics in snakes. We suggest that clade-level extinction may provide a key mechanism for explaining negative or hump-shaped relationships between clade age and diversity, and the prevalence of ancient, species-poor lineages in numerous groups.     

Is regional species diversity bounded or unbounded?

Two conflicting hypotheses have been proposed to explain large‐scale species diversity patterns and dynamics. The unbounded hypothesis proposes that regional diversity depends only on time and diversification rate and increases without limit. The bounded hypothesis proposes that ecological constraints place upper limits on regional diversity and that diversity is usually close to its limit. Recent evidence from the fossil record, phylogenetic analysis, biogeography, and phenotypic disparity during lineage diversification suggests that diversity is constrained by ecological processes but that it is rarely asymptotic. Niche space is often unfilled or can be more finely subdivided and still permit coexistence, and new niche space is often created before ecological limits are reached. Damped increases in diversity over time are the prevalent pattern, suggesting the need for a new ‘damped increase hypothesis'. The damped increase hypothesis predicts that diversity generally increases through time but that its rate of increase is often slowed by ecological constraints. However, slowing due to niche limitation must be distinguished from other possible mechanisms creating similar patterns. These include sampling artifacts, the inability to detect extinctions or declines in clade diversity with some methods, the distorting effects of correlated speciation‐extinction dynamics, the likelihood that opportunities for allopatric speciation will vary in space and time, and the role of undetected natural enemies in reducing host ranges and thus slowing speciation rates. The taxonomic scope of regional diversity studies must be broadened to include all ecologically similar species so that ecological constraints may be accurately inferred. The damped increase hypothesis suggests that information on evolutionary processes such as time‐for‐speciation and intrinsic diversification rates as well as ecological factors will be required to explain why regional diversity varies among times, places and taxa.     

Do Mediterranean‐type ecosystems have a common history?—Insights from the Buckthorn family (Rhamnaceae)

Mediterranean‐type ecosystems (MTEs) are remarkable in their species richness and endemism, but the processes that have led to this diversity remain enigmatic. Here, we hypothesize that continent‐dependent speciation and extinction rates have led to disparity in diversity between the five MTEs of the world: the Cape, California, Mediterranean Basin, Chile, and Western Australia. To test this hypothesis, we built a phylogenetic tree for 280 Rhamnaceae species, estimated divergence times using eight fossil calibrations, and used Bayesian methods and simulations to test for differences in diversification rates. Rhamnaceae lineages in MTEs generally show higher diversification rates than elsewhere, but speciation and extinction dynamics show a pattern of continent‐dependence. We detected high speciation and extinction rates in California and significantly lower extinction rates in the Cape and Western Australia. The independent colonization of four of five MTEs may have occurred conterminously in the Oligocene/Early Miocene, but colonization of the Mediterranean Basin happened later, in the Late Miocene. This suggests that the in situ radiations of these clades were initiated before the onset of winter rainfall in these regions. These results indicate independent evolutionary histories of Rhamnaceae in MTEs, possibly related to the intensity of climate oscillations and the geological history of the regions.     

Ecological limits and diversification rate: alternative paradigms to explain the variation in species richness among clades and regions

Diversification rate is one of the most important metrics in macroecological and macroevolutionary studies. Here I demonstrate that diversification analyses can be misleading when researchers assume that diversity increases unbounded through time, as is typical in molecular phylogenetic studies. If clade diversity is regulated by ecological factors, then species richness may be independent of clade age and it may not be possible to infer the rate at which diversity arose. This has substantial consequences for the interpretation of many studies that have contrasted rates of diversification among clades and regions. Often, it is possible to estimate the total diversification experienced by a clade but not diversification rate itself. I show that the evidence for ecological limits on diversity in higher taxa is widespread. Finally, I explore the implications of ecological limits for a variety of ecological and evolutionary questions that involve inferences about speciation and extinction rates from phylogenetic data.     

The ecological importance of crocodylians: towards evidence‐based justification for their conservation

Large‐bodied predators are well represented among the world's threatened and endangered species. A significant body of literature shows that in terrestrial and marine ecosystems large predators can play important roles in ecosystem structure and functioning. By contrast, the ecological roles and importance of large predators within freshwater ecosystems are poorly understood, constraining the design and implementation of optimal conservation strategies for freshwater ecosystems. Conservationists and environmentalists frequently promulgate ecological roles that crocodylians are assumed to fulfil, but often with limited evidence supporting those claims. Here, we review the available information on the ecological importance of crocodylians, a widely distributed group of predominantly freshwater‐dwelling, large‐bodied predators. We synthesise information regarding the role of crocodylians under five criteria within the context of modern ecological concepts: as indicators of ecological health, as ecosystem engineers, apex predators, keystone species, and as contributors to nutrient and energy translocation across ecosystems. Some crocodylians play a role as indicators of ecosystem health, but this is largely untested across the order Crocodylia. By contrast, the role of crocodylian activities in ecosystem engineering is largely anecdotal, and information supporting their assumed role as apex predators is currently limited to only a few species. Whether crocodylians contribute significantly to nutrient and energy translocation through cross‐ecosystem movements is unknown. We conclude that most claims regarding the importance of crocodylians as apex predators, keystone species, ecosystem engineers, and as contributors to nutrient and energy translocation across ecosystems are mostly unsubstantiated speculation, drawn from anecdotal observations made during research carried out primarily for other purposes. There is a paucity of biological research targeted directly at: understanding population dynamics; trophic interactions within their ecological communities; and quantifying the short‐ and long‐term ecological impacts of crocodylian population declines, extirpations, and recoveries. Conservation practices ideally need evidence‐based planning, decision making and justification. Addressing the knowledge gaps identified here will be important for achieving effective conservation of crocodylians.     

Permian–Triassic Osteichthyes (bony fishes): diversity dynamics and body size evolution

The Permian and Triassic were key time intervals in the history of life on Earth. Both periods are marked by a series of biotic crises including the most catastrophic of such events, the end‐Permian mass extinction, which eventually led to a major turnover from typical Palaeozoic faunas and floras to those that are emblematic for the Mesozoic and Cenozoic. Here we review patterns in Permian–Triassic bony fishes, a group whose evolutionary dynamics are understudied. Based on data from primary literature, we analyse changes in their taxonomic diversity and body size (as a proxy for trophic position) and explore their response to Permian–Triassic events. Diversity and body size are investigated separately for different groups of Osteichthyes (Dipnoi, Actinistia, ‘Palaeopterygii’, ‘Subholostei’, Holostei, Teleosteomorpha), within the marine and freshwater realms and on a global scale (total diversity) as well as across palaeolatitudinal belts. Diversity is also measured for different palaeogeographical provinces. Our results suggest a general trend from low osteichthyan diversity in the Permian to higher levels in the Triassic. Diversity dynamics in the Permian are marked by a decline in freshwater taxa during the Cisuralian. An extinction event during the end‐Guadalupian crisis is not evident from our data, but ‘palaeopterygians’ experienced a significant body size increase across the Guadalupian–Lopingian boundary and these fishes upheld their position as large, top predators from the Late Permian to the Late Triassic. Elevated turnover rates are documented at the Permian–Triassic boundary, and two distinct diversification events are noted in the wake of this biotic crisis, a first one during the Early Triassic (dipnoans, actinistians, ‘palaeopterygians’, ‘subholosteans’) and a second one during the Middle Triassic (‘subholosteans’, neopterygians). The origination of new, small taxa predominantly among these groups during the Middle Triassic event caused a significant reduction in osteichthyan body size. Neopterygii, the clade that encompasses the vast majority of extant fishes, underwent another diversification phase in the Late Triassic. The Triassic radiation of Osteichthyes, predominantly of Actinopterygii, which only occurred after severe extinctions among Chondrichthyes during the Middle–Late Permian, resulted in a profound change within global fish communities, from chondrichthyan‐rich faunas of the Permo‐Carboniferous to typical Mesozoic and Cenozoic associations dominated by actinopterygians. This turnover was not sudden but followed a stepwise pattern, with leaps during extinction events.     

Quantitative traits and diversification

Quantitative traits have long been hypothesized to affect speciation and extinction rates. For example, smaller body size or increased specialization may be associated with increased rates of diversification. Here, I present a phylogenetic likelihood-based method (quantitative state speciation and extinction [QuaSSE]) that can be used to test such hypotheses using extant character distributions. This approach assumes that diversification follows a birth-death process where speciation and extinction rates may vary with one or more traits that evolve under a diffusion model. Speciation and extinction rates may be arbitrary functions of the character state, allowing much flexibility in testing models of trait-dependent diversification. I test the approach using simulated phylogenies and show that a known relationship between speciation and a quantitative character could be recovered in up to 80% of the cases on large trees (500 species). Consistent with other approaches, detecting shifts in diversification due to differences in extinction rates was harder than when due to differences in speciation rates. Finally, I demonstrate the application of QuaSSE to investigate the correlation between body size and diversification in primates, concluding that clade-specific differences in diversification may be more important than size-dependent diversification in shaping the patterns of diversity within this group.     

Relationships of diversity,disparity, and their evolutionary rates in squirrels (Sciuridae)

Several theories predict that rapidly diversifying clades will also rapidly diverge phenotypically; yet, there are also reasons for suspecting that diversification and divergence might not be correlated. In the widely distributed squirrel clade (Sciuridae), we test for correlations between per lineage speciation rates, species richness, disparity, and a time‐invariant measure of disparity that allows for comparing rates when evolutionary modes differ, as they do in squirrels. We find that species richness and speciation rates are not correlated with clade age or with each other. Disparity appears to be positively correlated with clade age because young, rapidly diversifying Nearctic grassland clades are strongly pulled to a single stable optimum but older, slowly diversifying Paleotropical forest clades contain lineages that diverge along multiple ecological and morphological lines. That contrast is likely due to both the environments they inhabit and their phylogenetic community structure. Our results argue against a shared explanation for diversity and disparity in favor of geographically mediated modes of speciation and ecologically mediated modes of phenotypic evolution.     

Geographic range size, life history and rates of diversification in Australian mammals

Abstract What causes species richness to vary among different groups of organisms? Two hypotheses are that large geographical ranges and fast life history either reduce extinction rates or raise speciation rates, elevating a clade's rate of diversification. Here we present a comparative analysis of these hypotheses using data on the phylogenetic relationships, geographical ranges and life history of the terrestrial mammal fauna of Australia. By comparing species richness patterns to null models, we show that species are distributed nonrandomly among genera. Using sister‐clade comparisons to control for clade age, we then find that faster diversification is significantly associated with larger geographical ranges and larger litters, but there is no evidence for an effect of body size or age at first breeding on diversification rates. We believe the most likely explanation for these patterns is that larger litters and geographical ranges increase diversification rates because they buffer species from extinction. We also discuss the possibility that positive effects of litter size and range size on diversification rates result from elevated speciation rates.     

Statistical analysis of diversification with species traits

Testing whether some species traits have a significant effect on diversification rates is central in the assessment of macroevolutionary theories. However, we still lack a powerful method to tackle this objective. I present a new method for the statistical analysis of diversification with species traits. The required data are observations of the traits on recent species, the phylogenetic tree of these species, and reconstructions of ancestral values of the traits. Several traits, either continuous or discrete, and in some cases their interactions, can be analyzed simultaneously. The parameters are estimated by the method of maximum likelihood. The statistical significance of the effects in a model can be tested with likelihood ratio tests. A simulation study showed that past random extinction events do not affect the Type I error rate of the tests, whereas statistical power is decreased, though some power is still kept if the effect of the simulated trait on speciation is strong. The use of the method is illustrated by the analysis of published data on primates. The analysis of these data showed that the apparent overall positive relationship between body mass and species diversity is actually an artifact due to a clade-specific effect. Within each clade the effect of body mass on speciation rate was in fact negative. The present method allows to take both effects (clade and body mass) into account simultaneously.     

A conceptual and statistical framework for adaptive radiations with a key role for diversity dependence

Abstract In this article we propose a new framework for studying adaptive radiations in the context of diversity-dependent diversification. Diversity dependence causes diversification to decelerate at the end of an adaptive radiation but also plays a key role in the initial pulse of diversification. In particular, key innovations (which in our definition include novel traits as well as new environments) may cause decoupling of the diversity-dependent dynamics of the innovative clade from the diversity-dependent dynamics of its ancestral clade. We present a likelihood-based inference method to test for decoupling of diversity dependence using molecular phylogenies. The method, which can handle incomplete phylogenies, identifies when the decoupling took place and which diversification parameters are affected. We illustrate our approach by applying it to the molecular phylogeny of the North American clade of the legume tribe Psoraleeae (47 extant species, of which 4 are missing). Two diversification rate shifts were previously identified for this clade; our analysis shows that the first, positive shift can be associated with decoupling of two Pediomelum subgenera from the other Psoraleeae lineages, while we argue that the second, negative shift can be attributed to speciation being protracted. The latter explanation yields nonzero extinction rates, in contrast to previous findings. Our framework offers a new perspective on macroevolution: new environments and novel traits (ecological opportunity) and diversity dependence (ecological limits) cannot be considered separately.     

Primate extinction risk and historical patterns of speciation and extinction in relation to body mass

Body mass is thought to influence diversification rates, but previous studies have produced ambiguous results. We investigated patterns of diversification across 100 trees obtained from a new Bayesian inference of primate phylogeny that sampled trees in proportion to their posterior probabilities. First, we used simulations to assess the validity of previous studies that used linear models to investigate the links between IUCN Red List status and body mass. These analyses support the use of linear models for ordinal ranked data on threat status, and phylogenetic generalized linear models revealed a significant positive correlation between current extinction risk and body mass across our tree block. We then investigated historical patterns of speciation and extinction rates using a recently developed maximum-likelihood method. Specifically, we predicted that body mass correlates positively with extinction rate because larger bodied organisms reproduce more slowly, and body mass correlates negatively with speciation rate because smaller bodied organisms are better able to partition niche space. We failed to find evidence that extinction rates covary with body mass across primate phylogeny. Similarly, the speciation rate was generally unrelated to body mass, except in some tests that indicated an increase in the speciation rate with increasing body mass. Importantly, we discovered that our data violated a key assumption of sample randomness with respect to body mass. After correcting for this bias, we found no association between diversification rates and mass.     

Clade age and not diversification rate explains species richness among animal taxa

Animal taxa show remarkable variability in species richness across phylogenetic groups. Most explanations for this disparity postulate that taxa with more species have phenotypes or ecologies that cause higher diversification rates (i.e., higher speciation rates or lower extinction rates). Here we show that clade longevity, and not diversification rate, has primarily shaped patterns of species richness across major animal clades: more diverse taxa are older and thus have had more time to accumulate species. Diversification rates calculated from 163 species-level molecular phylogenies were highly consistent within and among three major animal phyla (Arthropoda, Chordata, Mollusca) and did not correlate with species richness. Clades with higher estimated diversification rates were younger, but species numbers increased with increasing clade age. A fossil-based data set also revealed a strong, positive relationship between total extant species richness and crown group age across the orders of insects and vertebrates. These findings do not negate the importance of ecology or phenotype in influencing diversification rates, but they do show that clade longevity is the dominant signal in major animal biodiversity patterns. Thus, some key innovations may have acted through fostering clade longevity and not by heightening diversification rate.     

Primate diversification inferred from phylogenies and fossils

Biodiversity arises from the balance between speciation and extinction. Fossils record the origins and disappearance of organisms, and the branching patterns of molecular phylogenies allow estimation of speciation and extinction rates, but the patterns of diversification are frequently incongruent between these two data sources. I tested two hypotheses about the diversification of primates based on ～600 fossil species and 90% complete phylogenies of living species: (1) diversification rates increased through time; (2) a significant extinction event occurred in the Oligocene. Consistent with the first hypothesis, analyses of phylogenies supported increasing speciation rates and negligible extinction rates. In contrast, fossils showed that while speciation rates increased, speciation and extinction rates tended to be nearly equal, resulting in zero net diversification. Partially supporting the second hypothesis, the fossil data recorded a clear pattern of diversity decline in the Oligocene, although diversification rates were near zero. The phylogeny supported increased extinction ～34 Ma, but also elevated extinction ～10 Ma, coinciding with diversity declines in some fossil clades. The results demonstrated that estimates of speciation and extinction ignoring fossils are insufficient to infer diversification and information on extinct lineages should be incorporated into phylogenetic analyses.