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.     

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.     

Climatic niche conservatism and the evolutionary dynamics in species range boundaries: global congruence across mammals and amphibians

Aim Comparative evidence for phylogenetic niche conservatism – the tendency for lineages to retain their ancestral niches over long time scales – has so far been mixed, depending on spatial and taxonomic scale. We quantify and compare conservatism in the climatic factors defining range boundaries in extant continental mammals and amphibians in order to identify those factors that are most evolutionarily conserved, and thus hypothesized to have played a major role in determining the geographic distributions of many species. We also test whether amphibians show stronger signals of climatic niche conservatism, as expected from their greater physiological sensitivity and lower dispersal abilities. Location Global; continental land masses excluding Antarctica. Methods We used nearly complete global distributional databases to estimate the climatic niche conservatism in extant continental mammals and amphibians. We characterized the climatic niche of each species by using a suite of variables and separately investigate conservatism in each variable using both taxonomic and phylogenetic approaches. Finally, we explored the spatial, taxonomic and phylogenetic patterns in recent climatic niche evolution. Results Amphibians and mammals showed congruent patterns of conservatism in cold tolerance, with assemblages of escapee species (i.e. those escaping most from the climatic constraints of their ancestors) aggregated in the North Temperate Zone. Main conclusions The relative strength of climatic niche conservatism varies across the variables tested, but is strongest for cold tolerance in both mammals and amphibians. Despite the apparent conservatism in this variable, there is also a strong signal of recent evolutionary shifts in cold tolerance in assemblages inhabiting the North Temperate Zone. Our results thus indicate that distribution patterns of both taxa are influenced by both niche conservatism and niche evolution.     

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.     

Zoogeographical regions and geospatial patterns of phylogenetic diversity and endemism of New World bats

The analysis of regional scale patterns of diversity allows insights into the processes that have shaped modern biodiversity at the macro‐scale. Previous analyses studying biogeographic regionalisation across different high‐level taxa have shown similar trends at a global scale. However, incorporating phylogenetic methods when comparing biogeographic regionalisation between subgroups facilitates identification of mechanisms leading to the biogeographic distribution of specific taxa. We analysed the spatial trends of phylogenetic diversity and phylogenetic endemism of 325 species of New World bats, using updated range maps of the modern distributions. These analyses showed phylogeographic signals that reflect the different evolutionary histories of these families. Zoogeographical zones were detected based on range‐weighted phylogenetic turnover. Values of high phylogenetic diversity and endemism were distributed differently across families, suggesting niche conservatism, but a general latitudinal trend of diversity was evident across taxa. Overall, two main bioregions were shared across New World bat taxa (Nearctic and Neotropical), with two additional subregions (Andean and La Platan). We found strong support for an additional transitional zone in the Pacific coast of South America for Emballonuridae and Molossidae. Differences in regionalisation across families indicate that niche conservatism, in situ diversification and dispersal ability are major drivers for the regionalisation of New World bats, within a dual‐centre of diversification scenario. We also found strong inter‐familial support for an independent Caribbean biogeographic region.     

Diversity dynamics of Miocene mammals in relation to the history of tectonism and climate

Continental biodiversity gradients result not only from ecological processes, but also from evolutionary and geohistorical processes involving biotic turnover in landscape and climatic history over millions of years. Here, we investigate the evolutionary and historical contributions to the gradient of increasing species richness with topographic complexity. We analysed a dataset of 418 fossil rodent species from western North America spanning 25 to 5 Ma. We compared diversification histories between tectonically active (Intermontane West) and quiescent (Great Plains) regions. Although diversification histories differed between the two regions, species richness, origination rate and extinction rate per million years were not systematically different over the 20 Myr interval. In the tectonically active region, the greatest increase in originations coincided with a Middle Miocene episode of intensified tectonic activity and global warming. During subsequent global cooling, species richness declined in the montane region and increased on the Great Plains. These results suggest that interactions between tectonic activity and climate change stimulate diversification in mammals. The elevational diversity gradient characteristic of modern mammalian faunas was not a persistent feature over geologic time. Rather, the Miocene rodent record suggests that the elevational diversity gradient is a transient feature arising during particular episodes of Earth''s history.     

Mixed evidence for early bursts of morphological evolution in extant clades

Macroevolutionary theory predicts high rates of evolution should occur early in a clade's history as species exploit ecological opportunity. Evidence from the fossil record has shown a high prevalence of early bursts in morphological evolution, but recent work has provided little evidence for early high rates in the evolution of extant clades. Here, I test the prevalence of early bursts in extant data using phylogenetic comparative methods. Existing models are extended to allow a shift from a background Brownian motion (BM) process to an early burst process within subclades of phylogenies, rather than an early burst being applied to an entire phylogenetic tree. This nested early burst model is compared to other modes of evolution that can occur within subclades, such as evolution with a constraint (Ornstein‐Uhlenbeck model) and nested BM rate shift models. These relaxed models are validated using simulations and then are applied to body size evolution of three major clades of amniotes (mammals, squamates and aves) at different levels of taxonomic organization (order, family). Applying these unconstrained models greatly increases the support for early bursts within nested subclades, and so early bursts are the most common model of evolution when only one shift is analysed. However, the relative fit of early burst models is worse than models that allow for multiple shifts of the BM or OU process. No single‐shift or homogenous model is superior to models of multiple shifts in BM or OU evolution, but the patterns shown by these multirate models are generally congruent with patterns expected from early bursts.     

Correlates of species richness in the largest Neotropical amphibian radiation

Although tropical environments are often considered biodiversity hotspots, it is precisely in such environments where least is known about the factors that drive species richness. Here, we use phylogenetic comparative analyses to study correlates of species richness for the largest Neotropical amphibian radiation: New World direct-developing frogs. Clade-age and species richness were nonsignificantly, negatively correlated, suggesting that clade age alone does not explain among-clade variation in species richness. A combination of ecological and morphological traits explained 65% of the variance in species richness. A more vascularized ventral skin, the ability to colonize high-altitude ranges, encompassing a large variety of vegetation types, correlated significantly with species richness, whereas larger body size was marginally correlated with species richness. Hence, whereas high-altitude ranges play a role in shaping clade diversity in the Neotropics, intrinsic factors, such as skin structures and possibly body size, might ultimately determine which clades are more speciose than others.     

A nuclear DNA phylogenetic perspective on the evolution of echolocation and historical biogeography of extant bats (chiroptera)

Bats (Order Chiroptera), the only mammals capable of powered flight and sophisticated laryngeal echolocation, represent one of the most species-rich and ubiquitous orders of mammals. However, phylogenetic relationships within this group are poorly resolved. A robust evolutionary tree of Chiroptera is essential for evaluating the phylogeny of echolocation within Chiroptera, as well as for understanding their biogeographical history. We generated 4 kb of sequence data from portions of four novel nuclear intron markers for multiple representatives of 17 of the 18 recognized extant bat families, as well as the putative bat family Miniopteridae. Three echolocation-call characters were examined by mapping them onto the combined topology: (1) high-duty cycle versus low-duty cycle, (2) high-intensity versus low-intensity call emission, and (3) oral versus nasal emission. Echolocation seems to be highly convergent, and the mapping of echolocation-call design onto our phylogeny does not appear to resolve the question of whether echolocation had a single or two origins. Fossil taxa may also provide insight into the evolution of bats; we therefore evaluate 195 morphological characters in light of our nuclear DNA phylogeny. All but 24 of the morphological characters were found to be homoplasious when mapped onto the supermatrix topology, while the remaining characters provided insufficient information to reconstruct the placement of the fossil bat taxa with respect to extant families. However, a morphological synapomorphy characterizing the Rhinolophoidea was identified and is suggestive of a separate origin of echolocation in this clade. Dispersal-Vicariance analysis together with a relaxed Bayesian clock were used to evaluate possible biogeographic scenarios that could account for the current distribution pattern of extant bat families. Africa was reconstructed as the center of origin of modern-day bat families.     

Exceptional among-lineage variation in diversification rates during the radiation of Australia's most diverse vertebrate clade

The disparity in species richness among groups of organisms is one of the most pervasive features of life on earth. A number of studies have addressed this pattern across higher taxa (e.g. 'beetles'), but we know much less about the generality and causal basis of the variation in diversity within evolutionary radiations at lower taxonomic scales. Here, we address the causes of variation in species richness among major lineages of Australia's most diverse vertebrate radiation, a clade of at least 232 species of scincid lizards. We use new mitochondrial and nuclear intron DNA sequences to test the extent of diversification rate variation in this group. We present an improved likelihood-based method for estimating per-lineage diversification rates from combined phylogenetic and taxonomic (species richness) data, and use the method in a hypothesis-testing framework to localize diversification rate shifts on phylogenetic trees. We soundly reject homogeneity of diversification rates among members of this radiation, and find evidence for a dramatic rate increase in the common ancestor of the genera Ctenotus and Lerista. Our results suggest that the evolution of traits associated with climate tolerance may have had a role in shaping patterns of diversity in this group.     

Functional differences in echolocation call design in an adaptive radiation of bats

All organisms have specialized systems to sense their environment. Most bat species use echolocation for navigation and foraging, but which and how ecological factors shaped echolocation call diversity remains unclear for the most diverse clades, including the adaptive radiation of neotropical leaf‐nosed bats (Phyllostomidae). This is because phyllostomids emit low‐intensity echolocation calls and many inhabit dense forests, leading to low representation in acoustic surveys. We present a field‐collected, echolocation call dataset spanning 35 species and all phyllostomid dietary guilds. We analyze these data under a phylogenetic framework to test the hypothesis that echolocation call design and parameters are specialized for the acoustic demands of different diets, and investigate the contributions of phylogeny and body size to echolocation call diversity. We further link call parameters to dietary ecology by contrasting minimum detectable prey size estimates (MDPSE) across species. We find phylogeny and body size explain a substantial proportion of echolocation call parameter diversity, but most species can be correctly assigned to taxonomic (61%) or functional (77%) dietary guilds based on call parameters. This suggests a degree of acoustic ecological specialization, albeit with interspecific similarities in call structure. Theoretical MDPSE are greatest for omnivores and smallest for insectivores. Omnivores significantly differ from other dietary guilds in MDPSE when phylogeny is not considered, but there are no differences among taxonomic dietary guilds within a phylogenetic context. Similarly, predators of non‐mobile/non‐evasive prey and predators of mobile/evasive prey differ in estimated MDPSE when phylogeny is not considered. Phyllostomid echolocation call structure may be primarily specialized for overcoming acoustic challenges of foraging in dense habitats, and then secondarily specialized for the detection of food items according to functional dietary guilds. Our results give insight into the possible ecological mechanisms shaping the diversity of sensory systems, and their reciprocal influence on resource use.     

Biotic and abiotic factors driving the diversification dynamics of Crocodylia

Species diversity patterns are governed by complex interactions among biotic and abiotic factors over time and space, but are essentially the result of the diversification dynamics (differential speciation and extinction rates) over the long-term evolutionary history of a clade. Previous studies have suggested that temporal variation in global temperature drove long-term diversity changes in Crocodylia, a monophyletic group of large ectothermic organisms. We use a large database of crocodylian fossil occurrences (192 spp.) and body mass estimations, under a taxic approach, to characterize the global diversification dynamics of crocodylians since the Cretaceous, and their correlation with multiple biotic and abiotic factors in a Bayesian framework. The diversification dynamic of crocodylians, which appears to have originated in the Turonian (c. 92.5 Ma), is characterized by several phases with high extinction and speciation rates within a predominantly low long-term mean rate. Our results reveal long-term diversification dynamics of Crocodylia to be a highly complex process driven by a combination of biotic and abiotic factors which influenced the speciation and extinction rates in dissimilar ways. Higher crocodylian extinction rates are related to low body mass disparity, indicating selective extinctions of taxa at both ends of the body mass spectrum. Speciation rate slowdowns are noted when the diversity of the clade is high and the warm temperate climatic belt is reduced. Our finding supports the idea that temporal variations of body mass disparity, self-diversity, and the warm climate belt size provided more direct mechanistic explanations for crocodylian diversification than do proxies of global temperature.     

Hierarchy in adaptive radiation: A case study using the Carnivora (Mammalia)

Simpson's “early burst” model of adaptive radiation was intended to explain the early proliferation of morphological and functional variation in diversifying clades. Yet, despite much empirical testing, questions remain regarding its frequency across the tree of life. Here, we evaluate the support for an early burst model of adaptive radiation in 14 ecomorphological traits plus body mass for the extant mammalian order Carnivora and its constituent families. We find strong support for early bursts of dental evolution, suggesting a classic Simpsonian adaptive radiation along dietary resource axes. However, the signal of this early burst is not consistently recovered in analyses at the family level, where support for a variety of different models emerges. Furthermore, we find no evidence for early burst–like dynamics in size–related traits, and Bayesian analyses of evolutionary correlations corroborate a decoupling of size and dental evolution, driven in part by dietary specialization. Our results are consistent with the perspective that trait diversification unfolds hierarchically, with early bursts restricted to traits associated with higher level niches, such as macrohabitat use or dietary strategy, and thus with the origins of higher taxa. The lack of support for early burst adaptive radiation in previous phylogenetic studies may be a consequence of focusing on low‐level niche traits (i.e., those associated with microhabitat use) in clades at shallow phylogenetic levels. A richer understanding of early burst adaptive radiation will require a renewed focus on functional traits and their evolution over higher level clades.     

The shape of mammalian phylogeny: patterns, processes and scales

Mammalian phylogeny is far too asymmetric for all contemporaneous lineages to have had equal chances of diversifying. We consider this asymmetry or imbalance from four perspectives. First, we infer a minimal set of 'regime changes'-points at which net diversification rate has changed-identifying 15 significant radiations and 12 clades that may be 'downshifts'. We next show that mammalian phylogeny is similar in shape to a large set of published phylogenies of other vertebrate, arthropod and plant groups, suggesting that many clades may diversify under a largely shared set of 'rules'. Third, we simulate six simple macroevolutionary models, showing that those where speciation slows down as geographical or niche space is filled, produce more realistic phylogenies than do models involving key innovations. Lastly, an analysis of the spatial scaling of imbalance shows that the phylogeny of species within an assemblage, ecoregion or larger area always tends to be more unbalanced than expected from the phylogeny of species at the next more inclusive spatial scale. We conclude with a verbal model of mammalian macroevolution, which emphasizes the importance to diversification of accessing new regions of geographical or niche space.     

Historical and contemporary processes drive global phylogenetic structure across geographical scales: Insights from bat communities

Aim

Patterns of evolutionary relatedness among co-occurring species are driven by scale-dependent contemporary and historical processes. Yet, we still lack a detailed understanding of how these drivers impact the phylogenetic structure of biological communities. Here, we focused on bats (one of the most species-rich and vagile groups of mammals) and tested the predictions of three general biogeographical hypotheses that are particularly relevant to understanding how palaeoclimatic stability, local diversification rates and geographical scales shaped their present-day phylogenetic community structure.

Location

World-wide, across restrictive geographical extents: global, east–west hemispheres, biogeographical realms, tectonic plates, biomes and ecoregions.

Time period

Last Glacial Maximum (~22,000 years ago) to the present.

Major taxa studied

Bats (Chiroptera).

Methods

We estimated bat phylogenetic community structure across restrictive geographical extents and modelled it as a function of palaeoclimatic stability and in situ net diversification rates.

Results

Limiting geographical extents from larger to smaller scales greatly changed the phylogenetic structure of bat communities. The magnitude of these effects is less noticeable in the western hemisphere, where frequent among-realm biota interchange could have been maintained through the adaptive traits of bats. Bat communities with high phylogenetic relatedness are generally more common in regions that have changed less in climate since the Last Glacial Maximum, supporting the expectation that stable climates allow for increased phylogenetic clustering. Finally, increased in situ net diversification rates are associated with greater phylogenetic clustering in bat communities.

Main conclusions

We show that the world-wide phylogenetic structure of bat assemblages varies as a function of geographical extents, dispersal barriers, palaeoclimatic stability and in situ diversification. The integrative framework used in our study, which can be applied to other taxonomic groups, has not only proved useful to explain the evolutionary dynamics of community assembly, but could also help to tackle questions related to scale dependence in community ecology and biogeography.     

Mass turnover and recovery dynamics of a diverse Australian continental radiation

Trends in global and local climate history have been linked to observed macroevolutionary patterns across a variety of organisms. These climatic pressures may unilaterally or asymmetrically influence the evolutionary trajectory of clades. To test and compare signatures of changing global (Eocene‐Oligocene boundary cooling) and continental (Miocene aridification) environments on a continental fauna, we investigated the macroevolutionary dynamics of one of Australia's most diverse endemic radiations, pygopodoid geckos. We generated a time‐calibrated phylogeny (>90% taxon coverage) to test whether (i) asymmetrical pygopodoid tree shape may be the result of mass turnover deep in the group's history, and (ii) how Miocene aridification shaped trends in biome assemblages. We find evidence of mass turnover in pygopodoids following the isolation of the Australian continental plate ～30 million years ago, and in contrast, gradual aridification is linked to elevated speciation rates in the young arid zone. Surprisingly, our results suggest that invasion of arid habitats was not an evolutionary end point. Instead, arid Australia has acted as a source for diversity, with repeated outward dispersals having facilitated diversification of this group. This pattern contrasts trends in richness and distribution of other Australian vertebrates, illustrating the profound effects historical biome changes have on macroevolutionary patterns.