Graham J. Slater

Multigene phylogeny of the Mustelidae: Resolving relationships, tempo and biogeographic history of a mammalian adaptive radiation

BackgroundAdaptive radiation, the evolution of ecological and phenotypic diversity from a common ancestor, is a central concept in evolutionary biology and characterizes the evolutionary histories of many groups of organisms. One such group is the Mustelidae, the most species-rich family within the mammalian order Carnivora, encompassing 59 species classified into 22 genera. Extant mustelids display extensive ecomorphological diversity, with different lineages having evolved into an array of adaptive zones, from fossorial badgers to semi-aquatic otters. Mustelids are also widely distributed, with multiple genera found on different continents. As with other groups that have undergone adaptive radiation, resolving the phylogenetic history of mustelids presents a number of challenges because ecomorphological convergence may potentially confound morphologically based phylogenetic inferences, and because adaptive radiations often include one or more periods of rapid cladogenesis that require a large amount of data to resolve.ResultsWe constructed a nearly complete generic-level phylogeny of the Mustelidae using a data matrix comprising 22 gene segments (~12,000 base pairs) analyzed with maximum parsimony, maximum likelihood and Bayesian inference methods. We show that mustelids are consistently resolved with high nodal support into four major clades and three monotypic lineages. Using Bayesian dating techniques, we provide evidence that mustelids underwent two bursts of diversification that coincide with major paleoenvironmental and biotic changes that occurred during the Neogene and correspond with similar bursts of cladogenesis in other vertebrate groups. Biogeographical analyses indicate that most of the extant diversity of mustelids originated in Eurasia and mustelids have colonized Africa, North America and South America on multiple occasions.ConclusionCombined with information from the fossil record, our phylogenetic and dating analyses suggest that mustelid diversification may have been spurred by a combination of faunal turnover events and diversification at lower trophic levels, ultimately caused by climatically driven environmental changes. Our biogeographic analyses show Eurasia as the center of origin of mustelid diversity and that mustelids in Africa, North America and South America have been assembled over time largely via dispersal, which has important implications for understanding the ecology of mustelid communities.

Diversity versus disparity and the radiation of modern cetaceans

Modern whales are frequently described as an adaptive radiation spurred by either the evolution of various key innovations (such as baleen or echolocation) or ecological opportunity following the demise of archaic whales. Recent analyses of diversification rate shifts on molecular phylogenies raise doubts about this interpretation since they find no evidence of increased speciation rates during the early evolution of modern taxa. However, one of the central predictions of ecological adaptive radiation is rapid phenotypic diversification, and the tempo of phenotypic evolution has yet to be quantified in cetaceans. Using a time-calibrated molecular phylogeny of extant cetaceans and a morphological dataset on size, we find evidence that cetacean lineages partitioned size niches early in the evolutionary history of neocetes and that changes in cetacean size are consistent with shifts in dietary strategy. We conclude that the signature of adaptive radiations may be retained within morphological traits even after equilibrium diversity has been reached and high extinction or fluctuations in net diversification have erased any signature of an early burst of diversification in the structure of the phylogeny.

INTEGRATING FOSSILS WITH MOLECULAR PHYLOGENIES IMPROVES INFERENCE OF TRAIT EVOLUTION

Comparative biologists often attempt to draw inferences about tempo and mode in evolution by comparing the fit of evolutionary models to phylogenetic comparative data consisting of a molecular phylogeny with branch lengths and trait measurements from extant taxa. These kinds of approaches ignore historical evidence for evolutionary pattern and process contained in the fossil record. In this article, we show through simulation that incorporation of fossil information dramatically improves our ability to distinguish among models of quantitative trait evolution using comparative data. We further suggest a novel Bayesian approach that allows fossil information to be integrated even when explicit phylogenetic hypotheses are lacking for extinct representatives of extant clades. By applying this approach to a comparative dataset comprising body sizes for caniform carnivorans, we show that incorporation of fossil information not only improves ancestral state estimates relative to those derived from extant taxa alone, but also results in preference of a model of evolution with trend toward large body size over alternative models such as Brownian motion or Ornstein–Uhlenbeck processes. Our approach highlights the importance of considering fossil information when making macroevolutionary inference, and provides a way to integrate the kind of sparse fossil information that is available to most evolutionary biologists.

Clade Age and Species Richness Are Decoupled Across the Eukaryotic Tree of Life

Explaining the dramatic variation in species richness across the tree of life remains a key challenge in evolutionary biology. At the largest phylogenetic scales, the extreme heterogeneity in species richness observed among different groups of organisms is almost certainly a function of many complex and interdependent factors. However, the most fundamental expectation in macroevolutionary studies is simply that species richness in extant clades should be correlated with clade age: all things being equal, older clades will have had more time for diversity to accumulate than younger clades. Here, we test the relationship between stem clade age and species richness across 1,397 major clades of multicellular eukaryotes that collectively account for more than 1.2 million described species. We find no evidence that clade age predicts species richness at this scale. We demonstrate that this decoupling of age and richness is unlikely to result from variation in net diversification rates among clades. At the largest phylogenetic scales, contemporary patterns of species richness are inconsistent with unbounded diversity increase through time. These results imply that a fundamentally different interpretative paradigm may be needed in the study of phylogenetic diversity patterns in many groups of organisms.

Iterative Ecological Radiation and Convergence during the Evolutionary History of Damselfishes (Pomacentridae)

Coral reef fishes represent one of the most spectacularly diverse assemblages of vertebrates on the planet, but our understanding of their mode of diversification remains limited. Here we test whether the diversity of the damselfishes (Pomacentridae), one of the most species-rich families of reef-associated fishes, was produced by a single or multiple adaptive radiation(s) during their evolutionary history. Tests of the tempo of lineage diversification using a time-calibrated phylogeny including 208 species revealed that crown pomacentrid diversification has not slowed through time as expected under a scenario of a single adaptive radiation resulting from an early burst of diversification. Evolutionary modeling of trophic traits similarly rejected the hypothesis of early among-lineage partitioning of ecologically important phenotypic diversity. Instead, damselfishes are shown to have experienced iterative convergent radiations wherein subclades radiate across similar trophic strategies (i.e., pelagic feeders, benthic feeders, intermediate) and morphologies. Regionalization of coral reefs, competition, and functional constraints may have fueled iterative ecological radiation and convergent evolution of damselfishes. Through the Pomacentridae, we illustrate that radiations may be strongly structured by the nature of the constraints on diversification.

geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees

SUMMARY Phylogenetic comparative methods are essential for addressing evolutionary hypotheses with interspecific data. The scale and scope of such data have increased dramatically in the past few years. Many existing approaches are either computationally infeasible or inappropriate for data of this size. To address both of these problems, we present geiger v2.0, a complete overhaul of the popular R package geiger. We have reimplemented existing methods with more efficient algorithms and have developed several new approaches for accomodating heterogeneous models and data types. AVAILABILITY AND IMPLEMENTATION  This R package is available on the CRAN repository http://cran.r-project.org/web/packages/geiger/. All source code is also available on github http://github.com/mwpennell/geiger-v2. geiger v2.0 depends on the ape package. CONTACT mwpennell@gmail.com SUPPLEMENTARY INFORMATION  Supplementary data are available at Bioinformatics online.

Phylogenetic evidence for a shift in the mode of mammalian body size evolution at the Cretaceous‐Palaeogene boundary

Summary Phylogenetic comparative methods provide a powerful way of addressing classic questions about tempo and mode of phenotypic evolution in the fossil record, such as whether mammals increased in body size diversity after the Cretaceous-Palaeogene (K-Pg) extinction. Most often, these kinds of questions are addressed in the context of variation in evolutionary rates. Shifts in the mode of phenotypic evolution provide an alternative and, in some cases, more realistic explanation for patterns of trait diversity in the fossil record, but these kinds of processes are rarely tested for. In this study, I use a time-calibrated phylogeny of living and fossil Mammaliaformes as a framework to test novel models of body size evolution derived from palaeontological theory. Specifically, I ask whether the K-Pg extinction resulted in a change in rates of body size evolution or release from a constrained adaptive zone. I found that a model comprising an Ornstein–Uhlenbeck process until the K-Pg event and a Brownian motion process from the Cenozoic onwards was the best supported model for these data. Surprisingly, results indicate a lower absolute rate of body size evolution during the Cenozoic than during the Mesozoic. This is explained by release from a stationary OU process that constrained realized disparity. Despite a lower absolute rate, body size disparity has in fact been increasing since the K-Pg event. The use of time-calibrated phylogenies of living and extinct taxa and realistic, process-based models provides unparalleled power in testing evolutionary hypotheses. However, researchers should take care to ensure that the models they use are appropriate to the question being tested and that the parameters estimated are interpreted in the context of the best fitting model.

Allometry and performance: the evolution of skull form and function in felids

Allometric patterns of skull‐shape variation can have significant impacts on cranial mechanics and feeding performance, but have received little attention in previous studies. Here, we examine the impacts of allometric skull‐shape variation on feeding capabilities in the cat family (Felidae) with linear morphometrics and finite element analysis. Our results reveal that relative bite force diminishes slightly with increasing skull size, and that the skulls of the smallest species undergo the least strain during biting. However, larger felids are able to produce greater gapes for a given angle of jaw opening, and they have overall stronger skulls. The two large felids in this study achieved increased cranial strength by increasing skull bone volume relative to surface area. Allometry of skull geometry in large felids reflects a trade‐off between the need to increase gape to access larger prey while maintaining the ability to resist unpredictable loading when taking large, struggling prey.

Long in the tooth: evolution of sabertooth cat cranial shape

Abstract Sabertooths exhibit one of the most extreme feeding adaptations seen in mammals. The functional consequences of accommodating extremely elongate upper canine teeth are severe, resulting in a well-documented suite of cranial modifications. We used geometric morphometric methods to study the evolution of overall shape in the skulls of extant and extinct feline and machairodontine felids, as well as extinct nimravids. Trends in skull evolution were evaluated by using relative warps analysis and tested for association with body size and canine tooth length. Primitive sabertooths from all lineages exhibit cranial shapes more similar to conical-toothed cats, despite the presence of moderately developed saberteeth. More-derived forms in both nimravids and felids diverge in skull morphospace to form two distinct sabertooth types (dirk-toothed and scimitar-toothed) that differ in canine shape. Skull shape in conical-toothed cats is strongly associated with body size, but not canine length. However, within each sabertooth lineage, skull shape is significantly correlated with canine length, suggesting that gape-related demands drove the evolution of sabertooth skull morphology.

Shape at the cross-roads: homoplasy and history in the evolution of the carnivoran skull towards herbivory

Patterns of skull shape in Carnivora provide examples of parallel and convergent evolution for similar ecomorphological adaptations. However, although most researchers report on skull homoplasies among hypercarnivorous taxa, evolutionary trends towards herbivory remain largely unexplored. In this study, we analyse the skull of the living herbivorous carnivorans to evaluate the importance of natural selection and phylogenetic legacy in shaping the skulls of these peculiar species. We quantitatively estimated shape variability using geometric morphometrics. A principal components analysis of skull shape incorporating all families of arctoid carnivorans recognized several common adaptations towards herbivory. Ancestral state reconstructions of skull shape and the reconstructed phylogenetic history of morphospace occupation more explicitly reveal the true patterns of homoplasy among the herbivorous carnivorans. Our results indicate that both historical constraints and adaptation have interplayed in the evolution towards herbivory of the carnivoran skull, which has resulted in repeated patterns of biomechanical homoplasy.