Bayesian Prediction of Multivariate Ecology from Phenotypic Data Yields New Insights into the Diets of Extant and Extinct Taxa.

AbstractMorphology often reflects ecology, enabling the prediction of ecological roles for taxa that lack direct observations, such as fossils. In comparative analyses, ecological traits, like diet, are often treated as categorical, which may aid prediction and simplify analyses but ignores the multivariate nature of ecological niches. Furthermore, methods for quantifying and predicting multivariate ecology remain rare. Here, we ranked the relative importance of 13 food items for a sample of 88 extant carnivoran mammals and then used Bayesian multilevel modeling to assess whether those rankings could be predicted from dental morphology and body size. Traditional diet categories fail to capture the true multivariate nature of carnivoran diets, but Bayesian regression models derived from living taxa have good predictive accuracy for importance ranks. Using our models to predict the importance of individual food items, the multivariate dietary niche, and the nearest extant analogs for a set of data-deficient extant and extinct carnivoran species confirms long-standing ideas for some taxa but yields new insights into the fundamental dietary niches of others. Our approach provides a promising alternative to traditional dietary classifications. Importantly, this approach need not be limited to diet but serves as a general framework for predicting multivariate ecology from phenotypic traits.

The Effects of Foraging Ecology and Allometry on Avian Skull Shape Vary across Levels of Phylogeny.

AbstractAvian skull shape diversity is classically thought to result from selection for structures that are well adapted for distinct ecological functions, but recent work has suggested that allometry is the dominant contributor to avian morphological diversity. If true, this hypothesis would overturn much conventional wisdom regarding the importance of form-function relationships in adaptive radiations, but it is possible that these results are biased by the low taxonomic levels of the clades that have been studied. Using 3D morphometric data from the skulls of a relatively old and ecologically diverse order of birds, the Charadriiformes (shorebirds and relatives), we found that foraging ecology explains more than two-thirds of the variation in skull shape across the clade. However, we also found support for the hypothesis that skull allometry evolves, contributing more to shape variation at the level of the family than the order. Allometry may provide an important source of shape variation on which selection can act over short timescales, but its potential to evolve complicates generalizations between clades. Foraging ecology remains a better predictor of avian skull shape over macroevolutionary timescales.

Extant species fail to estimate ancestral geographical ranges at older nodes in primate phylogeny.

A clade's evolutionary history is shaped, in part, by geographical range expansion, sweepstakes dispersal and local extinction. A rigorous understanding of historical biogeography may therefore yield insights into macroevolutionary dynamics such as adaptive radiation. Modern historical biogeographic analyses typically fit statistical models to molecular phylogenies, but it remains unclear whether extant species provide sufficient signal or if well-sampled phylogenies of extinct and extant taxa are necessary to produce meaningful estimates of past ranges. We investigated the historical biogeography of Primates and their euarchontan relatives using a novel meta-analytical phylogeny of over 900 extant (n= 419) and extinct (n = 483) species spanning their entire evolutionary history. Ancestral range estimates for young nodes were largely congruent with those derived from molecular phylogeny. However, node age exerts a significant effect on ancestral range estimate congruence, and the probability of congruent inference dropped below 0.5 for nodes older than the late Eocene, corresponding to the origins of higher-level clades. Discordance was not observed in analyses of extinct taxa alone. Fossils are essential for robust ancestral range inference and biogeographic analyses of extant clades originating in the deep past should be viewed with scepticism without them.

Empirical and Methodological Challenges to the Model-Based Inference of Diversification Rates in Extinct Clades.

Changes in speciation and extinction rates are key to the dynamics of clade diversification, but attempts to infer them from phylogenies of extant species face challenges. Methods capable of synthesizing information from extant and fossil species have yielded novel insights into diversification rate variation through time, but little is known about their behavior when analyzing entirely extinct clades. Here, we use empirical and simulated data to assess how two popular methods, PyRate and Fossil BAMM, perform in this setting. We inferred the first tip-dated trees for ornithischian dinosaurs and combined them with fossil occurrence data to test whether the clade underwent an end-Cretaceous decline. We then simulated phylogenies and fossil records under empirical constraints to determine whether macroevolutionary and preservation rates can be teased apart under paleobiologically realistic conditions. We obtained discordant inferences about ornithischian macroevolution including a long-term speciation rate decline (BAMM), mostly flat rates with a steep diversification drop (PyRate) or without one (BAMM), and episodes of implausibly accelerated speciation and extinction (PyRate). Simulations revealed little to no conflation between speciation and preservation, but yielded spuriously correlated speciation and extinction estimates while time-smearing tree-wide shifts (BAMM) or overestimating their number (PyRate). Our results indicate that the small phylogenetic data sets available to vertebrate paleontologists and the assumptions made by current model-based methods combine to yield potentially unreliable inferences about the diversification of extinct clades. We provide guidelines for interpreting the results of the existing approaches in light of their limitations and suggest how the latter may be mitigated. [BAMM; diversification; fossils; macroevolutionary rates; Ornithischia; PyRate.].

A Total-Group Phylogenetic Metatree for Cetacea and the Importance of Fossil Data in Diversification Analyses.

Phylogenetic trees provide a powerful framework for testing macroevolutionary hypotheses, but it is becoming increasingly apparent that inferences derived from extant species alone can be highly misleading. Trees incorporating living and extinct taxa are needed to address fundamental questions about the origins of diversity and disparity but it has proved challenging to generate robust, species-rich phylogenies that include large numbers of fossil taxa. As a result, most studies of diversification dynamics continue to rely on molecular phylogenies. Here, we extend and apply a recently developed meta-analytic approach for synthesizing previously published phylogenetic studies to infer a well-resolved set of species level, time-scaled phylogenetic hypotheses for extinct and extant cetaceans (whales, dolphins, and allies). Our trees extend sampling from the $\sim 90$ extant species to over 500 living and extinct species, and therefore allow for more robust inference of macroevolutionary dynamics. While the diversification scenarios, we recover are broadly concordant with those inferred from molecular phylogenies they differ in critical ways, notably in the relative contributions of extinction and speciation rate shifts in driving rapid radiations. The metatree approach provides the most immediate route for generating higher level phylogenies of extinct taxa and opens the door to re-evaluation of macroevolutionary hypotheses derived only from extant taxa.[Extinction; macroevolution; matrix representation with parsimony; morphology; supertree.].

Evolutionary history of quadrupedal walking gaits shows mammalian release from locomotor constraint.

Vertebrates employ an impressive range of strategies for coordinating their limb movements while walking. Although this gait variation has been quantified and hypotheses for its origins tested in select tetrapod lineages, a comprehensive understanding of gait evolution in a macroevolutionary context is currently lacking. We used freely available internet videos to nearly double the number of species with quantitative gait data, and used phylogenetic comparative methods to test key hypotheses about symmetrical gait origin and evolution. We find strong support for an ancestral lateral-sequence diagonal-couplet gait in quadrupedal gnathostomes, and this mode is remarkably conserved throughout tetrapod phylogeny. Evolutionary rate analyses show that mammals overcame this ancestral constraint, resulting in a greater range of phase values than any other tetrapod lineage. Diagonal-sequence diagonal-couplet gaits are significantly associated with arboreality in mammals, though this relationship is not recovered for other tetrapod lineages. Notably, the lateral-sequence lateral-couplet gait, unique to mammals among extant tetrapods, is not associated with any traditional explanations. The complex drivers of gait diversification in mammals remain unclear, but our analyses suggest that their success was due, in part, to release from a locomotor constraint that has probably persisted in other extant tetrapod lineages for over 375 Myr.

Disparities in the analysis of morphological disparity.

Analyses of morphological disparity have been used to characterize and investigate the evolution of variation in the anatomy, function and ecology of organisms since the 1980s. While a diversity of methods have been employed, it is unclear whether they provide equivalent insights. Here, we review the most commonly used approaches for characterizing and analysing morphological disparity, all of which have associated limitations that, if ignored, can lead to misinterpretation. We propose best practice guidelines for disparity analyses, while noting that there can be no 'one-size-fits-all' approach. The available tools should always be used in the context of a specific biological question that will determine data and method selection at every stage of the analysis.

Lineage Diversity and Size Disparity in Musteloidea: Testing Patterns of Adaptive Radiation Using Molecular and Fossil-Based Methods.

Adaptive radiation is hypothesized to be a primary mechanism that drives the remarkable species diversity and morphological disparity across the Tree of Life. Tests for adaptive radiation in extant taxa are traditionally estimated from calibrated molecular phylogenies with little input from extinct taxa. With 85 putative species in 33 genera and over 400 described extinct species, the carnivoran superfamily Musteloidea is a prime candidate to investigate patterns of adaptive radiation using both extant- and fossil-based macroevolutionary methods. The species diversity and equally impressive ecological and phenotypic diversity found across Musteloidea is often attributed to two adaptive radiations coinciding with two major climate events, the Eocene-Oligocene transition and the Mid-Miocene Climate Transition. Here, we compiled a novel time-scaled phylogeny for 88% of extant musteloids and used it as a framework for testing the predictions of adaptive radiation hypotheses with respect to rates of lineage diversification and phenotypic evolution. Contrary to expectations, we found no evidence for rapid bursts of lineage diversification at the origin of Musteloidea, and further analyses of lineage diversification rates using molecular and fossil-based methods did not find associations between rates of lineage diversification and the Eocene-Oligocene transition or Mid-Miocene Climate Transition as previously hypothesized. Rather, we found support for decoupled diversification dynamics driven by increased clade carrying capacity in the branches leading to a subclade of elongate mustelids. Supporting decoupled diversification dynamics between the subclade of elongate mustelids and the ancestral musteloid regime is our finding of increased rates of body length evolution, but not body mass evolution, within the decoupled mustelid subclade. The lack of correspondence in rates of body mass and length evolution suggest that phenotypic evolutionary rates under a single morphological metric, even one as influential as mass, may not capture the evolution of diversity in clades that exhibit elongate body shapes. The discordance in evolutionary rates between body length and body mass along with evidence of decoupled diversification dynamics suggests that body elongation might be an innovation for the exploitation of novel Mid-Miocene resources, resulting in the radiation of some musteloids.

Iterative adaptive radiations of fossil canids show no evidence for diversity-dependent trait evolution.

A long-standing hypothesis in adaptive radiation theory is that ecological opportunity constrains rates of phenotypic evolution, generating a burst of morphological disparity early in clade history. Empirical support for the early burst model is rare in comparative data, however. One possible reason for this lack of support is that most phylogenetic tests have focused on extant clades, neglecting information from fossil taxa. Here, I test for the expected signature of adaptive radiation using the outstanding 40-My fossil record of North American canids. Models implying time- and diversity-dependent rates of morphological evolution are strongly rejected for two ecologically important traits, body size and grinding area of the molar teeth. Instead, Ornstein-Uhlenbeck processes implying repeated, and sometimes rapid, attraction to distinct dietary adaptive peaks receive substantial support. Diversity-dependent rates of morphological evolution seem uncommon in clades, such as canids, that exhibit a pattern of replicated adaptive radiation. Instead, these clades might best be thought of as deterministic radiations in constrained Simpsonian subzones of a major adaptive zone. Support for adaptive peak models may be diagnostic of subzonal radiations. It remains to be seen whether early burst or ecological opportunity models can explain broader adaptive radiations, such as the evolution of higher taxa.

Independent evolution of baleen whale gigantism linked to Plio-Pleistocene ocean dynamics.

Vertebrates have evolved to gigantic sizes repeatedly over the past 250 Myr, reaching their extreme in today's baleen whales (Mysticeti). Hypotheses for the evolution of exceptionally large size in mysticetes range from niche partitioning to predator avoidance, but there has been no quantitative examination of body size evolutionary dynamics in this clade and it remains unclear when, why or how gigantism evolved. By fitting phylogenetic macroevolutionary models to a dataset consisting of living and extinct species, we show that mysticetes underwent a clade-wide shift in their mode of body size evolution during the Plio-Pleistocene. This transition, from Brownian motion-like dynamics to a trended random walk towards larger size, is temporally linked to the onset of seasonally intensified upwelling along coastal ecosystems. High prey densities resulting from wind-driven upwelling, rather than abundant resources alone, are the primary determinant of efficient foraging in extant mysticetes and Late Pliocene changes in ocean dynamics may have provided an ecological pathway to gigantism in multiple independent lineages.