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 dynamic adaptive landscape of cetacean body size.

Adaptive landscapes are central to evolutionary theory, forming a conceptual bridge between micro- and macroevolution.1,2,3,4 Evolution by natural selection across an adaptive landscape should drive lineages toward fitness peaks, shaping the distribution of phenotypic variation within and among clades over evolutionary timescales.5 The location and breadth of these peaks in phenotypic space can also evolve,4 but whether phylogenetic comparative methods can detect such patterns has largely remained unexplored.6 Here, we characterize the global and local adaptive landscape for total body length in cetaceans (whales, dolphins, and relatives), a trait that spans an order of magnitude, across their ∼53-million-year evolutionary history. Using phylogenetic comparative methods, we analyze shifts in long-term mean body length7 and directional changes in average trait values8 for 345 living and fossil cetacean taxa. Remarkably, we find that the global macroevolutionary adaptive landscape of cetacean body length is relatively flat, with very few peak shifts occurring after cetaceans entered the oceans. Local peaks are more numerous and manifest as trends along branches linked to specific adaptations. These results contrast with previous studies using only extant taxa,9 highlighting the vital role of fossil data for understanding macroevolution.10,11,12 Our results indicate that adaptive peaks are dynamic and are associated with subzones of local adaptations, creating moving targets for species adaptation. In addition, we identify limits in our ability to detect some evolutionary patterns and processes and suggest that multiple approaches are required to characterize complex hierarchical patterns of adaptation in deep time.

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.

Topographically distinct adaptive landscapes for teeth, skeletons, and size explain the adaptive radiation of Carnivora (Mammalia).

Models of adaptive radiation were originally developed to explain the early, rapid appearance of distinct modes of life within diversifying clades. Phylogenetic tests of this hypothesis have yielded limited support for temporally declining rates of phenotypic evolution across diverse clades, but the concept of an adaptive landscape that links form to fitness, while also crucial to these models, has received more limited attention. Using methods that assess the temporal accumulation of morphological variation and estimate the topography of the underlying adaptive landscape, I found evidence of an early partitioning of mandibulo-dental morphological variation in Carnivora (Mammalia) that occurs on an adaptive landscape with multiple peaks, consistent with classic ideas about adaptive radiation. Although strong support for this mode of adaptive radiation is present in traits related to diet, its signal is not present in body mass data or for traits related to locomotor behavior and substrate use. These findings suggest that adaptive radiations may occur along some axes of ecomorphological variation without leaving a signal in others and that their dynamics are more complex than simple univariate tests might suggest.

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.

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.

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.].

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.

Palaeoproteomics resolves sloth relationships.

The living tree sloths Choloepus and Bradypus are the only remaining members of Folivora, a major xenarthran radiation that occupied a wide range of habitats in many parts of the western hemisphere during the Cenozoic, including both continents and the West Indies. Ancient DNA evidence has played only a minor role in folivoran systematics, as most sloths lived in places not conducive to genomic preservation. Here we utilize collagen sequence information, both separately and in combination with published mitochondrial DNA evidence, to assess the relationships of tree sloths and their extinct relatives. Results from phylogenetic analysis of these datasets differ substantially from morphology-based concepts: Choloepus groups with Mylodontidae, not Megalonychidae; Bradypus and Megalonyx pair together as megatherioids, while monophyletic Antillean sloths may be sister to all other folivorans. Divergence estimates are consistent with fossil evidence for mid-Cenozoic presence of sloths in the West Indies and an early Miocene radiation in South America.

Shared extremes by ectotherms and endotherms: Body elongation in mustelids is associated with small size and reduced limbs.

An elongate body with reduced or absent limbs has evolved independently in many ectothermic vertebrate lineages. While much effort has been spent examining the morphological pathways to elongation in these clades, quantitative investigations into the evolution of elongation in endothermic clades are lacking. We quantified body shape in 61 musteloid mammals (red panda, skunks, raccoons, and weasels) using the head-body elongation ratio. We also examined the morphological changes that may underlie the evolution toward more extreme body plans. We found that a mustelid clade comprised of the subfamilies Helictidinae, Guloninae, Ictonychinae, Mustelinae, and Lutrinae exhibited an evolutionary transition toward more elongate bodies. Furthermore, we discovered that elongation of the body is associated with the evolution of other key traits such as a reduction in body size and a reduction in forelimb length but not hindlimb length. This relationship between body elongation and forelimb length has not previously been quantitatively established for mammals but is consistent with trends exhibited by ectothermic vertebrates and suggests a common pattern of trait covariance associated with body shape evolution. This study provides the framework for documenting body shapes across a wider range of mammalian clades to better understand the morphological changes influencing shape disparity across all vertebrates.

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.

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.

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.

Evolutionary Relationships among Extinct and Extant Sloths: The Evidence of Mitogenomes and Retroviruses.

Macroevolutionary trends exhibited by retroviruses are complex and not entirely understood. The sloth endogenized foamy-like retrovirus (SloEFV), which demonstrates incongruence in virus-host evolution among extant sloths (Order Folivora), has not been investigated heretofore in any extinct sloth lineages and its premodern history within folivorans is therefore unknown. Determining retroviral coevolutionary trends requires a robust phylogeny of the viral host, but the highly reduced modern sloth fauna (6 species in 2 genera) does not adequately represent what was once a highly diversified clade (∼100 genera) of placental mammals. At present, the amount of molecular data available for extinct sloth taxa is limited, and analytical results based on these data tend to conflict with phylogenetic inferences made on the basis of morphological studies. To augment the molecular data set, we applied hybridization capture and next-generation Illumina sequencing to two extinct and three extant sloth species to retrieve full mitochondrial genomes (mitogenomes) from the hosts and the polymerase gene of SloEFV. The results produced a fully resolved and well-supported phylogeny that supports dividing crown families into two major clades: 1) The three-toed sloth, Bradypus, and Nothrotheriidae and 2) Megalonychidae, including the two-toed sloth, Choloepus, and Mylodontidae. Our calibrated time tree indicates that the Miocene epoch (23.5 Ma), particularly its earlier part, was an important interval for folivoran diversification. Both extant and extinct sloths demonstrate multiple complex invasions of SloEFV into the ancestral sloth germline followed by subsequent introgressions across different sloth lineages. Thus, sloth mitogenome and SloEFV evolution occurred separately and in parallel among sloths.

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.

Placing cryptic, recently extinct, or hypothesized taxa into an ultrametric phylogeny using continuous character data: a case study with the lizard Anolis roosevelti.

In recent years, enormous effort and investment has been put into assembling the tree of life: a phylogenetic history for all species on Earth. Overwhelmingly, this progress toward building an ever increasingly complete phylogeny of living things has been accomplished through sophisticated analysis of molecular data. In the modern genomic age, molecular genetic data have become very easy and inexpensive to obtain for many species. However, some lineages are poorly represented in or absent from tissue collections, or are unavailable for molecular analysis for other reasons such as restrictive biological sample export laws. Other species went extinct recently and are only available in formalin museum preparations or perhaps even as subfossils. In this brief communication we present a new method for placing cryptic, recently extinct, or hypothesized taxa into an ultrametric phylogeny of extant taxa using continuous character data. This method is based on a relatively simple modification of an established maximum likelihood (ML) method for phylogeny inference from continuous traits. We show that the method works well on simulated trees and data. We then apply it to the case of placing the Culebra Island Giant Anole (Anolis roosevelti) into a phylogeny of Caribbean anoles. Anolis roosevelti is a "crown-giant" ecomorph anole hypothesized to have once been found throughout the Spanish, United States, and British Virgin Islands, but that has not been encountered or collected since the 1930s. Although this species is widely thought to be closely related to the Puerto Rican giant anole, A. cuvieri, our ML method actually places A. roosevelti in a different part of the tree and closely related to a clade of morphologically similar species. We are unable, however, to reject a phylogenetic position for A. roosevelti that places it as sister taxon to A. cuvieri; although close relationship with the remainder of Puerto Rican anole species is strongly rejected by our method.

Biogeography and taxonomy of extinct and endangered monk seals illuminated by ancient DNA and skull morphology.

Extinctions and declines of large marine vertebrates have major ecological impacts and are of critical concern in marine environments. The Caribbean monk seal, Monachus tropicalis, last definitively reported in 1952, was one of the few marine mammal species to become extinct in historical times. Despite its importance for understanding the evolutionary biogeography of southern phocids, the relationships of M. tropicalis to the two living species of critically endangered monk seals have not been resolved. In this study we present the first molecular data for M. tropicalis, derived from museum skins. Phylogenetic analysis of cytochrome b sequences indicates that M. tropicalis was more closely related to the Hawaiian rather than the Mediterranean monk seal. Divergence time estimation implicates the formation of the Panamanian Isthmus in the speciation of Caribbean and Hawaiian monk seals. Molecular, morphological and temporal divergence between the Mediterranean and "New World monk seals" (Hawaiian and Caribbean) is profound, equivalent to or greater than between sister genera of phocids. As a result, we classify the Caribbean and Hawaiian monk seals together in a newly erected genus, Neomonachus. The two genera of extant monk seals (Monachus and Neomonachus) represent old evolutionary lineages each represented by a single critically endangered species, both warranting continuing and concerted conservation attention and investment if they are to avoid the fate of their Caribbean relative.