Evolutionary ecomorphology for the twenty-first century: examples from mammalian carnivores.

Carnivores (cats, dogs and kin) are a diverse group of mammals that inhabit a remarkable range of ecological niches. While the relationship between ecology and morphology has long been of interest in carnivorans, the application of quantitative techniques has resulted in a recent explosion of work in the field. Therefore, they provide a case study of how quantitative techniques, such as geometric morphometrics (GMM), have impacted our ability to tease apart complex ecological signals from skeletal anatomy, and the implications for our understanding of the relationships between form, function and ecological specialization. This review provides a synthesis of current research on carnivoran ecomorphology, with the goal of illustrating the complex interaction between ecology and morphology in the skeleton. We explore the ecomorphological diversity across major carnivoran lineages and anatomical systems. We examine cranial elements (skull, sensory systems) and postcranial elements (limbs, vertebral column) to reveal mosaic patterns of adaptation related to feeding and hunting strategies, locomotion and habitat preference. We highlight the crucial role that new approaches have played in advancing our understanding of carnivoran ecomorphology, while addressing challenges that remain in the field, such as ecological classifications, form-function relationships and multi-element analysis, offering new avenues for future research.

Strategies of vascularization of the ethmoid labyrinth in selected even-toed ungulates (Artiodactyla) and carnivores (Carnivora).

The anatomy of the nasal cavity and its structures, as well as other elements building a scaffold for olfactory organs, differs significantly among various groups of mammals. Understanding anatomical conditions of quality of olfaction are being studied worldwide and is a complex problem. Among many studies regarding bone and epithelial structures of turbinates and connected anatomical structures, few studies describe the vascularization of turbinates. Ethmoid turbinates are above all covered in olfactory epithelium containing branched axons that receive olfactory stimuli and as olfactory nerves penetrate the cribriform lamina of the ethmoid bone conveying information from smell receptors to the brain. Differences in vascularization of the cribriform plate and turbinates may add crucial information complementing studies regarding the olfactory organ's bone and soft tissue structures. In the study, we describe the vascularization of the cribriform plate of the ethmoid bone of 54 Artiodactyla and Carnivora.

Giant Hyena Pachycrocuta brevirostris (Hyaenidae, Carnivora) from the Lower Pleistocene of Taurida Cave, Crimea.

The dental remains of a giant hyena Pachycrocuta brevirostris (Gervais, 1850) from the Early Pleistocene locality of the Taurida cave (Crimea, Late Villafranchian, 1.8-1.5 Ma) are described. This species was a typical representative of the Villafranchian fauna of the Eastern Mediterranean. The Taurida cave was occasionally used by hyenas and other carnivorans as a den and retreat.

Morphological evolution of the carnivoran sacrum.

The sacrum is a key piece of the vertebrate skeleton, since it connects the caudal region with the presacral region of the vertebral column and the hind limbs through the pelvis. Therefore, understanding its form and function is of great relevance in vertebrate ecomorphology. However, it is striking that morphometric studies that quantify its morphological evolution in relation to function are scarce. The main goal of this study is to investigate the morphological evolution of the sacrum in relation to its function in the mammalian order Carnivora, using three-dimensional (3D) geometric morphometrics. Principal component analysis under a phylogenetic background indicated that changes in sacrum morphology are mainly focused on the joint areas where it articulates with other parts of the skeleton allowing resistance to stress at these joints caused by increasing muscle loadings. In addition, we demonstrated that sacrum morphology is related to both the length of the tail relativised to the length of the body, and the length of the body relativised to body mass. We conclude that the sacrum in carnivores has evolved in response to the locomotor requirements of the species analysed, but in locomotion, each family has followed alternative morphological solutions to address the same functional demands.

Bayesian Estimation of Species Divergence Times Using Correlated Quantitative Characters.

Discrete morphological data have been widely used to study species evolution, but the use of quantitative (or continuous) morphological characters is less common. Here, we implement a Bayesian method to estimate species divergence times using quantitative characters. Quantitative character evolution is modeled using Brownian diffusion with character correlation and character variation within populations. Through simulations, we demonstrate that ignoring the population variation (or population "noise") and the correlation among characters leads to biased estimates of divergence times and rate, especially if the correlation and population noise are high. We apply our new method to the analysis of quantitative characters (cranium landmarks) and molecular data from carnivoran mammals. Our results show that time estimates are affected by whether the correlations and population noise are accounted for or ignored in the analysis. The estimates are also affected by the type of data analyzed, with analyses of morphological characters only, molecular data only, or a combination of both; showing noticeable differences among the time estimates. Rate variation of morphological characters among the carnivoran species appears to be very high, with Bayesian model selection indicating that the independent-rates model fits the morphological data better than the autocorrelated-rates model. We suggest that using morphological continuous characters, together with molecular data, can bring a new perspective to the study of species evolution. Our new model is implemented in the MCMCtree computer program for Bayesian inference of divergence times.

Brain Volume Fractions in Mammals in Relation to Behavior in Carnivores, Primates, Ungulates, and Rodents.

The volume fraction (VF) of a given brain region, or the proper mass, ought to reflect the importance of that region in the life of a given species. This study sought to examine the VF of various brain regions across 61 different species of mammals to discern if there were regularities or differences among mammalian orders. We examined the brains of carnivores (n = 17), ungulates (n = 8), rodents (n = 7), primates (n = 11), and other mammals (n = 18) from the online collections at the National Museum of Health and Medicine. We measured and obtained the VF of several brain regions: the striatum, thalamus, neocortex, cerebellum, hippocampus, and piriform area. We refined our analyses by using phylogenetic size correction, yielding the corrected (c)VF. Our groups showed marked differences in gross brain architecture. Primates and carnivores were divergent in some measures, particularly the cVF of the striatum, even though their overall brain size range was roughly the same. Rodents predictably had relatively large cVFs of subcortical structures due to the fact that their neocortical cVF was smaller, particularly when compared to primates. Not so predictably, rodents had the largest cerebellar cVF, and there were marked discrepancies in cerebellar data across groups. Ungulates had a larger piriform area than primates, perhaps due to their olfactory processing abilities. We provide interpretations of our results in the light of the comparative behavioral and neuroanatomical literature.

Taking a look into the orbit of mammalian carnivorans.

In this study, we explore the relationship between orbit anatomy and different ecological factors in carnivorous mammals from a phylogenetic perspective. We calculated the frontation (α), convergence (ß), and orbitotemporal (Ω) angles of the orbit from 3D coordinates of anatomical landmarks in a wide sample of carnivores with different kinds of visual strategy (i.e. photopic, scotopic, and mesopic), habitat (i.e. open, mixed, and closed), and substrate use (i.e. arboreal, terrestrial, and aquatic). We used Bloomberg's K and Pagel's λ to assess phylogenetic signal in frontation, convergence, and orbitotemporal angles. The association of orbit orientation with skull length and ecology was explored using phylogenetic generalized least squares and phylogenetic manova, respectively. Moreover, we also computed phylomorphospaces from orbit orientation. Our results indicate that there is not a clear association between orbit orientation and the ecology of living carnivorans. We hypothesize that the evolution of the orbit in mammalian carnivores represents a new case of an ecological bottleneck specific to carnivorans. New directions for future research are discussed in light of this new evidence.

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.

The Influence of Climatic Variability on Morphological Integration, Evolutionary Rates, and Disparity in the Carnivora.

Biodiversity is unevenly distributed in space and time. One possible explanation for this is the influence of climate on the ecology, evolution, and morphology of taxa. Here we investigated the link between climatic variability and phenotypic integration, rates of morphological evolution, and disparity (morphological diversity) in three carnivoran clades (Canidae, Felidae, and Mustelidae). We gathered landmark data from the lower jaw and extracted current temperature and precipitation data from range maps. We found a significant negative relationship between climatic variability and integration for canids and felids. Among canids, variability in temperature was the key climatic variable, while in felids it was a combination of variability in temperature and precipitation. In both cases, relatively variable climates were associated with low phenotypic integration. We also found evidence for a negative association between climatic variability and both disparity and rates of morphological evolution in canids and mustelids. Selection can drive the evolution of jaw shape along lines of least resistance defined by patterns of integration, and this study suggests that climate may be a predictor of phenotypic integration. As a result, taxa in more variable regions (e.g., temperate, montane) may be more evolvable and more able to respond to fluctuating environmental conditions over a period of generations.

Testing hypotheses for the function of the carnivoran baculum using finite-element analysis.

The baculum (os penis) is a mineralized bone within the glans of the mammalian penis and is one of the most morphologically diverse structures in the mammal skeleton. Recent experimental work provides compelling evidence for sexual selection shaping the baculum, yet the functional mechanism by which this occurs remains unknown. Previous studies have tested biomechanical hypotheses for the role of the baculum based on simple metrics such as length and diameter, ignoring the wealth of additional shape complexity present. For the first time, to our knowledge, we apply a computational simulation approach (finite-element analysis; FEA) to quantify the three-dimensional biomechanical performance of carnivoran bacula (n = 74) based upon high-resolution micro-computed tomography scans. We find a marginally significant positive correlation between sexual size dimorphism and baculum stress under compressive loading, counter to the 'vaginal friction' hypothesis of bacula becoming more robust to overcome resistance during initial intromission. However, a highly significant negative relationship exists between intromission duration and baculum stress under dorsoventral bending. Furthermore, additional FEA simulations confirm that the presence of a ventral groove would reduce deformation of the urethra. We take this as evidence in support of the 'prolonged intromission' hypothesis, suggesting the carnivoran baculum has evolved in response to pressures on the duration of copulation and protection of the urethra.

Reconstruction of body cavity volume in terrestrial tetrapods.

Although it is generally assumed that herbivores have more voluminous body cavities due to larger digestive tracts required for the digestion of plant fiber, this concept has not been addressed quantitatively. We estimated the volume of the torso in 126 terrestrial tetrapods (synapsids including basal synapsids and mammals, and diapsids including birds, non-avian dinosaurs and reptiles) classified as either herbivore or carnivore in digital models of mounted skeletons, using the convex hull method. The difference in relative torso volume between diet types was significant in mammals, where relative torso volumes of herbivores were about twice as large as that of carnivores, supporting the general hypothesis. However, this effect was not evident in diapsids. This may either reflect the difficulty to reliably reconstruct mounted skeletons in non-avian dinosaurs, or a fundamental difference in the bauplan of different groups of tetrapods, for example due to differences in respiratory anatomy. Evidently, the condition in mammals should not be automatically assumed in other, including more basal, tetrapod lineages. In both synapsids and diapsids, large animals showed a high degree of divergence with respect to the proportion of their convex hull directly supported by bone, with animals like elephants or Triceratops having a low proportion, and animals such as rhinoceros having a high proportion of bony support. The relevance of this difference remains to be further investigated.

Postcopulatory sexual selection influences baculum evolution in primates and carnivores.

The extreme morphological variability of the baculum across mammals is thought to be the result of sexual selection (particularly, high levels of postcopulatory selection). However, the evolutionary trajectory of the mammalian baculum is little studied and evidence for the adaptive function of the baculum has so far been elusive. Here, we use Markov chain Monte Carlo methods implemented in a Bayesian phylogenetic framework to reconstruct baculum evolution across the mammalian class and investigate the rate of baculum length evolution within the primate order. We then test the effects of testes mass (postcopulatory sexual selection), polygamy, seasonal breeding and intromission duration on the baculum in primates and carnivores. The ancestral mammal did not have a baculum, but both ancestral primates and carnivores did. No relationship was found between testes mass and baculum length in either primates or carnivores. Intromission duration correlated with baculum presence over the course of primate evolution, and prolonged intromission predicts significantly longer bacula in extant primates and carnivores. Both polygamous and seasonal breeding systems predict significantly longer bacula in primates. These results suggest the baculum plays an important role in facilitating reproductive strategies in populations with high levels of postcopulatory sexual selection.

A unique feeding strategy of the extinct marine mammal Kolponomos: convergence on sabretooths and sea otters.

Mammalian molluscivores feed mainly by shell-crushing or suction-feeding. The extinct marine arctoid, Kolponomos, has been interpreted as an otter-like shell-crusher based on similar dentitions. However, neither the masticatory biomechanics of the shell-crushing adaptation nor the way Kolponomos may have captured hard-shelled prey have been tested. Based on mandibular symphyseal morphology shared by Kolponomos and sabre-toothed carnivores, we hypothesize a sabretooth-like mechanism for Kolponomos prey-capture, whereby the mandible functioned as an anchor. Torque generated from jaw closure and head flexion was used to dislodge prey by prying, with prey then crushed using cheek teeth. We test this hypothesized feeding sequence using phylogenetically informed biomechanical simulations and shape analyses, and find a strongly supported, shared high mandibular stiffness in simulated prey-capture bites and mandibular shape in Kolponomos and the sabre-toothed cat Smilodon. These two distantly related taxa converged on using mandibles to anchor cranial torqueing forces when prying substrate-bound prey in the former and sabre-driving forces during prey-killing in the latter. Simulated prey-crushing bites indicate that Kolponomos and sea otters exhibit alternative structural stiffness-bite efficiency combinations in mandibular biomechanical adaptation for shell-crushing. This unique feeding system of Kolponomos exemplifies a mosaic of form-function convergence relative to other Carnivora.

Life history, cognition and the evolution of complex foraging niches.

Animal species that live in complex foraging niches have, in general, improved access to energy-rich and seasonally stable food sources. Because human food procurement is uniquely complex, we ask here which conditions may have allowed species to evolve into such complex foraging niches, and also how niche complexity is related to relative brain size. To do so, we divided niche complexity into a knowledge-learning and a motor-learning dimension. Using a sample of 78 primate and 65 carnivoran species, we found that two life-history features are consistently correlated with complex niches: slow, conservative development or provisioning of offspring over extended periods of time. Both act to buffer low energy yields during periods of learning, and may thus act as limiting factors for the evolution of complex niches. Our results further showed that the knowledge and motor dimensions of niche complexity were correlated with pace of development in primates only, and with the length of provisioning in only carnivorans. Accordingly, in primates, but not carnivorans, living in a complex foraging niche requires enhanced cognitive abilities, i.e., a large brain. The patterns in these two groups of mammals show that selection favors evolution into complex niches (in either the knowledge or motor dimension) in species that either develop more slowly or provision their young for an extended period of time. These findings help to explain how humans constructed by far the most complex niche: our ancestors managed to combine slow development (as in other primates) with systematic provisioning of immatures and even adults (as in carnivorans). This study also provides strong support for the importance of ecological factors in brain size evolution.

The more, the better: the use of multiple landmark configurations to solve the phylogenetic relationships in musteloids.

Although the use of landmark data to study shape changes along a phylogenetic tree has become a common practice in evolutionary studies, the role of this sort of data for the inference of phylogenetic relationships remains under debate. Theoretical issues aside, the very existence of historical information in landmark data has been challenged, since phylogenetic analyses have often shown little congruence with alternative sources of evidence. However, most analyses conducted in the past were based upon a single landmark configuration, leaving it unsettled whether the incorporation of multiple configurations may improve the rather poor performance of this data source in most previous phylogenetic analyses. In the present study, we present a phylogenetic analysis of landmark data that combines information derived from several skeletal structures to derive a phylogenetic tree for musteloids. The analysis includes nine configurations representing different skeletal structures for 24 species. The resulting tree presents several notable concordances with phylogenetic hypotheses derived from molecular data. In particular, Mephitidae, Procyonidae, and Lutrinae plus the genera Martes, Mustela, Galictis, and Procyon were retrieved as monophyletic. In addition, other groupings were in agreement with molecular phylogenies or presented only minor discordances. Complementary analyses have also indicated that the results improve substantially when an increasing number of landmark configurations are included in the analysis. The results presented here thus highlight the importance of combining information from multiple structures to derive phylogenetic hypotheses from landmark data.

Evolution of Gyrification in Carnivores.

The order Carnivora is a large and highly diverse mammalian group with a long and well-documented evolutionary history. Nevertheless, our knowledge on the degree of cortical folding (or degree of gyrification) is limited to just a few species. Here we investigate the degree of cortical folding in 64 contemporary and 37 fossil carnivore species. We do so by measuring the length of gyri impressions on endocranial casts. We use this approach because we have found that there is a very good correlation between the degree of cortical folding and the relative length of the gyri that are exposed on the outer surface of the hemispheres. Our results indicate that aquatic and semiaquatic carnivores have higher degrees of cortical folding than terrestrial carnivores. The degree of cortical folding varies among modern families, with viverrids having the lowest values. Furthermore, the scaling of cortical folding with brain size follows different patterns across specific carnivore families. Forty million years ago, the first carnivores had a relatively small cortex and limited cortical folding. Both the size of the cortex and the degree of cortical folding increased independently in each family during evolution.

Impact of the terrestrial-aquatic transition on disparity and rates of evolution in the carnivoran skull.

BACKGROUND: Which factors influence the distribution patterns of morphological diversity among clades? The adaptive radiation model predicts that a clade entering new ecological niche will experience high rates of evolution early in its history, followed by a gradual slowing. Here we measure disparity and rates of evolution in Carnivora, specifically focusing on the terrestrial-aquatic transition in Pinnipedia. We analyze fissiped (mostly terrestrial, arboreal, and semi-arboreal, but also including the semi-aquatic otter) and pinniped (secondarily aquatic) carnivorans as a case study of an extreme ecological transition. We used 3D geometric morphometrics to quantify cranial shape in 151 carnivoran specimens (64 fissiped, 87 pinniped) and five exceptionally-preserved fossil pinnipeds, including the stem-pinniped Enaliarctos emlongi. Range-based and variance-based disparity measures were compared between pinnipeds and fissipeds. To distinguish between evolutionary modes, a Brownian motion model was compared to selective regime shifts associated with the terrestrial-aquatic transition and at the base of Pinnipedia. Further, evolutionary patterns were estimated on individual branches using both Ornstein-Uhlenbeck and Independent Evolution models, to examine the origin of pinniped diversity. RESULTS: Pinnipeds exhibit greater cranial disparity than fissipeds, even though they are less taxonomically diverse and, as a clade nested within fissipeds, phylogenetically younger. Despite this, there is no increase in the rate of morphological evolution at the base of Pinnipedia, as would be predicted by an adaptive radiation model, and a Brownian motion model of evolution is supported. Instead basal pinnipeds populated new areas of morphospace via low to moderate rates of evolution in new directions, followed by later bursts within the crown-group, potentially associated with ecological diversification within the marine realm. CONCLUSION: The transition to an aquatic habitat in carnivorans resulted in a shift in cranial morphology without an increase in rate in the stem lineage, contra to the adaptive radiation model. Instead these data suggest a release from evolutionary constraint model, followed by aquatic diversifications within crown families.

A three-dimensional analysis of the morphological evolution and locomotor behaviour of the carnivoran hind limb.

BACKGROUND: The shape of the appendicular bones in mammals usually reflects adaptations towards different locomotor abilities. However, other aspects such as body size and phylogeny also play an important role in shaping bone design.We used 3D landmark-based geometric morphometrics to analyse the shape of the hind limb bones (i.e., femur, tibia, and pelvic girdle bones) of living and extinct terrestrial carnivorans (Mammalia, Carnivora) to quantitatively investigate the influence of body size, phylogeny, and locomotor behaviour in shaping the morphology of these bones. We also investigated the main patterns of morphological variation within a phylogenetic context. RESULTS: Size and phylogeny strongly influence the shape of the hind limb bones. In contrast, adaptations towards different modes of locomotion seem to have little influence. Principal Components Analysis and the study of phylomorphospaces suggest that the main source of variation in bone shape is a gradient of slenderness-robustness. CONCLUSION: The shape of the hind limb bones is strongly influenced by body size and phylogeny, but not to a similar degree by locomotor behaviour. The slender-robust "morphological bipolarity" found in bone shape variability is probably related to a trade-off between maintaining energetic efficiency and withstanding resistance to stresses. The balance involved in this trade-off impedes the evolution of high phenotypic variability. In fact, both morphological extremes (slender/robust) are adaptive in different selective contexts and lead to a convergence in shape among taxa with extremely different ecologies but with similar biomechanical demands. Strikingly, this "one-to-many mapping" pattern of evolution between morphology and ecology in hind limb bones is in complete contrast to the "many-to-one mapping" pattern found in the evolution of carnivoran skull shape. The results suggest that there are more constraints in the evolution of the shape of the appendicular skeleton than in that of skull shape because of the strong biomechanical constraints imposed by terrestrial locomotion.

Diversity, disparity, and evolutionary rate estimation for unresolved Yule trees.

The branching structure of biological evolution confers statistical dependencies on phenotypic trait values in related organisms. For this reason, comparative macroevolutionary studies usually begin with an inferred phylogeny that describes the evolutionary relationships of the organisms of interest. The probability of the observed trait data can be computed by assuming a model for trait evolution, such as Brownian motion, over the branches of this fixed tree. However, the phylogenetic tree itself contributes statistical uncertainty to estimates of rates of phenotypic evolution, and many comparative evolutionary biologists regard the tree as a nuisance parameter. In this article, we present a framework for analytically integrating over unknown phylogenetic trees in comparative evolutionary studies by assuming that the tree arises from a continuous-time Markov branching model called the Yule process. To do this, we derive a closed-form expression for the distribution of phylogenetic diversity (PD), which is the sum of branch lengths connecting the species in a clade. We then present a generalization of PD which is equivalent to the expected trait disparity in a set of taxa whose evolutionary relationships are generated by a Yule process and whose traits evolve by Brownian motion. We find expressions for the distribution of expected trait disparity under a Yule tree. Given one or more observations of trait disparity in a clade, we perform fast likelihood-based estimation of the Brownian variance for unresolved clades. Our method does not require simulation or a fixed phylogenetic tree. We conclude with a brief example illustrating Brownian rate estimation for 12 families in the mammalian order Carnivora, in which the phylogenetic tree for each family is unresolved.

CT scanning analysis of Megantereon whitei (Carnivora, Machairodontinae) from Monte Argentario (Early Pleistocene, central Italy): evidence of atavistic teeth.

CT scanning analysis applied to vertebrate palaeontology is providing an increasing number of data of great interest. This method can be used in many branches of palaeontology such as the investigation of all the fossilized elements in a hard matrix and the hidden structures in the bones. A large number of pathologies are "hidden", completely or partially invisible on the external surface of the bones because their development took place within the bones. However, the study of these diseases and abnormalities plays a crucial role in our understanding of evolutionary and adaptive processes of extinct taxa. The analysis of a partial skeleton of the sabre-toothed felid Megantereon whitei from the Early Pleistocene karst filling deposits of Monte Argentario (Tuscany, Italy) has been carried out. The CT scanning analysis put in evidence the presence of supernumerary teeth (P(2)) and the absence of P3 in the mandible. The occurrence of P(2) can be considered as an evidence of atavism. Such an archaic feature is recorded for the first time in Megantereon.