Uncovering the mosaic evolution of the carnivoran skeletal system.

The diversity of vertebrate skeletons is often attributed to adaptations to distinct ecological factors such as diet, locomotion, and sensory environment. Although the adaptive evolution of skull, appendicular skeleton, and vertebral column is well studied in vertebrates, comprehensive investigations of all skeletal components simultaneously are rarely performed. Consequently, we know little of how modes of evolution differ among skeletal components. Here, we tested if ecological and phylogenetic effects led to distinct modes of evolution among the cranial, appendicular and vertebral regions in extant carnivoran skeletons. Using multivariate evolutionary models, we found mosaic evolution in which only the mandible, hindlimb and posterior (i.e. last thoracic and lumbar) vertebrae showed evidence of adaptation towards ecological regimes whereas the remaining skeletal components reflect clade-specific evolutionary shifts. We hypothesize that the decoupled evolution of individual skeletal components may have led to the origination of distinct adaptive zones and morphologies among extant carnivoran families that reflect phylogenetic hierarchies. Overall, our work highlights the importance of examining multiple skeletal components simultaneously in ecomorphological analyses. Ongoing work integrating the fossil and palaeoenvironmental record will further clarify deep-time drivers that govern the carnivoran diversity we see today and reveal the complexity of evolutionary processes in multicomponent systems.

Scaling patterns of body plans differ among squirrel ecotypes.

Body size is often hypothesized to facilitate or constrain morphological diversity in the cranial, appendicular, and axial skeletons. However, how overall body shape scales with body size (i.e., body shape allometry) and whether these scaling patterns differ between ecological groups remains poorly investigated. Here, we test whether and how the relationships between body shape, body size, and limb lengths differ among species with different locomotor specializations, and describe the underlying morphological components that contribute to body shape evolution among squirrel (Sciuridae) ecotypes. We quantified the body size and shape of 87 squirrel species from osteological specimens held at museum collections. Using phylogenetic comparative methods, we first found that body shape and its underlying morphological components scale allometrically with body size, but these allometric patterns differ among squirrel ecotypes: chipmunks and gliding squirrels exhibited more elongate bodies with increasing body sizes whereas ground squirrels exhibited more robust bodies with increasing body size. Second, we found that only ground squirrels exhibit a relationship between forelimb length and body shape, where more elongate species exhibit relatively shorter forelimbs. Third, we found that the relative length of the ribs and elongation or shortening of the thoracic region contributes the most to body shape evolution across squirrels. Overall, our work contributes to the growing understanding of mammalian body shape evolution and how it is influenced by body size and locomotor ecology, in this case from robust subterranean to gracile gliding squirrels.

Decoupled evolution of the cranium and mandible in carnivoran mammals.

The relationship between skull morphology and diet is a prime example of adaptive evolution. In mammals, the skull consists of the cranium and the mandible. Although the mandible is expected to evolve more directly in response to dietary changes, dietary regimes may have less influence on the cranium because additional sensory and brain-protection functions may impose constraints on its morphological evolution. Here, we tested this hypothesis by comparing the evolutionary patterns of cranium and mandible shape and size across 100+ species of carnivoran mammals with distinct feeding ecologies. Our results show decoupled modes of evolution in cranial and mandibular shape; cranial shape follows clade-based evolutionary shifts, whereas mandibular shape evolution is linked to broad dietary regimes. These results are consistent with previous hypotheses regarding hierarchical morphological evolution in carnivorans and greater evolutionary lability of the mandible with respect to diet. Furthermore, in hypercarnivores, the evolution of both cranial and mandibular size is associated with relative prey size. This demonstrates that dietary diversity can be loosely structured by craniomandibular size within some guilds. Our results suggest that mammal skull morphological evolution is shaped by mechanisms beyond dietary adaptation alone.

Scaling patterns of cerebellar petrosal lobules in Euarchontoglires: Impacts of ecology and phylogeny.

The petrosal lobules (in whole or part homologous with the paraflocculi) of the cerebellum regulate functions associated with vision including smooth pursuit and velocity control of eye movements, suggesting a possible relationship between the petrosal lobules and behavioral adaptation. Previous studies have produced diverging conclusions regarding the lobules' ecological signal. The current study examines lobule scaling within an ecologically diverse but phylogenetically constrained sample of extant mammals to determine whether ecology influences relative petrosal lobule size. Using the endocasts of 140 Euarchontoglires (Primates, Scandentia, Dermoptera, Lagomorpha, Rodentia), petrosal lobule size was evaluated relative to endocranium and body size, accounting for phylogenetic relationships and ecology (locomotor behavior, diet, activity pattern). Results show a strong positive relationship between lobule size and both endocranial volume and body mass. Phylogeny is a major factor in the scaling of the petrosal lobules, with significant differences in relative size identified between orders and suborders. Concerning ecology, fossorial taxa were found to have significantly smaller petrosal lobules relative to body mass compared to other locomotor groups across Euarchontoglires. The small lobules possessed by this group may reflect an adaptation related to reduced visual reliance. In contrast to previous research, no relationship was identified between relative lobule size and any other ecological variables. While variation in relative lobule size may be adaptively significant in some groups (i.e., fossorial species), it is critical to study the evolution of petrosal lobule size within a narrow phylogenetic scope, with inclusion of fossil material to inform our understanding of evolutionary trajectories.

Different Evolutionary Pathways Lead to Incomplete Convergence of Elongate Body Shapes in Carnivoran Mammals.

Although convergence is often recognized as a ubiquitous feature across the Tree of Life, whether the underlying traits also exhibit similar evolutionary pathways towards convergent forms puzzles biologists. In carnivoran mammals, "elongate," "slender," and "long" are often used to describe and even to categorize mustelids (martens, polecats, and weasels), herpestids (mongooses), viverrids (civets and genets), and other carnivorans together. But just how similar these carnivorans are and whether there is convergence in the morphological component that contribute to elongation has never been assessed. Here, I found that these qualitatively described elongate carnivorans exhibited incomplete convergence towards elongate bodies compared to other terrestrial carnivorans. In contrast, the morphological components underlying body shape variation do not exhibit convergence despite evidence that these components are more elongate in elongate carnivorans compared to nonelongate carnivorans. Furthermore, these components also exhibited shorter but different phylogenetic half-lives towards more elongate adaptive peaks, indicating that different selective pressures can create multiple pathways to elongation. Incorporating the fossil record will facilitate further investigation of whether body elongation evolved adaptively or if it is simply a retained ancestral trait.[Axial skeleton; body elongation; convergent evolution; macroevolution; phylogenetic comparative methods; thoracolumbar vertebrae.].

Ecological Drivers of Carnivoran Body Shape Evolution.

AbstractMorphological diversity is often attributed as adaptations to distinct ecologies. Although biologists have long hypothesized that distinct ecologies drive the evolution of body shape, these relationships are rarely tested across macroevolutionary scales in mammals. Here, I tested hypotheses that locomotor, hunting, and dietary ecologies influenced body shape evolution in carnivorans, a morphologically and ecologically diverse clade of mammals. I found that adaptive models with ecological trait regimes were poor predictors of carnivoran body shape and the underlying morphological components that contribute to body shape variation. Instead, the best-supported model exhibited clade-based evolutionary shifts, indicating that the complexity and variation of body shape landscape cannot be effectively captured by a priori ecological regimes. However, ecological adaptations of body shapes cannot be ruled out, as aquatic and terrestrial carnivorans exhibited opposite allometric patterns of body shape that may be driven by different gravitational constraints associated with these different environments. Similar to body size, body shape is a prominent feature of vertebrate morphology that may transcend one-to-one mapping relationships between morphology and ecological traits, enabling species with distinct body shapes to exploit similar resources and exhibit similar ecologies. Together, these results demonstrate that the multidimensionality of both body shape morphology and ecology makes it difficult to disentangle the complex relationship among morphological evolution, ecological diversity, and phylogeny across macroevolutionary scales.

Linking ecomechanical models and functional traits to understand phenotypic diversity.

Physical principles and laws determine the set of possible organismal phenotypes. Constraints arising from development, the environment, and evolutionary history then yield workable, integrated phenotypes. We propose a theoretical and practical framework that considers the role of changing environments. This 'ecomechanical approach' integrates functional organismal traits with the ecological variables. This approach informs our ability to predict species shifts in survival and distribution and provides critical insights into phenotypic diversity. We outline how to use the ecomechanical paradigm using drag-induced bending in trees as an example. Our approach can be incorporated into existing research and help build interdisciplinary bridges. Finally, we identify key factors needed for mass data collection, analysis, and the dissemination of models relevant to this framework.

Evolutionary and morphological patterns underlying carnivoran body shape diversity.

The diversity of body shapes is one of the most prominent features of phenotypic variation in vertebrates. Biologists, however, still lack a full understanding of the underlying morphological components that contribute to its diversity, particularly in endothermic vertebrates such as mammals. In this study, hypotheses pertaining to the evolution of the cranial and axial components that contribute to the diversity of carnivoran body shapes were tested. Three trends were found in the evolution of carnivoran body shapes: (1) carnivorans exhibit diverse body shapes with intrafamilial variation predicted best by family clade age, (2) body shape is driven by strong allometric effects of body size where species become more elongate with decreasing size, and (3) the thoracic and lumbar regions and rib length contribute the most to body shape variation, albeit pathways differ between different families. These results reveal the morphological patterns that led to increased diversity in carnivoran body shapes and elucidate the similarities and dissimilarities that govern body shape diversity across vertebrates.

Sex-specific ontogenetic patterns of cranial morphology, theoretical bite force, and underlying jaw musculature in fishers and American martens.

The carnivoran cranium undergoes tremendous growth in size and development of shape to process prey as adults and, importantly, these ontogenetic processes can also differ between the sexes. How these ontogenetic changes in morphology actually relate to the underlying jaw musculature and overall bite performance has rarely been investigated. In this study, I examined sex-specific ontogenetic changes in cranial morphology, jaw adductor muscles, and theoretical bite force between subadults and adults in the fisher (Pekania pennanti) and American marten (Martes americana). I found evidence that cranial size alone does not completely explain ontogenetic increases in bite forces as found in other mammalian species. Instead, cranial shape development also drives ontogenetic increases in relative bite force by broadening the zygomatic arches and enlargement of the sagittal crest, both of which enable relatively larger jaw adductor muscles to attach. In contrast, examination of sexual dimorphism within each age-class revealed that cranial shape dimorphism did not translate to dimorphism in either size-corrected bite forces or size-corrected physiological cross-sectional area of the jaw adductor muscles. These results reveal that morphological size and shape variation can have different influences on bite performance depending on the level of intraspecific variation that is examined (i.e. ontogenetic versus sexual dimorphism).

Solitary meat-eaters: solitary, carnivorous carnivorans exhibit the highest degree of sexual size dimorphism.

Although sexual size dimorphism (SSD) is widespread across the animal tree of life, the underlying evolutionary processes that influence this phenomenon remains elusive and difficult to tease apart. In this study, I examined how social system (as a proxy for sexual selection) and diet (as a proxy for natural selection) influenced the evolution of SSD in terrestrial carnivorans (Carnivora; Mammalia). Using phylogenetic comparative methods, I found that are territorial solitary and carnivorous carnivorans exhibited selection towards increased degree of male-biased SSD compared to other carnivorans with alternative social systems and diets. I also found the absence of Rensch's rule across most carnivoran clades, suggestion a relaxation of the influences of sexual selection on SSD. These results together suggest that sexual selection and niche divergence together are important processes influencing the evolution of male-biased SSD in extant terrestrial carnivorans.

Dry versus wet and gross: Comparisons between the dry skull method and gross dissection in estimations of jaw muscle cross-sectional area and bite forces in sea otters.

Bite force is a measure of feeding performance used to elucidate links between animal morphology, ecology, and fitness. Obtaining live individuals for in vivo bite-force measurements or freshly deceased specimens for bite force modeling is challenging for many species. Thomason's dry skull method for mammals relies solely on osteological specimens and, therefore, presents an advantageous approach that enables researchers to estimate and compare bite forces across extant and even extinct species. However, how accurately the dry skull method estimates physiological cross-sectional area (PCSA) of the jaw adductor muscles and theoretical bite force has rarely been tested. Here, we use an ontogenetic series of southern sea otters (Enhydra lutris nereis) to test the hypothesis that skeletomuscular traits estimated from the dry skull method accurately predicts test traits derived from dissection-based biomechanical modeling. Although variables from these two methods exhibited strong positive relationships across ontogeny, we found that the dry skull method overestimates PCSA of the masseter and underestimates PCSA of the temporalis. Jaw adductor in-levers for both jaw muscles and overall bite force are overestimated. Surprisingly, we reveal that sexual dimorphism in craniomandibular shape affects temporalis PCSA estimations; the dry skull method predicted female temporalis PCSA well but underestimates male temporalis PCSA across ontogeny. These results highlight the importance of accounting for sexual dimorphism and other intraspecific variation when using the dry skull method. Together, we found the dry skull method provides an underestimation of bite force over ontogeny and that the underlying anatomical components driving bite force may be misrepresented.

Evolutionary shifts in extant mustelid (Mustelidae: Carnivora) cranial shape, body size and body shape coincide with the Mid-Miocene Climate Transition.

Environmental changes can lead to evolutionary shifts in phenotypic traits, which in turn facilitate the exploitation of novel adaptive landscapes and lineage diversification. The global cooling, increased aridity and expansion of open grasslands during the past 50 Myr are prime examples of new adaptive landscapes that spurred lineage and ecomorphological diversity of several mammalian lineages such as rodents and large herbivorous megafauna. However, whether these environmental changes facilitated evolutionary shifts in small- to mid-sized predator morphology is unknown. Here, I used a complete cranial and body morphological dataset to examine the timing of evolutionary shifts in cranial shape, body size and body shape within extant mustelids (martens, otters, polecats and weasels) during the climatic and environmental changes of the Cenozoic. I found that evolutionary shifts in all three traits occurred within extant mustelid subclades just after the onset of the Mid-Miocene Climate Transition. These mustelid subclades first shifted towards more elongate body plans followed by concurrent shifts towards smaller body sizes and more robust crania. I hypothesize that these cranial and body morphological shifts enabled mustelids to exploit novel adaptive zones associated with the climatic and environmental changes of the Mid to Late Miocene, which facilitated significant increases in clade carrying capacity.

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.

Effects of diet on cranial morphology and biting ability in musteloid mammals.

Size and shape are often considered important variables that lead to variation in performance. In studies of feeding, size-corrected metrics of the skull are often used as proxies of biting performance; however, few studies have examined the relationship between cranial shape in its entirety and estimated bite force across species and how dietary ecologies may affect these variables differently. Here, we used geometric morphometric and phylogenetic comparative approaches to examine relationships between cranial morphology and estimated bite force in the carnivoran clade Musteloidea. We found a strong relationship between cranial size and estimated bite force but did not find a significant relationship between cranial shape and size-corrected estimated bite force. Many-to-one mapping of form to function may explain this pattern because a variety of evolutionary shape changes rather than a single shape change may have contributed to an increase in relative biting ability. We also found that dietary ecologies influenced cranial shape evolution but did not influence cranial size nor size-corrected bite force evolution. Although musteloids with different diets exhibit variation in cranial shapes, they have similar estimated bite forces suggesting that other feeding performance metrics and potentially nonfeeding traits are also important contributors to cranial evolution. We postulate that axial and appendicular adaptations and the interesting feeding behaviours reported for species within this group also facilitate different dietary ecologies between species. Future work integrating cranial, axial and appendicular form and function with behavioural observations will reveal further insights into the evolution of dietary ecologies and other ecological variables.

Eat whole and less often: ontogenetic shift reveals size specialization on kelp bass by the California moray eel, Gymnothorax mordax.

Despite the importance of predation in many ecosystems, gaps remain in our understanding of nocturnal marine predators. Although the kelp forests of Southern California are some of the most well-studied ecosystems, California morays, Gymnothorax mordax, are predominately nocturnal predators that have remained largely unstudied and their predatory effects on the kelp forest ecosystem are unknown. We use a multi-year data set to examine the dietary breadth of G. mordax and to determine the functional role of this predator. We also quantify bite force to examine the potential performance limitations of morays in exploiting prey. Stomach content analyses and linear selectivity index values indicate that G. mordax specializes on kelp bass, Paralabrax clathratus. Average size of kelp bass consumed varies across years, suggesting that morays respond to fluctuations in prey size availability. The scaling relationship of kelp bass standard length and moray head length reveals an ontogenetic shift, where maximum prey size increases with moray size and small prey are dropped from the diet of larger individuals. Moray bite force exhibited strong positive allometry with moray head size, suggesting that larger morays exhibit greater bite forces for their head and body size. However, we found no relationship between prey size and bite force, suggesting that a disproportional increase in bite force does not facilitate the consumption of disproportionately larger prey. Our results indicate that while G. mordax of Catalina Island is a dietary specialist, it is capable of exhibiting functional shifts in prey size and species based on their abundance.

Carnivory maintains cranial dimorphism between males and females: Evidence for niche divergence in extant Musteloidea.

The evolution and maintenance of sexual dimorphism has long been attributed to sexual selection. Niche divergence, however, serves as an alternative but rarely tested selective pressure also hypothesized to drive phenotypic disparity between males and females. We reconstructed ancestral social systems and diet and used Ornstein-Uhlenbeck (OU) modeling approaches to test whether niche divergence is stronger than sexual selection in driving the evolution of sexual dimorphism in cranial size and bite force across extant Musteloidea. We found that multipeak OU models favored different dietary regimes over social behavior and that the greatest degree of cranial size and bite force dimorphism were found in terrestrial carnivores. Because competition for terrestrial vertebrate prey is greater than other dietary groups, increased cranial size and bite force dimorphism reduces dietary competition between the sexes. In contrast, neither dietary regime nor social system influenced the evolution of sexual dimorphism in cranial shape. Furthermore, we found that the evolution of sexual dimorphism in bite force is influenced by the evolution of sexual dimorphism in cranial size rather than cranial shape. Overall, our results highlight niche divergence as an important mechanism that maintains the evolution of sexual dimorphism in musteloids.

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.

Ontogenetic Scaling of Theoretical Bite Force in Southern Sea Otters (Enhydra lutris nereis).

Sexual dimorphism attributed to niche divergence is often linked to differentiation between the sexes in both dietary resources and characters related to feeding and resource procurement. Although recent studies have indicated that southern sea otters (Enhydra lutris nereis) exhibit differences in dietary preferences as well as sexual dimorphism in skull size and shape, whether these intersexual differences translate to differentiation in feeding performances between the sexes remains to be investigated. To test the hypothesis that scaling patterns of bite force, a metric of feeding performance, differ between the sexes, we calculated theoretical bite forces for 55 naturally deceased male and female southern sea otters spanning the size ranges encountered over ontogeny. We then used standardized major axis regressions to simultaneously determine the scaling patterns of theoretical bite forces and skull components across ontogeny and assess whether these scaling patterns differed between the sexes. We found that positive allometric increases in theoretical bite force resulted from positive allometric increases in physiological cross-sectional area for the major jaw adductor muscle and mechanical advantage. Closer examination revealed that allometric increases in temporalis muscle mass and relative allometric decreases in out-lever lengths are driving these patterns. In our analysis of sexual dimorphism, we found that scaling patterns of theoretical bite force and morphological traits do not differ between the sexes. However, adult sea otters differed in their absolute bite forces, revealing that adult males exhibited greater bite forces as a result of their larger sizes. We found intersexual differences in biting ability that provide some support for the niche divergence hypothesis. Continued work in this field may link intersexual differences in feeding functional morphology with foraging ecology to show how niche divergence has the potential to reinforce sexual dimorphism in southern sea otters.

Cleaners among wrasses: Phylogenetics and evolutionary patterns of cleaning behavior within Labridae.

Cleaner fishes remove and consume ectoparasites and are often categorized by whether they perform this behavior: (1) predominately as juveniles, (2) facultatively throughout ontogeny, or (3) obligately. Through a literature search, we confirmed that with at least 58 species exhibiting cleaning behavior, the Labridae (wrasses, parrotfishes, and allies) contain the highest diversity of cleaner fishes. In fact, there are 3-4 times as many cleaners within labrids as there are in any other marine group. The distribution and underlying causes of this exceptional diversity have not been determined. Here, we assess the topological and temporal patterns of labrid cleaner evolution. We used maximum likelihood and Bayesian approaches to infer the phylogenetic relationships and divergence times between 320 labrid species (50.7% of nominal species). We then employed stochastic character mapping to infer how and when cleaning behavior evolved. We estimate that cleaning has independently evolved 26-30 times in the Labridae, and all such events likely occurred no earlier than in the late Miocene. Given the current sampling and pattern of transitions, we hypothesize that the majority of facultative or obligate cleaning may have evolved through heterochrony.