The influence of the land-to-sea macroevolutionary transition on vertebral column disparification in Pinnipedia.

The repeated returns of vertebrates to the marine ecosystems since the Triassic serve as an evolutionary model to understand macroevolutionary change. Here we investigate the effects of the land-to-sea transition on disparity and constraint of the vertebral column in aquatic carnivorans (Carnivora; Pinnipedia) to assess how their functional diversity and evolutionary innovations influenced major radiations of crown pinnipeds. We use three-dimensional geometric morphometrics and multivariate analysis for high-dimensional data under a phylogenetic framework to quantify vertebral size and shape in living and extinct pinnipeds. Our analysis demonstrates an important shift in vertebral column evolution by 10-12 million years ago, from an unconstrained to a constrained evolutionary scenario, a point of time that coincides with the major radiation of crown pinnipeds. Moreover, we also demonstrate that the axial skeleton of phocids and otariids followed a different path of morphological evolution that was probably driven by their specialized locomotor strategies. Despite this, we found a significant effect of habitat preference (coastal versus pelagic) on vertebral morphology of crown taxa regardless of the family they belong. In summary, our analysis provides insights into how the land-to-sea transition influenced the complex evolutionary history of pinniped vertebral morphology.

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.

Intravertebral vs. intervertebral integration and modularity in the vertebral column of mammalian carnivorans.

The vertebral column is a multicomponent structure whose organization results from developmental and functional demands. According to their distinct somitic origins, individual vertebrae exhibit intravertebral modularity between the centrum and neural spine. However, vertebrae are also organized into larger units called intervertebral modules that result from integration between adjacent vertebrae due to locomotory demands or from common developmental origins due to resegmentation. A previous hypothesis suggested that the boundaries of intervertebral modules coincide with changes in the patterns of intravertebral integration. Here, we explicitly test whether the patterns of modularity and integration between the centrum and neural spine (i.e., intravertebral) in the boundary vertebrae among previously defined intervertebral modules change with respect to those in the vertebrae within intervertebral modules. We quantified intravertebral modularity patterns and quantified the strength of intravertebral integration for each vertebra of the presacral region in 41 species of carnivoran mammals using 3D geometric morphometrics. Our results demonstrate a significant intravertebral modular signal between the centrum and neural spine in all post-cervical vertebrae, including the boundary vertebrae among intervertebral modules. However, the strength of intravertebral integration decreases at the boundary vertebrae. We also found a significant correlation between the degree of intravertebral integration and intervertebral integration. Following our results, we hypothesize that natural selection does not override the integration between the centrum and neural spine at the boundary vertebrae, a pattern that should be influenced by their distinct somitic origins and separate ossification centers during early development. However, natural selection has probably influenced (albeit indirectly) the integration between the centrum and neural spine in the vertebrae that compose the intervertebral modules.

Elbow-joint morphology in the North American 'cheetah-like' cat Miracinonyx trumani.

The North American cheetah-like cat Miracinonyx trumani is an extinct species that roamed the Pleistocene prairies 13 000 years ago. Although M. trumani is more closely related to the cougar (Puma concolor) than to the living cheetah (Acinonyx jubatus), it is believed that both A. jubatus and M. trumani possess a highly specialized skeleton for fast-running, including limbs adapted for speed at the expense of restricting the ability of prey grappling. However, forelimb dexterity of M. trumani has not been yet investigated. Here, we quantify the 3D-shape of the humerus distal epiphysis as a proxy for elbow-joint morphology in a sample of living cats to determine whether the extinct M. trumani was specialized to kill open-country prey using predatory behaviour based on fast running across the prairies and steppe terrains of the North American Pleistocene. We show that M. trumani had an elbow morphology intermediate to that of P. concolor and A. jubatus, suggesting that M. trumani had a less specialized pursuit predatory behaviour than A. jubatus. We propose that M. trumani probably deployed a unique predatory behaviour without modern analogues. Our results bring into question the degree of ecomorphological convergence between M. trumani and its Old World vicar A. jubatus.

Body-axis organization in tetrapods: a model-system to disentangle the developmental origins of convergent evolution in deep time.

Convergent evolution is a central concept in evolutionary theory but the underlying mechanism has been largely debated since On the Origin of Species. Previous hypotheses predict that developmental constraints make some morphologies more likely to arise than others and natural selection discards those of the lowest fitness. However, the quantification of the role and strength of natural selection and developmental constraint in shaping convergent phenotypes on macroevolutionary timescales is challenging because the information regarding performance and development is not directly available. Accordingly, current knowledge of how embryonic development and natural selection drive phenotypic evolution in vertebrates has been extended from studies performed at short temporal scales. We propose here the organization of the tetrapod body-axis as a model system to investigate the developmental origins of convergent evolution over hundreds of millions of years. The quantification of the primary developmental mechanisms driving body-axis organization (i.e. somitogenesis, homeotic effects and differential growth) can be inferred from vertebral counts, and recent techniques of three-dimensional computational biomechanics have the necessary potential to reveal organismal performance even in fossil forms. The combination of both approaches offers a novel and robust methodological framework to test competing hypotheses on the functional and developmental drivers of phenotypic evolution and evolutionary convergence.

Sixty-six million years along the road of mammalian ecomorphological specialization.

The fossil record of the large terrestrial mammals of the North American Cenozoic has previously been quantitatively summarized in six sequential episodes of faunal associations-"evolutionary faunas"-that correspond well with previously proposed qualitative "Chronofaunas." Here, we investigate the ecological spectrum of these faunas by classifying their major taxonomic components into discrete ecomorphological categories of diet, locomotion, and body size. To specifically address the potential influence of long-term climatic shifts on the ecomorphological composition of these faunas, we analyze via contingency tables and detrended correspondence analyses the frequency distribution of ecomorph types within faunas. We show that each evolutionary fauna has a unique, nonrandom association of ecomorphs, and we identify a long-term trend toward greater ecomorphological specialization over successive faunas during the past 66 My. Major vegetation shifts induced by climatic changes appear to underlie the ecomorphological dynamics of these six temporal associations that summarize Cenozoic North American mammalian evolutionary history.

Morphological convergence obscures functional diversity in sabre-toothed carnivores.

The acquisition of elongated, sabre-like canines in multiple vertebrate clades during the last 265 Myr represents a remarkable example for convergent evolution. Due to striking superficial similarities in the cranial skeleton, the same or similar skull and jaw functions have been inferred for sabre-toothed species and interpreted as an adaptation to subdue large-bodied prey. However, although some sabre-tooth lineages have been classified into different ecomorphs (dirk-tooths and scimitar-tooths) the functional diversity within and between groups and the evolutionary paths leading to these specializations are unknown. Here, we use a suite of biomechanical simulations to analyse key functional parameters (mandibular gape angle, bending strength, bite force) to compare the functional performance of different groups and to quantify evolutionary rates across sabre-tooth vertebrates. Our results demonstrate a remarkably high functional diversity between sabre-tooth lineages and that different cranial function and prey killing strategies evolved within clades. Moreover, different biomechanical adaptations in coexisting sabre-tooth species further suggest that this functional diversity was at least partially driven by niche partitioning.

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.

Three-dimensional dental topography and feeding ecology in the extinct cave bear.

The cave bear (Ursus spelaeus s.l.) was an iconic extinct bear that inhabited the Pleistocene of Eurasia. The cause of extinction of this species is unclear and to identify the actual factors, it is crucial to understand its feeding preferences. Here, we quantified the shape descriptor metrics in three-dimensional (3D) models of the upper teeth (P4-M2) of the cave bear to make inferences about its controversial feeding behaviour. We used comparative samples, including representatives of all living bear species with known diets, as a template. Our topographic analyses show that the complexity of upper tooth rows in living bears is more clearly associated with the mechanical properties of the items consumed than with the type of food. Cave bears exhibit intermediate values on topographic metrics compared with the bamboo-feeder giant panda (Ailuropoda melanoleuca) and specialists in hard mast consumption (Ursus arctos and Ursus thibetanus). The crown topography of cave bear upper teeth suggests that they could chew on tough vegetal resources of low quality with high efficiency, a characteristic that no living bear currently displays. Our results align with a climate-driven hypothesis to explain the extinction of cave bear populations during the Late Pleistocene.

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.

Phenotypic integration and modularity drives skull shape divergence in the Arctic fox (Vulpes lagopus) from the Commander Islands.

Phenotypic integration and modularity influence morphological disparity and evolvability. However, studies addressing how morphological integration and modularity change for long periods of genetic isolation are scarce. Here, we investigate patterns of phenotypic integration and modularity in the skull of phenotypically and genetically distinct populations of the Artic fox (Vulpes lagopus) from the Commander Islands of the Aleutian belt (i.e. Bering and Mednyi) that were isolated ca 10 000 years by ice-free waters of the Bering sea. We use three-dimensional geometric morphometrics to quantify the strength of modularity and integration from inter-individual variation (static) and from fluctuating asymmetry (random developmental variation) in both island populations compared to the mainland population (i.e. Chukotka) and we investigated how changes in morphological integration and modularity affect disparity and the directionality of trait divergence. Our results indicate a decrease in morphological integration concomitant to an increase in disparity at a developmental level, from mainland to the smallest and farthest population of Mednyi. However, phenotypic integration is higher in both island populations accompanied by a reduction in disparity compared to the population of mainland at a static level. This higher integration may have favoured morphological adaptive changes towards specific feeding behaviours related to the extreme environmental settings of islands. Our study demonstrates how shifts in phenotypic integration and modularity can facilitate phenotypic evolvability at the intraspecific level that may lead to lineage divergence at macroevolutioanry scales.

Non-decoupled morphological evolution of the fore- and hindlimb of sabretooth predators.

Specialized organisms are useful for exploring the combined effects of selection of functional traits and developmental constraints on patterns of phenotypic integration. Sabretooth predators are one of the most interesting examples of specialization among mammals. Their hypertrophied, sabre-shaped upper canines and their powerfully built forelimbs have been interpreted as adaptations to a highly specialized predatory behaviour. Given that the elongated and laterally compressed canines of sabretooths were more vulnerable to fracture than the shorter canines of conical-tooth cats, it has been long hypothesized that the heavily muscled forelimbs of sabretooths were used for immobilizing prey before developing a quick and precise killing bite. However, the effect of this unique adaptation on the covariation between the fore- and the hindlimb has not been explored in a quantitative fashion. In this paper, we investigate if the specialization of sabretooth predators decoupled the morphological variation of their forelimb with respect to their hindlimb or, in contrast, both limbs vary in the same fashion as in conical-tooth cats, which do not show such extreme adaptations in their forelimb. We use 3D geometric morphometrics and different morphological indices to compare the fore- and hindlimb of conical- and sabretooth predators. Our results indicate that the limb bones of sabretooth predators covary following the same trend of conical-tooth cats. Therefore, we show that the predatory specialization of sabretooth predators did not result in a decoupling of the morphological evolution of their fore- and hindlimbs. The role of developmental constraints and natural selection on this coordinate variation between the fore- and the hindlimb is discussed in the light of this new evidence.

Cenozoic climate change influences mammalian evolutionary dynamics.

Global climate change is having profound impacts on the natural world. However, climate influence on faunal dynamics at macroevolutionary scales remains poorly understood. In this paper we investigate the influence of climate over deep time on the diversity patterns of Cenozoic North American mammals. We use factor analysis to identify temporally correlated assemblages of taxa, or major evolutionary faunas that we can then study in relation to climatic change over the past 65 million years. These taxa can be grouped into six consecutive faunal associations that show some correspondence with the qualitative mammalian chronofaunas of previous workers. We also show that the diversity pattern of most of these chronofaunas can be correlated with the stacked deep-sea benthic foraminiferal oxygen isotope (δ(18)O) curve, which strongly suggests climatic forcing of faunal dynamics over a large macroevolutionary timescale. This study demonstrates the profound influence of climate on the diversity patterns of North American terrestrial mammals over the Cenozoic.

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.

Three-dimensional computer simulations of feeding behaviour in red and giant pandas relate skull biomechanics with dietary niche partitioning.

The red (Ailurus fulgens) and giant (Ailuropoda melanoleuca) pandas are mammalian carnivores convergently adapted to a bamboo feeding diet. However, whereas Ailurus forages almost entirely on younger leaves, fruits and tender trunks, Ailuropoda relies more on trunks and stems. Such difference in foraging mode is considered a strategy for resource partitioning where they are sympatric. Here, we use finite-element analysis to test for mechanical differences and similarities in skull performance between Ailurus and Ailuropoda related to diet. Feeding simulations suggest that the two panda species have similar ranges of mechanical efficiency and strain energy profiles across the dentition, reflecting their durophagous diet. However, the stress distributions and peaks in the skulls of Ailurus and Ailuropoda are remarkably different for biting at all tooth locations. Although the skull of Ailuropoda is capable of resisting higher stresses than the skull of Ailurus, the latter is able to distribute stresses more evenly throughout the skull. These differences in skull biomechanics reflect their distinct bamboo feeding preferences. Ailurus uses repetitive chewing in an extended mastication to feed on soft leaves, and Ailuropoda exhibits shorter and more discrete periods of chomp-and-swallow feeding to break down hard bamboo trunks.

Evolution: Bridging the sabertooth gap(e).

Saber-toothed felids are models of how extreme biomechanical specialization can evolve. A new study reveals a continuous morphological spectrum between sabertooths and modern cats, with specialization acting as a macroevolutionary ratchet.

Comparing cranial biomechanics between Barbourofelis fricki and Smilodon fatalis: Is there a universal killing-bite among saber-toothed predators?

Saber-tooths, extinct apex predators with long and blade-like upper canines, have appeared iteratively at least five times in the evolutionary history of vertebrates. Although saber-tooths exhibit a relatively diverse range of morphologies, it is widely accepted that all killed their prey using the same predatory behavior. In this study, we CT-scanned the skull of Barbourofelis fricki and compared its cranial mechanics using finite element analysis (FEA) with that of Smilodon fatalis. Our aim was to investigate potential variations in killing behavior between two dirk-toothed sabretooths from the Miocene and Pleistocene of North America. The study revealed that B. fricki had a stoutly-built skull capable of withstanding stress in various prey-killing scenarios, while the skull of S. fatalis appeared less optimized for supporting stress, which highlights the highly derived saber-tooth morphology of the former. The results may indicate that B. fricki was more of a generalist in prey-killing compared to S. fatalis, which experiences lower stresses under stabbing loads. We hypothesize that morphological specialization in saber-tooths does not necessarily indicate ecological specialization. Our results support the notion that morphological convergence among saber-toothed cats may obscure differences in hunting strategies employed to dispatch their prey. Our findings challenge the assumption of the universally assumed canine-shear biting as the prey-killing behavior of all saber-toothed cats. However, further research involving a wider range of dirk and scimitar-toothed forms could provide additional insights into the diversity of cranial biomechanics within this fascinating group of extinct mammalian predators.

The impact of the land-to-sea transition on evolutionary integration and modularity of the pinniped backbone.

In this study, we investigate how the terrestrial-aquatic transition influenced patterns of axial integration and modularity in response to the secondary adaptation to a marine lifestyle. We use 3D geometric morphometrics to quantify shape covariation among presacral vertebrae in pinnipeds (Carnivora; Pinnipedia) and to compare with patterns of axial integration and modularity in their close terrestrial relatives. Our results indicate that the vertebral column of pinnipeds has experienced a decrease in the strength of integration among all presacral vertebrae when compared to terrestrial carnivores (=fissipeds). However, separate integration analyses among the speciose Otariidae (i.e., sea lions and fur seals) and Phocidae (i.e., true seals) also suggests the presence of different axial organizations in these two groups of crown pinnipeds. While phocids present a set of integrated "thoracic" vertebrae, the presacral vertebrae of otariids are characterized by the absence of any set of vertebrae with high integration. We hypothesize that these differences could be linked to their specific modes of aquatic locomotion -i.e., pelvic vs pectoral oscillation. Our results provide evidence that the vertebral column of pinnipeds has been reorganized from the pattern observed in fissipeds but is more complex than a simple "homogenization" of the modular pattern of their close terrestrial relatives.

The earliest Ethiopian wolf: implications for the species evolution and its future survival.

In 2017, a hemimandible (MW5-B208), corresponding to the Ethiopian wolf (Canis simensis), was found in a stratigraphically-controlled and radio-isotopically-dated sequence of the Melka Wakena paleoanthropological site-complex, on the Southeastern Ethiopian Highlands, ~ 2300 m above sea level. The specimen is the first and unique Pleistocene fossil of this species. Our data provide an unambiguous minimum age of 1.6-1.4 Ma for the species' presence in Africa and constitutes the first empirical evidence that supports molecular interpretations. Currently, C. simensis is one of the most endangered carnivore species of Africa. Bioclimate niche modeling applied to the time frame indicated by the fossil suggests that the lineage of the Ethiopian wolf faced severe survival challenges in the past, with consecutive drastic geographic range contractions during warmer periods. These models help to describe future scenarios for the survival of the species. Projections ranging from most pessimistic to most optimistic future climatic scenarios indicate significant reduction of the already-deteriorating territories suitable for the Ethiopian Wolf, increasing the threat to the specie's future survival. Additionally, the recovery of the Melka Wakena fossil underscores the importance of work outside the East African Rift System in research of early human origins and associated biodiversity on the African continent.

The brain of the North American cheetah-like cat Miracinonyx trumani.

The cheetah Acinonyx jubatus, the fastest living land mammal, is an atypical member of the family Felidae. The extinct feline Miracinonyx trumani, known as the North American cheetah, is thought to have convergently evolved with Acinonyx to pursue fast and open-country prey across prairies and steppe environments of the North American Pleistocene. The brain of Acinonyx is unique among the living felids, but it is unknown whether the brain of the extinct M. trumani is convergent to that of Acinonyx. Here, we investigate the brain of M. trumani from a cranium endocast, using a comparative sample of other big cats. We demonstrate that the brain of M. trumani was different from that of the living A. jubatus. Indeed, its brain shows a unique combination of traits among living cats. This suggests that the case of extreme convergence between Miracinonyx and its living Old World vicar should be reconsidered.