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 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.

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.

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.

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.

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.

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.

Déjà vu: a reappraisal of the taphonomy of quarry VM4 of the Early Pleistocene site of Venta Micena (Baza Basin, SE Spain).

Venta Micena, an Early Pleistocene site of the Baza Basin (SE Spain), preserves a rich and diverse assemblage of large mammals. VM3, the main excavation quarry of the site, has been interpreted as a den of the giant hyaena Pachycrocuta brevirostris in the plain that surrounded the Baza palaeolake. Taphonomic analysis of VM3 has shown that the hyaenas scavenged the prey previously hunted by the hypercarnivores, transported their remains to the communal den, and consumed the skeletal parts according to their marrow contents and mineral density. In a recent paper (Luzón et al. in Sci Rep 11:13977, https://doi.org/10.1038/s41598-021-93261-1 , 2021), a small sample of remains unearthed from VM4, an excavation quarry ~ 350 m distant from VM3, is analysed. The authors indicate several differences in the taphonomic features of this assemblage with VM3, and even suggest that a different carnivore could have been the agent involved in the bone accumulation process. Here, we make a comparative analysis of both quarries and analyse more skeletal remains from VM4. Our results indicate that the assemblages are broadly similar in composition, except for slight differences in the frequency of megaherbivores, carnivores and equids according to NISP values (but not to MNI counts), the degree of bone weathering, and the intensity of bone processing by the hyaenas. Given that VM4 and VM3 were not coeval denning areas of P. brevirostris, these differences suggest that during the years when the skeletal remains were accumulated by the hyaenas at VM3, the rise of the water table of the Baza palaeolake that capped with limestone the bones was delayed compared to VM4, which resulted in their more in-depth consumption by the hyaenas.

Serial disparity in the carnivoran backbone unveils a complex adaptive role in metameric evolution.

Organisms comprise multiple interacting parts, but few quantitative studies have analysed multi-element systems, limiting understanding of phenotypic evolution. We investigate how disparity of vertebral morphology varies along the axial column of mammalian carnivores - a chain of 27 subunits - and the extent to which morphological variation have been structured by evolutionary constraints and locomotory adaptation. We find that lumbars and posterior thoracics exhibit high individual disparity but low serial differentiation. They are pervasively recruited into locomotory functions and exhibit relaxed evolutionary constraint. More anterior vertebrae also show signals of locomotory adaptation, but nevertheless have low individual disparity and constrained patterns of evolution, characterised by low-dimensional shape changes. Our findings demonstrate the importance of the thoracolumbar region as an innovation enabling evolutionary versatility of mammalian locomotion. Moreover, they underscore the complexity of phenotypic macroevolution of multi-element systems and that the strength of ecomorphological signal does not have a predictable influence on macroevolutionary outcomes.

Phenotypic integration in the carnivoran backbone and the evolution of functional differentiation in metameric structures.

Explaining the origin and evolution of a vertebral column with anatomically distinct regions that characterizes the tetrapod body plan provides understanding of how metameric structures become repeated and how they acquire the ability to perform different functions. However, despite many decades of inquiry, the advantages and costs of vertebral column regionalization in anatomically distinct blocks, their functional specialization, and how they channel new evolutionary outcomes are poorly understood. Here, we investigate morphological integration (and how this integration is structured [modularity]) between all the presacral vertebrae of mammalian carnivorans to provide a better understanding of how regionalization in metameric structures evolves. Our results demonstrate that the subunits of the presacral column are highly integrated. However, underlying to this general pattern, three sets of vertebrae are recognized as presacral modules-the cervical module, the anterodorsal module, and the posterodorsal module-as well as one weakly integrated vertebra (diaphragmatic) that forms a transition between both dorsal modules. We hypothesize that the strength of integration organizing the axial system into modules may be associated with motion capability. The highly integrated anterior dorsal module coincides with a region with motion constraints to avoid compromising ventilation, whereas for the posterior dorsal region motion constraints avoid exceeding extension of the posterior back. On the other hand, the weakly integrated diaphragmatic vertebra belongs to the "Diaphragmatic joint complex"-a key region of the mammalian column of exceedingly permissive motion. Our results also demonstrate that these modules do not match with the traditional morphological regions, and we propose natural selection as the main factor shaping this pattern to stabilize some regions and to allow coordinate movements in others.

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.

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.

An eye for a tooth: Thylacosmilus was not a marsupial "saber-tooth predator".

BACKGROUND: Saber-toothed mammals, now all extinct, were cats or "cat-like" forms with enlarged, blade-like upper canines, proposed as specialists in taking large prey. During the last 66 Ma, the saber-tooth ecomorph has evolved convergently at least in five different mammalian lineages across both marsupials and placentals. Indeed, Thylacosmilus atrox, the so-called "marsupial saber-tooth," is often considered as a classic example of convergence with placental saber-tooth cats such as Smilodon fatalis. However, despite its superficial similarity to saber-toothed placentals, T. atrox lacks many of the critical anatomical features related to their inferred predatory behavior-that of employing their enlarged canines in a killing head strike. METHODS: Here we follow a multi-proxy approach using canonical correspondence analysis of discrete traits, biomechanical models of skull function using Finite Element Analysis, and 3D dental microwear texture analysis of upper and lower postcanine teeth, to investigate the degree of evolutionary convergence between T. atrox and placental saber-tooths, including S. fatalis. RESULTS: Correspondence analysis shows that the craniodental features of T. atrox are divergent from those of placental saber-tooths. Biomechanical analyses indicate a superior ability of T. atrox to placental saber-tooths in pulling back with the canines, with the unique lateral ridge of the canines adding strength to this function. The dental microwear of T. atrox indicates a soft diet, resembling that of the meat-specializing cheetah, but its blunted gross dental wear is not indicative of shearing meat. CONCLUSIONS: Our results indicate that despite its impressive canines, the "marsupial saber-tooth" was not the ecological analogue of placental saber-tooths, and likely did not use its canines to dispatch its prey. This oft-cited example of convergence requires reconsideration, and T. atrox may have had a unique type of ecology among mammals.

Biomechanical simulations reveal a trade-off between adaptation to glacial climate and dietary niche versatility in European cave bears.

The cave bear is one of the best known extinct large mammals that inhabited Europe during the "Ice Age," becoming extinct ≈24,000 years ago along with other members of the Pleistocene megafauna. Long-standing hypotheses speculate that many cave bears died during their long hibernation periods, which were necessary to overcome the severe and prolonged winters of the Last Glacial. Here, we investigate how long hibernation periods in cave bears would have directly affected their feeding biomechanics using CT-based biomechanical simulations of skulls of cave and extant bears. Our results demonstrate that although large paranasal sinuses were necessary for, and consistent with, long hibernation periods, trade-offs in sinus-associated cranial biomechanical traits restricted cave bears to feed exclusively on low energetic vegetal resources during the predormancy period. This biomechanical trade-off constitutes a new key factor to mechanistically explain the demise of this dominant Pleistocene megafaunal species as a direct consequence of climate cooling.

The bears from Dmanisi and the first dispersal of early Homo out of Africa.

We report on the taxonomy and paleodiet of the bear population that inhabited the emblematic palaeoanthropological Early Pleistocene (1.8 Ma) site of Dmanisi (Georgia), based on a dual approach combining morphometrics and microwear of upper and lower teeth. Given that the teeth of Ursus etruscus Cuvier, 1823 from Dmanisi show considerable size variability, their systematic position has been debated. However, a comparative study of the coefficients of variation for tooth size measurements in several modern bear species shows that the variability in tooth size of the ursid population from Dmanisi could result from sexual dimorphism. The analysis of tooth microwear indicates that these bears inhabited a mixed environment of open plain with forest patches, where they had a browsing diet with a substantial contribution of meat and/or fish. Comparative tooth morphometric analyses of modern ursids and fossil U. etruscus indicate that this extinct species had an omnivorous behavior similar to that of extant brown bears. The ecological interactions of the Dmanisi bears with other members of the large mammals community, including the first hominins that dispersed out of Africa, are discussed in the 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.