Unexpectedly uneven distribution of functional trade-offs explains cranial morphological diversity in carnivores.

Functional trade-offs can affect patterns of morphological and ecological evolution as well as the magnitude of morphological changes through evolutionary time. Using morpho-functional landscape modelling on the cranium of 132 carnivore species, we focused on the macroevolutionary effects of the trade-off between bite force and bite velocity. Here, we show that rates of evolution in form (morphology) are decoupled from rates of evolution in function. Further, we found theoretical morphologies optimising for velocity to be more diverse, while a much smaller phenotypic space was occupied by shapes optimising force. This pattern of differential representation of different functions in theoretical morphological space was highly correlated with patterns of actual morphological disparity. We hypothesise that many-to-one mapping of cranium shape on function may prevent the detection of direct relationships between form and function. As comparatively only few morphologies optimise bite force, species optimising this function may be less abundant because they are less likely to evolve. This, in turn, may explain why certain clades are less variable than others. Given the ubiquity of functional trade-offs in biological systems, these patterns may be general and may help to explain the unevenness of morphological and functional diversity across the tree of life.

Homo sapiens and Neanderthals share high cerebral cortex integration into adulthood.

There is controversy around the mechanisms that guided the change in brain shape during the evolution of modern humans. It has long been held that different cortical areas evolved independently from each other to develop their unique functional specializations. However, some recent studies suggest that high integration between different cortical areas could facilitate the emergence of equally extreme, highly specialized brain functions. Here, we analyse the evolution of brain shape in primates using three-dimensional geometric morphometrics of endocasts. We aim to determine, firstly, whether modern humans present unique developmental patterns of covariation between brain cortical areas; and secondly, whether hominins experienced unusually high rates of evolution in brain covariation as compared to other primates. On the basis of analyses including modern humans and other extant great apes at different developmental stages, we first demonstrate that, unlike our closest living relatives, Homo sapiens retain high levels of covariation between cortical areas into adulthood. Among the other great apes, high levels of covariation are only found in immature individuals. Secondly, at the macro-evolutionary level, our analysis of 400 endocasts, representing 148 extant primate species and 6 fossil hominins, shows that strong covariation between different areas of the brain in H. sapiens and Homo neanderthalensis evolved under distinctly higher evolutionary rates than in any other primate, suggesting that natural selection favoured a greatly integrated brain in both species. These results hold when extinct species are excluded and allometric effects are accounted for. Our findings demonstrate that high covariation in the brain may have played a critical role in the evolution of unique cognitive capacities and complex behaviours in both modern humans and Neanderthals.

Trapped in the morphospace: The relationship between morphological integration and functional performance.

The evolution of complex morphological structures can be characterized by the interplay between different anatomical regions evolving under functional integration in response to shared selective pressures. Using the highly derived humeral morphology of talpid moles as a model, here we test whether functional performance is linked to increased levels of evolutionary integration between humerus subunits and, if so, what the strength is of the relationship. Combining two-dimensional geometric morphometrics, phylogenetic comparative methods, and functional landscape modeling, we demonstrate that the high biomechanical performance of subterranean moles' humeri is coupled with elevated levels of integration, whereas taxa with low-performance values show intermediate or low integration. Theoretical morphs occurring in high-performance areas of the functional landscape are not occupied by any species, and show a marked drop in covariation levels, suggesting the existence of a strong relationship between integration and performance in the evolution of talpid moles' humeri. We argue that the relative temporal invariance of the subterranean environment may have contributed to stabilize humeral morphology, trapping subterranean moles in a narrow region of the landscape and impeding any attempt to reposition on a new ascending slope.

Skull shape of a widely distributed, endangered marsupial reveals little evidence of local adaptation between fragmented populations.

The biogeographic distribution of diversity among populations of threatened mammalian species is generally investigated using population genetics. However, intraspecific phenotypic diversity is rarely assessed beyond taxonomy-focused linear measurements or qualitative descriptions. Here, we use a technique widely used in the evolutionary sciences-geometric morphometrics-to characterize shape diversity in the skull of an endangered marsupial, the northern quoll, across its 5,000 km distribution range along Northern Australia. Skull shape is a proxy for feeding, behavior, and phenotypic differentiation, allowing us to ask whether populations can be distinguished and whether patterns of variation indicate adaptability to changing environmental conditions. We analyzed skull shape in 101 individuals across four mainland populations and several islands. We assessed the contribution of population, size, sex, rainfall, temperature, and geography to skull shape variation using principal component analysis, Procrustes ANOVA, and variation partitioning analyses. The populations harbor similar amounts of broadly overlapping skull shape variation, with relatively low geographic effects. Size predicted skull shape best, coinciding with braincase size variation and differences in zygomatic arches. Size-adjusted differences in populations explained less variation with far smaller effect sizes, relating to changes in the insertion areas of masticatory muscles, as well as the upper muzzle and incisor region. Climatic and geographic variables contributed little. Strikingly, the vast majority of shape variation-76%-remained unexplained. Our results suggest a uniform intraspecific scope for shape variation, possibly due to allometric constraints or phenotypic plasticity beyond the relatively strong allometric effect. The lack of local adaptation indicates that cross-breeding between populations will not reduce local morphological skull (and probably general musculoskeletal) adaptation because none exists. However, the potential for heritable morphological variation (e.g., specialization to local diets) seems exceedingly limited. We conclude that 3D geometric morphometrics can provide a comprehensive, statistically rigorous phenomic contribution to genetic-based conservation studies.

Head to head: the case for fighting behaviour in Megaloceros giganteus using finite-element analysis.

The largest antlers of any known deer species belonged to the extinct giant deer Megaloceros giganteus. It has been argued that their antlers were too large for use in fighting, instead being used only in ritualized displays to attract mates. Here, we used finite-element analysis to test whether the antlers of M. giganteus could have withstood forces generated during fighting. We compared the mechanical performance of antlers in M. giganteus with three extant deer species: red deer (Cervus elaphus), fallow deer (Dama dama) and elk (Alces alces). Von Mises stress results suggest that M. giganteus was capable of withstanding some fighting loads, provided that their antlers interlocked proximally, and that their antlers were best adapted for withstanding loads from twisting rather than pushing actions, as are other deer with palmate antlers. We conclude that fighting in M. giganteus was probably more constrained and predictable than in extant deer.

Impact of transition to a subterranean lifestyle on morphological disparity and integration in talpid moles (Mammalia, Talpidae).

BACKGROUND: Understanding the mechanisms promoting or constraining morphological diversification within clades is a central topic in evolutionary biology. Ecological transitions are of particular interest because of their influence upon the selective forces and factors involved in phenotypic evolution. Here we focused on the humerus and mandibles of talpid moles to test whether the transition to the subterranean lifestyle impacted morphological disparity and phenotypic traits covariation between these two structures. RESULTS: Our results indicate non-subterranean species occupy a significantly larger portion of the talpid moles morphospace. However, there is no difference between subterranean and non-subterranean moles in terms of the strength and direction of phenotypic integration. CONCLUSIONS: Our study shows that the transition to a subterranean lifestyle significantly reduced morphological variability in talpid moles. However, this reduced disparity was not accompanied by changes in the pattern of traits covariation between the humerus and the mandible, suggesting the presence of strong phylogenetic conservatism within this pattern.

Evolution of the vomer and its implications for cranial kinesis in Paraves.

Most living birds exhibit cranial kinesis-movement between the rostrum and braincase-in which force is transferred through the palatal and jugal bars. The palate alone distinguishes the Paleognathae from the Neognathae, with cranial kinesis more developed in neognaths. Most previous palatal studies were based on 2D data and rarely incorporated data from stem birds despite great interest in their kinetic abilities. Here we reconstruct the vomer of the Early Cretaceous stem bird Sapeornis and the troodontid Sinovenator, taxa spanning the dinosaur-bird transition. A 3D shape analysis including these paravians and an extensive sampling of neornithines reveals their strong similarity to paleognaths and indicates that morphological differences in the vomer between paleognaths and neognaths are intimately related to their different kinetic abilities. These results suggest the skull of Mesozoic paravians lacked the kinetic abilities observed in neognaths, a conclusion also supported by our identification of an ectopterygoid in Sapeornis here. We conclude that cranial kinesis evolved relatively late, likely an innovation of the Neognathae, and is linked to the transformation of the vomer. This transformation increased palatal mobility, enabling the evolution of a diversity of kinetic mechanisms and ultimately contributing to the extraordinary evolutionary success of this clade.

Morphological integration affects the evolution of midline cranial base, lateral basicranium, and face across primates.

OBJECTIVES: The basicranium and face are two integrated bony structures displaying great morphological diversity across primates. Previous studies in hominids determined that the basicranium is composed of two independent modules: the midline basicranium, mostly influenced by brain size, and the lateral basicranium, predominantly associated with facial shape. To better assess how morphological integration impacts the evolution of primate cranial shape diversity, we test to determine whether the relationships found in hominids are retained across the order. MATERIALS AND METHODS: Three-dimensional landmarks (29) were placed on 143 computed tomography scans of six major clades of extant primate crania. We assessed the covariation between midline basicranium, lateral basicranium, face, and endocranial volume using phylogenetically informed partial least squares analyses and phylogenetic generalized least squares models. RESULTS: We found significant integration between lateral basicranium and face and between midline basicranium and face. We also described a significant correlation between midline basicranium and endocranial volume but not between lateral basicranium and endocranial volume. DISCUSSION: Our findings demonstrate a significant and pervasive integration in the craniofacial structures across primates, differing from previous results in hominids. The uniqueness of module organization in hominids may explain this distinction. We found that endocranial volume is significantly integrated to the midline basicranium but not to the lateral basicranium. This finding underlines the significant effect of brain size on the shape of the midline structures of the cranial base in primates. With the covariations linking the studied features defined here, we suggest that future studies should focus on determining the causal links between them.

Raptor talon shape and biomechanical performance are controlled by relative prey size but not by allometry.

Most birds of prey (raptors), rely heavily on their talons for capturing prey. However, the relationship between talon shape and the ability to take prey is poorly understood. In this study we investigate whether raptor talons have evolved primarily in response to adaptive pressures exerted by different dietary demands, or if talon morphology is largely constrained by allometric or phylogenetic factors. We focus on the hallux talon and include 21 species in total varying greatly in body mass and feeding ecology, ranging from active predation on relatively large prey to obligate scavenging. To quantify the variation in talon shape and biomechanical performance within a phylogenetic framework, we combined three dimensional (3D) geometric morphometrics, finite element modelling and phylogenetic comparative methods. Our results indicate that relative prey size plays a key role in shaping the raptorial talon. Species that hunt larger prey are characterised by both distinct talon shape and mechanical performance when compared to species that predate smaller prey, even when accounting for phylogeny. In contrast to previous results of skull-based analysis, allometry had no significant effect. In conclusion, we found that raptor talon evolution has been strongly influenced by relative prey size, but not allometry and, that talon shape and mechanical performance are good indicators of feeding ecology.

Basicranium and face: Assessing the impact of morphological integration on primate evolution.

The basicranium and facial skeleton are two integrated structures displaying great morphological diversity across primates. Previous studies focusing on limited taxonomic samples have demonstrated that morphological integration has a significant impact on the evolution of these structures. However, this influence is still poorly understood. A more complete understanding of craniofacial integration across primates has important implications for functional hypotheses of primate evolution. In the present study, we analyzed a large sample of primate species to assess how integration affects the relationship between basicranial and facial evolutionary pathways across the order. First, we quantified integration and modularity between basicranium and face using phylogenetically-informed partial least squares analyses. Then, we defined the influence of morphological integration between these structures on rates of evolution, using a time-calibrated phylogenetic tree, and on disparity through time, comparing the morphological disparity across the tree with that expected under a pure Brownian process. Finally, we assessed the correlation between the basicranium and face, and three factors purported to have an important role in shaping these structures during evolution: endocranial volume, positional behavior (i.e., locomotion and posture), and diet. Our findings show that the face and basicranium, despite being highly integrated, display significantly different evolutionary rates. However, our results demonstrate that morphological integration impacted shape disparity through time. We also found that endocranial volume and positional behavior are important drivers of cranial shape evolution, partly affected by morphological integration.

Relationship between foramen magnum position and locomotion in extant and extinct hominoids.

From the Miocene Sahelanthropus tchadensis to Pleistocene Homo sapiens, hominins are characterized by a derived anterior position of the foramen magnum relative to basicranial structures. It has been previously suggested that the anterior position of the foramen magnum in hominins is related to bipedal locomotor behavior. Yet, the functional relationship between foramen magnum position and bipedal locomotion remains unclear. Recent studies, using ratios based on cranial linear measurements, have found a link between the anterior position of the foramen magnum and bipedalism in several mammalian clades: marsupials, rodents, and primates. In the present study, we compute these ratios in a sample including a more comprehensive dataset of extant hominoids and fossil hominins. First, we verify if the values of ratios can distinguish extant humans from apes. Then, we test whether extinct hominins can be distinguished from non-bipedal extant hominoids. Finally, we assess if the studied ratios are effective predictors of bipedal behavior by testing if they mainly relate to variation in foramen magnum position rather than changes in other cranial structures. Our results confirm that the ratios discriminate between extant bipeds and non-bipeds. However, the only ratio clearly discriminating between fossil hominins and other extant apes is that which only includes basicranial structures. We show that a large proportion of the interspecific variation in the other ratios relates to changes in facial, rather than basicranial, structures. In this context, we advocate the use of measurements based only on basicranial structures when assessing the relationship between foramen magnum position and bipedalism in future studies.

Digging adaptation in insectivorous subterranean eutherians. The enigma of Mesoscalops montanensis unveiled by geometric morphometrics and finite element analysis.

The enigmatic Early Miocene fossorial mammal Mesoscalops montanensis shows one of the most modified humeri among terrestrial mammals. It has been suggested, on qualitative considerations, that this species has no extant homologues for humerus kinematics and that, functionally, the closest extant group is represented by Chrysochloridae. We combine here three dimensional geometric morphometrics, finite element analysis and phylogenetic comparative methods to explore the shape and mechanical stress states of Mesoscalops montanensis as well as of extant and extinct Talpidae and Chrysochloridae under realistic digging simulations. Evolutionary convergence analyses reveal that the shape of Mesoscalops montanensis represents a unique morphology in the context of fossorial mammals and that its functional performance, albeit superficially similar to that of extant Chrysochloridae, still represents a nonconvergent optimum for adaptation to digging.

Morphological integration and functional modularity in the crocodilian skull.

We explored the morphological organization of the skull within Crocodylidae, analyzing functional and phylogenetic interactions between its 2 constituent functional modules: the rostrum and the postrostrum. We used geometric morphometrics to identify localized shape changes, focusing on the differences between the major clades of the crown-group Crocodylia: Alligatoridae and Crocodylidae. We used published bite performance data to correlate rostral function with postrostral morphology. The skull modules appear more integrated within Alligatoridae than within Crocodyliade. Phylogenetic effects on shape variation are more evident in Alligatoridae than in Crocodylidae, where functional parameters concerning the rostral morphology are proportionally more important than phylogeny. Long-snouted species are characterized by low structural performance, which is significantly associated with a reduction of the pterygoid-quadrate cranial nipper, suggesting that the nipper is important for the ingestion of large food items in generalist species. This functional association is coupled with a significant evolutionary allometry at the clade level, while Alligatoridae and Crocodylidae show different degrees of evolutionary allometry for their entire shape and rostrum. The postrostrum is more conservative than the rostrum in terms of morphospace occupation, evolutionary allometry and phylogenetic signal.