A switch in jaw form-function coupling during the evolution of mammals.

The evolutionary shift from a single-element ear, multi-element jaw to a multi-element ear, single-element jaw during the transition to crown mammals marks one of the most dramatic structural transformations in vertebrates. Research on this transformation has focused on mammalian middle-ear evolution, but a mandible comprising only the dentary is equally emblematic of this evolutionary radiation. Here, we show that the remarkably diverse jaw shapes of crown mammals are coupled with surprisingly stereotyped jaw stiffness. This strength-based morphofunctional regime has a genetic basis and allowed mammalian jaws to effectively resist deformation as they radiated into highly disparate forms with markedly distinct diets. The main functional consequences for the mandible of decoupling hearing and mastication were a trade-off between higher jaw stiffness versus decreased mechanical efficiency and speed compared with non-mammals. This fundamental and consequential shift in jaw form-function underpins the ecological and taxonomic diversification of crown mammals. This article is part of the theme issue 'The mammalian skull: development, structure and function'.

Adaptive landscapes challenge the "lateral-to-sagittal" paradigm for mammalian vertebral evolution.

The evolution of mammals from their extinct forerunners, the non-mammalian synapsids, is one of the most iconic locomotor transitions in the vertebrate fossil record. In the limb skeleton, the synapsid-mammal transition is traditionally characterized by a shift from a sprawling limb posture, resembling that of extant reptiles and amphibians, to more adducted limbs, as seen in modern-day mammals. Based on proposed postural similarities between early synapsids and extant reptiles, this change is thought to be accompanied by a shift from ancestral reptile-like lateral bending to mammal-like sagittal bending of the vertebral column. To test this "lateral-to-sagittal" evolutionary paradigm, we used combinatorial optimization to produce functionally informed adaptive landscapes and determined the functional trade-offs associated with evolutionary changes in vertebral morphology. We show that the synapsid adaptive landscape is different from both extant reptiles and mammals, casting doubt on the reptilian model for early synapsid axial function, or indeed for the ancestral condition of amniotes more broadly. Further, the synapsid-mammal transition is characterized by not only increasing sagittal bending in the posterior column but also high stiffness and increasing axial twisting in the anterior column. Therefore, we refute the simplistic lateral-to-sagittal hypothesis and instead suggest the synapsid-mammal locomotor transition involved a more complex suite of functional changes linked to increasing regionalization of the backbone. These results highlight the importance of fossil taxa for understanding major evolutionary transitions.

Functional adaptive landscapes predict terrestrial capacity at the origin of limbs.

The acquisition of terrestrial, limb-based locomotion during tetrapod evolution has remained a subject of debate for more than a century1,2. Our current understanding of the locomotor transition from water to land is largely based on a few exemplar fossils such as Tiktaalik3, Acanthostega4, Ichthyostega5 and Pederpes6. However, isolated bony elements may reveal hidden functional diversity, providing a more comprehensive evolutionary perspective7. Here we analyse 40 three-dimensionally preserved humeri from extinct tetrapodomorphs that span the fin-to-limb transition and use functionally informed ecological adaptive landscapes8-10 to reconstruct the evolution of terrestrial locomotion. We show that evolutionary changes in the shape of the humerus are driven by ecology and phylogeny and are associated with functional trade-offs related to locomotor performance. Two divergent adaptive landscapes are recovered for aquatic fishes and terrestrial crown tetrapods, each of which is defined by a different combination of functional specializations. Humeri of stem tetrapods share a unique suite of functional adaptations, but do not conform to their own predicted adaptive peak. Instead, humeri of stem tetrapods fall at the base of the crown tetrapod landscape, indicating that the capacity for terrestrial locomotion occurred with the origin of limbs. Our results suggest that stem tetrapods may have used transitional gaits5,11 during the initial stages of land exploration, stabilized by the opposing selective pressures of their amphibious habits. Effective limb-based locomotion did not arise until loss of the ancestral 'L-shaped' humerus in the crown group, setting the stage for the diversification of terrestrial tetrapods and the establishment of modern ecological niches12,13.

The evolutionary diversity of locomotor innovation in rodents is not linked to proximal limb morphology.

Rodents are the most species-rich order within Mammalia and have evolved disparate morphologies to accommodate numerous locomotor niches, providing an excellent opportunity to understand how locomotor innovation can drive speciation. To evaluate the connection between the evolutionary success of rodents and the diversity of rodent locomotor ecologies, we used a large dataset of proximal limb CT scans from across Myomorpha and Geomyoidea to examine internal and external limb shape. Only fossorial rodents displayed a major reworking of their proximal limbs in either internal or external morphology, with other locomotor modes plotting within a generalist morphospace. Fossorial rodents were also the only locomotor mode to consistently show increased rates of humerus/femur morphological evolution. We propose that these rodent clades were successful at spreading into ecological niches due to high behavioral plasticity and small body sizes, allowing them to modify their locomotor mode without requiring major changes to their proximal limb morphology.

Functional performance of turtle humerus shape across an ecological adaptive landscape.

The concept of the adaptive landscape has been invaluable to evolutionary biologists for visualizing the dynamics of selection and adaptation, and is increasingly being used to study morpho-functional data. Here, we construct adaptive landscapes to explore functional trade-offs associated with variation in humerus morphology among turtles adapted to three different locomotor environments: marine, semiaquatic, and terrestrial. Humerus shape from 40 species of cryptodire turtles was quantified using a pseudolandmark approach. Hypothetical shapes were extracted in a grid across morphospace and four functional traits (strength, stride length, mechanical advantage, and hydrodynamics) measured on those shapes. Quantitative trait modeling was used to construct adaptive landscapes that optimize the functional traits for each of the three locomotor ecologies. Our data show that turtles living in different environments have statistically different humeral shapes. The optimum adaptive landscape for each ecology is defined by a different combination of performance trade-offs, with turtle species clustering around their respective adaptive peak. Further, species adhere to pareto fronts between marine-semiaquatic and semiaquatic-terrestrial optima, but not between marine-terrestrial. Our study demonstrates the utility of adaptive landscapes in informing the link between form, function, and ecological adaptation, and establishes a framework for reconstructing turtle ecological evolution using isolated humeri from the fossil record.

Semicircular canals in Anolis lizards: ecomorphological convergence and ecomorph affinities of fossil species.

Anolis lizards are a model system for the study of adaptive radiation and convergent evolution. Greater Antillean anoles have repeatedly evolved six similar forms or ecomorphs: crown-giant, grass-bush, twig, trunk, trunk-crown and trunk-ground. Members of each ecomorph category possess a specific set of morphological, ecological and behavioural characteristics which have been acquired convergently. Here we test whether the semicircular canal system-the organ of balance during movement-is also convergent among ecomorphs, reflecting the shared sensory requirements of their ecological niches. As semicircular canal shape has been shown to reflect different locomotor strategies, we hypothesized that each Anolis ecomorph would have a unique canal morphology. Using three-dimensional semilandmarks and geometric morphometrics, semicircular canal shape was characterized in 41 Anolis species from the Greater Antilles and the relationship between canal shape and ecomorph grouping, phylogenetic history, size, head dimensions, and perch characteristics was assessed. Further, canal morphology of modern species was used to predict the ecomorph affinity of five fossil anoles from the Miocene of the Dominican Republic. Of the covariates tested, our study recovered ecomorph as the single-most important covariate of canal morphology in modern taxa; although phylogenetic history, size, and head dimensions also showed a small, yet significant correlation with shape. Surprisingly, perch characteristics were not found to be significant covariates of canal shape, even though they are important habitat variables. Using posterior probabilities, we found that the fossil anoles have different semicircular canals shapes to modern ecomorph groupings implying extinct anoles may have been interacting with their Miocene environment in different ways to modern Anolis species.