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.

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.

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.

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.