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How Bone Adapts to Heavy Weight? Bone Morphological and Microanatomical Adaptation to the Mechanical Constraints Imposed by Graviportality

Periodic Reporting for period 4 - GRAVIBONE (How Bone Adapts to Heavy Weight?Bone Morphological and Microanatomical Adaptation to the Mechanical Constraints Imposed by Graviportality)

Reporting period: 2021-10-01 to 2023-03-31

The skeleton adapts to the functional constraints undergone by organisms. Consequently, although bones are also the result of other constraints (historical, developmental, structural), they carry a strong functional signal. Understanding this form-function relationship is important for understanding the evolutionary history of organisms. To analyze and characterize the relationships between the shape of skeletal elements and the functional constraints they have to cope with, the main case studies are convergences. They make it possible to distinguish common adaptive traits, whatever the lineage, which reflect 'obligatory' acquisitions to respond to a specific function, but also various specific adaptations, which highlight how, with distinct heritages, species have succeeded differently in adapting to a particular function.

The convergent adaptation that GRAVIBONE has focused on is the adaptation to support and locomote a heavy weight (more than a tonne), a pattern that has evolved in numerous lineages throughout amniote evolutionary history. The term "graviportality" was introduced to characterize these heavy-bodied animals; these forms require specialized limbs (proportions, bone shape, arrangement between the bones) adapted to support their weight, since body mass (and therefore weight) is multiplied by eight when size is multiplied by two. The adaptive changes associated with graviportality had been little studied, and the definition of graviportality itself was imprecise. While only a few modern forms are well over a tonne (elephants, rhinoceroses and hippopotamuses), the fossil record is much richer in massive taxa that are very diverse, so that convergences can be clearly analyzed.

The ERC-StG GRAVIBONE project thus focused on the adaptation of the long bones of the limbs, at the anatomical and microanatomical levels, to the biomechanical constraints associated with graviportality, and on the way in which the external and internal structures of the bone co-evolve. The aim was to gain a precise understanding of the changes in the structure of the bone as a whole in response to the mechanical constraints imposed by a heavy skeleton in modern and fossil animals with different morphologies and locomotor behaviors, but also to combine anatomical and microanatomical analyses on whole bones with biomechanical modelling in order to characterize in detail form-function relationships to be able to characterize various modes of adaptation to graviportality. The ultimate aim was to model the relationship between bone anatomy, microanatomy and the functional requirements for body support and locomotion in graviportal amniotes, and thus to better understand how bone responds to biomechanical constraints.
We therefore analyzed the morphology and microanatomy of the limb bones of some of the heaviest modern and extinct terrestrial vertebrates, but also of comparatively less massive groups, for comparative purposes. We carried out studies at different taxonomic scales in order to analyze in detail the structural characteristics linked to the support of a massive weight in various lineages.

The group has acquired a large amount of 3D data that it makes/will make available to the community and has developed new innovative methodologies that are currently world-leading in 3D microanatomy.
We also performed a biomechanical model and biomechanical analyses on rhinocerotid bones.

Our methodological developments and the combination of our approaches enabled us to precisely characterize bone form-function relationships and, by comparing the microstructure of the bone with the biomechanical data, to show that trabecular bone structure strongly responds to the principal mechanical stresses applied to the skeleton.

Thus, in addition to 1) demonstrating increased bone strength and the development of insertion zones for powerful extensor muscles, as well as various patterns of heterogeneous increase in cortical thickness and extension of cancellous bone into the medullary cavity associated with the support of body weight in the long bones of various massive amniotes, our studies have shown 2) the co-evolution of external and internal bone structures and how changes in shape can relax mass-related microanatomical specialisations, and 3) how, above a certain weight, the columnar organisation allows the stresses associated with supporting body weight to be relaxed, so that the bones have only relatively limited mass-related specialisations. These results provide a better understanding of the adaptation of bones to high body weight and, more generally, of the combination of functional adaptations of bones at the morphological and microanatomical levels.

This work also led to a better understanding of the posture of extinct taxa and their locomotion and palaeoecology, and to better characterise postural changes in the different lineages that evolved from bipedal to quadrupedal forms (in dinosaurs in particular).

This project has enabled us to set up a group in which we combine morphological, microanatomical and muscular (albeit from the literature or in collaboration) data with biomechanical analyses to characterize in detail the form-function relationships in the musculoskeletal system in modern forms, and thus to be able to propose solid functional hypotheses for fossil forms and better document their palaeoecology and the evolutionary history of their lineages.
GRAVIBONE has focused on taxa that are rather poorly studied from a functional point of view, with rare and limited parallels between lineages, and has concentrated on bones that are also poorly studied from a biomechanical point of view. It has developed an innovative approach for comparing in detail bone microanatomical features with biomechanical constraints, an approach that has remained underdeveloped (except in humans) in the scientific community. The combination of morphological, microanatomical and biomechanical analyses in an evolutionary context has enabled us to go a step further in characterizing bone form-function relationships. Thanks to this project, we have a better understanding of the adaptation of long bones to heavy weight support and locomotion, we can better infer the palaeoecology of various fossil forms, and we have highlighted how the external and internal structures of bones co-evolve, in combination with changes in the architecture of the limbs, and the posture and the weight of the animal.
This project therefore provides a solid basis on which to explore other convergences, and characterise the functional adaptation of bone to various constraints.