Camille Bader

Captive environments induce plastic and adaptive phenotypic changes to the inner and outer anatomy of vertebrate bones. However, the respective effects of these changes are not well documented. This study examines the impact of captivity on the microanatomy of the talus, an ankle bone that lacks muscular attachment but is involved in supporting the body weight during locomotion. This study focuses on the wild boar ( Sus scrofa ) as a wild ungulate model and on an experimental setting through which these wild boars experienced different mobility patterns during their growth: 20 lived in their natural habitat, while 21 were born in the wild but raised in captivity, either in a large enclosure (10) or in a stable (11). We quantitatively investigated the microanatomical structure of their talus using 3D cartographies of compact bone thickness and five microanatomical parameters, while describing the distribution of compact bone and the trabecular network from the cartographies and virtual sections. While the absolute thickness of compact bone remains similar regardless of the mobility context, specimens that have been raised in captivity have tali with greater bone density and a tighter network of bone trabeculae but a lower relative maximum thickness of compact bone. Our results show that captivity induces a plastic response in the bone microanatomy, which could therefore serve as a valuable indicator of the early process of domestication of wild boars and, more generally, wild ungulates in the bioarchaeological records.

Terrestrial vertebrates rely on their skeleton to provide structural support and allow the movement of the body. Heavy, graviportal taxa, such as extant elephants, exhibit numerous adaptive features in their bone anatomy enabling them to withstand their immense weight. Conversely, dwarfing events impose novel biomechanical constraints on the skeleton. The case of dwarf elephants raises the question of how graviportal animals adapt when undergoing drastic size reduction, and whether they retain graviportal features or exhibit paedomorphic traits. In this study, we examine the morphology and microanatomy of the six long bones in two fossil species of dwarf elephants, Palaeoloxodon tiliensis (adults) and P. falconeri (juveniles), using both quantitative and qualitative approaches (3D geometric morphometrics, virtual slice comparisons, compact bone thickness cartographies). Our results show that in P. tiliensis , the reduction in body mass is reflected in the morphology and microanatomy of the bones, suggesting a more flexed limb posture and a reduced parasagittal orientation compared to in fully graviportal proboscideans. Despite this shift, several key graviportal adaptations are retained in P. tiliensis . Additionally, comparisons with early, non‐graviportal proboscideans indicate that dwarf elephants exhibit a partial reversion to ancestral limb traits, while maintaining essential weight‐bearing features. Finally, adult P. tiliensis and juvenile P. falconeri specimens exhibit a medullary area filled with trabecular bone, similar to that of extant elephants. Dwarf elephants are thus not scaled‐down versions of their mainland ancestors, but instead display a combination of juvenile, graviportal and ancestral traits reflecting the impact of dwarfism on their evolutionary trajectory.

Adaptation internes et externes des os longs à la graviportalité chez les Proboscidea, comparés à d'autres taxons lourds (Hippopotamidae, Rhinocerotidae): Les proboscidiens comptent parmi les animaux les plus lourds qui aient jamais existé. Les premiers proboscidiens étaient relativement petits et ont évolué vers des formes plus grandes, atteignant des formes graviportales massives. Bien que l'influence de la masse corporelle sur les os des membres soit bien documentée chez d'autres taxons graviporteurs, les recherches sur les proboscidiens sont limitées. Ce travail explore l'effet d'un poids massif sur les six os longs des proboscidiens actuels et éteints en les comparant à d'autres taxons graviporteurs, via des analyses de morphométrie géométrique 3D, robustesse et de microanatomie. Le premier chapitre porte sur les éléphants actuels, révélant des patrons d'allométrie ontogénétique négatifs similaires chez Elephas maximus et Loxodonta africana; ces patrons pourraient être liés à des adaptations au support du poids présentes dès la naissance. À l'échelle intraspécifique, la robustesse des os augmente avec la masse corporelle, améliorant la répartition des charges chez les individus les plus lourds. Les éléphants d'Asie présentent des os longs plus robustes que ceux de savane d'Afrique, avec de plus grandes zones d'insertions musculaires, suggérant une plus grande souplesse et dextérité des membres, possiblement liée aux différences d'habitat et de recherche de nourriture. Le deuxième chapitre étend ces analyses de forme aux proboscidiens fossiles. L'acquisition du membre columnaire est associée à des réorientations des surfaces articulaires et à une diminution de la robustesse, minimisant les contraintes de flexion. Deux morphotypes distincts sont identifiés chez les proboscidiens graviporteurs : l'un avec des diaphyses et des épiphyses relativement fines (ex., déinothères, éléphantidés), et l'autre avec des diaphyses et des épiphyses larges (ex., gomphothères, mammutidés). Ces morphologies distinctes suggèrent des stratégies différentes d'adaptation au poids, qui, une fois acquises, restent fixes au sein des lignées. Le chapitre 3 examine la microanatomie des os d'éléphants actuels, montrant une couche corticale relativement épaisse, en particulier près des centres de croissance, et une zone médullaire remplie d'os trabéculaire, améliorant le soutien du poids. Les travées sont fortement anisotropes et orientées de manière parasagittale, reflétant la distribution des charges mécaniques le long des membres. L'épaisseur corticale et l'orientation des travées varient entre les six os longs, reflétant leur spécialisation fonctionnelle. E. maximus et L. africana partagent un patron ontogénétique similaire, les juvéniles montrant des adaptations au poids dans leur épaisseur corticale, suivies de changements dans la distribution de cette dernière et d'augmentations de la densité et de l'anisotropie trabéculaires durant la croissance. Si des traits microanatomiques communs à d'autres mammifères lourds sont présents chez les éléphants, les os de leurs membres présentent une grande similitude avec ceux des sauropodes, due à leur posture columnaire commune, qui optimise le support de la compression axiale et permet de réduire les contraintes de support du poids. Enfin, le chapitre 4 explore l'effet du nanisme insulaire chez les proboscidiens (Palaeoloxodon tiliensis, P. falconeri). La réduction des contraintes de poids se reflète dans la morphologie et la microanatomie des os : P. tiliensis présente des membres plus fléchis et une zone médullaire majoritairement dépourvue de tissu trabéculaire, ainsi que des traits plésiomorphes. Si certains traits liés à la graviportalité ont été perdus au cours du nanisme, d'autres ont été conservés, suggérant que les éléphants nains présentent des membres généralement graviporteurs. Ce travail met en évidence la diversité des adaptations au support d'un poids massif dans les os longs des membres des proboscidiens, apportant des nouvelles informations sur l'adaptation de ces animaux à leur gigantisme.

The evolutionary increase in body size of terrestrial quadrupeds is closely associated with skeletal adaptations to support their mass. Following Cope's Rule, proboscideans evolved from relatively small early forms to increasingly large ones. Their limb long bones exhibit corresponding adaptations to these shifts in body mass through two main weight‐bearing strategies. The ankle joint is essential for weight bearing and locomotion and is therefore expected to show corresponding adaptations. This study investigates the morphological variation of the astragalus and calcaneus in extant and extinct proboscideans using three‐dimensional geometric morphometrics in a phylogenetic context to explore morphological adaptations related to body mass, locomotion and posture. The results show that the acquisition of a more columnar posture during the Miocene is accompanied by a reorganization of the foot anatomy reducing axial compression constraints. Astragalus and calcaneus morphologies of graviportal proboscideans are influenced by body mass, especially at the level of articular facets and ligament and muscle attachment sites. The results highlight two distinct morphotypes among graviportal proboscideans: Elephantidae, Mammutidae and Stegodontidae have an ankle morphology optimized for stability and rapid movement, but Gomphotheriidae, Amebelodontidae and Deinotheriidae show an ankle morphology adapted to powerful strokes, particularly in plantar–dorsiflexion. Both morphotypes are observed in taxa of similar mass, and, once acquired, remain fixed within the lineage even in cases of insular dwarfism. Finally, the overall hindlimb morphology highlights different combinations of robustness between the long‐bone and tarsal morphotypes depending on the taxon, reflecting different locomotor and weight‐bearing strategies within Proboscidea.

One of the greatest challenges of terrestrial locomotion is resisting gravity. The morphological adaptive features of the limb long-bones of extant elephants, the heaviest living terrestrial animals, have previously been highlighted; however, their bone microanatomy remains largely unexplored. Here we investigate the microanatomy of the six limb long-bones in Elephas maximus and Loxodonta africana, using comparisons of virtual slices as well as robustness analyses, to understand how they were adapted to heavy weight-bearing. We find that the long bones of elephant limbs display a relatively thick cortex and a medullary area almost entirely filled with trabecular bone. This trabecular bone is highly anisotropic with trabecular orientations reflecting the mechanical load distribution along the limb. The respective functional roles of the bones are reflected in their microanatomy through variations of cortical thickness distribution and main orientation of the trabeculae. We find microanatomical adaptations to heavy weight support that are common to other heavy mammals. Despite these shared characteristics, the long bones of elephants are closer to those of sauropods due to their shared columnar posture, which allows a relaxation of morphofunctional constraints, and thus relatively less robust bones with a thinner cortex than would be expected in such massive animals.

One of the greatest challenges of terrestrial locomotion is resisting gravity. The morphological adaptive features of the limb long-bones of extant elephants, the heaviest living terrestrial animals, have previously been highlighted; however, their bone microanatomy remains largely unexplored. Here we investigate the microanatomy of the six limb long-bones in Elephas maximus and Loxodonta africana, using comparisons of virtual slices as well as robustness analyses, to understand how they were adapted to heavy weight-bearing. We find that the long bones of elephant limbs display a relatively thick cortex and a medullary area almost entirely filled with trabecular bone. This trabecular bone is highly anisotropic with trabecular orientations reflecting the mechanical load distribution along the limb. The respective functional roles of the bones are reflected in their microanatomy through variations of cortical thickness distribution and main orientation of the trabeculae. We find microanatomical adaptations to heavy weight support that are common to other heavy mammals. Despite these shared characteristics, the long bones of elephants are closer to those of sauropods due to their shared columnar posture, which allows a relaxation of morphofunctional constraints, and thus relatively less robust bones with a thinner cortex than would be expected in such massive animals.

From its first small representatives to its later giant species, the Order Proboscidea evolved increasingly large forms. Limb long bones are heavily affected by shifts in body mass, and this is especially true in proboscideans, in which an increase in body mass is associated with a reorientation of the limb into the parasagittal plane, reducing the need for strong musculature. We investigated shape variation in the six long bones elements of the limb of extant and extinct proboscideans with regard to body mass evolution in this lineage. To do so, we used three‐dimensional geometric morphometrics and qualitative comparisons to describe shape variability. Our analysis indicates that the shift from a flexed posture to a columnar one results in reorientations of articular surfaces in the six bones, and a decrease in robustness, thus reducing bending stresses on the bones. We also identify two main morphotypes among graviportal proboscideans: one (MA) corresponding to bones with a thin diaphysis and narrow epiphyses, as in deinotheres and elephantids, and the other (MB) to bones with a large diaphysis and wide epiphyses, seen in gomphotheres and mammutids. Both morphotypes are observed in species of similar mass, indicating that adaptation to high body weight support has been achieved in two different ways among proboscideans, and that once acquired, it remains fixed within the taxon.

During evolution, several vertebrate lineages have shown trends towards an increase in mass. Such a trend is associated with physiological and musculoskeletal changes necessary to carry and move an increasingly heavy body. Due to their prominent role in the support and movement of the body, limb long bones are highly affected by these shifts in body mass. Elephants are the heaviest living terrestrial mammals, displaying unique features allowing them to withstand their massive weight, such as the columnarity of their limbs, and as such are crucial to understand the evolution towards high body mass in land mammals. In this study, we investigate the shape variation of the six limb long bones among the modern elephants, Elephas maximus and Loxodonta africana, to understand the effect of body mass and habitat on the external anatomy of the bones. To do so, we use three‐dimensional geometric morphometrics (GMMs) and qualitative comparisons to describe the shape variation, at both the intraspecific and interspecific levels. Our results reveal that the two species share similar negative ontogenetic allometric patterns (i.e. becoming stouter with increased length) in their humerus and femur, but not in the other bones: the proximal epiphyses of the stylopod bones develop considerably during growth, while the distal epiphyses, which are involved in load distribution in the elbow and knee joints, are already massive in juveniles. We attribute this pattern to a weight‐bearing adaptation already present in young specimens. Among adults of the same species, bone robustness increases with body mass, so that heavier specimens display stouter bones allowing for a better mechanical load distribution. While this robustness variation is significant for the humerus only, all the other bones appear to follow the same pattern. This is particularly visible in the ulna and tibia, but less so in the femur, which suggests that the forelimb and hindlimb adapted differently to high body mass support. Robustness analyses, while significant for the humerus only, suggest more robust long bones in Asian elephants than in African savanna elephants. More specifically, GMMs and qualitative comparisons indicate that three bones are clearly distinct when comparing the two species: in E. maximus the humerus, the ulna and the tibia display enlarged areas of muscular insertions for muscles involved in joint and limb stabilization, as well as in limb rotation. These results suggest a higher limb compliance in Asian elephants, associated with a higher dexterity, which could be linked to their habitat and foraging habits.

The long bones and associated musculature play a prominent role in the support and movement of the body and are expected to reflect the associated mechanical demands. But in addition to the functional response to adaptive changes, the conjoined effects of phylogenetic, structural and developmental constraints also shape the animal's body. In order to minimise the effect of the aforementioned constraints and to reveal the biomechanical adaptations in the musculoskeletal system to locomotor mode, we here study the forelimb of two closely related martens: the arboreal pine marten (Martes martes) and the more terrestrial stone marten (Martes foina), focusing on their forelimb muscle anatomy and long bone microanatomy; and, especially, on their covariation. To do so, we quantified muscle data and bone microanatomical parameters and created 3D and 2D maps of the cortical thickness distribution for the three long bones of the forelimb. We then analysed the covariation of muscle and bone data, both qualitatively and quantitatively. Our results reveal that species‐specific muscular adaptations are not clearly reflected in the microanatomy of the bones. Yet, we observe a global thickening of the bone cortex in the radius and ulna of the more arboreal pine marten, as well a stronger flexor muscle inserting on its elbow. We attribute these differences to variation in their locomotor modes.Analyses of our 2D maps revealed a shift of cortical thickness distribution pattern linked to ontogeny, rather than species‐specific patterns. We found that although intraspecific variation is not negligible, species distinction was possible when taking muscular and bone microanatomical data into consideration. Results of our covariation analyses suggest that the muscle‐bone correlation is linked to ontogeny rather than to muscular strength at zones of insertion. Indeed, if we find a correlation between cortical thickness distribution and the strength of some muscles in the humerus, that is not the case for the others and in the radius and ulna. Cortical thickness distribution appears rather linked to bone contact zones and ligament insertions in the radius and ulna, and to some extent in the humerus. We conclude that inference on muscle from bone microanatomy is possible only for certain muscles in the humerus.