Papers by Alexandra Houssaye
Journal of Anatomy, Mar 9, 2022
HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific r... more HAL is a multi-disciplinary open access archive for the deposit and dissemination of scientific research documents, whether they are published or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers. L'archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d'enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.
A Methodological Renaissance to Advance Perennial Issues in Vertebrate Paleohistology
CRC Press eBooks, May 29, 2021
A path to gigantism: Three‐dimensional study of the sauropodomorph limb long bone shape variation in the context of the emergence of the sauropod bauplan
Journal of Anatomy, Mar 6, 2022
Sauropodomorph dinosaurs include the largest terrestrial animals that ever lived on Earth. The ea... more Sauropodomorph dinosaurs include the largest terrestrial animals that ever lived on Earth. The early representatives of this clade were, however, relatively small and partially to totally bipedal, conversely to the gigantic and quadrupedal sauropods. Although the sauropod bauplan is well defined, notably by the acquisition of columnar limbs, the evolutionary sequence leading to its emergence remains debated. Here, we aim to tackle this evolutionary episode by investigating shape variation in the six limb long bones for the first time using three‐dimensional geometric morphometrics. The morphological features of the forelimb zeugopod bones related to the sauropod bauplan tend to appear abruptly, whereas the pattern is more gradual for the hindlimb zeugopod bones. The stylopod bones tend to show the same pattern as their respective zeugopods. The abrupt emergence of the sauropod forelimb questions the locomotor abilities of non‐sauropodan sauropodomorphs inferred as quadrupeds. Features characterizing sauropods tend to corroborate a view of their locomotion mainly based on stylopod retraction. An allometric investigation of the shape variation in accordance with size highlight differences in hindlimb bone allometries between the sauropods and the non‐sauropodan sauropodomorphs. These differences notably correspond to an unexpected robustness decrease trend in the sauropod hindlimb zeugopod. In addition to forelimb bones that appear to be proportionally more gracile than in non‐sauropodan sauropodomorphs, sauropods may have relied on limb architecture and features related to the size increase, rather than general robustness, to deal with the role of weight‐bearing.
3D quantitative comparative analysis of long bone diaphysis variations in microanatomy and cross‐sectional geometry
Journal of Anatomy, Feb 6, 2018
Long bone inner structure and cross‐sectional geometry display a strong functional signal, leadin... more Long bone inner structure and cross‐sectional geometry display a strong functional signal, leading to convergences, and are widely analyzed in comparative anatomy at small and large taxonomic scales. Long bone microanatomical studies have essentially been conducted on transverse sections but also on a few longitudinal ones. Recent studies highlighted the interest in analyzing variations of the inner structure along the diaphysis using a qualitative as well as a quantitative approach. With the development of microtomography, it has become possible to study three‐dimensional (3D) bone microanatomy and, in more detail, the form–function relationships of these features. This study focused on the selection of quantitative parameters to describe in detail the cross‐sectional shape changes and distribution of the osseous tissue along the diaphysis. Two‐dimensional (2D) virtual transverse sections were also performed in the two usual reference planes and results were compared with those obtained based on the whole diaphysis analysis. The sample consisted in 14 humeri and 14 femora of various mammalian taxa that are essentially terrestrial. Comparative quantitative analyses between different datasets made it possible to highlight the parameters that are strongly impacted by size and phylogeny and the redundant ones, and thus to estimate their relevance for use in form‐function analyses. The analysis illustrated that results based on 2D transverse sections are similar for both sectional planes; thus if a strong bias exists when mixing sections from the two reference planes in the same analysis, it would not problematic to use either one plane or the other in comparative studies. However, this may no longer hold for taxa showing a much stronger variation in bone microstructure along the diaphysis. Finally, the analysis demonstrated the significant contribution of the parameters describing variations along the diaphysis, and thus the interest in performing 3D analyses; this should be even more fruitful for heterogeneous diaphyses. In addition, covariation analyses showed that there is a strong interest in removing the size effect to access the differences in the microstructure of the humerus and femur. This methodological study provides a reference for future quantitative analyses on long bone inner structure and should make it possible, through a detailed knowledge of each descriptive parameter, to better interpret results from the multivariate analyses associated with these studies. This will have direct implications for studies in vertebrate anatomy, but also in paleontology and anthropology.
Anatomical Record-advances in Integrative Anatomy and Evolutionary Biology, May 7, 2019
Isolated ribs and vertebrae of Middle Triassic sauropterygians are studied. The vertebrae have a ... more Isolated ribs and vertebrae of Middle Triassic sauropterygians are studied. The vertebrae have a well-defined large cavity in their centra, which is a unique feature and is without any modern analogue. The articular facets of vertebrae are made of endochondral bone including calcified as well as uncalcified cartilage. Vertebrae are pachyosteosclerotic in the pachypleurosaurs Neusticosaurus and Serpianosaurus from the Alpine Triassic, and osteosclerotic in the placodont, in the medium-sized Nothosaurus marchicus, and in the pachypleurosaur Anarosaurus. In large Nothosaurus specimens, the vertebrae are cavernous. The ribs of all sampled specimens are osteosclerotic, which resembles the microanatomy of long bones in all studied taxa. The proximal to medial part of ribs mainly consist of a compact periosteal cortex surrounding an inner endosteal territory. Towards the distal end of the ribs, the periosteal thickness decreases whereas the endosteal territory increases. Despite a shift from periosteal vs. endosteal tissues, global rib compactness remains relatively constant. Osteosclerosis in ribs and vertebrae is reached by the same processes as in the long bones: by a relative increase in cortex thickness that is coupled by a reduction of the medullary cavity, by the persistence of calcified cartilage, and by an inhibition of remodelling although some resorption may occur but without complete redeposition of bone. Processes differ from those observed in Permian marine reptiles and some mosasaurines, where either extensive remodelling or inhibition of bone resorption leads to osteosclerosis.
Are Rhinoceros Graviportal? Morphofunctional 3D-Analysis of Modern Rhinoceros Limb Long Bones
HAL (Le Centre pour la Communication Scientifique Directe), Jul 21, 2019
PeerJ, May 11, 2021
Land mammals support and move their body using their musculoskeletal system. Their musculature us... more Land mammals support and move their body using their musculoskeletal system. Their musculature usually presents varying adaptations with body mass or mode of locomotion. Rhinocerotidae is an interesting clade in this regard, as they are heavy animals potentially reaching three tons but are still capable of adopting a galloping gait. However, their musculature has been poorly studied. Here we report the dissection of both forelimb and hindlimb of one neonate and one adult each for two species of rhinoceroses, the Indian rhinoceros ( Rhinoceros unicornis ) and the white rhinoceros ( Ceratotherium simum ). We show that their muscular organisation is similar to that of their relatives, equids and tapirs, and that few evolutionary convergences with other heavy mammals (e.g. elephants and hippopotamuses) are present. Nevertheless, they show clear adaptations to their large body mass, such as more distal insertions for the protractor and adductor muscles of the limbs, giving them longer le...
Ribs and vertebral micro-anatomical characteristics of hydropelvic mosasauroids
HAL (Le Centre pour la Communication Scientifique Directe), 2012
Shape variation in the limb long bones of modern elephants reveals adaptations to body mass and habitat
Journal of Anatomy
During evolution, several vertebrate lineages have shown trends towards an increase in mass. Such... more 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 intr...
Endocranial anatomy of two Elasmosauridae specimens (Reptilia, Plesiosauria) from the Late Cretaceous (Turonian) of Goulmima (Southern Morocco)
HAL (Le Centre pour la Communication Scientifique Directe), Apr 3, 2017
Bone Histology and the Adaptation to Aquatic Life in Tetrapods
CRC Press eBooks, May 29, 2021
Reassessing enigmatic Asian Hominoid dental remains
The 81st Annual Meeting of the American Association of Physical Anthropologists, Portland, OR, Mar 1, 2012
bioRxiv (Cold Spring Harbor Laboratory), Sep 21, 2022
Sexual dimorphism is challenging to detect among fossils, due to a lack of statistical representa... more Sexual dimorphism is challenging to detect among fossils, due to a lack of statistical representativeness. The Angeac-Charente Lagerstätte (France) represents a remarkable "snapshot" from a Berriasian (Early Cretaceous) ecosystem and offers a unique opportunity to study intraspecific variation among a herd of at least 61 coeval ornithomimosaurs. Herein, we investigated the hindlimb variation across the bestpreserved specimens from the herd through 3D Geometric Morphometrics and Gaussian Mixture Modelling. Our results based on complete and fragmented femora evidenced a dimorphism characterized by variations in the shaft curvature and the distal epiphysis width. Since the same features vary between sexes among modern avian dinosaurs, crocodilians, and more distant amniotes, we attributed this bimodal variation to sexual dimorphism based on the extant phylogenetic bracketing approach. Documenting sexual dimorphism in fossil dinosaurs allows a better characterization and accounting of intraspecific variations, which is particularly relevant to address ongoing taxonomical and ecological questions relative to dinosaur evolution. .
Sauropterygia: Nothosauria and Pachypleurosauria
HAL (Le Centre pour la Communication Scientifique Directe), Feb 1, 2021
PLOS ONE, Jul 8, 2016
Mid-diaphyseal cortical bone tissue in humeri of Nothosaurus spp. consists of coarse parallel-fib... more Mid-diaphyseal cortical bone tissue in humeri of Nothosaurus spp. consists of coarse parallel-fibered bone, finer and higher organized parallel-fibered bone, and lamellar bone. Vascular canals are mainly arranged longitudinally and radially in a dominantly radial system. Blood vessels are represented by simple vascular canals, incompletely lined primary osteons, and fully developed primary osteons. Nothosaurus spp. shows a variety of diaphyseal microanatomical patterns, ranging from thick to very thin-walled cortices. In the early Anisian (Lower Muschelkalk), small-and large-bodied Nothosaurus spp. generally exhibit bone mass increase (BMI). In the middle to late Anisian (Middle Muschelkalk) small-bodied nothosaurs retain BMI whereas larger-bodied forms tend to show a decrease in bone mass (BMD). During the latest Anisian to early Ladinian (Upper Muschelkalk), small-and few large-bodied nothosaurs retain BMI, whereas the majority of large-bodied forms exhibit BMD. The stratigraphically youngest nothosaurs document five microanatomical categories, two of which are unique among marine amniotes: One consists of a very heterogeneously distributed spongy periosteal organization, the other of very thin-walled cortices. The functional significance of the two unique microanatomical specializations seen in largebodied nothosaurs is the reduction of bone mass, which minimizes inertia of the limbs, and thus saves energy during locomotion. Transitions between the various microanatomical categories are rather gradual. Our results suggest that small-bodied Nothosaurus marchicus and other, not further assignable small-bodied nothosaurs seem to have been bound to near-shore, shallow marine environments throughout their evolution. Some large-bodied Nothosaurus spp. followed the same trend but others became more active swimmers and possibly inhabited open marine environments. The variety of microanatomical patterns may be related to taxonomic differences, developmental plasticity, and possibly sexual dimorphism. Humeral microanatomy documents the diversification of nothosaur species into different environments to avoid intraclade competition as well as competition with other
PeerJ, Jul 23, 2020
Sauropodomorph dinosaurs constitute a well-studied clade of dinosaurs, notably because of the acq... more Sauropodomorph dinosaurs constitute a well-studied clade of dinosaurs, notably because of the acquisition of gigantism within this group. The genus Plateosaurus is one of the best-known sauropodomorphs, with numerous remains from various localities. Its tumultuous taxonomic history suggests the relevance of addressing its intrageneric shape variability, mixed with taphonomic modifications of the original bone shape. Here we investigate quantitatively the morphological variation of Plateosaurus occurring at the genus level by studying the shape variation of a sample of limb long bones. By means of 3D geometric morphometrics, the analysis of the uncorrelated variation permits separation of the variation estimated as obviously taphonomically influenced from the more biologically plausible variation. Beyond the dominant taphonomic signal, our approach permits interpretation of the most biologically plausible features, even on anatomical parts influenced by taphonomic deformations. Those features are thus found on a quantitative basis from the variation of samples containing fossil specimens, by taking the impact of taphonomy into account, which is paramount in order to avoid making biologically ambiguous interpretations.
Biological Journal of The Linnean Society, Mar 2, 2017
The shape of long bones is linked to a species' ecology and is thought to reflect the constraints... more The shape of long bones is linked to a species' ecology and is thought to reflect the constraints imposed by locomotion. The evolution of the shape of the long bones in semi-aquatic mustelids has likely been shaped by the divergent mechanical properties of both water and land. Adaptation to a semi-aquatic lifestyle occurred independently in otters (Lutrinae) and minks (Mustelinae). Here we test the idea that these similar locomotor constraints led to morphological convergence between minks and otters, and between European and American minks. We use 3D geometric morphometrics to quantify shape differences in the humerus, radius, ulna, femur, tibia and fibula of ten species of mustelids belonging to the Lutrinae and Mustelinae subfamilies. Our results show convergence in all bones between the European and American minks, but this convergence is significant only for the humerus. We suggest that this strong convergence in humeral shape between the two minks results from functional demands on the forelimb as it produces most of the thrust when swimming in minks. The American minks show a slight but nonsignificant convergence with the Lutrinae for the shape of the ulna, femur and tibia. The sea otter (Enhydra lutris) shows an ulnar and radial shape that diverges from that observed in the other Lutrinae, possibly due to the strong manipulative abilities and unique locomotor mode of this species. In contrast to our initial hypothesis, bone shape in minks does not converge significantly with that of otters. Otters show a large variety of shapes suggesting that a semi-aquatic lifestyle can comprise a wide array of locomotor behaviours.
Biological Journal of The Linnean Society, Sep 8, 2015
Graviportal taxa show an allometric increase of the cross-sectional area of supportive bones and ... more Graviportal taxa show an allometric increase of the cross-sectional area of supportive bones and are assumed to display microanatomical changes associated with an increase in bone mass. This evokes osteosclerosis (i.e. an increase in bone compactness observed in some aquatic amniotes). The present study investigates the changes in bones' microanatomical organization associated with graviportality and how comparable they are with aquatically acquired osteosclerosis aiming to better understand the adaptation of bone to the different associated functional requirements. Bones of graviportal taxa show microanatomical changes that are not solely attributable to allometry. They display a thicker cortex and a proportionally smaller medullary cavity, with a wider transition zone between these domains. This inner cancellous structure may enable to better enhance energy absorption and marrow support. Moreover, the cross-sectional geometric parameters indicate increased resistance to stresses engendered by bending and torsion, as well as compression. Adaptation to a graviportal posture should be taken into consideration when analyzing possibly amphibious taxa with a terrestrial-like morphology. This is particularly important for palaeoecological inferences about large extinct tetrapods that might have been amphibious and, more generally, for the study of early stages of adaptation to an aquatic life in amniotes.
PLOS ONE, Feb 25, 2015
Cetacea are secondarily aquatic amniotes that underwent their land-to-sea transition during the E... more Cetacea are secondarily aquatic amniotes that underwent their land-to-sea transition during the Eocene. Primitive forms, called archaeocetes, include five families with distinct degrees of adaptation to an aquatic life, swimming mode and abilities that remain difficult to estimate. The lifestyle of early cetaceans is investigated by analysis of microanatomical features in postcranial elements of archaeocetes. We document the internal structure of long bones, ribs and vertebrae in fifteen specimens belonging to the three more derived archaeocete families -Remingtonocetidae, Protocetidae, and Basilosauridaeusing microtomography and virtual thin-sectioning. This enables us to discuss the osseous specializations observed in these taxa and to comment on their possible swimming behavior. All these taxa display bone mass increase (BMI) in their ribs, which lack an open medullary cavity, and in their femora, whereas their vertebrae are essentially spongious. Humeri and femora show opposite trends in microanatomical specialization in the progressive independence of cetaceans from a terrestrial environment. Humeri change from very compact to spongious, which is in accordance with the progressive loss of propulsive role for the forelimbs, which were used instead for steering and stabilizing. Conversely, hind-limbs in basilosaurids became strongly reduced with no involvement in locomotion but display strong osteosclerosis in the femora. Our study confirms that Remingtonocetidae and Protocetidae were almost exclusively aquatic in locomotion for the taxa sampled, which probably were shallow water suspended swimmers. Basilosaurids display osseous specializations similar to those of modern cetaceans and are considered more active open-sea swimmers. This study highlights the strong need for homologous sections in comparative microanatomical studies, and the importance of combining information from several bones of the same taxon for improved functional interpretation.
Integrative and Comparative Biology, Oct 29, 2016
The locomotor environment and behavior of quadrupedal mammals exert functional constraints on the... more The locomotor environment and behavior of quadrupedal mammals exert functional constraints on their limbs. Therefore long bone shapes are thought to reflect at least partially the species' locomotor ecology. Semi-aquatic species move through two media with distinct density and viscosity and their locomotor apparatus should therefore reflect a trade-off between the divergent functional constraints it faces. Adaptation to a semi-aquatic lifestyle occurred independently in otters (Lutrinae) and minks (Mustelinae). Analyzing semi-aquatic mustelids and their terrestrial relatives, we investigate long bone shape diversity, describe changes in long bone shape associated with a semi-aquatic lifestyle, and discuss the functional consequences of these shape changes. The robustness of the otter bones is highlighted and its potential ballast role discussed. Large epiphyses are observed in otters but this trend seems associated with terrestrial more than with aquatic locomotion. Thus, the most aquatic species, Enhydra lutris, presents narrow knee articulations compared to similar sized less aquatic species. Enhydra lutris presents a fore-and hind limb shape that diverge from that in other otters. Minks show bone shapes similar to each other but only Neovison vison tends to differ from its terrestrial relatives. The evolution of limb shape in this group is strongly correlated with size, locomotor mode, and phylogenetic history, leading to a morphological pattern where the roles of each of these factors are difficult to disentangle.
Uploads
Papers by Alexandra Houssaye