Alexandra Houssaye

Bone Inner Structure Suggests Increasing Aquatic Adaptations in Desmostylia (Mammalia, Afrotheria)

Background The paleoecology of desmostylians has been discussed controversially with a general consensus that desmostylians were aquatic or semi-aquatic to some extent. Bone microanatomy can be used as a powerful tool to infer habitat preference of extinct animals. However, bone microanatomical studies of desmostylians are extremely scarce. Methodology/Principal Findings We analyzed the histology and microanatomy of several desmostylians using thin-sections and CT scans of ribs, humeri, femora and vertebrae. Comparisons with extant mammals allowed us to better understand the mode of life and evolutionary history of these taxa. Desmostylian ribs and long bones generally lack a medullary cavity. This trait has been interpreted as an aquatic adaptation among amniotes. Behemotops and Paleoparadoxia show osteosclerosis (i.e. increase in bone compactness), and Ashoroa pachyosteosclerosis (i.e. combined increase in bone volume and compactness). Conversely, Desmostylus differs from these desmostylians in displaying an osteoporotic-like pattern. Conclusions/Significance In living taxa, bone mass increase provides hydrostatic buoyancy and body trim control suitable for poorly efficient swimmers, while wholly spongy bones are associated with hydrodynamic buoyancy control in active swimmers. Our study suggests that all desmostylians had achieved an essentially, if not exclusively, aquatic lifestyle. Behemotops, Paleoparadoxia and Ashoroa are interpreted as shallow water swimmers, either hovering slowly at a preferred depth, or walking on the bottom, and Desmostylus as a more active swimmer with a peculiar habitat and feeding strategy within Desmostylia. Therefore, desmostylians are, with cetaceans, the second mammal group showing a shift from bone mass increase to a spongy inner organization of bones in their evolutionary history.

Reptilian assemblages from the latest Cretaceous – Palaeogene phosphates of Morocco: from Arambourg to present time

Arambourg was the first to conduct methodical vertebrate palaeontological studies in the Oulad Abdoun and Ganntour phosphatic basins of Morocco between the 1930s and 1950s. As early as 1935, he identified the main stratigraphical levels of the phosphatic series, characterizing them by a specific association of vertebrates (mainly selachians), and proposed stratigraphical correlations between the phosphatic levels of these two basins. During the last decade, due to a French-Moroccan program of collaboration, vertebrate fossils have been collected in great abundance. Here we present an updated overview of the latest Cretaceous to Ypresian reptilian faunas from the Oulad Abdoun and Ganntour basins, on the basis of published data and new field records. In addition to advances in the study of the already known taxa (i.e., squamates, crocodyliforms, plesiosaurs), recent field works reveal new major reptilian taxa that were unknown (or undescribed) at Arambourgs time: very abundant and diversified marine chelonians (Maastrichtian to Ypresian), scarce dinosaurs and pterosaurs remains (Maastrichtian), and a well diversified marine avifauna (Thanetian and Ypresian). A significant increase in the number of described taxa (52 versus 13) and an improvement of the quality of the specimens found (articulated skeletons versus isolated remains) is worthy of consideration. The Maastrichtian reptilian assemblages are dominated by mosasaurid squamates whereas those of the Palaeogene are by the mirroring crocodyliforms (dyrosaurids and eusuchians).

Three-dimensional pelvis and limb anatomy of the Cenomanian hind-limbed snake Eupodophis descouensi (Squamata, Ophidia) revealed by synchrotron-radiation computed laminography

ABSTRACT Cretaceous marine hind-limbed snakes are considered to be key fossils for understanding the origin and evolution of snakes. In view of the rarity of such fossils, performing new analyses on described specimens using emerging, cuttingedge techniques should bring important new insights on these forms. We investigated the three-dimensional morphology and inner architecture of the pelvic girdle and hind-limb bones of the type specimen of Eupodophis descouensi Rage and Escuillié, 2000, one of the three taxa for which at least one hind-limb is known, using synchrotron-radiation computed laminography (SRCL), a recently developed non-destructive technique that overcomes some of the limitations of synchrotron microtomography for flat, laterally extended objects. This experiment allowed a virtual exhumation of the second, hidden leg of the specimen. The morphology and proportions of the regressed pelvic and hind-limb bones of Eupodophis resemble those of the hind-limbed snakes Pachyrhachis and Haasiophis. As in Haasiophis, four tarsals are observed in each limb, but there are no traces of metatarsals or phalanges. Moreover, despite the presence of osteosclerosis and pachyostosis in the vertebrae and the ribs of Eupodophis, the inner structure of its limb bones is devoid of these osseous specializations and displays a microanatomical organization similar to that of extant terrestrial lizards. This suggests that limb regression in Eupodophis was not due to a qualitative alteration of growth but, more likely, to a local decrease in growth rate or shortening of growth duration.

An Analysis of Vertebral ‘Pachyostosis’ In Carentonosaurus Mineaui (Mosasauroidea, Squamata) from the Cenomanian (Early Late Cretaceous) of France, with Comments on its Phylogenetic and Functional Significance

Abstract The study of the so-called vertebral ‘pachyostosis’ of Carentonosaurus mineaui, a plesiopedal mosasauroid sensu Bell & Polcyn from the Cenomanian (Late Cretaceous) of Charente-Maritime (Western France), has revealed that it actually corresponds to pachyosteosclerosis resulting from the combination of cortical hyperplasy with bone compaction due to an inhibition of chondroclastic and osteoclastic activities. This characteristic also occurs in other Cretaceous squamates such as Pachyvaranus crassispondylus and Simoliophis rochebrunei but it is absent in extant squamates. On the contrary, vertebrae of the latter display a very strong porosity due to intense bone remodelling during growth. The phylogenetic significance of pachyosteosclerosis in squamates is thus discussed. The peculiar structure of the vertebrae of Carentonosaurus may be regarded as the result of a heterochronic process, more specifically neoteny. Its association with an adaptation to shallow marine environment is consistent with the inferred ecology of C. mineaui. Moreover, the histological features of the periosteal bone of Carentonosaurus vertebrae provide information about its growth pattern (asymmetry, rate, cyclicity) which may be compared to the ones of Pachyvaranus and Simoliophis.

Palaeoecological and morphofunctional interpretation of bone mass increase: an example in Late Cretaceous shallow marine squamates.

Bone mass increase (BMI; i.e. osteosclerosis with possible additional pachyostosis) is characteristically displayed by many Late Cretaceous squamates that adapted to shallow marine environments—plesiopelvic mosasauroids, stem‐ophidians and pachyophiids. A combined morphological and microanatomical analysis of vertebrae and, to a lesser extent, ribs of these fossil squamates provides new data about the distribution and variability of this osseous specialization in these taxa. Classical thin sections and third generation synchrotron microtomography and laminography were used for the microanatomical analysis. Following the explanation of the likely involvement of this specialization in the control of buoyancy, body trim and Carriers constraint, new palaeoecological inferences and new hypotheses about the locomotor abilities and life environment of these organisms are produced. The taxa displaying BMI are considered to have undertaken long dives, hovering slowly and maintaining a horizontal trim, in shallow and protected water environments. Conversely, marine stem‐ophidians deprived of this specialization are regarded as slow surface swimmers able to live in more open marine environments. This study highlights the importance of microanatomical data for palaeoecological studies. It also discusses the significance of the use of this specialization as a character in phylogenetic studies.

Microanatomical and Histological Features in the Long Bones of Mosasaurine Mosasaurs (Reptilia, Squamata) - Implications for Aquatic Adaptation and Growth Rates

Background During their evolution in the Late Cretaceous, mosasauroids attained a worldwide distribution, accompanied by a marked increase in body size and open ocean adaptations. This transition from land-dwellers to highly marine-adapted forms is readily apparent not only at the gross anatomic level but also in their inner bone architecture, which underwent profound modifications. Methodology/Principal Findings The present contribution describes, both qualitatively and quantitatively, the internal organization (microanatomy) and tissue types and characteristics (histology) of propodial and epipodial bones in one lineage of mosasauroids; i.e., the subfamily Mosasaurinae. By using microanatomical and histological data from limb bones in combination with recently acquired knowledge on the inner structure of ribs and vertebrae, and through comparisons with extant squamates and semi-aquatic to fully marine amniotes, we infer possible implications on mosasaurine evolution, aquatic adaptation, growth rates, and basal metabolic rates. Notably, we observe the occurrence of an unusual type of parallel-fibered bone, with large and randomly shaped osteocyte lacunae (otherwise typical of fibrous bone) and particular microanatomical features in Dallasaurus, which displays, rather than a spongious inner organization, bone mass increase in its humeri and a tubular organization in its femora and ribs. Conclusions/Significance The dominance of an unusual type of parallel-fibered bone suggests growth rates and, by extension, basal metabolic rates intermediate between that of the extant leatherback turtle, Dermochelys, and those suggested for plesiosaur and ichthyosaur reptiles. Moreover, the microanatomical features of the relatively primitive genus Dallasaurus differ from those of more derived mosasaurines, indicating an intermediate stage of adaptation for a marine existence. The more complete image of the various microanatomical trends observed in mosasaurine skeletal elements supports the evolutionary convergence between this lineage of secondarily aquatically adapted squamates and cetaceans in the ecological transition from a coastal to a pelagic lifestyle.

Vertebral microanatomy in squamates: structure, growth and ecological correlates

The histological study of vertebrae in extant squamates shows that the internal vertebral structure in this group differs from that of other tetrapods. Squamate vertebrae are lightly built and basically composed of two roughly concentric osseous tubes – one surrounding the neural canal and the other constituting the peripheral cortex of the vertebra – connected by few thin trabeculae. This structure, which characteristically evokes that of a tubular bone, results from a peculiar remodelling process characterised by an imbalance between local bone resorption and redeposition; in both periosteal and endosteo‐endochondral territories, bone is extensively resorbed but not reconstructed in the same proportion by secondary deposits. This process is particularly intense in the deep region of the centrum, where originally compact cortices are made cancellous, and where the endochondral spongiosa is very loose. This remodelling process starts at an early stage of development and remains active throughout subsequent growth. The growth of squamate centra is also strongly asymmetrical, with the posterior (condylar) part growing much faster than the anterior (cotylar) part. Preliminary analyses testing for associations between vertebral structure and habitat use suggest that vertebrae of fossorial taxa are denser than those of terrestrial taxa, those in aquatic taxa being of intermediate density. However, phylogenetically informed analyses do not corroborate these findings, thus suggesting a strong phylogenetic signal in the data. As our analyses demonstrate that vertebrae in snakes are generally denser than those of lizards sensu stricto, this may drive the presence of a phylogenetic signal in the data. More comprehensive sampling of fossorial and aquatic lizards is clearly needed to more rigorously evaluate these patterns.

Dental Ontogeny in Pliocene and Early Pleistocene Hominins

Until recently, our understanding of the evolution of human growth and development derived from studies of fossil juveniles that employed extant populations for both age determination and comparison. This circular approach has led to considerable debate about the human-like and ape-like affinities of fossil hominins. Teeth are invaluable for understanding maturation as age at death can be directly assessed from dental microstructure, and dental development has been shown to correlate with life history across primates broadly. We employ non-destructive synchrotron imaging to characterize incremental development, molar emergence, and age at death in more than 20 Australopithecus anamensis, Australopithecus africanus, Paranthropus robustus and South African early Homo juveniles. Long-period line periodicities range from at least 6–12 days (possibly 5–13 days), and do not support the hypothesis that australopiths have lower mean values than extant or fossil Homo. Crown formation times of australopith and early Homo postcanine teeth fall below or at the low end of extant human values; Paranthropus robustus dentitions have the shortest formation times. Pliocene and early Pleistocene hominins show remarkable variation, and previous reports of age at death that employ a narrow range of estimated long-period line periodicities, cuspal enamel thicknesses, or initiation ages are likely to be in error. New chronological ages for SK 62 and StW 151 are several months younger than previous histological estimates, while Sts 24 is more than one year older. Extant human standards overestimate age at death in hominins predating Homo sapiens, and should not be applied to other fossil taxa. We urge caution when inferring life history as aspects of dental development in Pliocene and early Pleistocene fossils are distinct from modern humans and African apes, and recent work has challenged the predictive power of primate-wide associations between hominoid first molar emergence and certain life history variables.

Transition of Eocene Whales from Land to Sea: Evidence from Bone Microstructure

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 Basilosauridae — using 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.

A New Look at Ichthyosaur Long Bone Microanatomy and Histology: Implications for Their Adaptation to an Aquatic Life

Background Ichthyosaurs are Mesozoic reptiles considered as active swimmers highly adapted to a fully open-marine life. They display a wide range of morphologies illustrating diverse ecological grades. Data concerning their bone microanatomical and histological features are rather limited and suggest that ichthyosaurs display a spongious, “osteoporotic-like” bone inner structure, like extant cetaceans. However, some taxa exhibit peculiar features, suggesting that the analysis of the microanatomical and histological characteristics of various ichthyosaur long bones should match the anatomical diversity and provide information about their diverse locomotor abilities and physiology. Methodology/Principal Findings The material analyzed for this study essentially consists of mid-diaphyseal transverse sections from stylopod bones of various ichthyosaurs and of a few microtomographic (both conventional and synchrotron) data. The present contribution discusses the histological and microanatomical variation observed within ichthyosaurs and the peculiarities of some taxa (Mixosaurus, Pessopteryx). Four microanatomical types are described. If Mixosaurus sections differ from those of the other taxa analyzed, the other microanatomical types, characterized by the relative proportion of compact and loose spongiosa of periosteal and endochondral origin respectively, seem to rather especially illustrate variation along the diaphysis in taxa with similar microanatomical features. Our analysis also reveals that primary bone in all the ichthyosaur taxa sampled (to the possible exception of Mixosaurus) is spongy in origin, that cyclical growth is a common pattern among ichthyosaurs, and confirms the previous assumptions of high growth rates in ichthyosaurs. Conclusions/Significance The occurrence of two types of remodelling patterns along the diaphysis, characterized by bone mass decrease and increase respectively is described for the first time. It raises questions about the definition of the osseous microanatomical specializations bone mass increase and osteoporosis, notably based on the processes involved, and reveals the difficulty in determining the true occurrence of these osseous specializations in ichthyosaurs.