Adaptive Patterns in Aquatic Amniote Bone Microanatomy—More Complex than Previously Thought

Abstract

Numerous amniote groups adapted to an aquatic life. This change of habitat naturally led to numerous convergences. The various adaptive traits vary depending on the degree of adaptation to an aquatic life, notably between shallow water taxa still able to occasionally locomote on land and open-marine forms totally independent from the terrestrial environment, but also between surface swimmers and deep divers. As a consequence, despite convergences, there is a high diversity within aquatic amniotes in e.g., shape, size, physiology, swimming mode. Bone microanatomy is considered to be strongly associated with bone biomechanics and is thus a powerful tool to understand bone adaptation to functional constraints and to make functional inferences on extinct taxa. Two opposing major microanatomical specializations have been described in aquatic amniotes, referred to as bone mass increase and a spongious organization, respectively. They are assumed to be essentially linked with the hydrostatic or hydrodynamic control of buoyancy and body trim and with swimming abilities and velocity. However, between extremes in these specializations, a wide range of intermediary patterns occurs. The present study provides a state-of-the-art review of these inner bone adaptations in semi-aquatic and aquatic amniotes. The analysis of the various microanatomical patterns observed in long bones, vertebrae, and ribs of a large sample of (semi-)aquatic extant and extinct amniotes reveals the wide diversity in microanatomical patterns and the variation in combination of these different patterns within a single skeleton. This enables us to discuss the link between microanatomical features and habitat, swimming abilities, and thus functional requirements in the context of amniote adaptation to an aquatic lifestyle.

3D quantitative comparative analysis of long bone diaphysis variations in microanatomy and cross‐sectional geometry

“…The strong link with size for Zpol was already highlighted in previous studies (Houssaye et al. ; the other parameters that correlate with size were not measured in previous studies). The removal of these variables showed a relatively similar impact and relationships of and between all other parameters, but this time with no strong allometry (as highlighted by a nonsignificant correlation of the axes with size) on the two first axes of PCAs, which express a very high percentage of the total variance.…”

“…; Houssaye et al. , b). The bones sampled come from 15 mammalian species chosen with the aim of illustrating various ecologies (terrestrial, semi‐aquatic, fossorial, arboreal), morphologies and sizes, with a wide distribution across mammal phylogeny (Table ).…”

“…; Houssaye et al. , b) but also, to a much smaller extent, on a few longitudinal ones (Nakajima et al. ; Houssaye et al.…”

Vertebral bone microarchitecture and osteocyte characteristics of three toothed whale species with varying diving behaviour

“…Bone histomorphometric analyses revealed that the trabecular composition of the vertebral bodies is similar to that of other mammalian species and presents typical fibrolamellar bone and a unique and size-dependent trabecular organisation 11, 18 . In general, two major functional adaptations have been identified in vertebrates adapted to aquatic life, depending on the functional requirements: increased bone mass (i.e., osteosclerosis) and pronounced spongious organisation 19 . Previous studies on extinct mosasauroids have shown that adaptations to aquatic life are not always consistent with the overall bone mass increase or decrease and may be more closely associated with a peculiar trabecular microarchitecture that varies depending on the size of the species 20 .…”

A case study of developmental palaeontology in <i>Stereosternum tumidum</i> (Mesosauridae, Parareptilia)

“…Such a phenomenon has been demonstrated for secondarily aquatic skinks . Microanatomical analyses would help shed light on its internal strength parameters, such as bone density and cortical thickness (Houssaye et al, 2016), but are not possible with the present natural mold. Unfortunately, because no metacarpals are preserved, no predictions can be made about such a pattern in the autopodia.…”