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.