The crocodylian skull and osteoderms: A functional exaptation to ectothermy?

The crocodylians are ectothermic semi-aquatic vertebrates which are assessed to have evolved from endothermic terrestrial forms during the Mesozoic. Such a physiological transition should have involved modifications in their cardio-vascular system allowing to increase the heat transfers with the surrounding environment by growing a peripheral vascularization which would be mainly located in the dermal skeleton: the dermatocranium and the osteoderms. In order to assess the implication of these anatomical regions in thermal exchanges, we have recorded the temperature above a set of representative skin areas in order to draw comparisons between the skull, the osteoderms, and the rest of the body parts which present either none or residual dermal ossification. We computed the data after the specimens were successively laid in different stereotyped environmental conditions which involved significant variations in the environmental temperature. Our results show that the osteoderms collect the external heat during the basking periods as they become significantly warmer than the surrounding skin; they further release the heat into the core of the organism as they turn out to be colder than the surrounding skin after a significant cooling period. In disregard of the environmental temperature variations, the skull table (which encloses the braincase) remains warmer than the rest of the cranial regions and shows less temperature variations than the osteoderms; a result which has lead us to think that the braincase temperature is monitored and controlled by a thermoregulatory system. Therefore, as hypothesized by previous authors regarding the ectothermic diapsids, we assume that the crocodylian skull possesses shunting blood pathways which tend to maintain both the braincase and the main sensory organs at the nearest to the optimal physiological temperature depending on the external temperature variations. Concerning the skin vascularization, the study of an albino Alligator mississippiensis specimen permitted to observe the repartition of the superficial blood vessels by transparency through the skin. We thus testify that the skin which covers either the skull or the osteoderms is more vascularized than the skin which does not present any subjacent dermal ossification. We consequently deduce that the significant contrast in the thermal behavior between the dermal skeleton and the rest of the body is indeed correlated with a difference in the relative degree of skin vascularization. This last assessment confirms that the development of the dermal skeleton should have played a functional role in the crocodylian transition from endothermy to ectothermy through the set-up of a peripheral vessel network.

Vascularization in Ornamented Osteoderms: Physiological Implications in Ectothermy and Amphibious Lifestyle in the Crocodylomorphs?

Vascularization in the core of crocodylian osteoderms, and in their superficial pits has been hypothesized to be a key feature involved in physiological thermoregulation and/or acidosis buffering during anoxia (apnea). However, up to now, there have been no quantitative data showing that the inner, or superficial, blood supply of the osteoderms is greater than that occurring in neighboring dermal tissues. We provide such data: our results clearly indicate that the vascular networks in both the osteoderms and the pits forming their superficial ornamentation are denser than in the overlying dermis. These results support previous physiological assumptions and indicate that vascularization in pseudosuchian (crocodylians and close relatives) ornamented osteoderms could be part of a broad eco-physiological adaptation towards ectothermy and aquatic ambush predation acquired by the crocodylomorphs during their post-Triassic evolution. Moreover, regressions demonstrate that the number of enclosed vessels is correlated with the sectional area of the cavities housing them (superficial pits and inner cavities). These regressions can be used to infer the degree of vascularization on dry and fossilized osteoderms and thus document the evolution of the putative function of the osteoderms in the Pseudosuchia. Anat Rec, 2017. © 2017 Wiley Periodicals, Inc. Anat Rec, 301:175-183, 2018. © 2017 Wiley Periodicals, Inc.

Heterochronic patterns in primate evolution: evidence from endochondral ossification.

Heterochrony (evolutionary modifications in developmental timing and/or rates) is widely recognized as an important agent of morphological change. The adaptive significance of heterochronic changes might lie either in the advantages of the derived morphologies (organ size and shape) or the derived growth parameters themselves (rate and duration of growth). We have tested these hypotheses by comparing the growth rate, the duration of growth and the relative length of the adult tibia in Primates in a phylogenetic context. We report an evolutionary decrease in growth rates (paedochronocline) and an increase in the duration of growth (perachronocline), lying in the cline from the last common ancestor of Primates, passing through the last common ancestor of Haplorhini, that of Catarrhini, to the last common ancestor of the Hominidae. However, the variation in the relative length of the adult tibia does not show any phylogenetic pattern. The derived growth parameters in themselves (slower rate, longer duration) would be of adaptive significance and they would have been selected because a prolonged learning period prior to maturity conferred advantage. The proximate (developmental) causation of differences in bone growth rate were also investigated and it was found that cell production rate in the growth plates rather than the chondrocyte size, underlies the variation in bone growth rate.

Spreading, proliferation, and differentiation of the epidermis after wounding a cichlid fish, Hemichromis bimaculatus.

A large superficial wound has been experimentally provoked in the cichlid fish Hemichromis bimaculatus to study the interactions between the epidermal cells and the substrate on which they spread, on the one hand, and the restoration of the subepidermal tissues and the epithelial-mesenchymal interactions preceding scale regeneration, on the other hand. The re-epithelialization process, e.g., migration, spreading, differentiation, and proliferation of the epidermal cells, has been followed step by step, using light, scanning and transmission electron microscopy, and tritiated thymidine incorporation, until complete reorganization of the healing epidermis. Wound healing is fast (500 microm/hr) and proceeds centripetally from the wound margins. The epidermal cells spread on a wound surface which is composed of two different matrices: the remains of basement membrane materials covering the scale-pockets, and collagen fibrils of cut dermal strips. Even though both matrices favour cell spreading and attachment, migrating cells show a different behaviour. The re-epithelialization of the wound follows an orderly sequence similar to amphibian and mammalian wound healing, i.e., a "leap frog" mechanism of cell locomotion involving three epidermal layers. The basal layer cells, which spread on the substrate, and the superficial layer cells which protect the epidermis, differentiate first. Whatever the type of substrate over which the epithelium spreads (basement membrane material or collagen fibrils), the epidermal basal layer cells differentiate as soon as they become attached. The incorporation of tritiated thymidine has revealed that there is no proliferation in the healing epidermis until after complete closure of the wound, but that the rapid re-epithelialization of the large surface requires the recruitment of epidermal cells at the wound margins. The present study offers new data on the dynamics of re-epithelialisation and on the resistance of cichlid skin to such wounds. It is also clearly shown that the epidermal basal layer cells differentiate rapidly, a step which is interpreted as the first stage of epithelial-mesenchymal interactions that will lead to scale regeneration.

Scale development in zebrafish (Danio rerio).

In the course of an extensive comparative, structural and developmental study of the cranial and postcranial dermal skeleton (teeth and scales) in osteichthyan fishes, we have undertaken investigations on scale development in zebrafish (Danio (Brachydanio) rerio) using alizarin red staining, and light and transmission electron microscopy. The main goal was to know whether zebrafish scales can be used as a model for further research on the processes controlling the development of the dermal skeleton in general, especially epithelial-mesenchymal interactions. Growth series of laboratory bred specimens were used to study in detail: (1) the relationship of scale appearance with size and age; (2) the squamation pattern; and (3) the events taking place in the epidermis and in the dermis, before and during scale initiation and formation, with the aim of searching for morphological indications of epithelial-mesenchymal interactions. Scales form late in ontogeny, generally when zebrafish are more than 8.0 mm in standard length. Within a population of zebrafish of the same age scale appearance is related to standard length, but when comparing populations of different age the size of the fish at scale appearance is also related to age. Scales always appear first in the posterior region of the body and the squamation then extends anteriorly. Scales develop in the dermis but closely apposed to the epidermal-dermal boundary. Cellular modifications occurring in the basal layer of the epidermis and in the dermis before scale formation clearly indicate that the basal epidermal cells differentiate first, before any evidence of differentiation of the progenitors of the scale-forming cells in the dermis. This strongly suggests that scale differentiation could be initiated by the epidermal basal layer cells which probably produce a molecular signal towards the dermis below. Subsequently dermal cells accumulate close to the epidermis, and differentiate to form scale papillae. The late formation of the scales during ontogeny is due to a late colonisation of the dermis by the progenitors of the scale-forming cells. Because of their late formation during ontogeny and of their regular pattern of development, scales in zebrafish represent a good model for further investigations on the general mechanisms of epithelial-mesenchymal interactions during dermal skeleton development, and in particular for the study of the gene expression patterns.