Growth plate formation and development in alligator and mouse metapodials: evolutionary and functional implications

Abstract

Mammalian metapodials (metacarpals and metatarsals), unlike most long bones, form a single growth plate, and undergo longitudinal growth at only one end. The growth dynamics of non-mammalian tetrapod metapodials have not been systematically examined in order to determine if unidirectional growth is unique to mammals. Here we compare murine metapodial ossification in growth stages that parallel those of embryonic, juvenile and subadult American alligators (Alligator mississippiensis). Safranin O staining was used for qualitative histology, and chondrocyte differentiation and proliferation were assessed via immunohistochemistry for type X collagen and proliferative cell nuclear antigen (PCNA). We establish that growth plates form at both ends of alligator metapodials and are maintained in the subadult. PCNA results show that alligators and mice share common patterns of chondrocyte proliferation during growth plate formation. In addition, while alligators and mice differ initially in the degree of organization and pace of chondrocyte differentiation, these parameters are largely similar in established growth plates. However, the replacement of cartilage by bone is highly irregular throughout growth in the alligator, in contrast to the more uniform process in the mouse. These results indicate that while alligators and mammals share common mechanisms of chondrocyte regulation, they differ substantially in their processes of ossification. Phylogenetic analysis indicates that the direct ossification of one epiphysis and reliance on a single growth plate is a derived character (synapomorphy) in therian mammals and likely indicates an adaptation for erect quadrupedal gait.

Regulation of articular chondrocyte proliferation and differentiation by indian hedgehog and parathyroid hormone–related protein in mice

“…In addition to the ancient and embryonic iterations of the chondroepiphyseal growth zones, there exists a lesser-known iteration that occupies one end of the short bones of the hands and feet (8,9,20). Whether these short-bone chondroepiphyses represent a persistence of the primitive structure or evolved secondarily is unclear, but they phenocopy the ancient chondroepiphysis in every detail and might therefore serve as a model system of what a primitive joint structure might have been like.…”

Patterns of correlation and covariation of anthropoid distal forelimb segments correspond to Hoxd expression territories

“…Exactly where the first metacarpal falls with respect to these Hox expression domains is presently unclear. Although it is certainly possible that it lies within either the same domain as the remainder of digit one or that of the four posterior digits, it is equally possible that this morphologically distinct metacarpal, whose growth plate is unique in being proximal rather than distal in mammals (Reno et al, 2007), expresses a unique combination of Hox genes altogether. The Hox expression patterns described above suggest the existence of several potential distal forelimb growth modules (Fig.…”

“…As noted above, the mammalian MC1 has a unique structure. Unlike its posterior counterparts, its physis is proximal in mammals rather than distal (Reno et al, 2007), and therefore lies in the immediate proximity of the carpus. The first ray always exhibits a maximum of two phalanges, but very often in those cases in which it suffers distinct involution (e.g., Ateles, Colobus and hallux of Pongo), the effects of such reduction are far more dramatic in its phalanges than its metacarpal-which can sometimes remain large and robust (even though subcutaneous) within the palm, despite the loss of its phalanges.…”

Combining Prehension and Propulsion: The Foot of Ardipithecus ramidus

“…This is especially the case for eutherian tarsometatarsal joints, which appear to have sacrificed their proximal metapodial growth plate to encourage a more rigid syndesmosis (38). The markedly rugose tarsometatarsal joint capsule in the Ar.…”