Developmental evolution of the distal ankle in the dinosaur–bird transition

Abstract

The adult ankle of early reptiles had five distal tarsal (dt) bones, but in Dinosauria, these were reduced to only two: dt3 and dt4, articulated to metatarsals (mt) mt3 and mt4. Birds have a single distal tarsal ossification center that fuses to the proximal metatarsals to form a new adult skeletal structure: the composite tarsometatarsus. This ossification center develops within a single large embryonic cartilage, but it is unclear if this cartilage results from fusion of earlier cartilages. We studied embryos in species from four different bird orders, an alligatorid, and an iguanid. In all embryos, cartilages dt2, dt3, and dt4 are formed. In the alligatorid and the iguanid, dt2 failed to ossify: only dt3 and dt4 develop into adult bones. In birds, dt2, dt3, and dt4 fuse to form the large distal tarsal cartilage; the ossification center then develops above mt3, in cartilage presumably derived from dt3. During the entire dinosaur–bird transition, a dt2 embryonic cartilage was always formed, as inferred from the embryology of extant birds and crocodilians. We propose that in the evolution of the avian ankle, fusion of cartilages dt3 and dt2 allowed ossification from dt3 to progress into dt2, which began to contribute bone medially, while fusion of dt3 to dt4 enabled the evolutionary loss of the dt4 ossification center. As a result, a single ossification center expands into a plate-like unit covering the proximal ends of the metatarsals, that is key to the development of an integrated tarsometatarsus.