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.

A proposed standard for quantifying 3‐D hindlimb joint poses in living and extinct archosaurs

“…First, unfused distal tarsals are excluded from ACS creation. Given current uncertainty about the contribution of distal tarsals to ankle movement in extant crocodylians and their variable preservation, ossification, and fusion in fossils (Cruickshank, 1979 ; Holtz, 1995 ; Müller & Alberch, 1990 ; Ossa‐Fuentes et al, 2022 ; Padian, 2017 ; Sullivan, 2010 ), we use only the metatarsals. Second, we drop our preference for strict homology.…”

“…Calculation of an ACS for the guineafowl tarsometatarsus is relatively straightforward, following the same approach employed previously. A plane can be fit to Given current uncertainty about the contribution of distal tarsals to ankle movement in extant crocodylians and their variable preservation, ossification, and fusion in fossils (Cruickshank, 1979;Holtz, 1995;Müller & Alberch, 1990;Ossa-Fuentes et al, 2022;Padian, 2017;Sullivan, 2010), we use only the metatarsals.…”

Inner workings of the alligator ankle reveal the mechanistic origins of archosaur locomotor diversity

“…(c) Right ankles from example fossil taxa preliminarily placed into each complex. Illustrations modified from Allosaurus (Madsen, 1976; Ossa‐Fuentes et al, 2022), Asilisaurus (Nesbitt et al, 2020); Dinornis (Bishop et al, 2019; Farlow et al, 2014), Euparkeria (Ewer, 1965), Hallopus (Walker, 1970), Ingenia (Osmólska et al, 2004), Marasuchus (Sereno & Arcucci, 1994), Numida (Turner et al, 2020), Parasuchus (Padian et al, 2010); Poposaurus (Farlow et al, 2014; Schachner et al, 2020); Postosuchus (Peyer et al, 2008; Weinbaum, 2013); Protosuchus (Colbert et al, 1951); Tawa (Nesbitt et al, 2009); Teleocrater (Nesbitt, Butler, Ezcurra, Barrett, et al, 2017; Nesbitt, Butler, Ezcurra, Charig, et al, 2017); Terrestrisuchus (Crush, 1984); Ticinosuchus (Farlow et al, 2014). All diagrams and illustrations are in dorsal view.…”

Beyond recapitulation: Past, present, and future

“…The evolution of avian distal ankle developmental processes, as revealed by Ossa‐Fuentes et al (2020), suggests a potential role of developmentally transient patterns in evolution. By using experimental and paleontological data, they conclude that the distal ankle in modern birds has a single large distal cartilage, which arises from the fusion of three distal tarsals during embryogenesis.…”