Antiquity of forelimb ecomorphological diversity in the mammalian stem lineage (Synapsida)

Significance

Mammals and their closest fossil relatives use their shoulders and forelimbs for many functions, which is reflected by the great range of mammalian forelimb shapes. We found that forelimb shape diversity in the early mammalian lineage (Synapsida) began to increase about 270 million years ago, with the emergence of a group called Therapsida, and is accompanied by new forelimb functions. The functional diversification of therapsid forelimbs was curtailed by the Permo-Triassic mass extinction, but eventually continued as more mammal-like therapsids evolved new ecologies. Our analyses characterize the deep time origin of a quintessential part of the mammalian body plan: evolutionarily labile forelimbs that can be deployed in a wide range of functional and ecological roles.

Abstract

Mammals and their closest fossil relatives are unique among tetrapods in expressing a high degree of pectoral girdle and forelimb functional diversity associated with fully pelagic, cursorial, subterranean, volant, and other lifestyles. However, the earliest members of the mammalian stem lineage, the “pelycosaur”-grade synapsids, present a far more limited range of morphologies and inferred functions. The more crownward nonmammaliaform therapsids display novel forelimb morphologies that have been linked to expanded functional diversity, suggesting that the roots of this quintessentially mammalian phenotype can be traced to the pelycosaur–therapsid transition in the Permian period. We quantified morphological disparity of the humerus in pelycosaur-grade synapsids and therapsids using geometric morphometrics. We found that disparity begins to increase concurrently with the emergence of Therapsida, and that it continues to rise until the Permo-Triassic mass extinction. Further, therapsid exploration of new regions of morphospace is correlated with the evolution of novel ecomorphologies, some of which are characterized by changes to overall limb morphology. This evolutionary pattern confirms that nonmammaliaform therapsid forelimbs underwent ecomorphological diversification throughout the Permian, with functional elaboration initially being more strongly expressed in the proximal end of the humerus than the distal end. The role of the forelimbs in the functional diversification of therapsids foreshadows the deployment of forelimb morphofunctional diversity in the evolutionary radiation of mammals.