Adaptive landscapes unveil the complex evolutionary path to mammalian forelimb function and posture

Abstract

AbstractThe ‘sprawling-parasagittal’ postural transition is a key part of mammalian evolution, associated with sweeping reorganization of the postcranial skeleton in mammals compared to their forebears, the non-mammalian synapsids. However, disputes over forelimb function in fossil synapsids render the precise nature of the ‘sprawling-parasagittal’ transition controversial. We shed new light on the origins of mammalian posture, using evolutionary adaptive landscapes to integrate 3D humerus shape and functional performance data across a taxonomically comprehensive sample of fossil synapsids and extant comparators. We find that the earliest pelycosaur-grade synapsids had a unique mode of sprawling, intermediate between extant reptiles and monotremes. Subsequent evolution of synapsid humerus form and function showed little evidence of a direct progression from sprawling pelycosaurs to parasagittal mammals. Instead, posture was evolutionarily labile, and the ecological diversification of successive synapsid radiations was accompanied by variation in humerus morphofunctional traits. Further, synapsids frequently evolve towards parasagittal postures, diverging from the reconstructed optimal evolutionary path; the optimal path only aligns with becoming increasingly mammalian in derived cynodonts. We find the earliest support for habitual parasagittal postures in stem therians, implying that synapsids evolved and radiated with distinct forelimb trait combinations for most of their recorded history.