Conserved covariance structure underlies 60 million years of morphological diversification in primates

Abstract

Evolvability, the capacity of populations to respond to selection, is shaped by the structure and amount of variation transmitted from generation to generation. Whether the heritable covariance structure itself remains stable or evolves rapidly is a central, yet unresolved, question in phenotypic evolution. Competing hypotheses suggest that trait covariation may be constrained by developmental and genetic architectures or, alternatively, reshaped by persistent directional selection. Here, we test whether covariance structure and evolvability are stable over macroevolutionary timescales by applying a comparative evolutionary quantitative genetics framework on primates. We quantified cranial variation using over ten thousand specimens representing 309 species and compared phenotypic covariance matrices for 57 genera within a Bayesian framework. Our results show that despite extensive morphological divergence, primates show remarkably conserved patterns of variation, modular organization, and capacity to respond to selection. Reconstruction of selection gradients across the primate radiation revealed that selection was highly structured, with preferential directions aligned with major axes of cranial variation. These results suggest that the stability of evolvability does not reflect evolutionary stasis, but rather emerges from the alignment between conserved developmental architecture and selection. Our findings demonstrate that covariance structure and the evolutionary potential it provides can persist over deep evolutionary timescales, providing a mechanistic framework for understanding how developmental systems shape the trajectories of major radiations.