Cross-sex genetic covariances limit the evolvability of wing-shape within and among species of Drosophila.

The independent evolution of males and females is potentially constrained by both sexes inheriting the same alleles from their parents. This genetic constraint can limit the evolvability of complex traits; however, there are few studies of multivariate evolution that incorporate cross-sex genetic covariances in their predictions. Drosophila wing-shape has emerged as a model high-dimensional phenotype; wing-shape is highly evolvable in contemporary populations, and yet perplexingly stable across phylogenetic timescales. Here, we show that cross-sex covariances in Drosophila melanogaster, given by the B-matrix, may considerably bias wing-shape evolution. Using random skewers, we show that B would constrain the response to antagonistic selection by 90%, on average, but would double the response to concordant selection. Both cross-sex within-trait and cross-sex cross-trait covariances determined the predicted response to antagonistic selection, but only cross-sex within-trait covariances facilitated the predicted response to concordant selection. Similar patterns were observed in the direction of extant sexual dimorphism in D. melanogaster, and in directions of most and least dimorphic variation across the Drosophila phylogeny. Our results highlight the importance of considering between-sex genetic covariances when making predictions about evolution on both macro- and microevolutionary timescales, and may provide one more explanatory piece in the puzzle of stasis.