From constraint to opportunity: Relaxing sexual antagonism reveals adaptive potential maintained by balancing selection

Abstract

Despite ongoing selection, genetic variation in fitness-related traits often persists. Balancing selection can maintain polymorphisms through genetic trade-offs, including those between the sexes. Sexually antagonistic (SA) selection is challenging to detect at the genomic level and its broader evolutionary importance, especially for complex traits, remains unclear. To investigate this, we conducted an evolve-and-resequence experiment in Callosobruchus maculatus, manipulating the strength of SA trade-offs over body size and tracking genome-wide responses. When selection simultaneously favored larger females and smaller males, allele frequency changes were constrained and genome-wide divergence remained limited. In contrast, relaxing SA trade-offs by selecting on only one sex led to large, repeatable allele frequency shifts. These loci also showed signatures of long-term balancing selection in the ancestral population. Together, our results demonstrate that SA trade-offs can act both as a constraint, limiting sex-specific responses under antagonistic selection pressures, but also as a source of adaptive potential once antagonism is relaxed.