Sexual conflict, directional sexual selection and phenotypic plasticity jointly drive the evolution of extreme phenotypic variation

How broad phenotypic variation is maintained in natural populations in the face of selection is a central question in evolutionary biology. We address this question in the water strider Microvelia longipes, where males exhibit striking variation in rear leg length used in male-male contests for dominance. Using reaction norm experiments on inbred lines, we demonstrate that phenotypic plasticity contributes to expanding phenotypic variation, but requires high genetic variation to generate the broad range of trait expression observed in natural populations. Experimental evolution favouring trait exaggeration revealed that directional sexual selection not only fails to erode variation of male rear leg length, but rather amplifies it beyond the natural distribution. Additionally, male-limited selection in favour of dominance generated substantial fecundity costs in females, underscoring the role of sexual conflict driven by females in constraining exaggerated secondary sexual traits in males. Our findings show that sexually antagonistic selection and directional sexual selection jointly generate high genetic variation, which phenotypic plasticity inflates into broad phenotypic distribution of male weapon size. This provides an empirical explanation for the high variability of male exaggerated weapons in nature.