A primary role of developmental instability in sexual selection

Abstract

In evolutionary biology, fluctuating asymmetry (FA) is thought to reveal developmental instability (DI, inability to buffer development against perturbations), but its adaptive and genetic bases are being debated. In other fields, such as human clinical genetics, DI is being assessed as incidence of minor morphological abnormalities (MMAs) and used to predict certain fitness outcomes. Here, for the first time, we combine these complementary measures of DI in sexual selection and quantitative genetic studies of a natural population. Comprehensive multivariate analyses demonstrate that FA and MMAs in a condition-dependent sexual ornament, the male Drosophila bipectinata sex comb used in courtship, are sole significant targets of selection favouring their reduced expression in New Caledonia. Comb FA and MMAs are positively correlated, confirming that each are linked to a common buffering system. Ornament size and DI (as FA and MMAs) are positively correlated, genetically and phenotypically, contrary to theoretical expectation of negative size-FA scaling under the assumption that FA reveals overall genetic quality. There exists significant additive genetic variance for MMAs, demonstrating their evolutionary potential. Ornament DI in New Caledonia is markedly elevated compared with populations where such selection was not detected, suggesting that the increased population-level DI is capacitating adaptive evolution.