Balancing selection via life-history trade-offs maintains an inversion polymorphism in a seaweed fly

How genetic diversity is maintained in natural populations is an evolutionary puzzle. Over time, genetic variation within species can be eroded by drift and directional selection, leading to the fixation or elimination of alleles. However, some loci show persistent variants at intermediate frequencies for long evolutionary time-scales, implicating a role of balancing selection, but studies are seldom set up to uncover the underlying processes. Here, we identify and quantify the selective pressures involved in the widespread maintenance of an inversion polymorphism in the seaweed fly Coelopa frigida, using an experimental evolution approach to estimate fitness associated with different allelic combinations. By precisely evaluating reproductive success and survival rates separately, we show that the maintenance of the polymorphism is governed by a life-history trade-off, whereby each inverted haplotype has opposed pleiotropic effects on survival and reproduction. Using numerical simulations, we confirm that this uncovered antagonism between natural and sexual selection can maintain inversion variation in natural populations of C. frigida. Moreover, our experimental data highlights that inversion-associated fitness is affected differently by sex, dominance and environmental heterogeneity. The interaction between these factors promotes polymorphism maintenance through antagonistic pleiotropy. Taken together, our findings indicate that combinations of natural and sexual selective mechanisms enable the persistence of diverse trait in nature. The joint dynamics of life history trade-offs and antagonistic pleiotropy documented here is likely to apply to other species where large phenotypic variation is controlled by structural variants.