Role-reversed polyandry is associated with faster fast-Z in shorebirds

Abstract

In birds, males are homogametic and carry two copies of the Z chromosome (‘ZZ’), while females are heterogametic and exhibit a ‘ZW’ genotype. The Z chromosome evolves at a faster rate than similarly sized autosomes, a phenomenon termed ‘fast-Z evolution’. This is thought to be caused by two independent processes—greater Z chromosome genetic drift owing to a reduced effective population size, and stronger Z chromosome positive selection owing to the exposure of partially recessive alleles to selection. Here, we investigate the relative contributions of these processes by considering the effect of role-reversed polyandry on fast-Z in shorebirds, a paraphyletic group of wading birds that exhibit unusually diverse mating systems. We find stronger fast-Z effects under role-reversed polyandry, which is consistent with particularly strong selection on polyandrous females driving the fixation of recessive beneficial alleles. This result contrasts with previous research in birds, which has tended to implicate a primary role of genetic drift in driving fast-Z variation. We suggest that this discrepancy can be interpreted in two ways—stronger sexual selection acting on polyandrous females overwhelms an otherwise central role of genetic drift, and/or sexual antagonism is also contributing significantly to fast-Z and is exacerbated in sexually dimorphic species.