Can the Z:A ratio serve as a genomic index of sexual selection? An assessment across space and time in a genus of lekking birds

Abstract

Understanding the role of sexual selection in shaping evolutionary trajectories is a key goal of biology, and thus developing a genomic measure of sexual selection strength is desirable. In systems with ZW sex determination, the ratio of nucleotide diversity ({pi}) on the male-biased Z chromosome to that on the autosomes (the Z:A ratio) is expected to decline as male effective population size decreases under strong sexual selection, offering one such measure. However, non-equilibrium processes other than sexual selection (e.g., hybridization, changes in population size) can influence levels of Z-linked diversity relative to the rest of the genome, complicating interpretation of this metric and necessitating a systematic evaluation of how Z:A ratios vary across known demographic and selective circumstances. We leveraged longitudinal sampling over a [~]25-year period in Manacus manakin populations in western Panama, spanning a mainland transect (including M. candei, M. vitellinus, and their hybrid zone) and insular populations of the Bocas del Toro Archipelago. On the mainland, Z:A ratios were temporally stable within populations, but varied across populations: (1) Z:A ratios were lower in M. vitellinus than M. candei, likely due to stronger sexual selection in the former; and (2) Z:A ratios increased at the hybrid zone center, likely due to fast-Z effects in parentals inflating Z:A ratios in recent hybrids. Island populations exhibited significantly lower Z:A ratios than mainland populations, consistent with theoretical expectations of Z:A reductions following population contractions as the islands became isolated. Insular Z:A ratios increased with proximity to other landmasses, suggesting gene flow mitigates these effects in this system. While the Z:A ratio behaved predictably in relation to known non-equilibrium processes, our results demonstrate the potentially strong effects of demographic history and admixture on Z-linked diversity, which should be considered in studies aiming to use the Z:A ratio as a measure of sexual selection.