The X chromosome is a hot spot for sexually antagonistic fitness variation

TLDR

Sexually antagonistic alleles are selected discordantly between sexes and are abundant in the Drosophila melanogaster genome. Theory predicts that the X chromosome will be enriched with this type of variation. To test this prediction, the authors sampled and cytogenetically cloned 20 X chromosomes and compared their fitness variation to genome-wide levels. At the juvenile stage the X chromosome contributed no detectable fitness variation, but at the adult stage it harbored 45 % of genome‑wide fitness variation and 97 % of sexually antagonistic variation, implying that X‑linked antagonism drives negative intersexual heritability and that high‑fitness males produce low‑fitness daughters.

Abstract

Sexually antagonistic alleles are selected discordantly between the sexes. Experimental evidence indicates that sexually antagonistic fitness variation is abundant in the genome of Drosophila melanogaster. Theory predicts that the X chromosome will be enriched with this type of variation. To test this prediction in D. melanogaster, we sampled, and cytogenetically cloned, 20 X chromosomes and compared their fitness variation to genome-wide levels. At the juvenile stage, in which gender roles are most similar, the X chromosome made no detectable contribution to genome-wide fitness variation. At the adult stage, in which gender roles diverge, the X chromosome was estimated to harbour 45% of the genome-wide fitness variation and 97% of the genome-wide sexually antagonistic variation. This genomic structure has important implications for the process of sexual selection because X-linked sexually antagonistic variation contributes to negative intersexual heritability for fitness, i.e. high-fitness males (females) produce, on average, low-fitness daughters (sons).