Y-linked copy number polymorphism of target of rapamycin (TOR) is associated with sexual size dimorphism in seed beetles

Abstract

AbstractThe Y chromosome is theorized to facilitate evolution of sexual dimorphism by accumulating sexually antagonistic loci, but empirical support is scarce. Due to the lack of recombination Y chromosomes are prone to degenerative processes, which poses a constraint on their adaptive potential. Yet, in the seed beetleCallosobruchus maculatussegregating Y linked variation affects male body size and thereby sexual size dimorphism (SSD). Here we assembleC. maculatussex chromosome sequences and identify molecular differences associated with Y-linked SSD variation. The assembled Y chromosome is largely euchromatic and contains over 400 genes, many of which are ampliconic with a mixed autosomal and X chromosome ancestry. Functional annotation suggests that the Y chromosome plays important roles in males beyond primary reproductive functions. Crucially, we find that, besides an autosomal copy of the genetarget of rapamycin(TOR), males carry an additionalTORcopy on the Y chromosome. TOR is a conserved regulator of growth across taxa, and our results suggest that a Y-linkedTORprovides a male specific opportunity to alter body size. A comparison of Y haplotypes associated with male size difference uncovers a copy number variation forTOR, where the haplotype associated with decreased male size, and thereby increased sexual dimorphism, has two additionalTORcopies. This suggests that sexual conflict over growth has been mitigated by autosome to Y translocation ofTORfollowed by gene duplications. Our results reveal that despite of suppressed recombination, the Y chromosome can harbour adaptive potential as a male-limited supergene.