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

Abstract

The 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.TORis 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.

Ecology, the pace‐of‐life, epistatic selection and the maintenance of genetic variation in life‐history genes

“…Structural POL loci may also involve copy number variants of coding genes. A recent potential example is the polymorphism in copy number of TOR located on the Y-chromosome of seed beetles (Kaufmann et al, 2023). Two alternative Y haplotypes (single TOR copy and three TOR copies) segregate in at least one natural population and have very pronounced effects on male body size (Kaufmann et al, 2021) and growth rate (Kaufmann et al, 2023).…”

“…A recent potential example is the polymorphism in copy number of TOR located on the Y-chromosome of seed beetles (Kaufmann et al, 2023). Two alternative Y haplotypes (single TOR copy and three TOR copies) segregate in at least one natural population and have very pronounced effects on male body size (Kaufmann et al, 2021) and growth rate (Kaufmann et al, 2023). Interestingly, TOR is a major LH gene showing signs of balancing selection in other systems (see below) and Y polymorphism in seed beetles may thus reflect balancing selection though NFDS, which apparently contributes to the maintenance of Y polymorphism in some other taxa (e.g.…”