The evolution of sexual dimorphism and its genetic underpinnings

Abstract: Sexual dimorphism often constitutes the largest phenotypic variance within species but it is puzzling how sexual dimorphisms evolve because most of the genome is shared between the sexes. Sexually antagonistic (SA) selection on a shared genome sets the stage for intralocus sexual conflict. In this thesis, I investigate the genetic basis of sexual size dimorphism (SSD) in the seed beetle Callosobruchus maculatus to understand which mechanisms facilitate sex-specific trait evolution. I combine quantitative genetics with artificial selection to examine how shared and sex-specific genetic variances dictate the evolvability of SSD under different forms of selection and test the hypothesis that SA selection maintains shared genetic variance while fueling the evolution of increased sex differences. Using genomic approaches, I identify the Y chromosome in C. maculatus, investigate how it contributes to SSD, and explore signatures of sex-specific dominance in gene expression as a potential mechanism to alleviate sexual conflict.While both sexes largely share autosomal genetic variance underlying body size, I find significant differences in dominance and sex-linked additive genetic variances that facilitate rapid responses in SSD to male-limited and especially SA selection. Compared to sex-limited directional selection, SA selection maintains more additive and particularly female specific dominance genetic variance. Further, I detect sex-specific dominance in expression of genes associated with SA traits in C. maculatus. These results are compatible with predictions that sex-specific dominance may be central to maintaining genetic variance under, and evolve in response to, SA selection.Despite its degeneration, Y-linked additive genetic variance has a large effect on male size, mirrored in rapid male limited responses to artificial selection, which depleted Y-linked genetic variance. Isolating the effect of the Y chromosome by introgressing different Y lineages into an isogenic background, reveals two distinct Y haplotypes responsible for changing SSD by 30%. Long-read sequencing and assembling the majority of the previously unknown Y chromosome in C. maculatus identified that – while both sexes share an autosomal deeply conserved eukaryotic growth regulator target of rapamycin (TOR) – males carry additional TOR copies on the Y chromosome, which to our knowledge is the first description of TOR on a sex chromosome. This suggests that male specific regulation of growth through a private TOR underlies the overall sexual size dimorphism in C. maculatus. In accordance with this, I identify TOR copy number variation between the Y haplotypes, where the Y haplotype associated with the more pronounced SSD harbors two additional TOR copies.