Evolutionary age predicts sex-biased expression of paralogs in the seed beetle Callosobruchus maculatus

Sammanfattning

Sexually antagonistic selection arises when male and female reproductive interests diverge. Gene duplications have been proposed to alleviate conflicting selection on the same locus (intralocus sexual conflict) by allowing paralogs to evolve divergent sex-biased expression. In addition, the expansion of gene families with sex-biased expression may also create new targets for sexually antagonistic interactions (interlocus sexual conflict). Studying sex-biased gene expression dynamics of paralogs thus provides insights for how sexual conflict might be resolved through gene duplications. This thesis has explored sex-biased expression of paralogs across evolutionary time in the seed beetle Callosobruchus maculatus. First, we evaluated three transcript quantification approaches on this highly repetitive genome, showing that the quasi-mapping method Salmon is a justifiable alternative to classic genome alignment software for studies of paralogs in repeat-rich assemblies. Second, we developed a phylogenetically informed framework that integrates differential expression analyses with orthology inference across a Coleoptera phylogeny of 13 species, rooted with Drosophila as an outgroup. By utilizing OrthoFinder resolved gene trees, each duplication event was mapped to its corresponding species tree node, which allowed each paralog to be assigned a phylogenetic age rank, placing it on an evolutionary timeline shared across the phylogeny. We show that the pattern of sex-biased paralog expression increases notably during specific windows of time: Paralogs originating from duplication events following the Tenebrionoidea-Chrysomeloidea/Curculionoidea divergence show elevated sex-biased expression and are disproportionately male-biased. This pattern is driven by the emergence of novel male-biased gene family expansions in the Bruchinae/Curculionidae lineage. GO-term analysis points to detoxification and xenobiotic metabolism as the dominant biological functions in these gene families, consistent with adaptation to the chemical defences of seed host plants. We further show that gene families rarely contain both male- and female-biased paralogs, implying that the classic prediction that gene duplication resolves intralocus sexual conflict applies only to a small minority of gene families. Such candidate conflict resolution families were revealed to be involved in reproductive functions including pheromone biosynthesis, mating behaviour, sperm function and endocrine regulation. Together, these findings indicate that evolutionary timing of gene duplications shapes sex-biased expression in C. maculatus paralogs, and that this framework provides a way of identifying specific gene families where duplications may have driven sex-specific expression divergence.