Positive selection and relaxed purifying selection contribute to rapid evolution of male-biased genes in a dioecious flowering plant.

Sex-biased genes offer insights into the evolution of sexual dimorphism. Sex-biased genes, especially those with male bias, show elevated evolutionary rates of protein sequences driven by positive selection and relaxed purifying selection in animals. Although rapid sequence evolution of sex-biased genes and evolutionary forces have been investigated in animals and brown algae, less is known about evolutionary forces in dioecious angiosperms. In this study, we separately compared the expression of sex-biased genes between female and male floral buds and between female and male flowers at anthesis in dioecious Trichosanthes pilosa (Cucurbitaceae). In floral buds, sex-biased gene expression was pervasive, and had significantly different roles in sexual dimorphism such as physiology. We observed higher rates of sequence evolution for male-biased genes in floral buds compared to female-biased and unbiased genes. Male-biased genes under positive selection were mainly associated with functions to abiotic stress and immune responses, suggesting that high evolutionary rates are driven by adaptive evolution. Additionally, relaxed purifying selection may contribute to accelerated evolution in male-biased genes generated by gene duplication. Our findings, for the first time in angiosperms, suggest evident rapid evolution of male-biased genes, advance our understanding of the patterns and forces driving the evolution of sexual dimorphism in dioecious plants.

Sex-biased gene content is associated with sex chromosome turnover in Danaini butterflies.

Sex chromosomes play an outsized role in adaptation and speciation, and thus deserve particular attention in evolutionary genomics. In particular, fusions between sex chromosomes and autosomes can produce neo-sex chromosomes, which offer important insights into the evolutionary dynamics of sex chromosomes. Here, we investigate the evolutionary origin of the previously reported Danaus neo-sex chromosome within the tribe Danaini. We assembled and annotated genomes of Tirumala septentrionis (subtribe Danaina), Ideopsis similis (Amaurina), Idea leuconoe (Euploeina) and Lycorea halia (Itunina) and identified their Z-linked scaffolds. We found that the Danaus neo-sex chromosome resulting from the fusion between a Z chromosome and an autosome corresponding to the Melitaea cinxia chromosome (McChr) 21 arose in a common ancestor of Danaina, Amaurina and Euploina. We also identified two additional fusions as the W chromosome further fused with the synteny block McChr31 in I. similis and independent fusion occurred between ancestral Z chromosome and McChr12 in L. halia. We further tested a possible role of sexually antagonistic selection in sex chromosome turnover by analysing the genomic distribution of sex-biased genes in I. leuconoe and L. halia. The autosomes corresponding to McChr21 and McChr31 involved in the fusions are significantly enriched in female- and male-biased genes, respectively, which could have hypothetically facilitated fixation of the neo-sex chromosomes. This suggests a role of sexual antagonism in sex chromosome turnover in Lepidoptera. The neo-Z chromosomes of both I. leuconoe and L. halia appear fully compensated in somatic tissues, but the extent of dosage compensation for the ancestral Z varies across tissues and species.