title: The ontogeny and evolution of sex-biased gene expression in Drosophila melanogaster.
abstract: Sexually dimorphic phenotypes are thought to largely result from sex differences in gene expression, and genes with sex-biased expression have been well characterized in adults of many species. Although most sexual dimorphisms manifest in adults, many result from sex-specific developmental trajectories, implying that juveniles may exhibit significant levels of sex-biased expression. However, it is unclear how much sex-biased expression occurs before reproductive maturity and whether preadult sex-biased genes should exhibit the same evolutionary dynamics observed for adult sex-biased genes. In order to understand the continuity, or lack thereof, and evolutionary dynamics of sex-biased expression throughout the life cycle, we examined sex-biased genes in pre-gonad tissue of two preadult stages and compared them with the adult gonad of Drosophila melanogaster. We found that the majority of the genome is sex-biased at some point in the life cycle, with some genes exhibiting conserved sex-biased expression and others displaying stage-specific sex bias. Our results also reveal a far more complex pattern of evolution for sex-biased genes throughout development. The most rapid evolutionary divergence occurred in genes expressed only in larvae within each sex, compared with continuously expressed genes. In females-but not males-this pattern appeared to be due to relaxed purifying selection in larva-limited genes. Furthermore, genes that retained male bias throughout life evolved more rapidly than stage-specific male-biased genes, due to stronger purifying selection in stage-specific genes. However, female-biased genes that were specific to larvae evolved most rapidly, a pattern that could not be definitively attributed to differences in adaptive evolution or purifying selection, suggesting that pleiotropic constraints on protein-coding sequences can arise when genes are broadly expressed across developmental stages. These results indicate that the signature of sex-specific selection can be detected well before reproductive maturity and is strongest during development.
authors: Jesus College, University of Oxford, Oxford, United Kingdom.
authors: Jennifer C
authors: JC
authors: Perry
authors: Peter W
authors: PW
authors: Harrison
authors: Judith E
authors: JE
authors: Mank
mesh_terms: D000818:Animals; D030801:Animals, Genetically Modified; D004331:Drosophila melanogaster / Q000235:genetics* / Q000254:growth & development; D019143:Evolution, Molecular; D005260:Female; D018507:Gene Expression Regulation, Developmental; D063990:Gene Ontology; D017344:Genes, Insect; D006066:Gonads / Q000254:growth & development; D008297:Male; D012641:Selection, Genetic; D012727:Sex Characteristics; D012733:Sex Differentiation / Q000235:genetics
keywords: development; sex-specific selection; sexual conflict; sexual dimorphism