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Müller, Lena (2012): The influence of sex on gene expression and protein evolution in Drosophila melanogaster. Dissertation, LMU München: Fakultät für Biologie



A long-standing question in evolutionary biology concerns the molecular causes underlying adaptive evolution. These can either stem from structural changes in proteins or from changes in the expression patterns of proteins or mature RNAs. Over the last decade, many studies have shown that gene expression changes can have a huge impact on the phenotype of an organism and play an important role in adaptive evolution. A major prerequisite for adaptive evolution to occur at the gene expression level is the presence of expression variation among members of a population. This variation serves as the raw material for adaptive evolution. The genetic causes underlying changes in expression patterns can either be located in cis-regulatory regions of the affected gene, such as transcription factor binding sites, or in trans-regulatory regions, such as transcription factors. Mutations in cis-regulatory elements have relatively few pleiotropic effects and their effects are often additive, thus, cis-regulatory changes are thought to be especially well-suited targets of selection. A major factor influencing gene expression is the sex of an organism. The sex-bias of a gene also influences the pace at which proteins evolve, such that male-biased genes often show more rapid evolution than female-biased or unbiased genes between Drosophila species. Here, we investigated genome-wide gene expression variation in adult females of two populations of D. melanogaster, one from the ancestral species range (Zimbabwe) and one from the derived species range (the Netherlands). We found relatively little expression polymorphism present within the populations and high expression divergence between the populations. More than 500 genes were expressed differentially between the populations. These are candidate genes for those that have undergone adaptive regulatory evolution to the new, derived environment. When comparing our study of female adults to a study investigating male adult flies of the same populations, we found that there is significantly less expression polymorphism in females within the populations but significantly more expression divergence between the populations. Further, there was little overlap in genes that differ in expression between the populations in males and females. This suggests that general differences exist between the sexes in gene expression regulation and that regulatory evolution has been mainly sex-specific. Our findings show that extensive gene expression variation exists in D. melanogaster and further highlight the importance of accounting for sex when investigating gene expression. In order to elucidate the genetic and evolutionary mechanisms that underlie differential gene expression between the populations, we employed a candidate gene approach. Analysis of molecular variation in the coding and upstream regions of several differentially expressed genes in both populations revealed evidence for a recent selective sweep in the European population for the gene CG34330. In the putative promoter region of the gene, there is one indel and one SNP where a derived variant is fixed in the European population, but at low frequency in the African population. These are candidates for those variants that control the expression level of the gene. For another gene, Jon99Ciii, we found evidence for recurrent structural protein evolution acting since the split of D. melanogaster from D. simulans and D. sechellia. However, no evidence for recent regulatory evolution could be found for this gene. Motivated by findings that male-biased genes often evolve faster than both female- and unbiased genes between Drosophila species, we examined the molecular evolution of sex-biased genes and their contribution to within-population polymorphism, between-population divergence and between-species divergence in D. melanogaster and D. ananassae. This was studied on both the DNA-sequence level and the expression level. We found strong purifying selection limiting protein sequence variation within species. In contrast, a high proportion of divergence could be attributed to positive selection. In D. melanogaster, male-biased genes showed the highest fraction of adaptive substitutions, a pattern that was especially pronounced on the X chromosome. In contrast, male-biased genes did not show higher variation within or between populations, suggesting that inter-species divergence is not just a simple extension of inter-population divergence and intra-population variation. For D. ananassae, we did not observe a higher rate of adaptive evolution for male-biased genes, a finding that suggests that the type or strength of selection acting on sex-biased genes differs between lineages. Similarly, on the expression level, we found that sex-biased genes show high expression divergence between species, but low divergence between populations.