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Grath, Sonja (2010): Molecular Evolution of Sex-Biased Genes in Drosophila ananassae. Dissertation, LMU München: Faculty of Biology
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Abstract

Genes with sex-biased expression often show rapid molecular evolution between species. Previous population genetic and comparative genomic studies of Drosophila melanogaster and D. simulans revealed that male-biased genes have especially high rates of adaptive evolution. In this dissertation, I investigate the forces aecting the evolution of sex-biased genes in a Drosophila species other than the well-studied D. melanogaster. Using custom-made PCR-amplicon microarrays and published microarray data, I analyzed sex-biased gene expression in the cosmopolitan Drosophilid species D. ananassae which occurs in highly structured populations throughout the subtropical and tropical regions of the world, mainly in Southeast Asia. I assessed sex-biased gene expression for 129 D. ananassae protein-coding genes whose D. melanogaster orthologs had been extensively studied at the expression and population genetic level. For 43 of these genes, I surveyed DNA sequence polymorphism in a natural population of D. ananassae and determined divergence to the sister species D. atripex and D. phaeopleura. Seven of these genes were further analyzed in twelve populations located throughout the geographical range of D. ananassae. Sex-biased gene expression is generally conserved between D. melanogaster and D. ananassae, but about one-third of the genes have either gained or lost sex-biased gene expression in one of the species and about 4% of the genes have undergone a reversal in sex-bias. In contrast to the melanogaster lineage, the signal of adaptive protein evolution for male-biased genes is not as strong in D. ananassae and is limited to genes with conserved male-biased expression in both species. In addition, I made use of whole-genome data on sex-biased gene expression and the rate of evolution measured by the ratio of nonsynonymous substitution rate (dN) to the synonymous substitution rate (dS) to reveal that the degree of sex-bias is positively correlated with the rate of evolution over 30 million years of Drosophilid evolution. There is a general pattern of faster evolution for highly male-biased genes compared to male-biased genes with a lower degree of sex-bias in D. melanogaster, D. ananassae, and D. pseudoobscura. Moreover, up to 50% of genes are not conserved in degree of sex-bias between species. Additionally, I could assess patterns of molecular evolution in relation to ancestral states of sex-biased gene expression for orthologous genes using D. pseudoobscura as an outgroup. In most cases, genes that show conserved male-biased gene expression over longer evolutionary time scales have significantly higher rates of molecular evolution. Investigating mating discrimination and genetic differentiation at mitochondrial loci shed light on possible patterns of speciation within the species occurring in this geographical range. Finally, I found evidence for cold adaptation in D. ananassae strains collected from the more temperate regions of the species range and, in two populations, differences in cold tolerance between males and females.