Molecular evolution of sex and reproduction related genes and their role in speciation: The genomic architecture of hybrid male sterility

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Summary of the Proposal Understanding speciation, the evolutionary process of how new species form and give rise to the spectacular diversity of living organisms, is a central problem in evolutionary biology. Our understanding of speciation has been greatly advanced by using genetic and molecular approaches and over a dozen large-effects 'speciation genes' have been identified in many model organisms. The major remaining question is to understand how the functions of these speciation genes relate to the processes of genomic divergence during speciation. Investigation of the causal connections between the molecular evolution of sex and reproduction related (SRR) genes, sexual selection, and speciation among species of the Drosophila melanogaster complex form the core of our research program. Two conceptual advances form the basis of our research proposal. First, SRR genes are known to evolve faster, with male-biased genes evolving faster compared to female-biased genes. It is interesting to know that many of the known 'speciation genes' are characterized as SRR genes, all of which show signatures of rapid evolution. Second, it is expected that mutations affecting interspecific incompatibility would evolve from being minor to major as a result of the increasing number of incompatibilities caused by subsequent mutations over time. Using detailed gene expression studies with Drosophila and their hybrids, we propose to test two major hypotheses: (1) that the major, large-effects 'speciation genes' are a subset of rapidly evolving SRR genes, and (2) that during the speciation process, minor-effects speciation genes evolve into major-effects alleles as a result of a 'snowball effect', i.e. the increasing number of gene incompatibilities of subsequent mutations over time. The significance of these findings lies at the forefront of speciation research in deciphering the patterns of molecular evolution of SRR genes and relating them to genetic and ecological processes of speciation.