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

了解物种形成，即新物种如何形成并产生惊人的生物多样性的进化过程，是进化生物学的核心问题。通过使用遗传和分子方法，我们对物种形成的理解已经大大提高，并且在许多模式生物中已经确定了十多个大效应的“物种形成基因”。剩下的主要问题是了解这些物种形成基因的功能如何与物种形成过程中的基因组分化过程相关。研究黑腹果蝇（Drosophila melanogaster）复合体中性与生殖相关（SRR）基因的分子进化、性选择和物种形成之间的因果关系是我们研究项目的核心。两个概念上的进步构成了我们研究计划的基础。首先，已知SRR基因进化得更快，男性偏倚基因比女性偏倚基因进化得更快。有趣的是，许多已知的“物种形成基因”都具有SRR基因的特征，它们都显示出快速进化的特征。其次，随着时间的推移，由于后续突变引起的不相容数量的增加，预计影响种间不相容的突变将从小突变演变为大突变。通过对果蝇及其杂交种的详细基因表达研究，我们提出验证两个主要假设：(1)主要的、大影响的“物种形成基因”是快速进化的SRR基因的一个子集；(2)在物种形成过程中，小影响的物种形成基因作为“雪球效应”的结果进化成主要影响的等位基因，即随着时间的推移，随后突变的基因不相容数量不断增加。这些发现对于揭示SRR基因的分子进化模式，并将其与物种形成的遗传和生态过程联系起来，具有重要的意义。

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.