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

建议书摘要 了解物种形成是进化生物学中的一个中心问题。物种形成是新物种如何形成并产生生物惊人多样性的进化过程。通过使用遗传和分子方法，我们对物种形成的理解已经有了很大的进步，在许多模式生物中已经发现了十几个大效应的‘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有关。研究果蝇复合体中性别和生殖相关(SRR)基因的分子进化、性别选择和物种形成之间的因果关系是我们研究计划的核心。两个概念上的进步构成了我们研究提案的基础。首先，众所周知，SRR基因进化得更快，与偏向女性的基因相比，偏向男性的基因进化更快。有趣的是，许多已知的‘物种形成基因’被描述为SRR基因，所有这些基因都显示出快速进化的特征。其次，预计影响种间不亲和性的突变将从小到大，因为随着时间的推移，后续突变造成的不亲和性越来越多。利用对果蝇及其杂交后代的详细基因表达研究，我们建议检验两个主要假设：(1)主效‘物种形成基因’是快速进化的SRR基因的子集；(2)在物种形成过程中，由于‘滚雪球效应’，即后续突变的基因不相容数量的增加，微效物种形成基因进化为主效等位基因。这些发现的意义在于在物种形成研究的前沿，破译SRR基因的分子进化模式，并将它们与物种形成的遗传和生态过程联系起来。

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.