Characterising the genetic architecture and fitness effects of rapid morphological diversification.

解释地球上生命的多样性一直是生物学的一个目标。然而，我们对基因组的变化知之甚少，这些变化是细胞读取、解释和执行基因组编码指令方式变化的基础，以及这些变化如何相互作用以产生具有修改形状或大小的生物体。对于影响某一特定性状的基因变化是否也会导致其他性状的差异，以及它们对繁殖成功率的影响，人们也知之甚少。男性性特征通常是在近亲物种之间最先分化的特征之一。描述所涉及的基因、它们之间的相互作用、所涉及的进化力量以及这种快速进化的适应性后果，为理解动物多样化、生殖隔离和新物种进化的过程提供了一个很好的机会。在果蝇种类中，雄性在生殖器形态上表现出显著的差异。后裂片和钳片，特别是，不同种之间的大小，形状和刚毛数目不同。此外，在交配过程中，这些结构对雄性和雌性的适当依恋也很重要。尽管之前的图谱研究，没有一个涉及的基因被确定，这是描述潜在的基因变化如何相互作用所必需的，如果它们也引起其他特征的差异，以及它们对繁殖成功的影响。因此，在本提案中，我们的目标是确定毛里求斯海蛞蝓和模拟海蛞蝓之间的齿瓣和后叶形态差异的基因。我们的初步结果已经确定了几个小的基因组区域负责后叶和掌部变异的很大比例。在这里，我们建议研究在这些基因组区域中发现的候选基因在模型黑腹龙骨和后叶发育过程中的作用，然后验证它们在毛里求斯龙骨和模拟龙骨之间这些结构变异进化中的直接作用。一旦我们确定了导致生殖形态差异的基因，我们将通过在每个物种的几个菌株中对这些基因进行测序来调查自然变异，并测试这些序列是在定向选择下进化的还是偶然进化的。基因之间的相互作用既可以促进也可以延缓特定性状的进化。因此，我们将测试D. mauritiana和D. simulans的等位基因是如何与其他基因组区域相互作用的，这些基因组区域潜在于喙部和后叶的变异，以评估加性和/或非加性（epistatic）遗传相互作用对这两个性状的分化的贡献。此外，我们将测试致病基因是否会影响其他发育阶段和其他组织中的基因表达或形态（多效效应），以在动物发育的更广泛背景下评估这些变化以及这种变化是如何演变的。最后，我们将测试后叶和钩骨形态的变化是否影响生殖成功。我们的工作将为进一步的研究提供平台，以测试我们在生殖器进化方面的发现的普遍性，并拓宽我们对发育程序背后的遗传机制如何整合基因型信息来指定表型的认识，并帮助解释自然界中巨大的生物多样性是如何进化的。此外，我们对雄性生殖器多样性的研究也可能有助于解决有关数量性状遗传结构的问题，包括上位性的作用和任何多效性效应。考虑到将基因与外貌和行为联系起来的研究的重要性，以及我们对动物多样性的普遍迷恋，像我们这样的研究不仅提供了一个欣赏这种多样性的机会，而且还解释了形成这种多样性的遗传细节。

Explaining the diversity of life on earth has long been a goal of biology. However we understand very little about the changes in the genome that underlie variation in the way cells read, interpret and execute the instructions coded in that genome, and how such changes interact in order to produce an organism with a modified shape or size. There is also a paucity of knowledge about whether the genetic changes that affect a given trait also cause in differences in other traits, and even less about their effect on reproductive success. Male sexual characters are often among the first traits to diverge between closely related species. Characterising the genes involved, their interactions, the evolutionary forces involved and fitness consequences of this rapid evolution offers a great opportunity to understand the processes of animal diversification, reproductive isolation and the evolution of new species.Among Drosophila species, males exhibit striking differences in genitalia morphology. The posterior lobes and claspers, in particular, differ in size, shape and bristle number between species. Moreover these structures are important for proper attachment of the male to the female during mating. Despite previous mapping studies, none of the genes involved have been identified, which is required to characterise how the underling genetic changes interact, if they also cause differences in other traits, and their effect on reproductive success. Therefore, in this proposal, we aim to identify the genes underlying variation in the morphology of the clasper and posterior lobe between D. mauritiana and D. simulans. Our preliminary results have already identified several small genomic regions responsible for a large proportion of the variation in posterior lobe and clasper. Here we propose to investigate the role of candidate genes found in those regions of the genome during clasper and posterior lobe development in the model D. melanogaster, and then verify their direct role in the evolution of variation in these structures between D. mauritiana and D. simulans.Once we have identified the genes responsible for the differences in genital morphology, we will survey natural variation by sequencing those genes in several strains of each species and test if these sequences have evolved under directional selection or just by chance.Interaction between genes can either facilitate or delay the evolution of a given trait, Therefore, we will test how the D. mauritiana and D. simulans alleles interact with other genomic regions underlying variation in the clasper and posterior lobe to evaluate the contribution of additive and/or non-additive (epistatic) genetic interactions to the divergence of these two traits. Furthermore we will test if the causative genes affect gene expression or morphology, at other stages of development and in other tissues (pleiotropic effects), to evaluate these changes in the wider context of animals development and how this evolves. Finally we will test if the changes in posterior lobe and clasper morphology affect reproductive success.Our work will serve as platform for further research to test the generality our findings on genital evolution and broaden our knowledge of how the genetic mechanisms underlying developmental programs integrate genotypic information to specify the phenotype and help explain how the vast organismal diversity in the natural world has evolved. Moreover, our study of male genitalia diversity may also help to address questions regarding the genetic architecture of quantitative traits including the role of epistasis and any pleiotropic effects. Given both the prominence of studies relating genes to appearance and behaviour and our general fascination with animal diversity, research such as ours offers an opportunity to not only appreciate this diversity, but explain the genetic nuts and bolts that have shaped it.