Genomic analysis of inbreeding, DNA methylation and sexual trait expression in a lekking bird

自从达尔文首次提出“性选择”一词来解释夸张的雄性特征的进化以来，我们已经开始理解这些特征之间复杂的相互关系，它们所编码的信息以及它们所嵌入的动物的生活史。性选择是建立在这样一种观点之上的，即个体的品质是由这些性状的表达决定的，然而，对性性状的遗传结构和调节性性状表达的机制的清晰的机制理解仍然是难以捉摸的。我们知道近亲繁殖是个体素质的重要组成部分，一些研究已经记录了性选择性状的近亲繁殖抑制。此外，性状表达受年龄和环境变化等动态因素的影响，因此提出了由身体状况介导的表观遗传控制作为调节基因型依赖性性性状表达的手段。因此，解决长期存在的关于配偶选择和性选择的进化问题需要对性特征的遗传和表观遗传基础有一个基本的了解。我们将结合近交的基因组推断和全基因组甲基化分析来研究影响典型lek模型系统黑松鸡性性状表达和繁殖成功的遗传和表观遗传机制。首先，我们将使用精确的近交基因组估计来量化多性征近交抑制的程度。在此基础上，我们将使用结构方程模型来整合将近亲繁殖依赖的性特征表达与繁殖成功变异联系起来的潜在途径。为了阐明性性状的遗传结构，我们将量化不同基因组区域对近亲繁殖抑制的贡献。我们将评估对“基因捕获”假说的支持，该假说认为性特征受到分布在基因组中的大量基因座的累积效应的影响。或者，局部基因组区域可能不成比例地重要，例如，与免疫或代谢有关的基因途径。最后，我们将在最近一项通过差异甲基化将杂合性与性性状表达联系起来的试点研究的基础上，利用成本效益高的全基因组测定方法epi-GBS，鉴定与近交和雄性性性状表达相关的全基因组表观遗传特征。我们预计近亲繁殖依赖的DNA甲基化模式在性状表达最大化的时期是最强的，定位于特定的基因组区域，并且是性状特异性的。总之，我们的项目通过将个体寿命期间的多种性别特征的详细数据与经典泄漏物种的基因组和表观遗传数据相结合，解决了一个重要的知识缺口。这个项目具有无与伦比的潜力，可以改变我们对性选择的理解，并为下一代的详细研究奠定基础。

Since Darwin first coined the term “sexual selection” to explain the evolution of exaggerated male traits, we have come to understand the complex interrelationships among these traits, the information they encode and the life histories of the animals they are embedded into. Sexual selection is built on the idea that individual quality is signaled by the expression of these traits, yet a clear mechanistic understanding of the genetic architectures of sexual traits and the mechanisms regulating sexual trait expression remains elusive.We know that inbreeding is an important component of individual quality, and several studies have documented inbreeding depression for sexually-selected traits. Moreover, trait expression can be influenced by dynamic factors such as age and environmental variation, so epigenetic control mediated by body condition has been proposed as a means of regulating genotype-dependent sexual trait expression. Resolving long-standing evolutionary questions about mate choice and sexual selection therefore requires a fundamental understanding of the genetic and epigenetic basis of sexual traits.We will combine the genomic inference of inbreeding with genome-wide methylation analysis to investigate the genetic and epigenetic mechanisms affecting sexual trait expression and reproductive success in a classical lek model system, the black grouse. First, we will use precise genomic estimates of inbreeding to quantify the magnitude of inbreeding depression for multiple sexual traits. From there, we will use structural equation modeling to integrate potential pathways linking inbreeding-dependent sexual trait expression to variation in reproductive success.To shed light on the genetic architectures of sexual traits, we will quantify the contribution of different genomic regions to inbreeding depression. We will evaluate support for the ‘genic capture’ hypothesis, which posits that sexual traits are influenced by the cumulative effects of large numbers of loci distributed across the genome. Alternatively, localized genomic regions could be disproportionately important, e.g. gene pathways linked to immunity or metabolism.Finally, we will build upon a recent pilot study linking heterozygosity to sexual trait expression via differential methylation by using a cost-effective genome-wide assay, epi-GBS, to identify genome-wide epigenetic signatures associated with inbreeding and male sexual trait expression. We expect inbreeding-dependent DNA methylation patterns to be strongest during periods of maximal trait expression, to be localized to specific genomic regions, and to be trait-specific.In summary, our project tackles an important knowledge gap by combining detailed data from multiple sexual traits over individual lifespans with genomic and epigenetic data in a classical lekking species. This project has the unrivalled potential to transform our understanding of sexual selection and underpin the next generation of detailed studies.