The evolution and genetics of sexual dimorphism

同一物种的雄性和雌性往往受到不同甚至相互矛盾的选择压力。然而，除了Y染色体外，两性的绝大部分基因组是相同的。这种两性间的遗传关联创造了性冲突的可能性，而性冲突反过来又选择了冲突的解决和两性二态性的进化。冲突通常被认为阻碍了对自然选择的性别特异性反应，并起到了进化制动器的作用，然而越来越多的证据表明，它可以塑造种群的遗传多样性，并在适应中发挥重要作用。确定性冲突是否、如何以及何时可以解决，对其在生态适应中的作用具有关键意义。人们普遍认为，雌性和雄性之间基因调控的差异可以解决性冲突。然而，这种关系最近一直是争论的主题，不同基因调控机制的潜在作用尚未得到测试。此外，性别冲突的基因组研究主要集中在成人身上，但许多性别二态性是在胚胎发生期间建立的。因此，我们对性冲突的发展背景及其在发展过程中的持续和表现缺乏详细的了解。最近的研究表明，性别偏倚基因是性别特异性适应性的关键组成部分，但这些性别差异是如何建立并通过发育变化的尚不清楚。表观遗传修饰，如甲基化，已知在不改变DNA序列的情况下通过影响基因组结构在调节基因表达方面发挥重要作用。然而，表观遗传过程、性拮抗基因的表达和冲突解决之间的关系尚未得到严格的检验。最后，我们对解决冲突的可能性的理解是有限的。特别是，一种很少受到关注的基因调控机制是选择性剪接。剪接通过从一个位点产生多个转录本来增加蛋白质组学的复杂性，并且在不同物种、性别和组织中存在很大差异，并且在性别决定途径中起着关键作用。然而，性别特异性剪接的进化、其功能重要性以及在解决冲突中的作用尚未得到检验。本项目将结合最先进的基因组工具和高分辨率测序数据（RNA-seq, PacBio， WGBS）在鸟类系统发育方面的研究：DNA甲基化如何导致表达的性别差异？选择性剪接在性冲突解决中的作用是什么？性冲突在发展过程中是如何表现的？具体来说，这些问题将通过在四种鸟类的多个发育阶段从雄性和雌性身上取样的体细胞和性腺组织来解决；鸡、野鸡、珍珠鸡和野鸭。我们已经开发了种群基因组管道来识别性冲突的特征（Wright et al . 2018 evolution Letters），并研究选择性剪接（Rogers et al . in prep）和基因表达进化（Wright et al . 2017 Nat commons）。新颖性和及时性尽管近年来人们对性冲突的表现和持续产生了相当大的兴趣，但仍有许多问题没有得到解答，特别是冲突在进化变化中的作用。冲突是否有助于或阻碍适应的证据不一，而且尚不清楚未解决的冲突对适应的阻碍是否大于帮助。本博士将对基因调控在解决性冲突中的相关作用以及这些作用在发育过程中的表现进行综合理解。在此过程中，这项工作对进化生物学的多个领域具有广泛的意义，包括表型多样性、适应和物种形成。

BackgroundMales and females of the same species are often subject to different and even contradictory selection pressures. However, with the exception of the Y chromosome, the sexes share the vast majority of their genome. This intersexual genetic correlation creates the potential for sexual conflict, which in turn selects for conflict resolution and the evolution of sexual dimorphism. Conflict is typically thought to impede sex-specific responses to natural selection and act as an evolutionary brake, yet growing evidence indicates it can shape genetic diversity in populations and act as an important force in adaptation.Identifying if, how, and when sexual conflict can be resolved has key implications for its role in ecological adaptation. It is widely assumed that gene regulation differences between females and males can resolve sexual conflict. However, this relationship has been the subject of considerable recent debate and the potential roles of different gene regulatory mechanisms have not been tested. Furthermore, genomic studies of sexual conflict focus primarily on adults yet many sexual dimorphisms are established during embryogenesis. As a result, we lack a detailed understanding of the developmental context of sexual conflict, and its persistence and manifestation through development. Recent studies have shown that sex-biased genes are a key component of sex-specific fitness, but how these sex differences are established and change through development is unclear. Epigenetic modifications, such as methylation, are known to play important roles in regulating gene expression by influencing the structure of the genome without changing the DNA sequence. However, the relationship between epigenetic processes, the expression of sexually antagonistic genes, and conflict resolution has not yet been rigorously tested.Finally, our understanding of the potential for conflict to be resolved is limited. In particular, one mechanism of gene regulation that has received little attention is alternative splicing. Splicing increases proteomic complexity by generating multiple transcripts from one locus, and varies substantially across species, sexes, and tissues, as well as playing a key role in sex determination pathways. However, the evolution of sex-specific splicing, its functional importance, and role in resolving conflict has yet to be tested.ObjectivesThis project will combine state-of-the-art genomic tools and high-resolution sequencing data (RNA-seq, PacBio, WGBS) across the avian phylogeny to ask: 1. How does DNA methylation contribute to sex differences in expression?2. What is the role of alternative splicing in sexual conflict resolution?3. How is sexual conflict manifest during development?Specifically, these questions will be addressed using somatic and gonadal tissues sampled from males and females at multiple developmental stages across four avian species; chicken, pheasant, guineafowl and mallard duck. We have already developed population genomic pipelines to identify signatures of sexual conflict (Wright et al 2018 Evol Letters) and study alternative splicing (Rogers et al in prep) and gene expression evolution (Wright et al 2017 Nat Commun).Novelty and TimelinessDespite considerable recent interest in the manifestation and persistence of sexual conflict, many questions remain unanswered, particularly the role of conflict in evolutionary change. There is mixed evidence whether conflict aids or impedes adaptation, and it is not clear whether unresolved conflict hinders adaptation more than it helps. This PhD will generate an integrated understanding of the relative roles of gene regulation in resolving sexual conflict, and how these are manifest during development. In doing so, this work has broad implications for multiple fields of evolutionary biology, including phenotypic diversity, adaptation and speciation.