Beyond speciation genes: Is post-zygotic isolation maintaining species in sympatry?

新物种是如何出现并持续存在的，被认为是“神秘之谜”(达尔文1859)。虽然我们已经走了很长一段路来揭开多样性的一些秘密，但共生物种形成的现象仍然令人费解。哈姆雷特是一组关系密切的珊瑚礁鱼类，是研究这种现象的极好系统，因为它们最近出现了多样化，18种不同物种中有多达9种共存于同一珊瑚礁。哈姆雷特物种之间最显著的差异在于它们的颜色模式，这在基于视觉的分类交配中的生殖隔离中起着核心作用。然而，哈姆雷特物种之间的成功产卵事件可以在自然种群中发生。这些稀有的杂交种是可行的，但它们在野外或实验室中的适合性在很大程度上仍不清楚。然而，对于不同的哈姆雷特物种来说，要坚持没有受精障碍和不完全的配偶选择的共生，必须存在合子后的生殖障碍。这些障碍可以由(Epi)遗传不亲和性驱动，导致异常的表观遗传沉默或过度表达，转座元件的重新激活和基因组的不稳定，这些都是紧密相连的。即使在低流行率的情况下，这些机制也会导致杂交适合度降低，因此对维持不同的物种至关重要。我将用三个相互关联的目标来解决这一现象，目的是(I)评估杂交种的相对适合度，(Ii)表征哈姆雷特物种之间的功能分化(DNA甲基化和基因表达)，以及(Iii)识别维持不同物种共生的合子后障碍。哈姆雷特是研究这些目标的有力模型，不仅因为它们的生态进化史和可用的基因组资源，而且还因为它们的交配策略。作为同时的两性动物，哈姆雷特在一次产卵活动中交替扮演性别角色。这使我们能够在解决合子后障碍时描述性别的影响，这一点很重要，因为卵子和精子是RNA和DNA甲基化遗传的非常不同的载体。综上所述，该项目将提供对杂交不亲和性的无与伦比的见解，并探索高基因流动下海洋物种形成的合子后障碍。

How new species emerge and persist is considered “that mystery of mysteries” (Darwin 1859). While we have come a long way to uncover some of the secrets of diversification, the phenomenon of speciation in sympatry remains puzzling. The hamlets, a group of closely related coral reef fishes, are an excellent system to study this phenomenon, because of their recent diversification with as many as 9 out of 18 different species co-occurring on the same reef. The most notable difference between hamlet species lies in their color pattern, which plays a central role in reproductive isolation via visual based assortative mating. Yet, successful spawning events between hamlet species can occur in natural populations. These rare hybrids are viable, while their fitness in the wild or the laboratory remains largely unknown. However, for distinct hamlet species to persist in sympatry with no fertilization barriers and incomplete mate choice, post-zygotic reproductive barriers must exist. Such barriers can be driven by (epi)genetic incompatibilities resulting in aberrant epigenetic silencing or overexpression, the reactivation of transposable elements and genome instability, which are tightly interlinked. Even at low prevalence, these mechanisms would result in decreased hybrid fitness and thus be critical to maintaining distinct species. I will address this phenomenon with three interlinked objectives aiming at (I) assessing the relative fitness of hybrids, (II) characterizing the functional differentiation (DNA methylation and gene expression) between hamlet species, and (III) identifying post-zygotic barriers maintaining distinct species in sympatry. Hamlets are a powerful model to investigate these objectives not only because of their eco-evolutionary history and the genomic resources available, but also because of their mating strategy. As simultaneous hermaphrodites, hamlets alternate sex roles during one spawning event. This allows us to delineate the effect of sex when addressing post-zygotic barriers, which is important as egg and sperm are very different vectors for the inheritance of RNA and DNA methylation. Taken together, this project will provide unparalleled insights into hybrid incompatibilities and explore the post-zygotic barriers underlying marine speciation under high gene flow.