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

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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.