Genomics and the origin of marine species

• Applicant: Professor Oscar Puebla, Ph.D.
• Subject Area: Evolutionary Cell and Developmental Biology (Zoology) ; General Genetics and Functional Genome Biology ; Evolution, Anthropology
• Term: from 2015 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 277213305

How new species may arise and persist in the presence of gene flow is a fundamental and still unresolved question in our understanding of the origins of biodiversity. This question is particularly puzzling in the ocean, where physical barriers are often poorly defined and pelagic larvae provide potential for extensive gene flow, but which nonetheless harbours some of the most diverse communities on earth. Coral reefs in particular rival with tropical forests in terms of diversity, and coral reef fish communities are among the most species-rich assemblages of vertebrates. The origin of coral reef fish families and functional groups dates back to the Palaeocene; however, the majority of species arose within the last 5.3 myr, with closely related species often differing primarily with respect to colour pattern. How did this diversity arise? Building on my initial DFG grant, I propose to use the hamlets—a group of closely related reef fishes from the wider Caribbean that differ essentially in colour pattern—as a model system to address this question. I propose to extend this research in two directions in particular: the processes underlying marine speciation (objectives 1 & 2) and the specific traits driving reproductive isolation (objectives 3 & 4).We have established that gene flow is ongoing among hamlet species through the identification of high-probability hybrids and backcrosses in the field, but we don’t know whether gene flow occurred throughout the history divergence or upon secondary contact following an initial phase without gene flow. We will build a phylogeny for the hamlets and leverage our chromosome-resolution reference genome, our whole-genome resequencing data and new parent-offspring trio phased data to reconstruct the history of gene flow using state-of-the-art approaches based on the blockwise site frequency spectrum and segments of identity-by-descent (objective 1). Furthermore, preliminary phylogenetic analysis suggests that hamlets might have evolved in parallel in different locations. We will test this hypothesis using the same approach (objective 2). We have also identified candidate genes for pigmentation, but our analyses are now limited by the objective quantification of colour pattern variation. We will leverage our collection of standardized photographs and tissue samples to conduct the most in-depth genotype x phenotype association analysis of colour pattern in any coral reef fish so far using whole genomes and an objective quantification of colour pattern that does not involve human scoring (objective 3). Finally, we have identified a candidate gene with strong functional links to vision that also seems to be involved in pigmentation. This finding, if confirmed, would constitute a significant insight as a direct coupling between vision and pigmentation would facilitate speciation in the presence of gene flow. This hypothesis will be tested in the hamlets, and in zebrafish through a new collaboration (objective 4).

• DFG Programme: Research Grants