Beyond speciation genes: Is post-zygotic isolation maintaining species in sympatry?
General Genetics and Functional Genome Biology
Developmental Biology
Evolution, Anthropology
Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions
Systematics and Morphology (Zoology)
Final Report Abstract
The marine environment exhibits fewer geographic barriers allowing for wide-dispersing larvae and high gene flow, which typically hinders speciation. Yet, a group of coral reef fishes, the hamlets, recently underwent a particularly rapid radiation, with distinct color patterns playing a crucial role in reproductive isolation. This project aimed to uncover the evolutionary drivers that maintain hamlet species in sympatry, focusing on DNA methylation, transcriptomic analysis, and fitness measures to reveal isolation mechanisms. Our research added a new dimension to understanding color evolution beyond the established aggressive mimicry hypothesis by linking coloration, behavior and brain transcriptomic analyses. Studying predator avoidance strategies revealed that defensive behavior correlates with camouflage coloration, suggesting divergent camouflage strategies as a driver for speciation. Further, DNA methylation analyses showed that most variations are species-specific, reflecting epigenomic divergence among the hamlets. Higher levels of background differentiation in the methylome compared to the genome suggest that epigenomic divergence may proceed at a faster evolutionary pace, offering insights into different states of the speciation timeline. Additionally, we characterized a recent expansion of the LTR/Ngaro TE family, whose expression is ongoing. By examining differential TE expression, we identified candidate loci that might be implicated in postzygotic isolation if their differential mobilization translates into incompatibilities in TE silencing between species. Unexpectedly, the project also revealed an unprecedented expansion of greensensitive opsins (RH2) in the hamlet's visual system, with each species harboring 11-13 RH2s, which is – to the best of our knowledge – the highest number reported in fish. The onset of this gene expansion predates the hamlet radiation and suggests a unique adaptation in their visual perception. Lastly, we set out to investigate whether any readily available epigenomic tools could be applied in conservation. Demonstrating their potential to enhance current molecular monitoring frameworks, we summarized their applicability as biomarkers, to monitor management strategies and improve hatchery rearing. In conclusion, this project advanced our understanding of the evolutionary processes that drive speciation in marine environments, particularly among hamlet fishes. The findings provide novel insights into the (epi)genetic, transcriptomic, and behavioral mechanisms of reproductive isolation, highlighting the factors contributing to the exceptional biodiversity within this lineage.
Publications
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An epigenetic toolbox for conservation biologists. Evolutionary Applications, 17(6).
Balard, Alice; Baltazar‐Soares, Miguel; Eizaguirre, Christophe & Heckwolf, Melanie J.
