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Evolution of diapause in the African killifish by remodeling ancient gene regulatory landscape

ABSTRACT: Suspended animation (e.g. hibernation, diapause) allows organisms to survive extreme environments. But the mechanisms underlying the evolution of suspended animation states are unknown. The African turquoise killifish has evolved diapause as a form of suspended development to survive the complete drought that occurs every summer. Here, we show that gene duplicates – paralogs – exhibit specialized expression in diapause compared to normal development in the African turquoise killifish. Surprisingly, paralogs with specialized expression in diapause are evolutionarily very ancient and are present even in vertebrates that do not exhibit diapause. To determine if evolution of diapause is due to the regulatory landscape rewiring at ancient paralogs, we assessed chromatin accessibility genome-wide in fish species with or without diapause. This analysis revealed an evolutionary recent increase in chromatin accessibility at very ancient paralogs in African turquoise killifish. The increase in chromatin accessibility is linked to the presence of new binding sites for transcription factors, likely due to de novo mutations and transposable element (TE) insertion. Interestingly, accessible chromatin regions in diapause are enriched for lipid metabolism genes, and our lipidomics studies uncover a striking difference in lipid species in African turquoise killifish diapause, which could be critical for long-term survival. Together, our results show that diapause likely originated by repurposing pre-existing gene programs via recent changes in the regulatory landscape. This work raises the possibility that suspended animation programs could be reactivated in other species for long-term preservation via transcription factor remodeling and suggests a mechanism for how complex adaptations evolve in nature.

ORGANISM(S): Red-striped Killifish Aphyosemion Striatum Fish Nothobranchius Furzeri;aphyosemion Striatum Nothobranchius Furzeri

TISSUE(S): Embryonic Cells

SUBMITTER: Kevin Contrepois

PROVIDER: ST001898 | MetabolomicsWorkbench | Thu Aug 05 00:00:00 BST 2021

REPOSITORIES: MetabolomicsWorkbench

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Evolution of diapause in the African killifish by remodeling ancient gene regulatory landscape

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