Parallel adaptation to geothermally-warmed habitats due to common structural variation and functional developmental pathways

Abstract

Abstract Climate change is causing rapid temperature increases that drive adaptive changes. Predicting these outcomes remains challenging as the extremes of warming have not yet been experienced by natural populations. Contemporary populations inhabiting geothermally-warmed environments can provide valuable insights, including phenotypic and genomic responses involved in adaptation to warming. Here, we examine independent instances of divergence between geothermal and ambient ecotypes of threespine stickleback. While we identify similar patterns of phenotypic divergence in appetite, fat storage, and fat loss (during starvation), genomic divergence of loci is non-parallel. However, at a functional level, the mapk signalling pathway differs across ecotype pairs and expression of mapk genes differs between ecotypes, are thermally plastic, and influenced by hybridization. We also identify an inversion on chromosome XXI, previously attributed to freshwater colonization, diverging in parallel between ecotypes. Candidate genes within the inversion are associated with metabolic traits, including appetite regulation and fat storage in correspondence with our phenotypic findings. Overall, polygenic adaptation conferring functionally similar outcomes and structural variation are key genomic mechanisms facilitating adaptation to warmed environments. Functional molecular pathways should be prioritized in conservation, as precise allelic changes are difficult to predict and potentially less relevant to thermal adaptation than previously thought.