Rolling with the punches: Organism-environment interactions shape spatial pattern of adaptive differentiation in the widespread mantis shrimp Oratosquilla oratoria

Investigating spatial pattern of adaptive variation and its underlying processes can inform the adaptive potential distributed within species ranges, which is increasingly important in the context of a changing climate. A correct interpretation of adaptive variation pattern requires that population history and the ensuing population genetic structure are taken into account. Here we carried out such a study by integrating population genomic analyses, demographic model testing and species distribution modeling to investigate patterns and causes of adaptive differentiation in a widespread mantis shrimp, Oratosquilla oratoria, along a replicated, broad-scale temperature gradient in the northwestern Pacific (NWP). Our results supported a strong hierarchical ecogeographic structure dominated by habitat-linked divergence among O. oratoria populations accompanied with introgressive hybridization. A combined F_ST outlier and environmental correlation analyses revealed remarkable temperature-associated clines in allele frequency across paired North-South populations on Chinese and Japanese coasts, and identified a suite of loci associated with temperature adaptation. Further demographic model testing revealed the observed clinal variation derived partly from Pleistocene divergence followed by recent secondary contact. More importantly, the likelihood of hybridization is predicted to increase as climate change progresses, which would break barriers to gene flow and enable the spread of adaptive genetic variation. These results support that not only is temperature-driven adaptive differentiation occurs in O. oratoria but that such pattern is likely attributed to ancient adaptive variation, sustained by contemporary ocean conditions and a semi-permeable barrier to gene flow maintained by selection. They moreover provide genomic insights into the distribution of adaptive potential across O. oratoria' s species range. This work can serve as a case study to characterize adaptive diversity of marine species in the NWP by integrating environmental and genetic data at temporal and spatial scales in a population genomic framework, which would improve management and conservation actions under climate change.