Nicolas, L. A.; Berdan, E. L.; Colinet, H.; Clouard, A.; De Wit, P.; Glemin, S.; Merot, C.

Chromosomal inversions which form blocks of linked genes are increasingly recognized for their role in maintaining intra-specific diversity. They are predicted to be relevant genetic architectures for local adaptation in the face of gene flow. However, pinpointing the underlying traits and functional mechanisms under selection remains challenging. The seaweed fly Coelopa frigida harbors several large polymorphic inversions, one of which (Cf-Inv(4.1)) displays a latitudinal cline of frequencies along the North American Atlantic Coast. This distribution suggests a putative role in adaptation along the eco-climatic gradient. To further investigate this hypothesis, we designed a molecular marker to identify the different karyotypes and studied natural and experimental populations from America and Europe. We confirmed that this inversion is also present and polymorphic in Europe and displays parallel latitudinal clines across continents, providing strong indirect support that Cf-Inv(4.1) is under natural selection along similar environmental gradients. We found that Cf-Inv(4.1) had no effect on cold tolerance but a significant impact on egg-to-adult survival and fecundity under different thermal conditions. We speculate that fitness associated with the inversion may be shaped by subtle life-history differences whose relative advantage depend on climate. While our experimental approaches provided insights into genotype-phenotype associations, it is worth noting that natural selection acts on the overall fitness, involving complex sets of traits. This is especially relevant for inversions linking hundreds of genes. This multi-gene property also explains why inversions are particularly likely to be involved in repeated parallel adaptation to environmental gradients, as demonstrated here in the seaweed fly.