Disentangling the role of chromosome inversions in the structure of flat oyster (Ostrea edulis): origin, adaptation and phylogeography

Abstract

Chromosomal inversions are large-scale structural variants that disrupt recombination and contribute to population differentiation and local adaptation. In this study, we characterized the genomic features, frequency, and evolutionary significance of chromosomal inversions in the European flat oyster (Ostrea edulis), a species of ecological and commercial relevance. Using a low-density SNP array ([~]5K), we obtained confident genotyping data across the native European distribution of the species. The breakpoints of the inversions at chromosome (C) 2, C5 and C8, spanning 27, 7 and 35 Mb, respectively, were precisely mapped by combining linkage disequilibrium in a large sample and long-read sequencing. This enabled us to identify the SNPs and genes within the inversions for comparative population genomics and functional evaluation. A north to south cline was observed for the three inversions, although with low-moderate correlation between them. Strong signals for divergent selection were detected for the three inversions, although with specific profiles suggestive of adaptive peaks around highly divergent SNPs across the inversion length. The three inversions seem to be old considering genetic diversity and differentiation between arrangements. Phylogeographic events and adaptation to the current environment seem underlying the structural pattern observed. Gene content and enrichment analyses within inversions suggest that these polymorphisms may play a role in the immune system and response to different stressors including parasite resistance. Our results provide new insights into the genomic architecture of adaptation in O. edulis and highlight the potential of structural variants as targets for conservation and selective breeding.