Parallel differentiation extends beyond chromosomal inversions to small genomic islands on a background of rampant gene flow in the European flat oyster (Ostrea edulis)

Heterogeneous genomic landscapes of differentiation can reveal evolutionary processes acting over different timescales. Whereas genetic structure in the European flat oyster, Ostrea edulis, is mainly shaped by geography, previous work suggested parallel differentiation between western and eastern Mediterranean populations and between Atlantic and North Sea populations, resulting in genetic convergence between range margin populations in some genomic regions. Here, we analyzed 27 oysters from four locations using moderate-coverage (~20X) short-read whole-genome sequencing. We first examined three known chromosomal inversions and found evidence that they predate divergence with the sister species O. chilensis. We then scanned the genome for parallel differentiation at the individual-SNP rather than sliding-window scale using the product of allele-frequency differences across the two geographic contrasts. Two of the three inversions were detected, but we also identified 12 small non-inverted genomic regions showing even stronger signals of parallel differentiation. These 'islands of parallelism' typically overlap one or a few genes, and most showed elevated dXY consistent with long-term barriers to gene flow. Two islands overlap nuclear ATP synthase subunits, while mitochondrial ATP8 shows a convergent amino-acid change, suggesting possible nuclear-nuclear and mitonuclear incompatibilities. Finally, demographic inference with heterogeneous gene flow supported post-glacial secondary contact and a lineage-based rather than geography-based population topology. Our results suggest that the genomes of O. edulis lineages have been largely porous to gene flow upon secondary contact, except for chromosomal inversions and small genomic islands. These regions likely act as barrier loci, preserving a signal of a shared evolutionary history among marginal populations that has otherwise been erased by rampant gene flow.