The architecture underpinning genomic divergence is still a largely uncharted territory and likely case-dependent. Here, we investigated genome-wide variation in Ballan wrasse, a northeastern Atlantic fish species that displays two sympatric colour morphs, spotty and plain, that have been suggested to represent subspecies. We produced a chromosome-level reference genome and thereafter investigated genomic divergence among 152 individuals including both morphs, from two localities in Spain and Norway each and one in France. Differences between morphs dominated in Spain in accordance with sympatric divergence, whereas in Norway allopatric differentiation was prominent and repeated genomic signals of local divergence were found. Chromosomes had large low-recombining areas shared across all populations. Within the Spanish morphs, these areas contained large islands of divergence, totalling ~11% of the genome, and showed high morph specificity and strong selection. The same regions showed frequent admixture in the French morphs and no differentiation in Norway. In contrast, divergent regions observed between sampling localities in Norway were shorter and found throughout the genome. High inbreeding and lower diversity were observed in the Norwegian samples, consistent with the proposed recolonisation bottleneck and subsequent drift. Several genomic regions were significantly associated with morphs and contained tens of genes of diverse functions, suggesting that colouration is unlikely to be the sole driver of divergence. Our results do not support the hypothesis of shared larger genomic features underlying intraspecific colour divergence. Instead, we observe gradual accumulation of differences into low-recombining regions, likely when additional factors like assortative mating and/or lack of gene flow favour their development.
Keywords: cleaner fish; intraspecific divergence; island of divergence; run of homozygosity; speciation.
© 2025 The Author(s). Molecular Ecology published by John Wiley & Sons Ltd.