Abstract
Chromosomal inversions can play an important role in divergence and reproductive isolation by buildingand maintaining distinct allelic combinations between evolutionary lineages. Alternatively, they can takethe form of balanced polymorphisms that segregate within populations over time until one arrangementbecomes fixed. Many questions remain about how these different inversion polymorphisms arise, how themechanisms responsible for their long-term maintenance interact, and ultimately how they contribute tospeciation. The long-snouted seahorse (Hippocampus guttulatus) is known to be subdivided into partiallyisolated lineages and marine-lagoon ecotypes differentiated by structural variation. Here, we aim tocharacterise these differences along the entire genome, and to reconstruct their history and role inecotype formation. We generated a near chromosome-level reference genome assembly and describedgenome-wide patterns of diversity and divergence through the analysis of 112 whole-genome sequencesfrom Atlantic, Mediterranean, and Black Sea populations. Combined with linked-read sequencing data, wefound evidence for two megabase-scale chromosomal inversions showing contrasted allele frequencypatterns across the species range. We reveal that these inversions represent ancient intraspecificpolymorphisms, one being likely maintained by divergent selection, and the other by associativeoverdominance. Haplotype combinations characterising Mediterranean ecotypes also suggest theexistence of potential interactions between the two inversions, possibly driven by environment-dependentfitness effects. Lastly, we detected gene flux eroding divergence between inverted alleles at varying levelsbetween the two inversions, with a likely impact on their long-term dynamics.