Divergence and gene flow history at two large chromosomal inversions involved in long-snouted seahorse ecotype formation

Abstract

Chromosomal inversions can play an important role in divergence and reproductive isolation by building and maintaining distinct allelic combinations between evolutionary lineages. Alternatively, they can take the form of balanced polymorphisms that segregate within populations over time until one arrangement becomes fixed. Many questions remain about how these different inversion polymorphisms arise, how the mechanisms responsible for their long-term maintenance interact, and ultimately how they contribute to speciation. The long-snouted seahorse (Hippocampus guttulatus) is known to be subdivided into partially isolated lineages and marine-lagoon ecotypes differentiated by structural variation. Here, we aim to characterise these differences along the entire genome, and to reconstruct their history and role in ecotype formation. We generated a near chromosome-level reference genome assembly and described genome-wide patterns of diversity and divergence through the analysis of 112 whole-genome sequences from Atlantic, Mediterranean, and Black Sea populations. Combined with linked-read sequencing data, we found evidence for two megabase-scale chromosomal inversions showing contrasted allele frequency patterns across the species range. We reveal that these inversions represent ancient intraspecific polymorphisms, one being likely maintained by divergent selection, and the other by associative overdominance. Haplotype combinations characterising Mediterranean ecotypes also suggest the existence of potential interactions between the two inversions, possibly driven by environment-dependent fitness effects. Lastly, we detected gene flux eroding divergence between inverted alleles at varying levels between the two inversions, with a likely impact on their long-term dynamics.