Genetic divergence in the absence of strong ecological differences between coexisting white and common Atlantic marine sticklebacks

Abstract

Identifying taxa in the earliest phases of speciation is critical for understanding how reproductive isolation arises. In Nova Scotia, Canada, "white" threespine sticklebacks co-occur with common marine sticklebacks but differ in nuptial coloration, nesting behavior, and parental care, raising the possibility that they represent a nascent species. We combined population genomics, morphometrics, and stable isotope analysis to test whether white sticklebacks represent a distinct lineage and whether they have diverged along ecological axes as in other stickleback populations. Genotyping-by-sequencing revealed that male and female white sticklebacks form a genetic cluster distinct from sympatric common sticklebacks with evidence of ongoing gene flow yet with very low overall genomic divergence (FST {approx} 0.01). Genetic differences were distributed across many loci rather than localized to a single genomic region. Morphological and isotopic analyses revealed no differences in most classic ecological traits (body shape, armor, gill rakers, or trophic niche). Instead, whites are smaller-bodied, paler, and exhibit shorter spines, reduced testes size, and smaller but more numerous eggs compared to common sticklebacks. These results indicate that white sticklebacks are genetically distinct from the common Atlantic threespine stickleback but have not diverged conspicuously in their ecology, suggesting that their differentiation is driven by reproductive and sexual traits rather than trophic specialization. The white stickleback thus represents a promising new system for investigating the interplay of sexual selection, reproductive strategy, and gene flow in the early stages of speciation.