Balancing selection maintains intraspecific diversity in a deep-sea fish

Segregating alleles in natural populations can be driven to fixation or loss by genetic drift or directional selection, or may be maintained in a polymorphic state by balancing selection. Balancing selection in a panmictic population is theoretically well established, but not widely understood at the molecular level. In this study, we focus on the evolutionary processes affecting non-synonymous variants at eight functionally relevant loci (based on candidate SNP genotyping) in a deep-sea fish species (Coryphaenoides rupestris) that lives across habitat zones ranging from ~200 m to ~2000 m depth. At each of these loci, one allele is predominant in the deeper water. Across a shallower depth range, we find that minor allele frequencies show a highly significant increase or decline progressively across five defined age categories. At single depths below a threshold depth, the deep-water allele declines in frequency with age. Together, these data indicate segregation to different depths, either shallow or deep, and balancing selection to retain variants needed for each depth range. This is supported by signals for long-term balancing selection at these loci (based on published genomic data). We discuss alternative interpretations and conclude that balancing selection maintaining ecotype diversity is the best supported mechanism.