Adaptive genomic divergence parallels migratory behavior in Atlantic bluefin tuna

Abstract

Identifying and preserving biological diversity is fundamental for the conservation of wild populations. The Atlantic bluefin tuna (Thunnus thynnus, ABT) is an apex predator and vital species to the pelagic ecosystems of the North Atlantic Ocean, with populations now rebounding from decades of overfishing due to strict enforcement of conservation measures. Here, we combine high-resolution whole-genome sequencing data with spatial data from electronic tagging to improve our understanding of population structure in ABT. We analyzed 82 whole-genome sequences obtained from mature fish tracked to geographically distinct spawning grounds, as well as larvae representing the two recognized stocks (western and eastern) of ABT. We obtained 11,181,223 single-nucleotide polymorphisms (SNPs) and integrated these genomic data with 12,974 total geolocation days of adult ABT (mean individual deployment length: 271 ± 110.4 days). This extensive dataset of electronic tracks enables spatial assignment of individuals to their respective spawning grounds and the first whole-genome comparison of migratory phenotypes. Both neutral and adaptive SNP markers reflect the same genomic population structure as the spatial movement patterns, likely maintained by natal philopatry, and we highlight candidate genes with potentially adaptive roles. Our analyses show that the two populations diverged ∼27,000 years ago, overlapping with the Last Glacial Maximum, and we suggest that oceanographic variation of the spawning grounds has contributed to shaping present-day bluefin tuna genomic diversity. Overall, these results improve our understanding of adaptive variation in bluefin tuna, which will be important for management decisions.