Salinity exposure in early-life drives genomic adaptation to climate change in Antarctic toothfish (Dissostichus mawsoni)

Abstract

Antarctic marine ecosystems are undergoing rapid physical change, yet the capacity of long-lived polar fishes to adapt genomically remains poorly understood. Antarctic toothfish (Dissostichus mawsoni) are an exploited top fish predator whose early life stages develop beneath the sea-ice edge, where salinity, temperature and circulation are being reshaped by climate change. Using whole-genome resequencing data, we investigated how environmental exposure, particularly during early life, structures patterns of local adaptation in D. mawsoni. We analysed 2.4 million unlinked SNPs from 24 adults sampled across the circumpolar distribution of D mawsoni, and compared variability in putatively-adaptive loci with variation in environmental parameters from the ORAS5 global ocean reanalysis, including salinity, temperature, mixed-layer depth, sea-ice concentration and thickness, and surface currents. To capture uncertainty in ontogenetic exposure, we constructed three environmental scenarios differing in their spatial and temporal representation of conditions: Point of Capture-Time of Capture (POC-C), Spawning Ground-Time of Birth (SG-B), and Point of Capture-Time of Birth (POC-B). Genotype-environment association (GEA) was performed using redundancy analysis conditioned on fishing pressure and latent-factor mixed models, with high-confidence GEA loci being defined as SNPs jointly detected by both approaches and robust to random-predictor tests. The scenario that best explained genomic variation was SG-B, in which environmental variables were averaged over hypothesised spawning grounds during the egg incubation period of D. mawsoni (August - October). Within this scenario, the significant environmental axis, dominated by salinity, was strongly associated with 854 high-confidence GEA loci. Functional enrichment revealed over-representation of gene ontology terms linked to monoatomic ion transport, ion channel complexes and calcium signalling, consistent with salinity-driven selection on osmoregulatory pathways during early development. Our results provide genomic evidence that early-life salinity exposure is a key driver of local adaptation in D. mawsoni, underscore the importance of correctly representing life-stage-specific environments in climate genomics, and highlight a concrete pathway by which climate-induced freshening and sea-ice change may alter recruitment and stock resilience.