The genetic basis of salinity tolerance traits in Arctic charr (Salvelinus alpinus)

The capacity to maintain internal ion homeostasis amidst changing conditions is particularly important for teleost fishes whose reproductive cycle is dependent upon movement from freshwater to seawater. Although the physiology of seawater osmoregulation in mitochondria-rich cells of fish gill epithelium is well understood, less is known about the underlying causes of inter- and intraspecific variation in salinity tolerance. We used a genome-scan approach in Arctic charr (Salvelinus alpinus) to map quantitative trait loci (QTL) correlated with variation in four salinity tolerance performance traits and six body size traits. Comparative genomics approaches allowed us to infer whether allelic variation at candidate gene loci (e.g., ATP1α1b, NKCC1, CFTR, and cldn10e) could have underlain observed variation.

Combined parental analyses yielded genome-wide significant QTL on linkage groups 8, 14 and 20 for salinity tolerance performance traits, and on 1, 19, 20 and 28 for body size traits. Several QTL exhibited chromosome-wide significance. Among the salinity tolerance performance QTL, trait co-localizations occurred on chromosomes 1, 4, 7, 18 and 20, while the greatest experimental variation was explained by QTL on chromosomes 20 (19.9%), 19 (14.2%), 4 (14.1%) and 12 (13.1%). Several QTL localized to linkage groups exhibiting homeologous affinities, and multiple QTL mapped to regions homologous with the positions of candidate gene loci in other teleosts. There was no gene × environment interaction among body size QTL and ambient salinity.

Variation in salinity tolerance capacity can be mapped to a subset of Arctic charr genomic regions that significantly influence performance in a seawater environment. The detection of QTL on linkage group 12 was consistent with the hypothesis that variation in salinity tolerance may be affected by allelic variation at the ATP1α1b locus. IGF2 may also affect salinity tolerance capacity as suggested by a genome-wide QTL on linkage group 19. The detection of salinity tolerance QTL in homeologous regions suggests that candidate loci duplicated from the salmonid-specific whole-genome duplication may have retained their function on both sets of homeologous chromosomes. Homologous affinities suggest that loci affecting salinity tolerance in Arctic charr may coincide with QTL for smoltification and salinity tolerance traits in rainbow trout. The effects of body size QTL appear to be independent of changes in ambient salinity.