Antifreeze protein gene amplification facilitated niche exploitation and speciation in wolffish

Abstract

During winter, the coastal waters of Newfoundland can be considered a 'freeze risk ecozone' for teleost fishes, where the shallower habitats pose a high (and the deeper habitats a low) risk of freezing. Atlantic (Anarhichas lupus) and spotted (Anarhichas minor) wolffish, which inhabit these waters, reside at opposite ends of this ecozone, with the Atlantic wolffish being the species facing the greatest risk, because of its shallower niche. In order to resist freezing, this species secretes five times the level of antifreeze protein (AFP) activity into the plasma than does the spotted wolffish. The main basis for this interspecific difference in AFP levels is gene dosage, as the Atlantic wolffish has approximately three times as many AFP gene copies as the spotted wolffish. In addition, AFP transcript levels in liver (the primary source of circulating AFPs) are several times higher in the Atlantic wolffish. One explanation for the difference in gene dosage and transcript levels is the presence of tandemly arrayed repeats in the latter, which make up two-thirds of its AFP gene pool. Such repeats are not present in the spotted wolffish. The available evidence indicates that the two species diverged from a common ancestor at a time when the ebb and flow of northern glaciations would have resulted in the emergence of shallow water 'freeze risk ecozones'. The results of this study suggest that the duplication ⁄ amplification of AFP genes in a subpopulation of ancestral wolffish would have facilitated the exploitation of this high-risk habitat, resulting in the divergence and evolution of modern-day Atlantic and spotted wolffish species.

Copy number variants outperform SNPs to reveal genotype-temperature association in a marine species

“…Tigano et al, 2018;Weetman et al, 2018;Bazzicalupo et al, 2019;Nelson et al, 2018;Prunier et al, 2019;Ruytinx et al, 2019) but empirical studies on CNVs in marine systems remain limited. Previous studies in marine fishes supported a role for CNVs in freeze resistance (Hew et al, 1988;Hayes et al, 1991, Chen et al, 2008Desjardins et al, 2012). For instance, Hayes et al (1991) (Faucon et al, 2017, Weetman et al, 2018.…”

“…used DNA electrophoresis and southern blots to highlight differences in antifreeze proteins (AFPs) gene copy number and arrangement among some winter flounder (Pseudopleuronectes americanus) populations along the Northeastern Atlantic coast.Similarly,Desjardins et al (2012) found that multiple copies of AFPs genes improved gene-dosage effect and also transcript level between two close-related wolf fish species (Anarhichas lupus and Anarhichas minor), facilitating the colonization of a shallow-water habitat where the risk of freezing is elevated. By showing empirical evidence for CNV-environment association, our results thus bring additional evidence for the importance of structural variation for local adaptation in marine species.Processes underlying local adaptation by CNVs can imply various complex mechanisms suchas remodeling chromatin architecture(Dunaway et al, 2016) or the modulation of gene expression (i.e.…”

Freeze Tolerance in Sculpins (Pisces; Cottoidea) Inhabiting North Pacific and Arctic Oceans: Antifreeze Activity and Gene Sequences of the Antifreeze Protein

“…Many species decline or lose antifreeze activity in deep areas, such as wolffish, snailfish and flounder [24,50,51]. Generally, there is no freezing risk because of the absence of ice nuclei in the deep area.…”

Antifreeze protein dispersion in eelpouts and related fishes reveals migration and climate alteration within the last 20 Ma

“…Northern blotting was performed using various tissues from both the rock gunnel and the radiated shanny (S6 Fig) and the transcripts were most abundant in the liver. Moderate expression was found in skin, gill and stomach, indicating that that the liver-dominant expression originally observed in Zoarcidae [47] and Anarhichadidae [29] is also a feature that arose early in Zoarcales. A partial type III AFP sequence from an even more divergent species, the Alaskan ronquil (Fig 1), was amplified from genomic DNA in two overlapping fragments using seminested PCR (see Supplementary Methods).…”