Global, regional, and cryptic population structure in a high gene-flow transatlantic fish

Abstract

Lumpfish (Cyclopterus lumpus) is a transatlantic marine fish displaying large population sizes and a high potential for dispersal and gene-flow. These features are expected to result in weak population structure. Here, we investigated population genetic structure of lumpfish throughout its natural distribution in the North Atlantic using two approaches: I) 4,393 genome wide SNPs and 95 individuals from 10 locations, and II) 139 discriminatory SNPs and 1,669 individuals from 40 locations. Both approaches identified extensive population genetic structuring with a major split between the East and West Atlantic and a distinct Baltic Sea population, as well as further differentiation of lumpfish from the English Channel, Iceland, and Greenland. The discriminatory loci displayed ~2–5 times higher divergence than the genome wide approach, revealing further evidence of local population substructures. Lumpfish from Isfjorden in Svalbard were highly distinct but resembled most fish from Greenland. The Kattegat area in the Baltic transition zone, formed a previously undescribed distinct genetic group. Also, further subdivision was detected within North America, Iceland, West Greenland, Barents Sea, and Norway. Although lumpfish have considerable potential for dispersal and gene-flow, the observed high levels of population structuring throughout the Atlantic suggests that this species may have a natal homing behavior and local populations with adaptive differences. This fine-scale population structure calls for consideration when defining management units for exploitation of lumpfish stocks and in decisions related to sourcing and moving lumpfish for cleaner fish use in salmonid aquaculture.

Genomic Signatures of Local Adaptation under High Gene Flow in Lumpfish—Implications for Broodstock Provenance Sourcing and Larval Production

“…Although, a divergent subpopulation in mid-Norway was found to be highly differentiated from other Norwegian sampling populations [31]. Moreover, a subset panel of 139 'diagnostic' SNPs revealed that there were at least two genetic clusters in Norway, although not entirely concordant with geography [33]. Further, evidence for the adaptation to local oceanographic features across the pan-Atlantic was also evident in lumpfish [33].…”

“…Moreover, a subset panel of 139 'diagnostic' SNPs revealed that there were at least two genetic clusters in Norway, although not entirely concordant with geography [33]. Further, evidence for the adaptation to local oceanographic features across the pan-Atlantic was also evident in lumpfish [33]. Indeed, the abiotic environment acts as a selective force on natural populations, shaping and maintaining variation in heritable traits (morphology, physiology, and behaviour) that provide significantly greater fitness in their local environment (i.e., local adaptation) when compared to populations from other environments [34][35][36][37].…”

“…However, the stocking of cleaner fish in salmon sea cages has raised increasing concerns regarding the genetic integrity of natural populations following (accidental) escape events of cultured cleaners [27,28]. Accumulating genetics and genomics studies on natural populations of the lumpfish reveal varying patterns of population genetic structure across spatial gradients in the pan-Atlantic [28][29][30][31][32][33]. At large spatial scales, short tandem repeat (STR)-based studies revealed the existence of three major genetic groups of lumpfish: (1) western Atlantic, including samples from USA, Canada, and Greenland, (2) eastern Atlantic, including samples from Iceland and Norway, and (3) the Baltic [29][30][31], a pattern later confirmed with a panel of genome-wide SNPs [33].…”

“…Accumulating genetics and genomics studies on natural populations of the lumpfish reveal varying patterns of population genetic structure across spatial gradients in the pan-Atlantic [28][29][30][31][32][33]. At large spatial scales, short tandem repeat (STR)-based studies revealed the existence of three major genetic groups of lumpfish: (1) western Atlantic, including samples from USA, Canada, and Greenland, (2) eastern Atlantic, including samples from Iceland and Norway, and (3) the Baltic [29][30][31], a pattern later confirmed with a panel of genome-wide SNPs [33]. At finer scales, a genetic break among northwestern and southwestern populations in Greenland was found [30] while no such break was apparent between northeastern and southeastern lumpfish populations in Norway [28,32].…”

A Two-Eyed Seeing approach to describe Gumegwsis (Cyclopterus lumpus) ecology and fisheries interactions in the inner Mawipoqtapei (Chaleur Bay), Canada

“…A new study on Common lump sh genetic structures revealed natal homing behaviors (Jansson et al 2023). Therefore, ne scale management strategies must account for localized populations found in Mawipoqtapei, an area this study has not sampled.…”