Characterization of natural variation in North American Atlantic Salmon populations (Salmonidae: Salmo salar) at a locus with a major effect on sea age

Abstract

Age at maturity is a key life‐history trait of most organisms. In anadromous salmonid fishes such as Atlantic Salmon (Salmo salar), age at sexual maturity is associated with sea age, the number of years spent at sea before the spawning migration. For the first time, we investigated the presence of two nonsynonymous vgll3 polymorphisms in North American Atlantic Salmon populations that relate to sea age in European salmon and quantified the natural variation at these and two additional candidate SNPs from two other genes. A targeted resequencing assay was developed and 1,505 returning adult individuals of size‐inferred sea age and sex from four populations were genotyped. Across three of four populations sampled in Québec, Canada, the late‐maturing component (MSW) of the population of a given sex exhibited higher proportions of SNP genotypes 54Thrvgll3 and 323Lysvgll3 compared to early‐maturing fish (1SW), for example, 85% versus 53% of females from Trinité River carried 323Lysvgll3 (n MSW = 205 vs. n 1SW = 30; p < .001). However, the association between vgll3 polymorphism and sea age was more pronounced in females than in males in the rivers we studied. Logistic regression analysis of vgll3 SNP genotypes revealed increased probabilities of exhibiting higher sea age for 54Thrvgll3 and 323Lysvgll3 genotypes compared to alternative genotypes, depending on population and sex. Moreover, individuals carrying the heterozygous vgll3 SNP genotypes were more likely (>66%) to be female. In summary, two nonsynonymous vgll3 polymorphisms were confirmed in North American populations of Atlantic Salmon and our results suggest that variation at those loci correlates with sea age and sex. Our results also suggest that this correlation varies among populations. Future work would benefit from a more balanced sampling and from adding data on juvenile riverine life stages to contrast our data.

Transcription Profiles of Age-at-Maturity-Associated Genes Suggest Cell Fate Commitment Regulation as a Key Factor in the Atlantic Salmon Maturation Process

“…Sinclair-Waters, J. Ødegård, S. A. Korsvoll, T. Moen, S. Lien, C. R. Primmer and N. J. Barson, unpublished results). However, associations in North American-derived salmon populations and aquaculture stocks have been mixed, possibly due to little or no polymorphism at the locus in North American populations (Boulding et al 2019;Kusche et al 2017;Mohamed et al 2019). In addition to Atlantic salmon, VGLL3 has also been linked with pubertal timing, growth and body condition in humans (Elks et al 2010;Cousminer et al 2013;Tu et al 2015), which indicates that it may have an evolutionarily conserved role in the regulation of vertebrate maturation timing.…”

Atlantic salmon Salmo salar in the chalk streams of England are genetically unique

“…comm.). Future work on the populations assessed here could use molecular analysis to determine the number of years that each generation of chalk‐stream S. salar spends between hatching and spawning, which varies considerably over the range of the species (Klemetsen et al, ; Kusche et al, ).…”

“…Future work on the populations assessed here could use molecular 636 C . I K E D I A S H I E T A L. analysis to determine the number of years that each generation of chalk-stream S. salar spends between hatching and spawning, which varies considerably over the range of the species (Klemetsen et al, 2003;Kusche et al, 2017). The five chalk streams studied are currently managed following county borders and Environment Agency regional borders, so that the Rivers Frome, Piddle and Avon are managed within the Environment Agency region of Wessex, while the Rivers Test and Itchen are managed within the Environment Agency Solent and South Downs region.…”

Genomic signatures of fine‐scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence‐related genes

“…() showed that a single locus containing the gene vgll3 explained nearly 40% of this variation in age at maturity across three evolutionary lineages in Europe (see also Ayllon et al., ). This locus appears also to be associated with sea age at maturity in North American Atlantic salmon (Kusche et al., ) and is additionally located within a QTL underlying early (“precocious”) freshwater maturation (Lepais, Manicki, Glise, Buoro, & Bardonnet, ). The choice between residency and anadromy in many populations of rainbow trout/steelhead ( Oncorhynchus mykiss ) is associated with a large nonrecombining region on chromosome Omy05 (Hecht, Campbell, Holecek, & Narum, ; Hecht, Thrower, Hale, Miller, & Nichols, ; Martínez, Garza, & Pearse, ; Nichols, Edo, Wheeler, & Thorgaard, ; Pearse, Miller, Abadía‐Cardoso, & Garza, ).…”