Overruled by nature: A plastic response to environmental change disconnects a gene and its trait

Abstract

In Atlantic salmon, age at maturation is a life history trait governed by a sex‐specific trade‐off between reproductive success and survival. Following environmental changes across large areas of the Northeast Atlantic, many populations currently display smaller size at age and higher age at maturation. However, whether these changes reflect rapid evolution or plasticity is unknown. Approximately 1500 historical and contemporary salmon from the river Etne in Western Norway, genotyped at 50,000 SNPs, revealed three loci associated with age at maturation. These included vgll3 and six6 which collectively explained 36%–50% of the age at maturation variation in the 1983–1984 period. These two loci also displayed sex‐specific epistasis, as the effect of six6 was only detected in males bearing two copies of the late maturation allele for vgll3. Strikingly, despite allelic frequencies at vgll3 remaining unchanged, the combined influence of these genes was nearly absent in all samples from 2013 to 2016, and genome‐wide heritability strongly declined between the two time‐points. The difference in age at maturation between males and females was upheld in the population despite the loss of effect from the candidate loci, which strongly points towards additional causative mechanisms resolving the sexual conflict. Finally, because admixture with farmed escaped salmon was excluded as the origin of the observed disconnection between gene(s) and maturation age, we conclude that the environmental changes observed in the North Atlantic during the past decades have led to bypassing of the influence of vgll3 and six6 on maturation through growth‐driven plasticity.

Investigating the role of genetic variation in vgll3 and six6 in the domestication of gilthead seabream (Sparus aurata Linnaeus) and European seabass (Dicentrarchus labrax Linnaeus)

“…The latter suggests that the selection for enhanced growth and maturation may have influenced the genetic variation in these genes, leading to their possible association with the domestication process. Similar studies conducted on Atlantic salmon comparing domesticated and wild populations, have also reported strong association signals in regions encompassing vgll3 and/or six6 genes (Ayllon et al., 2015; Sinclair‐Waters et al., 2020), an outcome, however, that may be influenced by farming conditions such as the feeding regime (Ayllon et al., 2019; Besnier et al., 2023). Identifying causative SNPs in this dataset is impossible; however, it is worth noting that the studied SNP in the vgll3 gene of European seabass concerned a non‐synonymous mutation of a hydrophilic amino acid (serine) to a hydrophobic one (alanine).…”

Tissue-specific metabolic enzyme levels covary with whole-animal metabolic rates and life-history loci via epistatic effects

“…This may lead to slower resource acquisition, thus delaying maturation. Interestingly, a somewhat similar epistatic effect was observed as delayed maturation of Atlantic salmon males with six6 LL -vgll3 LL genotypes from historical samples [35]. The lack of such an effect in contemporary samples may have been explained by intensified environmental effects on maturation (e.g.…”

“…Atlantic salmon ( Salmo salar ) is an ideal species for testing the associations between adaptive life-history variation and metabolism at different levels of organization. Two loci in Atlantic salmon, so-called vestigial-like family member 3 ( vgll3 ) and SIX homeobox 6 ( six6 ) after the most prominent genes located in these genomic regions, explain a substantial part of variation in a key life-history trait, age-at-maturity [31–35]; their two alleles are named early (E) and late (L) after their associations with age-at-maturity. Vgll3 is also associated with other life-history traits, such as number of reproduction events and early (precocious) maturation of male salmon [36,37].…”

Environmental change unlinks a gene from its trait

“…This partial disassociation between the trait and the combined influence of these loci occurred despite the allelic frequencies of vgll3 remaining similar, and was paralleled by a decrease in genome-wide heritability for sea age. Besnier et al (2023) were able to exclude admixture of farmed salmon as the origin of the observed disconnection between gene(s) and sea age, and postulated that the unlinking was driven by growth-related plasticity. They proposed a scenario whereby the role of vgll3 in salmon experiencing either unlimited food supply (e.g.…”

“…Building on this rich foundation of knowledge, Besnier et al (2023) set out to investigate the evolutionary potential In Atlantic salmon (Salmo salar), sea age is a major life history trait governed by a sex-specific trade-off between reproductive success and survival. In this issue of Molecular Ecology, Besnier et al (Molecular Ecology, 2023) found evidence to suggest that the disassociation between sea age and major effect loci, including the previously identified candidate genes vgll3 and six6, may be related to the recently observed trend towards slower growth and later maturation.…”