Polygenic and major‐locus contributions to sexual maturation timing in Atlantic salmon

Abstract

Sexual maturation timing is a life‐history trait central to the balance between mortality and reproduction. Maturation may be triggered when an underlying compound trait, called liability, exceeds a threshold. In many different species and especially fishes, this liability is approximated by growth and body condition. However, environmental vs. genetic contributions either directly or via growth and body condition to maturation timing remain unclear. Uncertainty exists also because the maturation process can reverse this causality and itself affect growth and body condition. In addition, disentangling the contributions of polygenic and major loci can be important. In many fishes, males mature before females, enabling the study of associations between male maturation and maturation‐unbiased female liability traits. Using 40 Atlantic salmon families, longitudinal common‐garden experimentation, and quantitative genetic analyses, we disentangled environmental from polygenic and major locus (vgll3) effects on male maturation, and sex‐specific growth and condition. We detected polygenic heritabilities for maturation, growth, and body condition, and vgll3 effects on maturation and body condition but not on growth. Longitudinal patterns for sex‐specific phenotypic liability, and for genetic variances and correlations between sexes suggested that early growth and condition indeed positively affected maturation initiation. However, towards spawning time, causality appeared reversed for males whereby maturation affected growth negatively and condition positively via both the environmental and genetic effects. Altogether, the results indicate that growth and condition are useful traits to study liability for maturation initiation, but only until maturation alters their expression, and that vgll3 contributes to maturation initiation via condition.

Life-history genotype explains variation in migration activity in Atlantic salmon (Salmo salar)

“…which relates to higher condition, is also associated with increased migration activity while in males, the vgll3*L allele, which relates to lower condition, is associated with higher migration activity. Interestingly, body condition has been suggested to, at least partly, be a factor contributing to the detected vgll3 effects on maturation timing of male parr (Debes et al 2021). Our results add more evidence supporting the notion that vgll3 effects on trait expression might be mediated by body condition, although more research on the topic is needed.…”

“…For example, in Atlantic salmon (Salmo salar), variation in a genome region including the vestigial-like family member 3 gene (vgll3) on chromosome 25 has been shown to explain a large proportion of variation in the sea-age at maturity in males and females (Barson et al 2015). Since vgll3 is involved in fat cell regulation (Halperin et al 2013), potentially controlling resource allocation between energy reserves and somatic growth, and its effects are at least partially phylogenetically conserved, it potentially contributes to moderating the expression of life-history strategies across species (Debes et al 2021). Indeed, vgll3 is associated with size, as well as age, at maturity in both salmon and humans (Cousminer et al 2013;Barson et al 2015).…”

Standard metabolic rate does not associate with age-at-maturity genotype in juvenile Atlantic salmon

“…However, we did not detect any difference in either SMR or body condition between juvenile Atlantic salmon individuals of different homozygous vgll3 genotypes. The lack of difference in body condition might be related to body size or life-stage; the fish in the study by Debes et al (2021) were considerably more developmentally advanced, averaging 19 g, and had been reared for approximately 3100 degree days at stable daily temperatures with many of the males maturing the same autumn. In comparison, the fish in this study averaged just 1.08 g and had been reared at approximately 1900 degree days and also under a variable temperature regime, which could have further reduced growth (Imholt et al, 2011).…”

“…Vgll3 genotype has been shown to have a strong effect on salmon life-history (Ayllon et al, 2015;Barson et al, 2015;Verta et al, 2020), and recent findings have suggested that this effect might be mediated by vgll3-induced differences in body condition (Debes et al, 2021). Taking this together with the connections between standard metabolic rate (SMR) and resource acquisition and assimilation (Armstrong et al, 2011;Auer, Bassar, et al, 2020;Auer, Solowey, et al, 2020;Bochdansky et al, 2005;Millidine et al, 2009;Rosenfeld et al, 2015), we hypothesized that vgll3 genotype might be asserting some of its effects through changes in energetic physiology that would be reflected in SMR.…”

“…Taking studies of this gene to the lab, examining body condition and maturation probability in a common garden setting, Debes et al (2021) found that the vgll3*E allele associated with a higher body condition in males and females (but not body length), as well as a higher probability of male maturation in the first autumn after hatching. Interestingly, Debes et al (2021) also showed that maturation probability in males could be predicted using the body condition of their sisters (all immature), demonstrating a connection between vgll3 and body condition that is not caused by the enlarging gonads in maturing individuals. Additionally, expression of vgll3 has been linked with activation of the intracellular HIPPO signalling pathway, suggesting a role in inhibiting gonad development and promoting adipocyte differentiation (Kjaerner-Semb et al, 2018;Kurko et al, 2020;Verta et al, 2020).…”