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.
A major goal in biology is to understand how evolution shapes variation in individual life histories. Genome-wide association studies have been successful in uncovering genome regions linked with traits underlying life history variation in a range of species. However, lack of functional studies of the discovered genotype-phenotype associations severely restrains our understanding how alternative life history traits evolved and are mediated at the molecular level. Here, we report a cis-regulatory mechanism whereby expression of alternative isoforms of the transcription co-factor vestigial-like 3 (vgll3) associate with variation in a key life history trait, age at maturity, in Atlantic salmon (Salmo salar). Using a common-garden experiment, we first show that vgll3 genotype associates with puberty timing in one-year-old salmon males. By way of temporal sampling of vgll3 expression in ten tissues across the first year of salmon development, we identify a pubertal transition in vgll3 expression where maturation coincided with a 66% reduction in testicular vgll3 expression. The late maturation allele was not only associated with a tendency to delay puberty, but also with expression of a rare transcript isoform of vgll3 pre-puberty. By comparing absolute vgll3 mRNA copies in heterozygotes we show that the expression difference between the early and late maturity alleles is largely cis-regulatory. We propose a model whereby expression of a rare isoform from the late allele shifts the liability of its carriers towards delaying puberty. These results exemplify the potential importance of regulatory differences as a mechanism for the evolution of life history traits.
Knowledge of the relative importance of genetic versus environmental determinants of major developmental transitions is pertinent to understanding phenotypic evolution. In salmonid fishes, a major developmental transition enables a risky seaward migration that provides access to feed resources. In Atlantic salmon, initiation of the migrant phenotype, and thus age of migrants, is presumably controlled via thresholds of a quantitative liability, approximated by body size expressed long before the migration. However, how well size approximates liability, both genetically and environmentally, remains uncertain. We studied 32 Atlantic salmon families in two temperatures and feeding regimes (fully fed, temporarily restricted) to completion of migration status at age 1 year. We detected a lower migrant probability in the cold (0.42) than the warm environment (0.76), but no effects of male maturation status or feed restriction. By contrast, body length in late summer predicted migrant probability and its control reduced migrant probability heritability by 50–70%. Furthermore, migrant probability and length showed high heritabilities and between-environment genetic correlations, and were phenotypically highly correlated with stronger genetic than environmental contributions. Altogether, quantitative estimates for the genetic and environmental effects predicting the migrant phenotype indicate, for a given temperature, a larger importance of genetic than environmental size effects.
The optimal phenotypes to survive and reproduce in given evolutionary settings are often in conflict, which manifest as trade-offs in life history traits. Genome-wide association studies have been successful in uncovering genome regions controlling for life history trade-offs in a range of species [1][2][3][4][5][6][7][8] . However, lack of functional studies of the discovered genotype-phenotype associations restrains our understanding how alternative life history traits evolved and are mediated at the molecular level. Here we establish a molecular mechanism by which allelespecific expression differences of the transcription co-factor vgll3 mediate variation in age at maturity in male Atlantic salmon (Salmo salar). By way of a common-garden experiment and temporal sampling of vgll3 expression, we show that vgll3 genotype and expression control male puberty timing in one-year old salmon. Vgll3 expression was high in immature testicular tissue and males entering puberty reduced their vgll3 expression by 66% compared to immature males. Testicular expression of the early maturation associated allele in immature males was constitutively lower compared to the late maturation allele, shifting the liability of early allele carriers towards earlier maturation. These results reveal how gene regulatory differences can be a central mechanism for the evolution of life history variation. Main textSurvival and reproduction often require trade-offs because size and age at maturity are at odds with the risk of dying before reproduction. The molecular basis of variation in life history traits and such trade-offs have thus far remained elusive. In Atlantic salmon, age at maturity is a key life history trait that is evolving under a trade-off of survival and fecundity 2,[9][10][11] . Genetic variation in a single genome region including the transcription co-factor gene vestigial-like 3 (vgll3) was recently found to explain nearly 40% of variation in sea-age at maturity across 57 Northern-European salmon populations 2 . The functional basis of this genotype-phenotype association remains unknown. Seeing that the strongest association in natural populations maps to a single nucleotide polymorphism (SNP) in a non-coding region adjacent to vgll3 2 , we hypothesized that genetic variation in linked cis-regulatory sequences (e.g. enhancers) underlie the functional differences among salmon vgll3 genotypes by changing their expression level or pattern.To uncover the functional genetic basis of age at maturity variation in Atlantic salmon, we first validated that the genotype at the vgll3 locus on chromosome 25 (termed "E" for early sea-age at maturity and "L" for late sea-age at maturity after previous association study 2 ) is associated with age at maturity in controlled conditions by rearing 656 individuals with known vgll3 genotypes from 32 families in common garden conditions (Extended Data Fig. 1). Vgll3*EE males had a significantly higher probability of maturing during their first year compared to males with vgll3*LL genotypes (probit ...
Phone number: +358 2 9415 9537; Email: paul.debes@dal.ca; ORCID: 13 https://orcid.org/0000-0003-4491-9564 14 KeywordsSexual maturation, life-history evolution, lipid reserves, resource allocation trade-15 off, large effect locus 16Abstract 17Sexual maturation is a pivotal life-history trait that balances the probabilities between mortality and 18 reproduction. Environmental vs. genetic contributions to maturation component traits, such as somatic 19 growth and body condition, remain uncertain because of difficulties in determining causality. In Atlantic 20 salmon, maturation timing associates with a large-effect locus around vgll3, which also links with growth, 21 condition, and maturation in mammals. We investigate environmental vs. genetic contributions to 22Maturation timing is a central life-history trait that contributes to maximizing individual survival and 46 reproductive success and, thereby, per capita population growth rate (1-3). Maturation timing is assumed 47
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.