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Understanding the processes that link genotype to phenotype is a central challenge in biology. Despite progress in discovering genes associated with ecologically relevant traits, a poor understanding of the processes and functions via which molecules mediate evolutionary differences leaves us critically far from linking proximate and ultimate causes of evolution. This knowledge gap is particularly large in multifaceted phenotypes of ecological relevance such as life histories where multiple traits covary and influence fitness. In Atlantic salmon (Salmo salar), variation in a key life-history trait, maturation age, is largely linked to the transcription cofactor vestigial-like 3 (vgll3). Here, we show that despite this simple genetic architecture, vgll3 genotype influences maturation age through a complex regulatory mechanism whereby it controls the expression of diverse pubertal signaling pathways. Using a multiomic approach in salmon testes, we show that the vgll3 genotype conferring early maturity up-regulates key genes controlling androgen production, cellular energy and adiposity, and TGF-β signaling, thereby increasing the likelihood of earlier pubertal initiation. By mapping VGLL3 regulatory elements we further show its interaction with distinct transcription factors in a genotype-dependent manner, thus coordinating differential activation of regulatory pathways. This study reveals the proximate mechanisms through which a genetically simple association leads to functionally complex molecular differences in a spectrum of cellular traits, thus explaining the molecular basis of pleiotropy in a large-effect gene. Our results indicate that evolution in correlated phenotypes, as exemplified by alternative life history strategies, can be dictated by the function of major life-history genes. [ABSTRACT FROM AUTHOR]

Linking reproductive fitness with adaptive traits at the genomic level can shed light on the mechanisms that produce and maintain sex‐specific selection. Here, we construct a multigenerational pedigree to investigate sex‐specific selection on a maturation gene, vgll3, in a wild Atlantic salmon population. The vgll3 locus is responsible for ~40% of the variation in maturation (sea age at first reproduction). Genetic parentage analysis was conducted on 18,265 juveniles (parr) and 685 adults collected at the same spawning ground over eight consecutive years. A high proportion of females (26%) were iteroparous and reproduced two to four times in their lifetime. A smaller proportion of males (9%) spawned at least twice in their lifetime. Sex‐specific patterns of reproductive fitness were related to vgll3 genotype. Females showed a pattern of overdominance where vgll3*EL genotypes had three‐fold more total offspring than homozygous females. In contrast, males demonstrated that late‐maturing vgll3*LL individuals had two‐fold more offspring than either vgll3*EE or vgll3*EL males. Taken together, these data suggest that balancing selection in females contributes to the maintenance of variation at this locus via increased fitness of iteroparous vgll3*EL females. This study demonstrates the utility of multigenerational pedigrees for uncovering complex patterns of reproduction, sex‐specific selection and the maintenance of genetic variation. [ABSTRACT FROM AUTHOR]

Efforts to understand the genetic underpinnings of phenotypic variation are becoming more and more frequent in molecular ecology. Such efforts often lead to the identification of candidate regions showing signals of association and/or selection. These regions may contain multiple genes and therefore validation of which genes are actually responsible for the signal is required. In Atlantic salmon (Salmo salar), a large‐effect locus for maturation timing, an ecologically important trait, occurs in a genomic region including two genes, vgll3 and akap11, but data for clearly determining which of the genes (or both) contribute to the association have been lacking. Here, we take advantage of natural recombination events detected between the two candidate genes in a salmon broodstock to reduce linkage disequilibrium at the locus, thus enabling delineation of the influence of variation at these two genes on early maturation. By rearing 5,895 males to maturation age, of which 81% had recombinant vgll3/akap11 allelic combinations, we found that vgll3 single nucleotide polymorphism (SNP) variation was strongly associated with early maturation, whereas there was little or no association between akap11 SNP variation and early maturation. These findings provide strong evidence supporting vgll3 as the primary candidate gene in the chromosome 25 locus for influencing early maturation. This will help guide future research for understanding the genetic processes controlling early maturation. This also exemplifies the utility of natural recombinants to more precisely map causal variation underlying ecologically important phenotypic diversity. [ABSTRACT FROM AUTHOR]