Low but significant genetic differentiation underlies biologically meaningful phenotypic divergence in a large Atlantic salmon population

Aykanat, Tutku; Johnston, Susan E.; Orell, Panu; Niemelä, Eero; Erkinaro, Jaakko; Primmer, Craig R.

doi:10.1101/022178

Cited by 2 publications

(1 citation statement)

References 109 publications

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“…Scales were collected from salmon harvested by local fishermen using a variety of methods (nets, rod) from 2001 to 2003. In total, 326 and 137 individuals from subpopulations 1 and 2 were included69 .…”

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confidence: 99%

Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon

Barson

Aykanat

Hindar

et al. 2015

Nature

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537

942

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Males and females share many traits that have a common genetic basis; however, selection on these traits often differs between the sexes, leading to sexual conflict. Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict. Yet, despite intense theoretical and empirical interest, the specific loci underlying sexually antagonistic phenotypes have rarely been identified, limiting our understanding of how sexual conflict impacts genome evolution and the maintenance of genetic diversity. Here we identify a large effect locus controlling age at maturity in Atlantic salmon (Salmo salar), an important fitness trait in which selection favours earlier maturation in males than females, and show it is a clear example of sex-dependent dominance that reduces intralocus sexual conflict and maintains adaptive variation in wild populations. Using high-density single nucleotide polymorphism data across 57 wild populations and whole genome re-sequencing, we find that the vestigial-like family member 3 gene (VGLL3) exhibits sex-dependent dominance in salmon, promoting earlier and later maturation in males and females, respectively. VGLL3, an adiposity regulator associated with size and age at maturity in humans, explained 39% of phenotypic variation, an unexpectedly large proportion for what is usually considered a highly polygenic trait. Such large effects are predicted under balancing selection from either sexually antagonistic or spatially varying selection. Our results provide the first empirical example of dominance reversal allowing greater optimization of phenotypes within each sex, contributing to the resolution of sexual conflict in a major and widespread evolutionary trade-off between age and size at maturity. They also provide key empirical evidence for how variation in reproductive strategies can be maintained over large geographical scales. We anticipate these findings will have a substantial impact on population management in a range of harvested species where trends towards earlier maturation have been observed.

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mentioning

confidence: 99%

Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon

Barson

Aykanat

Hindar

et al. 2015

Nature

Self Cite

537

942

View full text Add to dashboard Cite

show abstract

Sex-dependent dominance at a single locus maintains variation in age at maturity in Atlantic salmon

Barson

Aykanat

Hindar

et al. 2015

Preprint

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Males and females share many traits that have a common genetic basis, however selection on these traits often differs between the sexes leading to sexual conflict 1,2 . Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict 2-6 . Yet, despite intense theoretical and empirical interest, the specific genetic loci behind sexually antagonistic phenotypes have rarely been identified, limiting our understanding of how sexual conflict impacts genome evolution 4,7,8 and the maintenance of genetic diversity 8,9 . Here, we identify a large effect locus controlling age at maturity in 57 salmon populations, an important fitness trait in which selection favours earlier maturation in males than females 10 , and show it is a clear example of sex dependent dominance reducing intralocus sexual conflict and maintaining adaptive variation in wild populations.Using high density SNP data and whole genome re-sequencing, we found that vestigial-like family member 3 (VGLL3) exhibits sex-dependent dominance in salmon, promoting earlier and later maturation in males and females, respectively. VGLL3, an adiposity regulator associated with size and age at maturity in humans, explained 39.4% of phenotypic variation, an unexpectedly high effect size for what is usually considered a highly polygenic trait. Such large effects are predicted under balancing selection from either sexually antagonistic or spatially varying selection 11-13 . Our results provide the first empirical example of dominance reversal permitting greater optimisation of phenotypes within each sex, contributing to the resolution of sexual conflict in a major and widespread evolutionary trade-off between age and size at maturity. They also provide key empirical evidence for how variation in reproductive strategies can be maintained over large geographical scales.We further anticipate these findings will have a substantial impact on population management in a range of harvested species where trends towards earlier maturation have been observed.

show abstract

Low but significant genetic differentiation underlies biologically meaningful phenotypic divergence in a large Atlantic salmon population

Cited by 2 publications

References 109 publications

Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon

Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon

Sex-dependent dominance at a single locus maintains variation in age at maturity in Atlantic salmon

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