Large single-locus effects for maturation timing are mediated via body condition in Atlantic salmon

Debes, Paul V.; Piavchenko, Nikolai; Ruokolainen, Annukka; Ovaskainen, Outi; Moustakas-Verho, Jacqueline Emmanuel; Parre, Noora; Aykanat, Tutku; Erkinaro, Jaakko; Primmer, Craig R.

doi:10.1101/780437

Cited by 14 publications

(21 citation statements)

References 48 publications

(1 reference statement)

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“…These results demonstrate that the vgll3 � E allele associated with young sea-age at maturity in natural populations is associated with earlier maturation also in controlled conditions, and also supports stronger dominance of vgll3 � E allele as observed in males from natural populations [4]. Seeing that concurring results were observed in another wild-derived stock of Atlantic salmon [30], the genotype-phenotype association between vgll3 and maturation timing is reproducible in controlled conditions and likely common in North-European strains of Atlantic salmon.…”

Section: Vgll3 Genotype Predicts Male Maturation Probabilitysupporting

confidence: 85%

“…We controlled-crossed eight 2x2 factorial matings of unrelated individuals that each included one vgll3 � EE and one vgll3 � LL male and female (see ref [30] for genotyping details), thereby resulting in 32 families with reciprocal vgll3 genotypes EE, EL, LE and LL (allele order denotes female and male parents of origin respectively, S1 Fig). We used parents from the "Oulujoki" broodstock, which is a mixture of several salmon populations from northern Baltic rivers and is maintained by the Natural Resources Institute Finland (LUKE) [56].…”

Section: Crosses Used In the Studymentioning

confidence: 99%

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Cis-regulatory differences in isoform expression associate with life history strategy variation in Atlantic salmon

et al. 2020

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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.

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Section: Vgll3 Genotype Predicts Male Maturation Probabilitysupporting

confidence: 85%

Section: Crosses Used In the Studymentioning

confidence: 99%

Cis-regulatory differences in isoform expression associate with life history strategy variation in Atlantic salmon

et al. 2020

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“…The so‐called vgll3 and six6 genomic regions are named after the most prominent genes in their respective haploblocks on chromosomes 25 and 9 respectively. The vgll3 genomic region on chromosome 25 has been shown to be associated with age at maturity (intially by GWAS, see: Ayllon et al., 2015; Barson et al., 2015), iteroparity (Aykanat et al., 2019) and precocious male maturation in Atlantic salmon (Debes et al., 2019; Lepais, Manicki, Glise, Buoro, & Bardonnet, 2017). This genomic region also exhibits strong spatial divergence (Barson et al., 2015; Pritchard et al., 2018), and it has recently been shown to have been affected by natural selection over the last 36 years (equivalent to 4–6 salmon generations) in parallel to the changing age structure in a large salmon population (Czorlich et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Life‐history genomic regions explain differences in Atlantic salmon marine diet specialization

Aykanat

Rasmussen

Ozerov

et al. 2020

Journal of Animal Ecology

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Animals employ various foraging strategies along their ontogeny to acquire energy, and with varying degree of efficiencies, to support growth, maturation and subsequent reproduction events. Individuals that can efficiently acquire energy early are more likely to mature at an earlier age, as a result of faster energy gain which can fuel maturation and reproduction. 2. We aimed to test the hypothesis that heritable resource acquisition variation that co-varies with efficiency along the ontogeny would influence maturation timing of individuals. 3. To test this hypothesis, we utilized Atlantic salmon as a model which exhibit a simple, hence trackable, genetic control of maturation age. We then monitored the variation in diet acquisition (quantified as stomach fullness and composition) of individuals with different ages, and linked it with genomic regions (haploblocks) that were previously identified to be associated with age-atmaturity. 4. Consistent with the hypothesis, we demonstrated that one of the life history genomic regions tested (six6) was indeed associated with age-dependent differences in stomach fullness. Prey composition was marginally linked to six6 and suggestively but non-significantly to vgll3 genomic regions. We further

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“…One large effect QTL was found on chromosome 25 that explained 20.6% of the variation in male parr maturation threshold values (Lepais et al, 2017). This QTL region spans the vgll3 gene, which has been previously identified as a large-effect locus for Atlantic salmon sea age (Ayllon et al, 2015;Barson et al, 2015) and its association with male parr maturation has recently been further supported in controlled experiments in several salmon populations (Debes et al, 2019;Verta et al, 2020). This result strongly suggests that the vgll3 locus plays a key role in sexual maturity in the freshwater phase.…”

Section: Freshwater Phasementioning

confidence: 79%

“…During the decades that followed, evidence for heritability of maturation processes has accumulated (reviewed in Garcia de Leaniz et al, 2007). For example, the timing of smoltification (Páez et al, 2011), sea age at maturity (Gjerde, 1984;Reed et al, 2018;Sinclair-Waters et al, 2020), and male parr maturation (Debes et al, 2019) all have high heritabilities. These results have generated interest in elucidating genomic regions and molecular functions linked to maturation traits.…”

Section: Genetics Of Maturationmentioning

confidence: 99%

Maturation in Atlantic salmon (Salmo salar, Salmonidae): a synthesis of ecological, genetic, and molecular processes

Mobley¹,

Aykanat²,

Czorlich³

et al. 2020

Preprint

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Over the past decades, Atlantic salmon (Salmo salar, Salmonidae) has emerged as a model system for sexual maturation research, owing to the high diversity of life history strategies, knowledge of trait genetic architecture, and their high economic value. The aim of this synthesis is to summarize the current state of knowledge concerning maturation in Atlantic salmon, outline knowledge gaps, and provide a roadmap for future work. Our summary of the current state of knowledge: 1) maturation in Atlantic salmon takes place over the entire life cycle, starting as early as embryo development, 2) variation in the timing of maturation promotes diversity in life history strategies, 3) ecological and genetic factors influence maturation, 4) maturation processes are sex-specific and may have fitness consequences for each sex, 5) genomic studies have identified large-effect loci that influence maturation, 6) the brain-pituitary-gonadal axis regulates molecular and physiological processes of maturation, 7) maturation is a key component of fisheries, aquaculture, conservation, and management, and 8) climate change, fishing pressure, and other anthropogenic stressors likely have major effects on salmon maturation. In the future, maturation research should focus on a broader diversity of life history stages, including early embryonic development, the marine phase and return migration. We recommend studies combining ecological and genetic approaches will help disentangle their relative contributions to maturation. Functional validation of large-effect loci should reveal how these genes influence maturation. Finally, continued research in maturation will improve our predictions concerning how salmon may adapt to fisheries, climate change, and other future challenges.

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Large single-locus effects for maturation timing are mediated via body condition in Atlantic salmon

Cited by 14 publications

References 48 publications

Cis-regulatory differences in isoform expression associate with life history strategy variation in Atlantic salmon

Cis-regulatory differences in isoform expression associate with life history strategy variation in Atlantic salmon

Life‐history genomic regions explain differences in Atlantic salmon marine diet specialization

Maturation in Atlantic salmon (Salmo salar, Salmonidae): a synthesis of ecological, genetic, and molecular processes

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