Refining the genomic location of SNP variation affecting Atlantic salmon maturation timing at a key large-effect locus

Sinclair-Waters, Marion; Piavchenko, Nikolai; Ruokolainen, Annukka; Aykanat, Tutku; Erkinaro, Jaakko; Primmer, Craig R.

doi:10.1101/2021.04.26.441431

Cited by 8 publications

(7 citation statements)

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“…In addition to underlying body condition variation may vgll3 also directly be involved in gonadal development via inhibition (Kjaerner‐Semb et al, 2018), whereby the different alleles associate with the expression variation of specific isoforms that may vary in their degree of maturation inhibition (Verta et al, 2020). Nonetheless, a final conclusion from our tentative results requires additional research, also because other plausible candidate genes close to vgll3 have been identified, such as akap11 (Ayllon et al, 2015; Barson et al, 2015; but see Sinclair‐Waters et al, 2021).…”

Section: Discussionmentioning

confidence: 85%

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

et al. 2021

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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.

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Section: Discussionmentioning

confidence: 85%

“…Nonetheless, a final conclusion from our tentative results requires additional research, also because other plausible candidate genes close to vgll3 have been identified, such as akap11(Ayllon et al, 2015;Barson et al, 2015; but seeSinclair-Waters et al, 2021).…”

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confidence: 88%

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

et al. 2021

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“…Atlantic salmon used for this study were a subset of individuals used in Sinclair-Waters et al, 2021. Offspring used for this study were selected from a single family resulting from crossing unrelated parents (Kymijoki origin, F1 hatchery generation) with heterozygous (vgll3*EL) genotypes, thus enabling assessment of expression patterns of all vgll3 genotypes within a similar genetic background.…”

Section: Animal Materials and Genotypingmentioning

confidence: 99%

“…In Atlantic salmon, the vestigial-like family member 3 gene (vgll3) is strongly associated with maturation timing in the wild in both sexes but also exhibits sex-specific maturation effects (Barson et al, 2015;Czorlich et al, 2018). This association between vgll3 and maturation probability has been subsequently validated in one year-old males in common garden settings (Debes et al, 2021;Sinclair-Waters et al, 2021;Verta et al, 2020). This makes vgll3 a potential candidate regulating reproductive axis genes in place of the absent gnrh1, however, the molecular details of the action of vgll3 on reproductive axis genes has remained unexplored.…”

Section: Introductionmentioning

confidence: 99%

Strong regulatory effects of vgll3 genotype on reproductive axis gene expression in immature male Atlantic salmon

Ahi

Sinclair-Waters

Moustakas-Verho

et al. 2021

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Age at maturity is a major contributor to the diversity of life history strategies in organisms. The process of maturation is influenced by both genetics and the environment, and includes changes in levels of sex hormones and behavior, but the specific factors leading to variation in maturation timing are not well understood. gnrh1 regulates the transcription of gonadotropin genes at the onset of puberty in many species, but this gene is lacking in certain teleost species including Atlantic salmon (Salmo salar), which raises the possibility of the involvement of other important regulatory factors during this process. Earlier research has reported a strong association of alternative alleles of the vgll3 gene with maturation timing in Atlantic salmon, suggesting it as a potential candidate regulating reproductive axis genes. Here, we investigated the expression of reproductive axis genes in immature Atlantic salmon males with different vgll3 genotypes during the spawning period. We detected strong vgll3 genotype-dependent differential expression of reproductive axis genes (such as fshb, lhb, amh and igf3) tested in the pituitary, and testis of one-year-old immature male Atlantic salmon. In addition, we observed differential expression of jun (ap1) and nr5a1b (sf1), potential upstream regulators of gonadotropins in the pituitary, as well as axin2, id3, insl3, itch, ptgs2a and ptger4b, the downstream targets of amh and igf3 in the testis. Hereby, we provide evidence of strong vgll3 genotype-dependent transcriptional regulation of reproductive axis genes prior to sexual maturation together with models for distinct actions of vgll3 genotypes on the molecular processes controlling spermatogenesis in Atlantic salmon.

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“…A fin clip was taken from the caudal fin and stored in ethanol for verifying the vgll3 genotype and for sex determination. We used Kompetitive allelespecific polymerase chain reaction (KASP TM , LGC, UK) assays (He et al, 2014) for the vgll3TOP SNP and the sex-specific SDY locus as described in (Sinclair-Waters et al, 2021).…”

Section: Respirometry Detailsmentioning

confidence: 99%

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

Åsheim

Prokkola

Morozov

et al. 2021

Preprint

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Atlantic salmon (Salmo salar) is a species with diverse life-history strategies, to which the timing of maturation contributes considerably. Recently, the genome region including the gene vgll3 has gained attention as a locus with a large effect on salmon maturation timing, and recent studies on the vgll3 locus in salmon have indicated that its effect might be mediated through body condition and accumulation of adipose tissue. However, the cellular and physiological pathways leading from vgll3 genotype to phenotype are still unknown. Standard metabolic rate is a potentially important trait for resource acquisition and assimilation and we hypothesized that this trait, being a proxy for the maintenance energy expenditure of an individual, could be an important link in the pathway from vgll3 genotype to maturation-timing phenotype. As a first step to studying links between vgll3 and the metabolic phenotype of Atlantic salmon, we measured the standard metabolic rate of 150 first year Atlantic salmon juveniles of both sexes, originating from 14 different families with either late maturing or early maturing vgll3 genotypes. No significant difference in mass-adjusted standard metabolic rate was detected between individuals with different vgll3 genotypes, indicating that juvenile salmon of different vgll3 genotypes have similar maintenance energy requirements in the experimental conditions used and that the effects of vgll3 on body condition and maturation are not strongly related to maintenance energy expenditure in either sex at this life stage.

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Refining the genomic location of SNP variation affecting Atlantic salmon maturation timing at a key large-effect locus

Cited by 8 publications

References 50 publications

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

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

Strong regulatory effects of vgll3 genotype on reproductive axis gene expression in immature male Atlantic salmon

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

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