Biology subjects

Primmer, C. R.

Publications and source records attributed to Primmer, C. R..

At least 37 records · Page 2Linked to original sources

bioRxiv2023

Genotype-specific variation in seasonal body condition at a large-effect maturation locus

O_LIOrganisms utilize varying lipid resource allocation strategies as a means to survive seasonal environmental changes and life-history stage transitions. In Atlantic salmon, a certain lipid threshold is needed to initiate sexual maturation. Because of this, an individuals maturation schedule may be affected by changes in temperature and food availability across the seasons that create natural fluctuations of lipid reserves. C_LIO_LIRecent studies have found a genome region, including the gene vgll3, that explains a large proportion of variation for size and age at maturity. Vgll3 encodes a transcription co-factor that acts as an inhibitor of adipogenesis in mice and also affects condition factor and other phenotypes in juvenile salmon. However, even with many studies investigating varying temperature effects, there is a lack of temporal studies examining the effects of seasonality on such phenotypes, nor have the effects of vgll3 genotype on condition factor and maturation in different temperatures at different life stages. C_LIO_LIHere, we investigate the influence of different larval and juvenile incubation temperatures, vgll3 genotype and their interactions on juvenile salmon phenotypes including body condition, and sexual maturation rate. We reared Atlantic salmon for 2 years in varying temperatures with an average 1.76 {degrees}C difference between warm and cold treatments in four different larval-juvenile phase treatment groups (Warm-Warm, Warm-Cold, Cold-Warm, and Cold-Cold) until the first occurrence of maturation in males. C_LIO_LIWe found no effect of larval temperature on the measured phenotypes or maturation rate, suggesting the occurrence of growth compensation over the course of the experiment. Agreeing with previous studies, an increased maturation rate was observed in individuals of the warm juvenile temperature treatment. C_LIO_LIIn addition, we observed differences in condition factor associated with vgll3 genotype, whereby vgll3*EE individuals (the genotype associated with early maturation) had a less variable condition factor across the seasons compared to the vgll3*LL (associated with late maturation) individuals. C_LIO_LIThis result suggests a vgll3 influence on resource acquisition and allocation strategies, possibly linked with the early maturation process, with individuals carrying the early maturation vgll3 genotype having a higher early maturation rate and a higher condition factor in the spring. C_LI

evolutionary biology↗

bioRxiv2022

Temperature and dietary energy content influence female maturation age and egg nutritional content in Atlantic salmon

The environment experienced by a female influences reproductive traits in many species of fish. Environmental factors such as temperature and diet are not only important mediators of female maturation and reproduction but also of egg traits and offspring fitness through maternal provisioning. In this study, we use three-year-old, tank-reared, Atlantic salmon from two Finnish populations to investigate the effect of temperature and diet on maturation and egg traits. We show that a temperature difference of 2{degrees}C is sufficient to delay maturation in female Atlantic salmon whereas a 22% reduction in dietary energy content had no effect on maturation. Diet did not influence the body size, condition, or fecundity of the mature females or the size or protein content of the eggs. However, a higher energy diet increased egg lipid content. Neither female body size nor condition were associated with egg size or fat/protein composition. Our results indicate that female salmon that have a poorer diet in terms of energy content may have a reproductive disadvantage due to lower energy provisioning of eggs. This disadvantage has the potential to translate into fitness consequences for their offspring.

ecology↗

bioRxiv2022

Expression of m6A RNA methylation markers in the hypothalamus of Atlantic salmon

Methylation at the N6-position of adenosine, m6A, is the most abundant mRNA modification in eukaryotes. It is a highly conserved universal regulatory mechanism controlling gene expression in a myriad of biological processes. The role of m6A methylation in sexual maturation, however, has remained largely unexplored. While the maturation process is known to be affected by many genetic and environmental factors, the molecular mechanisms causing variation in the timing of maturation are still poorly understood. Hence, investigation of whether a widespread mechanism like m6A methylation could be involved in controlling of the maturation timing is warranted. In Atlantic salmon (Salmo salar), two genes associated with the age at maturity in human, vgll3 and six6, have been shown to play an important role in maturation timing. In this study, we investigated the expression of 16 genes involved in the regulation of m6A RNA methylation in the hypothalamus of Atlantic salmon with different homozygous combinations of late (L) and early (E) alleles for vgll3 and six6 genes. We found differential expression of ythdf2.2 which encodes an m6A modification reader and promotes mRNA degradation. Its expression was higher in six6*LL compared to other genotypes as well as immature males compared to matures. In addition, we found that the expression levels of genes coding for an eraser, alkbh5, and for a reader, ythdf1, were higher in the hypothalamus of females than in males across all the different genotypes studied. Our results indicate a potential role of the m6A methylation process in sexual maturation of Atlantic salmon, and therefore, provide the first evidence for such regulatory mechanism in the hypothalamus of any vertebrate. Investigation of additional vertebrate species is warranted in order to determine the generality of these findings.

molecular biology↗

bioRxiv2022

Adipose tissue mitochondrial respiration in Atlantic salmon: implications for sex-dependent life-history variation

Adipose tissue is essential for energy homeostasis, with mitochondria having a central role in its function. Mitochondria-mediated white adipose tissue dysfunction has been linked to several metabolic disorders in humans but surprisingly little is known about natural variation in mitochondrial function in wild animal populations, and its evolutionary significance. Early sexual maturation (low age-at-maturity) in Atlantic salmon (Salmo salar) is promoted by higher adiposity and has a strong genetic association with the vgll3 locus. This makes Atlantic salmon a convenient wild model to study the potential role of mitochondria-mediated adipose tissue processes in relation to the timing of maturation. Yet, mitochondrial respiration has not been measured in the adipose tissue in fish, and the lack of data is restricting the development of informed hypotheses. Here, using 13 Atlantic salmon individuals reared in common-garden conditions, we first verified the feasibility of measuring mitochondrial respiration in the adipose tissue. As expected, the respiration level was generally low, but nonetheless we successfully quantified its biological variation in the adipose tissue. Next, we analysed the potential association of mitochondrial respiration with mitochondrial DNA (mtDNA) content, adipocyte size, sex, and the vgll3 genotype. Despite low samples sizes, mitochondrial respiration, leak respiration, and coupling capacity (P/E ratio) were marginally significantly decreased in immature females carrying with the vgll3 early maturation compared to the alternative genotype. Based on these results, we suggested two new hypotheses on how the coupling capacity of oxidative phosphorylation could be linked with the timing of maturation via adiposity and pave the way to study the mechanistic relationships between life-history variation and mitochondrial bioenergetics in wild populations.

physiology↗

bioRxiv2022

Strong effects of temperature, population and age-at-maturity genotype on maturation probability for Atlantic salmon in a common garden setting

O_LIAge at maturity is a key life history trait and involves a trade-off between survival risk and reproductive investment, has close connections to fitness, and is an important factor for population structures. Temperature can have a dramatic influence on life history in ectotherms, but this influence may differ between populations. While an increasing number of studies have examined population-dependent reactions with temperature, few have investigated this in the context of maturation timing. C_LIO_LIAtlantic salmon is a highly relevant study species for improving understanding of this topic as it displays considerable variation in life-history strategies, including maturation timing. Additionally, a large amount of this variation in maturation timing has been associated with a genomic region including the strong candidate gene vgll3, but the effect of this gene in the context of different environments and populations has not been studied. C_LIO_LIUsing a large-scale common-garden experiment, we find strong effects of temperature, population, and vgll3 genotype on maturation in 2-year-old male Atlantic salmon. Observed maturation probability was 4.8 times higher in individuals reared at a mean temperature of 8.6{degrees}C compared to 6.9{degrees}C. This temperature effect was population-specific and was higher in the southern population compared to the northern population, potentially due to a higher intrinsic growth in the southern population as well as growth-temperature interaction. C_LIO_LIThe early-maturation vgll3*E associated with a significantly higher maturation probability, but there was no vgll3-interaction with temperature or population. C_LIO_LIBoth body condition and body mass associated strongly with maturation; the body-condition association was stronger in fish carrying the vgll3*E allele, and the body mass association was only present in the warm treatment. C_LIO_LIOur findings demonstrate that the relative effect of vgll3 on maturation timing is similar for two populations and two thermal environments and gives new perspectives on the relative effect of vgll3 compared to such influences. Additionally, we show that populations can vary in their response to temperature change in terms of maturation timing, and that high intrinsic growth could potentially be associated with higher thermal sensitivity for life history variation. C_LI

evolutionary biology↗

bioRxiv2022

A pituitary gene network linking vgll3 to regulators of sexual maturation in male Atlantic salmon

Age at maturity is a key life history trait and a significant contributor to life history strategy variation. The maturation process is complex and influenced by genetic and environmental factors alike, but specific causes of variation in maturation timing remain elusive. In many species, the increase in the regulatory gonadotropin-releasing hormone 1 (GnRH1) marks the onset of puberty. Atlantic salmon, however, lack the gene encoding GnRH1, suggesting other regulatory factors are involved in the maturation process. Earlier research in Atlantic salmon has found a strong association between alternative alleles of vgll3 and maturation timing, making vgll3 a candidate reproductive axis gene regulator. Recently we reported strong induction of gonadotropin encoding genes (fshb and lhb) in the pituitary of male Atlantic salmon homozygous for the vgll3 allele linked with the early maturation allele (E). The induction of gonadotropins was accompanied by increased expression of their direct upstream regulators, c-jun and sf1 (nr5a1b) in the pituitary. In mammals, the transcriptional activation of c-jun and sf1 is also required for induction of fshb and lhb, however, GnRH1 is responsible for increased transcriptional activity of c-jun and sf1. The absence of gnrh1 in salmon raises the possibility of the involvement of other regulators upstream of these factors. In this study, we investigated such a possibility through a stepwise approach for identifying a gene regulatory network (GRN) containing c-jun and sf1 and using the zebrafish coexpression database and transcription factor motif enrichment analysis. We found a GRN containing c-jun with predicted upstream regulators, e2f1, egr1, foxj1 and klf4, which are also differentially expressed in the pituitary. Finally, we suggest a model for transcriptional regulation of c-jun and sf1in the absence of gnrh1 in the pituitary, which may have broader implications across vertebrates.

molecular biology↗

bioRxiv2021

Life-history genotype explains variation in migration activity in Atlantic salmon (Salmo salar).

One of the most important life-history continuums is the fast-slow axis, where "fast" individuals mature earlier than "slow" individuals. "Fast" individuals are predicted to be more active than "slow" individuals; high activity is required to maintain a fast life-history strategy. Recent meta-analyses revealed mixed evidence for such integration. Here, we test whether known life-history genotypes differ in activity expression by using Atlantic salmon (Salmo salar) as a model. In salmon, variation in Vgll3, a transcription co-factor, explains [~]40% of variation in maturation timing. We predicted that the allele related to early maturation (vgll3*E) would be associated with increased activity. We used an automated surveillance system to follow [~]1900 juveniles including both migrants and non-migrants (i.e. smolt and parr fish, respectively) in semi-natural conditions over 31 days ([~]580 000 activity measurements). Against our prediction, vgll3 did not explain variation in activity in pooled migrant and non-migrant data. However, in migrants, vgll3 explained variation in activity according to our prediction in a sex-dependent manner. Specifically, in females the vgll3*E allele was related to increasing activity, whereas in males the vgll3*L allele (later maturation allele) was related to increasing activity. These sex-dependent effects might be a mechanism maintaining within-population genetic life-history variation.

evolutionary biology↗

bioRxiv2021

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

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. Summary statementWe show that vgll3, a gene known to have significant effects on Atlantic salmon (Salmo salar) life-history strategy, does not associate with standard metabolic rate in salmon juveniles.

genetics↗

bioRxiv2021

Genetic coupling of life-history and aerobic performance in juvenile Atlantic salmon

A better understanding of the genetic and phenotypic architecture underlying life-history variation is a longstanding aim in biology. Theories suggest energy metabolism determines life-history variation by modulating resource acquisition and allocation trade-offs, but the genetic underpinnings of the relationship and its dependence on ecological conditions have rarely been demonstrated. The strong genetic determination of age-at-maturity by two unlinked genomic regions (vgll3 and six6) makes Atlantic salmon (Salmo salar) an ideal model to address these questions. Using more than 250 juveniles in common garden conditions, we quantified the covariation between metabolic phenotypes -standard and maximum metabolic rates (SMR and MMR), and aerobic scope (AS) - and the life-history genomic regions and tested if food availability modulates the relationships. We found that the early maturation genotype in vgll3 was associated with higher MMR and consequently AS. Additionally, MMR exhibited physiological epistasis; it was decreased when late maturation genotypes co-occurred in both genomic regions. Contrary to our expectation, the life-history genotypes had no effects on SMR. Further, food availability had no effect on the genetic covariation, suggesting a lack of genotype-by-environment interactions. Our results provide insights on the key organismal processes that link energy use at the juvenile-stage to age-at-maturity, indicating potential mechanisms by which metabolism and life-history can coevolve.

evolutionary biology↗

bioRxiv2021

Dissecting the loci underlying maturation timing in Atlantic salmon using haplotype and multi-SNP based association methods

Resolving the genetic architecture of fitness-related traits is key to understanding the evolution and maintenance of fitness variation. However, well-characterized genetic architectures of such traits in wild populations remain uncommon. In this study, we used haplotype-based and multi-SNP Bayesian association methods with sequencing data for 313 individuals from wild populations to further characterize known candidate regions for sea age at maturation in Atlantic salmon (Salmo salar). We detected an association at five loci (on chromosomes ssa06, ssa09, ssa21, and ssa25) out of 116 candidates previously identified in an aquaculture strain with maturation timing in wild Atlantic salmon. We found that at each of these five loci, variation explained by the locus was predominantly driven by a single SNP suggesting the genetic architecture of Atlantic salmon maturation includes multiple loci with simple, non-clustered alleles. This highlights the diversity of genetic architectures that can exist for fitness-related traits. Furthermore, this study provides a useful multi-SNP framework for future work using sequencing data to characterize genetic variation underlying phenotypes in wild populations.

evolutionary biology↗

bioRxiv2021

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

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, and thus enabling delineation of the influence of variation at these two genes on maturation timing. By rearing 5895 males to maturation age, of which 81% had recombinant vgll3/akap11 allelic combinations, we found that vgll3 SNP variation was strongly associated with maturation timing, whereas there was little or no association between akap11 SNP variation and maturation timing. These findings provide strong evidence supporting vgll3 as the primary candidate gene in the chromosome 25 locus for influencing maturation timing. This will help guide future research for understanding the genetic processes controlling maturation timing. This also exemplifies the utility of natural recombinants to more precisely map causal variation underlying ecologically important phenotypic diversity.

genetics↗

bioRxiv2021

Evolution in salmon life-history induced by direct and indirect effects of fishing

Understanding the drivers of evolution is a fundamental aim in biology. However, identifying the evolutionary impacts of human activities, both direct and indirect, is challenging because of lack of temporal data and limited knowledge of the genetic basis of most traits1. Atlantic salmon is a species exposed to intense anthropogenic pressures during its anadromous life cycle2. Previous research has shown that salmon age at maturity has evolved towards earlier maturation over the last 40 years, with an 18% decrease3 in the allele associated with late maturation at the large-effect vgll3 locus4; but the drivers of this change remain unknown. Here, we link genetic and phenotypic changes in a large Atlantic salmon population with salmon prey species biomass in the Barents Sea, temperature, and fishing effort in order to identify drivers of age at maturity evolution. We show that age at maturity evolution is associated with two different types of fisheries induced evolution acting in opposing directions: an indirect effect linked with commercial harvest of a salmon prey species (capelin) at sea (selection against late maturation), and a direct effect due to temporal changes in net fishing pressure in the river (surprisingly, selection against early maturation). Although the potential for direct and indirect evolutionary effects of fishing have been acknowledged, empirical evidence for induced changes at the genetic level has been lacking5. As capelin are primarily harvested to produce fish meal and oil for aquaculture6, we hereby identify an indirect path by which Atlantic salmon aquaculture may negatively affect wild populations.

evolutionary biology↗

bioRxiv2020

Genetic drift dominates genome-wide regulatory evolution following an ancient whole genome duplication in Atlantic salmon

Whole genome duplications (WGD) have been considered as springboards that potentiate lineage diversification through increasing functional redundancy. Divergence in gene regulatory elements is a central mechanism for evolutionary diversification, yet the patterns and processes governing regulatory divergence following events that lead to massive functional redundancy, such as WGD, remain largely unknown. We studied the patterns of divergence and strength of natural selection on regulatory elements in the Atlantic salmon (Salmo salar) genome, which has undergone WGD 100-80 Mya. Using ChIPmentation, we first show that H3K27ac, a histone modification typical to enhancers and promoters, is associated with genic regions, tissue specific transcription factor binding motifs, and with gene transcription levels in immature testes. Divergence in transcription between duplicated genes from WGD (ohnologs) correlated with difference in the number of proximal regulatory elements, but not with promoter elements, suggesting that functional divergence between ohnologs after WGD is mainly driven by enhancers. By comparing H3K27ac regions between duplicated genome blocks, we further show that a longer polyploid state post-WGD has constrained asymmetric regulatory evolution. Patterns of genetic diversity across natural populations inferred from re-sequencing indicate that recent evolutionary pressures on H3K27ac regions are dominated by largely neutral evolution. In sum, our results suggest that post-WGD functional redundancy in regulatory elements continues to have an impact on the evolution of the salmon genome, promoting largely neutral evolution of regulatory elements despite their association with transcription levels. These results highlight a case where genome-wide regulatory evolution following an ancient WGD is dominated by genetic drift. Significance statementRegulatory evolution following whole genome duplications (WGD) has been investigated at the gene expression level, but studies of the regulatory elements that control expression have been lacking. By investigating regulatory elements in the Atlantic salmon genome, which has undergone a whole genome duplication 100-80 million years ago, we discovered patterns suggesting that neutral divergence is the prevalent mode of regulatory element evolution post-WGD. Our results suggest mechanisms for explaining the prevalence of asymmetric gene expression evolution following whole genome duplication, as well as the mismatch between evolutionary rates in enhancers versus that of promoters.

evolutionary biology↗

bioRxiv2020

Sex-specific lipid profiles in muscle of Atlantic salmon juveniles

Energy allocation in juvenile fish can have important implications for future life-history progression. Inherited and environmental factors determine when and where individuals allocate energy, and timely and sufficient energy reserves are crucial for reaching key life stages involved in the timing of maturation and sea migration. In Atlantic salmon, lipid reserves are predominantly found in the viscera and myosepta in the muscle and have been shown to play a key role in determining the timing of maturity. This life-history trait is tightly linked to fitness in many species and can be different between males and females, however, the details of relative energy allocation in juveniles of different sexes is not well understood. Therefore, the aim of this study was to investigate the effects of sex, genetics and environment during juvenile development of salmon on the amount and composition of their lipid reserves. To do so, juvenile salmon were fed one of two different lipid food contents during their first summer and autumn under common-garden conditions. Muscle lipid composition and concentrations were determined by thin layer chromatography. The muscle lipid class concentrations covaried negatively with body length and males showed higher concentrations than females for phosphatidylcholine, cholesterol, sphingomyelin, and triacylglycerol. This sex-specific difference in major lipid classes presents a new scope for understanding the regulation of lipids during juvenile development and gives direction for understanding how lipids may interact and influence major life-history traits in Atlantic salmon.

molecular biology↗

bioRxiv2020

Heterogeneous genetic basis of age at maturity in salmonid fishes

Understanding the genetic basis of repeated evolution of the same phenotype across taxa is a fundamental aim in evolutionary biology and has applications to conservation and management. However, the extent to which interspecific life-history trait polymorphisms share evolutionary pathways remains under-explored. We address this gap by studying the genetic basis of a key life-history trait, age at maturity, in four species of Pacific salmon (genus Oncorhynchus) that exhibit intra- and interspecific variation in this trait - Chinook Salmon, Coho Salmon, Sockeye Salmon, and Steelhead Trout. We tested for associations in all four species between age at maturity and two genome regions, six6 and vgll3, that are strongly associated with the same trait in Atlantic Salmon (Salmo salar). We also conducted a genome-wide association analysis in Steelhead to assess whether additional regions were associated with this trait. We found the genetic basis of age at maturity to be heterogeneous across salmonid species. Significant associations between six6 and age at maturity were observed in two of the four species, Sockeye and Steelhead, with the association in Steelhead being particularly strong in both sexes (p = 4.46x10-9 after adjusting for genomic inflation). However, no significant associations were detected between age at maturity and the vgll3 genome region in any of the species, despite its strong association with the same trait in Atlantic Salmon. We discuss possible explanations for the heterogeneous nature of the genetic architecture of this key life-history trait, as well as the implications of our findings for conservation and management.

evolutionary biology↗

bioRxiv2020

The structural variation landscape in 492 Atlantic salmon genomes

Structural variants (SVs) are a major source of genetic and phenotypic variation, but remain challenging to accurately type and are hence poorly characterized in most species. We present an approach for reliable SV discovery in non-model species using whole genome sequencing and report 15,483 high-confidence SVs in 492 Atlantic salmon (Salmo salar L.) sampled from a broad phylogeographic distribution. These SVs recover population genetic structure with high resolution, include an active DNA transposon, widely affect functional features, and overlap more duplicated genes retained from an ancestral salmonid autotetraploidization event than expected. Changes in SV allele frequency between wild and farmed fish indicate polygenic selection on behavioural traits during domestication, targeting brain-expressed synaptic networks linked to neurological disorders in humans. This study offers novel insights into the role of SVs in genome evolution and the genetic architecture of domestication traits, along with resources supporting reliable SV discovery in non-model species.

genomics↗

bioRxiv2019

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

Maturation timing is a pivotal life-history trait balancing probabilities between mortality and reproduction. Environmental vs. genetic contributions to traits associated with maturation initiation, such as growth and body condition, remain uncertain because of difficulties in determining causality. In Atlantic salmon, maturation timing associates with a large-effect locus around vgll3, but how this locus affects maturation remains unknown. We combined controlled breeding with common-garden experimentation at two temperatures and show that vgll3 effects on maturation of males express primarily via body condition, which we demonstrate in the males non-maturing female relatives, thus avoiding reverse causality. Between homozygous vgll3 genotypes, maturation probability differed several folds and female condition differed 2% in both temperature environments. Vgll3 effects explained 25 and 16% of maturation probability heritability and 15 and 6% of female condition heritability, in the warm and cold environment, respectively. Non-significant vgll3 effects on female length were antagonistic to those on condition but of equal proportional size. When controlling for vgll3 effects, genetic correlations changed antagonistically between both maturation and condition vs. growth, suggesting vgll3 as a resource-allocation locus. The results support large vgll3 maturation effects being mediated via environmentally stable body condition effects, enabling rapid co-evolution between the life-history traits.

evolutionary biology↗

bioRxiv2019

Transcription profiles of age-at-maturity-associated genes suggest cell fate commitment regulation as a key factor in the Atlantic salmon maturation process

Despite recent taxonomic diversification in studies linking genotype with phenotype, follow-up studies aimed at understanding the molecular processes of such genotype-phenotype associations remain rare. The age at which an individual reaches sexual maturity is an important fitness trait in many wild species. However, the molecular mechanisms regulating maturation timing processes remain obscure. A recent genome-wide association study in Atlantic salmon (Salmo salar) identified large-effect age-at-maturity-associated chromosomal regions including genes vgll3, akap11 and six6, which have roles in adipogenesis, spermatogenesis and the hypothalamic-pituitary-gonadal (HPG) axis, respectively. Here, we determine expression patterns of these genes during salmon development and their potential molecular partners and pathways. Using Nanostring transcription profiling technology, we show development- and tissue-specific mRNA expression patterns for vgll3, akap11 and six6. Correlated expression levels of vgll3 and akap11, which have adjacent chromosomal location, suggests they may have shared regulation. Further, vgll3 correlating with arhgap6 and yap1, and akap11 with lats1 and yap1 suggests that Vgll3 and Akap11 take part in actin cytoskeleton regulation. Tissue-specific expression results indicate that vgll3 and akap11 paralogs have sex-dependent expression patterns in gonads. Moreover, six6 correlating with slc38a6 and rtn1, and Hippo signaling genes suggests that Six6 could have a broader role in the HPG neuroendrocrine and cell fate commitment regulation, respectively. We conclude that Vgll3, Akap11 and Six6 may influence Atlantic salmon maturation timing via affecting on adipogenesis and gametogenesis by regulating cell fate commitment and the HPG axis. These results may help to unravel general molecular mechanisms behind maturation.

genetics↗