Craig Robert Primmer

Fitness-related traits are shaped by both additive and nonadditive genetic effects, resulting in a complex and context-dependent genetic architecture. However, the relative contribution of these components remains poorly understood, particularly for major-effect loci underlying life-history traits. In this study, we investigated the additive genetic contributions and potential epistatic interactions between 2 unlinked major-effect loci, vgll3 and six6, that influence age-at-maturity in Atlantic salmon (Salmo salar). By crossing parents heterozygous at both loci to create and rear 6 large full-sib families in a common-garden environment, we assessed male maturation, and additional fitness-related traits, 1-year post fertilization. We found that vgll3 and six6 significantly influenced maturation probability in an additive manner, with the likelihood of early maturation increasing with the number of early-maturing (E) alleles. Double homozygote males with 4 E alleles, vgll3*EE;six6*EE, showed an estimated 60% probability of maturation, compared with only a 20% probability for double late (L) homozygotes, vgll3*LL;six6*LL. Models accounting for the interaction showed no evidence of epistasis between vgll3 and six6, supporting an additive relationship. Additionally, body condition differed by maturation status in a genotype-dependent manner, particularly at vgll3. Studied here in combination for the first time under controlled common-garden settings, we show that vgll3 and six6 contribute additively to the regulation of male maturation age in Atlantic salmon. This work, which complements earlier studies conducted separately on these 2 loci, shows the importance of distinguishing additive from nonadditive genetic effects when dissecting the genetic architecture of fitness-related traits, as this distinction is fundamental for quantifying heritable variation and more accurately predicting evolutionary responses to selection.

Parental qualities can influence the development and fitness of their offspring via genetic and non-genetic effects. Although these effects are often linked to parental phenotypes, the effect of parental genetic variation linked with relevant phenotypes is less well understood. We performed full factorial crosses based on parental genotypes for an age-at-maturity-related gene, vgll3, to investigate how the parental genotypes influence Atlantic salmon ( Salmo salar ) offspring survival, growth, and development in their early life. Beyond the connection with age at maturity, the additional association between vgll3 and body condition in Atlantic salmon offers a potential pathway by which the maternal vgll3 genotype could influence offspring early life fitness. Combined with measurements of maternal phenotype and egg characteristics, the crossing design therefore allowed us to disentangle the maternal and paternal genetic and non-genetic contributions to variation in offspring survival and phenotypic traits. The phenotypic traits measured were hatching length and yolk sac area, growth, and yolk sac consumption and conversion efficiency. Parental vgll3 genotype did not influence the majority of our measured egg traits or alevin traits except for a genetic effect of paternal vgll3 genotype on offspring survival, whereby the paternal late maturation allele was associated with higher survival. Maternal effects were strongest for survival and for traits associated with hatching and weaker for alevin growth and yolk sac usage. Paternal effects on the measured alevin traits were negligible. The results from our study demonstrate that both maternal and paternal effects have the potential to influence offspring early life fitness traits.

Local adaptation is often portrayed as uniform fitness disadvantages of immigrants relative to locals. Yet dispersal costs vary with origin, sex and life-history traits, shaping the balance between gene flow and adaptation. We quantified these heterogeneous costs by comparing the reproductive success (RS) of local and immigrant individuals using a 15-year genetic pedigree of Atlantic salmon (Salmo salar), including over 1100 adults and 3400 juveniles. Immigrants represented 19.5% of adults, showed male-biased dispersal and averaged 15% lower RS than locals. However, outcomes were strongly origin-dependent: immigrants from some populations suffered severe fitness costs while others matched or exceeded locals. Sex and life-history further modulated RS: male immigrants underperformed local males, whereas multi-sea-winter females often equalled or outperformed local females. Immigrant males partially compensated their lower RS by acquiring more mates. These findings highlight that philopatry and local adaptation are reciprocally linked, while showing that the origin of immigrants strongly modulates the fitness costs that shape gene flow–adaptation dynamics.

Intraspecific competition due to for example, density, has substantial influence on fitness dynamics and life histories, but the underlying physiological mechanisms are often complex and the molecular basis unclear. Further, designing laboratory experiments to measure physiological responses that reflect natural conditions is challenging. Here, we reared Atlantic salmon juveniles in semi‐wild conditions in two densities to investigate the molecular mechanism of density‐related changes in the hypothalamus, a key brain region regulating stress and energy homeostasis. We measured density‐dependent changes in the expression of 12 genes involved in appetite and stress regulation and 16 genes involved in post‐transcriptional regulation of gene expression via m ⁶ A RNA methylation. We also quantified genotype‐environment interactions between density and two major life‐history loci, vgll3 and six6 . We found significant density‐related differences in the expression of genes coding for corticotropin‐releasing factors, appetite stimulators and inhibitors and m ⁶ A RNA methylation actors. Moreover, a paralogue of an appetite inhibitor showed a density‐dependent pattern that was the opposite of what was expected. Six6 locus was also associated with changes in the expression of epitranscriptomic markers, including two writers and one eraser. Our results highlight that individuals' response to density in natural conditions is shaped by a complex interplay between stress, appetite and epitranscriptomic pathways in the hypothalamus. In addition, the functional divergence of paralogs indicates a potential role of genome duplication shaping such a response. We emphasise the value of integrating different physiological responses at the molecular level to better understand ecological processes affected by environmental change.

Atlantic Salmon life-histories are shaped by interactions between environmental and genetic factors. The mitochondrial NADP-dependent malic enzyme ( me3 or mMEP-2), historically described as a polymorphic allozyme varying across populations, has been associated with age at maturity in wild populations. However, more recently, other loci ( vgll3 and six6) have also been shown to influence age at maturity, and studies disentangling their relative effects are lacking. This is especially important given that me3 and vgll3 are located on the same chromosome. Here, we used a common-garden experiment to investigate the impact of the me3 locus on male parr maturation probability in a Finnish population while accounting for variation at the vgll3 and six6 loci. Although we found linkage disequilibrium between the me3 and vgll3 loci, me3 remained moderately associated with maturation probability even when vgll3 genotype was accounted for. Together, these results support observations from wild populations of a genetic effect of me3 on maturation probability, but they also highlight the importance of considering both me3 and vgll3 when investigating the mechanism linking these loci to maturation.

Background: Sexual maturation is a key developmental process important for reproductive success. Understanding the molecular mechanisms behind variation in sexual maturation can provide insights into reproductive biology and how life history variation is encoded in the genome. Atlantic salmon ( Salmo salar ) has become an excellent sexual maturation research model due to its diversity of life history strategies and its ecological and economic importance. A major challenge has been the lack of a comprehensive transcriptional investigation of reproductive tissues that captures the dynamic transcriptional changes across individuals, tissues, and developmental stages. Long non-coding RNAs (lncRNAs) also play crucial roles in maturation, yet their functions in salmon maturation remain underexplored. Results: In this study, we sequenced 98 transcriptomes and found substantial transcriptomic complexity in the gonad and pituitary tissues of Atlantic salmon. We identified transcripts corresponding to 2,364 putative newly characterized protein-coding genes and 4,421 putative long intergenic non-coding RNAs (lincRNAs), many with tissue-specific expression. Gene co-expression network analysis (WGCNA) revealed tissue-specific gene network modules, linked to GO terms including Wnt signaling in immature testis, lipid metabolism, and cilia assembly in mature testis, ribosome biogenesis and DNA repair in the ovary, and hormone activity in pituitary. We identified new copies of known genes, such as gh1 , pou3f2 , and ier5 associated with the regulation of gonadal and pituitary functions. Some lncRNAs and their nearest genes showed correlated expression within modules, suggesting potential regulatory roles. Candidate lincRNAs indicated cis-acting regulatory potential on genes like tnfrsf11b and fgl1 , which are implicated in immune privilege during gonadal development and sperm quality control. Conclusions: Our study provides a comprehensive transcriptomic analysis of Atlantic salmon gonad and pituitary tissues, significantly improving the functional annotation of the Atlantic salmon genome. These findings reveal key regulatory pathways and novel molecular players involved in sexual maturation, particularly in the testis. Importantly, our study highlights the regulatory potential of lncRNAs in reproductive biology and maturation age variation, advancing our understanding of the molecular mechanisms governing sexual maturation. They further unlock future gene expression analyses and regulatory network reconstruction for dissecting the roles of lncRNAs in Atlantic salmon life history variation.

A new single nucleotide polymorphism (SNP) panel for genetic stock identification in the Teno river Atlantic salmon, Salmo salar L., fishery was developed, with a view to improving on an existing microsatellite panel. Twenty‐two genetically differentiated reporting units were proposed based on population genetic analyses of 1212 individuals collected at 37 locations in the river and genotyped for >33,000 genome‐wide SNPs. A small subset of these SNPs was selected for genetic stock identification (GSI) using an iterative process that considered their diversity and differentiation across reporting units. A genotyping‐by‐sequencing assay was developed to simultaneously genotype 180 of these GSI SNPs plus a sexing marker. This new SNP panel showed comparative GSI power to the microsatellite panel, with anticipated improvements in terms of cost, speed and robustness, and transferability across laboratories and genotyping platforms. Mixed‐stock analysis of the 2018 Teno river salmon catch using the new panel inferred that all 22 reporting units contributed to the fishery. Estimated catch proportions positively scaled with an independent estimate of reporting unit productivity: target spawning female biomass. This demonstrates the usefulness and efficiency of the 180 SNP panel for Atlantic salmon GSI in the Teno river system. If conducted on a regular basis, GSI can enable fine‐tuning of management strategies to promote sustainable fishing.

Heterochrony, or shifts in developmental timing, drives phenotypic diversity within and between species and shapes life history traits that can be selected for in changing environments, which in turn promotes population resilience. Mutations in heterochronic genes that regulate these processes can induce stable timing shifts, impacting important life history traits such as pubertal timing. Age at maturity is a key adaptive trait across species, with vestigial-like family member 3 (vgll3), a Hippo pathway cofactor, as a main determinant in Atlantic salmon. Recent studies show that early (E) and late (L) vgll3 alleles affect reproductive gene expression in salmon, reinforcing its role in regulating developmental timing. This study examines whether vgll3 influences testicular heterochrony in Atlantic salmon by analyzing gene expression related to the Hippo pathway. We observed heterochronic divergence in Hippo pathway gene transcription, indicating accelerated changes linked to spermatogenesis in vgll3*EE individuals. Our results position vgll3 as a heterochronic gene with a key role in regulating developmental timing in salmon.

The Näätämö River, in the far north of Europe, hosts a large Atlantic salmon (Salmo salar) stock with high socio-economic value. The catchment has near-pristine environmental conditions, although there are recent signs of stock declines. It nevertheless offers a good opportunity to monitor the status of a near pristine wild salmon system. This study aimed to characterize the fine-scale genetic structure of Atlantic salmon in the Näätämö River and evaluated the possibility to assign individuals to their population of origin. We genotyped juveniles sampled from eight locations using a 60 K single nucleotide polymorphism (SNP) panel to characterize within-river genetic diversity and structure. We also tested the performance of a previously designed 180 SNP panel to assign individuals to their population of origin. The genetic structure of the Näätämö River salmon population appears weak (F_ST ranging from 0.001–0.035), possibly due to natural straying. The performance of the predesigned panel in assigning individuals to their population of origin was moderate to high (82–85%), but customization could further enhance its accuracy. Additionally, we described the life-history diversity of salmon within the river using a long-term scale archive of c. 22,000 individuals collected over 48 years, identifying 59 unique life-history strategies. We suggest that to protect the self-sustaining salmon population in the Näätämö River, it would be important to manage the salmon fishery and conserve the population by incorporating up-to-date knowledge of stock status, considering their genetic structure, substantial gene flow and diverse life history.