Panu Orell

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

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.

Genome-wide SNP analysis reveals a genetic basis for sea-age variation in a wild population of Atlantic salmon (Salmo salar).

Delaying sexual maturation can lead to larger body size and higher reproductive success, but carries an increased risk of death before reproducing. Classical life history theory predicts that trade‐offs between reproductive success and survival should lead to the evolution of an optimal strategy in a given population. However, variation in mating strategies generally persists, and in general, there remains a poor understanding of genetic and physiological mechanisms underlying this variation. One extreme case of this is in the Atlantic salmon (Salmo salar), which can show variation in the age at which they return from their marine migration to spawn (i.e. their ‘sea age’). This results in large size differences between strategies, with direct implications for individual fitness. Here, we used an Illumina Infinium SNP array to identify regions of the genome associated with variation in sea age in a large population of Atlantic salmon in Northern Europe, implementing individual‐based genome‐wide association studies (GWAS) and population‐based FST outlier analyses. We identified several regions of the genome which vary in association with phenotype and/or selection between sea ages, with nearby genes having functions related to muscle development, metabolism, immune response and mate choice. In addition, we found that individuals of different sea ages belong to different, yet sympatric populations in this system, indicating that reproductive isolation may be driven by divergence between stable strategies. Overall, this study demonstrates how genome‐wide methodologies can be integrated with samples collected from wild, structured populations to understand their ecology and evolution in a natural context.

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

Despite decades of research assessing the genetic structure of natural populations, the biological meaning of low yet significant genetic divergence often remains unclear due to a lack of associated phenotypic and ecological information. At the same time, structured populations with low genetic divergence and overlapping boundaries can potentially provide excellent models to study adaptation and reproductive isolation in cases where high‐resolution genetic markers and relevant phenotypic and life history information are available. Here, we combined single nucleotide polymorphism (SNP)‐based population inference with extensive phenotypic and life history data to identify potential biological mechanisms driving fine‐scale subpopulation differentiation in Atlantic salmon (Salmo salar) from the Teno River, a major salmon river in Europe. Two sympatrically occurring subpopulations had low but significant genetic differentiation (FST = 0.018) and displayed marked differences in the distribution of life history strategies, including variation in juvenile growth rate, age at maturity and size within age classes. Large, late‐maturing individuals were virtually absent from one of the two subpopulations, and there were significant differences in juvenile growth rates and size at age after oceanic migration between individuals in the respective subpopulations. Our findings suggest that different evolutionary processes affect each subpopulation and that hybridization and subsequent selection may maintain low genetic differentiation without hindering adaptive divergence.

Single nucleotide polymorphisms to discriminate different classes of hybrid between wild Atlantic salmon and aquaculture escapees.

Many wild Atlantic salmon (Salmo salar) populations are threatened by introgressive hybridization from domesticated fish that have escaped from aquaculture facilities. A detailed understanding of the hybridization dynamics between wild salmon and aquaculture escapees requires discrimination of different hybrid classes; however, markers currently available to discriminate the two types of parental genome have limited power to do this. Using a high‐density Atlantic salmon single nucleotide polymorphism (SNP) array, in combination with pooled‐sample allelotyping and an Fst outlier approach, we identified 200 SNPs that differentiated an important Atlantic salmon stock from the escapees potentially hybridizing with it. By simulating multiple generations of wild–escapee hybridization, involving wild populations in two major phylogeographic lineages and a genetically diverse set of escapees, we showed that both the complete set of SNPs and smaller subsets could reliably assign individuals to different hybrid classes up to the third hybrid (F3) generation. This set of markers will be a useful tool for investigating the genetic interactions between native wild fish and aquaculture escapees in many Atlantic salmon populations.

Genomic signatures of fine-scale local selection in Atlantic salmon suggest involvement of sexual maturation, energy homeostasis and immune defence-related genes

Elucidating the genetic basis of adaptation to the local environment can improve our understanding of how the diversity of life has evolved. In this study, we used a dense SNP array to identify candidate loci potentially underlying fine‐scale local adaptation within a large Atlantic salmon (Salmo salar) population. By combining outlier, gene–environment association and haplotype homozygosity analyses, we identified multiple regions of the genome with strong evidence for diversifying selection. Several of these candidate regions had previously been identified in other studies, demonstrating that the same loci could be adaptively important in Atlantic salmon at subdrainage, regional and continental scales. Notably, we identified signals consistent with local selection around genes associated with variation in sexual maturation, energy homeostasis and immune defence. These included the large‐effect age‐at‐maturity gene vgll3, the known obesity gene mc4r, and major histocompatibility complex II. Most strikingly, we confirmed a genomic region on Ssa09 that was extremely differentiated among subpopulations and that is also a candidate for local selection over the global range of Atlantic salmon. This region colocalized with a haplotype strongly associated with spawning ecotype in sockeye salmon (Oncorhynchus nerka), with circumstantial evidence that the same gene (six6) may be the selective target in both cases. The phenotypic effect of this region in Atlantic salmon remains cryptic, although allelic variation is related to upstream catchment area and covaries with timing of the return spawning migration. Our results further inform management of Atlantic salmon and open multiple avenues for future research.

Short sea migration and precocious maturation in reared Atlantic salmon post-smolts in the northern Baltic Sea

Short sea migration and precocious maturation in reared Atlantic salmon post-smolts in the northern Baltic Sea Panu Orell*, Jaakko Erkinaro, Mikko Kiljunen, Jyrki Torniainen, Tapio Sutela, Mikko Jaukkuri, and Aki Mäki-Petäys Natural Resources Institute Finland, University of Oulu, PO Box 413, Oulu FI 90014, Finland Department of Biological and Environmental Science, University of Jyvaskyla, PO Box 35, Jyvaskyla FI 40014, Finland Natural History Museum, University of Jyvaskyla, PO Box 35, Jyvaskyla FI 40014, Finland *Corresponding author: tel: þ358 405305830; e-mail: panu.orell@luke.fi

Genetic correlation between sea age at maturity and iteroparity in Atlantic salmon.

Genetic correlations in life history traits may result in unpredictable evolutionary trajectories if not accounted for in life-history models. Iteroparity (the reproductive strategy of reproducing more than once) in Atlantic salmon (Salmo salar) is a fitness trait with substantial variation within and among populations. In the Teno River in northern Europe, iteroparous individuals constitute an important component of many populations and have experienced a sharp increase in abundance in the last 20 years, partly overlapping with a general decrease in age structure. The physiological basis of iteroparity bears similarities to that of age at first maturity, another life history trait with substantial fitness effects in salmon. Sea age at maturity in Atlantic salmon is controlled by a major locus around the vgll3 gene, and we used this opportunity demonstrate that the two traits are genetically correlated around this genome region. The odds ratio of survival until second reproduction was up to 2.4 (1.8-3.5 90% CI) times higher for fish with the early-maturing vgll3 genotype (EE) compared to fish with the late-maturing genotype (LL). The association had a dominance architecture, although the dominant allele was reversed in the late-maturing group compared to younger groups that stayed only one year at sea before maturation. Post hoc analysis indicated that iteroparous fish with the EE genotype had accelerated growth prior to first reproduction compared to first-time spawners, across all age groups, while this effect was not detected in fish with the LL genotype. These results broaden the functional link around the vgll3 genome region and help us understand constraints in the evolution of life history variation in salmon. Our results further highlight the need to account for genetic correlations between fitness traits when predicting demographic changes in changing environments.

Bayesian arrival model for Atlantic salmon smolt counts powered by environmental covariates and expert knowledge

Annual run size and timing of Atlantic salmon smolt migration was estimated using Bayesian model framework and data from six years of a video monitoring survey. The model has a modular structure. It separates sub-processes of departing, traveling and observing, of which the first two together define the arrival distribution. The sub-processes utilize biological background and expert knowledge about the migratory behavior of smolts and about the probability to observe them from the video footage under varying environmental conditions. Daily mean temperature and discharge were used as environmental covariates. The model framework does not require assuming a simple distributional shape for the arrival dynamics and thus also allows for multimodal arrival distributions. Results indicate that 20% - 43% of smolts passed the Utsjoki monitoring site unobserved during the years of study. Predictive studies were made to estimate daily run size in cases with missing counts either at the beginning or in the middle of the run, indicating good predictive performance.

Home ground advantage: selection against dispersers promotes cryptic local adaptation in wild salmon

A long-held, but poorly tested, assumption in natural populations is that individuals that disperse into new areas for reproduction are at a disadvantage compared to individuals that reproduce in their natal habitat, underpinning the eco-evolutionary processes of local adaptation and ecological speciation. Here, we capitalize on fine-scale population structure and natural dispersal events to compare the reproductive success of local and dispersing individuals captured on the same spawning ground in four consecutive parent-offspring cohorts of wild Atlantic salmon (Salmo salar). Parentage analysis conducted on adults and juvenile fish showed that local females and males had 9.6 and 2.9 times higher reproductive success than dispersers, respectively. Our results reveal how higher reproductive success in local spawners compared to dispersers may act in natural populations to drive population divergence and promote local adaptation over microgeographic spatial scales without clear morphological differences between populations.Individuals that disperse into new areas for reproduction are potentially at a disadvantage compared to residents that are locally adapted to environmental conditions. Such local adaptation has the potential to drive population divergence and ultimately speciation, yet quantifying the effect of dispersal on fitness is rarely investigated in the wild. Here we capitalize on fine-scale population structure and natural dispersal events to compare the reproductive success, and hence fitness, of local and dispersing individuals in multiple parent-offspring cohorts of wild Atlantic salmon (Salmo salar) in the Teno River, Finland. A total of 264 sexually mature adults and 5223 juvenile fish were captured on a large spawning ground of the Utsjoki tributary over four cohort years. Genetic population assignment identified adults that had migrated back to their natal spawning grounds (local) and individuals that originated from other populations within the system (dispersers). Parentage analysis of juveniles sampled on the spawning grounds the following spring demonstrated that local females and males had 9.6 and 2.9 times higher reproductive success than dispersers, respectively. No phenotypic differences in body size between local and dispersers were found. Thus, the forces driving selection against dispersal remain cryptic. Taken together, these results demonstrate that local salmon have a distinct fitness advantage over dispersers, revealing how local adaptation may act to drive population divergence without clear morphological differences or physical barriers to gene flow.

Rapid sex-specific evolution of age at maturity is shaped by genetic architecture in Atlantic salmon

Understanding the mechanisms by which populations adapt to their environments is a fundamental aim in biology. However, it remains challenging to identify the genetic basis of traits, provide evidence of genetic changes and quantify phenotypic responses. Age at maturity in Atlantic salmon represents an ideal trait to study contemporary adaptive evolution as it has been associated with a single locus in the vgll3 region and has also strongly changed in recent decades. Here, we provide an empirical example of contemporary adaptive evolution of a large-effect locus driving contrasting sex-specific evolutionary responses at the phenotypic level. We identified an 18% decrease in the vgll3 allele associated with late maturity in a large and diverse salmon population over 36 years, induced by sex-specific selection during sea migration. Those genetic changes resulted in a significant evolutionary response only in males, due to sex-specific dominance patterns and vgll3 allelic effects. The vgll3 allelic and dominance effects differed greatly in a second population and were likely to generate different selection and evolutionary patterns. Our study highlights the importance of knowledge of genetic architecture to better understand fitness trait evolution and phenotypic diversity. It also emphasizes the potential role of adaptive evolution in the trend towards earlier maturation observed in numerous Atlantic salmon populations worldwide.Age at maturity in Atlantic salmon has been associated with a single locus with sex-specific effects. Here, the authors show rapid evolution towards early maturity in males of a large salmon population induced by sex-specific selection during sea migration.