Eero Niemelä

Life-history and habitat features influence the within-river genetic structure of Atlantic salmon

Defining populations and identifying ecological and life‐history characteristics affecting genetic structure is important for understanding species biology and hence, for managing threatened or endangered species or populations. In this study, populations of the worlds largest indigenous Atlantic salmon (Salmo salar) stock were first inferred using model‐based clustering methods, following which life‐history and habitat variables best predicting the genetic diversity of populations were identified. This study revealed that natal homing of Atlantic salmon within the Teno River system is accurate at least to the tributary level. Generally, defining populations by main tributaries was observed to be a reasonable approach in this large river system, whereas in the mainstem of the river, the number of inferred populations was fewer than the number of distinct sampling sites. Mainstem and headwater populations were genetically more diverse and less diverged, while each tributary fostered a distinct population with high genetic differentiation and lower genetic diversity. Population structure and variation in genetic diversity among populations were poorly explained by geographical distance. In contrast, age‐structure, as estimated by the proportion of multisea‐winter spawners, was the most predictive variable in explaining the variation in the genetic diversity of the populations. This observation, being in agreement with theoretical predictions, emphasizes the essence of large multisea‐winter females in maintaining the genetic diversity of populations. In addition, the unique genetic diversity of populations, as estimated by private allele richness, was affected by the ease of accessibility of a site, with more difficult to access sites having lower unique genetic diversity. Our results show that despite this species’ high capacity for migration, tributaries foster relatively closed populations with little gene flow which will be important to consider when developing management strategies for the system.

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.

Behaviour of gill-net and rod-captured Atlantic salmon (Salmo salar L.) during upstream migration and following radio tagging

The behaviour of radio-tagged Atlantic salmon (Salmo salar L.) was studied in the River Ohcejohka in subarctic Finland. The objective was to determine the effects of gill-net entanglement and catch and release angling on the behaviour of upstream migrating salmon. 23 grilse and one 2 sea-winter (SW) salmon were tagged with radio transmitters and some were tracked for a period of over 3 months. Gill-net caught fish exhibited extensive downstream running, presumably caused by stress from capture and tagging. Post-tagging downstream movement in rod-caught salmon was also observed, but was not as extensive. Upstream migration was delayed in all tagged fish. The results of this study suggest that gill-net capture negatively impacts the upstream migration behaviour of Atlantic salmon and that the negative effects of capture and radio tagging can well exceed those proposed in current literature.

Temporally stable genetic structure and low migration in an Atlantic salmon population complex: implications for conservation and management

The evolutionary potential of a population is closely related to two key population genetic parameters, namely the effective population size (Ne) and migration rate (m). Furthermore, knowledge of these parameters is required in order to assess potential constraints on local adaptation and for the development of biologically sound management strategies. We addressed these key issues by investigating the temporal and spatial genetic structure of over 2000 adult Atlantic salmon (Salmo salar) collected from 17 sites in the Teno and Näätämö rivers in northernmost Europe with up to five time points spanning temporal intervals up to 24 years (∼4 generations). In all cases except one, local populations were found to be temporally stable within the river system. Estimates of Ne were generally a magnitude larger for the mainstem and headwater populations (MS+HW, Ne∼340–1200) than for the tributary populations (Ne∼35–160), thus explaining the higher genetic diversity and lower divergence of the MS+HW populations compared to tributaries. The overall migration rates to tributaries were low, and in some cases, low enough for local adaptations to potentially evolve, despite their lower Ne. Signs of a population bottleneck and natural recruitment from nearby populations were detected in one local population. This highlights a fact which is relevant for the conservation and management of highly substructured population systems in general: that even when the overall census size is large, local populations can be vulnerable to perturbations. To preserve the current and to regain the historical distribution of salmon within the river system, we propose that the status of the total population complex should be evaluated at the local population level rather than from descriptive statistics at the system level.

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.

Growth differences between the Atlantic salmon parr, Salmo salar, of nursery brooks and natal rivers in the River Teno watercourse in northern Finland

SynopsisA comparison was done between growth in Atlantic salmon,Salmo salar, parr from natal rivers and small tributaries in the subarctic River Teno watercourse in northern Finland (70° N, 28° E). Salmon do not spawn in these tributaries but juveniles enter the brooks from their spawning rivers. Parr from these brooks (age groups 1 + and 2 +) were larger, so were their recorded annual growth increments, than those caught simultaneously in the River Teno. First year growth was also better in brook parr, although both groups had spent their first year in the main river. The brook water temperature was lower than that in the main rivers through-out the growing season. On the other hand, drifting food resources were more abundant in brooks. It has been suggested that better growth and a longer residence in fresh water result in the larger smolts being produced in the brooks relative to the main river. Differences in habitat selection and subsequent differences in the smolt age and size of fish from the same place of origin reflect the distinct life histories of the salmon in the River Teno.

Temporally stable population-specific differences in run timing of one-sea-winter Atlantic salmon returning to a large river system

The understanding of migration patterns can significantly contribute to conservation and management. The spawning migrations of Atlantic salmon (Salmo salar) cover thousands of kilometers from the feeding areas at sea to their natal rivers to reproduce. Migrating salmon are exposed to intensive harvest, but little is known of the population‐specific differences in migration behavior. In this study, timing of return migration was investigated among one‐sea‐winter Atlantic salmon within a river system. By utilizing knowledge of the genetic population structure, population of origin was reliably identified for c. 1500 fish caught in mixed stock fisheries after adopting an approach to minimize the complications arising from potential nonsampled populations. Results demonstrated significant and temporally stable differences among populations as well as between sexes. Generally, female salmon from tributary populations entered fresh water first. Run timing was not however related to in‐river migration distance. Rather, one‐sea‐winter salmon from larger populations and with a higher proportion of multi‐sea‐winter females arrived later in the season. These findings are a significant step toward a more thorough understanding of the salmon migration behavior and behavioral ecology, providing concrete tools for the management and conservation of the remaining indigenous Atlantic salmon stocks.

Migration of juvenile Atlantic salmon Salmo salar in small tributaries of the subarctic River Teno, northern Finland

Abstract Downstream migration of Atlantic salmon Salmo salar smolt and up and downstream migration of salmon parr were studied in two small tributaries of the large subarctic River Teno, northern Finland. The tributaries are not spawning areas for salmon, but juveniles enter them from the main stem of the river. The tributaries produced notable numbers of smolt, 300–700 a year, equivalent to approximately 70 smolt per km of river (1.0–1.2 smolt per 100 m 2 ). Substantial upstream migration of salmon parr, 100–200 specimens a year, was also detected, although the number of downstream migrants usually exceeded that of the upstream migrants. Most of the migrants in both directions were 1+ or 2+ ages, the older parr migrating earlier in the summer than the younger ones. Environmental factors, water temperature and water level, had some influence on the migration of both parr and smolt. Salmon parr show active exploratory behaviour in addition to the traditionally assumed sedentary, territorial behaviour. The importance of identifying all habitats used by salmon during their life-cycle is emphasized.

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.

Cost-effective genome-wide estimation of allele frequencies from pooled DNA in Atlantic salmon (Salmo salar L.)

BackgroundNew sequencing technologies have tremendously increased the number of known molecular markers (single nucleotide polymorphisms; SNPs) in a variety of species. Concurrently, improvements to genotyping technology have now made it possible to efficiently genotype large numbers of genome-wide distributed SNPs enabling genome wide association studies (GWAS). However, genotyping significant numbers of individuals with large number of SNPs remains prohibitively expensive for many research groups. A possible solution to this problem is to determine allele frequencies from pooled DNA samples, such ‘allelotyping’ has been presented as a cost-effective alternative to individual genotyping and has become popular in human GWAS. In this article we have tested the effectiveness of DNA pooling to obtain accurate allele frequency estimates for Atlantic salmon (Salmo salar L.) populations using an Illumina SNP-chip.ResultsIn total, 56 Atlantic salmon DNA pools from 14 populations were analyzed on an Atlantic salmon SNP-chip containing probes for 5568 SNP markers, 3928 of which were bi-allelic. We developed an efficient quality control filter which enables exclusion of loci showing high error rate and minor allele frequency (MAF) close to zero. After applying multiple quality control filters we obtained allele frequency estimates for 3631 bi-allelic loci. We observed high concordance (r > 0.99) between allele frequency estimates derived from individual genotyping and DNA pools. Our results also indicate that even relatively small DNA pools (35 individuals) can provide accurate allele frequency estimates for a given sample.ConclusionsDespite of higher level of variation associated with array replicates compared to pool construction, we suggest that both sources of variation should be taken into account. This study demonstrates that DNA pooling allows fast and high-throughput determination of allele frequencies in Atlantic salmon enabling cost-efficient identification of informative markers for discrimination of populations at various geographical scales, as well as identification of loci controlling ecologically and economically important traits.