Juha-Pekka Vähä

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.

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.

A proteomics approach reveals divergent molecular responses to salinity in populations of European whitefish (Coregonus lavaretus)

Osmoregulation is a vital physiological function for fish, as it helps maintain a stable intracellular concentration of ions in environments of variable salinities. We focused on a primarily freshwater species, the European whitefish (Coregonus lavaretus), to investigate the molecular mechanisms underlying salinity tolerance and examine whether these mechanisms differ between genetically similar populations that spawn in freshwater vs. brackishwater environments. A common garden experiment involving 27 families in two populations and five salinity treatments together with a large‐scale, high‐resolution mass spectrometry experiment that quantified 1500 proteins was conducted to assess phenotypic and proteomic responses during early development, from fertilization until hatching, in the studied populations. The populations displayed drastically different phenotypic and proteomic responses to salinity. Freshwater‐spawning whitefish showed a significantly higher mortality rate in higher salinity treatments. Calcium, an ion involved in osmotic stress sensing, had a central role in the observed proteomic responses. Brackishwater‐spawning fish were capable of viable osmoregulation, which was modulated by cortisol, an important seawater‐adaptation hormone in teleost fish. Several proteins were identified to play key roles in osmoregulation, most importantly a highly conserved cytokine, tumour necrosis factor, whereas calcium receptor activities were associated with salinity adaptation. These results imply that individuals from these populations are most likely adapted to their local environments, even though the baseline level of genetic divergence between them is low (FST = 0.049). They also provide clues for choosing candidate loci for studying the molecular basis of salinity adaptation in other species. Further, our approach provides an example of how proteomic methods can be successfully used to obtain novel insights into the molecular mechanisms behind adaptation in non‐model organism.

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.

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.

Finding Markers That Make a Difference: DNA Pooling and SNP-Arrays Identify Population Informative Markers for Genetic Stock Identification

Genetic stock identification (GSI) using molecular markers is an important tool for management of migratory species. Here, we tested a cost-effective alternative to individual genotyping, known as allelotyping, for identification of highly informative SNPs for accurate genetic stock identification. We estimated allele frequencies of 2880 SNPs from DNA pools of 23 Atlantic salmon populations using Illumina SNP-chip. We evaluated the performance of four common strategies (global F ST, pairwise F ST, Delta and outlier approach) for selection of the most informative set of SNPs and tested their effectiveness for GSI compared to random sets of SNP and microsatellite markers. For the majority of cases, SNPs selected using the outlier approach performed best followed by pairwise F ST and Delta methods. Overall, the selection procedure reduced the number of SNPs required for accurate GSI by up to 53% compared with randomly chosen SNPs. However, GSI accuracy was more affected by populations in the ascertainment group rather than the ranking method itself. We demonstrated for the first time the compatibility of different large-scale SNP datasets by compiling the largest population genetic dataset for Atlantic salmon to date. Finally, we showed an excellent performance of our top SNPs on an independent set of populations covering the main European distribution range of Atlantic salmon. Taken together, we demonstrate how combination of DNA pooling and SNP arrays can be applied for conservation and management of salmonids as well as other species.

Distribution and biological characteristics of escaped farmed salmon in a major subarctic wild salmon river: implications for monitoring.

We report the occurrence, distribution, and biological characteristics of escaped farmed salmon in the River Teno in northernmost Europe, which supports one of the largest and most versatile wild Atlantic salmon (Salmo salar) populations in the world. Farmed salmon were caught during the fishing season (May–August) when their proportion in the catch varied between 0.0% and 0.7%. Occasional sampling after the fishing season revealed much higher proportions of escapees, up to 47%, indicating a potential for a more severe impact of farmed fish than the in-season monitoring is able to uncover. Peak migration of the wild salmon was in June or July, but that of escaped farmed fish was in August. Up to 88% of the escaped salmon caught in August showed gonad development, and scale analysis indicated that 4.5% of them were repeat spawners. Genetic analyses using microsatellite markers revealed highly significant genetic differentiation between wild salmon and escaped farmed fish (FST = 0.05) caught in the River Te...

Genomewide introgressive hybridization patterns in wild Atlantic salmon influenced by inadvertent gene flow from hatchery releases

Many salmonid fish populations are threatened by genetic homogenization, primarily due to introgressive hybridization with hatchery‐reared conspecifics. By applying genomewide analysis using two molecular marker types (1986 SNPs and 17 microsatellites), we assessed the genetic impacts of inadvertent gene flow via straying from hatchery releases on wild populations of Atlantic salmon in the Gulf of Finland, Baltic Sea, over 16 years (1996–2012). Both microsatellites and SNPs revealed congruent population genetic structuring, indicating that introgression changed the genetic make‐up of wild populations by increasing genetic diversity and reducing genetic divergence. However, the degree of genetic introgression varied among studied populations, being higher in the eastern part and lower in the western part of Estonia, which most likely reflects the history of past stocking activities. Using kernel smoothing and permutation testing, we detected considerable heterogeneity in introgression patterns across the genome, with a large number of regions exhibiting nonrandom introgression widely dispersed across the genome. We also observed substantial variation in nonrandom introgression patterns within populations, as the majority of genomic regions showing elevated or reduced introgression were not consistently detected among temporal samples. This suggests that recombination, selection and stochastic processes may contribute to complex nonrandom introgression patterns. Our results suggest that (i) some genomic regions in Atlantic salmon are more vulnerable to introgressive hybridization, while others show greater resistance to unidirectional gene flow; and (ii) the hybridization of previously separated populations leads to complex and dynamic nonrandom introgression patterns that most likely have functional consequences for indigenous populations.

First record of proliferative kidney disease agent Tetracapsuloides bryosalmonae in wild brown trout and European grayling in Finland

The myxozoan endoparasite Tetracapsuloides bryosalmonae causes temperature-driven proliferative kidney disease (PKD) in salmonid fishes. Despite the economic and ecological importance of PKD, information about the distribution of the parasite is still scarce. Here, we report for the first time the occurrence of T. bryosalmonae in wild brown trout Salmo trutta and European grayling Thymallus thymallus populations in Finland. We detected T. bryosalmonae at high prevalence in both brown trout and European grayling from the transboundary Finnish-Russian River Koutajoki system (Rivers Oulankajoki, Kuusinkijoki, Kitkajoki, Maaninkajoki, and Juumajoki) in north-eastern Finland. In southern Finland, T. bryosalmonae was detected in River Siuntionjoki young-of-the-year brown trout collected both in 2015 and 2016 (100% prevalence), while the parasite was not observed in fish from 3 other rivers (Ingarskila, Mustajoki, and Vantaanjoki) flowing to the Gulf of Finland. Our results, together with those from recent studies of Atlantic salmon, indicate that T. bryosalmonae is distributed over much higher latitudes in northern Europe than previously appreciated. We expect that increasing water temperatures will likely cause new PKD outbreaks in these more northerly regions in the future.

Comprehensive microsatellite baseline for genetic stock identification of Atlantic salmon (Salmo salar L.) in northernmost Europe

Mikhail Ozerov, Juha-Pekka V€ah€a*, Vidar Wennevik, Eero Niemel€a, Martin-A. Svenning, Sergey Prusov, Rogelio Diaz Fernandez, Laila Unneland, Anti Vasem€agi, Morten Falkegård, Tiia Kalske, and Bente Christiansen Kevo Subarctic Research Institute, University of Turku, Turku FI-20014, Finland Department of Biology, University of Turku, Turku FI-20014, Finland Association for Water and Environment of Western Uusimaa, P.O. Box 51, Lohja FI-08101, Finland Institute of Marine Research (IMR), P.O. Box 1870 Nordnes, Bergen N-5817, Norway River Teno Fisheries Research Station, Natural Resources Institute Finland (Luke), Utsjoki FI-99980, Finland Arctic Ecology Department, Fram Centre, Norwegian Institute for Nature Research (NINA), P.O. Box 6600 Langnes, Tromsø N-9296, Norway The Knipovitch Polar Research Institute of Marine Fisheries and Oceanography (PINRO), Murmansk 183038, Russia Department of Aquaculture, Estonian University of Life Sciences, Tartu 51014, Estonia County Governor of Finnmark (FMFI), Vadsø N-9815, Norway *Corresponding author: tel: þ358 19 5682 940; fax: þ358 19 325 697; e-mail: juha-pekka.vaha@luvy.fi These authors contributed equally to this work. Present address: Department of Biology, University of Turku, FI-20014 Turku, Finland; Juha-Pekka V€ah€a, Association for Water and Environment of Western Uusimaa, POB 51, FI-08101 Lohja, Finland