Browsing by Subject "Atlantic salmon"

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  • Miettinen, Antti; Palm, Stefan; Dannewitz, Johan; Lind, Emma; Primmer, Craig R.; Romakkaniemi, Atso; Ostergren, Johan; Pritchard, Victoria L. (2021)
    Anadromous salmonid fishes frequently exhibit strong geographic population structuring. However, population genetic differentiation of Atlantic salmon (Salmo salar) at fine geographic scales differs across equivalent spatial extents in different regions. So far, fine-scale genetic differentiation has not been assessed in rivers of the Baltic Sea, a region that contains an evolutionarily distinct Atlantic salmon lineage. Thus, Baltic salmon are currently managed on the river level, without focus on potential genetic structure and diversity within rivers. Here, we used microsatellites to characterize the genetic structure of wild juvenile salmon sampled throughout the interconnected, northern Baltic Tornio and Kalix Rivers. We found genetic differentiation within the two rivers, but not between them: salmon in the upper reaches differed from individuals in the lower reaches, regardless of river system. Further, examining smolts migrating from the river to the sea and adults returning from the sea to spawn, we found an association between the genetic structure and seasonal migration timing. Out-migrating smolts genetically assigned to upper river reaches were older and tended to reach the sea later in the season than smolts from the lower reaches. In contrast, mature adults originating from the upper reaches returned to the river early in the season. Our observation of genetic population structuring between downstream and upstream reaches of the large Tornio and Kalix rivers, and its association with migration timing, implies that careful temporal management of the northern Baltic fisheries would help to preserve the diversity and sustainability of the wild salmon stocks of these rivers.
  • O'Sullivan, Ronan James; Aykanat, Tutku; Johnston, Susan E.; Rogan, Ger; Poole, Russell; Prodohl, Paulo A.; de Eyto, Elvira; Primmer, Craig R.; McGinnity, Philip; Reed, Thomas Eric (2020)
    The release of captive-bred animals into the wild is commonly practised to restore or supplement wild populations but comes with a suite of ecological and genetic consequences. Vast numbers of hatchery-reared fish are released annually, ostensibly to restore/enhance wild populations or provide greater angling returns. While previous studies have shown that captive-bred fish perform poorly in the wild relative to wild-bred conspecifics, few have measured individual lifetime reproductive success (LRS) and how this affects population productivity. Here, we analyse data on Atlantic salmon from an intensely studied catchment into which varying numbers of captive-bred fish have escaped/been released and potentially bred over several decades. Using a molecular pedigree, we demonstrate that, on average, the LRS of captive-bred individuals was only 36% that of wild-bred individuals. A significant LRS difference remained after excluding individuals that left no surviving offspring, some of which might have simply failed to spawn, consistent with transgenerational effects on offspring survival. The annual productivity of the mixed population (wild-bred plus captive-bred) was lower in years where captive-bred fish comprised a greater fraction of potential spawners. These results bolster previous empirical and theoretical findings that intentional stocking, or non-intentional escapees, threaten, rather than enhance, recipient natural populations.
  • Aykanat, Tutku; Ozerov, Mikhail; Vähä, Juha-Pekka; Orell, Panu; Niemelä, Eero; Erkinaro, Jaakko; Primmer, Craig R. (2019)
    Co-inheritance 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 these two traits are co-inherited 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 L allele was dominant in individuals remaining only one year at sea before maturation, but the dominance was reversed, with the E allele being dominant in individuals maturing after two or more years at sea. 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, whereas 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.
  • Partanen, Reeta-Maria (Helsingin yliopisto, 2020)
    There is a naturally reproducing Atlantic salmon population in the River Teno in northern Norway and Finland. The Teno population has a strong population structure and up to 28 subpopulations have been recognized. Estimation of effective population size is important in conservation of the subpopulations. Effective population size tells about genetic variation of a population and is among the most important concepts in conservation genetics. In this study, current and past effective population sizes of 28 subpopulations were estimated from high density SNP-data for 1137 individuals in total. The estimation was done with the linkage disequilibrium method and the effects of using different assumptions were studied. Current estimated effective population sizes in subpopulations were generally low and ranged from around nine to 272 individuals. Only four populations had a current effective population size bigger than 50 individuals. Past effective population sizes showed a clear declining trend from the most distant generations in all populations. The choice between physical and linkage map as well as female, male or average linkage map had an effect to estimates. Also, different sample size corrections resulted in different estimates. Furthermore, effective population size was estimated with temporal method in three populations. It was detected that the estimates from temporal and linkage disequilibrium method were different from each other. The results of this study suggest that Teno Atlantic salmon subpopulations have declined over the past 150 generations and are in risk of losing genetic variation due to current low effective population size. This should be taken into account in conservation plans.
  • O'Sullivan, Ronan James; Aykanat, Tutku; Johnston, Susan E.; Kane, Adam; Poole, Russell; Rogan, Ger; Prodöhl, Paulo A.; Primmer, Craig R.; McGinnity, Philip; Reed, Thomas Eric (2019)
    Comparing observed versus theoretically expected evolutionary responses is important for our understanding of the evolutionary process, and for assessing how species may cope with anthropogenic change. Here, we document directional selection for larger female size in Atlantic salmon, using pedigree-derived estimates of lifetime reproductive success as a fitness measure. We show the trait is heritable and, thus, capable of responding to selection. The Breeder's Equation, which predicts microevolution as the product of phenotypic selection and heritability, predicted evolution of larger size. This was at odds, however, with the observed lack of either phenotypic or genetic temporal trends in body size, a so-called "paradox of stasis." To investigate this paradox, we estimated the additive genetic covariance between trait and fitness, which provides a prediction of evolutionary change according to Robertson's secondary theorem of selection (STS) that is unbiased by missing variables. The STS prediction was consistent with the observed stasis. Decomposition of phenotypic selection gradients into genetic and environmental components revealed a potential upward bias, implying unmeasured factors that covary with trait and fitness. These results showcase the power of pedigreed, wild population studies-which have largely been limited to birds and mammals-to study evolutionary processes on contemporary timescales.
  • Verta, Jukka-Pekka; Barton, Henry Juho; Pritchard, Victoria; Primmer, Craig (2021)
    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 Ma. 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 regulatory divergence. Patterns of genetic diversity across natural populations inferred from resequencing 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.
  • Debes, Paul V.; Piavchenko, Nikolai; Erkinaro, Jaakko; Primmer, Craig R. (2020)
    Knowledge of the relative importance of genetic versus environmental determinants of major developmental transitions is pertinent to understanding phenotypic evolution. In salmonid fishes, a major developmental transition enables a risky seaward migration that provides access to feed resources. In Atlantic salmon, initiation of the migrant phenotype, and thus age of migrants, is presumably controlled via thresholds of a quantitative liability, approximated by body size expressed long before the migration. However, how well size approximates liability, both genetically and environmentally, remains uncertain. We studied 32 Atlantic salmon families in two temperatures and feeding regimes (fully fed, temporarily restricted) to completion of migration status at age 1 year. We detected a lower migrant probability in the cold (0.42) than the warm environment (0.76), but no effects of male maturation status or feed restriction. By contrast, body length in late summer predicted migrant probability and its control reduced migrant probability heritability by 50-70%. Furthermore, migrant probability and length showed high heritabilities and between-environment genetic correlations, and were phenotypically highly correlated with stronger genetic than environmental contributions. Altogether, quantitative estimates for the genetic and environmental effects predicting the migrant phenotype indicate, for a given temperature, a larger importance of genetic than environmental size effects.
  • Pritchard, Victoria L.; Makinen, Hannu; Vähä, Juha-Pekka; Erkinaro, Jaakko; Orell, Panu; Primmer, Craig R. (2018)
    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.
  • Zueva, Ksenia J.; Lumme, Jaakko; Veselov, Alexey E.; Kent, Matthew P.; Primmer, Craig R. (2018)
    Abstract Understanding the genomic basis of host-parasite adaptation is important for predicting the long-term viability of species and developing successful management practices. However, in wild populations, identifying specific signatures of parasite-driven selection often presents a challenge, as it is difficult to unravel the molecular signatures of selection driven by different, but correlated, environmental factors. Furthermore, separating parasite-mediated selection from similar signatures due to genetic drift and population history can also be difficult. Populations of Atlantic salmon (Salmo salar L.) from northern Europe have pronounced differences in their reactions to the parasitic flatworm Gyrodactylus salaris Malmberg 1957 and are therefore a good model to search for specific genomic regions underlying inter-population differences in pathogen response. We used a dense Atlantic salmon SNP array, along with extensive sampling of 43 salmon populations representing the two G. salaris response extremes (extreme susceptibility vs resistant), to screen the salmon genome for signatures of directional selection while attempting to separate the parasite effect from other factors. After combining the results from two independent genome scan analyses, 57 candidate genes potentially under positive selection were identified, out of which 50 were functionally annotated. This candidate gene set was shown to be functionally enriched for lymph node development, focal adhesion genes and anti-viral response, which suggests that the regulation of both innate and acquired immunity might be an important mechanism for salmon response to G. salaris. Overall, our results offer insights into the apparently complex genetic basis of pathogen susceptibility in salmon and highlight methodological challenges for separating the effects of various environmental factors.
  • Aykanat, Tutku; Rasmussen, Martin; Ozerov, Mikhail; Niemelä, Eero; Paulin, Lars; Vähä, Juha-Pekka; Hindar, Kjetil; Wennevik, Vidar; Pedersen, Torstein; Svenning, Martin-A.; Primmer, Craig R. (2020)
    1. Animals employ various foraging strategies along their ontogeny to acquire energy, and with varying degree of efficiencies, to support growth, maturation and subsequent reproduction events. Individuals that can efficiently acquire energy early are more likely to mature at an earlier age, as a result of faster energy gain which can fuel maturation and reproduction. 2. We aimed to test the hypothesis that heritable resource acquisition variation that covaries with efficiency along the ontogeny would influence maturation timing of individuals. 3. To test this hypothesis, we utilized Atlantic salmon as a model which exhibits a simple, hence trackable, genetic control of maturation age. We then monitored the variation in diet acquisition (quantified as stomach fullness and composition) of individuals with different ages, and linked it with genomic regions (haploblocks) that were previously identified to be associated with age-at-maturity. 4. Consistent with the hypothesis, we demonstrated that one of the life-history genomic regions tested (six6) was indeed associated with age-dependent differences in stomach fullness. Prey composition was marginally linked tosix6, and suggestively (but non-significantly) tovgll3genomic regions. We further showed Atlantic salmon switched to the so-called 'feast and famine' strategy along the ontogeny, where older age groups exhibited heavier stomach content, but that came at the expense of running on empty more often. 5. These results suggest genetic variation underlying resource utilization may explain the genetic basis of age structure in Atlantic salmon. Given that ontogenetic diet has a genetic component and the strong spatial diversity associated with these genomic regions, we predict populations with diverse maturation age will have diverse evolutionary responses to future changes in marine food web structures.
  • Aykanat, Tutku; Rasmussen, Martin; Ozerov, Mikhail; Niemelä, Eero; Paulin, Lars; Vähä, Juha-Pekka; Hindar, Kjetil; Wennevik, Vidar; Pedersen, Torstein; Svenning, Martin-A.; Primmer, Craig R. (2020)
    1. Animals employ various foraging strategies along their ontogeny to acquire energy, and with varying degree of efficiencies, to support growth, maturation and subsequent reproduction events. Individuals that can efficiently acquire energy early are more likely to mature at an earlier age, as a result of faster energy gain which can fuel maturation and reproduction. 2. We aimed to test the hypothesis that heritable resource acquisition variation that covaries with efficiency along the ontogeny would influence maturation timing of individuals. 3. To test this hypothesis, we utilized Atlantic salmon as a model which exhibits a simple, hence trackable, genetic control of maturation age. We then monitored the variation in diet acquisition (quantified as stomach fullness and composition) of individuals with different ages, and linked it with genomic regions (haploblocks) that were previously identified to be associated with age-at-maturity. 4. Consistent with the hypothesis, we demonstrated that one of the life-history genomic regions tested (six6) was indeed associated with age-dependent differences in stomach fullness. Prey composition was marginally linked tosix6, and suggestively (but non-significantly) tovgll3genomic regions. We further showed Atlantic salmon switched to the so-called 'feast and famine' strategy along the ontogeny, where older age groups exhibited heavier stomach content, but that came at the expense of running on empty more often. 5. These results suggest genetic variation underlying resource utilization may explain the genetic basis of age structure in Atlantic salmon. Given that ontogenetic diet has a genetic component and the strong spatial diversity associated with these genomic regions, we predict populations with diverse maturation age will have diverse evolutionary responses to future changes in marine food web structures.
  • Maamela, Katja (Helsingin yliopisto, 2021)
    In teleost fish, various egg traits play a crucial role in the development, growth, and survival of the offspring and thus affect maternal reproductive success. Atlantic salmon (Salmo salar) is a species where age at maturity, an important life-history trait influencing reproductive success, is under environmental and genetic control. In this study, I assessed how genetics of the vgll3 genotype and the dietary energy content affect egg traits and female maturation rate. The fish used in this study were lab-bred, three-year- old female Atlantic salmon with different vgll3 genotypes fed on one of two diets differing in energy content. The eggs traits included in the study were egg size, lipid, and protein content. Female maturation rate was not affected by the energy level of the diet or the vgll3 genotype. Egg size expressed as egg dry weight differed between females in the two feed treatments. These differences may be attributed to the increased lipid content of the eggs due to the higher fat content of the maternal diet. Females receiving high energy feed had a significantly higher egg lipid content compared to the low energy feed treatment. Females homozygous for the vgll3 allele associated with early maturity had a significantly lower egg lipid content in comparison to the females homozygous for the vgll3 late maturity allele indicating a potential reproductive fitness cost associated with early maturity. No effect of diet or vgll3 was found in egg protein content. This study provides the first evidence of vgll3 not only affecting Atlantic salmon age at maturity, as found in previous studies, but also egg lipids through maternal provisioning of nutrients.
  • Zueva, Ksenia J.; Lumme, Jaakko; Veselov, Alexey E.; Primmer, Craig R.; Pritchard, Victoria L. (2021)
    Our ability to examine genetic variation across entire genomes has enabled many studies searching for the genetic basis of local adaptation. These studies have identified numerous loci as candidates for differential local selection; however, relatively few have examined the overlap among candidate loci identified from independent studies of the same species in different geographic areas or evolutionary lineages. We used an allelotyping approach with a 220K SNP array to characterize the population genetic structure of Atlantic salmon in north-eastern Europe and ask whether the same genomic segments emerged as outliers among populations in different geographic regions. Genome-wide data recapitulated the phylogeographic structure previously inferred from mtDNA and microsatellite markers. Independent analyses of three genetically and geographically distinct groups of populations repeatedly inferred the same 17 haploblocks to contain loci under differential local selection. The most strongly supported of these replicated haploblocks had known strong associations with life-history variation or immune response in Atlantic salmon. Our results are consistent with these genomic segments harbouring large-effect loci which have a major role in Atlantic salmon diversification and are ideal targets for validation studies.
  • La Mere, Kelsey Maggan; Mäntyniemi, Samu; Haapasaari, Päivi (2020)
    In the Baltic Sea region, salmon are valued for the ecological, economic, and cultural benefits they provide. However, these fish are threatened due to historical overfishing, disease, and reduced access to spawning rivers. Climate change may pose another challenge for salmon management. Therefore, we conducted a problem-framing study to explore the effects climate change may have on salmon and the socio-ecological system they are embedded within. Addressing this emerging issue will require the cooperation of diverse stakeholders and the integration of their knowledge and values in a contentious management context. Therefore, we conducted this problem framing as a participatory process with stakeholders, whose mental models and questionnaire responses form the basis of this study. By framing the climate change problem in this way, we aim to provide a holistic understanding of the problem and incorporate stakeholder perspectives into the management process from an early stage to better address their concerns and establish common ground. We conclude that considering climate change is relevant for Baltic salmon management, although it may not be the most pressing threat facing these fish. Stakeholders disagree about whether climate change will harm or benefit salmon, when it will become a relevant issue in the Baltic context, and whether or not management efforts can mitigate any negative impacts climate change may have on salmon and their fishery. Nevertheless, by synthesizing the stakeholders' influence diagrams, we found 15 themes exemplifying: (1) how climate change may affect salmon, (2) goals for salmon management considering climate change, and (3) strategies for achieving those goals. Further, the stakeholders tended to focus on the riverine environment and the salmon life stages occurring therein, potentially indicating the perceived vulnerability of these life stages to climate change. Interestingly, however, the stakeholders tended to focus on traditional fishery management measures, like catch quotas, to meet their goals for these fish considering climate change. Further, social variables, like “politics,” “international cooperation,” and “employment” comprised a large proportion of the stakeholders' diagrams, demonstrating the importance of these factors for salmon management.
  • Kurko, Johanna; Debes, Paul V.; House, Andrew H.; Aykanat, Tutku; Erkinaro, Jaakko; Primmer, Craig R. (2020)
    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 adipogenesis and gametogenesis by regulating cell fate commitment and the HPG axis. These results may help to unravel general molecular mechanisms behind maturation.