Temporal allele frequency changes in large-effect loci reveal potential fishing impacts on salmon life-history diversity.

Fishing has the potential to influence the life-history traits of exploited populations. However, our understanding of how fisheries can induce evolutionary genetic changes remains incomplete. The discovery of large-effect loci linked with ecologically important life-history traits, such as age at maturity in Atlantic salmon (Salmo salar), provides an opportunity to study the impacts of temporally varying fishing pressures on these traits. A 93-year archive of fish scales from wild Atlantic salmon catches from the northern Baltic Sea region allowed us to monitor variation in adaptive genetic diversity linked with age at maturity of wild Atlantic salmon populations. The dataset consisted of samples from both commercial and recreational fisheries that target salmon on their spawning migration. Using a genotyping-by-sequencing approach (GT-seq), we discovered strong within-season allele frequency changes at the vgll3 locus linked with Atlantic salmon age at maturity: fishing in the early season preferentially targeted the vgll3 variant linked with older maturation. We also found within-season temporal variation in catch proportions of different wild Atlantic salmon subpopulations. Therefore, selective pressures of harvesting may vary depending on the seasonal timing of fishing, which has the potential to cause evolutionary changes in key life-history traits and their diversity. This knowledge can be used to guide fisheries management to reduce the effects of fishing practices on salmon life-history diversity. Thus, this study provides a tangible example of using genomic approaches to infer, monitor and help mitigate human impacts on adaptively important genetic variation in nature.

A century of genetic homogenization in Baltic salmon-evidence from archival DNA.

Intra-species genetic homogenization arising from anthropogenic impacts is a major threat to biodiversity. However, few taxa have sufficient historical material to systematically quantify long-term genetic changes. Using archival DNA collected over approximately 100 years, we assessed spatio-temporal genetic change in Atlantic salmon populations across the Baltic Sea, an area heavily impacted by hydropower exploitation and associated with large-scale mitigation stocking. Analysis was carried out by screening 82 SNPs in 1680 individuals from 13 Swedish rivers. We found an overall decrease in genetic divergence and diminished isolation by distance among populations, strongly indicating genetic homogenization over the past century. We further observed an increase in genetic diversity within populations consistent with increased gene flow. The temporal genetic change was lower in larger wild populations than in smaller wild and hatchery-reared ones, indicating that larger populations have been able to support a high number of native spawners in relation to immigrants. Our results demonstrate that stocking practices of salmon in the Baltic Sea have led to the homogenization of populations over the last century, potentially compromising their ability to adapt to environmental change. Stocking of reared fish is common worldwide, and our study is a cautionary example of the potentially long-term negative effects of such activities.

Close relatives in population samples: Evaluation of the consequences for genetic stock identification.

Determining the origin of individuals in mixed population samples is key in many ecological, conservation and management contexts. Genetic data can be analyzed using genetic stock identification (GSI), where the origin of single individuals is determined using Individual Assignment (IA) and population proportions are estimated with Mixed Stock Analysis (MSA). In such analyses, allele frequencies in a reference baseline are required. Unknown individuals or mixture proportions are assigned to source populations based on the likelihood that their multilocus genotypes occur in a particular baseline sample. Representative sampling of populations included in a baseline is important when designing and performing GSI. Here, we investigate the effects of family sampling on GSI, using both simulated and empirical genotypes for Atlantic salmon (Salmo salar). We show that nonrepresentative sampling leading to inclusion of close relatives in a reference baseline may introduce bias in estimated proportions of contributing populations in a mixed sample, and increases the amount of incorrectly assigned individual fish. Simulated data further show that the induced bias increases with increasing family structure, but that it can be partly mitigated by increased baseline population sample sizes. Results from standard accuracy tests of GSI (using only a reference baseline and/or self-assignment) gave a false and elevated indication of the baseline power and accuracy to identify stock proportions and individuals. These findings suggest that family structure in baseline population samples should be quantified and its consequences evaluated, before carrying out GSI.

Adaptive divergence in body size overrides the effects of plasticity across natural habitats in the brown trout.

The evolution of life-history traits is characterized by trade-offs between different selection pressures, as well as plasticity across environmental conditions. Yet, studies on local adaptation are often performed under artificial conditions, leaving two issues unexplored: (i) how consistent are laboratory inferred local adaptations under natural conditions and (ii) how much phenotypic variation is attributed to phenotypic plasticity and to adaptive evolution, respectively, across environmental conditions? We reared fish from six locally adapted (domesticated and wild) populations of anadromous brown trout (Salmo trutta) in one semi-natural and three natural streams and recorded a key life-history trait (body size at the end of first growth season). We found that population-specific reaction norms were close to parallel across different streams and Q ST was similar - and larger than F ST - within all streams, indicating a consistency of local adaptation in body size across natural environments. The amount of variation explained by population origin exceeded the variation across stream environments, indicating that genetic effects derived from adaptive processes have a stronger effect on phenotypic variation than plasticity induced by environmental conditions. These results suggest that plasticity does not "swamp" the phenotypic variation, and that selection may thus be efficient in generating genetic change.

Sperm from pheromone primed brown trout (Salmo trutta L.) produce more larvae.

Male goldfish (Carassius auratus) exposed to female hormonal pheromones express increased milt volumes and their sperm fertilize more eggs than sperm from unprimed males. Ovulated salmonid females also release odours that increase volumes of strippable milt in males. It is, however, not known if the priming pheromones affect the ability of sperm to fertilize eggs in salmonids. In this study, we compare the proportion of larvae produced from in vitro fertilization tests between primed brown trout (Salmo trutta) males exposed to a mix of female urine and ovarian fluids, and control males exposed only to 0.9 % sodium chloride. We also investigate priming effects on milt yield and sperm motility. Fertilization tests with sperm from single males, as well as sperm from two males (i.e., sperm competition), were performed. Primed males generated more larvae in both the single male and competition fertilization tests. No differences between treatments in milt yield and sperm motility could be established.

Strong divergence in trait means but not in plasticity across hatchery and wild populations of sea-run brown trout Salmo trutta.

There is ample evidence that organisms adapt to their native environment when gene flow is restricted. However, evolution of plastic responses across discrete environments is less well examined. We studied divergence in means and plasticity across wild and hatchery populations of sea-run brown trout (Salmo trutta) in a common garden experiment with two rearing environments (hatchery and a nearly natural experimental stream). Since natural and hatchery environments differ, this arrangement provides an experiment in contemporary adaptation across the two environments. A Q(ST) - F(ST) approach was used to investigate local adaptation in survival and growth over the first summer. We found evidence for divergent selection in survival in 1 year and in body length in both years and rearing environments. In general, the hatchery populations had higher survival and larger body size in both environments. Q(ST) in body size did not differ between the rearing environments, and constitutive divergence in the means was in all cases stronger than divergence in the plastic responses. These results suggest that in this system, constitutive changes in mean trait values are more important for local adaptation than increased plasticity. In addition, ex situ rearing conditions induce changes in trait means that are adaptive in the hatchery, but potentially harmful in the wild, suggesting that hatchery rearing is likely to be a suboptimal management strategy for trout populations facing selection in the stream environment.

Frequency distribution of coping strategies in four populations of brown trout (Salmo trutta).

In a challenging situation some animals respond by active avoidance, aggression and an activation of the sympathetic nervous system whereas others respond by immobility, low levels of aggression and a predominant adrenocortical stress response. When consistent over time and across situations such inter-individual differences in behavioural and physiological stress responses are referred to as stress coping strategies. In a previous study we reported the existence of two distinct stress coping strategies in a sea-ranched brown trout (Salmo trutta) population. Using the same method, we here show that four brown trout populations with different origin, but reared under identical conditions, differ in their endocrine stress response, behaviour during hypoxia and aggression. Further more, if individuals are classified as high- and low responsive based on post-stress blood plasma noradrenalin levels (indicator of sympathetic reactivity) the frequency distribution shows that populations with hatchery origin are biased towards having higher frequencies of high responsive individuals. However, the number of high responsive trout ranges from 14-48% in the different populations which shows that generally the frequency is biased towards lower levels of high responsive individuals. We discuss different frequency-dependent mechanisms that maintain multiple phenotypes in populations and speculate about differences in selection regime among the studied populations.

Panmixia in the European eel: a matter of time...

The European eel (Anguilla anguilla L.) has been a prime example of the panmixia paradigm because of its extraordinary adaptation to the North Atlantic gyral system, semelparous spawning in the Sargasso Sea and long trans-oceanic migration. Recently, this view was challenged by the suggestion of a genetic structure characterized by an isolation-by-distance (IBD) pattern. This is only likely if spawning subpopulations are spatially and/or temporally separated, followed by non-random larval dispersal. A limitation of previous genetic work on eels is the lack of replication over time to test for temporal stability of genetic structure. Here, we hypothesize that temporal genetic variation plays a significant role in explaining the spatial structure reported earlier for this species. We tested this by increasing the texture of geographical sampling and by including temporal replicates. Overall genetic differentiation among samples was low, highly significant and comparable with earlier studies (FST = 0.0014; p < 0.01). On the other hand, and in sharp contrast with current understandings, hierarchical analyses revealed no significant inter-location genetic heterogeneity and hence no IBD. Instead, genetic variation among temporal samples within sites clearly exceeded the geographical component. Our results provide support for the panmixia hypothesis and emphasize the importance of temporal replication when assessing population structure of marine fish species.