Interbreeding between domesticated and wild animals occurs in several species. This gene flow has long been anticipated to induce genetic changes in life-history traits of wild populations, thereby influencing population dynamics and viability. Here, we show that individuals with high levels of introgression (domesticated ancestry) have altered age and size at maturation in 62 wild Atlantic salmon Salmo salar populations, including seven ancestral populations to breeding lines of the domesticated salmon. This study documents widespread changes to life-history traits in wild animal populations following gene flow from selectively bred, domesticated conspecifics. The continued high abundance of escaped, domesticated Atlantic salmon thus threatens wild Atlantic salmon populations by inducing genetic changes in fitness-related traits. Our results represent key evidence and a timely warning concerning the potential ecological impacts of the globally increasing use of domesticated animals.
Gyrodactylus specimens infecting both anadromous Arctic charr (Salvelinus alpinus) from River Signaldalselva (northern Norway) and resident Arctic charr from Lake Pålsbufjorden (southern Norway) were identified as G. salaris using molecular markers and morphometrics. The infection in Pålsbufjorden represents the first record of a viable G. salaris population infecting a host in the wild in the absence of salmon (Salmo salar). G. salaris on charr from Signaldalselva and Pålsbufjorden bear different mitochondrial haplotypes. While parasites infecting charr in Signaldalselva carry the same mitochondrial haplotype as parasites from sympatric Atlantic salmon, G. salaris from charr in Pålsbufjorden bear a haplotype that has previously been found in parasites infecting rainbow trout (Oncorhynchus mykiss) and Atlantic salmon, and an IGS repeat arrangement that is very similar to those observed earlier in parasites infecting rainbow trout. Accordingly, the infection may result from 2 subsequent host-switches (from salmon via rainbow trout to charr). Morphometric analyses revealed significant differences between G. salaris infecting charr in the 2 localities, and between those on sympatric charr and salmon within Signaldalselva. These differences may reflect adaptations to a new host species, different environmental conditions, and/or inherited differences between the G. salaris strains. The discovery of G. salaris on populations of both anadromous and resident charr may have severe implications for Atlantic salmon stock-management as charr may represent a reservoir for infection of salmon.
Summary 1.Timing of birth ⁄ hatching may have strong effects on offspring fitness. Breeding time is generally considered to have evolved to match offspring arrival with optimal seasonal environmental conditions, though this is rarely tested experimentally and factors shaping the relations between timing of birth and reproductive success are often poorly understood. 2. By manipulating incubation temperature of Atlantic salmon embryos, and hence controlling for maternal and genetic effects, we obtained offspring emerging from nests prior to (accelerated), during and after (decelerated) normal emergence times, and accordingly experienced widely different seasonal environmental conditions at emergence (stream temperature range 4-16°C). The accelerated group emerged at temperatures that are generally considered to be highly sub-optimal for growth and likely imposes strong constraints on feeding and activity, and during a peak in water discharge which is expected to negatively influence habitat availability. 3. In the wild, overall mortality during the period after emergence was 79%, and was significantly affected by both release density and emergence timing. Accelerated offspring, which emerged earliest and experienced the harshest environmental conditions, had both highest survival and largest final body size. The effect was particularly strong at the high density release site, where survival of accelerated offspring was significantly higher than both the normal and decelerated groups. 4. In more controlled semi-natural environments, all developmental groups were able to perform well, but accelerated offspring had a relatively better performance than the later emerging offspring when density was high. Furthermore, the relative performance of the different groups was not sensitive to water discharge regimes (temporally stable vs. fluctuating). 5. These results suggest that the performance of offspring in relation to seasonal timing of emergence is highly affected by competitive interactions in Atlantic salmon. Although a match between phenology and optimal seasonal environmental conditions may be highly important for organisms depending on specific resources that are only available during a limited period of the season, such resources may be available in variable amounts year around for many organisms. For these, offspring success may to a larger degree be shaped by the timing of their hatching ⁄ birth relative to each other, and particularly so under high population densities.
By dispersing from localized aggregations of recruits, individuals may obtain energetic benefits due to reduced experienced density. However, this will depend on the spatial scale over which individuals compete. Here, we quantify this scale for juvenile Atlantic salmon (Salmo salar) following emergence and dispersal from nests. A single nest was placed in each of ten replicate streams during winter, and information on the individual positions (±1 m) and the body sizes of the resulting young-of-the-year (YOY) juveniles was obtained by sampling during the summer. In six of the ten streams, model comparisons suggested that individual body size was most closely related to the density within a mean distance of 11 m (range 2–26 m). A link between body size and density on such a restricted spatial scale suggests that dispersal from nests confers energetic benefits that can counterbalance any survival costs. For the four remaining streams, which had a high abundance of trout and older salmon cohorts, no single spatial scale could best describe the relation between YOY density and body size. Energetic benefits of dispersal associated with reduced local density therefore appear to depend on the abundance of competing cohorts or species, which have spatial distributions that are less predictable in terms of distance from nests. Thus, given a trade-off between costs and benefits associated with dispersal, and variation in benefits among environments, we predict an evolving and/or phenotypically plastic growth rate threshold which determines when an individual decides to disperse from areas of high local density.
The monogenean ectoparasite, Gyrodactylus salaris Malmberg, 1957, has had a devastating effect on wild Atlantic salmon (Salmo salar) since its introduction to Norway in the mid-1970s. In Lake Pålsbufjorden, southern Norway, upstream of the stretches of the River Numedalslågen with anadromous Atlantic salmon, a resident Arctic charr (Salvelinus alpinus) population has been reported to be infected with G. salaris which is viable in the absence of its normal host, the Atlantic salmon. Currently, there is no record of G. salaris infecting Atlantic salmon in the downstream sections of the River Numedalslågen. We studied experimentally the infectivity and reproductive capacity of G. salaris from Lake Pålsbufjorden on wild and hatchery-reared Atlantic salmon as well as on Arctic charr and rainbow trout (Oncorhynchus mykiss). Arctic charr and rainbow trout were moderately susceptible, whereas the Atlantic salmon stocks from River Numedalslågen and River Drammenselva were innately resistant to only slightly susceptible. Thus, the G. salaris from Arctic charr in Lake Pålsbufjorden is considered non-pathogenic to Atlantic salmon. This is the first observation of variation in host preference among Norwegian G. salaris populations. The observed differences in virulence between G. salaris populations could have important consequences for the international legislation and management of Atlantic salmon.
The viviparous monogenean Gyrodactylus salaris continues to devastate Norwegian Atlantic salmon populations despite the extreme measures taken to control this pathogen. Increased understanding of parasite biology is needed to develop alternative control and management strategies of wild Atlantic salmon. We have examined temperature-dependent survival of G. salaris, both on and off the host. At 18 degrees C, survival off the host was 1 day, but at 3 degrees C parasites survived for 4 days. However, in contrast to assumptions made by earlier authors, many parasites remained with their host following its death. Ultrastructural evidence indicated that G. salaris individuals can feed on a dead host, and laboratory tests demonstrated that worms on their hosts more than double their life-span compared with individuals maintained off the host. Experimental infections also demonstrated that establishment and subsequent population growth of parasites previously maintained on dead hosts for 3 days, was similar to that of parasites transferred directly between living hosts. Hence, for G. salaris, dead infected hosts may increase the chances of successful transmission and be a potential important infection source in rivers and hatcheries.
If competitive ability depends on body size, then the optimal natal movement from areas of high local population density can also be predicted to be size-dependent. Specifically, small, competitively-inferior individuals would be expected to benefit most from moving to areas of lower local density. Here we evaluate whether individual variation in natal movement following emergence from nests is consistent with such a size-dependent strategy in Atlantic salmon, and whether such a strategy is evident across a range of environmental conditions (principally predator presence and conspecific density). In stream channel experiments, those juveniles that stayed close to nests were larger than those that emigrated. This result was not sensitive to predator presence or conspecific density. These observations were mirrored in natural streams in which salmon eggs were planted in nests and the resulting offspring were sampled at high spatial resolution. A negative relationship was found between juvenile body size and distance from nests early in development whereas in those streams sampled later in ontogeny, individuals that had moved furthest were largest. Thus, movement away from nests appeared to result in a reduced competitive intensity and increased growth rate. The fact that there is ultimately a growth advantage associated with moving suggests that there is also a cost that selects against movement by the larger individuals. Thus, natal movement in juvenile Atlantic salmon appears to represent a body size-dependent strategy.
Summary 1.Maintenance of metabolic rate (MR, the energy cost of self-maintenance) is linked to behavioural traits and fitness and varies substantially within populations. Despite having received much attention, the causes and consequences of this variation remain obscure. 2. Theoretically, such within-population variation in fitness-related traits can be maintained by environmental heterogeneity in selection patterns, but for MR, this has rarely been tested in nature. 3. Here, we experimentally test whether the relationship between MR and performance can vary spatially by assessing survival, growth rate and movement of Atlantic salmon (Salmo salar L.) juveniles from 10 family groups differing in MR (measured as egg metabolism) that were stocked in parallel across 10 tributaries of a single watershed. 4. The relationship between MR and relative survival and growth rate varied significantly among tributaries. Specifically, the effect of MR ranged from negative to positive for relative survival, whereas it was negative for growth rate. The association between MR and movement was positive and did not vary significantly among tributaries. 5. These results are consistent with a fitness cost of traits associated with behavioural dominance that varies across relatively small spatial scales (within a single watershed). More generally, our results support the hypothesis that spatial heterogeneity in environmental conditions contributes to maintain within-population variation in fitness-related traits, such as MR.
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