Maternal inheritance influences homing and growth of hybrid offspring between wild and farmed Atlantic salmon

Abstract

The occurrence of domesticated organisms in nature is a major biological issue. Many can survive and reproduce with wild conspecifics, but little is known about the ecology of the hybrid offspring. Here, we investigated recapture, homing and growth of the released offspring of farmed (domesticated) and wild Atlantic salmon Salmo salar as well as their crosses. The fish were hatchery-reared for 1 yr and released as smolts in the River Imsa, Norway, the home river of the wild fish. The released fish migrated to the ocean. Many disappeared, but between 0.6 and 2% were sampled on their return as adults 1 or 2 yr later. Homing to the river of release was low for farmed salmon (88% strays). Among hybrids, having a wild mother provided increased homing accuracy (36% strays) relative to having a wild father (64% strays). Offspring of the local River Imsa salmon exhibited the best homing (28% strays). The growth capacity of the farmed salmon appeared to be not fully utilized in nature, as there was little difference in maximum size between wild and farmed salmon. However, minimum size at maturity was larger for farmed than wild conspecifics. Inheritance from a farmed mother increased minimum size of the hybrids versus that of the pure farmed salmon. Thus, maternal inheritance from domesticated, farmed salmon decreased homing and increased minimum size at adulthood of the offspring, making domesticated salmon a risk for locally adapted salmon in nature.

Modeling fitness changes in wild Atlantic salmon populations faced by spawning intrusion of domesticated escapees

“…Based upon results from these simulations, together with existing knowledge, we suggest that a combination of reduced spawning success of domesticated escapees, natural selection purging maladapted phenotypes/genotypes from the wild population, and phenotypic plasticity buffer the rate and magnitude of change in phenotypic and demographic characteristics of wild populations subject to spawning intrusion of domesticated escapees. These suggestions are in line with empirical data demonstrating that domesticated escapees display reduced spawning success in comparison with wild salmon (Fleming et al., , ), the offspring of domesticated salmon display reduced survival in the wild when compared to wild fish (Fleming et al., ; McGinnity et al., , ; Skaala et al., ) and that differences between domesticated and wild salmon in phenotypic traits, such as growth rate, are much less pronounced in the wild than in the hatchery (Besnier et al., ; Jonsson & Jonsson, ; Reed et al., ; Skaala et al., ).…”

“…Within regions displaying a mosaic of small and large populations, straying and the degree of genetic connectivity may be skewed, whereby large populations can act as net‐exporters of strayers to smaller neighboring wild populations (Hansen, Skaala, Jensen, Bekkevold, & Mensberg, ). Straying of wild fish between rivers (Stabell, ) also varies in time and space for Atlantic salmon (Jonsson & Jonsson, ; Jonsson et al., ; Pedersen et al., ; Skilbrei & Holm, ) and other salmonids (Bett, Hinch, Burnett, Donaldson, & Naman, ; Ford, Murdoch, & Hughes, ; King, Hillman, Elsmere, Stockley, & Stevens, ). Recent experimental work has also indicated that introgression of domesticated salmon may increase straying rates in impacted wild Atlantic salmon populations (Jonsson & Jonsson, ).…”

“…Domesticated Atlantic salmon display a wide range of genetic differences to wild salmon, and of these, growth and size at age are the traits displaying the greatest difference detected thus far (Glover et al., ). However, while very large (several fold or more in many cases) differences in growth and size at age are detected among domesticated, hybrid and wild salmon under controlled hatchery conditions (Debes, Fraser, Yates, & Hutchings, ; Fleming, Agustsson, Finstad, Johnsson, & Bjornsson, ; Glover et al., ; Harvey, Glover, Taylor, Creer, & Carvalho, ; Solberg, Glover et al., ; Solberg, Zhang et al., ), in the wild, growth rates and size at age differences between domesticated and wild salmon are much less distinct and overlap (Besnier et al., ; Fleming et al., ; Jonsson & Jonsson, ; Reed et al., ; Skaala et al., ). For example, size differences between domesticated and wild salmon in the river Burrishoole egg planting experiments conducted in Ireland in the late 1990s and early 2000s were reported to range from 5% to 20% (Reed et al., ), and the smolt size at age differences between domesticated, hybrid, and wild salmon from the egg planting experiments conducted in the river Guddal in Norway in the middle 2000s was typically only 0%–10% (Skaala et al., ).…”

“…However, differences between the domestication‐admixed and wild salmon (both magnitude and direction) were dependent both upon the age category of the fish, and also, the geographic region in which admixture occurred (i.e., northern Norway contra middle/southern Norway). Others have concluded that growth differences between domesticated, hybrid, and wild salmon in the marine phase are not necessarily very clear, with small differences in maximum size at age but significant differences in minimum size at age (Jonsson & Jonsson, ). While the response in adult size in the IBSEM outputs reported here is low in comparison with the observations between domestication‐admixed and nonadmixed salmon (Figure vs. results by Bolstad et al., ), it is pertinent to point out that the model outputs here reflect the population average.…”

“…In order to achieve this, strayers were set at 5% of the N ‐adults returning to the focal population (scenarios 1, 2, 5, 6), or fixed to 25, corresponding to 5% of the N ‐adults returning to the focal population in the first year of intrusion (scenarios 3, 4, 7, 8). This level of straying is within the variation displayed between Atlantic salmon populations (Jonsson & Jonsson, ; Jonsson, Jonsson, & Hansen, ; Pedersen, Rasmussen, Nielsen, Karlsson, & Nyberg, ; Skilbrei & Holm, ; Stabell, ) and was designed to reflect situations where the neighbor population remained demographically stable over time and thus provided a constant number of strayers to the focal wild population, or alternatively, varied in tandem with the focal wild population, reflecting a situation where it is ecologically connected to the focal wild population.…”