Consequences of farmed–wild hybridization across divergent wild populations and multiple traits in salmon

Abstract

Theory predicts that hybrid fitness should decrease as population divergence increases. This suggests that the effects of human-induced hybridization might be adequately predicted from the known divergence among parental populations. We tested this prediction by quantifying trait differentiation between multigenerational crosses of farmed Atlantic salmon (Salmo salar) and divergent wild populations from the Northwest Atlantic; the former escape repeatedly into the wild, while the latter are severely depleted. Under common environmental conditions and at the spatiotemporal scale considered (340 km, 12 000 years of divergence), substantial cross differentiation had a largely additive genetic basis at behavioral, life history, and morphological traits. Wild backcrossing did not completely restore hybrid trait distributions to presumably more optimal wild states. Consistent with theory, the degree to which hybrids deviated in absolute terms from their parental populations increased with increasing parental divergence (i.e., the collective environmental and life history differentiation, genetic divergence, and geographic distance between parents). Nevertheless, while these differences were predictable, their implications for risk assessment were not: wild populations that were equally divergent from farmed salmon in the total amount of divergence differed in the specific traits at which this divergence occurred. Combined with ecological data on the rate of farmed escapes and wild population trends, we thus suggest that the greatest utility of hybridization data for risk assessment may be through their incorporation into demographic modeling of the short- and long-term consequences to wild population persistence. In this regard, our work demonstrates that detailed hybridization data are essential to account for life-stage-specific changes in phenotype or fitness within divergent but interrelated groups of wild populations. The approach employed here will be relevant to risk assessments in a range of wild species where hybridization with domesticated relatives is a concern, especially where the conservation status of the wild species may preclude direct fitness comparisons in the wild.

Multigenerational hybridisation and its consequences for maternal effects in Atlantic salmon

“…Between the wild and domesticated populations used in the present study, large differences in maternal body size existed (see also Fraser et al, 2010). In our four dam crosses, egg size also generally increased with maternal body size.…”

“…DD salmon were derived from an aquaculture population founded by 50-100 wild-caught individuals that underwent three generations of selection, primarily for rapid growth (Glebe, 1998). The two wild river populations are naturally separated by B200 km (waterway distance) and are divergent for neutral genetic and ecological parameters (reviewed by Fraser et al, 2010).…”

“…This lack of concordance might have been caused by (i) too large variation for cross means to detect possible effect combinations (also because of few DD dam cross families), (ii) our use of a simple diallelic model with epistasis between two loci per level, whereas quantitative traits probably underlie several loci, each with many alleles. Moreover, (iii) Atlantic salmon possess many gene duplications due to a presumed family-specific genome duplication event, which might render a diploid model partly inappropriate (Fraser et al, 2010).…”

Rapid morphological divergence of cultured cod of the northwest Atlantic from their source population

“…These cultured phenotypes can be the product of a plastic response whereby different phenotypes can be expressed by a single genotype in response to different environmental conditions (Imre et al 2002, Skjae raasen et al 2008, Mayer et al 2011, Vehanen & Huusko 2011, or these phenotypes may be the result of genetic changes brought about through both intentional and unintentional selection , Einum & Fleming 2001, Fleming & Petersson 2001, Hutchings & Fraser 2008, Solberg et al 2013. The degree of phenotypic change, and its permanence, are both a function of the time an individual has spent in captive conditions (Pakkasmaa et al 1998, von Cramon-Taubadel et al 2005, as well as the degree of genetic change from the ancestral lineage due to captivity , Blanchet et al 2008, reviewed by Hutchings & Fraser 2008, Fraser et al 2010. Thus, if it is presumed that the phenotypes of wild fish are the product of adaptation to their local environment, then the degree to which the phenotype of cultured fish diverges from the wild type is likely a reflection of how maladaptive the cultured phenotype may be if exposed to the wild environment.…”

Feeding preference of recaptured Atlantic salmon Salmo salar following simulated escape from fish pens during autumn

“…One of the more serious challenges is that farming has been correlated with declines in natural salmon populations (Ford & Myers 2008). Escapees will interfere with the genetic make-up of wild stocks if they manage to interbreed and may potentially contribute to the spread of diseases and parasites (Lura & Saegrov 1991, Heuch & Mo 2001, McGinnity et al 2004, Naylor et al 2005, Hindar et al 2006, Skaala et al 2006, Ferguson et al 2007, Fraser et al 2010). …”