Can variation in standard metabolic rate explain context-dependent performance of farmed Atlantic salmon offspring?

Grethe Robertsen,Sigurd Einum,Tonje Aronsen,Ian A Fleming,Donald Reid,Sten Karlsson,Kjetil Hindar,Line E Sundt‐Hansen,Eli Kvingedal,Ola Ugedal

doi:10.1002/ece3.4716

Abstract

Escaped farmed Atlantic salmon interbreed with wild Atlantic salmon, leaving offspring that often have lower success in nature than pure wild salmon. On top of this, presence of farmed salmon descendants can impair production of wild‐type recruits. We hypothesize that both these effects connect with farmed salmon having acquired higher standard metabolic rates (SMR, the energetic cost of self‐maintenance) during domestication. Fitness‐related advantages of phenotypic traits associated with both high SMR and farmed salmon (e.g., social dominance) depend on environmental conditions, such as food availability. We hypothesize that farmed offspring have an advantage at high food availability due to, for example, dominance behavior but suffer increased risks of starvation when food is scarce because this behavior is energy‐demanding. To test these hypotheses, we first compare embryo SMR of pure farmed, farmed‐wild hybrids and pure wild offspring. Next, we test early‐life performance (in terms of survival and growth) of hybrids relative to that of their wild half‐siblings, as well as their competitive abilities, in semi‐natural conditions of high and low food availability. Finally, we test how SMR affects early‐life performance at high and low food availability. We find inconclusive support for the hypothesis that domestication has induced increased SMR. Further, wild and hybrid juveniles had similar survival and growth in the semi‐natural streams. Yet, the presence of hybrids led to decreased survival of their wild half‐siblings. Contrary to our hypothesis about context‐dependency, these effects were not modified by food availability. However, wild juveniles with high SMR had decreased survival when food was scarce, but there was no such effect at high food availability. This study provides further proof that farmed salmon introgression may compromise the viability of wild salmon populations. We cannot, however, conclude that this is connected to alterations in the metabolic phenotype of farmed salmon.

Highlights

Feral domestic animals commonly constitute a threat to the viability of wild populations since their hybridization with wild individuals can disrupt local adaptations and reduce population fitness (Frankham, 2008; Laikre, Schwartz, Waples, & Ryman, 2010)
This study advances the concern that feral domestic animals impact wild populations negatively since we found that the presence of farmed‐wild Atlantic salmon hybrids led to decreased early survival of their wild half‐siblings under controlled, semi‐natural conditions
This negative influence of hybrid offspring on survival of wild juveniles was, at least partly, caused by genes associated with farmed salmon since it prevailed irrespective of whether the wild juveniles competed with half‐siblings from wild or farmed mothers

Summary

| INTRODUCTION

Feral domestic animals commonly constitute a threat to the viability of wild populations since their hybridization with wild individuals can disrupt local adaptations and reduce population fitness (Frankham, 2008; Laikre, Schwartz, Waples, & Ryman, 2010). When interbreeding with escaped farmed salmon causes genetic introgression into wild populations (Glover et al, 2013; Karlsson, Diserud, Fiske, & Hindar, 2016; Skaala, Wennevik, & Glover, 2006), this increases the number of mal‐adapted individuals in nature (Bolstad et al, 2017). The presence of individuals with farmed salmon ancestry can entail decreased production of seaward migrants of the wild type (Fleming et al, 2000) Both the reduced success of farmed salmon and their descendants in nature, and the negative effect of their presence for production of wild salmon, are likely related to genomic and phenotypic alterations that have occurred during the domestication process (Bolstad et al, 2017; Liu et al, 2017). We test for effects of different levels of SMR on juvenile performance at high and low food availability by collating data on family‐level embryo SMR with data on performance at the individual and family level

| MATERIALS & METHODS

| DISCUSSION

Findings

CONFLICT OF INTEREST