Comparing the transcriptomes of embryos from domesticated and wild Atlantic salmon (Salmo salar L.) stocks and examining factors that influence heritability of gene expression

Abstract

BackgroundDue to selective breeding, domesticated and wild Atlantic salmon are genetically diverged, which raises concerns about farmed escapees having the potential to alter the genetic composition of wild populations and thereby disrupting local adaptation. Documenting transcriptional differences between wild and domesticated stocks under controlled conditions is one way to explore the consequences of domestication and selection. We compared the transcriptomes of wild and domesticated Atlantic salmon embryos, by using a custom 44k oligonucleotide microarray to identify perturbed gene pathways between the two stocks, and to document the inheritance patterns of differentially-expressed genes by examining gene expression in their reciprocal hybrids.ResultsData from 24 array interrogations were analysed: four reciprocal cross types (W♀ × W♂, D♀ × W♂; W♀ × D♂, D♀ × D♂) × six biological replicates. A common set of 31,491 features on the microarrays passed quality control, of which about 62 % were assigned a KEGG Orthology number. A total of 6037 distinct genes were identified for gene-set enrichment/pathway analysis. The most highly enriched functional groups that were perturbed between the two stocks were cellular signalling and immune system, ribosome and RNA transport, and focal adhesion and gap junction pathways, relating to cell communication and cell adhesion molecules. Most transcripts that were differentially expressed between the stocks were governed by additive gene interaction (33 to 42 %). Maternal dominance and over-dominance were also prevalent modes of inheritance, with no convincing evidence for a stock effect.ConclusionsOur data indicate that even at this relatively early developmental stage, transcriptional differences exist between the two stocks and affect pathways that are relevant to wild versus domesticated environments. Many of the identified differentially perturbed pathways are involved in organogenesis, which is expected to be an active process at the eyed egg stage. The dominant effects are more largely due to the maternal line than to the origin of the stock. This finding is particularly relevant in the context of potential introgression between farmed and wild fish, since female escapees tend to have a higher spawning success rate compared to males.Electronic supplementary materialThe online version of this article (doi:10.1186/s12711-016-0200-6) contains supplementary material, which is available to authorized users.

Half a century of genetic interaction between farmed and wild Atlantic salmon: Status of knowledge and unanswered questions

“…A handful of studies have investigated gene‐transcription profiles of farmed and wild salmon reared under controlled conditions. These have revealed a large number of different expression profiles during very early developmental stages (Bicskei et al., ; Bicskei, Taggart, Glover, & Bron, ; Roberge, Einum, Guderley, & Bernatchez, ; Roberge, Normandeau, Einum, Guderley, & Bernatchez, ), as well as later juvenile and post‐smoltification stages (Debes, Normandeau, Fraser, Bernatchez, & Hutchings, ; Normandeau et al., ) (Table ).…”

“…Evans, Hori, Rise, & Fleming, ), which makes extracting general trends in transcription patterns between farmed and wild fish, among the various studies conducted (which includes life stage and environmental variation), a challenge. This is further complicated by the fact that gene‐by‐environment effects play a significant role in the transcriptomic responses of farmed salmon (Evans et al., ) and that transcription profiles for genes that are differentially expressed between the farmed and wild salmon do not always display additive genetic variation, and thus, hybrids often display non‐intermediate profiles (Bicskei et al., ; Normandeau et al., ; Roberge et al., ). These complexities make our prediction of the consequences of different gene expression in farmed salmon and their offspring in the wild difficult.…”

Early life traits of farm and wild Atlantic salmon Salmo salar and first generation hybrids in the south coast of Newfoundland

“…The high prevalence of maternal effects on gene flow, however, as demonstrated by a recent study by Bicskei et al . () and confirmed by the present observations on life traits is of concern, since domesticated females are more likely to contribute to gene introduction from farm escapes than males (Fleming et al ., ). In the future, common‐garden field experiments are necessary to disentangle the effects of phenotypic plasticity from genetic effects (Garcia de Leaniz et al ., ) providing information on the extent of local adaptations and a better characterization of the effect of farm fish on wild populations.…”

“…e . hatching, nesting, fry emergence and transition to exogenous feeding (Bicskei et al ., ). Even if spawning time is similar, time of hatch and emergence of farmed or hybrid alevins could be maladaptive to the natural environment, resulting in a competitive disadvantage that may work as a potential barrier against introgression (Solberg et al ., ).…”

“…While numerous studies have investigated genetic differences between farmed and wild S. salar, to date, relatively few studies have specifically focused on the critical early-life stages, i.e. hatching, nesting, fry emergence and transition to exogenous feeding (Bicskei et al, 2016). Even if spawning time is similar, time of hatch and emergence of farmed or hybrid alevins could be maladaptive to the natural environment, resulting in a competitive disadvantage that may work as a potential barrier against introgression (Solberg et al, 2014).…”