The Transcriptional Landscape of Cross-Specific Hybrids and Its Possible Link With Growth in Brook Charr (Salvelinus fontinalis Mitchill)

Abstract

The genetic mechanisms underlying hybridization are poorly understood despite their potentially important roles in speciation processes, adaptative evolution, and agronomical innovation. In this study, transcription profiles were compared among three populations of brook charr and their hybrids using microarrays to assess the influence of hybrid origin on modes of transcription regulation inheritance and on the mechanisms underlying growth. We found that twice as many transcripts were differently expressed between the domestic population and the two wild populations (Rupert and Laval) than between wild ones, despite their deeper genetic distance. This could reflect the consequence of artificial selection during domestication. We detected that hybrids exhibited strikingly different patterns of mode of transcription regulation, being mostly additive (94%) for domestic 3 Rupert, and nonadditive for Laval 3 domestic (45.7%) and Rupert 3 Laval hybrids (37.5%). Both heterosis and outbreeding depression for growth were observed among the crosses. Our results indicated that prevalence of dominance in transcription regulation seems related to growth heterosis, while prevalence of transgressive transcription regulation may be more related to outbreeding depression. Our study clearly shows, for the first time in vertebrates, that the consequences of hybridization on both the transcriptome level and the phenotype are highly dependent on the specific genetic architectures of crossed populations and therefore hardly predictable.

Linking transcriptomic and genomic variation to growth in brook charr hybrids (Salvelinus fontinalis, Mitchill)

“…In our previous study (Bougas et al, 2010), microarrays were used to identify the mode of gene expression inheritance by comparison of transcript levels between hybrid and parental crosses. In order to associate the allelic imbalance patterns of the present study with their mode of gene expression inheritance, genes found in both this microarray and the 454 sequencing experiments D~R# and L~D# were used, as described in Supplementary Methods S1.…”

“…To confirm the mode of gene expression inheritance determined from our previous microarray study (Bougas et al, 2010), the transcript abundance for five genes with allelic imbalance was determined in hybrids and their parental populations using quantitative real-time PCR (qRT-PCR). Gene-specific primers and probes (Supplementary Table S1) were designed from the contig consensus sequences and no SNP was contained in either the primers or the probes.…”

“…To achieve this, microarray results from Bougas et al (2010) and new qRT-PCR results were used to link the mode of expression regulation inheritance with allelic imbalance for genes that were detected in the two experiments. Genes were classified as additive when the level of expression in the hybrids was not significantly different from the average value of parental populations.…”

“…For example, in hybrids, gene expression can be additive or dominant or the gene can be misexpressed (under/overdominant) relative to the expression level observed in their parents. Within species, the mode of transcription inheritance depends on the parental genetic architecture and cannot be predicted based on the information of parental phenotypes or the amount of genetic divergence between the parental populations (Bougas et al, 2010). Because of these complexities, the molecular mechanisms linking transcriptomic differences to the phenotype are still poorly understood, especially so in nonmodel species.…”

“…In the Province of Québec, Canada, it represents 57% of the fresh-water aquaculture production in weight (MAPAQ, 2010). Hybrids were produced using three genetically different populations, two wild and one domestic, and used to investigate phenotypic and genomic differences relative to their parental populations (Bougas et al, 2010). In this previous study, we found that the hybrid crosses exhibited contrasting modes of gene expression inheritance, being mostly additive for domestic~(D) Â Rupert # (R) hybrids and predominantly nonadditive for Laval~(L) Â domestic # (D) hybrids.…”