The transcriptomics of life‐history trade‐offs in whitefish species pairs (Coregonussp.)

Abstract

Despite the progress achieved in elucidating the ecological mechanisms of adaptive radiation, there has been little focus on documenting the extent of adaptive differentiation in physiological functions during this process. Moreover, a thorough understanding of the genomic basis underlying phenotypic adaptive divergence is still in its infancy. One important evolutionary process for which causal genetic mechanisms are largely unknown pertains to life-history trade-offs. We analysed patterns of gene transcription in liver tissue of sympatric dwarf and normal whitefish from two natural lakes, as well as from populations reared in controlled environments, using a 16,006-gene cDNA microarray in order to: (i) document the extent of physiological adaptive divergence between sympatric dwarf and normal species pairs, and (ii) explore the molecular mechanisms of differential life history trade-offs between growth and survival potentially involved in their adaptive divergence. In the two natural lakes, 6.45% of significantly transcribed genes showed regulation either in parallel fashion (2.39%) or in different directions (4.06%). Among genes showing parallelism in regulation patterns, we observed a higher proportion of over-expressed genes in dwarf relative to normal whitefish (70.6%). Patterns observed in controlled conditions were also generally congruent with those observed in natural populations. Dwarf whitefish consistently showed significant over-expression of genes potentially associated with survival through enhanced activity (energy metabolism, iron homeostasis, lipid metabolism, detoxification), whereas more genes associated with growth (protein synthesis, cell cycle, cell growth) were generally down-regulated in dwarf relative to normal whitefish. Overall, parallelism in patterns of gene transcription, as well as patterns of interindividual variation across controlled and natural environments, provide strong indirect evidence for the role of selection in the evolution of differential regulation of genes involving a vast array of potentially adaptive physiological processes between dwarf and normal whitefish. Our results also provide a first mechanistic, genomic basis for the observed trade-off in life-history traits distinguishing dwarf and normal whitefish species pairs, wherein enhanced survival via more active swimming, necessary for increased foraging and predator avoidance, engages energetic costs that translate into slower growth rate and reduced fecundity in dwarf relative to normal whitefish.

On the origin of species: insights from the ecological genomics of lake whitefish

“…The most represented functions were protein synthesis, cell growth, energy metabolism and muscle contraction. Transcripts involved in protein synthesis and cell growth exhibited systematically opposed additive effects to those associated with energy metabolism and muscle contraction , which is consistent with the observed trade-off in life-history traits and differential gene expression distinguishing dwarf and normal whitefish (St-Cyr et al 2008). Directional predominance of additive effects provides strong evidence for the role of directional selection in shaping genome architecture (Orr 1998).…”

“…It is also noteworthy that parallelism in patterns of gene expression was observed for the majority of those genes in microarray studies St-Cyr et al 2008) and that several loci linked to Lg3 had previously been found to be significantly resistant to introgression between whitefish from distinct glacial races (Rogers et al 2001). …”

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

“…Microarrays and, more recently, RNA-seq by means of NGS technologies have been used to compare the transcriptomes of phenotypically distinct individuals, namely in salmonid fishes St-Cyr et al, 2008;Goetz et al, 2010;Jeukens et al, 2010;Xu et al, 2010). Typically, many transcriptomic differences involved genes with functions related to energy production, muscular activity, immunity and cell cycle regulation processes.…”

“…Numerous studies have characterized genomewide patterns of gene expression among populations exhibiting phenotypic variation. In fishes in particular, the majority of such studies have not only used microarrays (Oleksiak et al, 2002;Whitehead and Crawford, 2005;Whitehead and Crawford, 2006;St-Cyr et al, 2008;Whiteley et al, 2008), but also next-generation sequencing to a lower extent (Elmer et al, 2010;Goetz et al, 2010;Jeukens et al, 2010;Shen et al, 2012). Hybridization can also lead to different modes of transcription regulation.…”

Insights into the role of differential gene expression on the ecological adaptation of the snail Littorina saxatilis

“…However, there is still much to be learned about how divergent populations adapt to different environments under the effect of natural selection, which ultimately may evolve into biological species [3]. The new "omics" technologies, despite being very young, can contribute to this since they have taken up a very important position in the biological scientific landscape during the last decade [4].…”