Parallelism in gene transcription among sympatric lake whitefish (Coregonus clupeaformisMitchill) ecotypes

Abstract

We tested the hypothesis that phenotypic parallelism between dwarf and normal whitefish ecotypes (Coregonus clupeaformis, Salmonidae) is accompanied by parallelism in gene transcription. The most striking phenotypic differences between these forms implied energetic metabolism and swimming activity. Therefore, we predicted that genes showing parallel expression should mainly belong to functional groups associated with these phenotypes. Transcriptome profiles were obtained from white muscle by using a 3557 cDNA gene microarray developed for the Atlantic salmon (Salmo salar). A total of 1181 genes expressed in both lake populations hybridized on the array. Significant differential expression between ecotypes was detected for 134 (11.3%) and 195 (16.5%) gene clones in Cliff Lake and Indian Pond, respectively. Fifty-one genes (4.3%) showed parallel differential expression between lakes, among which 35 were expressed in opposite directions. Sixteen genes (1.35%) showed true parallelism of transcription, which mainly belonged to energetic metabolism and regulation of muscle contraction functional groups. Variance in expression was significantly reduced for these genes compared to those not showing directionality in parallelism of expression. Candidate genes associated with parallelism in swimming activity and energetic metabolism based on their level and variance in expression were identified. These results add to the growing evidence that parallel phenotypic evolution also involves parallelism at both the genotypic and regulatory level, which may at least partly be associated with genetic constraints. It also provides further evidence for the determinant role of divergent natural selection in driving phenotypic divergence, and perhaps reproductive isolation, in the adaptive radiation of lake whitefish. This study adds to a nascent field employing microarrays as powerful tools for investigating the evolutionary processes of adaptive divergence among natural populations.

Linkage Maps of thedwarfand Normal Lake Whitefish (Coregonus clupeaformis) Species Complex and Their Hybrids Reveal the Genetic Architecture of Population Divergence

“…For example, parallel locus-specific reductions in gene flow for growth QTL have been found between dwarf and Normal ecotypes among independently diverging populations, indicating that growth differences among populations are maintained by divergent selection (Rogers and Bernatchez 2005). Evidence for parallel evolution indirectly demonstrated the role of divergent selection in maintaining differentiation between sympatric whitefish ecotypes for several traits, including morphology, behavior, as well as gene expression associated with swimming efficiency and energy metabolism Rogers et al 2002;Derome et al 2006). As such, understanding the consequences of population divergence in the lake whitefish will benefit from a population genomics approach that embraces a genomewide search for the genetic basis of phenotype-environment associations (Luikart et al 2003;Schö tterer 2003).…”

“…However, postglacial parallel phenotypic evolution of sympatric pairs ) exhibits bimodal adult size distributions whereby divergent selection for differential growth has maintained and promoted sympatric divergence between dwarf and Normal populations associated with the use of distinct limnetic and benthic trophic niches (Chouinard et al 1996;Campbell and Bernatchez 2004;Rogers and Bernatchez 2005). Altogether, these populations display adaptive trait differentiation with respect to life history , behavioral (Rogers et al 2002), physiological (Rogers and Bernatchez 2005), transcriptional (Derome et al 2006), and morphological traits Rogers et al 2002;Bernatchez 2004). A linkage mapping approach in young diverging populations of the lake whitefish could: (1) substantially improve our understanding of the genetic architecture of historically contingent and adaptive trait differences contributing to the population divergence between species and (2) help in identifying genomic regions permeable or resistant to gene flow.…”

The developmental transcriptome of contrasting Arctic charr (Salvelinus alpinus) morphs

“…RNA-seq was used to study salinity tolerance in Arctic charr, linking expression and quantitative trait loci 16 . Microarray studies of adult lake whitefish ( Coregonus clupeaformis ) pointed to parallel expression differences between benthic and limnetic forms 17 . Filteau et al (2013) 18 found that a set of coexpressed genes differentiated the two whitefish morphotypes, implicating Bone morphogenesis protein (BMP) signaling in the development of ecological differences in tropic morphology.…”

Transcriptome-wide signature of hybrid breakdown associated with intrinsic reproductive isolation in lake whitefish species pairs (Coregonus spp. Salmonidae)

“…Furthermore, the validity of this array has been amply demonstrated in lake whitefish, whereas hybridization signal is the same as for Atlantic salmon (von Schalburg et al, 2005). Sequence divergence between normal and dwarf is also very low and therefore did not affect hybridization kinetics (Derome et al, 2006;Whiteley et al, 2008). Samples of dwarf, normal, backcross-healthy and backcross-moribund were hybridized in a loop design, involving eight biological replicates for the backcross-healthy and backcrossmoribund comparison and six for the others.…”