The Phenomics and Expression Quantitative Trait Locus Mapping of Brain Transcriptomes Regulating Adaptive Divergence in Lake Whitefish Species Pairs (Coregonus sp.)

Abstract

We used microarrays and a previously established linkage map to localize the genetic determinants of brain gene expression for a backcross family of lake whitefish species pairs (Coregonus sp.). Our goals were to elucidate the genomic distribution and sex specificity of brain expression QTL (eQTL) and to determine the extent to which genes controlling transcriptional variation may underlie adaptive divergence in the recently evolved dwarf (limnetic) and normal (benthic) whitefish. We observed a sex bias in transcriptional genetic architecture, with more eQTL observed in males, as well as divergence in genome location of eQTL between the sexes. Hotspots of nonrandom aggregations of up to 32 eQTL in one location were observed. We identified candidate genes for species pair divergence involved with energetic metabolism, protein synthesis, and neural development on the basis of colocalization of eQTL for these genes with eight previously identified adaptive phenotypic QTL and four previously identified outlier loci from a genome scan in natural populations. Eighty-eight percent of eQTL-phenotypic QTL colocalization involved growth rate and condition factor QTL, two traits central to adaptive divergence between whitefish species pairs. Hotspots colocalized with phenotypic QTL in several cases, revealing possible locations where master regulatory genes, such as a zinc-finger protein in one case, control gene expression directly related to adaptive phenotypic divergence. We observed little evidence of colocalization of brain eQTL with behavioral QTL, which provides insight into the genes identified by behavioral QTL studies. These results extend to the transcriptome level previous work illustrating that selection has shaped recent parallel divergence between dwarf and normal lake whitefish species pairs and that metabolic, more than morphological, differences appear to play a key role in this divergence.

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

“…Proportion refers to the fraction of differentially expressed genes out of the total number of genes that were significantly expressed at a given life stage. and Whiteley et al (2008) distributed over numerous linkage groups with several overlapping with pQTL ( figure 3). More specifically, results for white muscle revealed 261 eQTL involving 138 unigenes (for a mean of about 1.9 eQTL per gene) distributed over 24 linkage groups and consisting of 15 eQTL that co-localized with pQTL.…”

“…These could represent mutations related to gene regulation and be interpreted as a form of early substitution of large effect theoretically predicted during adaptive divergence (Orr 2005), and hypothetically play a central role in the divergence of dwarf and normal whitefish. Another prominent feature of both eQTL maps was a pronounced sex bias in transcriptional genetic architecture observed for both brain and white muscle, with more eQTL observed in males in the case of brain and vice versa for white muscle Whiteley et al 2008). In addition, we detected differentially expressed transcripts associated with eQTL segregating in sex-specific datasets and mostly belonging to functional groups that differentiate dwarf and normal whitefish in natural populations.…”

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.…”

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

“…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.…”