Pervasive Sex-Linked Effects on Transcription Regulation As Revealed by Expression Quantitative Trait Loci Mapping in Lake Whitefish Species Pairs (Coregonus sp., Salmonidae)

Derôme, Nicolas; Bougas, Bérénice; Rogers, Sean M.; Whiteley, Andrew R.; Labbe, Aurélie; Laroche, Jérôme; Bernatchez, Louis

doi:10.1534/genetics.107.086306

Cited by 46 publications

(88 citation statements)

References 93 publications

(98 reference statements)

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“…In whitefish, a recent eQTL analysis of muscle tissue that used the same backcross individuals used in our study revealed that 21% of transcripts were differentially expressed between males and females . In addition, our observation of significantly more eQTL in males than in either the female-only or combined data set provides additional support for the results of Derome et al (2008), which observed divergence in the genetic architecture of gene expression between sexes. Together, these studies suggest that sex-biased genetic architecture of transcription may be an important component of evolutionary divergence in whitefish.…”

Section: Discussionsupporting

confidence: 76%

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

Whiteley

Derôme

Rogers³

et al. 2008

Genetics

107

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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.

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Section: Discussionsupporting

confidence: 76%

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

Whiteley

Derôme

Rogers³

et al. 2008

Genetics

107

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“…(b) Gene expression and genome scan in natural populations We used gene expression data obtained from the analysis of white muscle [35] and whole brain [34] tissues. Briefly, these studies used microarrays and the linkage map of Rogers et al [32] to localize eQTL of genes expressed in white muscle (262 transcripts localized) and brain (249 transcripts localized) for one of the backcross family (BC D map).…”

Section: Methods (A) Genetic Mappingmentioning

confidence: 99%

“…Combining both QTL and genome scan information revealed that a total of six eQTL regions co-localized with pQTL and were also outliers in a genome scan study [31,33]. Moreover, these genomic regions were nonrandomly distributed across the genome and hinted at the role of major regulatory hotspots controlling the expression of numerous genes [34,35].…”

Section: Methods (A) Genetic Mappingmentioning

confidence: 99%

Genome-wide patterns of divergence during speciation: the lake whitefish case study

Renaut

Maillet

Normandeau

et al. 2012

Phil. Trans. R. Soc. B

103

117

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The nature, size and distribution of the genomic regions underlying divergence and promoting reproductive isolation remain largely unknown. Here, we summarize ongoing efforts using young (12 000 yr BP) species pairs of lake whitefish (Coregonus clupeaformis) to expand our understanding of the initial genomic patterns of divergence observed during speciation. Our results confirmed the predictions that: (i) on average, phenotypic quantitative trait loci (pQTL) show higher F ST values and are more likely to be outliers (and therefore candidates for being targets of divergent selection) than nonpQTL markers; (ii) large islands of divergence rather than small independent regions under selection characterize the early stages of adaptive divergence of lake whitefish; and (iii) there is a general trend towards an increase in terms of numbers and size of genomic regions of divergence from the least (East L.) to the most differentiated species pair (Cliff L.). This is consistent with previous estimates of reproductive isolation between these species pairs being driven by the same selective forces responsible for environment specialization. Altogether, dwarf and normal whitefish species pairs represent a continuum of both morphological and genomic differentiation contributing to ecological speciation. Admittedly, much progress is still required to more finely map and circumscribe genomic islands of speciation. This will be achieved through the use of next generation sequencing data but also through a better quantification of phenotypic traits moulded by selection as organisms adapt to new environmental conditions.

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“…A total of 48 loci with an average of 14 loci per lake showed restricted gene flow relative to neutral expectation, suggesting a role of directional selection on their divergence. Further insight into the identity of these 'anonymous' AFLP markers was gained by combining information obtained from population genomics with that of pQTL and eQTL mapping Derome et al 2008;Whiteley et al 2008). Thus, homology between markers used in mapping and population genomics was found for 180 markers and for 24 of the 48 outlier loci.…”

Section: Finding Evidence For Natural Selection At the Genome Level Imentioning

confidence: 99%

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

Bernatchez

Renaut

Whiteley

et al. 2010

Phil. Trans. R. Soc. B

226

317

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In contrast to the large amount of ecological information supporting the role of natural selection as a main cause of population divergence and speciation, an understanding of the genomic basis underlying those processes is in its infancy. In this paper, we review the main findings of a long-term research programme that we have been conducting on the ecological genomics of sympatric forms of whitefish (Coregonus spp.) engaged in the process of speciation. We present this system as an example of how applying a combination of approaches under the conceptual framework of the theory of adaptive radiation has yielded substantial insight into evolutionary processes in a non-model species. We also discuss how the joint use of recent biotechnological developments will provide a powerful means to address issues raised by observations made to date. Namely, we present data illustrating the potential offered by combining next generation sequencing technologies with other genomic approaches to reveal the genomic bases of adaptive divergence and reproductive isolation. Given increasing access to these new genomic tools, we argue that non-model species studied in their ecological context such as whitefish will play an increasingly important role in generalizing knowledge of speciation.

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Pervasive Sex-Linked Effects on Transcription Regulation As Revealed by Expression Quantitative Trait Loci Mapping in Lake Whitefish Species Pairs (Coregonus sp., Salmonidae)

Cited by 46 publications

References 93 publications

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

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

Genome-wide patterns of divergence during speciation: the lake whitefish case study

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

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