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Divergence in gene regulation at young life history stages of whitefish (Coregonus sp.) and the emergence of genomic isolation.

ABSTRACT: BACKGROUND: The evolution of barriers to reproduction is of key interest to understand speciation. However, there may be a current bias towards studying intrinsic postzygotic isolation in old species pairs as compared to the emergence of barriers to gene flow through adaptive divergence. This study evaluates the relative importance of both processes in the evolution of genomic isolation in incipient species of whitefish (Coregonus clupeaformis) for which preliminary data suggest that postzygotic isolation emerges with intrinsic factors acting at embryo stages but also due to extrinsic factors during adult life. RESULTS: Gene expression data were screened using cDNA microarrays to identify regulatory changes at embryo and juvenile stages that provide evidence for genomic divergence at the underlying genetic factors. A comparison of different life history stages shows that 16-week old juvenile fish have 14 times more genes displaying significant regulatory divergence than embryos. Furthermore, regulatory changes in juvenile fish match patterns in adult fish suggesting that gene expression divergence is established early in juvenile fish and persists throughout the adult phase. Comparative analyses with results from previous studies on dwarf-normal species pairs show that at least 26 genetic factors identified in juvenile fish are candidate traits for adaptive divergence in adult fish. Eight of these show parallel directions of gene expression divergence independent of tissue type or age of the fish. The latter are associated with energy metabolism, a complex trait known to drive adaptive divergence in dwarf and normal whitefish. CONCLUSION: Although experimental evidence suggests the existence of genetic factors that cause intrinsic postzygotic isolation acting in embryos, the analysis presented here provided few candidate genes in embryos, which also corroborate previous studies showing a lack of ecological divergence between sympatric dwarf and normal whitefish at the larval stage. In contrast, gene expression divergence in juveniles can be linked to adaptive traits and seems to be driven by positive selection. The results support the idea that adaptive differentiation may be more important in explaining the emergence of barriers to gene flow in an early phase of speciation by providing a broad genomic basis for extrinsic postzygotic isolation rather than intrinsic barriers.

SUBMITTER: Nolte AW

PROVIDER: S-EPMC2662803 | biostudies-literature | 2009

REPOSITORIES: biostudies-literature

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Divergence in gene regulation at young life history stages of whitefish (Coregonus sp.) and the emergence of genomic isolation.

Nolte Arne W AW Renaut Sébastien S Bernatchez Louis L

BMC evolutionary biology 20090316

<h4>Background</h4>The evolution of barriers to reproduction is of key interest to understand speciation. However, there may be a current bias towards studying intrinsic postzygotic isolation in old species pairs as compared to the emergence of barriers to gene flow through adaptive divergence. This study evaluates the relative importance of both processes in the evolution of genomic isolation in incipient species of whitefish (Coregonus clupeaformis) for which preliminary data suggest that post ...[more]

PMID: 19291312

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Project description: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 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 based on co-localization 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. 88% of eQTL-phenotypic QTL co-localization involved growth rate and condition factor QTL, two traits central to adaptive divergence between whitefish species pairs. Hotspots co-localized 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 co-localization of brain eQTL with behavioral QTL, which provides insight on 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. Keywords: eQTL mapping, gene expression, linkage mapping, adaptive radiation, Coregonus, microarrays The objective of this study was to elucidate the genomic distribution and sex-specificity of brain eQTL in dwarf and normal lake whitefish. Dissected brain tissue (250-350 mg) was sampled for 55 individuals from a hybrid x dwarf backcross mapping family. We used a loop design (YANG and SPEED 2002; CHURCHILL 2002) to maximize the number of sampled meioses. Each of 55 samples was technically replicated on two distinct slides, while performing dye swapping (Cy3 and Alexa) to estimate the dye intensity variation bias. After correcting for local background, raw intensity values were both log2 transformed and normalized using the regional LOWESS method implemented in the R/MANOVA software (KERR et al. 2000). We used a previously generated linkage map based on the same backcross individuals for which gene expression was measured. eQTL mapping was performed with QTL Cartographer.

Dataset Information

Divergence in gene regulation at young life history stages of whitefish (Coregonus sp.) and the emergence of genomic isolation.

Publications

Divergence in gene regulation at young life history stages of whitefish (Coregonus sp.) and the emergence of genomic isolation.

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