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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:Understanding patterns of genetic structure and adaptive variation in natural populations is crucial for informing conservation and management. Past genetic research using 11 microsatellite loci identified six genetic stocks of lake whitefish (Coregonus clupeaformis) within Lake Michigan, USA. However, ambiguity in genetic stock assignments suggested those neutral microsatellite markers did not provide adequate power for delineating lake whitefish stocks in this system, prompting calls for a genomics approach to investigate stock structure. Here, we generated a dense genomic dataset to characterize population structure and investigate patterns of neutral and adaptive genetic diversity among lake whitefish populations in Lake Michigan. Using Rapture sequencing, we genotyped 829 individuals collected from 17 baseline populations at 197,588 SNP markers after quality filtering. Although the overall pattern of genetic structure was similar to the previous microsatellite study, our genomic data provided several novel insights. Our results indicated a large genetic break between the northwestern and eastern sides of Lake Michigan, and we found a much greater level of population structure on the eastern side compared to the northwestern side. Collectively, we observed five genomic islands of adaptive divergence on five different chromosomes. Each island displayed a different pattern of population structure, suggesting that combinations of genotypes at these adaptive regions are facilitating local adaptation to spatially heterogenous selection pressures. Additionally, we identified a large linkage disequilibrium block of ~8.5 Mb on chromosome 20 that is suggestive of a putative inversion but with a low frequency of the minor haplotype. Our study provides a comprehensive assessment of population structure and adaptive variation that can help inform the management of Lake Michigan's lake whitefish fishery and highlights the utility of incorporating adaptive loci into fisheries management.

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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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