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

Renaut, Sébastien; Bernatchez, Louis

doi:10.1038/hdy.2010.149

Cited by 59 publications

(65 citation statements)

References 42 publications

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“…The authors concluded that resource limitation resulted in increased potential for competition and selective pressure towards optimal normal and dwarf adaptive peaks. In addition, Lu & Bernatchez [47] and Renaut & Bernatchez [46] also showed that there was a continuum of differentiation among lakes both from a phenotypic and genetic standpoint, from East Lake being the least differentiated to Indian, Webster and Cliff L., being the most differentiated. Here, East L. generally differed from the three more differentiated species pairs, being characterized by a smaller number of putative islands of divergence.…”

Section: Discussion (A) Association Between F St and Quantitative Tramentioning

confidence: 99%

“…Fourth, the repeated independent parallel evolution of normal and dwarf phenotypes implies that populations evolved under similar selective pressures [31]. Lastly, these lake whitefish populations have small effective population sizes (Ne , 1000), low migration rates (m varying between 0.0004 and 0.0019) [41,44], as well as strong selection against hybrids [45][46][47]. Under these conditions, divergence hitchhiking is theoretically expected to facilitate the formation of large genomic islands of divergence [9].…”

Section: The Lake Whitefish Study Systemmentioning

confidence: 99%

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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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Section: Discussion (A) Association Between F St and Quantitative Tramentioning

confidence: 99%

Section: The Lake Whitefish Study Systemmentioning

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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“…In particular, Gibson et al (2004) showed that 2% of the 12 559 analyzed genes in F1 heterozygotes presented parental effects (that is, a resemblance to either paternal or maternal expression). In fishes, previous studies mostly emphasized differences in gene expression during embryogenesis to detect maternal-effect genes across developmental transitions or to detect differences in development rate in embryos (Mathavan et al, 2005;Bai et al, 2007;Nolte et al, 2009;Xu et al, 2010;Renaut et al, 2011). To our knowledge, however, no study has yet systematically focused on investigating the dynamics of parental effects on the transcriptome across different development stages.…”

Section: Introductionmentioning

confidence: 97%

The influence of parental effects on transcriptomic landscape during early development in brook charr (Salvelinus fontinalis, Mitchill)

2013

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Parental effects represent an important source of variation in offspring phenotypes. Depending on the specific mechanisms involved, parental effects may be caused to different degrees by either the maternal or the paternal parent, and these effects may in turn act at different stages of development. To detect parental effects acting on gene transcription regulation and length phenotype during ontogeny, the transcriptomic profiles of two reciprocal hybrids from Laval Â Rupert and Laval Â Domestic populations of brook charr were compared at hatching, yolk sac resorption and 15 weeks after exogenous feeding. Using a salmonid cDNA microarray, our results show that parental effects modulated gene expression among reciprocal hybrids only at the yolk sac resorption stage. In addition, Laval Â Domestic and Laval Â Rupert reciprocal hybrids differed in the magnitude of theses parental effects, with 199 and 630 differentially expressed transcripts, respectively. This corresponds to a maximum of 18.5% of the analyzed transcripts. These transcripts are functionally related to cell cycle, nucleic acid metabolism and intracellular protein traffic, which is consistent with observed differences associated with embryonic development and growth differences in other fish species. Our results thus illustrate how parental effects on patterns of gene transcription seem dependent on the genetic architecture of the parents. In addition, in absence of transcriptional differences, non-transcript deposits in the yolk sac could contribute to the observed length differences among the reciprocal hybrids before yolk sac resorption.

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“…Gene flow between these sympatric nascent species is still possible [22,23] despite the existence of hybrid incompatibilities leading to a dramatic reduction in embryonic survival in first and second generation hybrids [24 -26]. This mortality is associated with the appearance of a 'malformed', slow-growing phenotype in approximately 30-50% of backcross individuals, with the remaining embryos developing normally ('healthy' phenotype) [26]. Consistent with predictions from a BDM model integrating transcriptional data [27], previous studies have documented a much higher variance in gene expression in malformed backcrosses compared with parental forms [26,28].…”

Section: Introductionmentioning

confidence: 99%

Reproductive isolation in a nascent species pair is associated with aneuploidy in hybrid offspring

et al. 2015

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Speciation may occur when the genomes of two populations accumulate genetic incompatibilities and/or chromosomal rearrangements that prevent inter-breeding in nature. Chromosome stability is critical for survival and faithful transmission of the genome, and hybridization can compromise this. However, the role of chromosomal stability on hybrid incompatibilities has rarely been tested in recently diverged populations. Here, we test for chromosomal instability in hybrids between nascent species, the 'dwarf' and 'normal' lake whitefish (Coregonus clupeaformis). We examined chromosomes in pure embryos, and healthy and malformed backcross embryos. While pure individuals displayed chromosome numbers corresponding to the expected diploid number (2n ¼ 80), healthy backcrosses showed evidence of mitotic instability through an increased variance of chromosome numbers within an individual. In malformed backcrosses, extensive aneuploidy corresponding to multiples of the haploid number (1n ¼ 40, 2n ¼ 80, 3n ¼ 120) was found, suggesting meiotic breakdown in their F 1 parent. However, no detectable chromosome rearrangements between parental forms were identified. Genomic instability through aneuploidy thus appears to contribute to reproductive isolation between dwarf and normal lake whitefish, despite their very recent divergence (approx. 15 -20 000 generations). Our data suggest that genetic incompatibilities may accumulate early during speciation and limit hybridization between nascent species.

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

Cited by 59 publications

References 42 publications

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

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

The influence of parental effects on transcriptomic landscape during early development in brook charr (Salvelinus fontinalis, Mitchill)

Reproductive isolation in a nascent species pair is associated with aneuploidy in hybrid offspring

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