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

ABSTRACT: Genetic analyses of speciation have focused nearly exclusively on retrospective analyses of reproductive isolation between highly divergent species. Yet, a full understanding of the speciation process must encompass analysis of the consequences of genomic divergence in young lineages still capable of exchanging genes under natural conditions. The accumulation of conditionally neutral genetic variation may lead to the evolution of divergent gene networks. In a hybrid background, such mutations may no longer compensate one another, resulting in the appearance of selectively disadvantageous traits, including disruption of gene expression regulation. Here, we documented genome-wide patterns of gene expression divergence between young lineages of normal and dwarf lake whitefish and their backcross hybrids for which strong, yet incomplete post-zygotic isolation barriers exist. A significant proportion (33%) of backcross hybrids showed developmental abnormalities not seen in parental forms and eventually leading to death. While the transcriptome of parental forms was nearly identical during embryonic development, suggesting a role for stabilizing selection, all hybrids displayed strongly divergent patterns of gene expression. By comparing healthy, surviving hybrids against moribund ones, we observed that over 2000 genes were misregulated in these abnormal embryos. In particular, misregulation was significantly biased towards essential developmental genes which were strongly underexpressed. Furthermore, genes previously documented to be highly transgressive (exaggerated inter-individual variance) were almost invariably underexpressed in hybrids. Our results thus clearly showed a transcriptome-wide signature of hybrid breakdown in young, incipient species and demonstrated a persuasive link between misexpression of essential developmental genes and post zygotic isolation.

ORGANISM(S): Osmerus mordax Oncorhynchus tshawytscha Salmo salar Oncorhynchus mykiss Coregonus clupeaformis

PROVIDER: GSE23095 | GEO | 2010/08/01

SECONDARY ACCESSION(S): PRJNA131871

REPOSITORIES: GEO

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Project description:Genetic analyses of speciation have focused nearly exclusively on retrospective analyses of reproductive isolation between highly divergent species. Yet, a full understanding of the speciation process must encompass analysis of the consequences of genomic divergence in young lineages still capable of exchanging genes under natural conditions. The accumulation of conditionally neutral genetic variation may lead to the evolution of divergent gene networks. In a hybrid background, such mutations may no longer compensate one another, resulting in the appearance of selectively disadvantageous traits, including disruption of gene expression regulation. Here, we documented genome-wide patterns of gene expression divergence between young lineages of normal and dwarf lake whitefish and their backcross hybrids for which strong, yet incomplete post-zygotic isolation barriers exist. A significant proportion (33%) of backcross hybrids showed developmental abnormalities not seen in parental forms and eventually leading to death. While the transcriptome of parental forms was nearly identical during embryonic development, suggesting a role for stabilizing selection, all hybrids displayed strongly divergent patterns of gene expression. By comparing healthy, surviving hybrids against moribund ones, we observed that over 2000 genes were misregulated in these abnormal embryos. In particular, misregulation was significantly biased towards essential developmental genes which were strongly underexpressed. Furthermore, genes previously documented to be highly transgressive (exaggerated inter-individual variance) were almost invariably underexpressed in hybrids. Our results thus clearly showed a transcriptome-wide signature of hybrid breakdown in young, incipient species and demonstrated a persuasive link between misexpression of essential developmental genes and post zygotic isolation. Samples of dwarf, normal, backcross-healthy and backcross-moribund were hybridized in a loop design, involving eight biological replicates for the backcross-healthy and backcross-moribund comparison and six for the others. Dye swap was performed between each replicate. As a result, we obtained a final set of 32 microarray slides.

Project description:The formation of new species is often a consequence of genetic incompatibilities accumulated between populations during allopatric divergence. When divergent taxa interbreed, these incompatibilities impact physiology and have a direct cost resulting in reduced hybrid fitness. Recent surveys of gene regulation in interspecific hybrids have revealed anomalous expression across large proportions of the genome, with 30-70% of all genes apparently misexpressed, mostly in the direction of down-regulation. However, since most of these studies have focused on pairs of species exhibiting high degrees of reproductive isolation, the association between regulatory disruption and reduced hybrid fitness prior to species formation remains unclear. Within the copepod species Tigriopus californicus, interpopulation hybrids show reduced fitness associated with mitochondrial dysfunction. Here we show that in contrast to studies of interspecific hybrids, only 1.2% of the transcriptome was misexpressed in interpopulation hybrids of T. californicus, and nearly 80% of misexpressed genes were overexpressed rather than underexpressed. Moreover, many of the misexpressed genes were components of functional pathways impacted by mitonuclear incompatibilities in hybrid T. californicus (e.g., oxidative phosphorylation and antioxidant response). We also show that the magnitude of hybrid misregulation is not dependent on levels of protein sequence divergence, even though the latter is correlated with expression divergence between parental populations. Our results suggest that hybrid breakdown at early stages of speciation may result from initial incompatibilities amplified by the cost of compensatory physiological responses. Our experiment included nine RNA-seq samples: 3 San Diego, 2 Santa Cruz, and 4 hybrid samples. For each sample, 400-500 copepods across all developmental stages were collected from their stock cultures. They were transferred to fresh filtered seawater in a 50-mL Falcon tubes and immersed in a 20°C water bath for two hours. Water was then quickly removed, 4 mL of Tri-Reagent (Sigma) added, and tissue immediately disrupted using a tissue homogenizer. RNA was isolated following the manufacturer’s protocol. Re-suspended RNA pellets were further purified with RNeasy Mini columns (Qiagen), and final sample integrity and quantity were assessed with an Agilent 2100 BioAnalyzer. Please note that two samples (GSM1531288, GSM1531290) have been accessioned under BioProject PRJNA168170, SRA study SRP013608, while the remaining seven samples under BioProject PRJNA263967, SRA Study SRP048974. The current records including all 9 samples (PRJNA264820/SRP049247) were re-created for the convenient retrieval of the complete raw data from SRA

Project description:Background: The Dobzhansky-Muller (D-M) model of speciation by genic incompatibility is widely accepted as the primary cause of interspecific postzygotic isolation. Since the introduction of this model, there have been theoretical and experimental data supporting the existence of such incompatibilities. However, speciation genes have been largely elusive, with only a handful of candidate genes identified in a few organisms. The Saccharomyces sensu stricto yeasts have small genomes, can be easily cultured, and can mate interspecifically to produce sterile hybrids, are thus an ideal model for studying postzygotic isolation. Among them, only a single D-M pair has been found, between S. bayanus and S. cerevisiae, comprising the mitochondrially targeted product of a nuclear gene, AEP2, and a mitochondrially encoded locus, OLI1, the 5' region of whose transcript is bound by Aep2. Thus far, no D-M pair of nuclear genes has been identified between any sensu stricto yeasts. Methods: We report here the first detailed genome-wide analysis of rare F2 progeny from an otherwise sterile hybrid, and show that no classic D-M pairs of speciation genes exist between the nuclear genomes of the closely related yeasts S. cerevisiae and S. paradoxus. Instead, our analyses suggest that more complex interactions may be responsible for their post-zygotic separation. These interactions most likely involve multiple loci having weak effects, as there were multiple significant pairwise combinations of loci, with no single combination being completely excluded from the viable F2s. Conclusions: The lack of a nuclear encoded classic D-M pair between these two yeasts, yet the existence of multiple loci that may each exert a small effect through complex interactions, suggests that initial speciation events might not always be mediated by D-M pairs. An alternative explanation may be that "death by a thousand cuts" leads to speciation, whereby an accumulation of polymorphisms can lead to an incompatibility between the species "transcriptional and metabolic networks, with no single pair at least initially being responsible for the incompatibility. After such a speciation event, it is possible that one or more D-M pairs might subsequently arise following isolation. Genotypes for hybrids between S. cerevisiae and S. paradoxus. A genotyping experiment design type classifies an individual or group of individuals on the basis of alleles, haplotypes, SNP's.

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

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