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Rougeux, C.

Publications and source records attributed to Rougeux, C..

6 recordsLinked to original sources

Evidence for epigenetically influenced mutagenesis and genetic assimilation in nascent species complexes (Coregonus sp.)

Phenotypic diversification is classically associated with genetic differentiation and gene expression variation. However, increasing evidence suggests that DNA methylation is involved in evolutionary processes due to its phenotypic and transcriptional effects. Methylation can increase mutagenesis and could lead to increased genetic divergence between populations experiencing different environmental conditions for many generations, though there has been minimal empirical research on epigenetically induced mutagenesis in diversification and speciation. Whitefish, freshwater members of the salmonid family, are excellent systems to study phenotypic diversification and speciation due to the repeated divergence of benthic-limnetic species pairs serving as natural replicates. Here we investigate whole genome genetic and epigenetic differentiation between sympatric benthic-limnetic species pairs in lake and European whitefish (Coregonus clupeaformis and C. lavaretus) from four lakes (N=64). We found considerable, albeit variable, genetic and epigenetic differences between species pairs. All SNP types were enriched at CpG sites supporting the mutagenic nature of DNA methylation, though C>T SNPs were most common. We also found an enrichment of overlaps between outlier SNPs with the 5% highest FST between species and differentially methylated loci. This could possibly represent differentially methylated sites that have caused divergent genetic mutations between species, or divergent selection leading to both genetic and epigenetic variation at these sites. Our results support the hypothesis that DNA methylation contributes to phenotypic divergence and mutagenesis during whitefish speciation. Significance statementDNA methylation is an epigenetic mark known to change in response to the environment and induce genetic modifications such as point mutations, though its implications for evolution and speciation have not been thoroughly studied. We find considerable but variable genetic and epigenetic variation between whitefish benthic-limnetic species pairs, highlighting the potential for DNA methylation to contribute to mutagenesis and genetic evolution. Our study provides evidence that DNA methylation could have contributed to whitefish speciation, both through initially plastic methylation changes and by driving genetic divergence between species pairs.

evolutionary biology↗

Genome assembly, structural variants, and genetic differentiation between Lake Whitefish young species pairs (Coregonus sp.) with long and short reads

Nascent pairs of ecologically differentiated species offer an opportunity to get a better glimpse at the genetic architecture of speciation. Of particular interest is our recent ability to consider a wider range of genomic variants, not only single-nucleotide polymorphisms (SNPs), thanks to long-read sequencing technology. We can now identify structural variants (SVs) like insertions, deletions, and other rearrangements, allowing further insights into the genetic architecture of speciation and how different types of variants are involved in species differentiation. Here, we investigated genomic patterns of differentiation between sympatric species pairs (Dwarf and Normal) belonging to the Lake Whitefish (Coregonus clupeaformis) species complex. We assembled the first reference genomes for both C. clupeaformis sp. Normal and C. clupeaformis sp. Dwarf, annotated the transposable elements, and analysed the genomes in the light of related coregonid species. Next, we used a combination of long-read and short-read sequencing to characterize SVs and genotype them at population-scale using genome-graph approaches, showing that SVs cover five times more of the genome than SNPs. We then integrated both SNPs and SVs to investigate the genetic architecture of species differentiation in two different lakes and highlighted an excess of shared outliers of differentiation. In particular, a large fraction of SVs differentiating the two species correspond to insertions or deletions of transposable elements (TEs), suggesting that TE accumulation may represent a key component of genetic divergence between the Dwarf and Normal species. Altogether, our results suggest that SVs may play an important role in speciation and that, by combining second and third generation sequencing, we now have the ability to integrate SVs into speciation genomics.

evolutionary biology↗

Genome-wide DNA methylation predicts environmentally-driven life history variation in a marine fish

The molecular mechanisms underlying intraspecific variation in life history strategies are still poorly understood, despite the importance of this question for understanding of organisms responses to environmental variability. Theoretical work proposed that epigenetic mechanisms such as DNA methylation might regulate intraspecific variation in life history strategies, however this assumption has rarely been verified empirically in wild populations. We examined associations between genome-wide methylation changes and environmentally-driven life history variation in two lineages of a marine fish that diverged approximatively 2.5 Mya, the capelin (Mallotus villosus), from North America and Europe. In both lineages, capelin harbour two contrasted life history strategies: some are strictly semelparous, experience fast actuarial senescence, but benefit from high hatching success by spawning on demersal sites where water temperature is low and relatively stable. In contrast, others are facultative iteroparous, have slower actuarial senescence, and suffer from lower hatching success by breeding in the intertidal zone where temperature is warmer, thermohaline parameters are less stable, and egg desiccation risk is high. Performing whole genome and epigenome sequencing, we showed that these contrasted life history strategies are more likely governed by epigenetic changes than by differences in DNA sequence. While genetic differentiation between the capelin harbouring different life history strategies was negligible, we detected parallel genome-wide methylation changes across lineages. We identified 1,067 differentially methylated regions (DMRs) comprising 15,818 CpGs, with 22% of them located within 5-kb around genes comprising promotor regions. We found that all DMRs were hypermethylated in demersal-spawning individuals. This striking result suggests that lower water temperature at demersal sites leads to an overall hypermethylation of the genome determined during the epigenetic reprogramming occurring over embryonic development. Our study emphasizes that parallel epigenetics changes in lineages with divergent genetic background could have a functional role in the regulation of intraspecific life history variation.

evolutionary biology↗

The role of genomic vs. epigenomic variation in shaping patterns of convergent transcriptomic variation across continents in a young species complex

Repeated adaptive divergence in replicates of phenotypic diversification offers a propitious context to identify the molecular bases associated to adaptive divergence. A currently hotly debated topic pertains to the relative role of genomic vs. epigenomic variation in shaping patterns of phenotypic variation at the gene expression level. Here, we combined genomic, epigenomic and transcriptomic information from 64 individuals in order to quantify the relative role of SNPs and DNA methylation variation in the repeated evolution of four limnetic-benthic whitefish species pairs from Europe and North America. We first found evidence for 149 convergent differentially methylated regions (DMRs) between species across continents, which significantly influenced levels of gene expression. Hyper-methylated DMRs in the limnetic species were globally associated to an expression repression relatively to benthic species, and inversely. Furthermore, we identified 108 convergent genetic variants (eQTLs) associated to gene expression differences between species. Gene expression differences were more pronounced in genes harbouring eQTL compared to those associated with DMRs, thus revealing a greater effect of eQTLs on gene expression. Multivariate analyses allowed partitioning the relative contribution of epi-/genomic changes and their association to gene expression variation. Most of the gene expression variation was significantly explained by genomic (4.1%) and putatively genomic-epigenomic interactive variation (46.7%), while \"pure\" epigenomic variation explained marginally 2.3% of the gene expression variation across continents. This study provides a rare qualitative and quantitative documentation of the relative role of genomic, DNA methylation and their interaction in shaping patterns of convergent gene expression during the process of ecological speciation.

evolutionary biology↗

Convergent transcriptomic landscapes under polygenic selection accompany inter-continental parallel evolution within a Nearctic Coregonus (Salmonidae) sister-species complex.

In contrast to the plethora of studies focusing on the genomic basis of adaptive phenotypic divergence, the role of gene expression during speciation has been much less investigated and consequently, less understood. Yet, the convergence of differential gene expression patterns between closely related species-pairs might reflect the role of natural selection during the process of ecological speciation. Here, we test for intercontinental convergence in differential transcriptional signatures between limnetic and benthic sympatric species-pairs of Lake Whitefish (Coregonus clupeaformis) and its sister-lineage, the European Whitefish (C. lavaretus), using six replicated sympatric species-pairs (two in North America, two in Norway and two in Switzerland). We characterized both sequence variation in transcribed regions and differential gene expression between sympatric limnetic and benthic species across regions and continents. Our first finding was that differentially expressed genes (DEG) between limnetic and benthic whitefish tend to be enriched in shared polymorphism among sister-lineages. We then used both genotypes and co-variation in expression in order to infer polygenic selection at the gene level. We identified parallel outliers and DEG involving genes primarily over-expressed in limnetic species relative to the benthic species. Our analysis finally revealed the existence of shared genomic bases underlying parallel differential expression across replicated species pairs from both continents, such as a cis-eQTL affecting the pyruvate kinase expression level involved in glycolysis. Our results are consistent with a longstanding role of natural selection in maintaining transcontinental diversity at phenotypic traits involved in ecological speciation between limnetic and benthic whitefishes.

evolutionary biology↗

Sex matters in Massive Parallel Sequencing: Evidence for biases in genetic parameter estimation and investigation of sex determination systems

Using massively parallel sequencing data from two species with different life history traits -- American lobster (Homarus americanus) and Arctic Char (Salvelinus alpinus) -- we highlighted how an unbalanced sex ratio in the samples combined with a few sex-linked markers may lead to false interpretations of population structure and thus to potentially erroneous management recommendations. Multivariate analyses revealed two genetic clusters that separated males and females instead of showing the expected pattern of genetic differentiation among ecologically divergent (inshore vs. offshore in lobster) or geographically distant (east vs. west in Arctic Char) sampling locations. We created several subsamples artificially varying the sex ratio in the inshore/offshore and east/west groups, and then demonstrated that significant genetic differentiation could be observed despite panmixia for lobster, and that Fst values were overestimated for Arctic Char. This pattern was due to 12 and 94 sex-linked markers driving differentiation for lobster and Arctic Char, respectively. Removing sex-linked markers led to nonsignificant genetic structure (lobster) and a more accurate estimation of Fst (Arctic Char). We further characterized the putative functions of sex-linked markers. Given that only 9.6% of all marine/diadromous population genomic studies to date reported sex information, we urge researchers to collect and consider individual sex information. In summary, we argue that sex information is useful to (i) control sex ratio in sampling, (ii) overcome \"sex-ratio bias\" that can lead to spurious genetic differentiation signals and (iii) fill knowledge gaps regarding sex determining systems.

genomics↗