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Epigenetic adaptation of stickleback to sea and freshwater conditions: RNA-seq

ABSTRACT: Three-spined stickleback (Gasterosteus aculeatus) represents a convenient model to study microevolution - adaptation to freshwater environment. While genetic adaptations to freshwater are well-studied, epigenetic adaptations attracted little attention. In this work, we investigated the role of DNA methylation in the adaptation of marine stickleback population to freshwater conditions. DNA methylation profiling was performed in marine and freshwater populations of sticklebacks, as well as in marine sticklebacks placed into freshwater environment and freshwater sticklebacks placed into seawater. For the first time, we demonstrated that genes encoding ion channels kcnd3, cacna1fb, gja3 are differentially methylated between marine and freshwater populations. We also showed that after placing marine stickleback into fresh water, its DNA methylation profile partially converges to the one of a freshwater stickleback. This suggests that immediate epigenetic response to freshwater conditions can be maintained in freshwater population. Interestingly, we observed enhanced epigenetic plasticity in freshwater sticklebacks that may serve as a compensatory regulatory mechanism for the lack of genetic variation in the freshwater population. Some of the regions that were reported previously to be under selection in freshwater populations also show differential methylation. Thus, epigenetic changes might represent a parallel mechanism of adaptation along with genetic selection in freshwater environment. This is the RNA-seq experiment, DNA methylation data (bisulfite-seq) is provided under accession number GSE82310.

ORGANISM(S): Gasterosteus aculeatus

PROVIDER: GSE186925 | GEO | 2021/11/03

REPOSITORIES: GEO

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Genome-wide DNA methylation profiling reveals epigenetic adaptation of stickleback to sea and freshwater conditions

Project description:Three-spined stickleback (Gasterosteus aculeatus) represents a convenient model to study microevolution - adaptation to freshwater environment. While genetic adaptations to freshwater are well-studied, epigenetic adaptations attracted little attention. In this work, we investigated the role of DNA methylation in the adaptation of marine stickleback population to freshwater conditions. DNA methylation profiling was performed in marine and freshwater populations of sticklebacks, as well as in marine sticklebacks placed into freshwater environment and freshwater sticklebacks placed into seawater. For the first time, we demonstrated that genes encoding ion channels kcnd3, cacna1fb, gja3 are differentially methylated between marine and freshwater populations. We also showed that after placing marine stickleback into fresh water, its DNA methylation profile partially converges to the one of a freshwater stickleback. This suggests that immediate epigenetic response to freshwater conditions can be maintained in freshwater population. Interestingly, we observed enhanced epigenetic plasticity in freshwater sticklebacks that may serve as a compensatory regulatory mechanism for the lack of genetic variation in the freshwater population. Some of the regions that were reported previously to be under selection in freshwater populations also show differential methylation. Thus, epigenetic changes might represent a parallel mechanism of adaptation along with genetic selection in freshwater environment.

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Proteomics support the threespine stickleback egg coat as a protective oocyte envelope

Project description:After the end of the last ice age, ancestrally marine threespine stickleback fish (Gasterosteus aculeatus) have undergone an adaptive radiation into freshwater environments throughout the Northern Hemisphere, creating an excellent model system for studying molecular adaptation and speciation. Stickleback populations are reproductively isolated to varying degrees, despite the fact that they can be crossed in the lab to produce viable offspring. Ecological and behavioral factors have been suggested to underlie incipient stickleback speciation. However, reproductive proteins represent a previously unexplored driver of speciation. As mediators of gamete recognition during fertilization, reproductive proteins both create and maintain species boundaries. Gamete recognition proteins are also frequently found to be rapidly evolving, and their divergence may culminate in reproductive isolation and ultimately speciation. As an initial investigation into the contribution of reproductive proteins to stickleback reproductive isolation, we characterized the egg coat proteome of threespine stickleback eggs. In agreement with other teleosts, we find that stickleback egg coats are comprised of homologs to the zona pellucida (ZP) proteins ZP1 and ZP3. We explore aspects of stickleback ZP protein biology, including glycosylation, disulfide bonding, and sites of synthesis, and find many substantial differences compared to their mammalian homologs. Furthermore, molecular evolutionary analyses indicate that ZP3, but not ZP1, has experienced positive Darwinian selection across teleost fish. Taken together, these changes to stickleback ZP protein architecture suggest that the egg coats of stickleback fish, and perhaps fish more generally, have evolved to fulfill a more protective functional role than their mammalian counterparts.

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Marine and freshwater three-spined stickleback (Gasterosteus aculeatus) gene expression differences

Project description:In order to identify gene expression difference between marine and freshwater stickleback populations, we compared the transcriptomes of seven adult tissues (eye, gill, heart, hypothalumus, liver, pectoral muscle, telencephalon) between a marine population sampled from the mouth of the Little Campbell river in British Columbia (LITC) and a freshwater population (Fishtrap Creek, FTC) from northern Washington. For each population, the sampled individuals were the lab-reared progeny of a single pair of wild-caught parents. Four to five fish from each population were used as biological replicates for each of the seven tissues. For each population, the sampled individuals were the lab-reared progeny of a single pair of wild-caught parents. All fish were of similar age and were raised in the same aquarium (salinity: 3.5 ppt), with a plastic divider separating the marine and freshwater groups. One male and four females were sampled from each population. Microarray experiments were performed in a 2-color format on custom Agilent arrays: experimental RNA samples were labeled with Cy5, and the common reference RNA sample was labeled with Cy3. The reference RNA was total RNA isolated from a large number of 7-day-post-hatch embryos from the freshwater population of Bear Paw Lake, Alaska (BEPA). One technical replicate was used for each array, and one of the hypothalamus samples (Hyp_FTC#3) was excluded from further analysis due to poor quality indicators. FTC#1 liver and LITC#2 pectoral muscle samples did not yield RNA of sufficient quality for the microarray experiment, and were also excluded from hybridization.

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Gasterosteus aculeatus

Project description:Genome-wide DNA methylation profiling reveals epigenetic adaptation of stickleback to sea and freshwater conditions

| PRJNA324599 | ENA

Epigenetic adaptation of stickleback to sea and freshwater conditions: RNA-seq

Project description:Epigenetic adaptation of stickleback to sea and freshwater conditions: RNA-seq

| PRJNA776820 | ENA

Fine-scale contemporary recombination variation and its fitness consequences in adaptively diverging stickleback fish [ChIP-Seq]

Project description:Despite deep evolutionary conservation, recombination varies greatly across the genome, among individuals, sexes and populations and can be a major evolutionary force in the wild. Yet this variation in recombination and its impact on adaptively diverging populations is not well understood. To elucidate the nature and potential consequences of recombination rate variation, we characterized fine-scale recombination landscapes by combining pedigrees, functional genomics and field fitness measurements in an adaptively divergent pair of marine and freshwater threespine stickleback populations from River Tyne, Scotland. Through whole-genome sequencing of large nuclear families, we identified the genomic location of almost 50,000 crossovers and built recombination maps for 36 marine, freshwater, and hybrid individuals at 3.8 kilobase resolution. Using these maps, we quantified the factors driving variation in recombination rate: we find strong heterochiasmy between sexes (68% of the variation) but also differences among ecotypes (21.8%). Hybrids show evidence of significant recombination suppression, both in overall map length and in individual loci. We further tested and found reduced recombination rates both within single marine–freshwater adaptive loci and between loci on the same chromosome, suggestive of selection on linked ‘cassettes’. We tested theory supporting the evolution of linked selection using temporal sampling along a natural hybrid zone, and found that recombinants with shuffled alleles across loci show traits associated with reduced fitness. Our results support predictions that divergence in cis-acting recombination modifiers whose mechanisms are disrupted in hybrids, may have an important role to play in the maintenance of differences among adaptively diverging populations.

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