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Two different epigenetic information channels in wild three-spined sticklebacks are involved in salinity adaptation.

ABSTRACT: Epigenetic inheritance has been proposed to contribute to adaptation and acclimation via two information channels: (i) inducible epigenetic marks that enable transgenerational plasticity and (ii) noninducible epigenetic marks resulting from random epimutations shaped by selection. We studied both postulated channels by sequencing methylomes and genomes of Baltic three-spined sticklebacks (Gasterosteus aculeatus) along a salinity cline. Wild populations differing in salinity tolerance revealed differential methylation (pop-DMS) at genes enriched for osmoregulatory processes. A two-generation experiment demonstrated that 62% of these pop-DMS were noninducible by salinity manipulation, suggesting that they are the result of either direct selection or associated genomic divergence at cis- or trans-regulatory sites. Two-thirds of the remaining inducible pop-DMS increased in similarity to patterns detected in wild populations from corresponding salinities. The level of similarity accentuated over consecutive generations, indicating a mechanism of transgenerational plasticity. While we can attribute natural DNA methylation patterns to the two information channels, their interplay with genomic variation in salinity adaptation is still unresolved.

SUBMITTER: Heckwolf MJ

PROVIDER: S-EPMC7083608 | biostudies-literature | 2020 Mar

REPOSITORIES: biostudies-literature

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Two different epigenetic information channels in wild three-spined sticklebacks are involved in salinity adaptation.

Heckwolf Melanie J MJ Meyer Britta S BS Häsler Robert R Höppner Marc P MP Eizaguirre Christophe C Reusch Thorsten B H TBH

Science advances 20200320 12

Epigenetic inheritance has been proposed to contribute to adaptation and acclimation via two information channels: (i) inducible epigenetic marks that enable transgenerational plasticity and (ii) noninducible epigenetic marks resulting from random epimutations shaped by selection. We studied both postulated channels by sequencing methylomes and genomes of Baltic three-spined sticklebacks (<i>Gasterosteus aculeatus</i>) along a salinity cline. Wild populations differing in salinity tolerance reve ...[more]

PMID: 32219167

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Project description:BACKGROUND: Comparative genomics approaches help to shed light on evolutionary processes that shape differentiation between lineages. The nine-spined stickleback (Pungitius pungitius) is a closely related species of the ecological 'supermodel' three-spined stickleback (Gasterosteus aculeatus). It is an emerging model system for evolutionary biology research but has garnered less attention and lacks extensive genomic resources. To expand on these resources and aid the study of sticklebacks in a phylogenetic framework, we characterized nine-spined stickleback transcriptomes from brain and liver using deep sequencing. RESULTS: We obtained nearly eight thousand assembled transcripts, of which 3,091 were assigned as putative one-to-one orthologs to genes found in the three-spined stickleback. These sequences were used for evaluating overall differentiation and substitution rates between nine- and three-spined sticklebacks, and to identify genes that are putatively evolving under positive selection. The synonymous substitution rate was estimated to be 7.1 × 10(-9) per site per year between the two species, and a total of 165 genes showed patterns of adaptive evolution in one or both species. A few nine-spined stickleback contigs lacked an obvious ortholog in three-spined sticklebacks but were found to match genes in other fish species, suggesting several gene losses within 13 million years since the divergence of the two stickleback species. We identified 47 SNPs in 25 different genes that differentiate pond and marine ecotypes. We also identified 468 microsatellites that could be further developed as genetic markers in nine-spined sticklebacks. CONCLUSION: With deep sequencing of nine-spined stickleback cDNA libraries, our study provides a significant increase in the number of gene sequences and microsatellite markers for this species, and identifies a number of genes showing patterns of adaptive evolution between nine- and three-spined sticklebacks. We also report several candidate genes that might be involved in differential adaptation between marine and freshwater nine-spined sticklebacks. This study provides a valuable resource for future studies aiming to identify candidate genes underlying ecological adaptation in this and other stickleback species.

Project description:BackgroundMost evolutionary studies on the size of brains and different parts of the brain have relied on interspecific comparisons, and have uncovered correlations between brain architecture and various ecological, behavioural and life-history traits. Yet, similar intraspecific studies are rare, despite the fact that they could better determine how selection and phenotypic plasticity influence brain architecture. We investigated the variation in brain size and structure in wild-caught nine-spined sticklebacks (Pungitius pungitius) from eight populations, representing marine, lake, and pond habitats, and compared them to data from a previous common garden study from a smaller number of populations.ResultsBrain size scaled hypo-allometrically with body size, irrespective of population origin, with a common slope of 0.5. Both absolute and relative brain size, as well as relative telencephalon, optic tectum and cerebellum size, differed significantly among the populations. Further, absolute and relative brain sizes were larger in pond than in marine populations, while the telencephalon tended to be larger in marine than in pond populations. These findings are partly incongruent with previous common garden results. A direct comparison between wild and common garden fish from the same populations revealed a habitat-specific effect: pond fish had relatively smaller brains in a controlled environment than in the wild, while marine fish were similar. All brain parts were smaller in the laboratory than in the wild, irrespective of population origin.ConclusionOur results indicate that variation among populations is large, both in terms of brain size and in the size of separate brain parts in wild nine-spined sticklebacks. However, the incongruence between the wild and common garden patterns suggests that much of the population variation found in the wild may be attributable to environmentally induced phenotypic plasticity. Given that the brain is among the most plastic organs in general, the results emphasize the view that common garden data are required to draw firm evolutionary conclusions from patterns of brain size variability in the wild.

Dataset Information

Two different epigenetic information channels in wild three-spined sticklebacks are involved in salinity adaptation.

Publications

Two different epigenetic information channels in wild three-spined sticklebacks are involved in salinity adaptation.

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