Intergenerational epigenetic inheritance in reef-building corals

Abstract

The perception that the inheritance of phenotypic traits operates solely through genetic means is slowly being eroded: epigenetic mechanisms have been shown to induce heritable changes in gene activity in plants1,2 and metazoans1,3. Inheritance of DNA methylation patterns provides a potential pathway for environmentally induced phenotypes to contribute to evolution of species and populations1,2,3,4,5. However, in basal metazoans, it is unknown whether inheritance of CpG methylation patterns occurs across the genome (as in plants) or as rare exceptions (as in mammals)4. Here, we show that DNA methylation patterns in a reef-building coral are determined by genotype and developmental stage, as well as by parental environment. Transmission of CpG methylation from adults to their sperm and larvae demonstrates genome-wide inheritance. Variation in the hypermethylation of genes in adults and their sperm from distinct environments suggests intergenerational acclimatization to local temperature and salinity. Furthermore, genotype-independent adjustments of methylation levels in stress-related genes were strongly correlated with offspring survival rates under heat stress. These findings support a role of DNA methylation in the intergenerational inheritance of traits in corals, which could extend to enhancing their capacity to adapt to climate change.

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Fig. 1: Data acquisition and summarized findings showing intergenerational inheritance of DNA methylation patterns in P. daedalea.
Fig. 2: Environmental origin changes in epigenotype are mostly independent of genotype in P. daedalea.
Fig. 3: DNA methylation profiles are associated with environmental origin in P. daedalea.
Fig. 4: DNA methylation profiles vary considerably across developmental stages in P. daedalea.

Data availability

Whole-genome bisulfite sequencing data can be found in NCBI BioProject PRJNA430328. Individual SRA accessions are listed in Supplementary Dataset 1c. Genomic sequences and annotations are available at http://pdae.reefgenomics.org/ (ref. 55).

Code availability

Scripts used to analyse methylation data (and the underlying theoretical justifications) are detailed at https://github.com/lyijin/working_with_dna_meth. Other analytical and plotting scripts, key intermediate files and further explanatory notes are available at https://doi.org/10.5281/zenodo.3558476 (v.1.0.0).

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Acknowledgements

We thank D. Abrego, G. Vaughan and D. McParland for assistance with fieldwork, coral spawning and the collection of environmental data. We thank the NYUAD Core Research Vessel and The Palms Dive Center for fieldwork support. We thank the Environment Agency Abu Dhabi and Fujairah Municipality for research permits and the KAUST Sequencing Core Facility for the sequencing of the libraries. The research reported in this publication was supported by the KAUST OSR under grant no. URF/1/3447-01-01, as well as baseline support to M.A.; and by NYUAD research grant no. AD105 to Y.I.

Author information

E.J.H, Y.I. and M.A. conceived and coordinated the project. M.A., X.W. and J.A.B provided resources. E.J.H. collected samples from the wild, performed controlled crosses and extracted DNA from fixed samples. C.T.M. constructed libraries for WGBS and RNA-seq. Y.J.L., Y.I. and M.A. analysed data. Y.J.L., E.J.H. and M.A. wrote the manuscript. All authors read and approved the manuscript.

Correspondence to Manuel Aranda.

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The authors declare no competing interests.

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Peer review information Nature Climate Change thanks Eva Majerová and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Methylation in P. daedalea is more commonly found in genic regions, and concentrated closer to the 5’ and 3’ ends.

(a) Genic regions are significantly more frequently methylated than intergenic regions (3.9% versus 3.0%; Fisher’s exact P < 10-300). (b) Methylation levels are bimodally distributed in exons, introns and intergenic regions. Exons have the highest methylation levels, followed by introns and intergenic regions. (c) Relative frequencies of methylated positions across a standardized gene model with flanking 4 kb regions indicate that methylated positions are more frequently found at both ends of the gene model. Solid lines depict transcriptional start site (left) and transcription termination site (right) while dotted lines delineate the borders of the indicated genomic feature. The widths of the features correspond to mean normalized lengths of the respective exons and introns in P. daedalea (exons, from left to right: 286 bp, 320 bp, 225 bp, 203 bp, 270 bp, 380 bp; introns, from left to right: 1,971 bp, 1,744 bp, 1,598 bp, 1,728 bp).

Extended Data Fig. 2 Per-origin principal components analysis of DNA methylation patterns in P. daedalea.

Plots show variation explained by the first three principal components of PCAs carried out separately on samples from Fujairah (top row) and Abu Dhabi samples (bottom row). Samples from adults (squares) and sperm (circles) tend to pair by colony identity. Samples from reciprocal larval crosses E7 x S8 and E8 x S7 (red triangles) are positioned midway between S7 and S8 along all plotted axes, suggesting equal contribution from both parents to their DNA methylation patterns. The sole egg sample, E8, is located close to S8 and A8, indicating that the transmission of epigenetic patterns from parent to either gamete type is unbiased.

Extended Data Fig. 3 Methylation trends against FST are origin-agnostic.

Genes were split into two groups, corresponding to genes with higher methylation in Abu Dhabi relative to Fujairah (red), and vice versa (blue). When correlated against genetic factors, both groups showed trends similar to Fig. 2, where methylation differences were calculated as absolute differences.

Extended Data Fig. 4 Outline of statistical tests performed.

Numbers denote biological replicates of different developmental stages and sample origins, while boxes denote the groupings used in the statistical tests. The initial GLM (green) tested whether both variables had significant interaction. Subsequently, the pair of t-tests (blue) identified genes that were differentially methylated across developmental stages, while the t-test (red) identified genes that were differentially methylated across sample origins.

Supplementary information

Supplementary Information

Supplementary Tables 1 and 2.

Reporting Summary

Supplementary Dataset

Supplementary Data 1–8.

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Liew, Y.J., Howells, E.J., Wang, X. et al. Intergenerational epigenetic inheritance in reef-building corals. Nat. Clim. Chang. (2020). https://doi.org/10.1038/s41558-019-0687-2

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