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For sessile organisms at high risk from climate change, phenotypic plasticity can be critical to rapid acclimation. Epigenetic markers like DNA methylation are hypothesized as mediators of plasticity; methylation is associated with the regulation of gene expression, can change in response to ecological cues, and is a proposed basis for the inheritance of acquired traits. Within reef-building corals, gene-body methylation (gbM) can change in response to ecological stressors. If coral DNA methylation is transmissible across generations, this could potentially facilitate rapid acclimation to environmental change. We investigated methylation heritability in Acropora, a stony reef-building coral. Two Acropora millepora and two Acropora selago adults were crossed, producing eight offspring crosses (four hybrid, two of each species). We used whole-genome bisulfite sequencing to identify methylated loci and allele-specific alignments to quantify per-locus inheritance. If methylation is heritable, differential methylation (DM) between the parents should equal DM between paired offspring alleles at a given locus. We found a mixture of heritable and nonheritable loci, with heritable portions ranging from 44% to 90% among crosses. gBM was more heritable than intergenic methylation, and most loci had a consistent degree of heritability between crosses (i.e. the deviation between parental and offspring DM were of similar magnitude and direction). Our results provide evidence that coral methylation can be inherited but that heritability is heterogenous throughout the genome. Future investigations into this heterogeneity and its phenotypic implications will be important to understanding the potential capability of intergenerational environmental acclimation in reef building corals.

 

Abstract Background As human activity alters the planet, there is a pressing need to understand how organisms adapt to environmental change. Of growing interest in this area is the role of epigenetic modifications, such as DNA methylation, in tailoring gene expression to fit novel conditions. Here, we reanalyzed nine invertebrate (Anthozoa and Hexapoda) datasets to validate a key prediction of this hypothesis: changes in DNA methylation in response to some condition correlate with changes in gene expression. Results In accord with previous observations, baseline levels of gene body methylation (GBM) positively correlated with transcription, and negatively correlated with transcriptional variation between conditions. Correlations between changes in GBM and transcription, however, were negligible. There was also no consistent negative correlation between methylation and transcription at the level of gene body methylation class (either highly- or lowly-methylated), anticipated under the previously described “seesaw hypothesis”. Conclusion Our results do not support the direct involvement of GBM in regulating dynamic transcriptional responses in invertebrates. If changes in DNA methylation regulate invertebrate transcription, the mechanism must involve additional factors or regulatory influences. 

Interrogation of chromatin modifications, such as DNA methylation, has the potential to improve forecasting and conservation of marine ecosystems. The standard method for assaying DNA methylation (whole genome bisulphite sequencing), however, is currently too costly to apply at the scales required for ecological research. Here, we evaluate different methods for measuring DNA methylation for ecological epigenetics. We compare whole genome bisulphite sequencing (WGBS) with methylated CpG binding domain sequencing (MBD‐seq), and a modified version of MethylRAD we term methylation‐dependent restriction site‐associated DNA sequencing (mdRAD). We evaluate these three assays in measuring variation in methylation across the genome, between genotypes, and between polyp types in the reef‐building coralAcropora millepora. We find that all three assays measure absolute methylation levels similarly for gene bodies (gbM), as well as exons and 1 Kb windows with a minimum Pearson correlation 0.66. Differential gbM estimates were less correlated, but still concurrent across assays. We conclude that MBD‐seq and mdRAD are reliable and cost‐effective alternatives to WGBS. The considerably lower sequencing effort required for mdRAD to produce comparable methylation estimates makes it particularly useful for ecological epigenetics.

 

Restriction‐site‐associated DNA sequencing (RADseq) has become an accessible way to obtain genome‐wide data in the form of single‐nucleotide polymorphisms (SNPs) for phylogenetic inference. Nonetheless, how differences in RADseq methods influence phylogenetic estimation is poorly understood because most comparisons have largely relied on conceptual predictions rather than empirical tests. We examine how differences in ddRAD and 2bRAD data influence phylogenetic estimation in two non‐model frog groups. We compare the impact of method choice on phylogenetic information, missing data, and allelic dropout, considering different sequencing depths. Given that researchers must balance input (funding, time) with output (amount and quality of data), we also provide comparisons of laboratory effort, computational time, monetary costs, and the repeatability of library preparation and sequencing. Both 2bRAD and ddRAD methods estimated well‐supported trees, even at low sequencing depths, and had comparable amounts of missing data, patterns of allelic dropout, and phylogenetic signal. Compared to ddRAD, 2bRAD produced more repeatable datasets, had simpler laboratory protocols, and had an overall faster bioinformatics assembly. However, many fewer parsimony‐informative sites per SNP were obtained from 2bRAD data when using native pipelines, highlighting a need for further investigation into the effects of each pipeline on resulting datasets. Our study underscores the importance of comparing RADseq methods, such as expected results and theoretical performance using empirical datasets, before undertaking costly experiments.

 

Although reef-building corals are declining worldwide, responses to bleaching vary within and across species and are partly heritable. Toward predicting bleaching response from genomic data, we generated a chromosome-scale genome assembly for the coral Acropora millepora We obtained whole-genome sequences for 237 phenotyped samples collected at 12 reefs along the Great Barrier Reef, among which we inferred little population structure. Scanning the genome for evidence of local adaptation, we detected signatures of long-term balancing selection in the heat-shock co-chaperone sacsin We conducted a genome-wide association study of visual bleaching score for 213 samples, incorporating the polygenic score derived from it into a predictive model for bleaching in the wild. These results set the stage for genomics-based approaches in conservation strategies. 

As climate change progresses, reef‐building corals must contend more often with suboptimal conditions, motivating a need to understand coral stress response. Here, we test the hypothesis that there is a stereotyped transcriptional response that corals enact under all stressful conditions, functionally characterized by downregulation of growth, and activation of cell death, response to reactive oxygen species, immunity, and protein folding and degradation. We analyse RNA‐seq and Tag‐Seq data from 14 previously published studies and supplement them with four new experiments involving different stressors, totaling over 600 gene expression profiles from the genusAcropora. Contrary to expectations, we found not one, but two distinct types of response. The type A response was observed under all kinds of high‐intensity stress, was correlated between independent projects and was functionally consistent with the hypothesized stereotyped response. The consistent correlation between projects, irrespective of stress type, supports the type A response as the general coral environmental stress response (ESR), a blanket solution to severely stressful conditions. The distinct type B response was observed under lower intensity stress and was more variable among studies. Unexpectedly, at the level of individual genes and functional categories, the type B response was broadly opposite the type A response. Finally, taking advantage of the breadth of the data set, we present contextual annotations for previously unannotated genes based on consistent stress‐induced differences across independent projects.

 

Gene body methylation (GBM) has been hypothesized to modulate responses to environmental change, including transgenerational plasticity, but the evidence thus far has been lacking. Here we show that coral fragments reciprocally transplanted between two distant reefs respond predominantly by increase or decrease in genome-wide GBM disparity: The range of methylation levels between lowly and highly methylated genes becomes either wider or narrower. Remarkably, at a broad functional level this simple adjustment correlated very well with gene expression change, reflecting a shifting balance between expressions of environmentally responsive and housekeeping genes. In our experiment, corals in a lower-quality habitat up-regulated genes involved in environmental responses, while corals in a higher-quality habitat invested more in housekeeping genes. Transplanted fragments showing closer GBM match to local corals attained higher fitness characteristics, which supports GBM’s role in acclimatization. Fixed differences in GBM between populations did not align with plastic GBM changes and were mostly observed in genes with elevatedF_ST, which suggests that they arose predominantly through genetic divergence. However, we cannot completely rule out transgenerational inheritance of acquired GBM states.