Ocean acidification influences hostDNAmethylation and phenotypic plasticity in environmentally susceptible corals

Abstract

As climate change challenges organismal fitness by creating a phenotype–environment mismatch, phenotypic plasticity generated by epigenetic mechanisms (e.g., DNA methylation) can provide a temporal buffer for genetic adaptation. Epigenetic mechanisms may be crucial for sessile benthic marine organisms, such as reef‐building corals, where ocean acidification (OA) and warming reflect in strong negative responses. We tested the potential for scleractinian corals to exhibit phenotypic plasticity associated with a change in DNA methylation in response to OA. Clonal coral fragments of the environmentally sensitive Pocillopora damicornis and more environmentally robust Montipora capitata were exposed to fluctuating ambient pH (7.9–7.65) and low pH (7.6–7.35) conditions in common garden tanks for ~6 weeks. M. capitata responded weakly, or acclimated more quickly, to OA, with no difference in calcification, minimal separation of metabolomic profiles, and no change in DNA methylation between treatments. Conversely, P. damicornis exhibited diminished calcification at low pH, stronger separation in metabolomic profiles, and responsiveness of DNA methylation to treatment. Our data suggest corals differ in their temporal dynamics and sensitivity for environmentally triggered real‐time epigenetic reprogramming. The generation of potentially heritable plasticity via environmental induction of DNA methylation provides an avenue for assisted evolution applications in corals under rapid climate change.

Rapid adaptive responses to climate change in corals

“…2). Nevertheless, it remains to be seen whether this divergent methylation causes or is caused by differences in gene expression, whether it responds to environmental cues 14 , and whether it can be passed across generations. In summary, we do not dismiss a potential role for epigenetic inheritance in TGP of corals, but evidence is currently largely lacking, and mechanisms other than DNA methylation need increased attention.…”

“…Within a lifetime, some corals can modulate their gross colony growth form to optimize light environments for photosynthesizing endosymbionts 51 , physiologically acclimatize to elevated temperatures 22 , and show signs of acclimatization under pH stress 14,23 . These examples suggest that corals may retain phenotypic plasticity in their adult life stage, which can itself be a trait affected by the corals' environment 52 .…”

“…However, there are profound limitations to our current understanding of the underlying mechanisms of TGP and how these might interact with genetic adaptation 13 . While it has been suggested that epigenetic processes may be involved 14 , there are divergent opinions on the strength of evidence for transgenerational inheritance via epigenetic marks, even in some well-characterized model organisms 13,15 . Moreover, exact mechanisms and the extent to which they have an effect are still unclear and under discussion 15 .…”

Ecological Epigenetics in Marine Metazoans

“…Studies on plants have dominated the literature on ecological epigenetics (Schrey et al, 2013;Baulcombe and Dean, 2014;Verhoeven et al, 2016), especially in response to stress (Wang et al, 2011;Grativol et al, 2012;Al-Lawati et al, 2016). On the marine side, epigenetic and epigenomic approaches are being used to explore areas such as (1) sources of phenotypic plasticity, as created by differential gene expression (Dixon et al, 2014;Dimond and Roberts, 2016;Marsh et al, 2016), (2) mechanisms involved in development (Riviere et al, 2013), and (3) a possible rapid response to anthropogenic environmental change (Putnam et al, 2016). These studies are mechanistic, but importantly also bridge to understanding adaptive capacity of marine organisms in response to environmental change (Calosi et al, 2016).…”

“…These methods are exemplar of the tools that have become commercially available as the field of epigenetics expands in biomedical science and have already been used in studies of marine metazoans (Riviere et al, 2013;Putnam et al, 2016). The limitation here is that the data are only global levels with no information about changes in specific regions of the genome; however again, this is an affordable and approachable method to gain insight into changes in global patterns (e.g., tissue-wide, or as a function of developmental stage) of DNA methylation between discrete samples.…”