Intergenerational epigenetic inheritance in reef-building corals

Liew, Yi Jin; Howells, Emily J.; Wang, Xin; Michell, Craig; Burt, John A.; Idaghdour, Youssef; Aranda, Manuel

doi:10.1038/s41558-019-0687-2

Cited by 116 publications

(72 citation statements)

References 53 publications

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“…Recent studies on marine invertebrates [reviewed in Eirin-Lopez and Putnam (2019)] have shown that DNA methylation exerts a role on phenotypic acclimatization (Putnam et al, 2016;Liew et al, 2018;Durante et al, 2019) by modulating gene expression (Dixon et al, 2018). Moreover, epigenetic marks acquired throughout the lifespan of coral can be inherited intergenerationally, promoting acclimatized phenotypes in the offspring and thus increasing their fitness (Liew et al, 2020;Putnam et al, 2020). In addition, seasonal patterns of DNA methylation have been observed in vertebrates (Stevenson and Prendergast, 2013;Viitaniemi et al, 2019), invertebrates (Pegoraro et al, 2016;Suarez-Ulloa et al, 2019) and plants (Finnegan et al, 1998;Bastow et al, 2004;Ito et al, 2019).…”

Section: Temporal Differences Dominate Patterns Of Dna Methylationmentioning

confidence: 99%

Genome-Wide DNA Methylation Analysis Reveals a Conserved Epigenetic Response to Seasonal Environmental Variation in the Staghorn Coral Acropora cervicornis

et al. 2020

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Epigenetic modifications such as DNA methylation have been shown to participate in plastic responses to environmental change in a wide range of organisms, including scleractinian corals. Unfortunately, the current understanding of the links between environmental signals, epigenetic modifications, and the subsequent consequences for acclimatory phenotypic changes remain obscure. Such a knowledge gap extends also to the dynamic nature of epigenetic changes, hampering our ability to ascertain the magnitude and extent of these responses under natural conditions. The present work aims to shed light on these subjects by examining temporal changes in genomewide patterns of DNA methylation in the staghorn coral Acropora cervicornis in the island of Culebra, PR. During a 17-month period, a total of 162 polymorphic loci were identified using Methylation-Sensitive Amplified Polymorphism (MSAP). Among them, 83 of these restriction fragments displayed changes in DNA methylation that were significantly correlated to seasonal variation as determined mostly by changes in sea water temperature. Remarkably, the observed time-dependent variation in DNA methylation patterns is consistent across coral genets, coral source sites and sitespecific conditions studied. Overall, these results are consistent with a conserved epigenetic response to seasonal environmental variation. These findings highlight the importance of including seasonal variability into experimental designs investigating the role of epigenetic mechanisms such as DNA methylation in responses to stress.

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Section: Temporal Differences Dominate Patterns Of Dna Methylationmentioning

confidence: 99%

Genome-Wide DNA Methylation Analysis Reveals a Conserved Epigenetic Response to Seasonal Environmental Variation in the Staghorn Coral Acropora cervicornis

et al. 2020

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“…Epigenetic processes that regulate gene expression such as gene methylation are also a mechanism for transgenerational plasticity. While gene methylation has not been directly studied in the context of coral disease yet, studies looking at other stressors such as heat and nutrient addition do show methylation of immune-related adhesion and signaling genes in addition to housekeeping genes (Dimond and Roberts, 2016;Liew et al, 2020). It is important to note that these mechanisms will not benefit all coral species equally, and species that are relatively short-lived and brood their embryos may be better candidates for adaptation due to transgenerational plasticity that could lead to disease resistance, such as Porites astreoides (Pinzon et al, 2014;Fuess et al, 2017).…”

Section: Coral Immune Responses and Their Influences On Diseasementioning

confidence: 99%

Deciphering Coral Disease Dynamics: Integrating Host, Microbiome, and the Changing Environment

et al. 2020

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Diseases of tropical reef organisms is an intensive area of study, but despite significant advances in methodology and the global knowledge base, identifying the proximate causes of disease outbreaks remains difficult. The dynamics of infectious wildlife diseases are known to be influenced by shifting interactions among the host, pathogen, and other members of the microbiome, and a collective body of work clearly demonstrates that this is also the case for the main foundation species on reefs, corals. Yet, among wildlife, outbreaks of coral diseases stand out as being driven largely by a changing environment. These outbreaks contributed not only to significant losses of coral species but also to whole ecosystem regime shifts. Here we suggest that to better decipher the disease dynamics of corals, we must integrate more holistic and modern paradigms that consider multiple and variable interactions among the three major players in epizootics: the host, its associated microbiome, and the environment. In this perspective, we discuss how expanding the pathogen component of the classic host-pathogen-environment disease triad to incorporate shifts in the microbiome leading to dysbiosis provides a better model for understanding coral disease dynamics. We outline and discuss issues arising when evaluating each component of this trio and make suggestions for bridging gaps between them. We further suggest that to best tackle these challenges, researchers must adjust standard paradigms, like the classic one pathogen-one disease model, that, to date, have been ineffectual at uncovering many of the emergent properties of coral reef disease dynamics. Lastly, we make recommendations for ways forward in the fields of marine disease ecology and the future of coral reef conservation and restoration given these observations.

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“…To successfully conduct SB, adult colonies with relatively high heat tolerances need to be identified and used as broodstock. These colonies can come from different populations exposed to contrasting temperatures profiles at a range of spatial scales (Dixon et al, 2015; Liew et al, 2020; McClanahan et al, 2020), or among individuals from within a single population where there is sufficient intrapopulation variability. While it is well established that coral populations experiencing higher mean SSTs or more variable temperatures tend to be more tolerant to heat stress (Howells et al, 2012; Thomas et al, 2018), less is known about the extent of within-population variation in heat tolerance for corals (Bay and Palumbi, 2014; van Oppen et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

“…Competent coral larvae have been seeded en masse onto natural substrates to enhance recruitment (dela Cruz and Harrison, 2017; Doropoulos et al, 2019) and substrates have been designed to settle coral larvae for nursery rearing and outplantation improving early survivorship (Guest et al, 2014; Chamberland et al, 2017). Despite advances in the practice of CLP, most research has focused on the steps during and post-spawning, with little attention given to the provenance or phenotype of the broodstock colonies (apart from laboratory based studies e.g., Dixon et al, 2015; Liew et al, 2020; Quigley et al, 2020). To the best of our knowledge, there have been no attempts to select parents for adaptive traits, such as heat tolerance, as part of CLP for reef rehabilitation.…”

Section: Introductionmentioning

confidence: 99%

A framework for selectively breeding corals for assisted evolution

Humanes

Bythell

Beauchamp

et al. 2021

Preprint

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Coral cover on tropical reefs has declined during the last three decades due to the combined effects of climate change, destructive fishing, pollution, and land use change. Drastic reductions in greenhouse gas emissions combined with effective coastal management and conservation strategies are essential to slow this decline. Innovative approaches, such as selective breeding for adaptive traits combined with large-scale sexual propagation, are being developed with the aim of pre-adapting reefs to increased ocean warming. However, there are still major gaps in our understanding of the technical and methodological constraints to producing corals for such restoration interventions. Here we propose a framework for selectively breeding corals and rearing them from eggs to 2.5-year old colonies using the coral Acropora digitifera as a model species. We present methods for choosing colonies for selective crossing, enhancing early survivorship in ex situ and in situ nurseries, and outplanting and monitoring colonies on natal reefs. We used a short-term (7-day) temperature stress assay to select parental colonies based on heat tolerance of excised branches. From six parental colonies, we produced 12 distinct crosses, and compared survivorship and growth of colonies transferred to in situ nurseries or outplanted to the reef at different ages. We demonstrate that selectively breeding and rearing coral colonies is technically feasible at small scales and could be upscaled as part of restorative assisted evolution initiatives. Nonetheless, there are still challenges to overcome before selective breeding can be implemented as a viable conservation tool, especially at the post-settlement and outplanting phases. Although interdisciplinary approaches will be needed to overcome many of the challenges identified in this study, selective breeding has the potential to be a viable tool within reef managers toolbox to support the persistence of selected reefs in the face of climate change.

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Intergenerational epigenetic inheritance in reef-building corals

Cited by 116 publications

References 53 publications

Genome-Wide DNA Methylation Analysis Reveals a Conserved Epigenetic Response to Seasonal Environmental Variation in the Staghorn Coral Acropora cervicornis

Genome-Wide DNA Methylation Analysis Reveals a Conserved Epigenetic Response to Seasonal Environmental Variation in the Staghorn Coral Acropora cervicornis

Deciphering Coral Disease Dynamics: Integrating Host, Microbiome, and the Changing Environment

A framework for selectively breeding corals for assisted evolution

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