Phenotypic plasticity is defined as a property of individual genotypes to produce different phenotypes when exposed to different environmental conditions. This ability may be expressed at behavioral, biochemical, physiological, and/or developmental levels, exerting direct influence over species' demographic performance. In reef-building corals, a group critically threatened by global change in the Anthropocene, non-genetic mechanisms (i.e., epigenetic and microbiome variation) have been shown to participate in plastic physiological responses to environmental change. Yet, the precise way in which these mechanisms interact, contribute to such responses, and their adaptive potential is still obscure. The present work aims to fill this gap by using a multi-omics approach to elucidate the contribution and interconnection of the mechanisms modulating phenotypic plasticity in staghorn coral (Acropora cervicornis) clones subject to different depth conditions. Results show changes in lipidome, epigenome and transcriptome, but not in symbiotic and microbial communities. In addition, a potential shift toward a more heterotrophic feeding behavior was evidenced in corals at the deeper site. These observations are consistent with a multi-mechanism modulation of rapid acclimation in corals, underscoring the complexity of this process and the importance of a multifactorial approach to inform potential intervention to enhance coral adaptive capacity.
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Avenues of reef-building coral acclimatization in response to rapid environmental change
ABSTRACT The swiftly changing climate presents a challenge to organismal fitness by creating a mismatch between the current environment and phenotypes adapted to historic conditions. Acclimatory mechanisms may be especially crucial for sessile benthic marine taxa, such as reef-building corals, where climate change factors including ocean acidification and increasing temperature elicit strong negative physiological responses such as bleaching, disease and mortality. Here, within the context of multiple stressors threatening marine organisms, I describe the wealth of metaorganism response mechanisms to rapid ocean change and the ontogenetic shifts in organism interactions with the environment that can generate plasticity. I then highlight the need to consider the interactions of rapid and evolutionary responses in an adaptive (epi)genetic continuum. Building on the definitions of these mechanisms and continuum, I also present how the interplay of the microbiome, epigenetics and parental effects creates additional avenues for rapid acclimatization. To consider under what conditions epigenetic inheritance has a more substantial role, I propose investigation into the offset of timing of gametogenesis leading to different environmental integration times between eggs and sperm and the consequences of this for gamete epigenetic compatibility. Collectively, non-genetic, yet heritable phenotypic plasticity will have significant ecological and evolutionary implications for sessile marine organism persistence under rapid climate change. As such, reef-building corals present ideal and time-sensitive models for further development of our understanding of adaptive feedback loops in a multi-player (epi)genetic continuum.
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- Award ID(s):
- 1756623
- NSF-PAR ID:
- 10231213
- Date Published:
- Journal Name:
- Journal of Experimental Biology
- Volume:
- 224
- Issue:
- Suppl_1
- ISSN:
- 0022-0949
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract 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.
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ABSTRACT As climate change increases the rate of environmental change and the frequency and intensity of disturbance events, selective forces intensify. However, given the complicated interplay between plasticity and selection for ecological – and thus evolutionary – outcomes, understanding the proximate signals, molecular mechanisms and the role of environmental history becomes increasingly critical for eco-evolutionary forecasting. To enhance the accuracy of our forecasting, we must characterize environmental signals at a level of resolution that is relevant to the organism, such as the microhabitat it inhabits and its intracellular conditions, while also quantifying the biological responses to these signals in the appropriate cells and tissues. In this Commentary, we provide historical context to some of the long-standing challenges in global change biology that constrain our capacity for eco-evolutionary forecasting using reef-building corals as a focal model. We then describe examples of mismatches between the scales of external signals relative to the sensors and signal transduction cascades that initiate and maintain cellular responses. Studying cellular responses at this scale is crucial because these responses are the basis of acclimation to changing environmental conditions and the potential for environmental ‘memory’ of prior or historical conditions through molecular mechanisms. To challenge the field, we outline some unresolved questions and suggest approaches to align experimental work with an organism's perception of the environment; these aspects are discussed with respect to human interventions.more » « less
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Abstract Acclimatization through phenotypic plasticity represents a more rapid response to environmental change than adaptation and is vital to optimize organisms' performance in different conditions. Generally, animals are less phenotypically plastic than plants, but reef‐building corals exhibit plant‐like properties. They are light dependent with a sessile and modular construction that facilitates rapid morphological changes within their lifetime. We induced phenotypic changes by altering light exposure in a reciprocal transplant experiment and found that coral plasticity is a colony trait emerging from comprehensive morphological and physiological changes within the colony. Plasticity in skeletal features optimized coral light harvesting and utilization and paralleled significant methylome and transcriptome modifications. Network‐associated responses resulted in the identification of hub genes and clusters associated to the change in phenotype: inter‐partner recognition and phagocytosis, soft tissue growth and biomineralization. Furthermore, we identified hub genes putatively involved in animal photoreception–phototransduction. These findings fundamentally advance our understanding of how reef‐building corals repattern the methylome and adjust a phenotype, revealing an important role of light sensing by the coral animal to optimize photosynthetic performance of the symbionts.
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Abstract Climate change threatens organisms in a variety of interactive ways that requires simultaneous adaptation of multiple traits. Predicting evolutionary responses requires an understanding of the potential for interactions among stressors and the genetic variance and covariance among fitness‐related traits that may reinforce or constrain an adaptive response. Here we investigate the capacity of
Acropora millepora , a reef‐building coral, to adapt to multiple environmental stressors: rising sea surface temperature, ocean acidification, and increased prevalence of infectious diseases. We measured growth rates (weight gain), coral color (a proxy for Symbiodiniaceae density), and survival, in addition to nine physiological indicators of coral and algal health in 40 coral genets exposed to each of these three stressors singly and combined. Individual stressors resulted in predicted responses (e.g., corals developed lesions after bacterial challenge and bleached under thermal stress). However, corals did not suffer substantially more when all three stressors were combined. Nor were trade‐offs observed between tolerances to different stressors; instead, individuals performing well under one stressor also tended to perform well under every other stressor. An analysis of genetic correlations between traits revealed positive covariances, suggesting that selection to multiple stressors will reinforce rather than constrain the simultaneous evolution of traits related to holobiont health (e.g., weight gain and algal density). These findings support the potential for rapid coral adaptation under climate change and emphasize the importance of accounting for corals’ adaptive capacity when predicting the future of coral reefs.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1242/jeb.239319
