Some reef-building corals form symbioses with multiple algal partners that differ in ecologically important traits like heat tolerance. Coral bleaching and recovery can drive symbiont community turnover toward more heat-tolerant partners, and this ‘adaptive bleaching’ response can increase future bleaching thresholds by 1–2°C, aiding survival in warming oceans. However, this mechanism of rapid acclimatization only occurs in corals that are compatible with multiple symbionts, and only when the disturbance regime and competitive dynamics among symbionts are sufficient to bring about community turnover. The full scope of coral taxa and ecological scenarios in which symbiont shuffling occurs remains poorly understood, though its prevalence is likely to increase as warming oceans boost the competitive advantage of heat-tolerant symbionts, increase the frequency of bleaching events, and strengthen metacommunity feedbacks. Still, the constraints, limitations, and potential tradeoffs of symbiont shuffling suggest it will not save coral reef ecosystems; however, it may significantly improve the survival trajectories of some, or perhaps many, coral species. Interventions to manipulate coral symbionts and symbiont communities may expand the scope of their adaptive potential, which may boost coral survival until climate change is addressed.
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Analysis of a mechanistic model of corals in association with multiple symbionts: within-host competition and recovery from bleaching
Abstract Coral reefs are increasingly experiencing stressful conditions, such as high temperatures, that cause corals to undergo bleaching, a process where they lose their photosynthetic algal symbionts. Bleaching threatens both corals’ survival and the health of the reef ecosystems they create. One possible mechanism for corals to resist bleaching is through association with stress-tolerant symbionts, which are resistant to bleaching but may be worse partners in mild conditions. Some corals have been found to associate with multiple symbiont species simultaneously, which potentially gives them access to the benefits of both stress-sensitive and -tolerant symbionts. However, within-host competition between symbionts may lead to competitive exclusion of one partner, and the consequences of associating with multiple partners simultaneously are not well understood. We modify a mechanistic model of coral-algal symbiosis to investigate the effect of environmental conditions on within-host competitive dynamics between stress-sensitive and -tolerant symbionts and the effect of access to a tolerant symbiont on the dynamics of recovery from bleaching. We found that the addition of a tolerant symbiont can increase host survival and recovery from bleaching in high-light conditions. Competitive exclusion of the tolerant symbiont occurred slowly at intermediate light levels. Interestingly, there were some cases of post-bleaching competitive exclusion after the tolerant symbiont had helped the host recover.
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- NSF-PAR ID:
- 10421683
- Editor(s):
- Cooke, Steven
- Date Published:
- Journal Name:
- Conservation Physiology
- Volume:
- 10
- Issue:
- 1
- ISSN:
- 2051-1434
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Prospects for coral persistence through increasingly frequent and extended heatwaves seem bleak. Coral recovery from bleaching is only known to occur after temperatures return to normal, and mitigation of local stressors does not appear to augment coral survival. Capitalizing on a natural experiment in the equatorial Pacific, we track individual coral colonies at sites spanning a gradient of local anthropogenic disturbance through a tropical heatwave of unprecedented duration. Unexpectedly, some corals survived the event by recovering from bleaching while still at elevated temperatures. These corals initially had heat-sensitive algal symbiont communities, endured bleaching, and then recovered through proliferation of heat-tolerant symbionts. This pathway to survival only occurred in the absence of strong local stressors. In contrast, corals in highly disturbed areas were already dominated by heat-tolerant symbionts, and despite initially resisting bleaching, these corals had no survival advantage in one species and 3.3 times lower survival in the other. These unanticipated connections between disturbance, coral symbioses and heat stress resilience reveal multiple pathways to coral survival through future prolonged heatwaves.
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Abstract Algal symbiont shuffling in favour of more thermotolerant species has been shown to enhance coral resistance to heat‐stress. Yet, the mechanistic underpinnings and long‐term implications of these changes are poorly understood. This work studied the modifications in coral DNA methylation, an epigenetic mechanism involved in coral acclimatization, in response to symbiont manipulation and subsequent heat stress exposure. Symbiont composition was manipulated in the great star coral
Montastraea cavernosa through controlled thermal bleaching and recovery, producing paired ramets of three genets dominated by either their native symbionts (genusCladocopium ) or the thermotolerant species (Durusdinium trenchi ). Single‐base genome‐wide analyses showed significant modifications in DNA methylation concentrated in intergenic regions, introns and transposable elements. Remarkably, DNA methylation changes in response to heat stress were dependent on the dominant symbiont, with twice as many differentially methylated regions found in heat‐stressed corals hosting different symbionts (Cladocopium vs.D .trenchii ) compared to all other comparisons. Interestingly, while differential gene body methylation was not correlated with gene expression, an enrichment in differentially methylated regions was evident in repetitive genome regions. Overall, these results suggest that changes in algal symbionts favouring heat tolerant associations are accompanied by changes in DNA methylation in the coral host. The implications of these results for coral adaptation, along with future avenues of research based on current knowledge gaps, are discussed in the present work. -
Contrasting effects of Symbiodinium identity on coral host transcriptional profiles across latitudesmore » « less
Abstract Reef‐building corals can increase their resistance to heat‐induced bleaching through adaptation and acclimatization and/or by associating with a more thermo‐tolerant strain of algal symbiont (
Symbiodinium sp.). Here, we show that these two adaptive pathways interact. We collectedAcropora millepora corals from two contrasting thermal environments on the Great Barrier Reef: cooler, mid‐latitude Orpheus Island, where all corals hosted a heat‐sensitive clade CSymbiodinium , and warmer, low‐latitude Wilkie Island, where corals hosted either a clade C or a more thermo‐tolerant clade D. Corals were kept in a benign common garden to reveal differences in baseline gene expression, reflecting prior adaptation/long‐term acclimatization. Model‐based analysis identified gene expression differences between Wilkie and Orpheus corals that were negatively correlated with previously described transcriptome‐wide signatures of heat stress, signifying generally elevated thermotolerance of Wilkie corals. Yet, model‐free analyses of gene expression revealed that Wilkie corals hosting clade C were distinct from Wilkie corals hosting clade D, whereas Orpheus corals were more variable. Wilkie corals hosting clade C symbionts exhibited unique functional signatures, including downregulation of histone proteins and ion channels and upregulation of chaperones andRNA processing genes, putatively representing constitutive “frontloading” of stress response genes. Furthermore, clade CSymbiodinium exhibited constitutive expression differences between Wilkie and Orpheus, indicative of contrasting life history strategies. Our results demonstrate that hosting alternativeSymbiodinium types is associated with different pathways of local adaptation for the coral host. These interactions could play a significant role in setting the direction of genetic adaptation to global warming in the two symbiotic partners. -
The future of coral reefs in a warming world depends on corals’ ability to recover from bleaching, the loss of their symbiotic dinoflagellate algae (Symbiodiniaceae) during marine heatwaves. Heat-tolerant symbiont species can remain in symbiosis during heat stress, but often provide less photosynthate to the host than heat-sensitive species under ambient conditions. Understanding how heat stress changes the dynamics of this tradeoff between stress tolerance and mutualism contribution is crucial for predicting coral success under climate change. To test how symbiont resource allocation affects coral recovery from heat stress, we exposed the coral Montipora capitata hosting either heat-sensitive Cladocopium C31 (C) or heat-tolerant Durusdinium glynnii (D) to heat stress. D regained symbiont density and photochemical efficiency faster after heat treat- ment than C, but symbiont recovery did not restore coral biomass or calcification rates to pre-bleaching levels in the initial recovery period. D populations also contributed less photosynthate to the host relative to C, even during heat stress. Further, higher-density symbiont populations of both species retained more photosynthate than lower-density populations, and corals receiving less photosynthate exhibited reduced calcification rates and lower intracellular pH. This is the first evidence that symbiont density and carbon translocation are negatively related, and the first to establish a link between Symbiodiniaceae carbon translocation and coral cellular homeostasis. Together, these results suggest the energy demand of symbiont regrowth after bleaching reduces their mutualism contribution and can thus delay host recovery. Reestablishing a beneficial endos- ymbiosis imposes additional costs as holobionts overcome stress, and may explain latent mortality among coral populations after alleviation of heat stress in the field.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/conphys/coac066
