45 results on '"Cunning, R."'
Search Results
2. Comparative analysis of the Pocillopora damicornis genome highlights role of immune system in coral evolution
- Author
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Cunning, R, Bay, RA, Gillette, P, Baker, AC, and Traylor-Knowles, N
- Subjects
Environmental Sciences ,Biological Sciences ,Ecology ,Environmental Management ,Genetics ,Human Genome ,Biotechnology ,Inflammatory and immune system ,Animals ,Anthozoa ,Biological Evolution ,Gene Ontology ,Genetic Variation ,Genome ,Immune System ,Molecular Sequence Annotation ,Multigene Family ,Phylogeny ,Species Specificity - Abstract
Comparative analysis of the expanding genomic resources for scleractinian corals may provide insights into the evolution of these organisms, with implications for their continued persistence under global climate change. Here, we sequenced and annotated the genome of Pocillopora damicornis, one of the most abundant and widespread corals in the world. We compared this genome, based on protein-coding gene orthology, with other publicly available coral genomes (Cnidaria, Anthozoa, Scleractinia), as well as genomes from other anthozoan groups (Actiniaria, Corallimorpharia), and two basal metazoan outgroup phlya (Porifera, Ctenophora). We found that 46.6% of P. damicornis genes had orthologs in all other scleractinians, defining a coral 'core' genome enriched in basic housekeeping functions. Of these core genes, 3.7% were unique to scleractinians and were enriched in immune functionality, suggesting an important role of the immune system in coral evolution. Genes occurring only in P. damicornis were enriched in cellular signaling and stress response pathways, and we found similar immune-related gene family expansions in each coral species, indicating that immune system diversification may be a prominent feature of scleractinian coral evolution at multiple taxonomic levels. Diversification of the immune gene repertoire may underlie scleractinian adaptations to symbiosis, pathogen interactions, and environmental stress.
- Published
- 2018
3. Coral color and depth drive symbiosis ecology of Montipora capitata in Kāne‘ohe Bay, O‘ahu, Hawai‘i
- Author
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Innis, T., Cunning, R., Ritson-Williams, R., Wall, C. B., and Gates, R. D.
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- 2018
- Full Text
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4. Building consensus around the assessment and interpretation of Symbiodiniaceae diversity.
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Davies, SW, Gamache, MH, Howe-Kerr, LI, Kriefall, NG, Baker, AC, Banaszak, AT, Bay, LK, Bellantuono, AJ, Bhattacharya, D, Chan, CX, Claar, DC, Coffroth, MA, Cunning, R, Davy, SK, Del Campo, J, Díaz-Almeyda, EM, Frommlet, JC, Fuess, LE, González-Pech, RA, Goulet, TL, Hoadley, KD, Howells, EJ, Hume, BCC, Kemp, DW, Kenkel, CD, Kitchen, SA, LaJeunesse, TC, Lin, S, McIlroy, SE, McMinds, R, Nitschke, MR, Oakley, CA, Peixoto, RS, Prada, C, Putnam, HM, Quigley, K, Reich, HG, Reimer, JD, Rodriguez-Lanetty, M, Rosales, SM, Saad, OS, Sampayo, EM, Santos, SR, Shoguchi, E, Smith, EG, Stat, M, Stephens, TG, Strader, ME, Suggett, DJ, Swain, TD, Tran, C, Traylor-Knowles, N, Voolstra, CR, Warner, ME, Weis, VM, Wright, RM, Xiang, T, Yamashita, H, Ziegler, M, Correa, AMS, Parkinson, JE, Davies, SW, Gamache, MH, Howe-Kerr, LI, Kriefall, NG, Baker, AC, Banaszak, AT, Bay, LK, Bellantuono, AJ, Bhattacharya, D, Chan, CX, Claar, DC, Coffroth, MA, Cunning, R, Davy, SK, Del Campo, J, Díaz-Almeyda, EM, Frommlet, JC, Fuess, LE, González-Pech, RA, Goulet, TL, Hoadley, KD, Howells, EJ, Hume, BCC, Kemp, DW, Kenkel, CD, Kitchen, SA, LaJeunesse, TC, Lin, S, McIlroy, SE, McMinds, R, Nitschke, MR, Oakley, CA, Peixoto, RS, Prada, C, Putnam, HM, Quigley, K, Reich, HG, Reimer, JD, Rodriguez-Lanetty, M, Rosales, SM, Saad, OS, Sampayo, EM, Santos, SR, Shoguchi, E, Smith, EG, Stat, M, Stephens, TG, Strader, ME, Suggett, DJ, Swain, TD, Tran, C, Traylor-Knowles, N, Voolstra, CR, Warner, ME, Weis, VM, Wright, RM, Xiang, T, Yamashita, H, Ziegler, M, Correa, AMS, and Parkinson, JE
- Abstract
Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellyfish), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.
- Published
- 2023
5. Investigating the causes and consequences of symbiont shuffling in a multi-partner reef coral symbiosis under environmental change
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Cunning, R., Silverstein, R. N., and Baker, A. C.
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- 2015
6. Dynamic regulation of partner abundance mediates response of reef coral symbioses to environmental change
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Cunning, R., Vaughan, N., Gillette, P., Capo, T. R., Maté, J. L., and Baker, A. C.
- Published
- 2015
7. Temperature-mediated acquisition of rare heterologous symbionts promotes survival of coral larvae under ocean warming
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Matsuda, SB, Chakravarti, LJ, Cunning, R, Huffmyer, AS, Nelson, CE, Gates, RD, van Oppen, MJH, Matsuda, SB, Chakravarti, LJ, Cunning, R, Huffmyer, AS, Nelson, CE, Gates, RD, and van Oppen, MJH
- Abstract
Reef-building corals form nutritional symbioses with endosymbiotic dinoflagellates (Symbiodiniaceae), a relationship that facilitates the ecological success of coral reefs. These symbionts are mostly acquired anew each generation from the environment during early life stages ("horizontal transmission"). Symbiodiniaceae species exhibit trait variation that directly impacts the health and performance of the coral host under ocean warming. Here, we test the capacity for larvae of a horizontally transmitting coral, Acropora tenuis, to establish symbioses with Symbiodiniaceae species in four genera that have varying thermal thresholds (the common symbiont genera, Cladocopium and Durusdinium, and the less common Fugacium and Gerakladium). Over a 2-week period in January 2018, a series of both no-choice and four-way choice experiments were conducted at three temperatures (27, 30, and 31°C). Symbiont acquisition success and cell proliferation were measured in individual larvae. Larvae successfully acquired and maintained symbionts of all four genera in no-choice experiments, and >80% of larvae were infected with at least three genera when offered a four-way choice. Unexpectedly, Gerakladium symbionts increased in dominance over time, and at high temperatures outcompeted Durusdinium, which is regarded as thermally tolerant. Although Fugacium displayed the highest thermal tolerance in culture and reached similar cell densities to the other three symbionts at 31°C, it remained a background symbiont in choice experiments, suggesting host preference for other symbiont species. Larval survivorship at 1 week was highest in larvae associated with Gerakladium and Fugacium symbionts at 27 and 30°C, however at 31°C, mortality was similar for all treatments. We hypothesize that symbionts that are currently rare in corals (e.g., Gerakladium) may become more common and widespread in early life stages under climate warming. Uptake of such symbionts may function as a survival strategy in t
- Published
- 2022
8. The metabolic significance of symbiont community composition in the coral-algal symbiosis
- Author
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Matthews, JL, Cunning, R, Witson-Williams, R, Oakley, CA, Lutz, A, Roessner, U, Grossman, AR, Weis, VM, Gates, RD, Davy, SK, Matthews, JL, Cunning, R, Witson-Williams, R, Oakley, CA, Lutz, A, Roessner, U, Grossman, AR, Weis, VM, Gates, RD, and Davy, SK
- Abstract
Metabolite exchange between coral hosts and their dinoflagellate endosymbionts (family: Symbiodiniaceae) is one of the keys to the ecological success of coral reefs. Due to the physiological variation within Symbiodiniaceae, including amount of organic carbon and stress tolerance provided to the host, symbiont community composition has the potential to influence the nutrition and physiological success of the coral. However, the precise metabolic consequences of harboring different dominant Symbiodiniaceae species in nature is unknown. Using untargeted gas chromatography-mass spectrometry (GC-MS), we compared the metabolite profiles of both the host and symbiont relative to natural variations in the Symbiodiniaceae community composition in the reef coral Montipora capitata. The results show both host and symbiont metabolite profiles were unaffected by Symbiodiniaceae community composition under nonstressful conditions, which suggests that coral-Symbiodiniaceae symbioses have the potential to undergo physiological adjustment overtime to account for differences in their resident symbionts. Here, we discuss the project approach and findings and highlight specific workflow considerations when conducting coral symbiosis metabolomics analyses.
- Published
- 2022
9. Growth tradeoffs associated with thermotolerant symbionts in the coral Pocillopora damicornis are lost in warmer oceans
- Author
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Cunning, R., Gillette, P., Capo, T., Galvez, K., and Baker, A. C.
- Published
- 2015
- Full Text
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10. Flexible associations between Pocillopora corals and Symbiodinium limit utility of symbiosis ecology in defining species
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Cunning, R., Glynn, P. W., and Baker, A. C.
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- 2013
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11. Metabolite pools of the reef building coral Montipora capitata are unaffected by Symbiodiniaceae community composition
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Matthews, JL, Cunning, R, Ritson-Williams, R, Oakley, CA, Lutz, A, Roessner, U, Grossman, AR, Weis, VM, Gates, RD, and Davy, SK
- Subjects
fungi ,biochemical phenomena, metabolism, and nutrition ,04 Earth Sciences, 05 Environmental Sciences, 06 Biological Sciences ,Marine Biology & Hydrobiology - Abstract
© 2020, Springer-Verlag GmbH Germany, part of Springer Nature. Some reef corals form stable, dominant or codominant associations with multiple endosymbiotic dinoflagellate species (family Symbiodiniaceae). Given the immense genetic and physiological diversity within this family, Symbiodiniaceae community composition has the potential to impact the nutritional physiology and fitness of the cnidarian host and all associated symbionts. Here we assessed the impact of the symbiont community composition on the metabolome of the coral Montipora capitata in Kāne‘ohe Bay, Hawai‘i, where different colonies can be dominated by stress-tolerant Durusdinium glynnii or stress-sensitive Cladocopium spp. Based on our existing knowledge of these symbiont taxa, we hypothesised that the metabolite profile of D. glynnii-dominated corals would be consistent with poorer nutritional support of the host relative to those corals dominated by Cladocopium spp. However, comparative metabolite profiling revealed that the metabolite pools of the host and symbiont were unaffected by differences in the abundance of the two symbionts within the community. The abundance of the individual metabolites was the same in the host and in the endosymbiont regardless of whether the host was populated with D. glynnii or Cladocopium spp. These results suggest that coral-dinoflagellate symbioses have the potential to undergo physiological adjustments over time to accommodate differences in their resident symbionts. Such mechanisms may involve host heterotrophic compensation (increasing the level of nutrition generated by feeding relative to delivery from the algae), dynamic regulation of metabolic pathways when exchange of metabolites between the organisms differs, and/or modification of both the type and quantity of metabolites that are exchanged. We discuss these adjustments and the implications for the physiology and survival of reef corals under changing environmental regimes.
- Published
- 2020
12. Increasing comparability among coral bleaching experiments.
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Grottoli AG, Toonen RJ, van Woesik R, Vega Thurber R, Warner ME, McLachlan RH, Price JT, Bahr KD, Baums IB, Castillo K, Coffroth MA, Cunning R, Dobson K, Donahue M, Hench JL, Iglesias-Prieto R, Kemp DW, Kenkel CD, Kline DI, Kuffner IB, Matthews JL, Mayfield A, Padilla-Gamino J, Palumbi S, Voolstra CR, Weis VM, Wu HC, Grottoli AG, Toonen RJ, van Woesik R, Vega Thurber R, Warner ME, McLachlan RH, Price JT, Bahr KD, Baums IB, Castillo K, Coffroth MA, Cunning R, Dobson K, Donahue M, Hench JL, Iglesias-Prieto R, Kemp DW, Kenkel CD, Kline DI, Kuffner IB, Matthews JL, Mayfield A, Padilla-Gamino J, Palumbi S, Voolstra CR, Weis VM, and Wu HC
- Abstract
Coral bleaching is the single largest global threat to coral reefs worldwide. Integrating the diverse body of work on coral bleaching is critical to understanding and combating this global problem. Yet investigating the drivers, patterns, and processes of coral bleaching poses a major challenge. A recent review of published experiments revealed a wide range of experimental variables used across studies. Such a wide range of approaches enhances discovery, but without full transparency in the experimental and analytical methods used, can also make comparisons among studies challenging. To increase comparability but not stifle innovation, we propose a common framework for coral bleaching experiments that includes consideration of coral provenance, experimental conditions, and husbandry. For example, reporting the number of genets used, collection site conditions, the experimental temperature offset(s) from the maximum monthly mean (MMM) of the collection site, experimental light conditions, flow, and the feeding regime will greatly facilitate comparability across studies. Similarly, quantifying common response variables of endosymbiont (Symbiodiniaceae) and holobiont phenotypes (i.e., color, chlorophyll, endosymbiont cell density, mortality, and skeletal growth) could further facilitate cross-study comparisons. While no single bleaching experiment can provide the data necessary to determine global coral responses of all corals to current and future ocean warming, linking studies through a common framework as outlined here, would help increase comparability among experiments, facilitate synthetic insights into the causes and underlying mechanisms of coral bleaching, and reveal unique bleaching responses among genets, species, and regions. Such a collaborative framework that fosters transparency in methods used would strengthen comparisons among studies that can help inform coral reef management and facilitate conservation strategies to mitigate coral bleaching worldwide
- Published
- 2020
13. Elevated p CO 2 affects tissue biomass composition, but not calcification, in a reef coral under two light regimes
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Wall, C. B., primary, Mason, R. A. B., additional, Ellis, W. R., additional, Cunning, R., additional, and Gates, R. D., additional
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- 2017
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14. Peer Review #1 of "An updated assessment of Symbiodinium spp. that associate with common scleractinian corals from Moorea (French Polynesia) reveals high diversity among background symbionts and a novel finding of clade B (v0.1)"
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Cunning, R, additional
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- 2017
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15. Patterns of bleaching and recovery of Montipora capitata in Kāne‘ohe Bay, Hawai‘i, USA
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Cunning, R, primary, Ritson-Williams, R, additional, and Gates, RD, additional
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- 2016
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16. Growth tradeoffs associated with thermotolerant symbionts in the coral Pocillopora damicornis are lost in warmer oceans
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Cunning, R., primary, Gillette, P., additional, Capo, T., additional, Galvez, K., additional, and Baker, A. C., additional
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- 2014
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17. Diffuse pollution innovation through networks and demonstration.
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Haygarth, Philip M., Alcock, Ruth E., Oliver, D. M., Watson, N., Cunning, R., Heathwaite, A. Louise, Fox, J., Haygarth, Philip M., Alcock, Ruth E., Oliver, D. M., Watson, N., Cunning, R., Heathwaite, A. Louise, and Fox, J.
- Published
- 2010
18. Measuring multi-year changes in the Symbiodiniaceae algae in Caribbean corals on coral-depleted reefs.
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Cunning R, Lenz EA, and Edmunds PJ
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- Animals, Caribbean Region, United States Virgin Islands, Dinoflagellida genetics, Dinoflagellida physiology, Coral Reefs, Anthozoa microbiology, Symbiosis
- Abstract
Monitoring coral cover can describe the ecology of reef degradation, but rarely can it reveal the proximal mechanisms of change, or achieve its full potential in informing conservation actions. Describing temporal variation in Symbiodiniaceae within corals can help address these limitations, but this is rarely a research priority. Here, we augmented an ecological time series of the coral reefs of St. John, US Virgin Islands, by describing the genetic complement of symbiotic algae in common corals. Seventy-five corals from nine species were marked and sampled in 2017. Of these colonies, 41% were sampled in 2018, and 72% in 2019; 28% could not be found and were assumed to have died. Symbiodiniaceae ITS2 sequencing identified 525 distinct sequences (comprising 42 ITS2 type profiles), and symbiont diversity differed among host species and individuals, but was in most cases preserved within hosts over 3 yrs that were marked by physical disturbances from major hurricanes (2017) and the regional onset of stony coral tissue loss disease (2019). While changes in symbiont communities were slight and stochastic over time within colonies, variation in the dominant symbionts among colonies was observed for all host species. Together, these results indicate that declining host abundances could lead to the loss of rare algal lineages that are found in a low proportion of few coral colonies left on many reefs, especially if coral declines are symbiont-specific. These findings highlight the importance of identifying Symbiodiniaceae as part of a time series of coral communities to support holistic conservation planning. Repeated sampling of tagged corals is unlikely to be viable for this purpose, because many Caribbean corals are dying before they can be sampled multiple times. Instead, random sampling of large numbers of corals may be more effective in capturing the diversity and temporal dynamics of Symbiodiniaceae metacommunities in reef corals., Competing Interests: The authors declare that they have no competing interests., (© 2024 Cunning et al.)
- Published
- 2024
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19. Hawaiian coral holobionts reveal algal and prokaryotic host specificity, intraspecific variability in bleaching resistance, and common interspecific microbial consortia modulating thermal stress responses.
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Núñez-Pons L, Cunning R, Nelson CE, Amend AS, Sogin EM, Gates R, and Ritson-Williams R
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- Animals, Hawaii, Microbial Consortia, Host Specificity, RNA, Ribosomal, 16S genetics, Bacteria genetics, Anthozoa physiology, Dinoflagellida
- Abstract
Historically, Hawai'i had few massive coral bleaching events, until two consecutive heatwaves in 2014-2015. Consequent mortality and thermal stress were observed in Kāne'ohe Bay (O'ahu). The two most dominant local species exhibited a phenotypic dichotomy of either bleaching resistance or susceptibility (Montipora capitata and Porites compressa), while the third predominant species (Pocillopora acuta) was broadly susceptible to bleaching. In order to survey shifts in coral microbiomes during bleaching and recovery, 50 colonies were tagged and periodically monitored. Metabarcoding of three genetic markers (16S rRNA gene ITS1 and ITS2) followed by compositional approaches for community structure analysis, differential abundance and correlations for longitudinal data were used to temporally compare Bacteria/Archaea, Fungi and Symbiodiniaceae dynamics. P. compressa corals recovered faster than P. acuta and Montipora capitata. Prokaryotic and algal communities were majorly shaped by host species, and had no apparent pattern of temporal acclimatization. Symbiodiniaceae signatures were identified at the colony scale, and were often related to bleaching susceptibility. Bacterial compositions were practically constant between bleaching phenotypes, and more diverse in P. acuta and M. capitata. P. compressa's prokaryotic community was dominated by a single bacterium. Compositional approaches (via microbial balances) allowed the identification of fine-scale differences in the abundance of a consortium of microbes, driving changes by bleaching susceptibility and time across all hosts. The three major coral reef founder-species in Kāne'ohe Bay revealed different phenotypic and microbiome responses after 2014-2015 heatwaves. It is difficult to forecast, a more successful strategy towards future scenarios of global warming. Differentially abundant microbial taxa across time and/or bleaching susceptibility were broadly shared among all hosts, suggesting that locally, the same microbes may modulate stress responses in sympatric coral species. Our study highlights the potential of investigating microbial balances to identify fine-scale microbiome changes, serving as local diagnostic tools of coral reef fitness., Competing Interests: Declaration of competing interest The authors have no conflicts of interest to declare., (Copyright © 2023 Elsevier B.V. All rights reserved.)
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- 2023
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20. Marine heatwaves threaten cryptic coral diversity and erode associations among coevolving partners.
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Starko S, Fifer JE, Claar DC, Davies SW, Cunning R, Baker AC, and Baum JK
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- Animals, Genome, Genotype, Symbiosis, Coral Reefs, Anthozoa genetics, Dinoflagellida genetics
- Abstract
Climate change-amplified marine heatwaves can drive extensive mortality in foundation species. However, a paucity of longitudinal genomic datasets has impeded understanding of how these rapid selection events alter cryptic genetic structure. Heatwave impacts may be exacerbated in species that engage in obligate symbioses, where the genetics of multiple coevolving taxa may be affected. Here, we tracked the symbiotic associations of reef-building corals for 6 years through a prolonged heatwave, including known survivorship for 79 of 315 colonies. Coral genetics strongly predicted survival of the ubiquitous coral, Porites (massive growth form), with variable survival (15 to 61%) across three morphologically indistinguishable-but genetically distinct-lineages. The heatwave also disrupted strong associations between these coral lineages and their algal symbionts (family Symbiodiniaceae), with symbiotic turnover in some colonies, resulting in reduced specificity across lineages. These results highlight how heatwaves can threaten cryptic genotypes and decouple otherwise tightly coevolved relationships between hosts and symbionts.
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- 2023
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21. Building consensus around the assessment and interpretation of Symbiodiniaceae diversity.
- Author
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Davies SW, Gamache MH, Howe-Kerr LI, Kriefall NG, Baker AC, Banaszak AT, Bay LK, Bellantuono AJ, Bhattacharya D, Chan CX, Claar DC, Coffroth MA, Cunning R, Davy SK, Del Campo J, Díaz-Almeyda EM, Frommlet JC, Fuess LE, González-Pech RA, Goulet TL, Hoadley KD, Howells EJ, Hume BCC, Kemp DW, Kenkel CD, Kitchen SA, LaJeunesse TC, Lin S, McIlroy SE, McMinds R, Nitschke MR, Oakley CA, Peixoto RS, Prada C, Putnam HM, Quigley K, Reich HG, Reimer JD, Rodriguez-Lanetty M, Rosales SM, Saad OS, Sampayo EM, Santos SR, Shoguchi E, Smith EG, Stat M, Stephens TG, Strader ME, Suggett DJ, Swain TD, Tran C, Traylor-Knowles N, Voolstra CR, Warner ME, Weis VM, Wright RM, Xiang T, Yamashita H, Ziegler M, Correa AMS, and Parkinson JE
- Subjects
- Phylogeny, Consensus, Anthozoa, Symbiosis, Dinoflagellida classification, Dinoflagellida genetics, Genetic Variation, Coral Reefs
- Abstract
Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians ( e.g ., corals, octocorals, sea anemones, jellyfish), other marine invertebrates ( e.g. , sponges, molluscs, flatworms), and protists ( e.g ., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships., Competing Interests: Anastazia T. Banaszak and James Davis Reimer are Academic Editors for PeerJ., (© 2023 Davies et al.)
- Published
- 2023
- Full Text
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22. Analysis of a mechanistic model of corals in association with multiple symbionts: within-host competition and recovery from bleaching.
- Author
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Brown AL, Pfab F, Baxter EC, Detmer AR, Moeller HV, Nisbet RM, and Cunning R
- 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., (© The Author(s) 2022. Published by Oxford University Press and the Society for Experimental Biology.)
- Published
- 2022
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23. Cophylogeny and specificity between cryptic coral species (Pocillopora spp.) at Mo'orea and their symbionts (Symbiodiniaceae).
- Author
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Johnston EC, Cunning R, and Burgess SC
- Subjects
- Animals, Coral Reefs, Phylogeny, Symbiosis genetics, Anthozoa genetics, Dinoflagellida genetics
- Abstract
The congruence between phylogenies of tightly associated groups of organisms (cophylogeny) reflects evolutionary links between ecologically important interactions. However, despite being a classic example of an obligate symbiosis, tests of cophylogeny between scleractinian corals and their photosynthetic algal symbionts have been hampered in the past because both corals and algae contain genetically unresolved and morphologically cryptic species. Here, we studied co-occurring, cryptic Pocillopora species from Mo'orea, French Polynesia, that differ in their relative abundance across depth. We constructed new phylogenies of the host Pocillopora (using complete mitochondrial genomes, genomic loci, and thousands of single nucleotide polymorphisms) and their Symbiodiniaceae symbionts (using ITS2 and psbA
ncr markers) and tested for cophylogeny. The analysis supported the presence of five Pocillopora species on the fore reef at Mo'orea that mostly hosted either Cladocopium latusorum or C. pacificum. Only Pocillopora species hosting C. latusorum also hosted taxa from Symbiodinium and Durusdinium. In general, the Cladocopium phylogeny mirrored the Pocillopora phylogeny. Within Cladocopium species, lineages also differed in their associations with Pocillopora haplotypes, except those showing evidence of nuclear introgression, and with depth in the two most common Pocillopora species. We also found evidence for a new Pocillopora species (haplotype 10), that has so far only been sampled from French Polynesia, that warrants formal identification. The linked phylogenies of these Pocillopora and Cladocopium species and lineages suggest that symbiont speciation is driven by niche diversification in the host, but there is still evidence for symbiont flexibility in some cases., (© 2022 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)- Published
- 2022
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24. Fertilization by coral-dwelling fish promotes coral growth but can exacerbate bleaching response.
- Author
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Detmer AR, Cunning R, Pfab F, Brown AL, Stier AC, Nisbet RM, and Moeller HV
- Subjects
- Animals, Carbon, Coral Reefs, Fertilization, Fishes, Nitrogen, Symbiosis physiology, Anthozoa
- Abstract
Many corals form close associations with a diverse assortment of coral-dwelling fishes and other fauna. As coral reefs around the world are increasingly threatened by mass bleaching events, it is important to understand how these biotic interactions influence corals' susceptibility to bleaching. We used dynamic energy budget modeling to explore how nitrogen excreted by coral-dwelling fish affects the physiological performance of host corals. In our model, fish presence influenced the functioning of the coral-Symbiodiniaceae symbiosis by altering nitrogen availability, and the magnitude and sign of these effects depended on environmental conditions. Although our model predicted that fish-derived nitrogen can promote coral growth, the relationship between fish presence and coral tolerance of photo-oxidative stress was non-linear. Fish excretions supported denser symbiont populations that provided protection from incident light through self-shading. However, these symbionts also used more of their photosynthetic products for their own growth, rather than sharing with the coral host, putting the coral holobiont at a higher risk of becoming carbon-limited and bleaching. The balance between the benefits of increased symbiont shading and costs of reduced carbon sharing depended on environmental conditions. Thus, while there were some scenarios under which fish presence increased corals' tolerance of light stress, fish could also exacerbate bleaching and slow or prevent subsequent recovery. We discuss how the contrast between the potentially harmful effects of fish predicted by our model and results of empirical studies may relate to key model assumptions that warrant further investigation. Overall, this study provides a foundation for future work on how coral-associated fauna influence the bioenergetics of their host corals, which in turn has implications for how these corals respond to bleaching-inducing stressors., Competing Interests: Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2022 The Authors. Published by Elsevier Ltd.. All rights reserved.)
- Published
- 2022
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25. Timescale separation and models of symbiosis: state space reduction, multiple attractors and initialization.
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Pfab F, Brown AL, Detmer AR, Baxter EC, Moeller HV, Cunning R, and Nisbet RM
- Abstract
Dynamic Energy Budget models relate whole organism processes such as growth, reproduction and mortality to suborganismal metabolic processes. Much of their potential derives from extensions of the formalism to describe the exchange of metabolic products between organisms or organs within a single organism, for example the mutualism between corals and their symbionts. Without model simplification, such models are at risk of becoming parameter-rich and hence impractical. One natural simplification is to assume that some metabolic processes act on 'fast' timescales relative to others. A common strategy for formulating such models is to assume that 'fast' processes equilibrate immediately, while 'slow' processes are described by ordinary differential equations. This strategy can bring a subtlety with it. What if there are multiple, interdependent fast processes that have multiple equilibria, so that additional information is needed to unambiguously specify the model dynamics? This situation can easily arise in contexts where an organism or community can persist in a 'healthy' or an 'unhealthy' state with abrupt transitions between states possible. To approach this issue, we offer the following: (a) a method to unambiguously complete implicitly defined models by adding hypothetical 'fast' state variables; (b) an approach for minimizing the number of additional state variables in such models, which can simplify the numerical analysis and give insights into the model dynamics; and (c) some implications of the new approach that are of practical importance for model dynamics, e.g. on the bistability of flux dynamics and the effect of different initialization choices on model outcomes. To demonstrate those principles, we use a simplified model for root-shoot dynamics of plants and a related model for the interactions between corals and endosymbiotic algae that describes coral bleaching and recovery., (© The Author(s) 2022. Published by Oxford University Press and the Society for Experimental Biology.)
- Published
- 2022
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26. Will coral reefs survive by adaptive bleaching?
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Cunning R
- Subjects
- Animals, Coral Reefs, Ecosystem, Symbiosis, Anthozoa physiology, Thermotolerance
- Abstract
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., (© 2022 The Author(s). Published by Portland Press Limited on behalf of the Biochemical Society and the Royal Society of Biology.)
- Published
- 2022
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27. Temperature-mediated acquisition of rare heterologous symbionts promotes survival of coral larvae under ocean warming.
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Matsuda SB, Chakravarti LJ, Cunning R, Huffmyer AS, Nelson CE, Gates RD, and van Oppen MJH
- Subjects
- Animals, Coral Reefs, Larva, Oceans and Seas, Symbiosis, Temperature, Anthozoa, Dinoflagellida
- Abstract
Reef-building corals form nutritional symbioses with endosymbiotic dinoflagellates (Symbiodiniaceae), a relationship that facilitates the ecological success of coral reefs. These symbionts are mostly acquired anew each generation from the environment during early life stages ("horizontal transmission"). Symbiodiniaceae species exhibit trait variation that directly impacts the health and performance of the coral host under ocean warming. Here, we test the capacity for larvae of a horizontally transmitting coral, Acropora tenuis, to establish symbioses with Symbiodiniaceae species in four genera that have varying thermal thresholds (the common symbiont genera, Cladocopium and Durusdinium, and the less common Fugacium and Gerakladium). Over a 2-week period in January 2018, a series of both no-choice and four-way choice experiments were conducted at three temperatures (27, 30, and 31°C). Symbiont acquisition success and cell proliferation were measured in individual larvae. Larvae successfully acquired and maintained symbionts of all four genera in no-choice experiments, and >80% of larvae were infected with at least three genera when offered a four-way choice. Unexpectedly, Gerakladium symbionts increased in dominance over time, and at high temperatures outcompeted Durusdinium, which is regarded as thermally tolerant. Although Fugacium displayed the highest thermal tolerance in culture and reached similar cell densities to the other three symbionts at 31°C, it remained a background symbiont in choice experiments, suggesting host preference for other symbiont species. Larval survivorship at 1 week was highest in larvae associated with Gerakladium and Fugacium symbionts at 27 and 30°C, however at 31°C, mortality was similar for all treatments. We hypothesize that symbionts that are currently rare in corals (e.g., Gerakladium) may become more common and widespread in early life stages under climate warming. Uptake of such symbionts may function as a survival strategy in the wild, and has implications for reef restoration practices that use sexually produced coral stock., (© 2021 The Authors. Global Change Biology published by John Wiley & Sons Ltd.)
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- 2022
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28. Symbiont shuffling induces differential DNA methylation responses to thermal stress in the coral Montastraea cavernosa.
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Rodriguez-Casariego JA, Cunning R, Baker AC, and Eirin-Lopez JM
- Subjects
- Animals, Coral Reefs, DNA Methylation, Genome-Wide Association Study, Hot Temperature, Symbiosis genetics, Anthozoa genetics, Dinoflagellida genetics
- 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 (genus Cladocopium) 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., (© 2021 John Wiley & Sons Ltd.)
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- 2022
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29. Census of heat tolerance among Florida's threatened staghorn corals finds resilient individuals throughout existing nursery populations.
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Cunning R, Parker KE, Johnson-Sapp K, Karp RF, Wen AD, Williamson OM, Bartels E, D'Alessandro M, Gilliam DS, Hanson G, Levy J, Lirman D, Maxwell K, Million WC, Moulding AL, Moura A, Muller EM, Nedimyer K, Reckenbeil B, van Hooidonk R, Dahlgren C, Kenkel C, Parkinson JE, and Baker AC
- Subjects
- Animals, Censuses, Coral Reefs, Florida, Anthozoa physiology, Thermotolerance
- Abstract
The rapid loss of reef-building corals owing to ocean warming is driving the development of interventions such as coral propagation and restoration, selective breeding and assisted gene flow. Many of these interventions target naturally heat-tolerant individuals to boost climate resilience, but the challenges of quickly and reliably quantifying heat tolerance and identifying thermotolerant individuals have hampered implementation. Here, we used coral bleaching automated stress systems to perform rapid, standardized heat tolerance assays on 229 colonies of Acropora cervicornis across six coral nurseries spanning Florida's Coral Reef, USA. Analysis of heat stress dose-response curves for each colony revealed a broad range in thermal tolerance among individuals (approx. 2.5°C range in F
v /Fm ED50), with highly reproducible rankings across independent tests ( r = 0.76). Most phenotypic variation occurred within nurseries rather than between them, pointing to a potentially dominant role of fixed genetic effects in setting thermal tolerance and widespread distribution of tolerant individuals throughout the population. The identification of tolerant individuals provides immediately actionable information to optimize nursery and restoration programmes for Florida's threatened staghorn corals. This work further provides a blueprint for future efforts to identify and source thermally tolerant corals for conservation interventions worldwide.- Published
- 2021
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30. Dynamic symbioses reveal pathways to coral survival through prolonged heatwaves.
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Claar DC, Starko S, Tietjen KL, Epstein HE, Cunning R, Cobb KM, Baker AC, Gates RD, and Baum JK
- Subjects
- Animals, Anthozoa microbiology, Coral Reefs, Heat-Shock Response, Anthozoa physiology, Dinoflagellida physiology, Symbiosis physiology, Thermotolerance physiology, Tropical Climate adverse effects
- 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.
- Published
- 2020
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31. High light alongside elevated P CO 2 alleviates thermal depression of photosynthesis in a hard coral ( Pocillopora acuta ).
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Mason RAB, Wall CB, Cunning R, Dove S, and Gates RD
- Subjects
- Animals, Carbon Dioxide, Chlorophyll A, Coral Reefs, Humans, Hydrogen-Ion Concentration, Oceans and Seas, Photosynthesis, Seawater, Temperature, Anthozoa
- Abstract
The absorbtion of human-emitted CO
2 by the oceans (elevated PCO ) is projected to alter the physiological performance of coral reef organisms by perturbing seawater chemistry (i.e. ocean acidification). Simultaneously, greenhouse gas emissions are driving ocean warming and changes in irradiance (through turbidity and cloud cover), which have the potential to influence the effects of ocean acidification on coral reefs. Here, we explored whether physiological impacts of elevated P2 CO on a coral-algal symbiosis ( Pocillopora acuta- Symbiodiniaceae) are mediated by light and/or temperature levels. In a 39 day experiment, elevated P2 CO (962 versus 431 µatm P2 CO ) had an interactive effect with midday light availability (400 versus 800 µmol photons m2 -2 s-1 ) and temperature (25 versus 29°C) on areal gross and net photosynthesis, for which a decline at 29°C was ameliorated under simultaneous high- PCO and high-light conditions. Light-enhanced dark respiration increased under elevated P2 CO and/or elevated temperature. Symbiont to host cell ratio and chlorophyll a per symbiont increased at elevated temperature, whilst symbiont areal density decreased. The ability of moderately strong light in the presence of elevated P2 CO to alleviate the temperature-induced decrease in photosynthesis suggests that higher substrate availability facilitates a greater ability for photochemical quenching, partially offsetting the impacts of high temperature on the photosynthetic apparatus. Future environmental changes that result in moderate increases in light levels could therefore assist the P. acuta holobiont to cope with the 'one-two punch' of rising temperatures in the presence of an acidifying ocean., Competing Interests: Competing interestsThe authors declare no competing or financial interests., (© 2020. Published by The Company of Biologists Ltd.)2 - Published
- 2020
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32. Thermotolerant coral symbionts modulate heat stress-responsive genes in their hosts.
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Cunning R and Baker AC
- Subjects
- Animals, Caribbean Region, Coral Reefs, Heat-Shock Response genetics, Hot Temperature, Oceans and Seas, Symbiosis genetics, Anthozoa genetics, Dinoflagellida genetics, Thermotolerance genetics
- Abstract
Some corals may become more resistant to bleaching by shuffling their Symbiodiniaceae communities toward thermally tolerant species, and manipulations to boost the abundance of these symbionts in corals may increase resilience in warming oceans. However, the thermotolerant symbiont Durusdinium trenchii may reduce growth and fecundity in Caribbean corals, and these tradeoffs need to be better understood as this symbiont spreads through the region. We sought to understand how D. trenchii modulates coral gene expression by manipulating symbiont communities in Montastraea cavernosa to produce replicate ramets containing D. trenchii together with paired ramets of these same genets (n = 3) containing Cladocopium C3 symbionts. We then examined differences in global gene expression between corals hosting Durusdinium and Cladocopium under control temperatures, and in response to short-term heat stress. We identified numerous transcriptional differences associated with symbiont identity, which explained 2%-14% of the transcriptional variance. Corals with D. trenchii upregulated genes related to translation, ribosomal structure and biogenesis, and downregulated genes related to extracellular structures, and carbohydrate and lipid transport and metabolism, relative to corals with Cladocopium. Unexpectedly, these changes were similar to those observed in Cladocopium-dominated corals in response to heat stress, suggesting that thermotolerant D. trenchii may cause corals to increase expression of heat stress-responsive genes, explaining both the increased heat tolerance and the associated energetic tradeoffs in corals containing D. trenchii. These findings provide insight into the ecological changes occurring on contemporary coral reefs in response to climate change, and the diverse ways in which different symbionts modulate emergent phenotypes of their hosts., (© 2020 John Wiley & Sons Ltd.)
- Published
- 2020
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33. Competition and succession among coral endosymbionts.
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McIlroy SE, Cunning R, Baker AC, and Coffroth MA
- Abstract
Host species often support a genetically diverse guild of symbionts, the identity and performance of which can determine holobiont fitness under particular environmental conditions. These symbiont communities are structured by a complex set of potential interactions, both positive and negative, between the host and symbionts and among symbionts. In reef-building corals, stable associations with specific symbiont species are common, and we hypothesize that this is partly due to ecological mechanisms, such as succession and competition, which drive patterns of symbiont winnowing in the initial colonization of new generations of coral recruits. We tested this hypothesis using the experimental framework of the de Wit replacement series and found that competitive interactions occurred among symbionts which were characterized by unique ecological strategies. Aposymbiotic octocoral recruits within high- and low-light environments were inoculated with one of three Symbiodiniaceae species as monocultures or with cross-paired mixtures, and we tracked symbiont uptake using quantitative genetic assays. Priority effects, in which early colonizers excluded competitive dominants, were evidenced under low light, but these early opportunistic species were later succeeded by competitive dominants. Under high light, a more consistent competitive hierarchy was established in which competitive dominants outgrew and limited the abundance of others. These findings provide insight into mechanisms of microbial community organization and symbiosis breakdown and recovery. Furthermore, transitions in competitive outcomes across spatial and temporal environmental variation may improve lifetime host fitness., Competing Interests: All authors declare that there are no competing financial interests in relation to the work described., (© 2019 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.)
- Published
- 2019
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34. Extensive coral mortality and critical habitat loss following dredging and their association with remotely-sensed sediment plumes.
- Author
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Cunning R, Silverstein RN, Barnes BB, and Baker AC
- Subjects
- Animals, Coral Reefs, Ecosystem, Environmental Monitoring, Florida, Anthozoa, Geologic Sediments
- Abstract
Dredging poses a potential threat to coral reefs, yet quantifying impacts is often difficult due to the large spatial footprint of potential effects and co-occurrence of other disturbances. Here we analyzed in situ monitoring data and remotely-sensed sediment plumes to assess impacts of the 2013-2015 Port of Miami dredging on corals and reef habitat. To control for contemporaneous bleaching and disease, we analyzed the spatial distribution of impacts in relation to the dredged channel. Areas closer to dredging experienced higher sediment trap accumulation, benthic sediment cover, coral burial, and coral mortality, and our spatial analyses indicate that >560,000 corals were killed within 0.5 km, with impacts likely extending over 5-10 km. The occurrence of sediment plumes explained ~60% of spatial variability in measured impacts, suggesting that remotely-sensed plumes, when properly calibrated against in situ monitoring data, can reliably estimate the magnitude and extent of dredging impacts., (Copyright © 2019. Published by Elsevier Ltd.)
- Published
- 2019
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35. Attenuating Diabetic Vascular and Neuronal Defects by Targeting P2rx7.
- Author
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Pavlou S, Augustine J, Cunning R, Harkin K, Stitt AW, Xu H, and Chen M
- Subjects
- Animals, Biomarkers, Diabetes Mellitus, Experimental, Diabetic Retinopathy diagnosis, Electroretinography, Fluorescent Antibody Technique, Gene Expression, Immunohistochemistry, Lamivudine pharmacology, Male, Mice, Receptors, Purinergic P2X7 genetics, Retinal Neurons drug effects, Retinal Neurons pathology, Retinal Vessels drug effects, Retinal Vessels pathology, Tomography, Optical Coherence, Diabetic Retinopathy metabolism, Purinergic P2X Receptor Antagonists pharmacology, Receptors, Purinergic P2X7 metabolism, Retinal Neurons metabolism, Retinal Vessels metabolism
- Abstract
Retinal vascular and neuronal degeneration are established pathological features of diabetic retinopathy. Data suggest that defects in the neuroglial network precede the clinically recognisable vascular lesions in the retina. Therefore, new treatments that target early-onset neurodegeneration would be expected to have great value in preventing the early stages of diabetic retinopathy. Here, we show that the nucleoside reverse transcriptase inhibitor lamivudine (3TC), a newly discovered P2rx7 inhibitor, can attenuate progression of both neuronal and vascular pathology in diabetic retinopathy. We found that the expression of P2rx7 was increased in the murine retina as early as one month following diabetes induction. Compared to non-diabetic controls, diabetic mice treated with 3TC were protected against the formation of acellular capillaries in the retina. This occurred concomitantly with a maintenance in neuroglial function, as shown by improved a- and b-wave amplitude, as well as oscillatory potentials. An improvement in the number of GABAergic amacrine cells and the synaptophysin-positive area was also observed in the inner retina of 3TC-treated diabetic mice. Our data suggest that 3TC has therapeutic potential since it can target both neuronal and vascular defects caused by diabetes.
- Published
- 2019
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36. A dynamic bioenergetic model for coral-Symbiodinium symbioses and coral bleaching as an alternate stable state.
- Author
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Cunning R, Muller EB, Gates RD, and Nisbet RM
- Subjects
- Algorithms, Animals, Biomass, Climate Change, Coral Reefs, Energy Metabolism, Seasons, Anthozoa physiology, Dinoflagellida physiology, Models, Biological, Symbiosis physiology
- Abstract
Coral reef ecosystems owe their ecological success - and vulnerability to climate change - to the symbiotic metabolism of corals and Symbiodinium spp. The urgency to understand and predict the stability and breakdown of these symbioses (i.e., coral 'bleaching') demands the development and application of theoretical tools. Here, we develop a dynamic bioenergetic model of coral-Symbiodinium symbioses that demonstrates realistic steady-state patterns in coral growth and symbiont abundance across gradients of light, nutrients, and feeding. Furthermore, by including a mechanistic treatment of photo-oxidative stress, the model displays dynamics of bleaching and recovery that can be explained as transitions between alternate stable states. These dynamics reveal that "healthy" and "bleached" states correspond broadly to nitrogen- and carbon-limitation in the system, with transitions between them occurring as integrated responses to multiple environmental factors. Indeed, a suite of complex emergent behaviors reproduced by the model (e.g., bleaching is exacerbated by nutrients and attenuated by feeding) suggests it captures many important attributes of the system; meanwhile, its modular framework and open source R code are designed to facilitate further problem-specific development. We see significant potential for this modeling framework to generate testable hypotheses and predict integrated, mechanistic responses of corals to environmental change, with important implications for understanding the performance and maintenance of symbiotic systems., (Copyright © 2017 The Authors. Published by Elsevier Ltd.. All rights reserved.)
- Published
- 2017
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37. Using high-throughput sequencing of ITS2 to describe Symbiodinium metacommunities in St. John, US Virgin Islands.
- Author
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Cunning R, Gates RD, and Edmunds PJ
- Abstract
Symbiotic microalgae ( Symbiodinium spp.) strongly influence the performance and stress-tolerance of their coral hosts, making the analysis of Symbiodinium communities in corals (and metacommunities on reefs) advantageous for many aspects of coral reef research. High-throughput sequencing of ITS2 nrDNA offers unprecedented scale in describing these communities, yet high intragenomic variability at this locus complicates the resolution of biologically meaningful diversity. Here, we demonstrate that generating operational taxonomic units by clustering ITS2 sequences at 97% similarity within, but not across, samples collapses sequence diversity that is more likely to be intragenomic, while preserving diversity that is more likely interspecific. We utilize this 'within-sample clustering' to analyze Symbiodinium from ten host taxa on shallow reefs on the north and south shores of St. John, US Virgin Islands. While Symbiodinium communities did not differ between shores, metacommunity network analysis of host-symbiont associations revealed Symbiodinium lineages occupying 'dominant' and 'background' niches, and coral hosts that are more 'flexible' or 'specific' in their associations with Symbiodinium . These methods shed new light on important questions in coral symbiosis ecology, and demonstrate how application-specific bioinformatic pipelines can improve the analysis of metabarcoding data in microbial metacommunity studies., Competing Interests: The authors declare there are no competing interests.
- Published
- 2017
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38. Tenacious D: Symbiodinium in clade D remain in reef corals at both high and low temperature extremes despite impairment.
- Author
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Silverstein RN, Cunning R, and Baker AC
- Subjects
- Animals, Cold Temperature, Hot Temperature, Stress, Physiological, Acclimatization, Anthozoa physiology, Climate Change, Coral Reefs, Dinoflagellida physiology, Symbiosis
- Abstract
Reef corals are sensitive to thermal stress, which induces coral bleaching (the loss of algal symbionts), often leading to coral mortality. However, corals hosting certain symbionts (notably some members of Symbiodinium clade D) resist bleaching when exposed to high temperatures. To determine whether these symbionts are also cold tolerant, we exposed corals hosting either Symbiodinium C3 or D1a to incremental warming (+1°C week
-1 to 35°C) and cooling (-1°C week-1 to 15°C), and measured photodamage and symbiont loss. During warming to 33°C, C3 corals were photodamaged and lost >99% of symbionts, while D1a corals experienced photodamage but did not bleach. During cooling, D1a corals suffered more photodamage than C3 corals but still did not bleach, while C3 corals lost 94% of symbionts. These results indicate that photodamage does not always lead to bleaching, suggesting alternate mechanisms exist by which symbionts resist bleaching, and helping explain the persistence of D1a symbionts on recently bleached reefs, with implications for the future of these ecosystems., (© 2017. Published by The Company of Biologists Ltd.)- Published
- 2017
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39. Species-specific responses to climate change and community composition determine future calcification rates of Florida Keys reefs.
- Author
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Okazaki RR, Towle EK, van Hooidonk R, Mor C, Winter RN, Piggot AM, Cunning R, Baker AC, Klaus JS, Swart PK, and Langdon C
- Subjects
- Animals, Anthozoa, Caribbean Region, Florida, Population Dynamics, Seawater, Climate Change, Coral Reefs
- Abstract
Anthropogenic climate change compromises reef growth as a result of increasing temperatures and ocean acidification. Scleractinian corals vary in their sensitivity to these variables, suggesting species composition will influence how reef communities respond to future climate change. Because data are lacking for many species, most studies that model future reef growth rely on uniform scleractinian calcification sensitivities to temperature and ocean acidification. To address this knowledge gap, calcification of twelve common and understudied Caribbean coral species was measured for two months under crossed temperatures (27, 30.3 °C) and CO
2 partial pressures (pCO2 ) (400, 900, 1300 μatm). Mixed-effects models of calcification for each species were then used to project community-level scleractinian calcification using Florida Keys reef composition data and IPCC AR5 ensemble climate model data. Three of the four most abundant species, Orbicella faveolata, Montastraea cavernosa, and Porites astreoides, had negative calcification responses to both elevated temperature and pCO2 . In the business-as-usual CO2 emissions scenario, reefs with high abundances of these species had projected end-of-century declines in scleractinian calcification of >50% relative to present-day rates. Siderastrea siderea, the other most common species, was insensitive to both temperature and pCO2 within the levels tested here. Reefs dominated by this species had the most stable end-of-century growth. Under more optimistic scenarios of reduced CO2 emissions, calcification rates throughout the Florida Keys declined <20% by 2100. Under the most extreme emissions scenario, projected declines were highly variable among reefs, ranging 10-100%. Without considering bleaching, reef growth will likely decline on most reefs, especially where resistant species like S. siderea are not already dominant. This study demonstrates how species composition influences reef community responses to climate change and how reduced CO2 emissions can limit future declines in reef calcification., (© 2016 John Wiley & Sons Ltd.)- Published
- 2017
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40. The effects of Symbiodinium (Pyrrhophyta) identity on growth, survivorship, and thermal tolerance of newly settled coral recruits.
- Author
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McIlroy SE, Gillette P, Cunning R, Klueter A, Capo T, Baker AC, and Coffroth MA
- Subjects
- Animals, Anthozoa growth & development, Florida, Species Specificity, Anthozoa physiology, Dinoflagellida physiology, Symbiosis, Thermotolerance
- Abstract
For many coral species, the obligate association with phylogenetically diverse algal endosymbiont species is dynamic in time and space. Here, we used controlled laboratory inoculations of newly settled, aposymbiotic corals (Orbicella faveolata) with two cultured species of algal symbiont (Symbiodinium microadriaticum and S. minutum) to examine the role of symbiont identity on growth, survivorship, and thermal tolerance of the coral holobiont. We evaluated these data in the context of Symbiodinium photophysiology for 9 months post-settlement and also during a 5-d period of elevated temperatures Our data show that recruits that were inoculated with S. minutum grew significantly slower than those inoculated with S. microadriaticum (occasionally co-occurring with S. minutum), but that there was no difference in survivorship of O. faveolata polyps infected with Symbiodinium. However, photophysiological metrics (∆Fv/F'm, the efficiency with which available light is used to drive photosynthesis and α, the maximum light utilization coefficient) were higher in those slower growing recruits containing S. minutum. These findings suggest that light use (i.e., photophysiology) and carbon acquisition by the coral host (i.e., host growth) are decoupled, but did not distinguish the source of this difference. Neither Symbiodinium treatment demonstrated a significant negative effect of a 5-d exposure to temperatures as high as 32°C under low light conditions similar to those measured at settlement habitats., (© 2016 Phycological Society of America.)
- Published
- 2016
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41. Variability of Symbiodinium Communities in Waters, Sediments, and Corals of Thermally Distinct Reef Pools in American Samoa.
- Author
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Cunning R, Yost DM, Guarinello ML, Putnam HM, and Gates RD
- Subjects
- American Samoa, Animals, Computational Biology, Dinoflagellida genetics, High-Throughput Nucleotide Sequencing, Anthozoa microbiology, Biodiversity, Coral Reefs, Dinoflagellida classification, Geologic Sediments microbiology, Seawater microbiology, Temperature
- Abstract
Reef-building corals host assemblages of symbiotic algae (Symbiodinium spp.) whose diversity and abundance may fluctuate under different conditions, potentially facilitating acclimatization to environmental change. The composition of free-living Symbiodinium in reef waters and sediments may also be environmentally labile and may influence symbiotic assemblages by mediating supply and dispersal. The magnitude and spatial scales of environmental influence over Symbiodinium composition in different reef habitat compartments are, however, not well understood. We used pyrosequencing to compare Symbiodinium in sediments, water, and ten coral species between two backreef pools in American Samoa with contrasting thermal environments. We found distinct compartmental assemblages of clades A, C, D, F, and/or G Symbiodinium types, with strong differences between pools in water, sediments, and two coral species. In the pool with higher and more variable temperatures, abundance of various clade A and C types differed compared to the other pool, while abundance of D types was lower in sediments but higher in water and in Pavona venosa, revealing an altered habitat distribution and potential linkages among compartments. The lack of between-pool effects in other coral species was due to either low overall variability (in the case of Porites) or high within-pool variability. Symbiodinium communities in water and sediment also showed within-pool structure, indicating that environmental influences may operate over multiple, small spatial scales. This work suggests that Symbiodinium composition is highly labile in reef waters, sediments, and some corals, but the underlying drivers and functional consequences of this plasticity require further testing with high spatial resolution biological and environmental sampling.
- Published
- 2015
- Full Text
- View/download PDF
42. Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals.
- Author
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Silverstein RN, Cunning R, and Baker AC
- Subjects
- Analysis of Variance, Animals, Chlorophyll metabolism, DNA Primers genetics, Dinoflagellida genetics, Fluorometry, Polymerase Chain Reaction, Acclimatization physiology, Anthozoa physiology, Coral Reefs, Dinoflagellida physiology, Hot Temperature, Symbiosis
- Abstract
Mutualistic organisms can be particularly susceptible to climate change stress, as their survivorship is often limited by the most vulnerable partner. However, symbiotic plasticity can also help organisms in changing environments by expanding their realized niche space. Coral-algal (Symbiodinium spp.) symbiosis exemplifies this dichotomy: the partnership is highly susceptible to 'bleaching' (stress-induced symbiosis breakdown), but stress-tolerant symbionts can also sometimes mitigate bleaching. Here, we investigate the role of diverse and mutable symbiotic partnerships in increasing corals' ability to thrive in high temperature conditions. We conducted repeat bleaching and recovery experiments on the coral Montastraea cavernosa, and used quantitative PCR and chlorophyll fluorometry to assess the structure and function of Symbiodinium communities within coral hosts. During an initial heat exposure (32 °C for 10 days), corals hosting only stress-sensitive symbionts (Symbiodinium C3) bleached, but recovered (at either 24 °C or 29 °C) with predominantly (>90%) stress-tolerant symbionts (Symbiodinium D1a), which were not detected before bleaching (either due to absence or extreme low abundance). When a second heat stress (also 32 °C for 10 days) was applied 3 months later, corals that previously bleached and were now dominated by D1a Symbiodinium experienced less photodamage and symbiont loss compared to control corals that had not been previously bleached, and were therefore still dominated by Symbiodinium C3. Additional corals that were initially bleached without heat by a herbicide (DCMU, at 24 °C) also recovered predominantly with D1a symbionts, and similarly lost fewer symbionts during subsequent thermal stress. Increased thermotolerance was also not observed in C3-dominated corals that were acclimated for 3 months to warmer temperatures (29 °C) before heat stress. These findings indicate that increased thermotolerance post-bleaching resulted from symbiont community composition changes, not prior heat exposure. Moreover, initially undetectable D1a symbionts became dominant only after bleaching, and were critical to corals' resilience after stress and resistance to future stress., (© 2014 John Wiley & Sons Ltd.)
- Published
- 2015
- Full Text
- View/download PDF
43. Not just who, but how many: the importance of partner abundance in reef coral symbioses.
- Author
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Cunning R and Baker AC
- Abstract
The performance and function of reef corals depends on the genetic identity of their symbiotic algal partners, with some symbionts providing greater benefits (e.g., photosynthate, thermotolerance) than others. However, these interaction outcomes may also depend on partner abundance, with differences in the total number of symbionts changing the net benefit to the coral host, depending on the particular environmental conditions. We suggest that symbiont abundance is a fundamental aspect of the dynamic interface between reef corals and the abiotic environment that ultimately determines the benefits, costs, and functional responses of these symbioses. This density-dependent framework suggests that corals may regulate the size of their symbiont pool to match microhabitat-specific optima, which may contribute to the high spatiotemporal variability in symbiont abundance observed within and among colonies and reefs. Differences in symbiont standing stock may subsequently explain variation in energetics, growth, reproduction, and stress susceptibility, and may mediate the impacts of environmental change on these outcomes. However, the importance of symbiont abundance has received relatively little recognition, possibly because commonly-used metrics based on surface area (e.g., symbiont cells cm(-2)) may be only weakly linked to biological phenomena and are difficult to compare across studies. We suggest that normalizing symbionts to biological host parameters, such as units of protein or numbers of host cells, will more clearly elucidate the functional role of symbiont abundance in reef coral symbioses. In this article, we generate testable hypotheses regarding the importance of symbiont abundance by first discussing different metrics and their potential links to symbiosis performance and breakdown, and then describing how natural variability and dynamics of symbiont communities may help explain ecological patterns on coral reefs and predict responses to environmental change.
- Published
- 2014
- Full Text
- View/download PDF
44. Changes in coral microbial communities in response to a natural pH gradient.
- Author
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Meron D, Rodolfo-Metalpa R, Cunning R, Baker AC, Fine M, and Banin E
- Subjects
- Animals, Bacteria classification, Bacteria genetics, Hydrogen-Ion Concentration, Metagenome genetics, Phylogeny, RNA, Ribosomal, 16S genetics, Anthozoa microbiology, Bacterial Physiological Phenomena, Biodiversity, Metagenome physiology, Seawater chemistry
- Abstract
Surface seawater pH is currently 0.1 units lower than pre-industrial values and is projected to decrease by up to 0.4 units by the end of the century. This acidification has the potential to cause significant perturbations to the physiology of ocean organisms, particularly those such as corals that build their skeletons/shells from calcium carbonate. Reduced ocean pH could also have an impact on the coral microbial community, and thus may affect coral physiology and health. Most of the studies to date have examined the impact of ocean acidification on corals and/or associated microbiota under controlled laboratory conditions. Here we report the first study that examines the changes in coral microbial communities in response to a natural pH gradient (mean pH(T) 7.3-8.1) caused by volcanic CO(2) vents off Ischia, Gulf of Naples, Italy. Two Mediterranean coral species, Balanophyllia europaea and Cladocora caespitosa, were examined. The microbial community diversity and the physiological parameters of the endosymbiotic dinoflagellates (Symbiodinium spp.) were monitored. We found that pH did not have a significant impact on the composition of associated microbial communities in both coral species. In contrast to some earlier studies, we found that corals present at the lower pH sites exhibited only minor physiological changes and no microbial pathogens were detected. Together, these results provide new insights into the impact of ocean acidification on the coral holobiont.
- Published
- 2012
- Full Text
- View/download PDF
45. Development of gene expression markers of acute heat-light stress in reef-building corals of the genus Porites.
- Author
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Kenkel CD, Aglyamova G, Alamaru A, Bhagooli R, Capper R, Cunning R, deVillers A, Haslun JA, Hédouin L, Keshavmurthy S, Kuehl KA, Mahmoud H, McGinty ES, Montoya-Maya PH, Palmer CV, Pantile R, Sánchez JA, Schils T, Silverstein RN, Squiers LB, Tang PC, Goulet TL, and Matz MV
- Subjects
- Actins genetics, Animals, Biomarkers, Gene Expression Regulation, Heat-Shock Proteins genetics, Coral Reefs, Gene Expression Profiling, Hot Temperature adverse effects, Light adverse effects, Stress, Physiological genetics
- Abstract
Coral reefs are declining worldwide due to increased incidence of climate-induced coral bleaching, which will have widespread biodiversity and economic impacts. A simple method to measure the sub-bleaching level of heat-light stress experienced by corals would greatly inform reef management practices by making it possible to assess the distribution of bleaching risks among individual reef sites. Gene expression analysis based on quantitative PCR (qPCR) can be used as a diagnostic tool to determine coral condition in situ. We evaluated the expression of 13 candidate genes during heat-light stress in a common Caribbean coral Porites astreoides, and observed strong and consistent changes in gene expression in two independent experiments. Furthermore, we found that the apparent return to baseline expression levels during a recovery phase was rapid, despite visible signs of colony bleaching. We show that the response to acute heat-light stress in P. astreoides can be monitored by measuring the difference in expression of only two genes: Hsp16 and actin. We demonstrate that this assay discriminates between corals sampled from two field sites experiencing different temperatures. We also show that the assay is applicable to an Indo-Pacific congener, P. lobata, and therefore could potentially be used to diagnose acute heat-light stress on coral reefs worldwide.
- Published
- 2011
- Full Text
- View/download PDF
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