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Symbiont genotype influences holobiont response to increased temperature

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  • Loarie, S. R. et al. The velocity of climate change. Nature 462, 1052–1055 (2009).

    Article 
    ADS 
    PubMed 

    Google Scholar 

  • Yoshida, T., Jones, L. E., Ellner, S. P., Fussmann, G. F. & Hairston, N. G. Rapid evolution drives ecological dynamics in a predator–prey system. Nature 424, 303–306 (2003).

    Article 
    ADS 
    PubMed 

    Google Scholar 

  • terHorst, C. P., Miller, T. E. & Levitan, D. R. Evolution of prey in ecological time reduces the effect size of predators in experimental microcosms. Ecology 91, 629–636 (2010).

    Article 
    PubMed 

    Google Scholar 

  • Duffy, M. A. & Sivars-Becker, L. Rapid evolution and ecological host-parasite dynamics. Ecol. Lett. 10, 44–53 (2007).

    Article 
    PubMed 

    Google Scholar 

  • Diamond, S. E., Chick, L. D., Perez, A., Strickler, S. A. & Martin, R. A. Evolution of thermal tolerance and its fitness consequences: parallel and non-parallel responses to urban heat islands across three cities. Proc. Biol. Sci. 285, 20180036 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Franks, S. J., Sim, S. & Weis, A. E. Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc. Natl. Acad. Sci. USA 104, 1278–1282 (2007).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • terHorst, C. P., Lennon, J. T. & Lau, J. A. The relative importance of rapid evolution for plant-microbe interactions depends on ecological context. Proc. R. Soc. B Biol. Sci. 281, 20140028 (2014).

    Article 

    Google Scholar 

  • Bradshaw, W. E. & Holzapfel, C. M. Evolutionary response to rapid climate change. Science https://doi.org/10.1126/science.1127000 (2006).

    Article 
    PubMed 

    Google Scholar 

  • Gonzalez, A., Ronce, O., Ferriere, R. & Hochberg, M. E. Evolutionary rescue: an emerging focus at the intersection between ecology and evolution. Philos. Trans. R. Soc. B Biol. Sci. 368, 20120404 (2013).

    Article 

    Google Scholar 

  • Carlson, S. M., Cunningham, C. J. & Westley, P. A. H. Evolutionary rescue in a changing world. Trends Ecol. Evol. 29, 521–530 (2014).

    Article 
    PubMed 

    Google Scholar 

  • Lau, J. A. & terHorst, C. P. Evolutionary responses to global change in species-rich communities. Ann. N. Y. Acad. Sci. 1476, 43–58 (2020).

    Article 
    ADS 
    PubMed 

    Google Scholar 

  • Lau, J. A., Shaw, R. G., Reich, P. B. & Tiffin, P. Indirect effects drive evolutionary responses to global change. New Phytol. 201, 335–343 (2014).

    Article 
    PubMed 

    Google Scholar 

  • Tseng, M. & O’Connor, M. I. Predators modify the evolutionary response of prey to temperature change. Biol. Lett. 11, 20150798 (2015).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • terHorst, C. P. et al. Evolution in a community context: Trait responses to multiple species interactions. Am. Nat. 191, 368–380 (2018).

    Article 

    Google Scholar 

  • Hussa, E. A. & Goodrich-Blair, H. It takes a village: Ecological and fitness impacts of multipartite mutualism. Annu. Rev. Microbiol. 67, 161–178 (2013).

    Article 
    PubMed 

    Google Scholar 

  • Hoegh-Guldberg, O. Climate change, coral bleaching and the future of the world’s coral reefs. Mar. Freshw. Res. 50, 839–866 (1999).

    Google Scholar 

  • Death, G., Fabricius, K. E., Sweatman, H. & Puotinen, M. The 27–year decline of coral cover on the Great Barrier Reef and its causes. PNAS 109, 17995–17999 (2012).

    Article 
    ADS 

    Google Scholar 

  • Heron, S. F., Maynard, J. A., van Hooidonk, R. & Eakin, C. M. Warming trends and bleaching stress of the world’s coral reefs 1985–2012. Sci. Rep. 6, 38402 (2016).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • van Hooidonk, R. et al. Local-scale projections of coral reef futures and implications of the Paris Agreement. Sci Rep 6, 39666 (2016).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Oliver, J. K., Berkelmans, R. & Eakin, C. M. Coral bleaching in space and time. In Coral Bleaching: Patterns, Processes, Causes and Consequences (eds. van Oppen, M. J. H. & Lough, J. M.) 27–49 (Springer, 2018). https://doi.org/10.1007/978-3-540-69775-6_3.

  • Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).

    Article 
    ADS 
    PubMed 

    Google Scholar 

  • Impacts of 1.5°C global warming on natural and human systems. In Global Warming of 1.5°C: IPCC Special Report on Impacts of Global Warming of 1.5°C above Pre-industrial Levels in Context of Strengthening Response to Climate Change, Sustainable Development, and Efforts to Eradicate Poverty (ed. IPCC) 175–312 (Cambridge University Press, 2022). https://doi.org/10.1017/9781009157940.005.

  • Glynn, P. W. & D’Croz, L. Experimental evidence for high temperature stress as the cause of El Niño-coincident coral mortality. Coral Reefs 8, 181–191 (1990).

    Article 
    ADS 

    Google Scholar 

  • Eakin, C. M. et al. Caribbean corals in crisis: Record thermal stress, bleaching, and mortality in 2005. PLoS ONE 5, e13969 (2010).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Eakin, C. M., Sweatman, H. P. A. & Brainard, R. E. The 2014–2017 global-scale coral bleaching event: insights and impacts. Coral Reefs 38, 539–545 (2019).

    Article 
    ADS 

    Google Scholar 

  • Baker, A. C., Starger, C. J., McClanahan, T. R. & Glynn, P. W. Corals’ adaptive response to climate change. Nature 430, 741–741 (2004).

    Article 
    ADS 
    PubMed 

    Google Scholar 

  • Mieog, J. C., Van Oppen, M. J. H., Berkelmans, R., Stam, W. T. & Olsen, J. L. Quantification of algal endosymbionts (Symbiodinium) in coral tissue using real-time PCR. Mol. Ecol. Resour. 9, 74–82 (2009).

    Article 
    PubMed 

    Google Scholar 

  • Silverstein, R. N., Correa, A. M. S. & Baker, A. C. Specificity is rarely absolute in coral–algal symbiosis: Implications for coral response to climate change. Proc. R. Soc. B Biol. Sci. 279, 2609–2618 (2012).

    Article 

    Google Scholar 

  • Hoadley, K. D. et al. Host–symbiont combinations dictate the photo-physiological response of reef-building corals to thermal stress. Sci. Rep. 9, 9985 (2019).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Parkinson, J. E. & Baums, I. B. The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations. Front. Microbiol. 5, 445 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Karim, W., Nakaema, S. & Hidaka, M. Temperature effects on the growth rates and photosynthetic activities of symbiodinium cells. J. Mar. Sci. Eng. 3, 368–381 (2015).

    Article 

    Google Scholar 

  • Grégoire, V., Schmacka, F., Coffroth, M. A. & Karsten, U. Photophysiological and thermal tolerance of various genotypes of the coral endosymbiont Symbiodinium sp. (Dinophyceae). J. Appl. Phycol. 29, 1893 (2017).

    Article 

    Google Scholar 

  • Díaz-Almeyda, E. M. et al. Intraspecific and interspecific variation in thermotolerance and photoacclimation in Symbiodinium dinoflagellates. Proc. R. Soc. B Biol. Sci. 284, 20171767 (2017).

    Article 

    Google Scholar 

  • Bayliss, S. L. J., Scott, Z. R., Coffroth, M. A. & terHorst, C. P. Genetic variation in Breviolum antillogorgium, a coral reef symbiont, in response to temperature and nutrients. Ecol. Evol. 9, 2803–2813 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pelosi, J., Eaton, K. M., Mychajliw, S., terHorst, C. P. & Coffroth, M. A. Thermally tolerant symbionts may explain Caribbean octocoral resilience to heat stress. Coral Reefs 40, 1113–1125 (2021).

    Article 

    Google Scholar 

  • Zilber-Rosenberg, I. & Rosenberg, E. Role of microorganisms in the evolution of animals and plants: The hologenome theory of evolution. Fems Microbiol. Rev. 32, 723–735 (2008).

    Article 
    PubMed 

    Google Scholar 

  • Howells, E. J. et al. Coral thermal tolerance shaped by local adaptation of photosymbionts. Nat. Clim. Chang. 2, 116–120 (2012).

    Article 
    ADS 

    Google Scholar 

  • Chakravarti, L. J., Beltran, V. H. & van Oppen, M. J. H. Rapid thermal adaptation in photosymbionts of reef-building corals. Glob. Chang. Biol. 23, 4675–4688 (2017).

    Article 
    ADS 
    PubMed 

    Google Scholar 

  • Chakravarti, L. J. & van Oppen, M. J. H. Experimental evolution in coral photosymbionts as a tool to increase thermal tolerance. Front. Mar. Sci. 5, 227 (2018).

    Article 

    Google Scholar 

  • Buerger, P. et al. Heat-evolved microalgal symbionts increase coral bleaching tolerance. Sci. Adv. https://doi.org/10.1126/sciadv.aba2498 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hofmann, D. K. & Kremer, B. P. Carbon metabolism and strobilation in Cassiopea andromedea (Cnidaria: Scyphozoa): Significance of endosymbiotic dinoflagellates. Mar. Boil. 65, 25 (1981).

    Article 

    Google Scholar 

  • Welsh, D., Dunn, R. & Meziane, T. Oxygen and nutrient dynamics of the upside down jellyfish (Cassiopea sp.) and its influence on benthic nutrient exchanges and primary production. Hydrobiologia 635, 351 (2009).

    Article 

    Google Scholar 

  • Freeman, C. J., Stoner, E. W., Easson, C. G., Matterson, K. O. & Baker, D. M. Symbiont carbon and nitrogen assimilation in the Cassiopea-Symbiodinium mutualism. Mar. Ecol. Prog. Ser. https://doi.org/10.3354/meps11605 (2016).

    Article 

    Google Scholar 

  • Bigelow, R. P. The Anatomy and Development of Cassiopea xamachana. 1–72 (Pub. by the Boston Society of Natural History, 1900). https://doi.org/10.5962/bhl.title.31420.

  • Colley, N. J. & Trench, R. K. Selectivity in phagocytosis and persistence of symbiotic algae in the scyphistoma stage of the jellyfish Cassiopeia xamachana. Proc. R. Soc. Lond. B Biol. Sci. 219, 61–82 (1983).

    Article 
    ADS 
    PubMed 

    Google Scholar 

  • Hofmann, D. K., Fitt, W. K. & Fleck, J. Checkpoints in the life-cycle of Cassiopea spp.: Control of metagenesis and metamorphosis in a tropical jellyfish. Int. J. Dev. Biol. 40, 331–338 (1996).

    PubMed 

    Google Scholar 

  • Stat, M. & Gates, R. D. Clade D symbiodinium in scleractinian corals: A “Nugget” of hope, a selfish opportunist, an ominous sign, or all of the above?. J. Mar. Biol. 2011, e730715 (2010).

    Google Scholar 

  • Correa, A. M. S. & Baker, A. C. Disaster taxa in microbially mediated metazoans: how endosymbionts and environmental catastrophes influence the adaptive capacity of reef corals. Glob. Change Biol. 17, 68–75 (2011).

    Article 
    ADS 

    Google Scholar 

  • Silverstein, R. N., Cunning, R. & Baker, A. C. Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Glob. Chang. Biol. 21, 236–249 (2015).

    Article 
    ADS 
    PubMed 

    Google Scholar 

  • Leal, M. C. et al. Symbiont type influences trophic plasticity of a model cnidarian-dinoflagellate symbiosis. J. Exp. Biol. 218, 858–863 (2015).

    Article 
    PubMed 

    Google Scholar 

  • Klein, S. G. et al. Symbiodinium mitigate the combined effects of hypoxia and acidification on a noncalcifying cnidarian. Glob. Chang. Biol. 23, 3690–3703 (2017).

    Article 
    ADS 
    PubMed 

    Google Scholar 

  • Cziesielski, M. J. et al. Multi-omics analysis of thermal stress response in a zooxanthellate cnidarian reveals the importance of associating with thermotolerant symbionts. Proc. R. Soc. B. 285, 20172654 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cunning, R. & Baker, A. C. Thermotolerant coral symbionts modulate heat stress-responsive genes in their hosts. Mol. Ecol. 29, 2940–2950 (2020).

    Article 
    PubMed 

    Google Scholar 

  • Newkirk, C. R., Frazer, T. K., Martindale, M. Q. & Schnitzler, C. E. Adaptation to bleaching: Are thermotolerant symbiodiniaceae strains more successful than other strains under elevated temperatures in a model symbiotic cnidarian?. Front. Microbiol. 11, 822 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Trench, R. K. MICROALGAL-INVERTEBRATESYMBIOSES: A REVIEW. Cell Res. 41 (1993).

  • Yellowlees, D., Rees, T. A. V. & Leggat, W. Metabolic interactions between algal symbionts and invertebrate hosts. Plant Cell Environ. 31, 679–694 (2008).

    Article 
    PubMed 

    Google Scholar 

  • Swain, T. D., Chandler, J., Backman, V. & Marcelino, L. Consensus thermotolerance ranking for 110 Symbiodinium phylotypes: an exemplar utilization of a novel iterative partial-rank aggregation tool with broad application potential. Funct. Ecol. 31, 172–183 (2017).

    Article 

    Google Scholar 

  • Klueter, A., Trapani, J., Archer, F. I., McIlroy, S. E. & Coffroth, M. A. Comparative growth rates of cultured marine dinoflagellates in the genus Symbiodinium and the effects of temperature and light. PLoS ONE 12, e0187707 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Chen, B. et al. Dispersal, genetic variation, and symbiont interaction network of heat-tolerant endosymbiont Durusdinium trenchii: Insights into the adaptive potential of coral to climate change. Sci. Total Environ. 723, 138026 (2020).

    Article 
    ADS 
    PubMed 

    Google Scholar 

  • van Oppen, M. J. H., Souter, P., Howells, E. J., Heyward, A. & Berkelmans, R. Novel genetic diversity through somatic mutations: Fuel for adaptation of reef corals?. Diversity 3, 405–423 (2011).

    Article 

    Google Scholar 

  • van Oppen, M. J. H., Oliver, J. K., Putnam, H. M. & Gates, R. D. Building coral reef resilience through assisted evolution. Proc. Natl. Acad. Sci. USA 112, 2307–2313 (2015).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ohdera, A. H. et al. Upside-down but headed in the right direction: Review of the highly versatile Cassiopea xamachana system. Front. Ecol. Evol. 6, 35 (2018).

    Article 

    Google Scholar 

  • Fitt, W. K. & Costley, K. The role of temperature in survival of the polyp stage of the tropical rhizostome jellyfish Cassiopea xamachana. J. Exp. Mar. Biol. Ecol. 222, 79–91 (1998).

    Article 

    Google Scholar 

  • Aljbour, S. M., Zimmer, M. & Kunzmann, A. Cellular respiration, oxygen consumption, and trade-offs of the jellyfish Cassiopea sp. in response to temperature change. Journal of Sea Research 128, 92–97 (2017).

  • Rahat, M. & Adar, O. Effect of symbiotic zooxanthellae and temperature on budding and strobiliation in Cassiopeia andromeda (Eschscholz). Biol. Bull. 159, 394–401 (1980).

    Article 

    Google Scholar 

  • Cole, L. C. The population consequences of life history phenomena. Q. Rev. Biol. 29, 103–137 (1954).

    Article 
    PubMed 

    Google Scholar 

  • Brommer, J. E., Merilä, J. & Kokko, H. Reproductive timing and individual fitness. Ecol. Lett. 5, 802–810 (2002).

    Article 

    Google Scholar 

  • Hofmann, D. K., Neumann, R. & Henne, K. Strobilation, budding and initiation of scyphistoma morphogenesis in the rhizostome Cassiopea andromeda (Cnidaria: Scyphozoa). Mar. Biol. 47, 161–176 (1978).

    Article 

    Google Scholar 

  • Thornhill, D. J., LaJeunesse, T. C., Kemp, D. W., Fitt, W. K. & Schmidt, G. W. Multi-year, seasonal genotypic surveys of coral-algal symbioses reveal prevalent stability or post-bleaching reversion. Mar. Biol. 148, 711–722 (2006).

    Article 

    Google Scholar 

  • Mellas, R. E., McIlroy, S. E., Fitt, W. K. & Coffroth, M. A. Variation in symbiont uptake in the early ontogeny of the upside-down jellyfish, Cassiopea spp.. J. Exp. Mar. Biol. Ecol. 459, 38–44 (2014).

    Article 

    Google Scholar 

  • Fransolet, D., Roberty, S. & Plumier, J.-C. Establishment of endosymbiosis: The case of cnidarians and Symbiodinium. J. Exp. Mar. Biol. Ecol. 420–421, 1–7 (2012).

    Article 

    Google Scholar 

  • Jones, A. M., Berkelmans, R., van Oppen, M. J. H., Mieog, J. C. & Sinclair, W. A community change in the algal endosymbionts of a scleractinian coral following a natural bleaching event: field evidence of acclimatization. Proc. R. Soc. B Biol. Sci. 275, 1359–1365 (2008).

    Article 

    Google Scholar 

  • Baskett, M. L., Gaines, S. D. & Nisbet, R. M. Symbiont diversity may help coral reefs survive moderate climate change. Ecol. Appl. 19, 3–17 (2009).

    Article 
    PubMed 

    Google Scholar 

  • Baker, A. C. Reef corals bleach to survive change. Nature 411, 765–766 (2001).

    Article 
    ADS 
    PubMed 

    Google Scholar 

  • Berkelmans, R. & van Oppen, M. J. H. The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change. Proc. R. Soc. B Biol. Sci. 273, 2305–2312 (2006).

    Article 

    Google Scholar 

  • Davy, S. K., Allemand, D. & Weis, V. M. Cell biology of cnidarian-dinoflagellate symbiosis. Microbiol. Mol. Biol. Rev. 76, 229–261 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wolfowicz, I. et al. Aiptasia sp. larvae as a model to reveal mechanisms of symbiont selection in cnidarians. Sci. Rep. 6, 32366 (2016).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Little, A. F., van Oppen, M. J. H. & Willis, B. L. Flexibility in algal endosymbioses shapes growth in reef corals. Science https://doi.org/10.1126/science.1095733 (2004).

    Article 
    PubMed 

    Google Scholar 

  • Jones, A. & Berkelmans, R. Potential costs of acclimatization to a warmer climate: Growth of a reef coral with heat tolerant vs sensitive symbiont types. PLOS ONE 5, e10437 (2010).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ortiz, J. C., González-Rivero, M. & Mumby, P. J. Can a thermally tolerant symbiont improve the future of Caribbean coral reefs?. Glob. Change Biol. 19, 273–281 (2013).

    Article 
    ADS 

    Google Scholar 

  • Sprouffske, K. & Wagner, A. Growthcurver: An R package for obtaining interpretable metrics from microbial growth curves. BMC Bioinform. 17, 172 (2016).

    Article 

    Google Scholar 


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