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Abstract Reef‐building corals in the genusPoritesare one of the most important constituents of Indo‐Pacific reefs. Many species within this genus tolerate abnormally warm water and exhibit high specificity for particular kinds of endosymbiotic dinoflagellates that cope with thermal stress better than those living in other corals. Still, during extreme ocean heating, somePoritesexhibit differences in their stress tolerance. While corals have different physiological qualities, it remains unknown whether the stability and performance of these mutualisms is influenced by the physiology and genetic relatedness of their symbionts. We investigated two ubiquitous Pacific reef corals,Porites rusandPorites cylindrica, from warmer inshore and cooler offshore reef systems in Palau. While these corals harbored a similar kind of symbiont in the genusCladocopium(within the ITS2C15 subclade), rapidly evolving genetic markers revealed evolutionarily diverged lineages corresponding to eachPoritesspecies living in each reef habitat. Furthermore, these closely relatedCladocopiumlineages were differentiated by their densities in host tissues, cell volume, chlorophyll concentration, gross photosynthesis, and photoprotective pathways. When assessed using several physiological proxies, these previously undifferentiated symbionts contrasted in their tolerance to thermal stress. Symbionts withinP.cylindricawere relatively unaffected by exposure to 32℃ for 14 days, whereasP.ruscolonies lost substantial numbers of photochemically compromised symbionts. Heating reduced the ability of the offshore symbiont associated withP.rusto translocate carbon to the coral. By contrast, high temperatures enhanced symbiont carbon assimilation and delivery to the coral skeleton of inshoreP.cylindrica. This study indicates that large physiological differences exist even among closely related symbionts, with significant implications for thermal susceptibility among reef‐buildingPorites.
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Holobiont Traits Shape Climate Change Responses in Cryptic Coral Lineages
ABSTRACT As ocean warming threatens reefs worldwide, identifying corals with adaptations to higher temperatures is critical for conservation. Genetically distinct but morphologically similar (i.e. cryptic) coral populations can be specialized to extreme habitats and thrive under stressful conditions. These corals often associate with locally beneficial microbiota (Symbiodiniaceae photobionts and bacteria), obscuring the main drivers of thermal tolerance. Here, we leverage a holobiont (massivePorites) with high fidelity for C15 photobionts to investigate adaptive variation across classic (“typical” conditions) and extreme reefs characterized by higher temperatures and light attenuation. We uncovered three cryptic lineages that exhibit limited micro‐morphological variation; one lineage dominated classic reefs (L1), one had more even distributions (L2), and a third was restricted to extreme reefs (L3). L1 and L2 were more closely related to populations ~4300 km away, suggesting that some lineages are widespread. All corals harboredCladocopiumC15 photobionts; L1 and L2 shared a photobiont pool that differed in composition between reef types, yet L3 mostly harbored unique photobiont strains not found in the other lineages. Assemblages of bacterial partners differed among reef types in lineage‐specific ways, suggesting that lineages employ distinct microbiome regulation strategies. Analysis of light‐harvesting capacity and thermal tolerance revealed adaptive variation underpinning survival in distinct habitats: L1 had the highest light absorption efficiency and lowest thermal tolerance, suggesting that it is a classic reef specialist. L3 had the lowest light absorption efficiency and the highest thermal tolerance, showing that it is an extreme reef specialist. L2 had intermediate light absorption efficiency and thermal tolerance, suggesting that is a generalist lineage. These findings reveal diverging holobiont strategies to cope with extreme conditions. Resolving coral lineages is key to understanding variation in thermal tolerance among coral populations, can strengthen our understanding of coral evolution and symbiosis, and support global conservation and restoration efforts.
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- Award ID(s):
- 2048678
- PAR ID:
- 10574268
- Publisher / Repository:
- Wiley
- Date Published:
- Journal Name:
- Global Change Biology
- Volume:
- 30
- Issue:
- 11
- ISSN:
- 1354-1013
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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