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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. 

Abstract Increasing ocean temperatures are causing dysbiosis between coral hosts and their symbionts. Previous work suggests that coral host gene expression responds more strongly to environmental stress compared to their intracellular symbionts; however, the causes and consequences of this phenomenon remain untested. We hypothesized that symbionts are less responsive because hosts modulate symbiont environments to buffer stress. To test this hypothesis, we leveraged the facultative symbiosis between the scleractinian coralOculina arbusculaand its symbiontBreviolum psygmophilumto characterize gene expression responses of both symbiotic partners in and ex hospite under thermal challenges. To characterize host and in hospite symbiont responses, symbiotic and aposymbioticO. arbusculawere exposed to three treatments: (1) control (18°C), (2) heat (32°C), and (3) cold (6°C). This experiment was replicated withB. psygmophilumcultured fromO. arbusculato characterize ex hospite symbiont responses. Both thermal challenges elicited classic environmental stress responses (ESRs) inO. arbuscularegardless of symbiotic state, with hosts responding more strongly to cold challenge. Hosts also exhibited stronger responses than in hospite symbionts. In and ex hospiteB. psygmophilumboth down‐regulated gene ontology pathways associated with photosynthesis under thermal challenge; however, ex hospite symbionts exhibited greater gene expression plasticity and differential expression of genes associated with ESRs. Taken together, these findings suggest thatO. arbusculahosts may buffer environments ofB. psygmophilumsymbionts; however, we outline the future work needed to confirm this hypothesis.