The role and risks of selective adaptation in extreme coral habitats

Scucchia, Federica; Zaslansky, Paul; Boote, Chloë; Doheny, Annabelle; Mass, Tali; Camp, Emma F.

doi:10.1038/s41467-023-39651-7

Cited by 6 publications

(2 citation statements)

References 96 publications

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“…One important question remaining is whether there are tradeoffs to the increased thermal tolerance in lineages of massive Porites. For example, colonies of massive Porites from extreme mangrove habitat had lower gene expression variation, reduced skeletal density, and increased porosity compared to populations on "classic" reefs (Scucchia et al, 2023). In Palau, Rivera et al, (2022) found that L3 had lower skeletal density, calcification, and extension rates than the other lineages.…”

Section: Response Variation Among Holobiont Lineages To Thermal Chall...mentioning

confidence: 99%

Distinct modes of holobiont specialization among cryptic coral lineages

Grupstra,

Meyer-Kaiser,

Bennett

et al. 2024

Preprint

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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), clouding interpretation of the drivers of thermal tolerance. Here, we leverage a holobiont (massivePorites) with high host-partner fidelity 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). Two lineages were more closely related to populations ∼4300 km away, suggesting that these lineages are widespread. All corals harboredCladocopiumC15 photobionts, but strain-level compositions differed among lineages and reef types. L1 associated with distinct photobionts and bacteria in each reef type, whereas L2 had relatively stable associations. L3 hosted unique photobiont strains, signaling high host-photobiont fidelity. Analysis of light harvesting capacity and thermal tolerance revealed key adaptive variation underpinning survival in distinct habitats. L1 had the highest light absorption efficiency and lowest thermal tolerance, suggesting 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, signaling habitat generalism, potentially explaining how it survives well in both habitat types. 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; uncovering thermally-tolerant holobionts can strengthen our understanding of coral evolution and symbiosis, and support global conservation and restoration efforts.

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Section: Response Variation Among Holobiont Lineages To Thermal Chall...mentioning

confidence: 99%

Distinct modes of holobiont specialization among cryptic coral lineages

Grupstra,

Meyer-Kaiser,

Bennett

et al. 2024

Preprint

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“…This severe bleaching event was the first to be recorded after 2016, when a mass coral bleaching event impacted entire reefs in New Caledonia [ 40 ], while only a mild paling of corals was observed in Bouraké (Rodolfo-Metalpa, in situ observations). There is increasing work being undertaken to reveal diverse strategies undertaken by these corals to survive under chronic disturbances [ 20 , 33 , 38 , 41 , 42 ], yet what intraspecific stress-induced physiological response of extreme corals (i.e., corals that live at the edge of their environmental limits [ 43 , 44 ], occur during a stress event remains entirely unexplored.…”

Section: Introductionmentioning

confidence: 99%

Algal symbiont diversity in Acropora muricata from the extreme reef of Bouraké associated with resistance to coral bleaching

Alessi,

Lemonnier,

Camp

et al. 2024

PLoS ONE

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Widespread coral bleaching has generally been linked to high water temperatures at larger geographic scales. However, the bleaching response can be highly variable among individual of the same species, between different species, and across localities; what causes this variability remains unresolved. Here, we tracked bleached and non-bleached colonies of Acropora muricata to see if they recovered or died following a stress event inside the semi-enclosed lagoon of Bouraké (New Caledonia), where corals are long-term acclimatized to extreme conditions of temperature, pH and dissolved oxygen, and at a nearby control reef where conditions are more benign. We describe Symbiodiniaceae community changes based on next-generation sequencing of the ITS2 marker, metabolic responses, and energetic reserve measures (12 physiological traits evaluated) during the La Niña warm and rainy summer in 2021. Widespread coral bleaching (score 1 and 2 on the coral colour health chart) was observed only in Bouraké, likely due to the combination of the high temperatures (up to 32°C) and heavy rain. All colonies (i.e., Bouraké and reference site) associated predominantly with Symbiodinaceae from the genera Cladocopium. Unbleached colonies in Bouraké had a specific ITS2-type profile (proxies for Symbiodiniaceae genotypes), while the bleached colonies in Bouraké had the same ITS2-type profile of the reef control colonies during the stress event. After four months, the few bleached colonies that survived in Bouraké (B2) acquired the same ITS2 type profiles of the unbleached colonies in Bouraké. In terms of physiological performances, all bleached corals showed metabolic depression (e.g., Pgross and Rdark). In contrast, unbleached colonies in Bouraké maintained higher metabolic rates and energetic reserves compared to control corals. Our study suggests that Acropora muricata enhanced their resistance to bleaching thanks to specific Symbiodiniaceae associations, while energetic reserves may increase their resilience after stress.

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The role and risks of selective adaptation in extreme coral habitats

et al. 2023

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The alarming rate of climate change demands new management strategies to protect coral reefs. Environments such as mangrove lagoons, characterized by extreme variations in multiple abiotic factors, are viewed as potential sources of stress-tolerant corals for strategies such as assisted evolution and coral propagation. However, biological trade-offs for adaptation to such extremes are poorly known. Here, we investigate the reef-building coral Porites lutea thriving in both mangrove and reef sites and show that stress-tolerance comes with compromises in genetic and energetic mechanisms and skeletal characteristics. We observe reduced genetic diversity and gene expression variability in mangrove corals, a disadvantage under future harsher selective pressure. We find reduced density, thickness and higher porosity in coral skeletons from mangroves, symptoms of metabolic energy redirection to stress response functions. These findings demonstrate the need for caution when utilizing stress-tolerant corals in human interventions, as current survival in extremes may compromise future competitive fitness.

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The role and risks of selective adaptation in extreme coral habitats

Cited by 6 publications

References 96 publications

Distinct modes of holobiont specialization among cryptic coral lineages

Distinct modes of holobiont specialization among cryptic coral lineages

Algal symbiont diversity in Acropora muricata from the extreme reef of Bouraké associated with resistance to coral bleaching

The role and risks of selective adaptation in extreme coral habitats

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