Dataset Information

Resistance and robustness of the global coral-symbiont network.

ABSTRACT: Increasing ocean temperatures have widespread consequences for coral reefs, one of which is coral bleaching. We analyzed a global network of associations between coral species and Symbiodiniaceae for resistance to temperature stress and robustness to perturbations. Null networks were created by changing either the physiological parameters of the nodes or the structures of the networks. We developed a bleaching model in which each link, association, is given a weight based on temperature thresholds for specific host-symbiont pairs and links are removed as temperature increases. Resistance to temperature stress was determined from the response of the networks to the bleaching model. Ecological robustness, defined by how much perturbation is needed to decrease the number of nodes by 50%, was determined for multiple removal models that considered traits of the hosts, symbionts, and their associations. Network resistance to bleaching and robustness to perturbations differed from the null networks and varied across spatial scales, supporting that thermal tolerances, local association patterns, and environment play an important role in network persistence. Networks were more robust to attacks on associations than to attacks on species. Although the global network was fairly robust to random link removals, when links are removed according to the bleaching model, robustness decreases by about 20%. Specific environmental attacks, in the form of increasing temperatures, destabilize the global network of coral species and Symbiodiniaceae. On a global scale, the network was more robust to removals of links with susceptible Symbiodiniaceae than it was to removals of links with susceptible hosts. Thus, the symbionts convey more stability to the symbiosis than the hosts when the system is under an environmental attack. However, our results also provide evidence that the environment of the networks affects robustness to link perturbations. Our work shows that ecological resistance and robustness can be assessed through network analysis that considers specific biological traits and functional weaknesses. The global network of associations between corals and Symbiodiniaceae and its distribution of thermal tolerances are non-random, and the evolution of this architecture has led to higher sensitivity to environmental perturbations.

SUBMITTER: Williams SD

PROVIDER: S-EPMC7317464 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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Resistance and robustness of the global coral-symbiont network.

Williams Sara D SD Patterson Mark R MR

Ecology 20200214 5

Increasing ocean temperatures have widespread consequences for coral reefs, one of which is coral bleaching. We analyzed a global network of associations between coral species and Symbiodiniaceae for resistance to temperature stress and robustness to perturbations. Null networks were created by changing either the physiological parameters of the nodes or the structures of the networks. We developed a bleaching model in which each link, association, is given a weight based on temperature threshol ...[more]

PMID: 31961452

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Project description:The complex network of associations between corals and their dinoflagellates (family Symbiodiniaceae) are the basis of coral reef ecosystems but are sensitive to increasing global temperatures. Coral-symbiont interactions are restricted by ecological and evolutionary determinants that constrain partner choice and influence holobiont response to environmental stress; however, little is known about how these processes shape thermal resilience of the holobiont. Here, we built a network of global coral-Symbiodiniaceae associations, mapped species traits (e.g., symbiont transmission mode and biogeography) and phylogenetic relationships of both partners onto the network, and assigned thermotolerance to both host and symbiont nodes. Using network analysis and phylogenetic comparative methods, we determined the contribution of species traits to thermal resilience of the holobiont, while accounting for evolutionary patterns among species. We found that the network shows nonrandom interactions among species, which are shaped by evolutionary history, symbiont transmission mode (horizontally transmitted [HT] or vertically transmitted [VT] corals) and biogeography. Coral phylogeny, but not Symbiodiniaceae phylogeny, symbiont transmission mode, or biogeography, was a good predictor of thermal resilience. Closely related corals have similar Symbiodiniaceae interaction patterns and bleaching susceptibilities. Nevertheless, the association patterns that explain increased host thermal resilience are not generalizable across the entire network but are instead unique to HT and VT corals. Under nonstress conditions, thermally resilient VT coral species associate with thermotolerant phylotypes and limit their number of unique symbionts and overall symbiont thermotolerance diversity, while thermally resilient HT coral species associate with a few host-specific symbiont phylotypes.IMPORTANCE Recent advances have revealed a complex network of interactions between coral and Symbiodiniaceae. Specifically, nonrandom association patterns, which are determined in part by restrictions imposed by symbiont transmission mode, increase the sensitivity of the overall network to thermal stress. However, little is known about the extent to which coral-Symbiodiniaceae network resistance to thermal stress is shaped by host and symbiont species phylogenetic relationships and host and symbiont species traits, such as symbiont transmission mode. We built a frequency-weighted global coral-Symbiodiniaceae network and used network analysis and phylogenetic comparative methods to show that evolutionary relatedness, but not transmission mode, predicts thermal resilience of the coral-Symbiodiniaceae holobiont. Consequently, thermal stress events could result in nonrandom pruning of susceptible lineages and loss of taxonomic diversity with catastrophic effects on community resilience to future events. Our results show that inclusion of the contribution of evolutionary and ecological processes will further our understanding of the fate of coral assemblages under climate change.

Project description: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.

Dataset Information

Resistance and robustness of the global coral-symbiont network.

Publications

Resistance and robustness of the global coral-symbiont network.

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