Census of heat tolerance among Florida's threatened staghorn corals finds resilient individuals throughout existing nursery populations.

The rapid loss of reef-building corals owing to ocean warming is driving the development of interventions such as coral propagation and restoration, selective breeding and assisted gene flow. Many of these interventions target naturally heat-tolerant individuals to boost climate resilience, but the challenges of quickly and reliably quantifying heat tolerance and identifying thermotolerant individuals have hampered implementation. Here, we used coral bleaching automated stress systems to perform rapid, standardized heat tolerance assays on 229 colonies of Acropora cervicornis across six coral nurseries spanning Florida's Coral Reef, USA. Analysis of heat stress dose-response curves for each colony revealed a broad range in thermal tolerance among individuals (approx. 2.5°C range in Fv/Fm ED50), with highly reproducible rankings across independent tests (r = 0.76). Most phenotypic variation occurred within nurseries rather than between them, pointing to a potentially dominant role of fixed genetic effects in setting thermal tolerance and widespread distribution of tolerant individuals throughout the population. The identification of tolerant individuals provides immediately actionable information to optimize nursery and restoration programmes for Florida's threatened staghorn corals. This work further provides a blueprint for future efforts to identify and source thermally tolerant corals for conservation interventions worldwide.

Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic.

Active coral restoration typically involves two interventions: crossing gametes to facilitate sexual larval propagation; and fragmenting, growing, and outplanting adult colonies to enhance asexual propagation. From an evolutionary perspective, the goal of these efforts is to establish self-sustaining, sexually reproducing coral populations that have sufficient genetic and phenotypic variation to adapt to changing environments. Here, we provide concrete guidelines to help restoration practitioners meet this goal for most Caribbean species of interest. To enable the persistence of coral populations exposed to severe selection pressure from many stressors, a mixed provenance strategy is suggested: genetically unique colonies (genets) should be sourced both locally as well as from more distant, environmentally distinct sites. Sourcing three to four genets per reef along environmental gradients should be sufficient to capture a majority of intraspecies genetic diversity. It is best for practitioners to propagate genets with one or more phenotypic traits that are predicted to be valuable in the future, such as low partial mortality, high wound healing rate, high skeletal growth rate, bleaching resilience, infectious disease resilience, and high sexual reproductive output. Some effort should also be reserved for underperforming genets because colonies that grow poorly in nurseries sometimes thrive once returned to the reef and may harbor genetic variants with as yet unrecognized value. Outplants should be clustered in groups of four to six genets to enable successful fertilization upon maturation. Current evidence indicates that translocating genets among distant reefs is unlikely to be problematic from a population genetic perspective but will likely provide substantial adaptive benefits. Similarly, inbreeding depression is not a concern given that current practices only raise first-generation offspring. Thus, proceeding with the proposed management strategies even in the absence of a detailed population genetic analysis of the focal species at sites targeted for restoration is the best course of action. These basic guidelines should help maximize the adaptive potential of reef-building corals facing a rapidly changing environment.

Subtle Differences in Symbiont Cell Surface Glycan Profiles Do Not Explain Species-Specific Colonization Rates in a Model Cnidarian-Algal Symbiosis.

Mutualisms between cnidarian hosts and dinoflagellate endosymbionts are foundational to coral reef ecosystems. These symbioses are often re-established every generation with high specificity, but gaps remain in our understanding of the cellular mechanisms that control symbiont recognition and uptake dynamics. Here, we tested whether differences in glycan profiles among different symbiont species account for the different rates at which they initially colonize aposymbiotic polyps of the model sea anemone Aiptasia (Exaiptasia pallida). First, we used a lectin array to characterize the glycan profiles of colonizing Symbiodinium minutum (ITS2 type B1) and noncolonizing Symbiodinium pilosum (ITS2 type A2), finding subtle differences in the binding of lectins Euonymus europaeus lectin (EEL) and Urtica dioica agglutinin lectin (UDA) that distinguish between high-mannoside and hybrid-type protein linked glycans. Next, we enzymatically cleaved glycans from the surfaces of S. minutum cultures and followed their recovery using flow cytometry, establishing a 48-72 h glycan turnover rate for this species. Finally, we exposed aposymbiotic host polyps to cultured S. minutum cells masked by EEL or UDA lectins for 48 h, then measured cell densities the following day. We found no effect of glycan masking on symbiont density, providing further support to the hypothesis that glycan-lectin interactions are more important for post-phagocytic persistence of specific symbionts than they are for initial uptake. We also identified several methodological and biological factors that may limit the utility of studying glycan masking in the Aiptasia system.

Gene Expression Variation Resolves Species and Individual Strains among Coral-Associated Dinoflagellates within the Genus Symbiodinium.

Reef-building corals depend on symbiotic mutualisms with photosynthetic dinoflagellates in the genus Symbiodinium. This large microalgal group comprises many highly divergent lineages ("Clades A-I") and hundreds of undescribed species. Given their ecological importance, efforts have turned to genomic approaches to characterize the functional ecology of Symbiodinium. To date, investigators have only compared gene expression between representatives from separate clades-the equivalent of contrasting genera or families in other dinoflagellate groups-making it impossible to distinguish between clade-level and species-level functional differences. Here, we examined the transcriptomes of four species within one Symbiodinium clade (Clade B) at ∼20,000 orthologous genes, as well as multiple isoclonal cell lines within species (i.e., cultured strains). These species span two major adaptive radiations within Clade B, each encompassing both host-specialized and ecologically cryptic taxa. Species-specific expression differences were consistently enriched for photosynthesis-related genes, likely reflecting selection pressures driving niche diversification. Transcriptional variation among strains involved fatty acid metabolism and biosynthesis pathways. Such differences among individuals are potentially a major source of physiological variation, contributing to the functional diversity of coral holobionts composed of unique host-symbiont genotype pairings. Our findings expand the genomic resources available for this important symbiont group and emphasize the power of comparative transcriptomics as a method for studying speciation processes and interindividual variation in nonmodel organisms.

The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations.

Reef-building corals owe much of their success to a symbiosis with dinoflagellate microalgae in the genus Symbiodinium. In this association, the performance of each organism is tied to that of its partner, and together the partners form a holobiont that can be subject to selection. Climate change affects coral reefs, which are declining globally as a result. Yet the extent to which coral holobionts will be able to acclimate or evolve to handle climate change and other stressors remains unclear. Selection acts on individuals and evidence from terrestrial systems demonstrates that intraspecific genetic diversity plays a significant role in symbiosis ecology and evolution. However, we have a limited understanding of the effects of such diversity in corals. As molecular methods have advanced, so too has our recognition of the taxonomic and functional diversity of holobiont partners. Resolving the major components of the holobiont to the level of the individual will help us assess the importance of intraspecific diversity and partner interactions in coral-algal symbioses. Here, we hypothesize that unique combinations of coral and algal individuals yield functional diversity that affects not only the ecology and evolution of the coral holobiont, but associated communities as well. Our synthesis is derived from reviewing existing evidence and presenting novel data. By incorporating the effects of holobiont extended phenotypes into predictive models, we may refine our understanding of the evolutionary trajectory of corals and reef communities responding to climate change.

A genetics-based description of Symbiodinium minutum sp. nov. and S. psygmophilum sp. nov. (Dinophyceae), two dinoflagellates symbiotic with cnidaria.

Traditional approaches for describing species of morphologically cryptic and often unculturable forms of endosymbiotic dinoflagellates are problematic. Two new species in the genus Symbiodinium Freudenthal 1962 are described using an integrative evolutionary genetics approach: Symbiodinium minutum sp. nov. are harbored by widespread tropical anemones in the genus Aiptasia; and Symbiodinium psygmophilum sp. nov. are harbored by subtropical and temperate stony corals (e.g., Astrangia, Cladocora, and Oculina) from the Atlantic Ocean and Mediterranean Sea. Both new species are readily distinguished from each other by phylogenetic disparity and reciprocal monophyly of several nucleic acid sequences including nuclear ribosomal internal transcribed spacers 1 and 2, single copy microsatellite flanker Sym15, mitochondrial cytochrome b, and the chloroplast 23S rRNA gene. Such molecular evidence, combined with well-defined differences in cell size, physiology (thermal tolerance), and ecology (host compatibility) establishes these organisms as distinct species. Future descriptions of Symbiodinium spp. will need to emphasize genetics-based descriptions because significant morphological overlap in this group obscures large differences in ecology and evolutionary divergence. By using molecular evidence based on conserved and rapidly evolving genes analyzed from a variety of samples, species boundaries are defined under the precepts of Evolutionary and Biological Species Concepts without reliance on an arbitrary genetic distance metric. Because ecological specialization arises through genetic adaptations, the Ecological Species Concept can also serve to delimit many host-specific Symbiodinium spp.