Many cnidarians host single-celled algae within gastrodermal cells, yielding a mutually beneficial exchange of nutrients between host and symbiont, and dysbiosis can lead to host mortality. Previous research has uncovered symbiosis tradeoffs, including suppression of immune pathways in hosts, and correlations between symbiotic state and pathogen susceptibility. Here, we used a multiomic approach to characterize symbiotic states of the facultatively symbiotic coral Oculina arbuscula by generating genotype-controlled fragments of symbiotic and aposymbiotic tissue. 16S rRNA gene sequencing showed no difference in bacterial communities between symbiotic states. Whole-organism proteomics revealed differential abundance of proteins related to immunity, confirming immune suppression during symbiosis. Single-cell RNAseq identified diverse cell clusters within seven cell types across symbiotic states. Specifically, the gastrodermal cell clusters containing algal-hosting cells from symbiotic tissue had higher expression of nitrogen cycling and lipid metabolism genes than aposymbiotic gastrodermal cells. Furthermore, differential enrichment of immune system gene pathways and lower expression of genes involved in immune regulation were observed in these gastrodermal cells from symbiotic tissue. However, there were no differences in gene expression in the immune cell cluster between symbiotic states. We conclude that there is evidence for compartmentalization of immune system regulation in specific gastrodermal cells in symbiosis. This compartmentalization may limit symbiosis tradeoffs by dampening immunity in algal-hosting cells while simultaneously maintaining general organismal immunity.

The resilience of coral reefs in oligotrophic, (sub)tropical oceans is largely due to the symbiotic relationship between scleractinian corals and Symbiodiniaceae algae, which enables efficient internal nutrient recycling. Investigating the history of this coral symbiosis can provide insights into its role in sustaining the health of both present and future coral reefs. The isotopic composition of organic nitrogen (15N/14N or δ15N) bound within coral skeletons has been utilized to trace the existence of symbiosis in fossil corals, suggesting that coral symbiosis dates back to at least 210 million years ago. The basis of this proxy is that symbiotic corals are expected to exhibit lower δ15N compared to their non-symbiotic (aposymbiotic) counterparts within the same environments, owing to internal nitrogen recycling between the coral host and algal symbiont, and reduced leakage of low-δ15N ammonium into seawater. However, this hypothesis has not been adequately tested in contemporary settings. In a laboratory experiment, we examined the δ15N differences between the symbiotic and aposymbiotic branches within the same genetic backgrounds of the facultatively symbiotic coral Oculina arbuscula under well-fed conditions. Across five different genotypes in two separate experiments, symbiotic branches consistently showed lower δ15N than their aposymbiotic counterparts. These findings corroborate the use of δ15N as a proxy for identifying coral symbiosis in the past, particularly when multiple species of corals coexisted in the same environments.

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 (massive Porites ) 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 harbored Cladocopium C15 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.

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 (massive Porites ) 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 harbored Cladocopium C15 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. ### Competing Interest Statement The authors have declared no competing interest.

Heterotrophy has been shown to mitigate coral-algal dysbiosis (coral bleaching) under heat challenge, but the molecular mechanisms underlying this phenomenon remain largely unexplored. Here, we quantified coral physiology and gene expression of fragments from 13 genotypes of symbiotic Oculina arbuscula after a 28-d feeding experiment under (1) fed, ambient (24 °C); (2) unfed, ambient; (3) fed, heated (ramp to 33 °C); and (4) unfed, heated treatments. We monitored algal photosynthetic efficiency throughout the experiment, and after 28 d, profiled coral and algal carbohydrate and protein reserves, coral gene expression, algal cell densities, and chlorophyll-a and chlorophyll-c2 pigments. Contrary to previous findings, heterotrophy did little to mitigate the impacts of temperature, and we observed few significant differences in physiology between fed and unfed corals under heat challenge. Our results suggest the duration and intensity of starvation and thermal challenge play meaningful roles in coral energetics and stress response; future work exploring these thresholds and how they may impact coral responses under changing climate is urgently needed. Gene expression patterns under heat challenge in fed and unfed corals showed gene ontology enrichment patterns consistent with classic signatures of the environmental stress response. While gene expression differences between fed and unfed corals under heat challenge were subtle: Unfed, heated corals uniquely upregulated genes associated with cell cycle functions, an indication that starvation may induce the previously described, milder "type B" coral stress response. Future studies interested in disentangling the influence of heterotrophy on coral bleaching would benefit from leveraging the facultative species studied here, but using the coral in its symbiotic and aposymbiotic states.

Abstract Genomic methods are becoming increasingly valuable and established in ecological research, particularly in nonmodel species. Supporting their progress and adoption requires investment in resources that promote (i) reproducibility of genomic analyses, (ii) accessibility of learning tools and (iii) keeping pace with rapidly developing methods and principles. We introduce marineomics.io, an open‐source, living document to disseminate tutorials, reproducibility tools and best principles for ecological genomic research in marine and nonmodel systems. The website's existing content spans population and functional genomics, including current recommendations for whole‐genome sequencing, RAD‐seq, Pool‐seq and RNA‐seq. With the goal to facilitate the development of new, similar resources, we describe our process for aggregating and synthesizing methodological principles from the ecological genomics community to inform website content. We also detail steps for authorship and submission of new website content, as well as protocols for providing feedback and topic requests from the community. These web resources were constructed with guidance for doing rigorous, reproducible science. Collaboration and contributions to the website are encouraged from scientists of all skill sets and levels of expertise.

Ocean warming is killing corals, but heat-tolerant populations exist; if protected, they could replenish affected reefs naturally or through restoration. Palau’s Rock Islands experience consistently higher temperatures and extreme heatwaves, yet their diverse coral communities bleach less than those on Palau’s cooler outer reefs. Here, we combined genetic analyses, bleaching histories and growth rates of Porites cf. lobata colonies to identify thermally tolerant genotypes, map their distribution, and investigate potential growth trade-offs. We identified four genetic lineages of P . cf. lobata . On Palau’s outer reefs, a thermally sensitive lineage dominates. The Rock Islands harbor two lineages with enhanced thermal tolerance; one of which shows no consistent growth trade-off and also occurs on several outer reefs. This suggests that the Rock Islands provide naturally tolerant larvae to neighboring areas. Finding and protecting such sources of thermally-tolerant corals is key to reef survival under 21 st century climate change.

ABSTRACT Parental effects can prepare offspring for different environments and facilitate survival across generations. We exposed parental populations of the estuarine anemone, Nematostella vectensis, from Massachusetts to elevated temperatures and quantified larval mortality across a temperature gradient. We found that parental exposure to elevated temperatures resulted in a consistent increase in larval thermal tolerance, as measured by the temperature at which 50% of larvae die (LT50), with a mean increase in LT50 of 0.3°C. Larvae from subsequent spawns returned to baseline thermal thresholds when parents were returned to normal temperatures, indicating plasticity in these parental effects. Histological analyses of gametogenesis in females suggested that these dynamic shifts in larval thermal tolerance may be facilitated by maternal effects in non-overlapping gametic cohorts. We also compared larvae from North Carolina (a genetically distinct population with higher baseline thermal tolerance) and Massachusetts parents, and observed that larvae from heat-exposed Massachusetts parents had thermal thresholds comparable to those of larvae from unexposed North Carolina parents. North Carolina parents also increased larval thermal tolerance under the same high-temperature regime, suggesting that plasticity in parental effects is an inherent trait for N. vectensis. Overall, we find that larval thermal tolerance in N. vectensis shows a strong genetic basis and can be modulated by parental effects. Further understanding of the mechanisms behind these shifts can elucidate the fate of thermally sensitive ectotherms in a rapidly changing thermal environment.

Phenotypic plasticity can serve as a stepping stone towards adaptation. Recently, studies have shown that gene expression contributes to emergent stress responses such as thermal tolerance, with tolerant and susceptible populations showing distinct transcriptional profiles. However, given the dynamic nature of gene expression, interpreting transcriptomic results in a way that elucidates the functional connection between gene expression and the observed stress response is challenging. Here, we present a conceptual framework to guide interpretation of gene expression reaction norms in the context of stress tolerance. We consider the evolutionary and adaptive potential of gene expression reaction norms and discuss the influence of sampling timing, transcriptomic resilience, as well as complexities related to life history when interpreting gene expression dynamics and how these patterns relate to host tolerance. We highlight corals as a case study to demonstrate the value of this framework for non-model systems. As species face rapidly changing environmental conditions, modulating gene expression can serve as a mechanistic link from genetic and cellular processes to the physiological responses that allow organisms to thrive under novel conditions. Interpreting how or whether a species can employ gene expression plasticity to ensure short-term survival will be critical for understanding the global impacts of climate change across diverse taxa.

Success and impact metrics in science are based on a system that perpetuates sexist and racist "rewards" by prioritizing citations and impact factors. These metrics are flawed and biased against already marginalized groups and fail to accurately capture the breadth of individuals' meaningful scientific impacts. We advocate shifting this outdated value system to advance science through principles of justice, equity, diversity, and inclusion. We outline pathways for a paradigm shift in scientific values based on multidimensional mentorship and promoting mentee well-being. These actions will require collective efforts supported by academic leaders and administrators to drive essential systemic change.

As many as 1 billion people across the planet depend on coral reefs for food, coastal protection, cultural practices, and income [1, 2]. Corals, the animals that create these immensely biodiverse habitats, are particularly vulnerable to climate change and inadequately protected. Increasing ocean temperatures leave corals starved as they lose their primary source of food: the photosynthetic algae that live within their tissue. Ocean warming has been impacting coral reefs around the globe for decades, with the latest 2014-2016 heat stress event affecting more than 75% of the world’s corals [3, 4]. Here, we discuss the benefits humans derive from healthy reefs, the threats corals face, and review current policies and management efforts. We also identify management and policy gaps in preserving coral habitats. The gain and urgency of protecting coral reefs is evident from their vast economic and ecological value. Management and restoration efforts are growing across the globe, and many of these have been influential in mitigating local stressors to reefs such as overfishing, nutrient inputs, and water quality. However, the current trajectory of ocean temperatures requires sweeping global efforts to reduce greenhouse gas emissions in order to effectively safeguard the future of coral reefs. The U.S. should stand as a world leader in addressing climate change and in preserving one of the planet’s most valuable ecosystems.

Figure 2 in the original article has been updated with this figure 2 due to discrepancies related to incorrect mapping with one of the islands.

Considerable advances in chronobiology have been made through controlled laboratory studies, but distinct temporal rhythms can emerge under natural environmental conditions. Lab-reared Nematostella vectensis sea anemones exhibit circadian behavioral and physiological rhythms. Given that these anemones inhabit shallow estuarine environments subject to tidal inputs, it was unclear whether circadian rhythmicity would persist following entrainment in natural conditions, or whether circatidal periodicity would predominate. Nematostella were conditioned within a marsh environment, where they experienced strong daily temperature cycles as well as brief tidal flooding around the full and new moons. Upon retrieval, anemones exhibited strong circadian (similar to 24 h) activity rhythms under a light-dark cycle or continuous darkness, but reduced circadian rhythmicity under continuous light. However, some individuals in each light condition showed circadian rhythmicity, and a few individuals showed circatidal rhythmicity. Consistent with the behavioral studies, a large number of transcripts (1640) exhibited diurnal rhythmicity compared with very few (64) with semidiurnal rhythmicity. Diurnal transcripts included core circadian regulators, and 101 of 434 (23%) genes that were previously found to be upregulated by exposure to ultraviolet radiation. Together, these behavioral and transcriptional studies show that circadian rhythmicity predominates and suggest that solar radiation drives physiological cycles in this sediment-dwelling subtidal animal.

The oceans are warming and coral reefs are bleaching with increased frequency and severity, fueling concerns for their survival through this century. Yet in the central equatorial Pacific, some of the world’s most productive reefs regularly experience extreme heat associated with El Niño. Here we use skeletal signatures preserved in long-lived corals on Jarvis Island to evaluate the coral community response to multiple successive heatwaves since 1960. By tracking skeletal stress band formation through the 2015-16 El Nino, which killed 95% of Jarvis corals, we validate their utility as proxies of bleaching severity and show that 2015-16 was not the first catastrophic bleaching event on Jarvis. Since 1960, eight severe (>30% bleaching) and two moderate (<30% bleaching) events occurred, each coinciding with El Niño. While the frequency and severity of bleaching on Jarvis did not increase over this time period, 2015–16 was unprecedented in magnitude. The trajectory of recovery of this historically resilient ecosystem will provide critical insights into the potential for coral reef resilience in a warming world.