• Energy Research

AbstractStudying the mechanisms that enable coral populations to inhabit spatially varying thermal environments can help evaluate how they will respond in time to the effects of global climate change and elucidate the evolutionary forces that enable or constrain adaptation. Inshore reefs in the Florida Keys experience higher temperatures than offshore reefs for prolonged periods during the summer. We conducted a common garden experiment with heat stress as our selective agent to test for local thermal adaptation in corals from inshore and offshore reefs. We show that inshore corals are more tolerant of a 6‐week temperature stress than offshore corals. Compared with inshore corals, offshore corals in the 31 °C treatment showed significantly elevated bleaching levels concomitant with a tendency towards reduced growth. In addition, dinoflagellate symbionts (Symbiodinium sp.) of offshore corals exhibited reduced photosynthetic efficiency. We did not detect differences in the frequencies of major (>5%) haplotypes comprising Symbiodinium communities hosted by inshore and offshore corals, nor did we observe frequency shifts (‘shuffling’) in response to thermal stress. Instead, coral host populations showed significant genetic divergence between inshore and offshore reefs, suggesting that in Porites astreoides, the coral host might play a prominent role in holobiont thermotolerance. Our results demonstrate that coral populations inhabiting reefs <10‐km apart can exhibit substantial differences in their physiological response to thermal stress, which could impact their population dynamics under climate change.

AbstractAs coral reefs continue to decline due to climate change and other stressors, scientists have proposed adopting genomic tools, such as biomarkers, to aid in the conservation and restoration of these threatened ecosystems. Biomarkers are easily measured indicators of biological processes that can be used to predict or diagnose health, resilience, and other key performance metrics. The ultimate goal of developing biomarkers is to determine the conservation value and utility of a given coral colony, including the host animal, its algal symbionts, and their microbial partners. However, this goal remains distant because most efforts have not yet moved beyond the initial discovery phase. We review recent progress in the development of coral molecular biomarkers from a practical standpoint and consider the many challenges that remain as roadblocks to large‐scale implementation. We caution practitioners that, while biomarkers are a promising technology, they are unlikely to be available for field application in the near future barring a rapid shift in research focus from discovery to subsequent validation and field trials. To facilitate such a shift, we propose a stepwise framework to guide additional study in this area, with the aim of accelerating practical molecular biomarker development to enhance coral restoration practice.

AbstractCoral reefs are declining globally as climate change and local water quality press environmental conditions beyond the physiological tolerances of holobionts—the collective of the host and its microbial symbionts. To assess the relationship between symbiont composition and holobiont stress tolerance, community diversity metrics were quantified for dinoflagellate endosymbionts (Family: Symbiodiniaceae) from eight Acropora millepora genets that thrived under or responded poorly to various stressors. These eight selected genets represent the upper and lower tails of the response distribution of 40 coral genets that were exposed to four stress treatments (and control conditions) in a 10‐day experiment. Specifically, four ‘best performer’ coral genets were analyzed at the end of the experiment because they survived high temperature, high pCO2, bacterial exposure, or combined stressors, whereas four ‘worst performer’ genets were characterized because they experienced substantial mortality under these stressors. At the end of the experiment, seven of eight coral genets mainly hosted Cladocopium symbionts, whereas the eighth genet was dominated by both Cladocopium and Durusdinium symbionts. Symbiodiniaceae alpha and beta diversity were higher in worst performing genets than in best performing genets. Symbiont communities in worst performers also differed more after stress exposure relative to their controls (based on normalized proportional differences in beta diversity), than did best performers. A generalized joint attribute model estimated the influence of host genet and treatment on Symbiodiniaceae community composition and identified strong associations among particular symbionts and host genet performance, as well as weaker associations with treatment. Although dominant symbiont physiology and function contribute to host performance, these findings emphasize the importance of symbiont community diversity and stochasticity as components of host performance. Our findings also suggest that symbiont community diversity metrics may function as indicators of resilience and have potential applications in diverse disciplines from climate change adaptation to agriculture and medicine.

A formidable challenge for global change biologists is to predict how natural populations will respond to the emergence of conditions not observed at present, termed novel climates. Popular approaches to predict population vulnerability are based on the expected degree of novelty relative to the amplitude of historical climate fluctuations experienced by a population. Here, we argue that predictions focused on amplitude may be inaccurate because they ignore the predictability of environmental fluctuations in driving patterns of evolution and responses to climate change. To address this disconnect, we review major findings of evolutionary theory demonstrating the conditions under which phenotypic plasticity is likely to evolve in natural populations, and how plasticity decreases population vulnerability to novel environments. We outline key criteria that experimental studies should aim for to effectively test theoretical predictions, while controlling for the degree of climate novelty. We show that such targeted tests of evolutionary theory are rare, with marine systems being overall underrepresented in this venture despite exhibiting unique opportunities to test theory. We conclude that with more robust experimental designs that manipulate both the amplitude and predictability of fluctuations, while controlling for the degree of novelty, we may better predict population vulnerability to climate change.

AbstractLittle is known about the potential for acclimatization or adaptation of corals to ocean acidification and even less about the molecular mechanisms underpinning these processes. Here, we examine global gene expression patterns in corals and their intracellular algal symbionts from two replicate population pairs in Papua New Guinea that have undergone long‐term acclimatization to natural variation in pCO2. In the coral host, only 61 genes were differentially expressed in response to pCO2 environment, but the pattern of change was highly consistent between replicate populations, likely reflecting the core expression homeostasis response to ocean acidification. Functional annotations highlight lipid metabolism and a change in the stress response capacity of corals as key parts of this process. Specifically, constitutive downregulation of molecular chaperones was observed, which may impact response to combined climate change‐related stressors. Elevated CO2 has been hypothesized to benefit photosynthetic organisms but expression changes of in hospite Symbiodinium in response to acidification were greater and less consistent among reef populations. This population‐specific response suggests hosts may need to adapt not only to an acidified environment, but also to changes in their Symbiodinium populations that may not be consistent among environments, adding another challenging dimension to the physiological process of coping with climate change.

As environments are rapidly reshaped due to climate change, phenotypic plasticity plays an important role in the ability of organisms to persist and is considered an especially important acclimatization mechanism for long-lived sessile organisms such as reef-building corals. Often, this ability of a single genotype to display multiple phenotypes depending on the environment is modulated by changes in gene expression, which can vary in response to environmental changes via two mechanisms: baseline expression and expression plasticity. We used transcriptome-wide expression profiling of eleven genotypes of common-gardened Acropora cervicornis to explore genotypic variation in the expression response to thermal and acidification stress, both individually and in combination. We show that the combination of these two stressors elicits a synergistic gene expression response, and that both baseline expression and expression plasticity in response to stress show genotypic variation. Additionally, we demonstrate that frontloading of a large module of coexpressed genes is associated with greater retention of algal symbionts under combined stress. These results illustrate that variation in the gene expression response of individuals to climate change stressors can persist even when individuals have shared environmental histories, affecting their performance under future climate change scenarios.

Despite decades of monitoring global reef decline, we are still largely unable to explain patterns of reef deterioration at local scales, which precludes the development of effective management strategies. Offshore reefs of the Florida Keys, USA, experience milder temperatures and lower nutrient loads in comparison to inshore reefs yet remain considerably more degraded than nearshore patch reefs. A year‐long reciprocal transplant experiment of the mustard hill coral (Porites astreoides) involving four source and eight transplant locations reveals that corals adapt and/or acclimatize to their local habitat on a <10‐km scale. Surprisingly, transplantation to putatively similar environmental types (e.g., offshore corals moved to a novel offshore site, or along‐shore transplantation) resulted in greater reductions in fitness proxies, such as coral growth, than cross‐channel transplantation between inshore and offshore reefs. The only abiotic factor showing significantly greater differences between along‐shore sites was daily temperature range extremes (rather than the absolute high or low temperatures reached), providing a possible explanation for this pattern. Offshore‐origin corals exhibited significant growth reductions at sites with greater daily temperature ranges, which explained up to 39% of the variation in their mass gain. In contrast, daily temperature range explained at most 9% of growth variation in inshore‐origin corals, suggesting that inshore corals are more tolerant of high‐frequency temperature fluctuations. Finally, corals incur trade‐offs when specializing to their native reef. Across reef locations the coefficient of selection against coral transplants was 0.07 ± 0.02 (mean ± SE). This selection against immigrants could hinder the ability of corals to recolonize devastated reefs, whether through assisted migration efforts or natural recruitment events, providing a unifying explanation for observed patterns of coral decline in this reef system.

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.