Article

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

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Abstract

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 F v /F m 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.

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... For example, recent high-throughput approaches for assessing thermal tolerance at the whole coral level (e.g., coral bleaching automated stress systems (CBASS; Voolstra et al., 2020) and single cell levels (Behrendt et al., 2020) have incorporated short thermal challenges followed by stress characterization through the measurement of 1-2 physiological variables such as maximum PSII photochemical efficiency (Fv/Fm) and cell density. While single-phenotype assays can be informative within the context of ecosystem service values (e.g., identifying thermally tolerant corals for nursery propagation; Cunning et al., 2021), identification of functionally distinct Symbiodiniaceae phenotypes will benefit from measuring a broader spectrum of physiological metrics (Hoadley et al., 2021). Phenotypic characterization using multiple photosynthetic metrics can provide some species-specific resolution (Suggett et al., 2015), and the non-invasive nature of chlorophyll a fluorometry lends itself to high-throughput approaches. ...
... Single-cell transcriptomics (i.e., isolating individual cells and sequencing their transcriptomes) could solve this issue as gene expression could be explored within and among each symbiont cell in hospite. The generation of a cell atlas for the coral Stylophora pistillata enabled the characterization of fine-scale metabolic interactions between symbionts and host gastrodermal cells (Levy et al., 2021). Single-cell sequencing can also enable high-resolution interrogations of how Symbiodiniaceae and host cells interact during symbiosis establishment, maintenance, and breakdown, particularly when Symbiodiniaceae cells can be isolated from different parts of the host coral that exhibit contrasting physiologies. ...
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Within microeukaryotes, genetic and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians (e.g., corals, octocorals, sea anemones, jellies), other marine invertebrates (e.g., sponges, molluscs, flatworms), and protists (e.g., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.
... Restoration practitioners have been forced to focus on stop-gap measures to ensure that at least some coral species persist into the future (National Academies of Sciences Engineering and Medicine, 2018). Key examples include establishing nurseries wherein corals can be grown and later outplanted onto reefs (Young et al., 2012), identifying heat-tolerant individuals for nursery propagation (Cunning et al., 2021), and facilitating the natural ability of corals to adapt through interventions like assisted gene flow (Baums et al., 2019). ...
... In addition to observing how evolution "plays out" in natural populations by screening corals from these populations for variability with respect to resilience or susceptibility to stress, there is an opportunity to identify highly resilient individuals (genotypes) or populations that may be useful for studying the molecular basis of evolved stress tolerance and for conservation efforts. This approach has already proven successful in identifying resilient coral in other reefs (Brown et al. 2020;Cunning et al. 2021). However, the isolated, simpler nature of the Hawaiian Islands system should enable relatively tractable approaches to determine how stress tolerant individuals are distributed and maintained across the Archipelago. ...
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Degradation and loss of coral reefs due to climate change and other anthropogenic stressors has fueled genomics, proteomics, and genetics research to investigate coral stress response pathways and to identify resilient species, genotypes, and populations to restore these biodiverse ecosystems. Much of the research and conservation effort has understandably focused on the most taxonomically rich regions, such as the Great Barrier Reef in Australia and the Coral Triangle in the western Pacific. These ecosystems are analogous to tropical rainforests that also house enormous biodiversity and complex biotic interactions among different trophic levels. An alternative model ecosystem for studying coral reef biology is the relatively species poor but abundant coral reefs in the Hawaiian Archipelago that exist at the northern edge of the Indo‐Pacific coral distribution. The Hawaiian Islands are the world's most isolated archipelago, geographically isolated from other Pacific reef systems. This region houses about 80 species of scleractinian corals in three dominant genera (Porites, Montipora, and Pocillopora). Here we briefly review knowledge about the Hawaiian coral fauna with a focus on our model species, the rice coral Montipora capitata. We suggest that this simpler, relatively isolated reef system provides an ideal platform for advancing coral biology and conservation using multi‐omics and genetic tools.
... This is an application where corals from hotspots of coral resilience that have enhanced tolerance to persist under anticipated future climate conditions can be targeted as potential source populations for restoration [117]. Rapid stress testing [126,127], reciprocal transplantation experimentation [116,128], phenotyping assays and biomarkers [129] are some of the current tools available to guide selection of stress tolerant individuals for restoration. Inclusion of naturally stress tolerant corals in propagation efforts may increase the long-term likelihood of survival and reduce wasted efforts by practitioners [117]. ...
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Reducing the global reliance on fossil fuels is essential to ensure the long-term survival of coral reefs, but until this happens, alternative tools are required to safeguard their future. One emerging tool is to locate areas where corals are surviving well despite the changing climate. Such locations include refuges, refugia, hotspots of resilience, bright spots, contemporary near-pristine reefs, and hope spots that are collectively named reef ‘safe havens' in this mini-review. Safe havens have intrinsic value for reefs through services such as environmental buffering, maintaining near-pristine reef conditions, or housing corals naturally adapted to future environmental conditions. Spatial and temporal variance in physicochemical conditions and exposure to stress however preclude certainty over the ubiquitous long-term capacity of reef safe havens to maintain protective service provision. To effectively integrate reef safe havens into proactive reef management and contingency planning for climate change scenarios, thus requires an understanding of their differences, potential values, and predispositions to stress. To this purpose, I provide a high-level review on the defining characteristics of different coral reef safe havens, how they are being utilised in proactive reef management and what risk and susceptibilities they inherently have. The mini-review concludes with an outline of the potential for reef safe haven habitats to support contingency planning of coral reefs under an uncertain future from intensifying climate change.
... This approach has been shown to determine differences in coral thermotolerance similarly to a classic longterm heat stress assay Evensen et al., 2021). We chose to use this 1-day ramp-hold assay in 2019 rather than repeat the 2014-style assay due to the logistical advantage of a 1-day assay and to be more comparable to recent studies using CBASS Cunning et al., 2021;Evensen et al., 2021;Savary et al., 2021). This assay consists of four replicate tanks to test three experimental temperature treatments and one control, for a total of eight tanks. ...
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Determining the adaptive potential of foundation species, such as reef-building corals, is urgent as the oceans warm and coral populations decline. Theory predicts that corals may adapt to climate change via selection on standing genetic variation. Yet, corals face not only rising temperatures but also novel diseases. We studied the interaction between two major stressors affecting colonies of the threatened coral, Acropora cervicornis: white-band disease and high water temperature. We determined that 27% of A. cervicornis were disease resistant prior to a thermal anomaly. However, disease resistance was largely lost during a bleaching event because of more compromised coral hosts or increased pathogenic dose/virulence. There was no tradeoff between disease resistance and temperature tolerance; disease susceptibility was independent of Symbiodinium strain. The present study shows that susceptibility to temperature stress creates an increased risk in disease-associated mortality, and only rare genets may maintain or gain infectious disease resistance under high temperature. We conclude that A. cervicornis populations in the lower Florida Keys harbor few existing genotypes that are resistant to both warming and disease.
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Population genomic surveys suggest that climate-associated genetic variation occurs widely across species, but whether it is sufficient to allow population persistence via evolutionary adaptation has seldom been quantified. To ask whether rapid adaptation in reef-building corals can keep pace with future ocean warming, we measured genetic variation at predicted warm-adapted loci and simulated future evolution and persistence in a high-latitude population of corals from Rarotonga, Cook Islands. Alleles associated with thermal tolerance were present but at low frequencies in this cooler, southerly locality. Simulations based on predicted ocean warming in Rarotonga showed rapid evolution of heat tolerance resulting in population persistence under mild warming scenarios consistent with low CO2 emission plans, RCP2.6 and RCP4.5. Under more severe scenarios, RCP6.0 and RCP8.5, adaptation was not rapid enough to prevent extinction. Population adaptation was faster for models based on smaller numbers of additive loci that determine thermal tolerance and for higher population growth rates. Finally, accelerated migration via transplantation of thermally tolerant individuals (1 to 5%/year) sped adaptation. These results show that cool-water corals can adapt to warmer oceans but only under mild scenarios resulting from international emissions controls. Incorporation of genomic data into models of species response to climate change offers a promising method for estimating future adaptive processes.
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Coral gardening plays an important role in the recovery of depleted populations of threatened Acropora cervicornis in the Caribbean. Over the past decade, high survival coupled with fast growth of in situ nursery corals have allowed practitioners to create healthy and genotypically diverse nursery stocks. Currently, thousands of corals are propagated and outplanted onto degraded reefs on a yearly basis, representing a substantial increase in the abundance, biomass, and overall footprint of A. cervicornis. Here, we combined an extensive dataset collected by restoration practitioners to document early (1–2 yr) restoration success metrics in Florida and Puerto Rico, USA. By reporting region-specific data on the impacts of fragment collection on donor colonies, survivorship and productivity of nursery corals, and survivorship and productivity of outplanted corals during normal conditions, we provide the basis for a stop-light indicator framework for new or existing restoration programs to evaluate their performance. We show that current restoration methods are very effective, that no excess damage is caused to donor colonies, and that once outplanted, corals behave just as wild colonies. We also provide science-based benchmarks that can be used by programs to evaluate successes and challenges of their efforts, and to make modifications where needed. We propose that up to 10% of the biomass can be collected from healthy, large A. cervicornis donor colonies for nursery propagation. We also propose the following benchmarks for the first year of activities for A. cervicornis restoration: (1) >75% live tissue cover on donor colonies; (2) >80% survivorship of nursery corals; and (3) >70% survivorship of outplanted corals. Finally, we report productivity means of 4.4 cm yr⁻¹ for nursery corals and 4.8 cm yr⁻¹ for outplants as a frame of reference for ranking performance within programs. Such benchmarks, and potential subsequent adaptive actions, are needed to fully assess the long-term success of coral restoration and species recovery programs.
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Concern over rapid environmental shifts associated with climate change has led to a search for molecular markers of environmental tolerance. Climate‐associated gene expression profiles exist for a number of systems, but have rarely been tied to fitness outcomes, especially in nonmodel organisms. We reciprocally transplanted corals between two backreef locations with more and less variable temperature regimes to disentangle effects of recent and native environment on survival and growth. Coral growth over 12 months was largely determined by local environment. Survival, however, was impacted by native environment; corals from the more variable environment had 22% higher survivorship. By contrast, corals native to the less variable environment had more variable survival. This might represent a “selective sieve” where poor survivors are filtered from the more stressful environment. We also find a potential fitness trade‐off—corals with high survival under stressful conditions grew less in the more benign environment. Transcriptome samples taken a year before transplantation were used to examine gene expression patterns that predicted transplant survival and growth. Two separate clusters of coexpressed genes were predictive of survival in the two locations. Genes from these clusters are candidate biomarkers for predicting persistence of corals under future climate change scenarios.
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The relationship between the coral genotype and the environment is an important area of research in degraded coral reef ecosystems. We used a reciprocal outplanting experiment with 930 corals representing ten genotypes on each of eight reefs to investigate the influence of genotype and the environment on growth and survivorship in the threatened Caribbean staghorn coral, Acropora cervicornis. Coral genotype and site were strong drivers of coral growth and individual genotypes exhibited flexible, non-conserved reaction norms, complemented by ten-fold differences in growth between specific G-E combinations. Growth plasticity may diminish the influence of local adaptation, where foreign corals grew faster than native corals at their home sites. Novel combinations of environment and genotype also significantly affected disturbance response during and after the 2015 bleaching event, where these factors acted synergistically to drive variation in bleaching and recovery. Importantly, small differences in temperature stress elicit variable patterns of survivorship based on genotype and illustrate the importance of novel combinations of coral genetics and small differences between sites representing habitat refugia. In this context, acclimatization and flexibility is especially important given the long lifespan of corals coping with complex environmental change. The combined influence of site and genotype creates short-term differences in growth and survivorship, contributing to the standing genetic variation needed for adaptation to occur over longer timescales and the recovery of degraded reefs through natural mechanisms.
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Reef restoration activities have proliferated in response to the need to mitigate coral declines and recover lost reef structure, function, and ecosystem services. Here, we describe the recent shift from costly and complex engineering solutions to recover degraded reef structure to more economical and efficient ecological approaches that focus on recovering the living components of reef communities. We review the adoption and expansion of the coral gardening framework in the Caribbean and Western Atlantic where practitioners now grow and outplant 10,000’s of corals onto degraded reefs each year. We detail the steps for establishing a gardening program as well as long-term goals and direct and indirect benefits of this approach in our region. With a strong scientific basis, coral gardening activities now contribute significantly to reef and species recovery, provide important scientific, education, and outreach opportunities, and offer alternate livelihoods to local stakeholders. While challenges still remain, the transition from engineering to ecological solutions for reef degradation has opened the field of coral reef restoration to a wider audience poised to contribute to reef conservation and recovery in regions where coral losses and recruitment bottlenecks hinder natural recovery.
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In preparation for a large-scale coral restoration project, we surveyed host population genetic structure and symbiont diversity of two reef-building corals in four reef zones along the Florida reef tract (FRT). There was no evidence for coral population subdivision along the FRT in Acropora cervicornis or Montastraea faveolata based on microsatellite markers. However, in A. cervicornis, significant genetic differentiation was apparent when extending the analysis to broader scales (Caribbean). Clade diversity of the zooxanthellae differed along the FRT. A. cervicornis harbored mostly clade A with clade D zooxanthellae being prominent in colonies growing inshore and in the mid-channel zones that experience greater temperature fluctuations and receive significant nutrient and sediment input. M. faveolata harbored a more diverse array of symbionts, and variation in symbiont diversity among four habitat zones was more subtle but still significant. Implications of these results are discussed for ongoing restoration and conservation work. KeywordsMexico-Bahamas-Honduras- Acropora cervicornis - Montastraea faveolata - Symbiodinium Clade D
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Dose-response analysis can be carried out using multi-purpose commercial statistical software, but except for a few special cases the analysis easily becomes cumbersome as relevant, non-standard output requires manual programming. The extension package drc for the statistical environment R provides a flexible and versatile infrastructure for dose-response analyses in general. The present version of the package, reflecting extensions and modifications over the last decade, provides a user-friendly interface to specify the model assumptions about the dose-response relationship and comes with a number of extractors for summarizing fitted models and carrying out inference on derived parameters. The aim of the present paper is to provide an overview of state-of-the-art dose-response analysis, both in terms of general concepts that have evolved and matured over the years and by means of concrete examples.
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Naturally extreme temperature environments can provide important insights into the processes underlying coral thermal tolerance. We determined the bleaching resistance of Acropora aspera and Dipsastraea sp. from both intertidal and subtidal environments of the naturally extreme Kimberley region in northwest Australia. Here tides of up to 10 m can cause aerial exposure of corals and temperatures as high as 37 °C that fluctuate daily by up to 7 °C. Control corals were maintained at ambient nearshore temperatures which varied diurnally by 4-5 °C, while treatment corals were exposed to similar diurnal variations and heat stress corresponding to ~20 degree heating days. All corals hosted Symbiodinium clade C independent of treatment or origin. Detailed physiological measurements showed that these corals were nevertheless highly sensitive to daily average temperatures exceeding their maximum monthly mean of ~31 °C by 1 °C for only a few days. Generally, Acropora was much more susceptible to bleaching than Dipsastraea and experienced up to 75% mortality, whereas all Dipsastraea survived. Furthermore, subtidal corals, which originated from a more thermally stable environment compared to intertidal corals, were more susceptible to bleaching. This demonstrates that while highly fluctuating temperatures enhance coral resilience to thermal stress, they do not provide immunity to extreme heat stress events.
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The capacity of coral-dinoflagellate mutualisms to adapt to a changing climate relies in part on standing variation in host and symbiont populations, but rarely have the interactions between symbiotic partners been considered at the level of individuals. Here, we tested the importance of inter-individual variation with respect to the physiology of coral holobionts. We identified six genetically distinct Acropora palmata coral colonies that all shared the same isoclonal Symbiodinium 'fitti' dinoflagellate strain. No other Symbiodinium could be detected in host tissues. We exposed fragments of each colony to extreme cold and found that the stress-induced change in symbiont photochemical efficiency varied up to 3.6-fold depending on host genetic background. The S. 'fitti' strain was least stressed when associating with hosts that significantly altered the expression of 184 genes under cold shock; it was most stressed in hosts that only adjusted 14 genes. Key expression differences among hosts were related to redox signaling and iron availability pathways. Fine-scale interactions among unique host colonies and symbiont strains provide an underappreciated source of raw material for natural selection in coral symbioses.
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As global warming continues, reef-building corals could avoid local population declines through “genetic rescue” involving exchange of heat-tolerant genotypes across latitudes, but only if latitudinal variation in thermal tolerance is heritable. Here, we show an up–to–10-fold increase in odds of survival of coral larvae under heat stress when their parents come from a warmer lower-latitude location. Elevated thermal tolerance was associated with heritable differences in expression of oxidative, extracellular, transport, and mitochondrial functions that indicated a lack of prior stress. Moreover, two genomic regions strongly responded to selection for thermal tolerance in interlatitudinal crosses. These results demonstrate that variation in coral thermal tolerance across latitudes has a strong genetic basis and could serve as raw material for natural selection.
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a r t i c l e i n f o The calcification and extension rates of two species of scleractinian coral (Montastraea cavernosa, Porites astreoides) were measured in corals experimentally transplanted to paired inshore and offshore locations in the Upper, Middle, and Lower Florida Keys from 2010 to 2011. Growth rates were compared with respect to 1) shelf location, 2) species, 3) region, and 4) temperature. Transplanted corals on inshore reefs generally calcified less than those at paired offshore sites, but these differences were only significant in a few cases. This difference in growth is likely because of two thermal stress events that occurred inshore, but not offshore, as growth records from cores of P. astreoides revealed significantly higher extension and calcification inshore from 2001–2013. The core data confirmed that the years 2010–2012 were a period of depressed growth inshore. Calcification and extension rates of the experimental corals were not statistically different between M. cavernosa and P. astreoides within a given site. The only exceptions were that calcification was higher in M. cavernosa at the Middle Keys inshore site. The Middle Florida Keys sites had the lowest rates of calcification, supporting the hypothesis that the influence of Florida Bay waters in this region contributes to poor reef development. Mean calcification rates negatively correlated with metrics of cold stress in M. cavernosa and heat stress in P. astreoides. The lack of a significant correlation between heat stress and mean calcification in M. cavernosa may help explain this species persistence on today's reefs. Maximum calcification and mean extension, however, were negatively correlated with maximum running 30-day mean temperature, showing that the growth of M. cavernosa is not completely insensitive to warm water stress. The 'weedy' life-history strategy of P. astreoides may compensate for the sensitivity of calcification rates to heat stress reported here, allowing this species to maintain the stable populations that have been observed throughout Florida and the wider Caribbean. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
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The genetic enhancement of wild animals and plants for characteristics that benefit human populations has been practiced for thousands of years, resulting in impressive improvements in commercially valuable species. Despite these benefits, genetic manipulations are rarely considered for noncommercial purposes, such as conservation and restoration initiatives. Over the last century, humans have driven global climate change through industrialization and the release of increasing amounts of CO2, resulting in shifts in ocean temperature, ocean chemistry, and sea level, as well as increasing frequency of storms, all of which can profoundly impact marine ecosystems. Coral reefs are highly diverse ecosystems that have suffered massive declines in health and abundance as a result of these and other direct anthropogenic disturbances. There is great concern that the high rates, magnitudes, and complexity of environmental change are overwhelming the intrinsic capacity of corals to adapt and survive. Although it is important to address the root causes of changing climate, it is also prudent to explore the potential to augment the capacity of reef organisms to tolerate stress and to facilitate recovery after disturbances. Here, we review the risks and benefits of the improvement of natural and commercial stocks in noncoral reef systems and advocate a series of experiments to determine the feasibility of developing coral stocks with enhanced stress tolerance through the acceleration of naturally occurring processes, an approach known as (human)-assisted evolution, while at the same time initiating a public dialogue on the risks and benefits of this approach.
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Coral reef restoration has gained recent popularity in response to the steady decline of corals and the recognition that coral reefs may not be able to recover naturally without human intervention. To synthesize collective knowledge about reef restoration focused particularly on the threatened genus Acropora in the Caribbean and western Atlantic, we conducted a literature review combined with personal communications with restoration practitioners and an online questionnaire to identify the most effective reef restoration methods and the major obstacles hindering restoration success. Most participants (90%) strongly believe that Acropora populations are severely degraded, continue to decline, and may not recover without human intervention. Low-cost methods such as coral gardening and fragment stabilization were ranked as the most effective restoration activities for this genus. High financial costs, the small footprint of restoration activities, and the potential damage to wild populations were identified as major concerns, while increased public awareness and education were ranked as the highest benefits of coral reef restoration. This study highlights the advantages and outlines the concerns associated with coral reef restoration and creates a unique synthesis of coral restoration activities as a complementary management tool to help guide “best-practices” for future restoration efforts throughout the region.
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Reef corals are highly sensitive to heat, yet populations resistant to climate change have recently been identified. To determine the mechanisms of temperature tolerance, we reciprocally transplanted corals between reef sites experiencing distinct temperature regimes and tested subsequent physiological and gene expression profiles. Local acclimatization and fixed effects, such as adaptation, contributed about equally to heat tolerance and are reflected in patterns of gene expression. In less than 2 years, acclimatization achieves the same heat tolerance that we would expect from strong natural selection over many generations for these long-lived organisms. Our results show both short-term acclimatory and longer-term adaptive acquisition of climate resistance. Adding these adaptive abilities to ecosystem models is likely to slow predictions of demise for coral reef ecosystems.
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Sexual propagation of corals specifically for reef rehabilitation remains largely experimental. In this study, we refined low technology culture and transplanta-tion approaches and assessed the role of colony size and age, at time of transfer from nursery to reef, on subsequent survival. Larvae from Acropora millepora were reared from gametes and settled on engineered substrates, called coral plug-ins, that were designed to simplify transplanta-tion to areas of degraded reef. Plug-ins, with laboratory spawned and settled coral recruits attached, were main-tained in nurseries until they were at least 7 months old before being transplanted to replicate coral limestone out-crops within a marine protected area until they were 31 months old. Survival rates of transplanted corals that remained at the protected in situ nursery the longest were 3.9–5.6 times higher than corals transplanted to the reef earlier, demonstrating that an intermediate ocean nursery stage is critical in the sexual propagation of corals for reef rehabilitation. 3 years post-settlement, colonies were reproductively mature, making this one of few published studies to date to rear a broadcasting scleractinian from eggs to spawning adults. While our data show that it is technically feasible to transplant sexually propagated cor-als and rear them until maturity, producing a single 2.5-year-old coral on the reef cost at least US$60. 'What if' scenarios indicate that the cost per transplantable coral could be reduced by almost 80 %, nevertheless, it is likely that the high cost per coral using sexual propagation methods would constrain delivery of new corals to rela-tively small scales in many countries with coral reefs.
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Rising ocean temperatures associated with global climate change are causing mass coral bleaching and mortality worldwide. Understanding the genetic and environmental factors that mitigate coral bleaching susceptibility may aid local management efforts to help coral reefs survive climate change. Although bleaching susceptibility depends partly on the genetic identity of a coral's algal symbionts, the effect of symbiont density, and the factors controlling it, remain poorly understood. By applying a new metric of symbiont density to study the coral Pocillopora damicornis during seasonal warming and acute bleaching, we show that symbiont cell ratio density is a function of both symbiont type and environmental conditions, and that corals with high densities are more susceptible to bleaching. Higher vulnerability of corals with more symbionts establishes a quantitative mechanistic link between symbiont density and the molecular basis for coral bleaching, and indicates that high densities do not buffer corals from thermal stress, as has been previously suggested. These results indicate that environmental conditions that increase symbiont densities, such as nutrient pollution, will exacerbate climate-change-induced coral bleaching, providing a mechanistic explanation for why local management to reduce these stressors will help coral reefs survive future warming.
Article
Marine heat waves are increasing in magnitude, duration, and frequency as a result of climate change and are the principal global driver of mortality in reef‐building corals. Resilience‐based genetic management may increase coral heat tolerance, but it is unclear how temperature responses are regulated at the genome level and thus how corals may adapt to warming naturally or through selective breeding. Here we combine phenotypic, pedigree, and genomic marker data from colonies sourced from a warm reef on the Great Barrier Reef reproductively crossed with conspecific colonies from a cooler reef to produce combinations of warm purebreds and warm‐cool hybrid larvae and juveniles. Inter‐population breeding created significantly greater genetic diversity across the coral genome compared to breeding between populations and maintained diversity in key regions associated with heat tolerance and fitness. High‐density genome‐wide scans of single nucleotide polymorphisms (SNPs) identified alleles significantly associated with larval families reared at 27.5°C (87 – 2,224 loci), including loci putatively associated with proteins involved in responses to heat stress (cell membrane formation, metabolism, and immune responses). Underlying genetics of these families explained 43% of PCoA multilocus variation in survival, growth, and bleaching responses at 27.5°C and 31°C at the juvenile stage. Genetic marker contribution to total variation in fitness traits (narrow‐sense heritability) was high for survival but not for growth and bleaching in juveniles, with heritability of these traits being higher at 31°C relative to 27.5°C. While based on only a limited number of crosses, the mechanistic understanding presented here demonstrates that allele frequencies are affected by one generation of selective breeding, key information for the assessments of genetic intervention feasibility and modelling of reef futures.
Article
Coral reefs are under extreme threat due to a number of stressors, but temperature increases due to changing climate are the most severe. Rising ocean temperatures coupled with local extremes lead to extensive ‘bleaching’, where the coral‐algal symbiosis breaks down and corals may die, compromising the structure and function of reefs. Although the symbiotic nature of the coral colony has historically been a focus of research on coral resilience, the host itself is a foundational component in the response to thermal stress. Fixed effects in the coral host set trait baselines through evolutionary processes, acting on many loci of small effect to create mosaics of thermal tolerance across latitudes and individual coral reefs. These genomic differences can be strongly heritable, producing wide variation among clones of different genotypes or families of a specific larval cross. Phenotypic plasticity is overlaid on these baselines and a growing body of knowledge demonstrates the potential for acclimatization of reef‐building corals through a variety of mechanisms that promote resilience and stress tolerance. The long‐term persistence of coral reefs will require many of these mechanisms to adjust to warmer temperatures within a generation, bridging the gap to reproductive events that allow recombination of standing diversity and adaptive change. Business‐as‐usual climate scenarios will likely lead to the loss of some coral populations or species in the future, so the interaction between intragenerational effects and evolutionary pressure is critical for the survival of reefs.
Article
Climate change threatens organisms in a variety of interactive ways that requires simultaneous adaptation of multiple traits. Predicting evolutionary responses requires an understanding of the potential for interactions among stressors and the genetic variance and covariance among fitness‐related traits that may reinforce or constrain an adaptive response. Here we investigate the capacity of Acropora millepora, a reef‐building coral, to adapt to multiple environmental stressors: rising sea surface temperature, ocean acidification, and increased prevalence of infectious diseases. We measured growth rates (weight gain), coral color (a proxy for Symbiodiniaceae density), and survival, in addition to nine physiological indicators of coral and algal health in 40 coral genets exposed to each of these three stressors singly and combined. Individual stressors resulted in predicted responses (e.g., corals developed lesions after bacterial challenge and bleached under thermal stress). However, corals did not suffer substantially more when all three stressors were combined. Nor were tradeoffs observed between tolerances to different stressors; instead, individuals performing well under one stressor also tended to perform well under every other stressor. An analysis of genetic correlations between traits revealed positive co‐variances, suggesting that selection to multiple stressors will reinforce rather than constrain the simultaneous evolution of traits related to holobiont health (e.g., weight gain and algal density). These findings support the potential for rapid coral adaptation under climate change and emphasize the importance of accounting for corals’ adaptive capacity when predicting the future of coral reefs. This article is protected by copyright. All rights reserved.
Article
Scleractinian corals occur in tropical regions near their upper thermal limits and are severely threatened by rising ocean temperatures. However, several recent studies have shown coral populations can harbor genetic variation in thermal tolerance. Here we have extended these approaches to study heat tolerance of corals in the Persian/Arabian Gulf, where heat‐tolerant local populations experience extreme summer temperatures (up to 36°C). To evaluate whether selection has depleted genetic variation in thermal tolerance, estimate potential future adaptive responses and understand the functional basis for these corals’ unusual heat tolerance, we conducted controlled crosses in the Gulf coral Platygyra daedalea. Heat tolerance is highly heritable in this population (h²=0.487‐0.748), suggesting substantial potential for adaptive responses to selection for elevated temperatures. To identify genetic markers associated with this variation, we conducted genome‐wide SNP genotyping in parental corals and tested for relationships between paternal genotype and offspring thermal tolerance. Resulting multilocus SNP genotypes explained a large fraction of variation in thermal tolerance in these crosses (69%). To investigate the functional basis of these differences in thermal tolerance, we profiled transcriptional responses in tolerant and susceptible families, revealing substantial sire effects on transcriptional responses to thermal stress. We also studied sequence variation in these expressed sequences, identifying alleles and functional groups of differentially expressed genes associated with thermal tolerance. Our findings demonstrate that corals in this population harbor extensive genetic variation in thermal tolerance, and heat‐tolerant phenotypes differ in both gene sequences and transcriptional stress responses from their susceptible counterparts. This article is protected by copyright. All rights reserved.
Book
This new edition to the classic book by ggplot2 creator Hadley Wickham highlights compatibility with knitr and RStudio. ggplot2 is a data visualization package for R that helps users create data graphics, including those that are multi-layered, with ease. With ggplot2, it's easy to: • produce handsome, publication-quality plots with automatic legends created from the plot specification • superimpose multiple layers (points, lines, maps, tiles, box plots) from different data sources with automatically adjusted common scales • add customizable smoothers that use powerful modeling capabilities of R, such as loess, linear models, generalized additive models, and robust regression • save any ggplot2 plot (or part thereof) for later modification or reuse • create custom themes that capture in-house or journal style requirements and that can easily be applied to multiple plots • approach a graph from a visual perspective, thinking about how each component of the data is represented on the final plot This book will be useful to everyone who has struggled with displaying data in an informative and attractive way. Some basic knowledge of R is necessary (e.g., importing data into R). ggplot2 is a mini-language specifically tailored for producing graphics, and you'll learn everything you need in the book. After reading this book you'll be able to produce graphics customized precisely for your problems, and you'll find it easy to get graphics out of your head and on to the screen or page. New to this edition:< • Brings the book up-to-date with ggplot2 1.0, including major updates to the theme system • New scales, stats and geoms added throughout • Additional practice exercises • A revised introduction that focuses on ggplot() instead of qplot() • Updated chapters on data and modeling using tidyr, dplyr and broom
Article
Many ecosystems around the world are rapidly deteriorating due to both local and global pressures, and perhaps none so precipitously as coral reefs. Management of coral reefs through maintenance (e.g., marine-protected areas, catchment management to improve water quality), restoration, as well as global and national governmental agreements to reduce greenhouse gas emissions (e.g., the 2015 Paris Agreement) is critical for the persistence of coral reefs. Despite these initiatives, the health and abundance of corals reefs are rapidly declining and other solutions will soon be required. We have recently discussed options for using assisted evolution (i.e., selective breeding, assisted gene flow, conditioning or epigenetic programming, and the manipulation of the coral microbiome) as a means to enhance environmental stress tolerance of corals and the success of coral reef restoration efforts. The 2014–2016 global coral bleaching event has sharpened the focus on such interventionist approaches. We highlight the necessity for consideration of alternative (e.g., hybrid) ecosystem states, discuss traits of resilient corals and coral reef ecosystems, and propose a decision tree for incorporating assisted evolution into restoration initiatives to enhance climate resilience of coral reefs.
Article
Although genetic diversity is recognized as an important consideration for coral restoration, genotypes for use in restoration are not typically selected based on an evaluation of phenotype. Systematic documentation of phenotypic variability within coral nurseries could inform restoration efforts. To quantify differences in phenotype, ten known genotypes of Acropora cervicornis in an established coral nursery in the Florida Keys were selected for study. Twelve 5-cm replicate colonies of each genotype were individually tagged for identification and suspended from four identical PVC tree structures within the nursery for grow-out. Total linear extension (TLE) and number of branches were measured at approximately 45-day intervals for a period of 13 months. Buoyant weight was determined for each colony initially and after five and 13 months in order to quantify calcification. Sub-lethal bleaching was observed among experimental colonies following a natural thermal stress event, and significant differences in bleaching prevalence were present among genotypes. At the conclusion of the study, significant differences in all growth parameters were detected among genotypes. Specific growth rate across genotypes decreased following bleaching. The ratio of buoyant weight to TLE varied among genotypes and decreased with increasing TLE, suggesting a potential tradeoff between extension and skeletal density in nursery-reared A. cervicornis. Phenotypic variation documented in this study has implications for nursery management and may be useful in selecting genotypes for A. cervicornis population enhancement.
Article
As ocean warming causes more frequent and severe coral bleaching worldwide, it is critical to identify biotic and abiotic factors that promote bleaching resistance and recovery. In October 2014, many colonies of the key reef-building coral Montipora capitata in Ka ̄ ne‘ohe Bay, O‘ahu, Hawai‘i, USA, were severely bleached, while others appeared unaffected. To elucidate the role of symbiotic algae in these contrasting responses and study subsequent patterns of recovery, we tracked abundances (symbiont to host cell ratios) of clade C and D Symbiodinium for 6 mo in 10 bleached and 10 non-bleached colonies at 3 reefs in the northern, central, and southern regions of Ka ̄ ne‘ohe Bay (n = 60 colonies) using quantitative PCR. Bleaching resistance was significantly associated with the dominant symbiont clade. All bleached colonies (n = 30) were dominated by clade C symbionts, while many non-bleached colonies (n = 16) were dominated by thermotolerant clade D. However, clade C Symbiodinium dominated 14 other colonies that did not bleach, indi- cating that an alternate mechanism such as host genetic adaptation may play a role in thermal tol- erance of these colonies. Bleached corals recovered their symbionts within 1−3 mo (excepting 1 mortality) and remained C-dominated. However, colonies recovered 3 times faster at the northern reef, which experiences similar temperature but lower irradiance and higher water flow and turn- over compared to the southern reef. This work indicates that both biotic (e.g. symbiont and host genotypic) and abiotic (e.g. hydrodynamic) factors influence the natural resistance and recovery of M. capitata, which can inform ecological predictions and conservation strategies for coral reefs under climate change.
Article
Luxuriant growths of reef-building corals and associated biota are characteristic of easterly facing margins of the Florida and Bahamas platforms. Along the eastern margins the reef community is most luxuriant and continuous seaward of islands; it is absent or poorly developed where islands are absent. The reef community is absent along almost all the western margins of the platforms and its few occurrences seaward of islands or shoals are small, discontinuous, and without the variety and vitality of the eastern examples. The reef community favors the eastern margins because wave agitation and circulation of oceanic water that promotes its growth is more intense there than on the western margins. The western margins are unfavorable because water from the platform interiors, warmer and saltier than normal, is moved westward across them by the prevailing easterly winds. The most luxuriant growths of the reef community are seaward of islands because the islands protect these areas from unfavorable currents. The islands prevent the existence of the normal cross-platform currents that produce bottom-sediment movement (oolitic sands) unfavorable for the reef community. The islands shield areas seaward of them from tidal runoff of platform-interior water that is inimical to the growth of the reef community. Can these "principles" be applied to ancient reefs? End_of_Article - Last_Page 527------------
Article
Mutualistic organisms can be particularly susceptible to climate change stress, as their survivorship is often limited by the most vulnerable partner. However, symbiotic plasticity can also help organisms in changing environments by expanding their realized niche space. Coral-algal (Symbiodinium spp.) symbiosis exemplifies this dichotomy: the partnership is highly susceptible to “bleaching” (stress-induced symbiosis breakdown), but stress-tolerant symbionts can also sometimes mitigate bleaching. Here, we investigate the role of diverse and mutable symbiotic partnerships in increasing corals’ ability to thrive in high temperature conditions. We conducted repeat bleaching and recovery experiments on the coral Montastraea cavernosa, and used quantitative PCR and chlorophyll fluorometry to assess the structure and function of Symbiodinium communities within coral hosts. During an initial heat exposure (32°C for 10 days), corals hosting only stress-sensitive symbionts (Symbiodinium C3) bleached, but recovered (at either 24°C or 29°C) with predominantly (>90%) stress-tolerant symbionts (Symbiodinium D1a), which were not detected before bleaching (either due to absence or extreme low abundance). When a second heat stress (also 32°C for 10 days) was applied 3 months later, corals that previously bleached and were now dominated by D1a Symbiodinium experienced less photodamage and symbiont loss compared to control corals that had not been previously bleached, and were therefore still dominated by Symbiodinium C3. Additional corals that were initially bleached without heat by a herbicide (DCMU, at 24°C) also recovered predominantly with D1a symbionts, and similarly lost fewer symbionts during subsequent thermal stress. Increased thermotolerance was not observed in C3-dominated corals that were acclimated for three months to warmer temperatures (29°C) before heat stress. These findings indicate that increased thermotolerance post-bleaching resulted from symbiont community composition changes, not prior heat exposure. Moreover, initially undetectable D1a symbionts became dominant only after bleaching, and were critical to corals’ resilience after stress and resistance to future stress.This article is protected by copyright. All rights reserved.
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