Intersection of coral molecular responses to a localized mortality event and ex situ deoxygenation.

In July 2016, East Bank of Flower Garden Banks (FGB) National Marine Sanctuary experienced a localized mortality event (LME) of multiple invertebrate species that ultimately led to reductions in coral cover. Abiotic data taken directly after the event suggested that acute deoxygenation contributed to the mortality. Despite the large impact of this event on the coral community, there was no direct evidence that this LME was driven by acute deoxygenation, and thus we explored whether gene expression responses of corals to the LME would indicate what abiotic factors may have contributed to the LME. Gene expression of affected and unaffected corals sampled during the mortality event revealed evidence of the physiological consequences of the LME on coral hosts and their algal symbionts from two congeneric species (Orbicella franksi and Orbicella faveolata). Affected colonies of both species differentially regulated genes involved in mitochondrial regulation and oxidative stress. To further test the hypothesis that deoxygenation led to the LME, we measured coral host and algal symbiont gene expression in response to ex situ experimental deoxygenation (control = 6.9 ± 0.08 mg L-1, anoxic = 0.083 ± 0.017 mg L-1) in healthy O. faveolata colonies from the FGB. However, this deoxygenation experiment revealed divergent gene expression patterns compared to the corals sampled during the LME and was more similar to a generalized coral environmental stress response. It is therefore likely that while the LME was connected to low oxygen, it was a series of interconnected stressors that elicited the unique gene expression responses observed here. These in situ and ex situ data highlight how field responses to stressors are unique from those in controlled laboratory conditions, and that the complexities of deoxygenation events in the field likely arise from interactions between multiple environmental factors simultaneously.

Symbiosis modulates gene expression of symbionts, but not coral hosts, under thermal challenge.

Increasing ocean temperatures are causing dysbiosis between coral hosts and their symbionts. Previous work suggests that coral host gene expression responds more strongly to environmental stress compared to their intracellular symbionts; however, the causes and consequences of this phenomenon remain untested. We hypothesized that symbionts are less responsive because hosts modulate symbiont environments to buffer stress. To test this hypothesis, we leveraged the facultative symbiosis between the scleractinian coral Oculina arbuscula and its symbiont Breviolum psygmophilum to characterize gene expression responses of both symbiotic partners in and ex hospite under thermal challenges. To characterize host and in hospite symbiont responses, symbiotic and aposymbiotic O. arbuscula were exposed to three treatments: (1) control (18°C), (2) heat (32°C), and (3) cold (6°C). This experiment was replicated with B. psygmophilum cultured from O. arbuscula to characterize ex hospite symbiont responses. Both thermal challenges elicited classic environmental stress responses (ESRs) in O. arbuscula regardless of symbiotic state, with hosts responding more strongly to cold challenge. Hosts also exhibited stronger responses than in hospite symbionts. In and ex hospite B. psygmophilum both down-regulated gene ontology pathways associated with photosynthesis under thermal challenge; however, ex hospite symbionts exhibited greater gene expression plasticity and differential expression of genes associated with ESRs. Taken together, these findings suggest that O. arbuscula hosts may buffer environments of B. psygmophilum symbionts; however, we outline the future work needed to confirm this hypothesis.

Integrating cryptic diversity into coral evolution, symbiosis and conservation.

Understanding how diversity evolves and is maintained is critical to predicting the future trajectories of ecosystems under climate change; however, our understanding of these processes is limited in marine systems. Corals, which engineer reef ecosystems, are critically threatened by climate change, and global efforts are underway to conserve and restore populations as attempts to mitigate ocean warming continue. Recently, sequencing efforts have uncovered widespread undescribed coral diversity, including 'cryptic lineages'-genetically distinct but morphologically similar coral taxa. Such cryptic lineages have been identified in at least 24 coral genera spanning the anthozoan phylogeny and across ocean basins. These cryptic lineages co-occur in many reef systems, but their distributions often differ among habitats. Research suggests that cryptic lineages are ecologically specialized and several examples demonstrate differences in thermal tolerance, highlighting the critical implications of this diversity for predicting coral responses to future warming. Here, we draw attention to recent discoveries, discuss how cryptic diversity affects the study of coral adaptation and acclimation to future environments, explore how it shapes symbiotic partnerships, and highlight challenges and opportunities for conservation and restoration efforts.

Distinct Phenotypes Associated with Mangrove and Lagoon Habitats in Two Widespread Caribbean Corals, Porites astreoides and Porites divaricata.

AbstractAs coral reefs experience dramatic declines in coral cover throughout the tropics, there is an urgent need to understand the role that non-reef habitats, such as mangroves, play in the ecological niche of corals. Mangrove habitats present a challenge to reef-dwelling corals because they can differ dramatically from adjacent reef habitats with respect to key environmental parameters, such as light. Because variation in light within reef habitats is known to drive intraspecific differences in coral phenotype, we hypothesized that coral species that can exploit both reef and mangrove habitats will exhibit predictable differences in phenotypes between habitats. To investigate how intraspecific variation, driven by either local adaptation or phenotypic plasticity, might enable particular coral species to exploit these two qualitatively different habitat types, we compared the phenotypes of two widespread Caribbean corals, Porites divaricata and Porites astreoides, in mangrove versus lagoon habitats on Turneffe Atoll, Belize. We document significant differences in colony size, color, structural complexity, and corallite morphology between habitats. In every instance, the phenotypic differences between mangrove prop root and lagoon corals exhibited consistent trends in both P. divaricata and P. astreoides. We believe this study is the first to document intraspecific phenotypic diversity in corals occupying mangrove prop root versus lagoonal patch reef habitats. A difference in the capacity to adopt an alternative phenotype that is well suited to the mangrove habitat may explain why some reef coral species can exploit mangroves, while others cannot.

A framework for understanding gene expression plasticity and its influence on stress tolerance.

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.

Adaptive divergence, neutral panmixia, and algal symbiont population structure in the temperate coral Astrangia poculata along the Mid-Atlantic United States.

Astrangia poculata is a temperate scleractinian coral that exists in facultative symbiosis with the dinoflagellate alga Breviolum psygmophilum across a range spanning the Gulf of Mexico to Cape Cod, Massachusetts. Our previous work on metabolic thermal performance of Virginia (VA) and Rhode Island (RI) populations of A. poculata revealed physiological signatures of cold (RI) and warm (VA) adaptation of these populations to their respective local thermal environments. Here, we used whole-transcriptome sequencing (mRNA-Seq) to evaluate genetic differences and identify potential loci involved in the adaptive signature of VA and RI populations. Sequencing data from 40 A. poculata individuals, including 10 colonies from each population and symbiotic state (VA-white, VA-brown, RI-white, and RI-brown), yielded a total of 1,808 host-associated and 59 algal symbiont-associated single nucleotide polymorphisms (SNPs) post filtration. Fst outlier analysis identified 66 putative high outlier SNPs in the coral host and 4 in the algal symbiont. Differentiation of VA and RI populations in the coral host was driven by putatively adaptive loci, not neutral divergence (Fst = 0.16, p = 0.001 and Fst = 0.002, p = 0.269 for outlier and neutral SNPs respectively). In contrast, we found evidence of neutral population differentiation in B. psygmophilum (Fst = 0.093, p = 0.001). Several putatively adaptive host loci occur on genes previously associated with the coral stress response. In the symbiont, three of four putatively adaptive loci are associated with photosystem proteins. The opposing pattern of neutral differentiation in B. psygmophilum, but not the A. poculata host, reflects the contrasting dynamics of coral host and algal symbiont population connectivity, dispersal, and gene by environment interactions.

Nearshore coral growth declining on the Mesoamerican Barrier Reef System.

Anthropogenic global change and local stressors are impacting coral growth and survival worldwide, altering the structure and function of coral reef ecosystems. Here, we show that skeletal extension rates of nearshore colonies of two abundant and widespread Caribbean corals (Siderastrea siderea, Pseudodiploria strigosa) declined across the Belize Mesoamerican Barrier Reef System (MBRS) over the past century, while offshore coral conspecifics exhibited relatively stable extension rates over the same temporal interval. This decline has caused nearshore coral extension rates to converge with those of their historically slower growing offshore coral counterparts. For both species, individual mass coral bleaching events were correlated with low rates of skeletal extension within specific reef environments, but no single bleaching event was correlated with low skeletal extension rates across all reef environments. We postulate that the decline in skeletal extension rates for nearshore corals is driven primarily by the combined effects of long-term ocean warming and increasing exposure to higher levels of land-based anthropogenic stressors, with acute thermally induced bleaching events playing a lesser role. If these declining trends in skeletal growth of nearshore S. siderea and P. strigosa continue into the future, the structure and function of these critical nearshore MBRS coral reef systems is likely to be severely impaired.

Adaptive signatures in thermal performance of the temperate coral Astrangia poculata.

Variation in environmental characteristics and divergent selection pressures can drive adaptive differentiation across a species' range. Astrangia poculata is a temperate scleractinian coral that provides unique opportunities to understand the roles of phenotypic plasticity and evolutionary adaptation in coral physiological tolerance limits. This species inhabits hard-bottom ecosystems from the northwestern Atlantic to the Gulf of Mexico and withstands an annual temperature range of up to 20°C. Additionally, A. poculata is facultatively symbiotic and co-occurs in both symbiotic ('brown') and aposymbiotic ('white') states. Here, brown and white A. poculata were collected from Virginia (VA) and Rhode Island (RI), USA, and exposed to heat (18-32°C) and cold (18-6°C) stress, during which respiration of the coral host along with photosynthesis and photochemical efficiency (Fv/Fm) of Breviolum psygmophilum photosymbionts were measured. Thermal performance curves (TPCs) of respiration revealed a pattern of countergradient variation with RI corals exhibiting higher respiration rates overall, and specifically at 6, 15, 18, 22 and 26°C. Additionally, thermal optimum (Topt) analyses show a 3.8°C (brown) and 6.9°C (white) higher Topt in the VA population, corresponding to the warmer in situ thermal environment in VA. In contrast to respiration, no origin effect was detected in photosynthesis rates or Fv/Fm, suggesting a possible host-only signature of adaptation. This study is the first to consider A. poculata's response to both heat and cold stress across symbiotic states and geography, and provides insight into the potential evolutionary mechanisms behind the success of this species along the East Coast of the USA.

Corals sustain growth but not skeletal density across the Florida Keys Reef Tract despite ongoing warming.

Through the continuous growth of their carbonate skeletons, corals record information about past environmental conditions and their effect on colony fitness. Here, we characterize century-scale growth records of inner and outer reef corals across ~200 km of the Florida Keys Reef Tract (FKRT) using skeletal cores extracted from two ubiquitous reef-building species, Siderastrea siderea and Pseudodiploria strigosa. We find that corals across the FKRT have sustained extension and calcification rates over the past century but have experienced a long-term reduction in skeletal density, regardless of reef zone. Notably, P. strigosa colonies exhibit temporary reef zone-dependent reductions in extension rate corresponding to two known extreme temperature events in 1969-1970 and 1997-1998. We propose that the subtropical climate of the FKRT may buffer corals from chronic growth declines associated with climate warming, though the significant reduction in skeletal density may indicate underlying vulnerability to present and future trends in ocean acidification.

Heterotrophy mitigates the response of the temperate coral Oculina arbuscula to temperature stress.

Anthropogenic increases in atmospheric carbon dioxide concentration have caused global average sea surface temperature (SST) to increase by approximately 0.11°C per decade between 1971 and 2010 - a trend that is projected to continue through the 21st century. A multitude of research studies have demonstrated that increased SSTs compromise the coral holobiont (cnidarian host and its symbiotic algae) by reducing both host calcification and symbiont density, among other variables. However, we still do not fully understand the role of heterotrophy in the response of the coral holobiont to elevated temperature, particularly for temperate corals. Here, we conducted a pair of independent experiments to investigate the influence of heterotrophy on the response of the temperate scleractinian coral Oculina arbuscula to thermal stress. Colonies of O. arbuscula from Radio Island, North Carolina, were exposed to four feeding treatments (zero, low, moderate, and high concentrations of newly hatched Artemia sp. nauplii) across two independent temperature experiments (average annual SST (20°C) and average summer temperature (28°C) for the interval 2005-2012) to quantify the effects of heterotrophy on coral skeletal growth and symbiont density. Results suggest that heterotrophy mitigated both reduced skeletal growth and decreased symbiont density observed for unfed corals reared at 28°C. This study highlights the importance of heterotrophy in maintaining coral holobiont fitness under thermal stress and has important implications for the interpretation of coral response to climate change.

Temperature Regimes Impact Coral Assemblages along Environmental Gradients on Lagoonal Reefs in Belize.

Coral reefs are increasingly threatened by global and local anthropogenic stressors such as rising seawater temperature, nutrient enrichment, sedimentation, and overfishing. Although many studies have investigated the impacts of local and global stressors on coral reefs, we still do not fully understand how these stressors influence coral community structure, particularly across environmental gradients on a reef system. Here, we investigate coral community composition across three different temperature and productivity regimes along a nearshore-offshore gradient on lagoonal reefs of the Belize Mesoamerican Barrier Reef System (MBRS). A novel metric was developed using ultra-high-resolution satellite-derived estimates of sea surface temperatures (SST) to classify reefs as exposed to low (lowTP), moderate (modTP), or high (highTP) temperature parameters over 10 years (2003 to 2012). Coral species richness, abundance, diversity, density, and percent cover were lower at highTP sites relative to lowTP and modTP sites, but these coral community traits did not differ significantly between lowTP and modTP sites. Analysis of coral life history strategies revealed that highTP sites were dominated by hardy stress-tolerant and fast-growing weedy coral species, while lowTP and modTP sites consisted of competitive, generalist, weedy, and stress-tolerant coral species. Satellite-derived estimates of Chlorophyll-a (chl-a) were obtained for 13-years (2003-2015) as a proxy for primary production. Chl-a concentrations were highest at highTP sites, medial at modTP sites, and lowest at lowTP sites. Notably, thermal parameters correlated better with coral community traits between site types than productivity, suggesting that temperature (specifically number of days above the thermal bleaching threshold) played a greater role in defining coral community structure than productivity on the MBRS. Dominance of weedy and stress-tolerant genera at highTP sites suggests that corals utilizing these two life history strategies may be better suited to cope with warmer oceans and thus may warrant protective status under climate change.