Evidence for a host role in thermotolerance divergence between populations of the mustard hill coral (Porites astreoides) from different reef environments

Studying 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.     

Symbiodinium (Dinophyceae) community patterns in invertebrate hosts from inshore marginal reefs of the southern Great Barrier Reef,Australia

The broad range in physiological variation displayed by Symbiodinium spp. has proven imperative during periods of environmental change and contribute to the survival of their coral host. Characterizing how host and Symbiodinium community assemblages differ across environmentally distinct habitats provides useful information to predict how corals will respond to major environmental change. Despite the extensive characterizations of Symbiodinium diversity found amongst reef cnidarians on the Great Barrier Reef (GBR) substantial biogeographic gaps exist, especially across inshore habitats. Here, we investigate Symbiodinium community patterns in invertebrates from inshore and mid‐shelf reefs on the southern GBR, Australia. Dominant Symbiodinium types were characterized using denaturing gradient gel electrophoresis fingerprinting and sequencing of the ITS2 region of the ribosomal DNA. Twenty one genetically distinct Symbiodinium types including four novel types were identified from 321 reef‐invertebrate samples comprising three sub‐generic clades (A, C, and D). A range of host genera harbored C22a, which is normally rare or absent from inshore or low latitude reefs in the GBR. Multivariate analysis showed that host identity and sea surface temperature best explained the variation in symbiont communities across sites. Patterns of changes in Symbiodinium community assemblage over small geographic distances (100s of kilometers or less) indicate the likelihood that shifts in Symbiodinium distributions and associated host populations, may occur in response to future climate change impacting the GBR.     

Host adaptation and unexpected symbiont partners enable reef‐building corals to tolerate extreme temperatures

Understanding the potential for coral adaptation to warming seas is complicated by interactions between symbiotic partners that define stress responses and the difficulties of tracking selection in natural populations. To overcome these challenges, we characterized the contribution of both animal host and symbiotic algae to thermal tolerance in corals that have already experienced considerable warming on par with end‐of‐century projections for most coral reefs. Thermal responses in Platygyra daedalea corals from the hot Persian Gulf where summer temperatures reach 36°C were compared with conspecifics from the milder Sea of Oman. Persian Gulf corals had higher rates of survival at elevated temperatures (33 and 36°C) in both the nonsymbiotic larval stage (32–49% higher) and the symbiotic adult life stage (51% higher). Additionally, Persian Gulf hosts had fixed greater potential to mitigate oxidative stress (31–49% higher) and their Symbiodinium partners had better retention of photosynthetic performance under elevated temperature (up to 161% higher). Superior thermal tolerance of Persian Gulf vs. Sea of Oman corals was maintained after 6‐month acclimatization to a common ambient environment and was underpinned by genetic divergence in both the coral host and symbiotic algae. In P. daedalea host samples, genomewide SNP variation clustered into two discrete groups corresponding with Persian Gulf and Sea of Oman sites. Symbiodinium within host tissues predominantly belonged to ITS2 rDNA type C3 in the Persian Gulf and type D1a in the Sea of Oman contradicting patterns of Symbiodinium thermal tolerance from other regions. Our findings provide evidence that genetic adaptation of both host and Symbiodinium has enabled corals to cope with extreme temperatures in the Persian Gulf. Thus, the persistence of coral populations under continued warming will likely be determined by evolutionary rates in both, rather than single, symbiotic partners.     

Molecular signatures of host specificity linked to habitat specialization in Exaiptasia sea anemones

Rising ocean temperatures associated with global climate change induce breakdown of the symbiosis between coelenterates and photosynthetic microalgae of the genus Symbiodinium. Association with more thermotolerant partners could contribute to resilience, but the genetic mechanisms controlling specificity of hosts for particular Symbiodinium types are poorly known. Here, we characterize wild populations of a sea anemone laboratory model system for anthozoan symbiosis, from contrasting environments in Caribbean Panama. Patterns of anemone abundance and symbiont diversity were consistent with specialization of holobionts for particular habitats, with Exaiptasia pallida/S. minutum (ITS2 type B1) abundant on vertical substrate in thermally stable, shaded environments but E. brasiliensis/Symbiodinium sp. (ITS2 clade A) more common in shallow areas subject to high temperature and irradiance. Population genomic sequencing revealed a novel E. pallida population from the Bocas del Toro Archipelago that only harbors S. minutum. Loci most strongly associated with divergence of the Bocas‐specific population were enriched in genes with putative roles in cnidarian symbiosis, including activators of the complement pathway of the innate immune system, thrombospondin‐type‐1 repeat domain proteins, and coordinators of endocytic recycling. Our findings underscore the importance of unmasking cryptic diversity in natural populations and the role of long‐term evolutionary history in mediating interactions with Symbiodinium.     

Symbiotic specificity,association patterns,and function determine community responses to global changes: defining critical research areas for coral‐Symbiodinium symbioses

Climate change‐driven stressors threaten the persistence of coral reefs worldwide. Symbiotic relationships between scleractinian corals and photosynthetic endosymbionts (genus Symbiodinium) are the foundation of reef ecosystems, and these associations are differentially impacted by stress. Here, we couple empirical data from the coral reefs of Moorea, French Polynesia, and a network theoretic modeling approach to evaluate how patterns in coral‐Symbiodinium associations influence community stability under climate change. To introduce the effect of climate perturbations, we simulate local ‘extinctions’ that represent either the loss of coral species or the ability to engage in symbiotic interactions. Community stability is measured by determining the duration and number of species that persist through the simulated extinctions. Our results suggest that four factors greatly increase coral‐Symbiodinium community stability in response to global changes: (i) the survival of generalist hosts and symbionts maximizes potential symbiotic unions; (ii) elevated symbiont diversity provides redundant or complementary symbiotic functions; (iii) compatible symbiotic assemblages create the potential for local recolonization; and (iv) the persistence of certain traits associate with symbiotic diversity and redundancy. Symbiodinium may facilitate coral persistence through novel environmental regimes, but this capacity is mediated by symbiotic specificity, association patterns, and the functional performance of the symbionts. Our model‐based approach identifies general trends and testable hypotheses in coral‐Symbiodinium community responses. Future studies should consider similar methods when community size and/or environmental complexity preclude experimental approaches.     

One‐year experiment on the physiological response of the Mediterranean crustose coralline alga,Lithophyllum cabiochae,to elevated pCO2 and temperature

The response of respiration, photosynthesis, and calcification to elevated pCO₂ and temperature was investigated in isolation and in combination in the Mediterranean crustose coralline alga Lithophyllum cabiochae. Algae were maintained in aquaria during 1 year at near‐ambient conditions of irradiance, at ambient or elevated temperature (+3°C), and at ambient (ca. 400 μatm) or elevated pCO₂ (ca. 700 μatm). Respiration, photosynthesis, and net calcification showed a strong seasonal pattern following the seasonal variations of temperature and irradiance, with higher rates in summer than in winter. Respiration was unaffected by pCO₂ but showed a general trend of increase at elevated temperature at all seasons, except in summer under elevated pCO₂. Conversely, photosynthesis was strongly affected by pCO₂ with a decline under elevated pCO₂ in summer, autumn, and winter. In particular, photosynthetic efficiency was reduced under elevated pCO₂. Net calcification showed different responses depending on the season. In summer, net calcification increased with rising temperature under ambient pCO₂ but decreased with rising temperature under elevated pCO₂. Surprisingly, the highest rates in summer were found under elevated pCO₂ and ambient temperature. In autumn, winter, and spring, net calcification exhibited a positive or no response at elevated temperature but was unaffected by pCO₂. The rate of calcification of L. cabiochae was thus maintained or even enhanced under increased pCO₂. However, there is likely a trade‐off with other physiological processes. For example, photosynthesis declines in response to increased pCO₂ under ambient irradiance. The present study reports only on the physiological response of healthy specimens to ocean warming and acidification, however, these environmental changes may affect the vulnerability of coralline algae to other stresses such as pathogens and necroses that can cause major dissolution, which would have critical consequence for the sustainability of coralligenous habitats and the budgets of carbon and calcium carbonate in coastal Mediterranean ecosystems.     

The Occurrence of Mixed Infections of Symbiodinium (Dinoflagellata) within Individual Hosts

Coral reef ecosystems depend on symbiosis between dinoflagellates of the genus Symbiodinium Freudenthal and their various hosts. The physiological characteristics associated with a particular lineage or species of Symbiodinium can determine a host's susceptibility to harmful bleaching. Therefore, the threat posed by global climate change on a host may be reduced if it can switch or shuffle its dominant algal symbiont type. An important prerequisite to this potential to switch or shuffle is the ability to host multiple alternative dominant symbiont genotypes. To examine the distribution of this trait, we review reports of mixed Symbiodinium infections in corals and nonscleractinian hosts from a phylogenetic perspective. Hosts showing evidence of mixed infection are broadly distributed across the most deeply divergent host lineages, including foraminifera, mollusks, sponges, and cnidarians. The occurrence of mixed infections is also broadly distributed across most clades of scleractinian corals. Individual colonies of certain well‐studied cosmopolitan coral genera, such as Acropora, Montastraea, and Pocillopora, yield many reports of mixed infection, while other genera, such as Porites, do not. We further discuss mixed Symbiodinium infections in the context of evolutionary ecology theory. Selection pressures that affect the prevalence of mixed infection may be exerted by variation in host environment, host ontogeny, symbiont transmission strategy, host regulation of symbiont populations, availability of free‐living symbiont lineages, competition between symbiont lineages, and niche partitioning of the internal host environment.     

Different strategies of energy storage in cultured and freshly isolated Symbiodinium sp.

The endosymbiotic relationship between cnidarians and Symbiodinium is critical for the survival of coral reefs. In this study, we developed a protocol to rapidly and freshly separate Symbiodinium from corals and sea anemones. Furthermore, we compared these freshly‐isolated Symbiodinium with cultured Symbiodinium to investigate host and Symbiodinium interaction. Clade B Symbiodinium had higher starch content and lower lipid content than those of clades C and D in both freshly isolated and cultured forms. Clade C had the highest lipid content, particularly when associated with corals. Moreover, the coral‐associated Symbiodinium had higher protein content than did cultured and sea anemone‐associated Symbiodinium. Regarding fatty acid composition, cultured Symbiodinium and clades B, C, and D shared similar patterns, whereas sea anemone‐associated Symbiodinium had a distinct pattern compared coral‐associated Symbiodinium. Specifically, the levels of monounsaturated fatty acids were lower than those of the saturated fatty acids, and the level of polyunsaturated fatty acids (PUFAs) were the highest in all examined Symbiodinium. Furthermore, PUFAs levels were higher in coral‐associated Symbiodinium than in cultured Symbiodinium. These results altogether indicated that different Symbiodinium clades used different energy storage strategies, which might be modified by hosts.     

Corals in the hottest reefs in the world exhibit symbiont fidelity not flexibility

Reef‐building corals are at risk of extinction from ocean warming. While some corals can enhance their thermal limits by associating with dinoflagellate photosymbionts of superior stress tolerance, the extent to which symbiont communities will reorganize under increased warming pressure remains unclear. Here we show that corals in the hottest reefs in the world in the Persian Gulf maintain associations with the same symbionts across 1.5 years despite extreme seasonal warming and acute heat stress (≥35°C). Persian Gulf corals predominantly associated with Cladocopium (clade C) and most also hosted Symbiodinium (clade A) and/or Durusdinium (clade D). This is in contrast to the neighbouring and milder Oman Sea, where corals associated with Durusdinium and only a minority hosted background levels of Cladocopium. During acute heat stress, the higher prevalence of Symbiodinium and Durusdinium in bleached versus nonbleached Persian Gulf corals indicates that genotypes of these background genera did not confer bleaching resistance. Within symbiont genera, the majority of ITS2 rDNA type profiles were unique to their respective coral species, confirming the existence of host‐specific symbiont lineages. Notably, further differentiation among Persian Gulf sites demonstrates that symbiont populations are either isolated or specialized over tens to hundreds of kilometres. Thermal tolerance across coral species was associated with the prevalence of a single ITS2 intragenomic sequence variant (C3gulf), definitive of the Cladocopium thermophilum group. The abundance of C3gulf was highest in bleaching‐resistant corals and at warmer sites, potentially indicating a specific symbiont genotype (or set of genotypes) that may play a role in thermal tolerance that warrants further investigation. Together, our findings indicate that co‐evolution of host–Symbiodiniaceae partnerships favours fidelity rather than flexibility in extreme environments and under future warming.     

Viral attack exacerbates the susceptibility of a bloom‐forming alga to ocean acidification

Both ocean acidification and viral infection bring about changes in marine phytoplankton physiological activities and community composition. However, little information is available on how the relationship between phytoplankton and viruses may be affected by ocean acidification and what impacts this might have on photosynthesis‐driven marine biological CO₂ pump. Here, we show that when the harmful bloom alga Phaeocystis globosa is infected with viruses under future ocean conditions, its photosynthetic performance further decreased and cells became more susceptible to stressful light levels, showing enhanced photoinhibition and reduced carbon fixation, up‐regulation of mitochondrial respiration and decreased virus burst size. Our results indicate that ocean acidification exacerbates the impacts of viral attack on P. globosa, which implies that, while ocean acidification directly influences marine primary producers, it may also affect them indirectly by altering their relationship with viruses. Therefore, viruses as a biotic stressor need to be invoked when considering the overall impacts of climate change on marine productivity and carbon sequestration.     

Spatial and temporal genetic structure of Symbiodinium populations within a common reef‐building coral on the Great Barrier Reef

The dinoflagellate photosymbiont Symbiodinium plays a fundamental role in defining the physiological tolerances of coral holobionts, but little is known about the dynamics of these endosymbiotic populations on coral reefs. Sparse data indicate that Symbiodinium populations show limited spatial connectivity; however, no studies have investigated temporal dynamics for in hospite Symbiodinium populations following significant mortality and recruitment events in coral populations. We investigated the combined influences of spatial isolation and disturbance on the population dynamics of the generalist Symbiodinium type C2 (ITS1 rDNA) hosted by the scleractinian coral Acropora millepora in the central Great Barrier Reef. Using eight microsatellite markers, we genotyped Symbiodinium in a total of 401 coral colonies, which were sampled from seven sites across a 12‐year period including during flood plume–induced coral bleaching. Genetic differentiation of Symbiodinium was greatest within sites, explaining 70–86% of the total genetic variation. An additional 9–27% of variation was explained by significant differentiation of populations among sites separated by 0.4–13 km, which is consistent with low levels of dispersal via water movement and historical disturbance regimes. Sampling year accounted for 6–7% of total genetic variation and was related to significant coral mortality following severe bleaching in 1998 and a cyclone in 2006. Only 3% of the total genetic variation was related to coral bleaching status, reflecting generally small (8%) reductions in allelic diversity within bleached corals. This reduction probably reflected a loss of genotypes in hospite during bleaching, although no site‐wide changes in genetic diversity were observed. Combined, our results indicate the importance of disturbance regimes acting together with limited oceanographic transport to determine the genetic composition of Symbiodinium types within reefs.     

Calcification is not the Achilles’ heel of cold‐water corals in an acidifying ocean

Ocean acidification is thought to be a major threat to coral reefs: laboratory evidence and CO₂ seep research has shown adverse effects on many coral species, although a few are resilient. There are concerns that cold‐water corals are even more vulnerable as they live in areas where aragonite saturation (Ω_ara) is lower than in the tropics and is falling rapidly due to CO₂ emissions. Here, we provide laboratory evidence that net (gross calcification minus dissolution) and gross calcification rates of three common cold‐water corals, Caryophyllia smithii, Dendrophyllia cornigera, and Desmophyllum dianthus, are not affected by pCO₂ levels expected for 2100 (pCO₂ 1058 μatm, Ω_ara 1.29), and nor are the rates of skeletal dissolution in D. dianthus. We transplanted D. dianthus to 350 m depth (pH_T 8.02; pCO₂ 448 μatm, Ω_ara 2.58) and to a 3 m depth CO₂ seep in oligotrophic waters (pH_T 7.35; pCO₂ 2879 μatm, Ω_ara 0.76) and found that the transplants calcified at the same rates regardless of the pCO₂ confirming their resilience to acidification, but at significantly lower rates than corals that were fed in aquaria. Our combination of field and laboratory evidence suggests that ocean acidification will not disrupt cold‐water coral calcification although falling aragonite levels may affect other organismal physiological and/or reef community processes.     

Population genetic data of a model symbiotic cnidarian system reveal remarkable symbiotic specificity and vectored introductions across ocean basins

The Aiptasia–Symbiodinium symbiosis is a promising model for experimental studies of cnidarian–dinoflagellate associations, yet relatively little is known regarding the genetic diversity of either symbiotic partner. To address this, we collected Aiptasia from 16 localities throughout the world and examined the genetic diversity of both anemones and their endosymbionts. Based on newly developed SCAR markers, Aiptasia consisted of two genetically distinct populations: one Aiptasia lineage from Florida and a second network of Aiptasia genotypes found at other localities. These populations did not conform to the distributions of described Aiptasia species, suggesting that taxonomic re‐evaluation is needed in the light of molecular genetics. Associations with Symbiodinium further demonstrated the distinctions among Aiptasia populations. According to 18S RFLP, ITS2‐DGGE and microsatellite flanker region sequencing, Florida anemones engaged in diverse symbioses predominantly with members of Symbiodinium Clades A and B, but also C, whereas anemones from elsewhere harboured only S. minutum within Clade B. Symbiodinium minutum apparently does not form a stable symbiosis with other hosts, which implies a highly specific symbiosis. Fine‐scale differences among S. minutum populations were quantified using six microsatellite loci. Populations of S. minutum had low genotypic diversity and high clonality (R = 0.14). Furthermore, minimal population structure was observed among regions and ocean basins, due to allele and genotype sharing. The lack of genetic structure and low genotypic diversity suggest recent vectoring of Aiptasia and S. minutum across localities. This first ever molecular‐genetic study of a globally distributed cnidarian and its Symbiodinium assemblages reveals host–symbiont specificity and widely distributed populations in an important model system.