Positive genetic associations among fitness traits support evolvability of a reef‐building coral under multiple stressors

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 trade‐offs 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 covariances, 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.     

Diverse staghorn corals (Acropora) in high-latitude Eocene assemblages: implications for the evolution of modern diversity patterns of reef corals

Acropora is the most diverse genus of reef-building corals in the world today. It occurs in all three major oceans; it is restricted to latitudes 31 degrees N-31 degrees S, where most coral reefs occur, and reaches greatest diversity in the central Indo-Pacific. As an exemplar genus, the long-term history of Acropora has implications for the evolution and origins of present day biodiversity patterns of reef corals and for predicting their response to future climate change. Diversification of Acropora was thought to have occurred in the central Indo-Pacific within the previous two million years. We examined Eocene fossils from southern England and northern France and found evidence that precursors of up to nine of 20 currently recognized Acropora species groups existed 49-34 Myr, at palaeolatitudes far higher than current limits, to 51 degrees N. We propose that pre-existing diversity contributed to later rapid speciation in this important functional group of corals.     

A 'fair go' for coral hybridization

Hybridisation between coral species clearly occurs in vitro, but the evolutionary significance of this cross-fertility is still the subject of much debate. Compelling genetic and reproductive evidence support introgressive hybridization amongst Indo-Pacific members of the scleractinian genus Acropora. Although population genetic analyses indicate that interspecific hybridization events are relatively rare, they are likely be important on evolutionary time scales, creating the capacity for adaptive evolution by increasing genomic diversity and heterozygosity. However, in a recent paper based exclusively on the three endemic Caribbean Acropora species, Vollmer and Palumbi (2002) dispute the occurrence of reticulation in corals. Here we use data from both the Vollmer and Palumbi study and our earlier paper on the same species (van Oppen et al., 2000) to show that reticulation has occurred amongst the Caribbean Acropora species. Furthermore, conclusions based on the limited Caribbean Acropora fauna cannot simply be extrapolated to Indo-Pacific corals, and it is inappropriate to view some coral species as 'immortal mules'.     

Threatened Caribbean Coral Is Able to Mitigate the Adverse Effects of Ocean Acidification on Calcification by Increasing Feeding Rate

Global climate change threatens coral growth and reef ecosystem health via ocean warming and ocean acidification (OA). Whereas the negative impacts of these stressors are increasingly well-documented, studies identifying pathways to resilience are still poorly understood. Heterotrophy has been shown to help corals experiencing decreases in growth due to either thermal or OA stress; however, the mechanism by which it mitigates these decreases remains unclear. This study tested the ability of coral heterotrophy to mitigate reductions in growth due to climate change stress in the critically endangered Caribbean coral Acropora cervicornis via changes in feeding rate and lipid content. Corals were either fed or unfed and exposed to elevated temperature (30°C), enriched pCO₂ (800 ppm), or both (30°C/800 ppm) as compared to a control (26°C/390 ppm) for 8 weeks. Feeding rate and lipid content both increased in corals experiencing OA vs. present-day conditions, and were significantly correlated. Fed corals were able to maintain ambient growth rates at both elevated temperature and elevated CO₂, while unfed corals experienced significant decreases in growth with respect to fed conspecifics. Our results show for the first time that a threatened coral species can buffer OA-reduced calcification by increasing feeding rates and lipid content.     

Profiling gene expression responses of coral larvae (Acropora millepora) to elevated temperature and settlement inducers using a novel RNA-Seq procedure

Elevated temperatures resulting from climate change pose a clear threat to reef-building corals; however, the traits that might influence corals' survival and dispersal during climate change remain poorly understood. Global gene expression profiling is a powerful hypothesis-forming tool that can help elucidate these traits. Here, we applied a novel RNA-Seq protocol to study molecular responses to heat and settlement inducers in aposymbiotic larvae of the reef-building coral Acropora millepora. This analysis of a single full-sibling family revealed contrasting responses between short- (4-h) and long-term (5-day) exposures to elevated temperatures. Heat shock proteins were up-regulated only in the short-term treatment, while the long-term treatment induced the down-regulation of ribosomal proteins and up-regulation of genes associated with ion transport and metabolism (Ca(2+) and CO(3)(2-)). We also profiled responses to settlement cues using a natural cue (crustose coralline algae, CCA) and a synthetic neuropeptide (GLW-amide). Both cues resulted in metamorphosis, accompanied by differential expression of genes with known developmental roles. Some genes were regulated only by the natural cue, which may correspond to the recruitment-associated behaviour and morphology changes that precede metamorphosis under CCA treatment, but are bypassed under GLW-amide treatment. Validation of these expression profiles using qPCR confirmed the quantitative accuracy of our RNA-Seq approach. Importantly, qPCR analysis of different larval families revealed extensive variation in these responses depending on genetic background, including qualitative differences (i.e. up-regulation in one family and down-regulation in another). Future studies of gene expression in corals will have to address this genetic variation, which could have important adaptive consequences for corals during global climate change.     

Changes in gametogenesis and fecundity of acroporid corals that were exposed to elevated nitrogen and phosphorus during the ENCORE experiment

Colonies of two scleractinian reef coral species, Acropora longicyathus and Acropora aspera were transplanted into patch reefs at One Tree Reef, Great Barrier Reef, Australia as part of the ENCORE experiment. These corals and colonies of A. aspera which were naturally present in the patch reefs were exposed to four treatments over two years: controls with normal seawater, elevated levels of nitrogen only, phosphorus only, or nitrogen plus phosphorus. These corals were sampled and used to determine whether gametogenic cycles and fecundity were affected by nutrient enrichment. Acropora longicyathus had a single annual gametogenic cycle. Corals exposed to elevated nitrogen produced significantly smaller and fewer eggs and contained less testes material than those which were not exposed to nitrogen. Exposure to elevated phosphorus only resulted in corals producing more but smaller eggs, and more testes material. Egg numbers of colonies from other treatments decreased as the gametogenic cycles continued, but those of the phosphorus colonies showed almost no reduction in egg numbers between the early and late stages of the gametogenic cycles. These results have important management implications for coral reefs as they demonstrate that small increases in concentrations of nitrogen and phosphorus can have severe effects on reproductive activity in these species of scleractinian corals.     

Reef‐coral refugia in a rapidly changing ocean

This study sought to identify climate‐change thermal‐stress refugia for reef corals in the Indian and Pacific Oceans. A species distribution modeling approach was used to identify refugia for 12 coral species that differed considerably in their local response to thermal stress. We hypothesized that the local response of coral species to thermal stress might be similarly reflected as a regional response to climate change. We assessed the contemporary geographic range of each species and determined their temperature and irradiance preferences using a k‐fold algorithm to randomly select training and evaluation sites. That information was applied to downscaled outputs of global climate models to predict where each species is likely to exist by the year 2100. Our model was run with and without a 1 °C capacity to adapt to the rising ocean temperature. The results show a positive exponential relationship between the current area of habitat that coral species occupy and the predicted area of habitat that they will occupy by 2100. There was considerable decoupling between scales of response, however, and with further ocean warming some ‘winners’ at local scales will likely become ‘losers’ at regional scales. We predicted that nine of the 12 species examined will lose 24–50% of their current habitat. Most reductions are predicted to occur between the latitudes 5–15°, in both hemispheres. Yet when we modeled a 1 °C capacity to adapt, two ubiquitous species, Acropora hyacinthus and Acropora digitifera, were predicted to retain much of their current habitat. By contrast, the thermally tolerant Porites lobata is expected to increase its current distribution by 14%, particularly southward along the east and west coasts of Australia. Five areas were identified as Indian Ocean refugia, and seven areas were identified as Pacific Ocean refugia for reef corals under climate change. All 12 of these reef‐coral refugia deserve high‐conservation status.     

Resistance to thermal stress in corals without changes in symbiont composition

Discovering how corals can adjust their thermal sensitivity in the context of global climate change is important in understanding the long-term persistence of coral reefs. In this study, we showed that short-term preconditioning to higher temperatures, 3°C below the experimentally determined bleaching threshold, for a period of 10 days provides thermal tolerance for the symbiosis stability between the scleractinian coral, Acropora millepora and Symbiodinium. Based on genotypic analysis, our results indicate that the acclimatization of this coral species to thermal stress does not come down to simple changes in Symbiodinium and/or the bacterial communities that associate with reef-building corals. This suggests that the physiological plasticity of the host and/or symbiotic components appears to play an important role in responding to ocean warming. The further study of host and symbiont physiology, both of Symbiodinium and prokaryotes, is of paramount importance in the context of global climate change, as mechanisms for rapid holobiont acclimatization will become increasingly important to the long-standing persistence of coral reefs.     

Bacterial communities associated with healthy and Acropora white syndrome-affected corals from American Samoa

Acropora white syndrome (AWS) is characterized by rapid tissue loss revealing the white underlying skeleton and affects corals worldwide; however, reports of causal agents are conflicting. Samples were collected from healthy and diseased corals and seawater around American Samoa and bacteria associated with AWS characterized using both culture-dependent and culture-independent methods, from coral mucus and tissue slurries, respectively. Bacterial 16S rRNA gene clone libraries derived from coral tissue were dominated by the Gammaproteobacteria, and Jaccard's distances calculated between the clone libraries showed that those from diseased corals were more similar to each other than to those from healthy corals. 16S rRNA genes from 78 culturable coral mucus isolates also revealed a distinct partitioning of bacterial genera into healthy and diseased corals. Isolates identified as Vibrionaceae were further characterized by multilocus sequence typing, revealing that whilst several Vibrio spp. were found to be associated with AWS lesions, a recently described species, Vibrio owensii, was prevalent amongst cultured Vibrio isolates. Unaffected tissues from corals with AWS had a different microbiota than normal Acropora as found by others. Determining whether a microbial shift occurs prior to disease outbreaks will be a useful avenue of pursuit and could be helpful in detecting prodromal signs of coral disease prior to manifestation of lesions.     

Diversities of coral-associated bacteria differ with location, but not species, for three acroporid corals on the Great Barrier Reef

Patterns in the diversity of bacterial communities associated with three species of Acropora ( Acropora millepora, Acropora tenuis and Acropora valida ) were compared at two locations (Magnetic Island and Orpheus Island) on the Great Barrier Reef to better understand the nature and specificity of coral–microbial symbioses. Three culture-independent techniques demonstrated consistent bacterial communities among replicate samples of each coral species, confirming that corals associate with specific microbiota. Profiles were also conserved among all three species of Acropora within each location, suggesting that closely related corals of the same genus harbor similar bacterial types. Bacterial community profiles of A. millepora at Orpheus Island were consistent in samples collected throughout the year, indicating a stable community despite temporal changes. However, DGGE and T-RFLP profiles differed on corals from different reefs. Nonmetric multidimensional scaling of T-RFLP profiles showed that samples grouped according to location rather than coral species. Although similar sequences were retrieved from clone libraries of corals at both Magnetic and Orpheus Island, differences in the relative dominant bacterial ribotypes within the libraries drive bacterial community structure at different geographical locations. These results indicate certain bacterial groups associated specifically with corals, but the dominant bacterial genera differ between geographically-spaced corals.     

The role of zooxanthellae in the thermal tolerance of corals: a 'nugget of hope' for coral reefs in an era of climate change

The ability of coral reefs to survive the projected increases in temperature due to global warming will depend largely on the ability of corals to adapt or acclimatize to increased temperature extremes over the next few decades. Many coral species are highly sensitive to temperature stress and the number of stress (bleaching) episodes has increased in recent decades. We investigated the acclimatization potential of Acropora millepora, a common and widespread Indo-Pacific hard coral species, through transplantation and experimental manipulation. We show that adult corals, at least in some circumstances, are capable of acquiring increased thermal tolerance and that the increased tolerance is a direct result of a change in the symbiont type dominating their tissues from Symbiodinium type C to D. Our data suggest that the change in symbiont type in our experiment was due to a shuffling of existing types already present in coral tissues, not through exogenous uptake from the environment. The level of increased tolerance gained by the corals changing their dominant symbiont type to D (the most thermally resistant type known) is around 1-1.5 degrees C. This is the first study to show that thermal acclimatization is causally related to symbiont type and provides new insight into the ecological advantage of corals harbouring mixed algal populations. While this increase is of huge ecological significance for many coral species, in the absence of other mechanisms of thermal acclimatization/adaptation, it may not be sufficient to survive climate change under predicted sea surface temperature scenarios over the next 100 years. However, it may be enough to 'buy time' while greenhouse reduction measures are put in place.     

Fluorescent protein candidate genes in the coral Acropora digitifera genome

The vivid coloration of corals depends on fluorescent proteins that include cyan (CFP), green (GFP) and red (RFP) fluorescent proteins, and a non-fluorescent blue/purple chromoprotein. We examined how many genes encoding fluorescent proteins are present in the recently sequenced genome of the coral Acropora digitifera. Based on molecular phylogenetic analysis, we found one, five, one, and three candidate genes for CFP, GFP, RFP, and chromoprotein, respectively. The CFP and GFP genes are clustered in a ~80-kb-long genomic region, suggesting that they originated from an ancestral gene by tandem duplication. Since CFP and GFP possess the same chromophore, the gene clustering may provide the first genomic evidence for a common origin of the two proteins. Comparison between the fluorescent protein genes of closely related coral species suggests an expansion of chromoprotein genes in the A. digitifera genome, and of RFP genes in the A. millepora genome. The A. digitifera fluorescent protein genes are expressed during embryonic and larval developmental stages and in adults, suggesting that the genes play a variety of roles in coral physiology.     

Evidence of an inflammatory-like response in non-normally pigmented tissues of two scleractinian corals

Increasing evidence of links between climate change, anthropogenic stress and coral disease underscores the importance of understanding the mechanisms by which reef-building corals resist infection and recover from injury. Cellular inflammation and melanin-producing signalling pathway are two mechanisms employed by invertebrates to remove foreign organisms such as pathogens, but they have not been recorded previously in scleractinian corals. This study demonstrates the presence of the phenoloxidase (PO) activating melanin pathway in two species of coral, Acropora millepora and a massive species of Porites, which both develop local pigmentation in response to interactions with a variety of organisms. L-DOPA (3-(3,4-dihydroxyphenyl)-L-alanine) substrate-based enzyme activation assays demonstrated PO activity in healthy tissues of both species and upregulation in pigmented tissues of A. millepora. Histological staining conclusively identified the presence of melanin in Porites tissues. These results demonstrate that the PO pathway is active in both coral species. Moreover, the upregulation of PO activity in areas of non-normal pigmentation in A. millepora and increased melanin production in pigmented Porites tissues suggest the presence of a generalized defence response to localized stress. Interspecific differences in the usage of pathways involved in innate immunity may underlie the comparative success of massive Porites sp. as long-lived stress tolerators.     

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.     

造礁石珊瑚与其共生藻(Symbiodinium)共生研究进展

对造礁石珊瑚与其共生藻共生研究现状及其在全球变化下的适应能力进行较全面的综述.造礁石珊瑚与遗传和生理功能独特的共生藻组成内共生关系是成功演化的范例.近年来对珊瑚共生体的分子系统学研究表明共生藻遗传多样性极为丰富,当前认为共生藻属至少包括8个(A-H)各自包含亚系群的世系或系群.珊瑚-共生藻共生功能体对诸如全球变化引起的海水温度上升等环境变化十分敏感.由于珊瑚以及珊瑚礁面临气候变化的严峻挑战,对珊瑚与其共生藻共生关系和共生功体适应能力的研究将是未来重要的研究领域之一.     

Specific Expression of BMP2/4 Ortholog in Biomineralizing Tissues of Corals and Action on Mouse BMP Receptor

Bone morphogenetic proteins (BMPs) are members of the transforming growth factor β superfamily, and have been identified by their ability to induce bone formation in vertebrates. The biomineral-forming process, called biomineralization, is a widespread process, present in all kingdoms of living organisms and among which stony corals are one of the major groups of calcifying animals. Here, we report the presence of a BMP2/4 ortholog in eight species of adult corals. The synthesis of such a protein by the calcifying epithelium of corals suggests that coral BMP2/4 plays a role in skeletogenesis, making BMP the first common protein involved in biomineralization among Eumetazoans. In addition we show that recombinant coral BMP2/4 is able to inhibit human BMP2-induced osteoblastic differentiation in mesenchymal C2C12 cells. We suggest that this inhibition results from a competition between coral BMP2/4 and human BMP2, indicating conservation of binding affinity of BMP and its receptor during evolution from corals to vertebrates. Further studies are needed to understand interactions between coral BMP2/4 and its receptors, and, thus, the action of BMP2/4 in adult corals. Nucleotide sequence of the coral BMP2/4 genes cloned in this study is available in the GenBank under the accession number EU785981 (Stylophora pistillata) and EU785982 (Acropora sp.).