Diagnostic gene expression biomarkers of coral thermal stress

Gene expression biomarkers can enable rapid assessment of physiological conditions in situ, providing a valuable tool for reef managers interested in linking organism physiology with large‐scale climatic conditions. Here, we assessed the ability of quantitative PCR (qPCR)‐based gene expression biomarkers to evaluate (i) the immediate cellular stress response (CSR) of Porites astreoides to incremental thermal stress and (ii) the magnitude of CSR and cellular homeostasis response (CHR) during a natural bleaching event. Expression levels largely scaled with treatment temperature, with the strongest responses occurring in heat‐shock proteins. This is the first demonstration of a ‘tiered’ CSR in a coral, where the magnitude of expression change is proportional to stress intensity. Analysis of a natural bleaching event revealed no signature of an acute CSR in normal or bleached corals, indicating that the bleaching stressor(s) had abated by the day of sampling. Another long‐term stress CHR‐based indicator assay was significantly elevated in bleached corals, although assay values overall were low, suggesting good prospects for recovery. This study represents the first step in linking variation in gene expression biomarkers to stress tolerance and bleaching thresholds in situ by quantifying the severity of ongoing thermal stress and its accumulated long‐term impacts.     

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.     

Functional genomic analysis of corals from natural CO2‐seeps reveals core molecular responses involved in acclimatization to ocean acidification

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

Climate‐change refugia in the sheltered bays of Palau: analogs of future reefs

Coral bleaching and mortality are predicted to increase as climate change‐induced thermal‐stress events become more frequent. Although many studies document coral bleaching and mortality patterns, few studies have examined deviations from the expected positive relationships among thermal stress, coral bleaching, and coral mortality. This study examined the response of >30,000 coral colonies at 80 sites in Palau, during a regional thermal‐stress event in 2010. We sought to determine the spatial and taxonomic nature of bleaching and examine whether any habitats were comparatively resistant to thermal stress. Bleaching was most severe in the northwestern lagoon, in accordance with satellite‐derived maximum temperatures and anomalous temperatures above the long‐term averages. Pocillopora populations suffered the most extensive bleaching and the highest mortality. However, in the bays where temperatures were higher than elsewhere, bleaching and mortality were low. The coral‐community composition, constant exposure to high temperatures, and high vertical attenuation of light caused by naturally high suspended particulate matter buffered the corals in bays from the 2010 regional thermal‐stress event. Yet, nearshore reefs are also most vulnerable to land‐use change. Therefore, nearshore reefs should be given high conservation status because they provide refugia for coral populations as the oceans continue to warm.     

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.     

Development of gene expression markers of acute heat-light stress in reef-building corals of the genus Porites

Coral reefs are declining worldwide due to increased incidence of climate-induced coral bleaching, which will have widespread biodiversity and economic impacts. A simple method to measure the sub-bleaching level of heat-light stress experienced by corals would greatly inform reef management practices by making it possible to assess the distribution of bleaching risks among individual reef sites. Gene expression analysis based on quantitative PCR (qPCR) can be used as a diagnostic tool to determine coral condition in situ. We evaluated the expression of 13 candidate genes during heat-light stress in a common Caribbean coral Porites astreoides, and observed strong and consistent changes in gene expression in two independent experiments. Furthermore, we found that the apparent return to baseline expression levels during a recovery phase was rapid, despite visible signs of colony bleaching. We show that the response to acute heat-light stress in P. astreoides can be monitored by measuring the difference in expression of only two genes: Hsp16 and actin. We demonstrate that this assay discriminates between corals sampled from two field sites experiencing different temperatures. We also show that the assay is applicable to an Indo-Pacific congener, P. lobata, and therefore could potentially be used to diagnose acute heat-light stress on coral reefs worldwide.