Knowledge of the degree to which corals undergo physiological acclimatization or genetic adaptation in response to changes in their thermal environment is crucial to the success of coral reef conservation strategies. The potential of corals to acclimatize to temperatures exceeding historical thermal regimes was investigated by reciprocal transplantation of Acropora millepora colonies between the warm central and cool southern regions of the Great Barrier Reef (GBR) for a duration of 14 months. Colony fragments retained at native sites remained healthy, whereas transplanted fragments, although healthy over initial months when temperatures remained within native thermal regimes, subsequently bleached and suffered mortality during seasonal temperature extremes. Corals hosting Symbiodinium D transplanted to the southern GBR bleached in winter and the majority suffered whole (40%; n = 20 colonies) or partial (50%) mortality at temperatures 1.1°C below their 15‐year native minimum. In contrast, corals hosting Symbiodinium C2 transplanted to the central GBR bleached in summer and suffered whole (50%; n = 10 colonies) or partial (42%) mortality at temperatures 2.5°C above their 15‐year native maximum. During summer bleaching, the dominant Symbiodinium type changed from C2 to D within corals transplanted to the central GBR. Corals transplanted to the cooler, southern GBR grew 74–80% slower than corals at their native site, and only 50% of surviving colonies reproduced, at least partially because of cold water bleaching of transplants. Despite the absence of any visual signs of stress, corals transplanted to the warmer, central GBR grew 52–59% more slowly than corals at their native site before the summer bleaching (i.e., from autumn to spring). Allocation of energy to initial acclimatization or reproduction may explain this pattern, as the majority (65%) of transplants reproduced one month earlier than portions of the same colonies retained at the southern native site. All parameters investigated (bleaching, mortality, Symbiodinium type fidelity, reproductive timing) demonstrated strong interactions between genotype and environment, indicating that the acclimatization potential of A. millepora populations may be limited by adaptation of the holobiont to native thermal regimes.

The perception that the inheritance of phenotypic traits operates solely through genetic means is slowly being eroded: epigenetic mechanisms have been shown to induce heritable changes in gene activity in plants^1,2 and metazoans^1,3. Inheritance of DNA methylation patterns provides a potential pathway for environmentally induced phenotypes to contribute to evolution of species and populations^1,2,3,4,5. However, in basal metazoans, it is unknown whether inheritance of CpG methylation patterns occurs across the genome (as in plants) or as rare exceptions (as in mammals)⁴. Here, we show that DNA methylation patterns in a reef-building coral are determined by genotype and developmental stage, as well as by parental environment. Transmission of CpG methylation from adults to their sperm and larvae demonstrates genome-wide inheritance. Variation in the hypermethylation of genes in adults and their sperm from distinct environments suggests intergenerational acclimatization to local temperature and salinity. Furthermore, genotype-independent adjustments of methylation levels in stress-related genes were strongly correlated with offspring survival rates under heat stress. These findings support a role of DNA methylation in the intergenerational inheritance of traits in corals, which could extend to enhancing their capacity to adapt to climate change.

Climate change is one of the greatest threats to the persistence of coral reefs. Sustained and ongoing increases in ocean temperatures and acidification are altering the structure and function of reefs globally. Here, we summarise recent advances in our understanding of the effects of climate change on scleractinian corals and reef fish. Although there is considerable among-species variability in responses to increasing temperature and seawater chemistry, changing temperature regimes are likely to have the greatest influence on the structure of coral and fish assemblages, at least over short–medium timeframes. Recent evidence of increases in coral bleaching thresholds, local genetic adaptation and inheritance of heat tolerance suggest that coral populations may have some capacity to respond to warming, although the extent to which these changes can keep pace with changing environmental conditions is unknown. For coral reef fishes, current evidence indicates increasing seawater temperature will be a major determinant of future assemblages, through both habitat degradation and direct effects on physiology and behaviour. The effects of climate change are, however, being compounded by a range of anthropogenic disturbances, which may undermine the capacity of coral reef organisms to acclimate and/or adapt to specific changes in environmental conditions.

Adaptation of reef corals to climate change is an issue of much debate, and often viewed as too slow a process to be of relevance over decadal time scales. This notion is based on the long sexual generation times typical for some coral species. However, the importance of somatic mutations during asexual reproduction and growth on evolution and adaptation (i.e., cell lineage selection) is rarely considered. Here we review the existing literature on cell lineage selection and show that the scope for somatic mutations to arise in the coral animal and associated Symbiodinium is large. For example, we estimate that ~100 million somatic mutations can arise within a branching Acropora coral colony of average size. Similarly, the large population sizes and rapid turn-over times of in hospite Symbiodinium likely result in considerable numbers of somatic mutations. While the fate of new mutations depends on many factors, including ploidy level and force and direction of selection, we argue that they likely play a key role in the evolution of reef corals.