Many ecosystems around the world are rapidly deteriorating due to both local and global pressures, and perhaps none so precipitously as coral reefs. Management of coral reefs through maintenance (e.g., marine-protected areas, catchment management to improve water quality), restoration, as well as global and national governmental agreements to reduce greenhouse gas emissions (e.g., the 2015 Paris Agreement) is critical for the persistence of coral reefs. Despite these initiatives, the health and abundance of corals reefs are rapidly declining and other solutions will soon be required. We have recently discussed options for using assisted evolution (i.e., selective breeding, assisted gene flow, conditioning or epigenetic programming, and the manipulation of the coral microbiome) as a means to enhance environmental stress tolerance of corals and the success of coral reef restoration efforts. The 2014-2016 global coral bleaching event has sharpened the focus on such interventionist approaches. We highlight the necessity for consideration of alternative (e.g., hybrid) ecosystem states, discuss traits of resilient corals and coral reef ecosystems, and propose a decision tree for incorporating assisted evolution into restoration initiatives to enhance climate resilience of coral reefs.

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Prospects for coral persistence through increasingly frequent and extended heatwaves seem bleak. Coral recovery from bleaching is only known to occur after temperatures return to normal, and mitigation of local stressors does not appear to augment coral survival. Capitalizing on a natural experiment in the equatorial Pacific, we track individual coral colonies at sites spanning a gradient of local anthropogenic disturbance through a tropical heatwave of unprecedented duration. Unexpectedly, some corals survived the event by recovering from bleaching while still at elevated temperatures. These corals initially had heat-sensitive algal symbiont communities, endured bleaching, and then recovered through proliferation of heat-tolerant symbionts. This pathway to survival only occurred in the absence of strong local stressors. In contrast, corals in highly disturbed areas were already dominated by heat-tolerant symbionts, and despite initially resisting bleaching, these corals had no survival advantage in one species and 3.3 times lower survival in the other. These unanticipated connections between disturbance, coral symbioses and heat stress resilience reveal multiple pathways to coral survival through future prolonged heatwaves.

The establishment of coral microbial communities in early developmental stages is fundamental to coral fitness, but its drivers are largely unknown, particularly for bacteria. Using an in situ reciprocal transplant experiment, we examined the influence of parental, planulation and early recruit environments on the microbiome of brooded offspring in the coral Pocillopora damicornis. 16S rRNA and ITS2 rDNA gene metabarcoding showed that bacterial and microalgal endosymbiont communities varied according to parental and planulation environments, but not with early recruit environment. Only a small number of bacterial strains were shared between offspring and their respective parents, revealing bacterial establishment as largely environmentally driven in very early life stages. Conversely, microalgal communities of recruits were highly similar to those of their respective parents, but also contained additional low abundance strains, suggesting both vertical transmission and novel ('horizontal') acquisition. Altogether, recruits harboured more variable microbiomes compared to their parents, indicating winnowing occurs as corals mature.

The world's coral reefs are under unparalleled pressure due to climate change, stimulating research focused on preventing further damage and loss in these ecosystems. The coral microbiome has been widely acknowledged as crucial to coral health and function, playing multiple roles in key biological processes. Recent empirical studies suggest that microbes may contribute to coral host tolerance of thermal stress, and harnessing these benefits through microbiome engineering (ME) may provide a mechanism for enhancing climate resilience in corals. Although coral ME is in its infancy, similar and successful ME approaches that are already underway in other fields – including agriculture, medicine, and wastewater treatment – may serve to guide and improve ME techniques in corals. We discuss current applications of ME, identify three key research priorities that will help elucidate the viability of ME for corals, and consider the implications of using these approaches for reef restoration.

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The coral microbiome is known to fluctuate in response to environmental variation and has been suggested to vary seasonally. However, most studies to date, particularly studies on bacterial communities, have examined temporal variation over a time frame of less than 1 year, which is insufficient to establish if microbiome variations are indeed seasonal in nature. The present study focused on expanding our understanding of long-term variability in microbial community composition using two common coral species, Acropora hyacinthus , and Acropora spathulata , at two mid-shelf reefs on the Great Barrier Reef. By sampling over a 2-year time period, this study aimed to determine whether temporal variations reflect seasonal cycles. Community composition of both bacteria and Symbiodiniaceae was characterized through 16S rRNA gene and ITS2 rDNA metabarcoding. We observed significant variations in community composition of both bacteria and Symbiodiniaceae among time points for A. hyacinthus and A. spathulata . However, there was no evidence to suggest that temporal variations were cyclical in nature and represented seasonal variation. Clear evidence for differences in the microbial communities found between reefs suggests that reef location and coral species play a larger role than season in driving microbial community composition in corals. In order to identify the basis of temporal patterns in coral microbial community composition, future studies should employ longer time series of sampling at sufficient temporal resolution to identify the environmental correlates of microbiome variation.