Diseases of tropical reef organisms is an intensive area of study, but despite significant advances in methodology and the global knowledge base, identifying the proximate causes of disease outbreaks remains difficult. The dynamics of infectious wildlife diseases are known to be influenced by shifting interactions among the host, pathogen, and other members of the microbiome, and a collective body of work clearly demonstrates that this is also the case for the main foundation species on reefs, corals. Yet, among wildlife, outbreaks of coral diseases stand out as being driven largely by a changing environment. These outbreaks contributed not only to significant losses of coral species but also to whole ecosystem regime shifts. Here we suggest that to better decipher the disease dynamics of corals, we must integrate more holistic and modern paradigms that consider multiple and variable interactions among the three major players in epizootics: the host, its associated microbiome, and the environment. In this perspective, we discuss how expanding the pathogen component of the classic host-pathogen-environment disease triad to incorporate shifts in the microbiome leading to dysbiosis provides a better model for understanding coral disease dynamics. We outline and discuss issues arising when evaluating each component of this trio and make suggestions for bridging gaps between them. We further suggest that to best tackle these challenges, researchers must adjust standard paradigms, like the classic one pathogen-one disease model, that, to date, have been ineffectual at uncovering many of the emergent properties of coral reef disease dynamics. Lastly, we make recommendations for ways forward in the fields of marine disease ecology and the future of coral reef conservation and restoration given these observations.

Echinoderms, positioned taxonomically at the base of deuterostomes, provide an important system for the study of the evolution of the immune system. However, there is little known about the cellular components and genes associated with echinoderm immunity. The 2013–2014 sea star wasting disease outbreak is an emergent, rapidly spreading disease, which has led to large population declines of asteroids in the North American Pacific. While evidence suggests that the signs of this disease, twisting arms and lesions, may be attributed to a viral infection, the host response to infection is still poorly understood. In order to examine transcriptional responses of the sea star Pycnopodia helianthoides to sea star wasting disease, we injected a viral sized fraction (0.2 μm) homogenate prepared from symptomatic P. helianthoides into apparently healthy stars. Nine days following injection, when all stars were displaying signs of the disease, specimens were sacrificed and coelomocytes were extracted for RNA-seq analyses. A number of immune genes, including those involved in Toll signaling pathways, complement cascade, melanization response, and arachidonic acid metabolism, were differentially expressed. Furthermore, genes involved in nervous system processes and tissue remodeling were also differentially expressed, pointing to transcriptional changes underlying the signs of sea star wasting disease. The genomic resources presented here not only increase understanding of host response to sea star wasting disease, but also provide greater insight into the mechanisms underlying immune function in echinoderms.

Outbreaks of marine infectious diseases have caused widespread mass mortalities, but the lack of baseline data has precluded evaluating whether disease is increasing or decreasing in the ocean. We use an established literature proxy method from Ward and Lafferty (Ward and Lafferty 2004 PLoS Biology 2 , e120 ( doi:10.1371/journal.pbio.0020120 )) to analyse a 44-year global record of normalized disease reports from 1970 to 2013. Major marine hosts are combined into nine taxonomic groups, from seagrasses to marine mammals, to assess disease swings, defined as positive or negative multi-decadal shifts in disease reports across related hosts. Normalized disease reports increased significantly between 1970 and 2013 in corals and urchins, indicating positive disease swings in these environmentally sensitive ectotherms. Coral disease reports in the Caribbean correlated with increasing temperature anomalies, supporting the hypothesis that warming oceans drive infectious coral diseases. Meanwhile, disease risk may also decrease in a changing ocean. Disease reports decreased significantly in fishes and elasmobranchs, which have experienced steep human-induced population declines and diminishing population density that, while concerning, may reduce disease. The increases and decreases in disease reports across the 44-year record transcend short-term fluctuations and regional variation. Our results show that long-term changes in disease reports coincide with recent decades of widespread environmental change in the ocean.

Co-infection is the reality in natural populations, but few studies incorporate the players that matter in the wild. We integrate the environment, host demography, two parasites, and host immunity in a study of co-infection to determine the drivers of parasite interactions. Here, we use an ecologically important Caribbean sea fan octocoral, Gorgonia ventalina, that is co-infected by a copepod and a labyrinthulid protist. We first expanded upon laboratory studies by showing that immune suppression is associated with the labyrinthulid in a natural setting. Histological analyses revealed that immune cells (amoebocytes) were significantly suppressed in both labyrinthulid infections and co-infections relative to healthy sea fans, but remained unchanged in copepod infections. However, surveys of natural coral populations demonstrated a critical role for the environment and host demography in this co-infection: the prevalence of copepod infections increased with sea fan size while labyrinthulid prevalence increased with water depth. Although we predicted that immune suppression by the labyrinthulid would facilitate copepod infection, the two parasites did not co-occur in the sea fans more often than expected by chance. These results suggest that the distinct ecological drivers for each parasite overwhelm the role of host immune suppression in determining the distribution of parasites among hosts. This interplay of the environment and parasite-mediated immune suppression in sea fan co-infection provides insights into the factors underlying co-occurrence patterns in wild co-infections. Moving forward, simultaneous consideration of co-occurring parasites, host traits, and the environmental context will improve the understanding of host - parasite interactions and their consequences.

The response of corals to warm temperature anomalies includes changes in coral bacterial assemblages. There are clear differences between the microbiota of bleached and healthy corals. However, few studies have tracked the microbiota of individual colonies throughout a warming event. We used 454 pyrosequencing and repeated measures to characterize bacterial assemblages in 15 Gorgonia ventalina colonies before, during, 4 months after, and 1 year after the 2010 Caribbean warm thermal anomaly. In the latter three sampling times, the G. ventalina microbiota differed significantly from the microbiota of Orbicella faveolata colonies, which were sampled only at these three times. O. faveolata microbiota did not exhibit coordinated shifts through time. Notably, the microbiota of the repeatedly sampled G. ventalina colonies shifted persistently from before to during, after, and long after the warming event. The same pattern emerges from the norm of reaction for the individual G. ventalina colonies. This is the first study to show persistent shifts in coral microbiota in association with a warm thermal anomaly. Whether shifting microbiota is adaptive or maladaptive, the lasting change in bacterial assemblages following this warming event identifies a new way that coral microbiota shape the response of coral colonies under thermal stress.