Host species often support a genetically diverse guild of symbionts, the identity and performance of which can determine holobiont fitness under particular environmental conditions. These symbiont communities are structured by a complex set of potential interactions, both positive and negative, between the host and symbionts and among symbionts. In reef‐building corals, stable associations with specific symbiont species are common, and we hypothesize that this is partly due to ecological mechanisms, such as succession and competition, which drive patterns of symbiont winnowing in the initial colonization of new generations of coral recruits. We tested this hypothesis using the experimental framework of the de Wit replacement series and found that competitive interactions occurred among symbionts which were characterized by unique ecological strategies. Aposymbiotic octocoral recruits within high‐ and low‐light environments were inoculated with one of three Symbiodiniaceae species as monocultures or with cross‐paired mixtures, and we tracked symbiont uptake using quantitative genetic assays. Priority effects, in which early colonizers excluded competitive dominants, were evidenced under low light, but these early opportunistic species were later succeeded by competitive dominants. Under high light, a more consistent competitive hierarchy was established in which competitive dominants outgrew and limited the abundance of others. These findings provide insight into mechanisms of microbial community organization and symbiosis breakdown and recovery. Furthermore, transitions in competitive outcomes across spatial and temporal environmental variation may improve lifetime host fitness.

In the face of global warming and unprecedented coral bleaching, a new avenue of research is focused on relatively rare algal symbionts and their ability to confer thermal tolerance to their host by association. Yet, thermal tolerance is just one of many physiological attributes inherent to the diversity of symbiodinians, a result of millions of years of competition and niche partitioning. Here, we revealed that competition among cocultured symbiodinians alters nutrient assimilation and compound production with species-specific responses. For Cladocopium goreaui, a species ubiquitous within stable coral associations, temperature stress increased sensitivity to competition eliciting a shift toward investment in cell replication, i.e., putative niche exploitation. Meanwhile, competition led Durusdinium trenchii, a thermally tolerant “background” symbiodinian, to divert resources from immediate growth to storage. As such, competition may be driving the dominance of C. goreaui outside of temperature stress, the destabilization of symbioses under thermal stress, the repopulation of coral tissues by D. trenchii following bleaching, and ultimately undermine the efficacy of symbiont turnover as an adaptive mechanism.

Reef-building corals owe their evolutionary success to their symbiosis with unicellular algae (Symbiodiniaceae). However, increasingly frequent heat waves lead to coral mass-bleaching events and pose a serious threat to the survival of reef ecosystems. Despite significant efforts, a mechanistic understanding of coral–algal symbiosis functioning, what leads to its breakdown and what can prevent it, remains incomplete. The main obstacles are low amenability of corals to experimental handling and, owing to its obligatory nature, the difficulties of manipulating the coral–algal association. Indeed, many studies on the symbiotic partnership are conducted on other cnidarian model organisms and their results may therefore not be fully transferable to tropical reef-building corals. Here, we identify the tropical stony coral species Galaxea fascicularis as a novel candidate coral model system. Individual polyps of this species can be separated, enabling highly replicated genotype studies, and are well suited to experimental investigation of the symbiosis as they can be easily and effectively rid of their algal symbionts (bleached). We show that bleached adult individuals can reestablish symbiosis with non-native symbionts, and we report the completion of the gametogenic cycle ex situ, with the successful spawning in aquaria over multiple years. These achievements help overcome several of the major limitations to direct research on corals and highlight the potential of G. fascicularis as an important new model system for investigations of symbiosis functioning and manipulation.

Background: Symbionts provide a variety of reproductive, nutritional, and defensive resources to their hosts, but those resources can vary depending on symbiont community composition. As genetic techniques open our eyes to the breadth of symbiont diversity within myriad microbiomes, symbiosis research has begun to consider what ecological mechanisms affect the identity and relative abundance of symbiont species and how this community structure impacts resource exchange among partners. Here, we manipulated the in hospite density and relative ratio of two species of coral endosymbionts (Symbiodinium microadriaticum and Breviolum minutum) and used stable isotope enrichment to trace nutrient exchange with the host, Briareum asbestinum. Results: The patterns of uptake and translocation of carbon and nitrogen varied with both density and ratio of symbionts. Once a density threshold was reached, carbon acquisition decreased with increasing proportions of S. microadriaticum. In hosts dominated by B. minutum, nitrogen uptake was density independent and intermediate. Conversely, for those corals dominated by S. microadriaticum, nitrogen uptake decreased as densities increased, and as a result, these hosts had the overall highest (at low density) and lowest (at high density) nitrogen enrichment. Conclusions: Our findings show that the uptake and sharing of nutrients was strongly dependent on both the density of symbionts within the host, as well as which symbiont species was dominant. Together, these complex interactive effects suggest that host regulation and the repression of in hospite symbiont competition can ultimately lead to a more productive mutualism.

Concomitant to the decline of tropical corals caused by increasing global sea temperatures is the potential removal of barriers to species range expansions into subtropical and temperate habitats. In these habitats, species must tolerate lower annual mean temperature, wider annual temperature ranges and lower minimum temperatures. To understand ecophysiological traits that will impact geographical range boundaries, we monitored populations of five coral species within a marginal habitat and used a year of in situ measures to model thermal performance of vital host, symbiont and holobiont physiology. Metabolic responses to temperature revealed two acclimatization strategies: peak productivity occurring at annual midpoint temperatures (4–6°C lower than tropical counterparts), or at annual maxima. Modelled relationships between temperature and P:R were compared to a year of daily subtropical sea temperatures and revealed that the relatively short time spent at any one temperature, limited optimal performance of all strategies to approximately half the days of the year. Thus, while subtropical corals can adjust their physiology to persist through seasonal lows, seasonal variation seems to be the key factor limiting coral productivity. This constraint on rapid reef accretion within subtropical environments provides insight into the global distribution of future coral reefs and their ecosystem services.