High physiological function for corals with thermally tolerant, host-adapted symbionts.

The flexibility to associate with more than one symbiont may considerably expand a host's niche breadth. Coral animals and dinoflagellate micro-algae represent one of the most functionally integrated and widespread mutualisms between two eukaryotic partners. Symbiont identity greatly affects a coral's ability to cope with extremes in temperature and light. Over its broad distribution across the Eastern Pacific, the ecologically dominant branching coral, Pocillopora grandis, depends on mutualisms with the dinoflagellates Durusdinium glynnii and Cladocopium latusorum. Measurements of skeletal growth, calcification rates, total mass increase, calyx dimensions, reproductive output and response to thermal stress were used to assess the functional performance of these partner combinations. The results show both host-symbiont combinations displayed similar phenotypes; however, significant functional differences emerged when exposed to increased temperatures. Negligible physiological differences in colonies hosting the more thermally tolerant D. glynnii refute the prevailing view that these mutualisms have considerable growth tradeoffs. Well beyond the Eastern Pacific, pocilloporid colonies with D. glynnii are found across the Pacific in warm, environmentally variable, near shore lagoonal habitats. While rising ocean temperatures threaten the persistence of contemporary coral reefs, lessons from the Eastern Pacific indicate that co-evolved thermally tolerant host-symbiont combinations are likely to expand ecologically and spread geographically to dominate reef ecosystems in the future.

Formal recognition of host-generalist species of dinoflagellate (Cladocopium, Symbiodiniaceae) mutualistic with Indo-Pacific reef corals.

The existence of widespread species with the capacity to endure diverse, or variable, environments are of importance to ecological and genetic research, and conservation. Such "ecological generalists" are more likely to have key adaptations that allow them to better tolerate the physiological challenges of rapid climate change. Reef-building corals are dependent on endosymbiotic dinoflagellates (Family: Symbiodiniaceae) for their survival and growth. While these symbionts are biologically diverse, certain genetic types appear to have broad geographic distributions and are mutualistic with various host species from multiple genera and families in the order Scleractinia that must acquire their symbionts through horizontal transmission. Despite the considerable ecological importance of putative host-generalist symbionts, they lack formal species descriptions. In this study, we used molecular, ecological, and morphological evidence to verify the existence of five new host-generalist species in the symbiodiniacean genus Cladocopium. Their geographic distribution and prevalence among host communities corresponds to prevailing environmental conditions at both regional and local scales. The influence that each species has on host physiology may partially explain regional differences in thermal sensitivities among coral communities. The potential increased prevalence of a generalist species that endures environmental instability is a consequential ecological response to warming oceans. Large-scale shifts in symbiont dominance could ensure reef coral persistence and productivity in the near term. Ultimately, these formal designations should advance scientific communication and generate informed research questions on the physiology and ecology of coral-dinoflagellate mutualisms.

Similarities in biomass and energy reserves among coral colonies from contrasting reef environments.

Coral reefs are declining worldwide, yet some coral populations are better adapted to withstand reductions in pH and the rising frequency of marine heatwaves. The nearshore reef habitats of Palau, Micronesia are a proxy for a future of warmer, more acidic oceans. Coral populations in these habitats can resist, and recover from, episodes of thermal stress better than offshore conspecifics. To explore the physiological basis of this tolerance, we compared tissue biomass (ash-free dry weight cm-2), energy reserves (i.e., protein, total lipid, carbohydrate content), and several important lipid classes in six coral species living in both offshore and nearshore environments. In contrast to expectations, a trend emerged of many nearshore colonies exhibiting lower biomass and energy reserves than colonies from offshore sites, which may be explained by the increased metabolic demand of living in a warmer, acidic, environment. Despite hosting different dinoflagellate symbiont species and having access to contrasting prey abundances, total lipid and lipid class compositions were similar in colonies from each habitat. Ultimately, while the regulation of colony biomass and energy reserves may be influenced by factors, including the identity of the resident symbiont, kind of food consumed, and host genetic attributes, these independent processes converged to a similar homeostatic set point under different environmental conditions.

Mutualistic microalgae co-diversify with reef corals that acquire symbionts during egg development.

The application of molecular genetics has reinvigorated and improved how species are defined and investigated scientifically, especially for morphologically cryptic micro-organisms. Here we show how species recognition improves understanding of the ecology and evolution of mutualisms between reef-building corals and their mutualistic dinoflagellates (i.e. Symbiodiniaceae). A combination of genetic, ecological, and morphological evidence defines two sibling species of Cladocopium (formerly Symbiodinium Clade C), specific only to host corals in the common genus Pocillopora, which transmit their obligate symbionts during oogenesis. Cladocopium latusorum sp. nov. is symbiotic with P. grandis/meandrina while the smaller-celled C. pacificum sp. nov. associates with P. verrucosa. Both symbiont species form mutualisms with Pocillopora that brood their young. Populations of each species, like their hosts, are genetically well connected across the tropical and subtropical Pacific Ocean, indicating a capacity for long-range dispersal. A molecular clock approximates their speciation during the late Pliocene or early Pleistocene as Earth underwent cycles of precipitous cooling and warming; and corresponds to when their hosts were also diversifying. The long temporal and spatial maintenance of high host fidelity, as well as genetic connectivity across thousands of kilometers, indicates that distinct ecological attributes and close evolutionary histories will restrain the adaptive responses of corals and their specialized symbionts to rapid climate warming.

Phylogeographic patterns in the Philippine archipelago influence symbiont diversity in the bobtail squid-Vibrio mutualism.

Marine microbes encounter a myriad of biotic and abiotic factors that can impact fitness by limiting their range and capacity to move between habitats. This is especially true for environmentally transmitted bacteria that cycle between their hosts and the surrounding habitat. As geologic history, biogeography, and other factors such as water temperature, salinity, and physical barriers can inhibit bacterial movement to novel environments, we chose to examine the genetic architecture of Euprymna albatrossae (Mollusca: Cephalopoda) and their Vibrio fischeri symbionts in the Philippine archipelago using a combined phylogeographic approach. Eleven separate sites in the Philippine islands were examined using haplotype estimates that were examined via nested clade analysis to determine the relationship between E. albatrossae and V. fischeri populations and their geographic location. Identical analyses of molecular variance (AMOVA) were used to estimate variation within and between populations for host and symbiont genetic data. Host animals demonstrated a significant amount of variation within island groups, while symbiont variation was found within individual populations. Nested clade phylogenetic analysis revealed that hosts and symbionts may have colonized this area at different times, with a sudden change in habitat. Additionally, host data indicate restricted gene flow, whereas symbionts show range expansion, followed by periodic restriction to genetic flow. These differences between host and symbiont networks indicate that factors "outside the squid" influence distribution of Philippine V. fischeri. Our results shed light on how geography and changing environmental factors can impact marine symbiotic associations at both local and global scales.