Reef-building corals are obligate, mutualistic symbioses of heterotrophic animals and phototrophic dinoflagellates (Symbiodinium spp.). Contrary to the earlier, widely accepted belief that corals harbour only one symbiont, we found that the ecologically dominant Caribbean corals Montastraea annularis and M. faveolata can act as hosts to dynamic, multi-species communities of Symbiodinium. Composition of these communities follows gradients of environmental irradiance, implying that physiological acclimatization is not the only mechanism by which corals cope with environmental heterogeneity. The importance of this diversity was underlined by analysis of a natural episode of coral bleaching. Patterns of bleaching could be explained by the preferential elimination of a symbiont associated with low irradiance from the brightest parts of its distribution. Comparative analyses of symbionts before and after bleaching from the same corals supported this interpretation, and suggested that some corals were protected from bleaching by hosting an additional symbiont that is more tolerant of high irradiance and temperature. This 'natural experiment' suggests that temporal and spatial variability can favour the coexistence of diverse symbionts within a host, despite the potential for destabilizing competition among them.

Many corals bleach as a result of increased seawater temperature, which causes them to lose their vital symbiotic algae (Symbiodinium spp.) - unless these symbioses are able to adapt to global warming, bleaching threatens coral reefs worldwide. Here I show that some corals have adapted to higher temperatures, at least in part, by hosting specifically adapted Symbiodinium. If other coral species can host these or similar Symbiodinium taxa, they might adapt to warmer habitats relatively easily.

All reef-building corals are obligately associated with photosynthetic microalgal endosymbionts called zooxanthellae. Zooxanthella taxonomy has emphasized differences between species of hosts, but the possibility of ecologically significant zooxanthella diversity within hosts has been the subject of speculation for decades. Analysis of two dominant Caribbean corals showed that each associates with three taxa of zooxanthellae that exhibit zonation with depth-the primary environmental gradient for light-dependent marine organisms. Some colonies apparently host two taxa of symbionts in proportions that can vary across the colony. This common occurrence of polymorphic, habitat-specific symbioses challenges conventional understanding of the units of biodiversity but also illuminates many distinctive aspects of marine animal-algal associations. Habitat specificity provides ecological explanations for the previously documented poor concordance between host and symbiont phylogenies and the otherwise surprising lack of direct, maternal transmission of symbionts in many species of hosts. Polymorphic symbioses may underlie the conspicuous and enigmatic variability characteristic of responses to environmental stress (e.g., coral "bleaching") and contribute importantly to the phenomenon of photoadaptation.Montastraea annularis sensu lato is the predominant reefbuilding coral of the Caribbean Sea (1). In shallow to intermediate depths, it consists of three "sibling" species that are morphologically and genetically distinct (2): M. annularis (Ellis and Solander, 1786) sensu stricto plus the recently resurrected M. faveolata (Ellis and Solander, 1786) and M. franksi (Gregory, 1895) (3). Like all other reef-building corals, these species are obligately associated with symbiotic dinoflagellates that, as far as is known, belong to the genus Symbiodinium (4). Diversity among these microalgae (4-7), commonly referred to as zooxanthellae, can be recognized in some instances by restriction fragment length polymorphism (RFLP) in small ribosomal subunit RNA (ssRNA) genes (8, 9). We used this method to assess zooxanthella diversity in these corals on Panamanian reefs at depths of 0-14 m.5 MATERIALS AND METHODS Samples were collected from apparently healthy coral colonies at Salar-1 (June 1992) and Aguadargana (April 1992 and January 1993) reefs (3) in San Blas, Panama. These two sites are protected and semi-exposed, respectively. At the depths sampled, they consist of mixed species assemblages in which the three sibling species overlap in distribution and are easily identified by their characteristic colony morphologies (2, 3). Sampled colonies were in open, unshaded areas; they were otherwise selected haphazardly across the sampled depth range, without regard to colony color. Conspecific samples were taken from colonies separated by at least 5 m. Samples were frozen on dry ice and stored at -70°C. After thawing, zooxanthella DNA was isolated (9) from 5-10 cm2 of tissue; MgSO4 was omitted from the zooxanthella isolation buffer.Fo...

Zooxanthellae are unicellular algae that occur as endosymbionts in many hundreds of marine invertebrate species. Because zooxanthellae have traditionally been difficult to classify, little is known about the natural history of these symbioses. Zooxanthellae were isolated from 131 individuals in 22 host taxa and characterized by the use of restriction fragment length polymorphisms (RFLPs) in nuclear genes that encode small ribosomal subunit RNA (ssRNA). Six algal RFLPs, distributed host species specifically, were detected. Individual hosts contained one algal RFLP. Zooxanthella phylogenetic relationships were estimated from 22 algal ssRNA sequences-one from each host species. Closely related algae were found in dissimilar hosts, suggesting that animal and algal lineages have maintained a flexible evolutionary relation with each other.