The existence of coral reef ecosystems relies critically on the mutualistic relationship between calcifying cnidarians and photosynthetic, dinoflagellate endosymbionts in the genus Symbiodinium. Reef-corals have declined globally due to anthropogenic stressors, for example, rising sea-surface temperatures and pollution that often disrupt these symbiotic relationships (known as coral bleaching), exacerbating mass mortality and the spread of disease. This threatens one of the most biodiverse marine ecosystems providing habitats to millions of species and supporting an estimated 500 million people globally (Hoegh-Guldberg et al. 2007). Our understanding of cnidarian–dinoflagellate symbioses has improved notably with the recent application of genomic and transcriptomic tools (e.g. Voolstra et al. 2009; Bayer et al. 2012; Davy et al. 2012), but a model system that allows for easy manipulation in a laboratory environment is needed to decipher underlying cellular mechanisms important to the functioning of these symbioses. To this end, the sea anemone Aiptasia, otherwise known as a ‘pest’ to aquarium hobbyists, is emerging as such a model system (Schoenberg & Trench 1980; Sunagawa et al. 2009; Lehnert et al. 2012). Aiptasia is easy to grow in culture and, in contrast to its stony relatives, can be maintained aposymbiotically (i.e. dinoflagellate free) with regular feeding. However, we lack basic information on the natural distribution and genetic diversity of these anemones and their endosymbiotic dinoflagellates. These data are essential for placing the significance of this model system into an ecological context. In this issue of Molecular Ecology, Thornhill et al. (2013) are the first to present genetic evidence on the global distribution, diversity and population structure of Aiptasia and its associated Symbiodinium spp. By integrating analyses of the host and symbiont, this research concludes that the current Aitpasia taxonomy probably needs revision and that two distinct Aiptasia lineages are prevalent that have probably been spread through human activity. One lineage engages in a specific symbiosis with Symbiodinium minutum throughout the tropics, whereas a second, local Aiptasia sp. population in Florida appears more flexible in partnering with more than one symbiont. The existence of symbiont-specific and symbiont-flexible Aiptasia lineages can greatly complement laboratory-based experiments looking into mechanisms of symbiont selectivity. In a broader context, the study by Thornhill et al. (2013) should inspire more studies to target the natural environment of model systems in a global context targeting all participating member species when establishing ecological and genetic baselines.
The advent of model systems in the last century to study specific aspects of organismal biology paved the way to scientific discovery. While initially the characterization and understanding of the natural environment of a particular model species was not in the focus of interest, this notion has changed. Today the fruit fly, house mouse or thale cress Arabidopsis thaliana are not only invaluable model systems to study gene function, development, or disease, but are used in studies to understand evolution and adaptation on a molecular level (Eyre-Walker 2006; Voolstra et al. 2007; Hancock et al. 2011). Environmental change and worldwide ecosystem degradation have heightened the need to understand species' resilience and adaptive capabilities in their natural environment. The continuous decline of coral reefs, for instance, has called to an understanding of the symbiosis between coral hosts and dinoflagellate symbionts that provide the basis of this ecosystem. In recent years, Aiptasia is being developed as a tractable model for cnidarian–dinoflagellate symbiosis (Fig. 1). In contrast to the development of the ‘classic’ model organisms, an understanding of the ecological context and natural environment of this genus is crucial for our ability to conduct meaningful experiments and to correctly interpret data regarding symbiotic function, specificity and flexibility.
The specificity and biogeography of host and symbiont populations
The findings of Thornhill et al. (2013) contribute significantly to the value of the Aiptasia as a model system. While the system not only offers useful characteristics such as ease of culturing and propagation, it also seems to be less complex than previously thought. Rather than confirming the presence of 2 globally distributed species (i.e. A. pulchella and A. pallida) (Fautin 2011), the authors determined the existence of a ‘global’ (i.e. present in Australia, Bermuda, Hawaii, Japan and the Red Sea) and a ‘local’ (i.e. present in Florida) genetically distinct lineages that differ in their symbiont specificity. Furthermore, the organismal distributions that the authors identified did not conform to any of the 16 Aiptasia species that are considered valid (Fautin 2011), but further work is needed to unequivocally resolve this controversy. Nevertheless, the study highlights how molecular genetic data can validate or dispute traditional species designations.
The population structure of the associated Symbiodinium symbionts revealed several interesting findings. The genus Symbiodinium is a diverse and heterogeneous group consisting of nine divergent clades (A-I) (Pochon & Gates 2010) that can be further subdivided into types and species (Sampayo et al. 2009) (Fig. 2). In contrast to what has been observed in other systems, anemones of the ‘global’ Aiptasia population associated exclusively with Symbiodinium minutum within clade B and did not exhibit significant population genetic structure. This suggests that dispersal and gene flow maintain connectivity among many sampling localities and over tremendous distances, most likely from vectored introductions (such as ballast, fouling of ships, aquaculture or the aquarium trade) as observed connectivity did not correspond to major ocean currents. Although the study used a comparatively small number of molecular markers, the microsatellites used exhibited high allelic diversity in other studies emphasizing the utility of these loci. The ‘local’ Aiptasia population, in contrast, was more flexible and associated at differing frequencies with Symbiodinium spp. from clades A and C, in addition to S. minutum.
Combining population genetic data from Aiptasia and Symbiodinium, this study shows that host–symbiont pairings in this system are highly structured as genetic differences in the host anemones correlated with both, genetic differences in the symbiont as well as the degree of symbiotic flexibility in Aiptasia–Symbiodinium associations. While this not only indicates that a certain level of coevolution exists, it exemplifies the ability of Symbiodinium population genetic data to reveal patterns for both the host and endosymbiont, and strongly stimulates conducting population genetic studies in a global context and with the incorporation of data from all participating member species.
Poised for a surge in knowledge about cnidarian–dinoflagellate symbiosis
The sea anemone Aiptasia and its dinoflagellate symbionts provide a powerful model system for the study of cnidarian–dinoflagellate symbioses, the building block of coral reef ecosystems. Thornhill et al. (2013) further add to this notion. The existence of 2 genetically distinct Aiptasia populations (‘global’ and ‘local’) with differing symbiont specificities (‘specific’ and ‘flexible’) provides a structure in which we are able to study adaptation and evolution in host–symbiont pairings as well as the cellular mechanisms of specificity and flexibility of symbioses. Despite the apparent specificity of the ‘global’ Aiptasia to form symbioses with S. minutum in nature, it may be possible to induce symbioses with different Symbiodinium spp. under experimental settings. This option should be further explored, as it provides an opportunity to gain insight into potential environmental conditions that are able to alter symbiont specificity. Furthermore, Aiptasia, in contrast to its coral relatives, do not calcify, complementing the picture of cnidarian model systems from nonsymbiotic, noncalcifying (Nematostella sp.) over symbiotic, noncalcifying (Aiptasia sp.) to symbiotic, calcifying (e.g. Stylphora pistillata or Acropora digitifera), which should make for exciting comparative genome studies. The availability of current genomic data centred on Aiptasia that originated from Florida (Sunagawa et al. 2009; Lehnert et al. 2012) will greatly facilitate the development of resources for the ‘global’ lineage and will allow conducting analyses in an evolutionary comparative framework. Future studies should meticulously incorporate experimental data from ‘global’ Aiptasia, highlighted by their highly specific, invariant symbiotic system, and compare these data to experiments conducted under the flexible symbiont biology of ‘local’ Aiptasia. Further, we have a model system with the ability to culture both symbiotic partners, together or in isolation from each other. This strongly facilitates experimental studies and manipulation. Last, genetic manipulations of Aiptasia hosts (Dunn et al. 2007) and Symbiodinium symbionts (ten Lohuis & Miller 1998) have been shown to work in principle and should be further developed in order to expand the genomics toolbox available. In this regard, the work by Thornhill et al. (2013) marks the beginning and not the end of studying cnidarian–dinoflagellate symbioses in a model system framework, together with the understanding that providing an ecological and phylogenetic context to model organisms might be invaluable to inform and device laboratory-based experiments.
The article was written by C.R.V. C.R.V. is an Assistant Professor at the Red Sea Research Center in KAUST studying and sequencing the coral Stylophora pistillata, its associated symbiont Symbiodinium microadriaticum as well as associated bacteria.