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High Diversity and Host Specificity Observed Among Symbiotic Coral Reefs (2004) 23: 596–603 DOI 10.1007/s00338-004-0428-4 REPORT Todd C. LaJeunesse Æ Daniel J. Thornhill Evelyn F. Cox Æ Frank G. Stanton Æ William K. Fitt Gregory W. Schmidt High diversity and host specificity observed among symbiotic dinoflagellates in reef coral communities from Hawaii Received: 22 October 2003 / Accepted: 30 July 2004 / Published online: 11 September 2004 Ó Springer-Verlag 2004 Abstract The Hawaiian Islands represent one of the Introduction most geographically remote locations in the Indo- Pacific, and are a refuge for rare, endemic life. The Encircled by the waters of the North American diversity of symbiotic dinoflagellates (Symbiodinium sp.) Countercurrent, the Hawaiian archipelago is among inhabiting zooxanthellate corals and other symbiotic the most isolated subtropical regions in the Indo-Pa- cnidarians from the High Islands region was surveyed. cific (Simon 1987; Veron 1995). Due to its limited From the 18 host genera examined, there were 20 exchange with other central Pacific reef systems, Ha- genetically distinct symbiont types (17 in clade C, 1 in waii has the highest number of endemic corals in the clade A, 1 in clade B, and 1 in clade D) distinguished by Pacific (Hughes et al. 2002) and may potentially be a internal transcribed spacer region 2 sequences. Most place of unusual symbiont-host combinations. ‘‘types’’ were found to associate with a particular host Although, the Hawaiian High Islands experienced genus or species and nearly half of them have not been some coral bleaching in 1996, Hawaii’s high latitude identified in surveys of Western and Eastern Pacific and proximity to up-welled cold eastern Pacific waters hosts. A clear dominant generalist symbiont is lacking has mostly spared its corals from the severe bleaching among Hawaiian cnidarians. This is in marked contrast and mortality accompanying abnormally warm sea- with the symbiont community structures of the western surface temperatures associated with El Nino-Southern Pacific and Caribbean, which are dominated by a few ˜ Oscillations (Jokiel and Brown 2004). Such events prevalent generalist symbionts inhabiting numerous host have severely impacted shallow reef systems through- taxa. Geographic isolation, low host diversity, and a out the Indo-Pacific and Caribbean (Hoegh-Guldberg high proportion of coral species that directly transmit 1999) and have led, in some cases, to community their symbionts from generation to generation are shifts among coral taxa and their symbionts (Glynn implicated in the formation of a coral reef community et al. 2001; Loya et al. 2001). Collectively, these exhibiting high symbiont diversity and specificity. geographic, environmental, and biological attributes prompted our investigation of coral-algal symbioses in this region of the tropics. Communicated by H.R. Lasker We have learned much about the diversity, ecology, T. C. LaJeunesse (&) Æ D. J. Thornhill Æ G. W. Schmidt and evolution of Symbiodinium spp. and their host Department of Plant Biology, relations through the use of molecular genetic markers University of Georgia, GA 30602, USA (e.g. Rowan and Powers 1991; Rowan et al. 1997; E-mail: lajeunes@fiu.edu Baker and Rowan 1997; Coffroth et al. 2001; LaJeu- Tel.: +1-305-348 1317 Fax: +1-305-348 1986 nesse 2002; Baker 2003; LaJeunesse et al. 2003; Santos et al. 2004). Numerous biological, hydrogeological, T. C. LaJeunesse Æ D. J. Thornhill Æ W. K. Fitt Department of Ecology, University of Georgia, environmental, and historical factors determine the GA 30602, USA diversity of corals in a particular location (Veron 1995). For Symbiodinium spp., the taxonomic diversity E. F. Cox Department of Zoology, and relative abundance of host taxa (i.e. habitat Hawaii Institute of Marine Biology, USA diversity and availability from the symbiont point of view) seem to be an additional axis governing their F. G. Stanton Department of Biology, evolutionary diversification and ecological distribution Leeward Community College, Hawaii, USA (LaJeunesse 2002). Host communities are usually 597 dominated by few symbionts that occupy a broad LaJeunesse (2002). Products from these PCR reactions range of host taxa; however, host-specific, regionally were electrophoresed on denaturing gradient gels endemic, and/or ecologically rare lineages comprise the (45–80%) using a CBScientific system (Del Mar, CA). majority of symbiont diversity (>90%) (LaJeunesse As described in detail by LaJeunesse (2002) and 2002; LaJeunesse et al. 2003, 2004). These observa- LaJeunesse et al. (2003), prominent bands characteristic tions suggest that niche partitioning through host of each unique fingerprint/profile were excised, ream- specialization and geographic isolation is important in plified, and sequenced. symbiont speciation (Futuyma and Moreno 1988). The redundancy PCR-DGGE and direct sequencing The evaluation of Symbiodinium spp. diversity in provides an important cross check of sequence identity Hawaii, as assessed by ribosomal internal transcribed with migration characteristics. PCR-DGGE also pro- spacer (ITS) DNA, was conducted under the same duces a fingerprint that shows dominant sequences methods and criteria as carried out on other reefs attributed to either intragenomic variation across (LaJeunesse 2002; LaJeunesse et al. 2003, 2004). The multiple ribosomal loci and/or the presence of multiple enumeration of the symbiont diversity and patterns of symbiont types (LaJeunesse 2002). A large proportion host association from this highly endemic, sub-prov- of ribosomal variants reported by investigators ince of the Pacific contributes to our understanding of sequencing ‘blindly’ appear to be artifacts, possibly Symbiodinium spp. biogeography, host specificity, and resulting from PCR and cloning errors (Speksnijder evolution. Moreover, the relatively low host diversity et al. 2001). Perhaps a greater source of variation is at this location allows a test of the hypothesis that from the sequencing of rare variants (occurring biological interactions influence the apparent inverse throughout the repeat region, but low in copy num- relation between host and symbiont diversity. ber) that are not indicative of a genome’s entire ribosomal array (Diekmann et al. 2003; LaJeunesse et al., unpublished). Materials and methods Collections Phylogenetic analyses Host Cnidarians (multiple individuals from each tax- on) were collected using SCUBA or mask and snorkel Sequences were aligned manually using Sequence from Kaneohe Bay on the southeastern side of Oahu, Navigator version 1.0 software (ABI, Division of and from Haleiwa Trench, Wailua Bay on its north Perkin-Elmer, Foster City, CA). Sister lineages Fr1 shore. Coral fragments of 3–5 cm2 were stripped of (sensu Pochon et al. 2001) and type F1 in clade F tissue using an airbrush (Baker and Rowan 1997) and (Symbiodinium kawagutii (LaJeunesse 2001)) were used the resultant slurry of mucus, animal cell debris, and as outgroups (Genbank sequences AJ291520 and dinoflagellates was homogenized using a Tissue Tearor AF333515). ITS sequences among clade C types have a homogenizer (Biospec Ind.). After centrifugation at high proportion of invariant characters (only 17 800–1,000 g, the resulting algal pellets were transferred characters out of 308 are parsimony-informative). Base to a 1.5-ml microcentrifuge tube and preserved in 20% substitutions across the ITS rDNA in these Symbi- dimethylsulfoxide (DMSO), 0.25 M EDTA, sodium odinium spp. are far from approaching saturation. chloride-saturated water solution (Seutin et al. 1991). Therefore, maximum parsimony (under heuristic The symbionts from soft-bodied Actinarian, Zoanthi- search mode), which does not assume a particular dian, and Scyphozoan taxa were isolated as previously model of molecular evolution and allows for use of described (LaJeunesse 2002). Porites compressa and informative sequence gaps and insertions (considered a Montipora capitata (= verrucosa Maragos 1995), 5th character state), is thus a conservative method for displaying wide morphological variation under identi- phylogenetic inference of clade C. Maximum likeli- cal environmental conditions, were sampled extensively hood and neighbor-joining analyses (with gaps ex- to determine if any of these showed differences in their cluded) were also performed on the data using PAUP* symbiont affiliations. V. 4.0b10 software (Swofford 1999). A fourth method of phylogenetic inference using Baysian statistics was implemented using the software MrBayes version 3.0b4 DNA extractions, PCR-DGGE, and sequencing (Huelsenbeck and Ronquiest 2001). Under the HKY85 and general time reversible (GTR) models of sequence Nucleic acid extractions on 10 to 30 mg of dinoflagellate evolution, beginning with an unspecified tree topology, material were conducted using a modified Promega log probability of observing the data plateaued Wizard genomic DNA extraction protocol (LaJeunesse reaching stationarity early between 10,000 and 20,000 et al. 2003). The internal transcribed spacer region (ITS) generations. Both one-hundred thousand and one 2 was amplified from each extract using primers ‘‘ITS 2 million generations (with no discard, i.e. no burn-in, clamp’’ and ‘‘ITSintfor 2’’ (LaJeunesse and Trench hence probabilities are conservative estimates) under 2000) with the touch-down thermal cycle given in repeated trials produced near identical values. 598 The occurrence of a particular symbiont in the ecosys- Results tem was therefore dependent on the presence of a par- ticular host taxon. Because a majority of host species A total of 20 distinctive
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