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<I>Heliopora Coerulea</I>

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<I>Heliopora Coerulea</I> Bull Mar Sci. 90(1):233–255. 2014 research paper http://dx.doi.org/10.5343/bms.2012.1105 Genetic structure and cryptic speciation in the threatened reef-building coral Heliopora coerulea along Kuroshio Current 1 Department of Marine Biology 1 * and Environmental Sciences, Nina Yasuda 2 University of Miyazaki, Faculty Coralie Taquet of Agriculture, Gakuen- Satoshi Nagai 3 kibanadai-nishi-1-1, Miyazaki, 4 Japan 889-2192. Miguel Fortes 5 2 Tokyo Institute of Technology Tung-Yung Fan 6 2-12-1 Ookayama, Meguro-ku, Niphon Phongsuwan Tokyo, Japan 152-8552 and UMR Kazuo Nadaoka 2 241 Ecosystèmes Insulaires Océaniens, Université de la Polynésie Française, B.P. 6570, ABSTRACT. —The blue coral Heliopora coerulea (Pallas, 98702 FAA’A Aéroport, Tahiti, French Polynesia. 1766), a reef-building coral, is the sole member of the alcyonarian order Coenothecalia. Recently, local and global 3 National Research Institute anthropogenic stresses on its habitat have led to this species of Fisheries Science, Aquatic being listed as threatened. Strong genetic differentiation has Genomics Research Center, been observed between populations of H. coerulea that have 2-12-4 Fukuura, Kanazawa-ku, been found only 500 m apart. Despite the wide geographical Yokohama, Kanagawa 236-8648, distribution of H. coerulea in the Indo-Pacific oceans, such Japan. localized genetic structuring has led to speculation about 4 Marine Science Institute CS whether H. coerulea populations are completely isolated University of the Philippines over different geographic scales (including speciation). To Diliman, Quezon City 1101, The investigate gene flow in H. coerulea, we genotyped seven Philippines and Aurora Marine Research and Development microsatellite loci in 611 H. coerulea colonies collected from Institute, Baler, Aurora, The along the Kuroshio Current. Genetic admixture analysis Philippines. and principal coordinate analysis suggested the existence of two cryptic species in the studied area. In addition, distinct 5 National Museum of Marine Biology and Aquarium, 2 typical gross morphologies were shown by both these cryptic Houwan Road, Checheng, species. Patterns of isolation by distance were more obvious Pingtung, Taiwan, R.O.C. and significant when each genetic clade was analyzed separately than when the populations were analyzed together. 6 Marine and Coastal Biology and Ecology Unit, Phuket Marine In addition, we found that some populations had extremely Biological Center, 51 Sakdidej low genotypic diversity. These findings indicate that these Rd., Muang District, Phuket populations may be more threatened than previously believed 83000, Thailand. and emphasize the threatened status of H. coerulea. * Corresponding author email: <[email protected]>. Submitted: 19 December, 2012. Accepted: 24 June, 2013. Available Online: 18 November, 2013. Coral reef ecosystems have some of the highest biodiversity levels among the coastal ecosystems and account for food, resources, and services worth an estimat- ed $30 billion annually (Cesar et al. 2003). Recent anthropogenic stresses that are Bulletin of Marine Science 233 © 2014 Rosenstiel School of Marine & Atmospheric Science of OA the University of Miami Open access content 234 Bulletin of Marine Science. Vol 90, No 1. 2014 intimately associated with the severe decline in coral reefs worldwide include land- based pollution, overexploitation, and global warming. Greater than one-third of the coral reefs are estimated to disappear or be under threat in the next three decades (Wilkinson 2008). Because the coral reef ecosystem is under various environmen- tal threats (Hughes et al. 2003, Pandolfi et al. 2003), conservation and management plans are necessary. Marine protected areas (MPAs) or marine reserves are beneficial for conserving this type of ecosystem and can produce almost immediate and long- lasting effects (Halpern and Warner 2002). MPAs play a key role in protecting the target fraction of a key habitat and also act as a source of recruits, which are needed to maintain and replenish populations through larval dispersal. Therefore, designing effective MPAs requires knowledge of larval dispersal of key species in the ecosys- tems, such as reef-building corals. Despite the importance of reef-building corals, population genetic studies of these corals have generally lagged behind those of most other organisms owing to the dif- ficulties in developing easily accessible and highly polymorphic genetic markers, e.g., the mitochondrial genome of these corals is highly conserved (Shearer et al. 2002, Ridgway and Gates 2006), and there is a low abundance of nuclear microsatellites in their relatively small genomes (Marquez et al. 2000). Previous population genet- ic studies of corals revealed that larval dispersal is more restricted than previously thought and that coral larvae generally disperse over an area of 70 km or less; this holds true even for spawner species with relatively long larval durations (i.e., >3 d; Van Oppen and Gates 2006). Given that low reef-connectivity leads to smaller meta- population size, an MPA unit of a finer scale than that used for species with strong reef-connectivity may be required. However, not many studies have examined the genetic structures of reef-building coral species with short larval dispersal potential (i.e., most larvae settle in <1 d). Population genetic studies of Seriatopora hystrix Dana, 1846 revealed that most larvae settle within a few hours and that larval dis- persal occurs on a scale of <100 m (Underwood et al. 2007). Another study revealed that high-latitude S. hystrix populations are supplemented by infrequent long-dis- tance migrants from the Great Barrier Reef and appear to have adequate popula- tion sizes to maintain viability and resist severe loss of genetic diversity (Noreen et al. 2009). These findings suggest that population genetic studies of species showing limited larval dispersal require different geographic scales, especially in areas where strong oceanic currents govern larval dispersal. Heliopora coerulea Pallas, 1766 is a type of octocoral but has a hard skeleton like other reef-building corals. Heliopora coerulea has been classified as a threatened species by the International Union for Conservation of Nature and Natural Resources because although specific population trends are unknown, population reduction can be inferred from declines in habitat quality based on the combined estimates of both destroyed reefs and reefs at the crit- ical stage of degradation within its distribution range (Obura et al. 2008). Heliopora coerulea is a gonochoric brooding species with low fecundity whose oocytes are fer- tilized internally and larvae are brooded externally on the female surface once a year (Babcock 1990, Liu et al. 2005). A laboratory experiment showed that most H. coeru- lea larvae (74%) settle within 1 d of release (Harii et al. 2002), which is indicative of a very short larval dispersal range. A previous study showed strong genetic differentia- tion between two populations with a high FST value (0.123) across the reef crest in the Shiraho reef along southwest Japan, even though they are separated by only 500 m (Yasuda et al. 2010). Despite the wide geographical distribution of H. coerulea in the Yasuda et al.: Cryptic speciation in blue coral 235 Indo-Pacific oceans, such localized genetic structuring has led to speculation about whether H. coerulea populations are completely isolated over different geographic scales and whether speciation occurs in the peripheral populations. In the present study, we examined the population genetic structure of H. coeru- lea along the Kuroshio Current at different geographic scales by using microsatellite markers. We found the following: (1) two cryptic species coexist along the Kuroshio Current, (2) strong genetic differentiation and significant IBD patterns within each of the two cryptic species, and (3) some populations of H. coerulea have extremely low genetic diversity but no clear correlation was found along different latitudes. Materials and Methods Study Area and Sampling.—To examine larval dispersal, we collected 611 H. coerulea specimens from 47 sampling sites along the Kuroshio Current including three intensive local samplings (Yaeyama in Japan, south Taiwan, and Verde Island Passage in the Philippines) from 2005 to 2011 (Fig. 1). We collected specimens by scuba or skin diving and obtained 1–2-cm fragments to minimize the damage to cor- als. All the specimens were preserved in 99.5% ethanol immediately after sampling. We collected the specimens at different depths, ranging from almost 0 (the top of the microatoll) to 14 m. The geographic distances between sampling sites ranged from approximately 1 km (e.g., SENW and SENA in Sekisei Lagoon, TWNC and TWND) to >1800 km (e.g., Amami and Philippines) (Table 1, Fig. 1). Although there are many variations of coral morphology, we classified the specimens into two typical morphs: small branch and flat shapes (Fig. 2). We collected as many H. coerulea samples as possible within 45 min. Therefore, the sampling size n( < 23) was mainly constrained by the maximum number of coral colonies that could be found within the sampling period. No colony was sampled twice, and all colonies were at least 3 m apart. DNA Extraction and PCR Amplification.—Genomic DNA was extracted us- ing a DNeasy Blood & Tissue Kit (QIAGEN) by following the manufacturer’s proto- col. Seven nuclear microsatellite loci, Saki 06, Saki 08, Mayu41, Mayu49, Miho33, Emi20, and Kumiko02 (Yasuda et al.
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