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Concepcion Et Al. 2014 Bull Mar Sci. 90(1):257–275. 2014 research paper http://dx.doi.org/10.5343/bms.2012.1109 Regional population structure of Montipora capitata across the Hawaiian Archipelago 1 Pacific Biosciences, 1380 Willow GT Concepcion 1 * Rd, Menlo Park, California 94025. IB Baums 2 2 Department of Biology, The RJ Toonen 3 Pennsylvania State University, 208 Mueller Laboratory University Park, Pennsylvania 16802. ABSTRACT.—Montipora capitata Dana, 1846 is one of 3 Hawai‘i Institute of Marine the most successful reef-building corals in the Hawaiian Biology, University of Hawai‘i, Archipelago, both in terms of geographic distribution and PO Box 1346, Kaneohe, Hawaii relative abundance. Here, we examine population genetic 96744. structure using eight microsatellite loci to make inferences * Corresponding author email: about exchange among geographical regions throughout <[email protected]>. Hawaiian waters to inform management and conservation efforts. We collected biopsy samples n( = 560) from colonies at each of 11 islands/atolls along the archipelago in addition to Johnston Atoll, about 1328 km to the southwest. We found very few potential clones (<2%) in our sampling (551 of 560 colonies had unique multi-locus genotypes), indicating that reproduction is predominantly sexual. Likewise, significant genetic structuring among most locations (pairwise F΄ST = 0.05 to 0.49, only two <0.10; P < 0.01) indicates that gene flow between islands is highly limited. Overall, we found four main regional genetic groupings of M. capitata within state waters, one comprised of the Main Hawaiian Islands, one off the three northwestern-most Hawaiian Islands, and two groupings encompassing the middle of the northwestern chain and Johnston Atoll. Despite the potential for extended pelagic larval development periods (>200 d), estimates of contemporary dispersal were uniformly low, with most sites being estimated at >90% self-recruitment. These data imply that the majority of M. capitata colonies found at a given Date Submitted: 3 January, 2013. island/atoll across the Hawaiian Archipelago are derived from Date Accepted: 5 December, 2013. self-recruitment, and argue for more local-scale management Available Online: 9 January, 2014. of coral reef resources than has been considered to date. Aside from physical barriers such as the Isthmus of Panama, distance is among the most obvious isolating mechanisms in the sea (Grigg and Hey 1992, Lessios and Robertson 2006, Baums et al. 2012). The Hawaiian Archipelago, spanning a distance of approximately 2500 km with a mean distance of about 250 km separating islands, is one of the most isolated on the planet (Hourigan and Reese 1987). Bounded on either side by deep oceanic water unsuitable for coral reef organisms, the Hawaiian Archipelago also hosts one of the highest proportions of endemic marine species (Hourigan and Reese 1987, Kay and Palumbi 1987, Eldredge 2003). As isolated volca- nic islands in the mid-ocean, all lineages present in Hawaii must have colonized from Bulletin of Marine Science 257 © 2014 Rosenstiel School of Marine & Atmospheric Science of OA the University of Miami Open access content 258 Bulletin of Marine Science. Vol 90, No 1. 2014 elsewhere, which is evidence of their ancestral or occasional ability to disperse, and subsequent adaptation and evolution to a novel environment (Hourigan and Reese 1987). Thus, the Hawaiian Archipelago provides a model system for investigating the population biology and phylogeography of ecologically dominant coral reef species. Oriented nearly linearly in a northwest–southeast direction, the islands also serve as the northern limit to tropical coral reef diversity in the Pacific Ocean, separating the rest of the greater Indo-Pacific region from the cold waters of the North Pacific. Additionally, there are well-measured gradients of human impact and island age along the archipelago, with human impacts generally increasing and island age de- creasing as one moves from the northwest to the southeast (Fleischer et al. 1998, Price and Clague 2002, Selkoe et al. 2008, 2009). The islands are already consid- ered a spectacular “natural laboratory” for the study of evolution in a suite of ter- restrial species such as passerine birds (Freed et al. 1987), silverswords (Baldwin and Sanderson 1998), happy-face spiders (Gillespie 2004), and picture-wing Drosophila (Carson 1997, reviewed by Wagner and Funk 1995); but to date, marine examples of diversification within the islands include only the recent report of Hawaiian en- demic limpets known locally as ‘opihi (Bird et al.2007, 2011, Bird 2011). The rea- son for this dichotomy is thought to be that marine species disperse better than do terrestrial ones (Kinlan and Gaines 2003), such that the isolation of the Hawaiian Archipelago has resulted in the marine fauna becoming differentiated from its Indo– West Pacific roots, but not diversifying (Hourigan and Reese 1987, Kay and Palumbi 1987). Because larvae of some coral species can persist for weeks or months through a coupled strategy of both autotrophy (via symbiotic dinoflagellates) and yolk stores (Richmond 1987a, Graham et al. 2008, Harii et al. 2010), it has long been assumed that the pelagic larvae have great potential to disperse and maintain broad species ranges (Jablonski and Lutz 1983, Babcock and Heyward 1986, Jackson and Coates 1986, Richmond 1987b, Ayre and Hughes 2000). Despite physical barriers such as ocean currents or freshwater intrusions, many studies of population genetic struc- ture in corals have found evidence for gene flow over large geographic scales (e.g., Hellberg 1996, Ayre and Hughes 2000, Rodriguez-Lanetty and Hoegh-Guldberg 2002, van Oppen et al. 2008, Baums et al. 2012). Nevertheless, many have questioned the relationship between the duration of pe- lagic development and ability to disperse using data from population genetics (e.g., Bradbury et al. 2008, Shanks 2009, Weersing and Toonen 2009, Riginos et al. 2011, Selkoe and Toonen 2011) and range sizes (e.g., Lester and Ruttenburg 2005, Lester et al. 2007, Mercier et al. 2013). Additionally, several recent studies have documented local recruitment in fishes (e.g., Saenz-Agudelo et al. 2011, Beldade et al. 2012, Buston et al. 2012, D’Aloia et al. 2013) and kin associations of both fishes (e.g., Selkoe et al. 2006, Buston et al. 2009, Bernardi et al. 2012) and invertebrates (Iacchei et al. 2013). Data supporting or contradicting predictions about gene flow and range size based on life-history remain extremely equivocal in corals (e.g., McFadden 1997, Baums et al. 2005, Foster et al. 2007, van Oppen et al. 2008, Miller and Ayre 2008, Souter et al. 2009, Starger et al. 2010, Pinzon and LaJeunesse 2011, Combosch and Vollmer 2011, Forsman et al. 2013, Schmidt-Roach et al. 2013, Marti-Puig et al. 2014). Clearly, knowledge of pelagic larval duration and range size of a given species are not alone sufficient to predict its level of population differentiation. Concepcion et al.: Population structure of Montipora capitata in Hawaii 259 The broadcast spawner, Montipora capitata Dana 1846, is a dominant reef builder throughout the entire Hawaiian Archipelago. With considerable phenotypic plas- ticity, M. capitata is able to persist in a wide range of reef habitats and form both branching and plating morphologies, depending on environmental conditions (Todd 2008, Forsman et al. 2010). As one of the primary reef-building species in the Hawaiian Archipelago and an ecologically dominant species in lagoonal habi- tats throughout the archipelago, there is considerable interest in understanding its population structure for management. The only other coral for which population ge- netic structure has been reported across the Hawaiian Archipelago to date is Porites lobata Dana, 1846. Relatively little population structure in P. lobata was found, but with a significant pattern of isolation-by-distance among sites along the Hawaiian island chain (Polato et al. 2010, Baums et al. 2012). In the present study, we sampled the broadcast spawning scleractinian coral M. capitata throughout the entire length of the Hawaiian Archipelago, Johnston Atoll, and Kwajalein Atoll in the Marshall Islands to describe population genetic structure and infer patterns of gene flow. Methods Sample Collection, Processing and Genotyping.—Fragments of M. capitata (approximately 1 cm in length) were collected from 11 island/atoll localities (30 sites) spanning the entire Hawaiian Archipelago (approximately 2500 km) with a mean distance between localities of about 250 km. Additionally, samples were collected from five sites at Johnston Atoll and three sites at Kwajalein Atoll in the Marshall Islands at distances of about 800 and 2500 km, respectively, from the Hawaiian Archipelago (Table 1, Online Table 1). Samples were stored in 95% ethanol or DMSO saturated salt-buffer at room temperature (Gaither et al. 2011). DNA was extracted from all samples using a 96-well Qiagen DNeasy extraction kit according to the man- ufacturer protocol. All samples were genotyped at each of eight microsatellite loci and one nuclear intron region, atpsβ (Jarman et al. 2004, Concepcion et al. 2010). In brief, a three- primer method for fluorescently labeling PCR amplicons (following Concepcion et al. 2010) was used to amplify products from each microsatellite locus in each sam- ple separately. Subsequently, for each sample, PCRs were combined into two pools, each containing four loci with uniquely labeled fluorescent dyes (Pool I: Mc0004, Mc0067, Mc0163, Mc0701; and Pool II: Mc0797, Mc0872, Mc0903, Mc0947) prior to sizing on an ABI-3100 Genetic Analyzer (Applied Biosystems). Electropherogram peaks were binned and named according to peak size with GeneMapper 4.0 (Applied Biosystems). Because computational phasing of a diploid nuclear locus is cheaper, more efficient, and can be just as accurate as cloning (Harrigan et al. 2008), nuclear locus atpsβ was amplified and sequenced directly n( = 501) following Concepcion et al. (2010). To jointly analyze locus atpsβ with the microsatellite data set, the atpsβ haplotype phas- es were determined with PhaSE (Stephens et al. 2001, Stephens and Donelly 2003) as implemented in DnaSP v.5.0 (Librado et al.
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