Phylogeography of the Manybar Goatfish, Parupeneus Multifasciatus, Reveals Isolation of the Hawaiian Archipelago and a Cryptic Species in the Marquesas Islands

Bull Mar Sci. 90(1):493–512. 2014 research paper http://dx.doi.org/10.5343/bms.2013.1032 Phylogeography of the manybar goatfish, Parupeneus multifasciatus, reveals isolation of the Hawaiian Archipelago and a cryptic species in the Marquesas Islands 1 Hawai‘i Institute of Marine Zoltán Szabó 1 * Biology, University of Hawai‘i, 2 Kaneohe, Hawaii 96744. Brent Snelgrove Matthew T Craig 3 2 Department of Biology, 4 University of Hawai‘i, Honolulu, Luiz A Rocha Hawaii 96822. Brian W Bowen 1 3 Department of Marine Science and Environmental Studies, University of San Diego, San Diego, California 92110. ABSTRACT.—To assess genetic connectivity in a common and abundant goatfish (family Mullidae), we surveyed 4 Section of Ichthyology, California Academy of Sciences, 637 specimens of Parupeneus multifasciatus (Quoy and 55 Music Concourse Dr, San Gaimard, 1825) from 15 locations in the Hawaiian Islands Francisco, California 94118. plus Johnston Atoll, two locations in the Line Islands, two locations in French Polynesia, and two locations in the * Corresponding author email: <[email protected]>. northwestern Pacific. Based on mitochondrial cytochrome b sequences, we found no evidence of population structure across Hawaii and the North Pacific; however, we observed genetic structuring between northern and southern Pacific locations with the equator-straddling Line Islands affiliated with the southern population. The Marquesas Islands sample in the South Pacific was highly divergent d( = 4.12% average sequence divergence from individuals from all other locations) indicating a cryptic species. These findings demonstrate that this goatfish is capable of extensive dispersal consistent with early life history traits in Mullidae, Date Submitted: 4 April, 2013. Date Accepted: 5 December, 2013. and provide further evidence for the biogeographic isolation Available Online: 10 January, 2014. of the Marquesas Islands. With more than 60 species in six genera, goatfishes (family Mullidae) represent a major component of reef ecosystem assemblages (Uiblein 2007). Their benthic forag- ing behavior is facilitated by chemosensory barbels that invoke their common name. This excavation of soft sediments can shape benthic community structure and at- tract other fishes to the feeding foray, and thus goatfishes are regarded as community builders and keystone species in benthic feeding assemblages (Johnson and Gill 1998, Uiblein 2007). In addition to the chemosensory barbels, goatfishes have other unusual adaptations, including the ability to change coloration rapidly, mimic the coloration of other species in mixed-species schools (Randall and Guézé 1980), and survive in a pelagic environment long after transforming from larval to juvenile stage (Lo-Yat et al. 2006). Goatfishes are also economically important species, caught in artisanal fisheries throughout the tropical and subtropical oceans. The manybar goatfish, Parupeneus multifasciatus (Quoy and Gaimard, 1825), is probably the most common Indo-Pacific member of the family Mullidae (Friedlander Bulletin of Marine Science 493 © 2014 Rosenstiel School of Marine & Atmospheric Science of OA the University of Miami Open access content 494 Bulletin of Marine Science. Vol 90, No 1. 2014 et al. 2007, ZS pers obs). It occurs inshore around coral reefs and adjacent habitats of the Pacific and can be found to at least 161 m depth R( andall 2007). While specific life history data on the manybar goatfish indicate a pelagic larval duration of 24–28 d in captivity and a short generation time (Pavlov et al. 2011, 2012, 2013), other mem- bers of this family have a relatively long larval stage of about 50 d (Robertson et al. 2004) followed by a pelagic juvenile stage that eventually settles on reefs at lengths of 5–10 cm (Lo-Yat et al. 2006). These pelagic juveniles have been recovered over 1000 km from the nearest shallow water habitat (Clarke 1995), and this trait is likely to translate into high connectivity in population genetic assays (Craig et al. 2007, Horne et al. 2008, Reece et al. 2011), an expectation we hold for P. multifasciatus. Manybar goatfish are distributed throughout the Pacific Ocean, from the Northwestern Hawaiian Islands to the Marquesas in the central Pacific, east of Pitcairn Islands through the islands of Oceania to northwestern Australia and Christmas and Cocos-Keeling Islands in the Indian Ocean, north to Southern Japan, and south to New South Wales, Lord Howe, Norfolk, and Rapa Islands (Randall 2005, and http://www.iucnredlist.org). A similar distribution is common among many demersal fish species (Woodland 1983, Briggs 1999) and encompasses three rec- ognized biogeographic provinces. Based on high levels of endemism, the Hawaiian Archipelago in the North Pacific (25% endemism, Randall 2007) and the Marquesas Archipelago in the South Pacific (12% endemism, Randall and Earle 2000) represent independent provinces. The remainder of the range encompasses the vast Indo- Polynesian province (Briggs and Bowen 2012) from the eastern Indian Ocean to the central Pacific. This area spans about half the planet, and biogeographic cohesiveness is likely maintained by the relatively small distances among island and coastal habitats. As noted by Schultz et al. (2008), dispersive propagules never have to travel >800 km to reach adjacent habitat across this region. To the east of this region, the range of the manybar goatfish is presumably constrained by the East Pacific Barrier (EPB), the 5000 km gap in shallow habitat between the central Pacific and the Americas. In recent phylogeographic appraisals of Pacific reef fishes, genetic partitions tend to be concordant with the biogeographic provinces noted above (Gaither et al. 2010, 2011, Leray et al. 2010, DiBattista et al. 2011, Eble et al. 2011a). Hence our initial expectations are genetic breaks distinguishing the Marquesas and Hawaii from the rest of the Pacific range. The present study is also part of a multi-species initiative to explore genetic connectivity of reef organisms within the Hawaiian Archipelago (reviewed in Toonen et al. 2011). In particular, the 1600 km expanse of the uninhabited Northwestern Hawaiian Islands (NWHI) was designated as the Papahānaumokuākea Marine National Monument (PMNM, Fig. 1) in 2006, and intensive research efforts were initiated to examine its efficacy in preserving biodiversity and replenishing exploited fish stocks in the densely populated Main Hawaiian Islands (MHI). While very lim- ited artesian bottom fishing existed before the PMNM, public access and fishing was further reduced at the formation of the PMNM. In contrast, the MHI have a current population of approximately 1.4 million people and are heavily fished by local anglers and spearfishers, impacted by sports and tour operators, beach use, land erosion, and development. Here, we focus on the manybar goatfish to address the following questions: (1) Is there genetic partitioning within the range of the species? (2) Is there population genetic structuring within the Hawaiian Archipelago (e.g., NWHI vs MHI)? (3) If so, Szabó et al.: Phylogeography of the manybar goatfish 495 Figure 1. Map of manybar goatfish, Parupeneus multifasciatus, collection sites with number of samples at each site. Species distribution range is indicated in blue shading. On the large-scale map, the Hawaiian Archipelago is represented only by its northernmost and southernmost islands, Kure and Hawaii, respectively. Inset details collections within the Hawaiian Archipelago. Photo credit: J Williams. what is the present rate and direction of gene flow among populations? and (4) What are the management implications? Materials and Methods Sample Collections Between 2005 and 2010, 637 specimens of P. multifasciatus were collected with pole spears while scuba diving or snorkeling at 22 locations across the Pacific Ocean: 15 sites in the Hawaiian Archipelago (MHI: The islands of Hawaii, Oahu, Kauai and Niihau; Kaula Rock; NWHI: Nihoa Island, Necker Island, French Frigate Shoals, Gardner Pinnacles, Maro Reef, Laysan Island, Lisianski Island, Pearl and Hermes Atoll, Midway Atoll, Kure Atoll), Johnston Atoll, Palmyra and Kiritimati in the Line Islands, Palau and Okinawa in the northwest Pacific, and Moorea and Nuku Hiva (Marquesas Islands) in French Polynesia (Fig. 1, first column of Table 1). The uninhabited Ka‘ula Rock was grouped with the NWHI for the purpose of our study. Tissue samples were stored in a saturated salt-DMSO buffer (Amos and Hoelzel 1991) or in 70% ethanol at room temperature until DNA extraction. Specimens collected from the NWHI were obtained on the NOAA Ship Hi’ialakai as part of an initiative to document and monitor resources in the PMNM. 496 Bulletin of Marine Science. Vol 90, No 1. 2014 Table 1. Collection sites, sample sizes (n), number of haplotypes (HN) and unique haplotypes (HU) observed in a single individual, molecular diversity indices, and estimated age of the analyzed Parupeneus multifasciatus populations. Time since most recent population collapse was calculated from mismatch distributions assuming 1% nucleotide sequence divergence / MY within lineages. Significant P( < 0.02) Fu’s FS values are in bold. Haplotype Allelic Percent nucleotide Location n HN HU diversity, h (SD) richness [r(9)] diversity, π (SD) Fu’s FS Age (yrs) Kure Atoll 29 8 3 0.808 (0.046) 3.806 0.22 (0.16) −2.87 116,343 Midway 45 16 5 0.868 (0.032) 4.856 0.28 (0.18) −10.75 146,197 Pearl and Hermes 37 8 1 0.764 (0.047) 3.352 0.21 (0.15) −2.54 117,880 Lisianski 28 12 3 0.884 (0.036) 4.996

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