Coral Reefs

, Volume 37, Issue 2, pp 355–371 | Cite as

Evidence of host-associated divergence from coral-eating snails (genus Coralliophila) in the Coral Triangle

  • Sara E. Simmonds
  • Vincent Chou
  • Samantha H. Cheng
  • Rita Rachmawati
  • Hilconida P. Calumpong
  • G. Ngurah Mahardika
  • Paul H. Barber


We studied how host-associations and geography shape the genetic structure of sister species of marine snails Coralliophila radula (A. Adams, 1853) and C. violacea (Kiener, 1836). These obligate ectoparasites prey upon corals and are sympatric throughout much of their ranges in coral reefs of the tropical and subtropical Indo-Pacific. We tested for population genetic structure of snails in relation to geography and their host corals using mtDNA (COI) sequences in minimum spanning trees and AMOVAs. We also examined the evolutionary relationships of their Porites host coral species using maximum likelihood trees of RAD-seq (restriction site-associated DNA sequencing) loci mapped to a reference transcriptome. A maximum likelihood tree of host corals revealed three distinct clades. Coralliophila radula showed a pronounced genetic break across the Sunda Shelf (ΦCT = 0.735) but exhibited no genetic structure with respect to host. C. violacea exhibited significant geographic structure (ΦCT = 0.427), with divergence among Hawaiian populations, the Coral Triangle and the Indian Ocean. Notably, C. violacea showed evidence of ecological divergence; two lineages were associated with different groups of host coral species, one widespread found at all sites, and the other restricted to the Coral Triangle. Sympatric populations of C. violacea found on different suites of coral species were highly divergent (ΦCT = 0.561, d = 5.13%), suggesting that symbiotic relationships may contribute to lineage diversification in the Coral Triangle.


Marine gastropod Parasite Sister species Porites RAD-seq 



This work was supported by three National Science Foundation programs (OISE-0730256, OISE-1243541 and OCE-0349177), and a US Agency for International Development Grant (497-A-00-10-00008-00). The Lemelson Foundation Fellowship, Conchologists of America, Sigma Xi and the UCLA Department of Ecology and Evolutionary Biology provided additional funding to S. Simmonds. We acknowledge support from the Indonesia government including the Indonesian Ministry of Research and Technology (RISTEK), Indonesian Institute of Sciences (LIPI), Nature Conservation Agency (BKSDA) and the National Marine Park offices of Bunaken and Wakatobi. Sampling was covered under research permits obtained in Indonesia (RISTEK 2011, 198/SIP/FRP/SMNl/2012, 187/SIP/FRP/SM/VI/2013), Timor-Leste (Direccao nacional de Pescase Aquicultura 0042/DNPA/IOP/VII/11), Vietnam, the Philippines (Department of Agriculture-Bureau of Fisheries and Aquatic Resources), the Maldives (Ministry of Fisheries and Aquaculture Permit No. (OTHR)30-D/INDIV/2013/116) and Hawai'i (Department of Land and Natural Resources SAP 2013-11). Thanks to C. Meyer for comments that stimulated this study. Thank you to A. Fritts-Penniman, B. Stockwell, M. Weber, H. Nuetzel and D. Willette for collecting specimens. Thanks also to Z. Forsman and C. Reboton for help identifying Porites. Thank you to M. Campbell, N. Vu and D. Eardley at the Eagle Fish Genetics Laboratory (Eagle, Idaho) for sequencing the coral DNA. Thanks to those that provided advice about or assistance with fieldwork and permits: A. Fritts-Penniman, D. Cahyani, A. Wahyu, Z.A. Muchlisin, E. Rudi, A. Muhardy, F. Hadinata, P. Usef, A. Ackiss, G. Arlotti, D. Smith, M. Sweet and R. Pooley. Diving support provided by Bali Diving Academy, Critters@Lembeh, Lorenso’s Cottages, Cubadak Paradiso Village, Komodo National Park, Freddies Santai Sumurtiga, Lumba-lumba Diving Centre, Cendrawasih Bay National Park, Papua State University, Papua Diving, Kri Eco Resorts and the Korallion Lab. We also thank the Indonesian Biodiversity Research Center at Udayana University, Institute for Environmental and Marine Sciences at Silliman University, Nha Trang University and the Korallion Lab in the Maldives for institutional support.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

338_2018_1661_MOESM1_ESM.docx (26 kb)
Supplementary material 1 (DOCX 27 kb)


  1. Ali OA, O’Rourke SM, Amish SJ, Meek MH, Luikart G, Jeffres C, Miller MR (2016) RAD Capture (Rapture): flexible and efficient sequence-based genotyping. Genetics 202:389–400Google Scholar
  2. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  3. Barber PH, Cheng SH, Erdmann MV, Tenggardjaja K, Ambariyanto (2011) Evolution and conservation of marine biodiversity in the Coral Triangle: Insights from stomatopod Crustacea. In: Held C, Koenemann S, Schubart CD (eds) Phylogeography and population genetics in Crustacea. Crustean Issues. CRC Press, Boca Raton, pp 129–156CrossRefGoogle Scholar
  4. Barraclough TG, Vogler AP (2000) Detecting the geographical pattern of speciation from species-level phylogenies. Am Nat 155:419–434PubMedGoogle Scholar
  5. Bastian M, Heymann S, Jacomy M (2009) Gephi: an open source software for exploring and manipulating networks. International AAAI Conference on Weblogs and Social MediaGoogle Scholar
  6. Baums IB, Miller MW, Szmant AM (2003) Ecology of a corallivorous gastropod, Coralliophila abbreviata, on two scleractinian hosts. I: Population structure of snails and corals. Mar Biol 142:1083–1091CrossRefGoogle Scholar
  7. Baums IB, Boulay JN, Polato NR, Hellberg ME (2012) No gene flow across the Eastern Pacific Barrier in the reef-building coral Porites lobata. Mol Ecol 21:5418–5433CrossRefPubMedGoogle Scholar
  8. Bhattacharya D, Agrawal S, Aranda M, Baumgarten S, Belcaid M, Drake JL, Erwin D, Foret S, Gates RD, Gruber DF, Kamel B, Lesser MP, Levy O, Liew YJ, MacManes M, Mass T, Medina M, Mehr S, Meyer E, Price DC, Putnam HM, Qiu H, Shinzato C, Shoguchi E, Stokes AJ, Tambutté S, Tchernov D, Voolstra CR, Wagner N, Walker CW, Weber APM, Weis V, Zelzion E, Zoccola D, Falkowski PG (2016) Comparative genomics explains the evolutionary success of reef-forming corals. Elife 5:e13288. Google Scholar
  9. Bird CE, Holland BS, Bowen BW, Toonen RJ (2011) Diversification of sympatric broadcast-spawning limpets (Cellana spp.) within the Hawaiian archipelago. Mol Ecol 20:2128–2141CrossRefPubMedGoogle Scholar
  10. Bird CE, Fernandez-Silva I, Skillings DJ, Toonen RJ (2012) Sympatric speciation in the post “Modern Synthesis” era of evolutionary biology. Evol Biol 39:158–180CrossRefGoogle Scholar
  11. Bongaerts P, Riginos C, Hay KB, van Oppen MJ, Hoegh-Guldberg O, Dove S (2011) Adaptive divergence in a scleractinian coral: physiological adaptation of Seriatopora hystrix to shallow and deep reef habitats. BMC Evol Biol 11:303CrossRefPubMedPubMedCentralGoogle Scholar
  12. Bowen BW, Rocha LA, Toonen RJ, Karl SA (2013) The origins of tropical marine biodiversity. Trends Ecol Evol 28:359–366CrossRefPubMedGoogle Scholar
  13. Briggs JC, Bowen BW (2013) Marine shelf habitat: Biogeography and evolution. J Biogeogr 40:1023–1035CrossRefGoogle Scholar
  14. Bush GL (1969) Sympatric host race formation and speciation in frugivorous flies of the genus Rhagoletis (Diptera, Tephritidae). Evolution 23:237–251CrossRefPubMedGoogle Scholar
  15. Carpenter KE, Barber PH, Crandall ED, Ablan-Lagman MCA, Ambariyanto Mahardika GN, Manjaji-Matsumoto BM, Juinio-Meñez MA, Santos MD, Starger CJ, Toha AHA (2011) Comparative phylogeography of the Coral Triangle and implications for marine management. J Mar Biol 2011:1–14CrossRefGoogle Scholar
  16. Chen M-H, Soong K, Tsai M-L (2004) Host effect on size structure and timing of sex change in the coral-inhabiting snail Coralliophila violacea. Mar Biol 144:287–293CrossRefGoogle Scholar
  17. Connell J (1973) Population Ecology of Reef-Building Corals. In: Jones O, Endean R (eds) Biology and Geology of Coral Reefs V2: Biology 1. Academic Press, INC, pp 205–244CrossRefGoogle Scholar
  18. Crandall ED, Frey MA, Grosberg RK, Barber PH (2008) Contrasting demographic history and phylogeographical patterns in two Indo-Pacific gastropods. Mol Ecol 17:611–626CrossRefPubMedGoogle Scholar
  19. Crandall ED, Sbrocco EJ, DeBoer TS, Barber PH, Carpenter KE (2011) Expansion dating: Calibrating molecular clocks in marine species from expansions onto the Sunda Shelf following the Last Glacial Maximum. Mol Biol Evol 29:707–719CrossRefPubMedGoogle Scholar
  20. DeBoer TS, Subia MD, Ambariyanto Erdmann M V, Kovitvongsa K, Barber PH (2008) Phylogeography and limited genetic connectivity in the endangered boring giant clam across the Coral Triangle. Conserv Biol 22:1255–1266CrossRefPubMedGoogle Scholar
  21. Dres M, Mallet J (2002) Host races in plant-feeding insects and their importance in sympatric speciation. Philos Trans R Soc B Biol Sci 357:471–492CrossRefGoogle Scholar
  22. Duffy JE (1996) Resource-associated population subdivision in a symbiotic coral-reef shrimp. Evolution 50:360–373CrossRefPubMedGoogle Scholar
  23. Excoffier E, Lischer H (2011) ARLEQUIN: An integrated software package for population genetics data analysis. Whats New 1–174Google Scholar
  24. Faucci A, Toonen RJ, Hadfield MG (2007) Host shift and speciation in a coral-feeding nudibranch. Proc R Soc B Biol Sci 274:111–119CrossRefGoogle Scholar
  25. Fernández-González S, Pérez-Rodríguez A, de la Hera I, Proctor HC, Pérez-Tris J (2015) Different space preferences and within-host competition promote niche partitioning between symbiotic feather mite species. Int J Parasitol 45:655–662CrossRefPubMedGoogle Scholar
  26. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  27. Fordyce JA (2010) Host shifts and evolutionary radiations of butterflies. Proc R Soc B Biol Sci 277:3735–3743CrossRefGoogle Scholar
  28. Forsman ZH, Barshis DJ, Hunter CL, Toonen RJ (2009) Shape-shifting corals: molecular markers show morphology is evolutionarily plastic in Porites. Evol Biol 9:45–54Google Scholar
  29. Forsman Z, Wellington GM, Fox GE, Toonen RJ (2015) Clues to unraveling the coral species problem: distinguishing species from geographic variation in Porites across the Pacific with molecular markers and microskeletal traits. PeerJ 3:e751CrossRefPubMedPubMedCentralGoogle Scholar
  30. Forsman ZH, Knapp ISS, Tisthammer K, Eaton DAR, Belcaid M, Toonen RJ (2017) Coral hybridization or phenotypic variation? Genomic data reveal gene flow between Porites lobata and P. compressa. Mol Phylogenet Evol 111:132–148CrossRefPubMedGoogle Scholar
  31. Fritts-Penniman A (2016) Ecological speciation and cryptic diversity of coral-associated nudibranchs. University of California, Los Angeles, PhD dissertationGoogle Scholar
  32. Fujioka Y, Yamazato K (1983) Host selection of some Okinawan coral associated gastropods belonging to the genera Drupella, Coralliophila and Quoyula. Galaxea 2:59–73Google Scholar
  33. Gaither MR, Jones SA, Kelley C, Newman SJ, Sorenson L, Bowen BW (2011) High connectivity in the deepwater snapper Pristipomoides filamentosus (Lutjanidae) across the Indo-Pacific with isolation of the Hawaiian Archipelago. PLoS One 6:e28913CrossRefPubMedPubMedCentralGoogle Scholar
  34. Gaither MR, Rocha LA (2013) Origins of species richness in the Indo-Malay-Philippine biodiversity hotspot: Evidence for the centre of overlap hypothesis. J Biogeogr 40:1638–1648CrossRefGoogle Scholar
  35. Gittenberger A, Gittenberger E (2011) Cryptic, adaptive radiation of endoparasitic snails: Sibling species of Leptoconchus (Gastropoda: Coralliophilidae) in corals. Org Divers Evol 11:21–41CrossRefGoogle Scholar
  36. Hatfield T, Schluter D (1999) Ecological speciation in sticklebacks: environment-dependent hybrid fitness. Evolution 53:866–873CrossRefPubMedGoogle Scholar
  37. Hoeksema B (2007) Delineation of the Indo-Malayan centre of maximum marine biodiversity: the Coral Triangle. In: Renema W. (eds) Biogeography, Time, and Place: Distributions, Barriers, and lslands. Topics in Geobiology, vol 29. Springer, Dordrecht, pp 117–178Google Scholar
  38. Hurt C, Silliman K, Anker A, Knowlton N (2013) Ecological speciation in anemone-associated snapping shrimps (Alpheus armatus species complex). Mol Ecol 22:4532–4548CrossRefPubMedGoogle Scholar
  39. Iacchei M, Gaither MR, Bowen BW, Toonen RJ (2016) Testing dispersal limits in the sea: Range-wide phylogeography of the pronghorn spiny lobster Panulirus penicillatus. J Biogeogr 43:1032–1044CrossRefGoogle Scholar
  40. Johannesson K, Panova M, Kemppainen P, Andre C, Rolan-Alvarez E, Butlin RK (2010) Repeated evolution of reproductive isolation in a marine snail: unveiling mechanisms of speciation. Philos Trans R Soc B Biol Sci 365:1735–1747CrossRefGoogle Scholar
  41. Johnston L, Miller MW, Baums IB (2012) Assessment of host-associated genetic differentiation among phenotypically divergent populations of a coral-eating gastropod across the Caribbean. PLoS One 7:e47630CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kinlan B, Gaines S (2003) Propagule dispersal in marine and terrestrial environments: a community perspective. Ecology 84:2007–2020CrossRefGoogle Scholar
  44. Kochzius M, Nuryanto A, Genetics M (2008) Strong genetic population structure in the boring giant clam, Tridacna crocea, across the Indo-Malay Archipelago: implications related to evolutionary processes and connectivity. Mol Ecol 17:3775–3787CrossRefPubMedGoogle Scholar
  45. Kool JT, Paris CB, Barber PH, Cowen RK (2011) Connectivity and the development of population genetic structure in Indo-West Pacific coral reef communities. Glob Ecol Biogeogr 20:695–706CrossRefGoogle Scholar
  46. Krug PJ (2011) Patterns of speciation in marine gastropods: A review of the phylogenetic evidence for localized radiations in the sea. Am Malacol Bull 29:169–186CrossRefGoogle Scholar
  47. LaJeunesse TC (2005) “Species” radiations of symbiotic dinoflagellates in the Atlantic and Indo-Pacific since the Miocene-Pliocene transition. Mol Biol Evol 22:570–581CrossRefPubMedGoogle Scholar
  48. Lessios HA (2008) The great American schism: divergence of marine organisms after the rise of the Central American Isthmus. Annu Rev Ecol Evol Syst 39:63–91CrossRefGoogle Scholar
  49. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760CrossRefPubMedPubMedCentralGoogle Scholar
  50. Li J, O’Foighil D (2012) Host-specific morphologies but no host races in the commensal bivalve Neaeromya rugifera. Invertebr Biol 131:197–203CrossRefGoogle Scholar
  51. Litsios G, Sims CA, Wüest RO, Pearman PB, Zimmermann NE, Salamin N (2012) Mutualism with sea anemones triggered the adaptive radiation of clownfishes. BMC Evol Biol 12:212CrossRefPubMedPubMedCentralGoogle Scholar
  52. Ludt WB, Rocha LA (2015) Shifting seas: The impacts of Pleistocene sea-level fluctuations on the evolution of tropical marine taxa. J Biogeogr 42:25–38CrossRefGoogle Scholar
  53. Marko PB (2002) Fossil calibration of molecular clocks and the divergence times of geminate species pairs separated by the Isthmus of Panama. Mol Biol Evol 19:2005–2021CrossRefPubMedGoogle Scholar
  54. Marko PB, Hart MW (2011) The complex analytical landscape of gene flow inference. Trends Ecol Evol 26:448–456CrossRefPubMedGoogle Scholar
  55. Matsubayashi KW, Ohshima I, Nosil P (2010) Ecological speciation in phytophagous insects. Entomol Exp Appl 134:1–27CrossRefGoogle Scholar
  56. Miglietta MP, Faucci A, Santini F (2011) Speciation in the sea: Overview of the symposium and discussion of future directions. Integr Comp Biol 51:449–455CrossRefPubMedGoogle Scholar
  57. Moura AE, Kenny JG, Chaudhuri RR, Hughes MA, Reisinger RR, de Bruyn PJN, Dahlheim ME, Hall N, Hoelzel AR (2015) Phylogenomics of the killer whale indicates ecotype divergence in sympatry. Heredity 114:48–55CrossRefPubMedGoogle Scholar
  58. Mullen LM, Hoekstra HE (2008) Natural selection along an environmental gradient: A classic cline in mouse pigmentation. Evolution 62:1555–1570CrossRefPubMedGoogle Scholar
  59. Munday PL, Herwerden LV, Dudgeon CL (2004) Evidence for sympatric speciation by host shift in the sea. Curr Biol 14:1498–1504CrossRefPubMedGoogle Scholar
  60. Nosil P, Gompert Z, Farkas TE, Comeault AA, Feder JL, Buerkle CA, Parchman TL (2012) Genomic consequences of multiple speciation processes in a stick insect. Proc R Soc B Biol Sci 279:5058–5065CrossRefGoogle Scholar
  61. Nuryanto A, Kochzius M (2009) Highly restricted gene flow and deep evolutionary lineages in the giant clam Tridacna maxima. Coral Reefs 28:607–619CrossRefGoogle Scholar
  62. Oliverio M, Barco A, Richter A, Modica MV (2009) The coralliophiline (Gastropoda: Muricidae) radiation: Repeated colonizations of the deep sea? Nautilus 123:113–120Google Scholar
  63. Oren U, Brickner I, Loya Y (1998) Prudent sessile feeding by the corallivore snail Coralliophila violacea on coral energy sinks. Proc R Soc London Ser B 265:2043–2050CrossRefGoogle Scholar
  64. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  65. Peccoud J, Ollivier A, Plantegenest M, Simon J-C (2009) A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proc Natl Acad Sci 106:7495–7500CrossRefPubMedPubMedCentralGoogle Scholar
  66. Polato NR, Concepcion GT, Toonen RJ, Baums IB (2010) Isolation by distance across the Hawaiian Archipelago in the reef-building coral Porites lobata. Mol Ecol 19:4661–4677CrossRefPubMedGoogle Scholar
  67. Prada C, Hellberg ME (2013) Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral. Proc Natl Acad Sci 110:3961–3966CrossRefPubMedPubMedCentralGoogle Scholar
  68. Prada C, De Biasse MB, Neigel JE, Yednock B, Stake JL, Forsman ZH, Baums IB, Hellberg ME (2014a) Genetic species delineation among branching Caribbean Porites corals. Coral Reefs 33:1019–1030CrossRefGoogle Scholar
  69. Prada C, McIlroy SE, Beltrán DM, Valint DJ, Ford SA, Hellberg ME, Coffroth MA (2014b) Cryptic diversity hides host and habitat specialization in a gorgonian-algal symbiosis. Mol Ecol 23:3330–3340CrossRefPubMedGoogle Scholar
  70. Prunier R, Holsinger KE, Carlson JE (2012) The effect of historical legacy on adaptation: Do closely related species respond to the environment in the same way? J Evol Biol 25:1636–1649CrossRefPubMedGoogle Scholar
  71. Puebla O (2009) Ecological speciation in marine v. freshwater fishes. J Fish Biol 75:960–996CrossRefPubMedGoogle Scholar
  72. Riginos C, Liggins L (2013) Seascape genetics: populations, individuals, and genes marooned and adrift. Geogr Compass 7:197–216CrossRefGoogle Scholar
  73. Ritson-Williams R, Shjegstad SM, Paul VJ (2009) Larval metamorphosis of Phestilla spp. in response to waterborne cues from corals. J Exp Mar Bio Ecol 375:84–88CrossRefGoogle Scholar
  74. Rocha LA (2003) Patterns of distribution and processes of speciation in Brazilian reef fishes. J Biogeogr 30:1161–1171CrossRefGoogle Scholar
  75. Schluter D, Conte GL (2009) Genetics and ecological speciation. Proc Natl Acad Sci 106:9955–9962CrossRefPubMedPubMedCentralGoogle Scholar
  76. Skillings DJ, Bird CE, Toonen RJ (2011) Gateways to Hawai'i: genetic population structure of the tropical sea cucumber Holothuria atra. J Mar Biol 2011:1–16CrossRefGoogle Scholar
  77. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792CrossRefPubMedGoogle Scholar
  78. Soong K, Chen JL (1991) Population structure and sex-change in the coral-inhabiting snail Coralliophila violacea at Hsiao-Liuchiu, Taiwan. Mar Biol 111:81–86CrossRefGoogle Scholar
  79. Sotka EE (2005) Local adaptation in host use among marine invertebrates. Ecol Lett 8:448–459CrossRefGoogle Scholar
  80. Sotka EE, Wares JP, Hay ME (2003) Geographic and genetic variation in feeding preference for chemically defended seaweeds. Evolution 57:2262–2276CrossRefPubMedGoogle Scholar
  81. Tornabene L, Ahmadia GN, Berumen ML, Smith DJ, Jompa J, Pezold F (2013) Evolution of microhabitat association and morphology in a diverse group of cryptobenthic coral reef fishes (Teleostei: Gobiidae: Eviota). Mol Phylogenet Evol 66:391–400CrossRefPubMedGoogle Scholar
  82. Tsang LM, Chan BKK, Shih F-L, Chu KH, Allen Chen C (2009) Host-associated speciation in the coral barnacle Wanella milleporae (Cirripedia: Pyrgomatidae) inhabiting the Millepora coral. Mol Ecol 18:1463–1475CrossRefPubMedGoogle Scholar
  83. Villesen P (2007) FaBox: An online toolbox for FASTA sequences. Mol Ecol Notes 7:965–968CrossRefGoogle Scholar
  84. Voris H (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167CrossRefGoogle Scholar
  85. Waldrop E, Hobbs JPA, Randall JE, Dibattista JD, Rocha LA, Kosaki RK, Berumen ML, Bowen BW (2016) Phylogeography, population structure and evolution of coral-eating butterflyfishes (Family Chaetodontidae, genus Chaetodon, subgenus Corallochaetodon). J Biogeogr 43:1116–1129CrossRefGoogle Scholar
  86. Walsh PS, Metzger DA, Higuchi R (2013) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 54:506–513CrossRefGoogle Scholar
  87. Wang CY, Liu HY, Shao CL, Wang YN, Li L, Guan HS (2008) Research progress on chemical defensive substances from soft corals and gorgonians. Acta Ecol Sin 28:2320–2328CrossRefGoogle Scholar
  88. Williams ST, Benzie JAH (1998) Evidence of a phylogeographic break between populations of a high-dispersal starfish: congruent regions within the Indo-West Pacific defined by color morphs, mtDNA and allozyme data. Evolution 52:87–99PubMedGoogle Scholar
  89. Yamashiro H, Oku H, Higa H, Chinen I, Sakai K (1999) Composition of lipids, fatty acids and sterols in Okinawan corals. Comp Biochem Physiol - B Biochem Mol Biol 122:397–407CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Sara E. Simmonds
    • 1
  • Vincent Chou
    • 1
  • Samantha H. Cheng
    • 1
  • Rita Rachmawati
    • 1
  • Hilconida P. Calumpong
    • 2
  • G. Ngurah Mahardika
    • 3
  • Paul H. Barber
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyUniversity of California Los AngelesLos AngelesUSA
  2. 2.Institute of Environment and Marine SciencesSilliman UniversityDumaguete CityPhilippines
  3. 3.Animal Biomedical and Molecular Biology Laboratory, Faculty of Veterinary MedicineUdayana University BaliDenpasarIndonesia

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