Coral Reefs

, Volume 30, Issue 4, pp 977–990 | Cite as

Evolution of corallivory in the gastropod genus Drupella

Report

Abstract

Although muricid gastropods in the genus Drupella are well-known consumers of Indo-Pacific corals, their evolutionary and ecological history is unclear, as is their relationship to the apparently facultative coral-feeder Ergalatax margariticola, which has been reported to feed upon corals in Hong Kong. We use a well resolved molecular phylogeny (reconstructed from one nuclear and two mitochondrial genes) to show that the monophyletic genus Drupella falls into the muricid subfamily Ergalataxinae and that the genus includes ‘E. margariticola’, which is composed of two cryptic species. We show that genetic structure within the here reassigned ‘Drupella margariticola’ species complex does not relate to feeding mode, but instead seems to correspond to broad patterns of habitat ecology found in other gastropod taxa. Our analyses suggest that Drupella originated in the late Miocene (approximately 9.6 Ma) and diversified approximately 5.0 Ma, much later than the appearance of modern coral reefs in the early Cenozoic. Thus, it is possible that corallivory in Drupella evolved in response to the major expansion and reorganization of reefs that took place in the early Miocene.

Keywords

Muricidae Speciation Coral feeding Molecular phylogeny Ergalatax margariticola 

Notes

Acknowledgments

We are indebted to R. Houart for advice and the loan of the fossil Taurasia sacyi. We are also very grateful for the assistance and loans provided by the staff of museums and research institutions, especially P. Bouchet, V. Héros, B. Buge and N. Puillandre of Museum nationale d’Histoire naturelle, Paris (MNHN); I. Loch and A. Miller of the Australian Museum, Sydney. We appreciated useful discussions with J. Taylor and B. Rosen. We would also like to thank the many others who provided specimens and assisted us in various ways including L. Alsayegh, C. Bird, T. Haga, T. Hamada, G. Herbert, Y. Ito, R. Jones, Y. Kano, P. Kuklinski, M. V. Modica, T. Nakano, B. Ng, S. Nielson, N. Razalli, K. S. Tan, S. H. Tan, J. D. True, R. C. Willan and Z. Yasin. We would also like to thank the PANGLAO 2004 Marine Biodiversity Project (funded by the Total Foundation and the French Ministry of Foreign Affairs) and the MNHN-IRD-PNI Santo 2006 expedition (made possible by grants, among others, from the Total Foundation and the Stavros Niarchos Foundation) for collecting some of the specimens that we used. M. C. is supported by a studentship from the Natural History Museum, London and by an Imperial College Deputy Rector’s studentship. Photography of specimens by H. Taylor, Natural History Museum, London. We thank the editor and two anonymous referees for helpful comments.

Supplementary material

338_2011_788_MOESM1_ESM.doc (54 kb)
Positions of fixed differences in the 28S rRNA gene among species/ESUs in the genus Drupella (DOC 54 kb)
338_2011_788_MOESM2_ESM.eps (2 mb)
Fig. S1 MrBayes Bayesian phylogenies of Drupella and muricid outgroups based on single gene analysis of (a) 28S rRNA, (b) 12S rRNA and (c) cytochrome c oxidase subunit I (COI). Support values are posterior probabilities; intraspecific support values and those <90% are not shown for the sake of clarity. Codes indicate general localities; detailed information can be found in Table 1 (EPS 2,022 kb)

References

  1. Alfaro ME, Santini F, Brock CD (2007) Do reefs drive diversification in marine teleosts? Evidence from the pufferfish and their allies (order Tetraodontiformes). Evolution 61:2104–2126PubMedCrossRefGoogle Scholar
  2. Antonius A, Riegl B (1997) A possible link between coral diseases and a corallivorous snail (Drupella cornus) outbreak in the Red Sea. Atoll Res Bull 447:1–9Google Scholar
  3. Antonius A, Riegl B (1998) Coral diseases and Drupella cornus invasion in the Red Sea. Coral Reefs 17:48CrossRefGoogle Scholar
  4. Arakawa KY (1965) A study on the radulae of the Japanese Muricidae (3): the genera Drupa, Drupina, Drupella, Cronia, Morula, Morulina, Phrygiomurex, Cymia and Tenguella gen. nov. Venus 24:113–126Google Scholar
  5. Barco A, Claremont M, Reid DG, Houart R, Bouchet P, Williams ST, Cruaud C, Couloux A, Oliverio M (2010) A molecular phylogenetic framework for the Muricidae, a diverse family of carnivorous gastropods. Mol Phylogenet Evol 56:1025–1039PubMedCrossRefGoogle Scholar
  6. Baums IB, Miller MW, Szmant AM (2003) Ecology of a corallivorous gastropod, Coralliophila abbreviata, on two scleractinian hosts. II. Feeding, respiration and growth. Mar Biol 142:1093–1101Google Scholar
  7. Bellwood DR, Klanten S, Cowman PF, Pratchett MS, Konow N, van Herwerden L (2010) Evolutionary history of the butterflyfishes (f: Chaetodontidae) and the rise of coral feeding fishes. J Evol Biol 23:335–349PubMedCrossRefGoogle Scholar
  8. Broderip WJ (1833) Characters of new species of Mollusca and Conchifera, collected by Mr. Cuming. Proceedings of the Committee of Science and Correspondence of the Zoological Society of London 1832:173–179Google Scholar
  9. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552PubMedGoogle Scholar
  10. Claremont M, Reid DG, Williams ST (2008) A molecular phylogeny of the Rapaninae and Ergalataxinae (Neogastropoda: Muricidae). J Molluscan Stud 74:215–221CrossRefGoogle Scholar
  11. Claremont M, Williams ST, Barraclough TG, Reid DG (2011) The geographic scale of speciation in a marine snail with high dispersal potential. J Biogeogr 38:1016–1032CrossRefGoogle Scholar
  12. Cope M, Morton B (1988) The scleractinian coral community at Hoi Ha Wan, Hong Kong. Asian Mar Biol 5:41–52Google Scholar
  13. Cowman PF, Bellwood DR, van Herwerden L (2009) Dating the evolutionary origins of wrasse lineages (Labridae) and the rise of trophic novelty on coral reefs. Mol Phylogenet Evol 52:621–631PubMedCrossRefGoogle Scholar
  14. Crame J, Rosen BR (2002) Cenozoic palaeogeography and the rise of modern biodiversity patterns. Spec Publ Geol Soc Lond 194:153–168CrossRefGoogle Scholar
  15. Cumming RL (2009a) Case study: impact of Drupella spp. on reef-building corals of the Great Barrier Reef. Research publication No. 97. Great Barrier Reef Marine Park Authority. Townsville, QLD, Australia, p 44Google Scholar
  16. Cumming RL (2009b) Population outbreaks and large aggregations of Drupella on the Great Barrier Reef. Research Publication No. 96. Great Barrier Reef Marine Park Authority. Townsville, QLD, Australia, p 26Google Scholar
  17. Cumming RL, McCorry D (1998) Corallivorous gastropods in Hong Kong. Coral Reefs 17:178CrossRefGoogle Scholar
  18. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214PubMedCrossRefGoogle Scholar
  19. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology 4:e88PubMedCrossRefGoogle Scholar
  20. Ezard T, Fujisawa T, Barraclough TG (2009) splits: SPecies’ LImits by Threshold Statistics. R package version 1.0-11/r29. http://www.R-Forge.R-project.org/projects/splits/
  21. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299PubMedGoogle Scholar
  22. Fontaneto D, Herniou EA, Boschetti C, Caprioli M, Melone G, Ricci C, Barraclough TG (2007) Independently evolving species in asexual bdelliod rotifers. PLoS Biology 5:914–921CrossRefGoogle Scholar
  23. Forde M (1992) Populations, behaviour and effects of Drupella cornus on the Ningaloo Reef, Western Australia. In: Turner S (ed) Western Australia: Department of Conservation and Land Management, CALM Occasional Paper No. 3/92, pp 45–50Google Scholar
  24. Fujioka Y (1982) On the secondary sexual characters found in the dimorphic radula of Drupella (Gastropoda: Muricidae) with reference to its taxonomic revision. Venus 40:203–223Google Scholar
  25. Fujioka Y (1984) Remarks on two species of Drupella (Muricidae). Venus 43:44–54Google Scholar
  26. Fujioka Y (1985) Systematic evaluation of radular characters in Thaidinae (Gastropoda: Muricidae). Journal of Science of the Hiroshima University, Series B, Division 1 31:235–287Google Scholar
  27. Gittenberger A (2006) De evolutionaire geschiedenis van parasitaire slakken en hun gastheer koralen in de Indo-Pacific. PhD thesis, Universiteit Leiden, Leiden, The Netherlands, p 249Google Scholar
  28. Gittenberger A, Gittenberger E (2011) Cryptic, adaptive radiation of endoparasitic snails: sibling species of Leptoconchus (Gastropoda: Coralliophilidae) in corals. Org Divers Evol 11:21–41Google Scholar
  29. Glynn P (1990) Feeding ecology of selected coral-reef macroconsumers: patterns and effects on coral community structure. In: Dubinsky Z (ed) Ecosystems of the world, vol 25. Elsevier Science, Amsterdam, The Netherlands, pp 365–400Google Scholar
  30. Hadfield MG (1976) Molluscs associated with living tropical corals. Micronesica 12:133–148Google Scholar
  31. Hayes J (1990) Prey preference in a caribbean corallivore, Coralliophlla abbreviata (Lamarck)(Gastropoda, Coralliophilidae). Bull Mar Sci 47:557–560Google Scholar
  32. Heled J, Drummond A (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27:570–580PubMedCrossRefGoogle Scholar
  33. Herbert GS, Merle D, Gallard CS (2007) A developmental perspective on evolutionary innovation in the radula of the predatory neogastropod family Muricidae. Am Malacol Bull 23:17–32CrossRefGoogle Scholar
  34. Héros V, Lozouet P, Maestrati P, Von Cosel R, Brabant D, Bouchet P (2007) Mollusca of New Caledonia. In: Payri C, Richer De Forges B (eds) Compendium of marine species of New Caledonia, Doc. Sci. Tech. II7, 2nd edn. Institut de recherche pour le développement, Nouméa, New Caledonia, pp 199–254Google Scholar
  35. Houart R, Héros V (2008) Muricidae (Mollusca: Gastropoda) from Fiji and Tonga. In: Héros V, Cowie R, Bouchet P (eds) Tropical Deep-Sea Benthos 25: Mémoires du Muséum national d’Histoire naturelle 196. Muséum national d’Histoire naturelle, Paris, pp 437–480Google Scholar
  36. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  37. Hughes TP, Bellwood DR, Connolly SR (2002) Biodiversity hotspots, centres of endemicity, and the conservation of coral reefs. Ecol Lett 5:775–784CrossRefGoogle Scholar
  38. Ishida S (2001) An analysis of feeding aggregations in intertidal muricids: species-specific modes of foraging–initial predation and parasitism. Asian Mar Biol 18:1–13Google Scholar
  39. Ishida S (2004a) Life history of the muricid gastropod, Cronia margariticola (Broderip, 1833): growth mode transition with season and sexual maturity. Benthos Research 59:35–44Google Scholar
  40. Ishida S (2004b) Initial predation and parasitism by muricid whelks demonstrated by the correspondence between drilled holes and their apparent enveloper. J Exp Mar Biol Ecol 305:233–245CrossRefGoogle Scholar
  41. Johnson K, Jackson J, Budd A (2008) Caribbean reef development was independent of coral diversity over 28 million years. Science 319:1521–1523PubMedCrossRefGoogle Scholar
  42. Johnson MS, Cumming RL (1995) Genetic distinctness of 3 widespread and morphologically variable species of Drupella (Gastropoda, Muricidae). Coral Reefs 14:71–78CrossRefGoogle Scholar
  43. Johnston L, Miller MW (2007) Variation in life-history traits of the corallivorous gastropod Coralliophila abbreviata on three coral hosts. Mar Biol 150:1215–1225CrossRefGoogle Scholar
  44. Lirman D (2000) Fragmentation in the branching coral Acropora palmata (Lamarck): growth, survivorship, and reproduction of colonies and fragments. J Exp Mar Biol Ecol 251:41–57PubMedCrossRefGoogle Scholar
  45. Lorenz F, Fehse D (2009) The living Ovulidae: a manual of the families of allied cowries: Ovulidae, Pediculariidae and Eocypraeidae. ConchBooks, Hackenheim, Germany, p 651Google Scholar
  46. Lozouet P, Renard P (1998) The Coralliophilidae, Gastropoda from the Oligocene and Lower Miocene of the Aquitaine (Southwestern France): systematics and details of coral hosts. Geobios 31:171–185CrossRefGoogle Scholar
  47. Maddison D, Maddison W (2003) MacClade. Version 4.06 OSX. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  48. Massin C, Dupont S (2003) Study on Leptoconchus species (Gastropoda, Coralliophilidae) infesting Fungiidae (Anthozoa : Scleractinia). 1. Presence of nine Operational Taxonomic Units (OTUs) based on anatomical and ecological characters. Belg J Zool 133:121–126Google Scholar
  49. McCormack JE, Heled J, Delaney KS, Peterson AT, Knowles LL (2011) Calibrating divergence times on species trees versus gene trees: implications for speciation history of Aphelocoma jays. Evolution 65:184–202PubMedCrossRefGoogle Scholar
  50. McIlwain JL, Jones GP (1997) Prey selection by an obligate coral-feeding wrasse and its response to small-scale disturbance. Mar Ecol-Prog Ser 155:189–198CrossRefGoogle Scholar
  51. Miller I, Dolman A (2008) Relative role of disease and predators as drivers of decline in coral cover on the Great Barrier Reef. Proc 11th Int Coral Reef Symp 6:216–220Google Scholar
  52. Modica M-V, Holford M (2010) The Neogastropoda: evolutionary innovations of predatory marine snails with remarkable pharmacological potential. In: Pontarotti P (ed) Evolutionary biology: concepts, molecular and morphological evolution. Springer-Verlag, Berlin, pp 249–270CrossRefGoogle Scholar
  53. Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–374PubMedCrossRefGoogle Scholar
  54. Morton B, Blackmore G (2009) Seasonal variations in the density of and corallivory by Drupella rugosa and Cronia margariticola (Caenogastropoda: Muricidae) from the coastal waters of Hong Kong: (‘plagues’ or ‘aggregations’)? J Mar Biol Assoc U K 89:147–159CrossRefGoogle Scholar
  55. Morton B, Blackmore G, Kwok CT (2002) Corallivory and prey choice by Drupella rugosa (Gastropoda : Muricidae) in Hong Kong. J Molluscan Stud 68:217–223CrossRefGoogle Scholar
  56. Moyer JT, Emerson WK, Ross M (1982) Massive destruction of scleractinian corals by the muricid gastropod Drupella in Japan and the Philippines. Nautilus 96:69–82Google Scholar
  57. Nylander J (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala UniversityGoogle Scholar
  58. Okutani T (2000) Marine mollusks in Japan. University of Tokyo Press, Tokyo, JapanGoogle Scholar
  59. Oliverio M, Mariottini P (2001a) Contrasting morphological and molecular variation in Coralliophila meyendorffii (Muricidae, Coralliophilinae). J Molluscan Stud 67:243–246CrossRefGoogle Scholar
  60. Oliverio M, Mariottini P (2001b) A molecular framework for the phylogeny of Coralliophila and related muricoids. J Molluscan Stud 67:215–224CrossRefGoogle Scholar
  61. 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
  62. Padilla DK (1998) Inducible phenotypic plasticity of the radula in Lacuna (Gastropoda: Littorinidae). Veliger 41:201–204Google Scholar
  63. Pons J, Barraclough TG, Gomez-Zurita J, Cardosa A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55:595–609PubMedCrossRefGoogle Scholar
  64. Poppe GT (2008) Philippine marine mollusks, vol II. ConchBooks, Germany, p 848Google Scholar
  65. Reeder TW (2003) A phylogeny of the Australian Sphenomorphus group (Scincidae: Squamata) and the phylogenetic placement of the crocodile skinks (Tribolonotus): Bayesian approaches to assessing congruence and obtaining confidence in maximum likelihood inferred relationships. Mol Phylogenet Evol 27:384–397PubMedCrossRefGoogle Scholar
  66. Reid DG (2007) The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the Indo-West Pacific Ocean. Zootaxa 1420:1–161Google Scholar
  67. Reid DG (2009) The genus Echinolittorina Habe, 1956 (Gastropoda: Littorinidae) in the western Atlantic Ocean. Zootaxa 2184:1–103Google Scholar
  68. Reid D, Lal K, Mackenzie-Dodds J, Kaligis F, Littlewood D, Williams S (2006) Comparative phylogeography and species boundaries in Echinolittorina snails in the central Indo-West Pacific. J Biogeogr 33:990–1006CrossRefGoogle Scholar
  69. Robertson DR, Karg F, de Moura RL, Victor BC, Bernardi G (2006) Mechanisms of speciation and faunal enrichment in Atlantic parrotfishes. Mol Phylogenet Evol 40:795–807PubMedCrossRefGoogle Scholar
  70. Robertson R (1970) Review of the predators and parasites of stony corals, with special reference to symbiotic prosobranch gastropods. Pac Sci 24:43–54Google Scholar
  71. Rocha LA, Robertson DR, Roman J, Bowen BW (2005) Ecological speciation in tropical reef fishes. Proc R Soc Biol Sci Ser B 272:573–579Google Scholar
  72. Schluter D (1996) Ecological causes of adaptive radiation. Am Nat 148:S40–S64CrossRefGoogle Scholar
  73. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony methods. Mol Biol Evol. doi: 10.1093/molbev/msr121
  74. Tan KS (1995) Taxonomy of the Thais and Morula (Mollusca: Gastropoda: Muricidae) in Singapore and vicinity. Ph.D. thesis, National University of Singapore, Singapore, p 546Google Scholar
  75. Tan KS (2003) Feeding ecology of common intertidal Muricidae (Mollusca: Neogastropoda) from the Burrup Peninsula, Western Australia. In: Wells FE, Walker D, Jones D (eds) The marine flora and fauna of Dampier, Western Australia. Western Australian Museum, Perth, pp 172–192Google Scholar
  76. Taylor JD (1976) Habitats, abundance and diets of muricacean gastropods at Aldabra Atoll. Zool J Linn Soc 59:155–193CrossRefGoogle Scholar
  77. Taylor JD (1980) Diets and habitats of shallow water predatory gastropods around Tolo Channel, Hong Kong. In: Morton B (ed) Proceedings of the First International Workshop on the Malacofauna of Hong Kong and Southern China, Hong Kong, 1977. Hong Kong University Press, Hong Kong, pp 163–165Google Scholar
  78. Taylor JD (1993) Dietary and anatomical specialization of mitrid gastropods (Mitridae) at Rottnest Island, Western Australia. Proceedings Fifth International Marine Biological Workshop: The Marine Flora and Fauna of Rottnest Island, Western Australia. Western Australian Museum, Perth, pp 583–599Google Scholar
  79. Taylor JD, Morton B (1996) The diets of predatory gastropods in the Cape D’Aguilar Marine Reserve, Hong Kong. Asian Mar Biol 13:141–166Google Scholar
  80. Thiele J (1925) Gastropoda der Deutschen Tiefsee-Expedition, II Teil: Deutsch Tiefsee-Expedition auf dem Dampfer “Valdivia” 1898–1899. Wissenschaftliche Ergebnisse 17:35–382Google Scholar
  81. Thompson JD, Gibson TJ, Plewniak E, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  82. Tröndlé J, Boutet M (2009) Inventory of marine molluscs of French Polynesia. Atoll Res Bull 570:1–87Google Scholar
  83. Turner SJ (1992) The biology and population outbreaks of the corallivorous gastropod Drupella on Indo-Pacific reefs. Oceanogr Mar Biol Annu Rev 32:461–530Google Scholar
  84. Vermeij GJ (2001) Community assembly in the sea: geologic history of the living shore biota. In: Bertness M, Gaines S, Hay ME (eds) Marine community ecology. Sinauer Associates, Sunderland, Massachusetts, pp 39–60Google Scholar
  85. Vermeij GJ (2010) Crucibles of creativity: the geographic origins of tropical molluscan innovations. Evol Ecol. doi: 10.1007/s10682-010-9458-2
  86. Vermeij GJ, Carlson SJ (2000) The muricid gastropod subfamily Rapaninae: phylogeny and ecological history. Paleobiology 26:19–46CrossRefGoogle Scholar
  87. Wallace CC, Rosen BR (2006) Diverse staghorn corals (Acropora) in high-latitude Eocene assemblages: implications for the evolution of modern diversity patterns of reef corals. Proc R Soc Biol Sci Ser B 273:975–982CrossRefGoogle Scholar
  88. Wiens JJ (1998) Combining data sets with different phylogenetic histories. Syst Biol 47:568–581PubMedCrossRefGoogle Scholar
  89. Williams ST (2007) Origins and diversification of Indo-West Pacific marine fauna: evolutionary history and biogeography of turban shells (Gastropoda, Turbinidae). Biol J Linn Soc 92:573–592CrossRefGoogle Scholar
  90. Williams ST, Ozawa T (2006) Molecular phylogeny suggests polyphyly of both the turban shells (family Turbinidae) and the superfamily Trochoidea (Mollusca, Vetigastropoda). Mol Phylogenet Evol 39:33–55PubMedCrossRefGoogle Scholar
  91. Williams ST, Duda TF (2008) Did tectonic activity stimulate Oligo-Miocene speciation in the Indo-West Pacific? Evolution 62:1618–1634PubMedCrossRefGoogle Scholar
  92. Wilson M, Rosen BR (1998) Implications of paucity of corals in the Paleogene of SE Asia: plate tectonics or centre of origin. In: Hall R, Holloway J (eds) Biogeography and geological evolution of SE Asia. Backhuys Publishers, Leiden, The Netherlands, pp 165–195Google Scholar
  93. Wood R (1999) Reef evolution. Oxford University Press, Oxford, UK, p 354Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Department of ZoologyNatural History MuseumLondonUK
  2. 2.Division of BiologyImperial College LondonAscotUK

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