Advertisement

The Neogastropoda: Evolutionary Innovations of Predatory Marine Snails with Remarkable Pharmacological Potential

  • Maria Vittoria Modica
  • Mandë Holford
Chapter

Abstract

The Neogastropoda include many familiar molluscs, such as cone snails (Conidae), purple dye snails (Muricidae), mud snails (Nassariidae), olive snails (Olividae), oyster drills (Muricidae), tulip shells (Fasciolariidae), and whelks (Buccinidae). Due to their amazing predatory specializations, neogastropods are often dominant members of the benthic community at the top of the food chain. In a dazzling display that ranges from boring holes to darting harpoons, neogastropods have developed several prey hunting innovations with specialized compounds pharmaceutical companies could only dream about. It has been hypothesized that evolutionary innovations related to feeding were the main drivers of the rapid neogastropod radiation in the late Cretaceous. The anatomical, behavioral, and biochemical specializations of neogastropod families that are promising targets in drug discovery and development are addressed within an evolutionary framework in this chapter.

Keywords

Salivary Gland Venom Gland Venom Peptide Marine Snail Cone Snail 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors thank Marco Oliverio for invaluable advice and helpful comments on the manuscript. Yuri Kantor, Alisa Kosyan, Gregory Herbert, Paolo Mariottini, Marco Oliverio, and Guido and Philippe Poppe are acknowledged for images used in the figures. MH acknowledges support from NIH grant GM088096-01.

References

  1. Andrews EB (1991) The fine structure and function of the salivary glands of Nucella lapillus (Gastropoda: Muricidae). J Moll Stud 57:111–126Google Scholar
  2. Andrews EB, Elphick MR, Thorndyke MC (1991) Pharmacologically active constituents of the accessory salivary and hypobranchial glands of Nucella lapillus. J Moll Stud 57:136–138Google Scholar
  3. Angulo Y, Escolano J, Lomonte B, Gutiérrez JM, Sanz L, Calvete JJ (2007) Snake venomics of Central American pitvipers: clues for rationalizing the distinct envenomation profiles of Atropoides nummifer and Atropoides picadoi. J Proteome Res 7(2):706–719Google Scholar
  4. Asano M, Itoh M (1959) Occurrence of tetramine and choline compounds in the salivary gland of a marine gastropod Neptunea arthritica (Bernardi). J Agric Res 10:209Google Scholar
  5. Asano M, Itoh M (1960) Salivary poison of a marine gastropod, Neptunea arthritica Bernardi, and the seasonal variation of its toxicity. Ann N Y Acad Sci 90:675–688Google Scholar
  6. Bigatti G, Sanchez Antelo CJM, Miloslavich P, Penchaszadeh PE (2009) Feeding behavior of Adelomelon ancilla (Lighfoot, 1786): a predatory neogastropod (Gastropoda: Volutidae) in Patagonian benthic communities. The Nautilus 123(3):159–165Google Scholar
  7. Biggs JS, Olivera BM, Kantor YI (2008) α-Conopeptides specifically expressed in the salivary gland of Conus pulicarius. Toxicon 52:101–105PubMedGoogle Scholar
  8. Bouchet P (1989) A marginellid gastropod parasitize sleeping fishes. Bull Mar Sci 45:76–84Google Scholar
  9. Bouchet P, Perrine D (1996) More gastropods feeding at night on parrotfishes. Bull Mar Sci 59(1):224–228Google Scholar
  10. Bouchet P, Rocroi JP (2005) Classification and nomenclator of gastropod families. Malacologia 47(1–2):1–397Google Scholar
  11. Brinkman DL, Burnell JN (2009) Biochemical and molecular characterisation of cubozoan protein toxins. Toxicon 54:1162–1173PubMedGoogle Scholar
  12. Bulaj G (2008) Integrating the discovery pipeline for novel compounds targeting ion channels. Curr Opin Chem Biol 12:441–447PubMedGoogle Scholar
  13. Carriker MR (1961) Comparative functional morphology of boring mechanisms in gastropods. Am Zool 1(2):263–266Google Scholar
  14. Carriker MR (1981) Shell penetration and feeding by naticacean and muricacean predatory neogastropods: a synthesis. Malacologia 20:403–422Google Scholar
  15. Colgan DJ, Ponder WF, Beacham E, Macaranas JM (2007) Molecular phylogenetics of Caenogastropoda (Gastropoda: Mollusca). Mol Phylogenet Evol 42(3):717–737PubMedGoogle Scholar
  16. Darragh TA, Ponder WF (1998) Family Volutidae. In: Beesley PL, Ross JGB, Wells A (eds) Mollusca: the Southern synthesis. Fauna of Australia, vol 5. CSIRO Publishing, Melbourne, pp 833–835, part BGoogle Scholar
  17. Dietl GP, Herbert GS (2005) Influence of alternative shell-drilling behaviours on attack duration of the predatory snail Chicoreus dilectus. J Zool 265:201–206Google Scholar
  18. Duda TFJ, Palumbi SR (1999) Molecular genetics of ecological diversification: duplication and rapid evolution of toxin genes of the venomous gastropod Conus. Proc Natl Acad Sci USA 96:6820–6823PubMedGoogle Scholar
  19. Emmelin N, Fänge R (1958) Comparison between biological effects of neurine and a salivary glands extract of Neptunea antiqua. Acta Zool 39:47–52Google Scholar
  20. Endean R (1972) Aspects of molluscan pharmacology. In: Florkin M, Scheer BT (eds) Chemical zoology, vol 7, Mollusca. Academic Press, New York, pp 421–466Google Scholar
  21. Endean R, Parrish G, Gyr P (1974) Pharmacology of the venom of Conus geographus. Toxicon 12:131PubMedGoogle Scholar
  22. Escoubas P, Sollod B, King GF (2006) Venom landscapes: mining the complexity of spider venoms via a combined cDNA and mass spectrometric approach. Toxicon 47:650–663PubMedGoogle Scholar
  23. Fänge R (1960) The salivary gland of Neptunea antiqua. Ann N Y Acad Sci 90:689–694PubMedGoogle Scholar
  24. Favreau P, Stöcklin R (2009) Marine snail venoms: use and trends in receptor and channel neuropharmacology. Curr Opin Pharmacol 9:594–601PubMedGoogle Scholar
  25. Fleming C (1971) Case of poisoning from red whelks. Br Med J 3:250–251Google Scholar
  26. Fox JW, Serrano SM (2007) Approaching the golden age of natural product pharmaceuticals from venom libraries: an overview of toxins and toxin-derivatives currently involved in therapeutic or diagnostic applications. Curr Pharm Res 13:2927–2934Google Scholar
  27. Fretter V, Graham A (1994) British prosobranch molluscs. Revised and updated edition, Ray Society, LondonGoogle Scholar
  28. Fry BG (2005) From genome to “venome”: molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins. Genome Res 15:403–420PubMedGoogle Scholar
  29. Fry BG, Wüster W (2004) Assembling an arsenal: origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences. Mol Biol Evol 21(5):870–883PubMedGoogle Scholar
  30. Fujii R, Moriwaki N, Tanaka K, Ogawa T, Mori E, Saitou M (1992) Spectrophotometric determination of tetramine in carnivorous gastropods with tetrabromophenolphthalein ethyl ester. J Food Hyg Soc Japan 33(3):237–240Google Scholar
  31. Harasewych MG (2009) Anatomy and biology of Mitra cornea Lamarck, 1811 (Mollusca, Caenogastropoda, Mitridae) from the Azores. Açoreana 6:121–135Google Scholar
  32. Haynes JA (1990) Distribution movement and impact of the corallivorous gastropod Coralliophila abbreviata (Lamarck) in a Panamanian patch. J Exp Mar Biol Ecol 142:25–42Google Scholar
  33. Hemingway GT (1978) Evidence for a paralytic venom in the intertidal snail Acanthina spirata (Neogastropoda: Thaisidae). Comp Biochem Physiol 60C:79–81Google Scholar
  34. Heralde FM, Imperial J, Bandyopadhyay P, Olivera BM, Concepcion GP, Santos AD (2008) A rapidly diverging superfamily of peptide toxins in venomous Gemmula species. Toxicon 51:890–897PubMedGoogle Scholar
  35. Holford M, Puillandre N, Modica MV, Watkins M, Collin R, Bermingham E, Olivera BM (2009a) Correlating molecular phylogeny with venom apparatus occurrence in panamic auger snails (Terebridae). PLoS ONE 4(11):e7667. doi:10.1371/journal.pone.0007667PubMedGoogle Scholar
  36. Holford M, Puillandre N, Terryn Y, Cruaud C, Olivera BM, Bouchet P (2009b) Evolution of the Toxoglossa venom apparatus as inferred by molecular phylogeny of the Terebridae. Mol Biol Evol 26(1):15–25PubMedGoogle Scholar
  37. Huang CL, Mir GN (1972) Pharmacological investigation of salivary gland of Thais haemastoma (Clench). Toxicon 10:111–117PubMedGoogle Scholar
  38. Imperial JS, Watkins M, Chen P, Hillyard DR, Cruz LJ, Olivera BM (2003) The augertoxins: biochemical characterization of venom components from the toxoglossate gastropod Terebra subulata. Toxicon 42:391–398PubMedGoogle Scholar
  39. Imperial JS, Kantor YI, Watkins M, Heralde FM, Stevenson B, Chen P, Hansson K, Stenflo J, Ownby J-P, Bouchet P, Olivera BM (2007) Venomous auger snail Hastula (Impages) hectica (Linnaeus, 1758): molecular phylogeny, foregut anatomy and comparative toxinology. J Exp Zool 308B:744–756Google Scholar
  40. Johnson S, Johnson J, Jazwinski S (1995) Parasitism of sleeping fish by gastropod mollusks in the Colubrariidae and Marginellidae at Kwajalein, Marshall Islands. The Festivus 27(11):121–126Google Scholar
  41. Kantor YI (1996) Phylogeny and relationships of Neogastropoda. In: Taylor J (ed) Origin and evolutionary radiation of the Mollusca. Oxford University Press, Oxford, pp 221–230Google Scholar
  42. Kantor YI (2002) Morphological prerequisite for understanding neogastropod phylogeny. Boll Malacol Suppl 4:161–174Google Scholar
  43. Kantor YI, Fedosov A (2009) Morphology and development of the valve of Leiblein: possible evidence for paraphyly of the Neogastropoda. The Nautilus 123(3):73–82Google Scholar
  44. Kohn AJ (1956) Piscivorous gastropods of the genus Conus. Proc Natl Acad Sci USA 42:168–171PubMedGoogle Scholar
  45. Kohn AJ (1959) The ecology of Conus Hawaii. Ecol Monogr 29:47–90Google Scholar
  46. Kohn AJ (1968) Microhabitats, abundance and food of Conus (Gastropoda) on atoll reefs in the Maldive and Chagos islands. Ecology 49:1046–1062Google Scholar
  47. Kohn AJ (1978) Ecological shift and release in an isolated reefs: the significance of prey size. Ecology 59:614–631Google Scholar
  48. Kohn AJ, Nybakken JW (1975) Ecology of Conus on eastern Indian ocean fringing reefs: diversity of species and resource utilization. Mar Biol 29:211–234Google Scholar
  49. Kohn AJ, Saunders PR, Wiener S (1960) Preliminary studies on the venom of the marine snail Conus. Ann N Y Acad Sci 90:706–725PubMedGoogle Scholar
  50. Kosuge S (1986) Description of a new species of ecto-parasitic snail on fish. Bull Inst Malacol 2(5):77Google Scholar
  51. Leviten PJ (1980) The foraging strategy of vermivorous conid gastropods. Ecol Monogr 46:157–178Google Scholar
  52. Marcus E, Marcus E (1959) Studies on Olividae. Bol Fac Fil Ciênc Let Univ S Paulo Zool 22:99–188Google Scholar
  53. Marko PB, Vermeij GJ (1999) Molecular phylogenetics and the evolution of labral spines among eastern pacific ocenebrine gastropods. Mol Phylogenet Evol 13(2):275–288PubMedGoogle Scholar
  54. Marsh M (1971) The foregut glands of some vermivorous cone shells. Aust J Zool 19:313–326Google Scholar
  55. Martoja M (1964) Contribution a l’étude de l’appareil digestif et la digestion chez les gastéropodes carnivores de la famille Nassaridés. Cell 64:237–334Google Scholar
  56. Martoja M (1971) Données histologiques sur les glandes salivaires et oesophagiennes de Thais lapillus (L.) (= Nucella lapillus. Prosobranche Néogastropode) Arch Zool Exp Gen 112:249–291Google Scholar
  57. McGraw KA, Gunter G (1972) Observations on killing of the Virginia oyster by the Gulf oyster borer, Thais haemastoma, with evidence for a paralytic secretion. Proc Natl Shellfish Assoc 62:95–97Google Scholar
  58. Miljanich GP (2004) Ziconotide: neuronal calcium channel blocker for treating severe chronic pain. Curr Med Chem 11:3029–3040PubMedGoogle Scholar
  59. Millar JG, Dey A (1987) Food poisoning due to the consumption of red whelks Neptunea antiqua. Comm Dis Scotl Wkly Rep 21(38):5–6Google Scholar
  60. Minniti F (1986) Morphological and histochemical study of pharynx of Leiblein, salivary glands and gland of Leiblein in the carnivorous Gastropoda Amyclina tinei Maravigna and Cyclope neritea Lamarck (Nassariidae: Prosobranchia Stenoglossa). Zool Anz 217:14–22Google Scholar
  61. Modica MV, Kosyan A, Oliverio M (2009) The relationships of the enigmatic gastropod Tritonoharpa: new data on early neogastropod evolution? The Nautilus 123(3):177–188Google Scholar
  62. Morton B, Chan K (1997) The first report of shell-boring predation by a representative of the Nassariidae (Gastropoda). J Moll Stud 63:480–482Google Scholar
  63. Naegel LCA, Aguilar-Cruz CA (2006) The hypobranchial gland from the purple snail Plicopurpura pansa (Gould, 1853) (Prosobranchia, Muricidae). J Shellfish Res 25(2):391–394Google Scholar
  64. Nascimento DG, Rates B, Santos DM, Verano-Braga T, Barbosa-Silva A, Dutra AAA, Biondi I, Martin-Euclaire MF, De Lima ME, Pimenta AMC (2006) Moving pieces in a taxonomic puzzle: venom 2D-LC/MS and data clustering analyses to infer phylogenetic relationships in some scorpions from the Buthidae family (Scorpiones). Toxicon 47:628–639PubMedGoogle Scholar
  65. Nielsen C (1975) Observations on Buccinum undatum L. attacking bivalves and on prey responses, with a short review on attacking methods of other prosobranchs. Ophelia 13:87–108Google Scholar
  66. Norton RS, Olivera BM (2006) Conotoxins down under. Toxicon 48:780–798PubMedGoogle Scholar
  67. O’Sullivan JB, McConnaughey RR, Huber ME (1987) A blood-sucking snail: the Cooper’s nutmeg Cancellaria cooperi Gabb, parasitizes the California electric ray, Torpedo californica Ayres. Biol Bull 172:362–366Google Scholar
  68. Ohno S (1970) Evolution by gene duplication. Springer, BerlinGoogle Scholar
  69. Olivera BM (2002) Conus venom peptides: Reflections from the biology of clades and species. Annu Rev Ecol Syst 33:25–47Google Scholar
  70. Olivera BM (2006) Conus peptides: biodiversity-based discovery and exogenomics. J Biol Chem 281:31173–31177PubMedGoogle Scholar
  71. Olivera BM, Teichert RW (2007) Diversity of the neurotoxic Conus peptides: a model for concerted pharmacological discovery. Mol Interv 7(5):253–262Google Scholar
  72. Olivera BM, Rivier J, Clark C, Ramilo CA, Corpuz GP, Abogadie FC, Mena EE, Woodward SR, Hillyard DR, Cruz LJ (1990) Diversity of Conus neuropeptides. Science 249:257–263PubMedGoogle Scholar
  73. Oliverio M, Modica MV (2009) Relationships of the haematophagous marine snail Colubraria (Rachiglossa, Colubrariidae), within the neogastropod phylogenetic framework. Zool J Linn Soc. 158:779–800Google Scholar
  74. Oliverio M, Barco A, Modica MV, Richter A, Mariottini P (2008) Ecological barcoding of corallivory by ITS2 sequences: hosts of coralliophiline gastropods detected by the cnidarian DNA in their stomach. Mol Ecol Resour 9(1):94–103PubMedGoogle Scholar
  75. Palmer AR (1990) Effect of crab effluent and scent of damaged conspecifics on feeding, growth, and shell morphology of the Atlantic dogwhelk, Nucella lapillus (L.). Hydrobiologia 193:155–182Google Scholar
  76. Peterson CH, Black R (1995) Drilling by buccinid gastropods of the genus Cominella in Australia. The Veliger 38:37–42Google Scholar
  77. Petit RE, Harasewych MG (1986) New Philippine Cancellariidae (Gastropoda: Cancellariacea), with notes on the fine structure and function of the nematoglossan radula. The Veliger 28(4):436–443Google Scholar
  78. Ponder WF (1970) The morphology of Alcithoe arabica (Mollusca: Volutidae). Malacol Rev 3:127–165Google Scholar
  79. Ponder WF (1972) The morphology of some mitriform gastropods with special reference to their alimentary and reproductive system (Neogastropoda). Malacologia 11(2):295–342Google Scholar
  80. Ponder WF (1973) The origin and evolution of the Neogastropoda. Malacologia 12:295–338PubMedGoogle Scholar
  81. Ponder WF (1998a) Infraorder Neogastropoda. In: Beesley PL, Ross JGB, Wells A (eds) Mollusca: the Southern synthesis. Fauna of Australia, vol 5. CSIRO Publishing, Melbourne, p 819 part BGoogle Scholar
  82. Ponder WF (1998b) Family Costellariidae. In: Beesley PL, Ross JGB, Wells A (eds) Mollusca: the Southern synthesis. Fauna of Australia, vol 5. CSIRO Publishing, Melbourne, pp 843–845, part BGoogle Scholar
  83. Ponder WF, Lindberg DR (1996) Gastropod phylogeny – challenges for the 90s. In: Taylor J (ed) Origin and evolutionary radiation of the Mollusca. Oxford University Press, London, pp 135–154Google Scholar
  84. Ponder WF, Lindberg DR (1997) Towards a phylogeny of gastropod molluscs: an analysis using morphological characters. Zool J Linn Soc 119:83–265Google Scholar
  85. Ponder WF, Taylor JD (1992) Predatory shell drilling by two species of Austroginella (Gastropoda: Marginellidae). J Zool 228:317–328Google Scholar
  86. Power AJ, Keegan BF, Nolan K (2002) The seasonality and role of the neurotoxin tetramine in the salivary glands of the red whelk Neptunea antiqua L. Toxicon 40:419–425PubMedGoogle Scholar
  87. Puillandre N, Samadi S, Boisselier M-C, Sysoev AV, Kantor YI, Cruaud C, Couloux A, Bouchet P (2008) Starting to unravel the toxoglossan knot: molecular phylogeny of the “turrids” (Neogastropoda: Conoidea). Mol Phylogenet Evol 47:1122–1134PubMedGoogle Scholar
  88. Radwin GE, D’Attilio A (1976) Murex shells of the world. Stanford University Press, StanfordGoogle Scholar
  89. Reid TMS, Gould IM, Mackie IM, Ritchie AH, Hobbs G (1988) Food poisoning due to the consumption of red whelks Neptunea antiqua. Epidemiol Infect 101:419PubMedGoogle Scholar
  90. Remigio EA, Duda TFJ (2008) Evolution of ecological specialization and venom of a predatory marine gastropod. Mol Ecol 17:1156–1162PubMedGoogle Scholar
  91. Richter A, Luque AA (2002) Current knowledge on Coralliophilidae (Gastropoda) and phylogenetic implication of anatomical and reproductive characters. Boll Malacol 38:5–19Google Scholar
  92. 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
  93. Romeo C, Di Francesco L, Oliverio M, Palazzo P, Raybaudi Massilia G, Ascenzi P, Polticelli F, Schininà ME (2008) Conus ventricosus venom peptides profiling by HPLC-MS: a new insight in the intraspecific variation. J Sep Sci 31:488–498PubMedGoogle Scholar
  94. Roseghini M, Severini C, Falconieri Erspamer G, Erspamer V (1996) Choline esters and biogenic amines in the hypobranchial gland of 55 molluscan species of the neogastropod Muricoidea superfamily. Toxicon 34(1):33–55PubMedGoogle Scholar
  95. Saitoh H, Oikawa K, Takano T, Kamimura K (1983) Determination of tetramethylammonium ion in shellfish by ion chromatography. J Chromatogr 281:397PubMedGoogle Scholar
  96. Shiomi K, Mizukami M, Shimakura K, Nagashima Y (1994) Toxins in the salivary gland of some marine carnivorous gastropods. Comp Biochem Physiol 107B:427–432Google Scholar
  97. Smith EH (1967) The neogastropod midgut, with notes on the digestive diverticula and intestine. Trans R Soc Edinburgh 67:23–42Google Scholar
  98. Strong EE (2003) Refining molluscan characters: morphology, character coding and a phylogeny of the Caenogastropoda. Zool J Linn Soc 137:447–554Google Scholar
  99. Taylor JD (1976) Habitats, abundance and diets of muricacean gastropods at Aldabra Atoll. Zool J Linn Soc 59:155–193Google Scholar
  100. Taylor JD (1978) Habitats and diet of predatory gastropods at Addu Atoll, Maldives. J Exp Mar Biol Ecol 31:83–103Google Scholar
  101. Taylor JD, Morris NJ (1988) Relationships of neogastropoda. Malacol Rev 4:167–179Google Scholar
  102. Taylor JD, Morris NJ, Taylor CN (1980) Food specialization and the evolution of predatory prosobranch gastropods. Palaentology 23(2):375–409Google Scholar
  103. Taylor JD, Kantor YI, Sysoev AV (1993) Foregut anatomy, feeding mechanisms, relationships and classification of the Conoidea (=Toxoglossa) (Gastropoda). Bull Br Mus Nat Hist 59:125–170Google Scholar
  104. Terlau H, Olivera BM (2004) Conus venoms: a rich source of novel ion channel-targeted peptides. Pysiol Rev 84:41–68Google Scholar
  105. Twede VD, Miljanich GP, Olivera BM, Bulaj G (2009) Neuroprotective and cardioprotective conopeptides: an emerging class of drug leads. Curr Opin Drug Discov Dev 12:231–239Google Scholar
  106. Ward J (1965) The digestive tract and its relation to feeding habits in the stenoglossan prosobranch Coralliophila abbreviata (Lamarck). Can J Zool 43:447–464PubMedGoogle Scholar
  107. Watkins M, Hillyard DR, Olivera BM (2006) Genes expressed in a turrid venom duct: divergence and similarity to conotoxins. J Mol Evol 62:247–256PubMedGoogle Scholar
  108. Watson-Wright WM, Sims GG, Smyth C, Gillis M, Maher M, Trottier T, Van Sinclair DE, Gilgan M (1992) Identification of tetramine as toxin causing food poisoning in Atlantic Canada following consumption of whelks Neptunea decemcostata. In: Gopalakrishnakone P, Tan CK (eds) Recent advances in toxinology research, vol 2. University of Singapore, Singapore, pp 551–561Google Scholar
  109. Wells HW (1958) Feeding habits of Murex fulvescens. Ecology 39:556–558Google Scholar
  110. West DJ, Andrews EB, Bowman D, McVean AR, Thorndyke MC (1996) Toxins from some poisonous and venomous marine snails. Comp Biochem Physiol 113C:l–10Google Scholar
  111. Wu SK (1965) Comparative functional studies of the digestive system of the muricid gastropods Drupa ricina and Morula granulata. Malacologia 3:211–233Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  1. 1.Dipartimento di Biologia Animale e dell’Uomo“La Sapienza”, University of RomeRomeItaly
  2. 2.The City University of New York – York College & Graduate Center, and The American Museum of Natural HistoryNYUSA

Personalised recommendations