Biodiversity of cone snails and other venomous marine gastropods: Evolutionary success through neuropharmacology

Annual Review of Animal Biosciences

Volumn 2, Issue , 2014, Pages 487-513

  Olivera, Baldomero M ^a   Corneli, Patrice Showers ^a   Watkins, Maren ^a   Fedosov, Alexander ^b  

^a UNIVERSITY OF UTAH   (United States)

^b SEVERTSOV INSTITUTE OF ECOLOGY AND EVOLUTION   (Russian Federation)

Author keywords

Conoidea; diversity; gene families; venom peptide

Indexed keywords

MOLLUSC VENOM;

ANIMAL; BIODIVERSITY; CLASSIFICATION; EVOLUTION; GASTROPOD; GENETICS; PHYSIOLOGY;

ANIMALS; BIODIVERSITY; BIOLOGICAL EVOLUTION; GASTROPODA; MOLLUSK VENOMS;

EID: 84904756170     PISSN: 21658102     EISSN: 21658110     Source Type: Journal    
DOI: 10.1146/annurev-animal-022513-114124     Document Type: Article

References (89)

1. Olivera BM. 1997. E.E. Just Lecture, 1996: Conus venom peptides, receptor and ion channel targets and drug design: 50 million years of neuropharmacology. Mol. Biol. Cell 8:2101-9
2. Olivera BM. 2002. Conus venom peptides: Reflections from the biology of clades and species. Annu. Rev. Ecol. Evol. Syst. 33:25-42
3. Puillandre N, Kantor Y, Sysoev AV, Couloux A, Meyer CP, et al. 2011. The dragon tamed? A molecular phylogeny of the Conoidea (Mollusca, Gastropoda). J. Molluscan Stud. 77:259-72
4. Puillandre N, Samadi S, Boisselier MC, Sysoev AV, Kantor YI, et al. 2007. Starting to unravel the toxoglossan knot: Molecular phylogeny of the "turrids" (Neogastropoda: Conoidea). Mol. Phylogenetics Evol. 47:1122-34
5. Bouchet P, Rocroi JP. 2005. Malacologia: International Journal of Malacology, Classification and Nomenclator of Gastropod Families. Hackenheim, Ger.: ConchBooks
6. Ponder WF, Waren A. 1988. Classification of Caenogastropoda and Heterostropha-a list of familygroup names and higher taxa. Malacol. Rev. 21(Suppl.):288-317
7. Taylor JD, Morris NJ. 1988. Relationships of Neogastropoda. Malacol. Rev. 21(Suppl. 4):167-79
8. Olivera BM, Bulaj G, Garrett JE, Terlau H, Imperial JS. 2009. Peptide toxins from the venoms of cone snails and other toxoglossan gastropods. In Animal Toxins-State of the Art: Perspectives in Health and Biotechnology, ed. ME De Lima, pp. 25-48. Belo Horizonte, Braz.: Editora UFMG
9. OliveraBM,WatkinsM,Bandyopadhyay P, Imperial JS, de la Cotera EP, et al. 2012. Adaptive radiation of venomous marine snail lineages and the accelerated evolution of venom peptide genes. Ann. N.Y. Acad. Sci. 1267:61-70
10. Olivera BM, Teichert RW. 2007. Diversity of the neurotoxic Conus peptides: A model for concerted pharmacological discovery. Mol. Interv. 7:251-60
11. Tucker JK, Tenorio MJ. 2009. Systematic Classification of Recent and Fossil Conoidean Gastropods. Hackenheim, Ger.: ConchBooks
12. Castelin M, Puillandre N, Kantor Y, Modica MV, Terryn Y, et al. 2012. Macroevolution of venom apparatus innovations in auger snails (Gastropoda; Conoidea; Terebridae). Mol. Phylogenetics Evol. 64:21-44
13. Bratcher T, Cernohorsky WO. 1987. Living Terebras of the World. New York: Am. Malacol.
14. HolfordM, Puillandre N, Terryn Y, Cruaud C, Olivera B, Bouchet P. 2009. Evolution of the Toxoglossa venom apparatus as inferred by molecular phylogeny of the Terebridae. Mol. Biol. Evol. 26:15-25
15. Imperial JS, Kantor Y, Watkins M, Heralde FM III, Stevenson B, et al. 2007. Venomous auger snail Hastula (Impages) hectica (Linnaeus, 1758): Molecular phylogeny, foregut anatomy and comparative toxinology. J. Exp. Zool. B Mol. Dev. Evol. 308B:744-56
16. Puillandre N, Holford M. 2010. The Terebridae and teretoxins: Combining phylogeny and anatomy for concerted discovery of bioactive compounds. BMC Chem. Biol. 10:7
17. Bouchet P, Kantor Y, Sysoev AV, Puillandre N. 2011. A new operational classification of the Conoidea (Gastropoda). J. Molluscan Stud. 77:273-308
18. Powell AWB. 1966. The molluscan families Speightiidae and Turridae. Bull. Auckl. Inst. Mus. 5:1-184 (and 23 plates)
19. Taylor JD, Kantor Y, Sysoev AV. 1993. Foregut anatomy, feeding mechanisms, relationships and classification of the Conoidea (5Toxoglossa) (Gastropoda). Bull. Nat. Hist. Mus. Lond. Zool. 59:125-70
20. Bouchet P, Ng P, Largo D, Tan SH. 2009. Panglao 2004-investigations of the marine species richness in the Philippines. Raffles Bull. Zool. 20:1-19
21. Bouchet P, Lozouet P, Maestrati P, Heros V. 2002. Assessing the magnitude of species richness in tropical marine environments: High numbers of molluscs at a New Caledonia site. Biol. J. Linn. Soc. Lond. 75:421-36
22. Bouchet P, Lozouet P, Sysoev AV. 2009. An inordinate fondness for turrids. Deep Sea Res. II Top. Stud. Oceanogr. 56:1724-31
23. Seronay RA, Fedosov AE, Astilla MA, Watkins M, Saguil N, et al. 2010. Accessing novel conoidean venoms: Biodiverse lumun-lumun marine communities, an untapped biological and toxinological resource. Toxicon 56:1257-66
24. Duda TF Jr, Kohn AJ. 2005. Species-level phylogeography and evolutionary history of the hyperdiverse marine gastropod genus Conus. Mol. Phylogenetics Evol. 34:257-72
25. Duda TF Jr, Kohn AJ, Palumbi S.R. 2001. Origins of diverse feeding ecologies within Conus, a genus of venomous marine gastropods. Biol. J. Linn. Soc. Lond. 73:391-409
26. Espiritu DJD, Watkins M, Dia-Monje V, Cartier GE, Cruz LJ, Olivera BM. 2001. Venomous cone snails: Molecular phylogeny and the generation of toxin diversity. Toxicon 39:1899-916
27. Monje VD, Ward R, Olivera BM, Cruz LJ. 1999. 16S mitochondrial ribosomal RNA gene sequences: A comparison of seven Conus species. Philipp. J. Sci. 128:225-37
28. Kraus NJ, Corneli PS, Watkins M, Bandyopadhyay PK, Seger J, Olivera BM. 2011. Against expectation:A short sequence with high signal elucidates cone snail phylogeny. Mol. Phylogenetics Evol. 58:383-89
29. Kraus NJ, Watkins M, Bandyopadhyay PK, Seger J, Olivera BM, Corneli PS. 2012. A very short, functionally constrained sequence diagnoses cone snails in several Conasprella clades. Mol. Phylogenetics Evol. 65:335-38
30. Nam HH, Corneli PS, Watkins M, Olivera B, Bandyopadhyay P. 2009. Multiple genes elucidate the evolution of venomous snail-hunting Conus species. Mol. Phylogenetics Evol. 53:645-52
31. Cunha RL, Tenorio MJ, Afonso C, Castilho R, Zardoya R. 2008. Replaying the tape: Recurring biogeographical patterns in Cape Verde Conus after 12 million years. Mol. Ecol. 17:885-901
32. Duda TF Jr, Palumbi S.R. 1999. Molecular genetics of ecological diversification: Duplication and rapid evolution of toxin genes of the venomous gastropod Conus. Proc. Natl. Acad. Sci. USA 96:6820-23
33. Duda TF Jr, Palumbi S.R. 1999. Developmental shifts and species selection in gastropods. Proc. Natl. Acad. Sci. USA 96:10272-77
34. Kantor YI, Taylor JD. 2000. Formation of marginal radular teeth in Conoidea (Neogastropoda) and the evolution of the hypodermic envenomation mechanism. J. Zool. 252:251-62
35. Kilburn RN, Fedosov AE, Olivera BM. 2012. Revision of the genus Turris Batsch, 1789 (Gastropoda: Conoidea: Turridae) with the description of six new species. Zootaxa 3244:1-58
36. Kohn AJ. 1956. Piscivorous gastropods of the genus Conus. Proc. Natl. Acad. Sci. USA 42:168-71
37. Kohn AJ. 1960. Ecological notes on Conus (Mollusca, Gastropoda) in the Trincoma-lee region of Ceylon. Ann. Mag. Nat. Hist. 13:309-20
38. Schulz JR, Norton AG, Gilly WF. 2004. The projectile tooth of a fish-hunting cone snail: Conus catus injects venom into fish prey using a high-speed ballistic mechanism. Biol. Bull. 207:77-79
39. Salisbury SM,Martin GG, Kier WM, Schulz JR. 2010. Venom kinematics during prey capture in Conus: The biomechanics of a rapid injection system. J. Exp. Biol. 213:673-82
40. Fedosov A, Watkins M, Heralde FM III, Showers Corneli P, Concepcion GP, Olivera BM. 2011. Phylogeny of the genus Turris: Correlating molecular markers with radular anatomy and shell morphology. Mol. Phylogenetics Evol. 59:263-70
41. Kantor Y, Puillandre N. 2012. Evolution of the radular apparatus in Conoidea (Gastropoda: Neogastropoda) as inferred from a molecular phylogeny. Malacologia 55:55-90
42. Kantor YI, PuillandreN, Olivera BM, Bouchet P. 2008. Morphological proxies for taxonomic decision in turrids (Mollusca, Neogastropoda): A test of the value of shell and radula characters using molecular data. Zool. Sci. 25:1156-70
43. Taylor JD. 1990. The anatomy of the foregut and relationships in the Terebridae. Malacologia 32:19-34
44. Fedosov AE, Kantor Y. 2008. Toxoglossan gastropods of the subfamily Crassispirinae (Turridae) lacking a radula, and a discussion of the status of the subfamily Zemaciinae. J. Molluscan Stud. 74:27-35
45. Medinskaya AI, Sysoev AV. 2003. The anatomy of Zemacies excelsa, with a description of a new subfamily of Turridae. Ruthenica 13:81-87
46. Kantor YI, Taylor JD. 2002. Foregut anatomy and relationships of raphitomine gastropods (Gastropoda: Conoidea: Raphitominae). Int. J. Malacol. 4:83-110
47. Fedosov AE. 2007. Anatomy of accessory rhynchodeal organs of Veprecula vepratica and Tritonoturris subrissoides: New types of foregut morphology in Raphitominae (Conoidea). Ruthenica 17:33-41
48. Olivera BM, Gray WR, Zeikus R, McIntosh JM, Varga J, et al. 1985. Peptide neurotoxins from fishhunting cone snails. Science 230:1338-43
49. Olivera BM, Rivier J, Clark C, Ramilo CA, Corpuz GP, et al. 1990. Diversity of Conus neuropeptides. Science 249:257-63
50. Teichert RW, Raghuraman S, MemonT, Cox JL, Foulkes T, et al. 2012. Characterization of two neuronal subclasses through constellation pharmacology. Proc. Natl. Acad. Sci. USA 109:12758-63
51. Terlau H, Shon K, Grilley M, Stocker M, Stühmer W, Olivera BM. 1996. Strategy for rapid immobilization of prey by a fish-hunting cone snail. Nature 381:148-51
52. Terlau H, Olivera BM. 2004. Conus venoms: A rich source of novel ion channel-targeted peptides. Physiol. Rev. 84:41-68
53. Teichert RW, Smith NJ, Raghuraman S, Yoshikami D, Light AR, Olivera BM. 2012. Functional profiling of neurons through cellular neuropharmacology. Proc. Natl. Acad. Sci. USA 109:1388-95
54. Kohn AJ. 1959. The ecology of Conus in Hawaii. Ecol. Monogr. 29:47-90
55. Röckel D, Korn W, Kohn AJ. 1995. Manual of the Living Conidae. Wiesbaden, Ger.: Verlag Christa Hemmen. 517 pp.
56. Nybakken J, Perron FE. 1988. Ontogenetic change in the radula of Conus magus (Gastropoda). Mar. Biol. 98:239-42
57. Williams ST, Duda TF Jr. 2008. Did tectonic activity stimulate oligo-miocene speciation in the Indo-West Pacific? Evolution 62:1618-34
58. Olivera BM, Cruz L. 2001. Conotoxins, in retrospect. Toxicon 39:7-14
59. Kohn AJ. 1966. Food specialization in Conus in Hawaii and California. Ecology 47:1041-43
60. Kohn AJ. 1968. Microhabitats, abundance and food of Conus on atoll reefs in the Maldive and Chagos Islands. Ecology 49:1046-62
61. Kohn AJ. 1978. Ecological shift and release in an isolated population: Conus milaris at Easter Island. Ecol. Monogr. 48:323-36
62. Santos AD, McIntosh JM, Hillyard DR, Cruz LJ, Olivera BM. 2004. The A-superfamily of conotoxins: Structural and functional divergence. J. Biol. Chem. 279:17596-606
63. McIntosh JM, Santos AD, Olivera BM. 1999. Conus peptides targeted to specific nicotinic acetylcholine receptor subtypes. Annu. Rev. Biochem. 68:59-88
64. Naranjo D. 2002. Inhibition of single Shaker K channels by k-conotoxin-PVIIA. Biophys. J. 82:3003-11
65. Imperial J, Silverton N, Olivera BM, Bandyopadhyay P, Sporning A, et al. 2007. Using chemistry to reconstruct evolution: On the origins of fish-hunting in venomous cone snails. Proc. Am. Philos. Soc. 151:185-200
66. Kohn AJ. 2003. The feeding process in Conus victoriae. In The Marine Flora and Fauna of Dampier, Western Australia, ed. FE Wells, DI Walker, DS Jones, pp. 1-8. Perth: West. Aust. Mus.
67. Kohn AJ, Nybakken JW. 1975. Ecology of Conus on eastern Indian Ocean fringing reefs: Diversity of species and resource utilization. Mar. Biol. 29:211-34
68. Marsh H. 1971. Observations on the food and feeding of some vermivorous Conus on the Great Barrier Reef. Veliger 14:45-53
69. Biggs JS, Watkins M, Puillandre N, Ownby J-P, Lopez-Vera E, et al. 2010. Evolution of Conus peptide toxins: Analysis of Conus californicus Reeve, 1844. Mol. Phylogenetics Evol. 56:1-12
70. Marshall J, Kelley WP, Rubakhin SS, Bingham JP, Sweedler JV, Gilly WF. 2002. Anatomical correlates of venom production in Conus californicus. Biol. Bull. 203:27-41
71. Bingham JP, Burlingame AL, Moczydlowski E, Gilly WF. 2000. Highly selective conotoxin from Conus californicus that targets voltage-gated neuronal Na\+ channels of squid. J. Gen. Physiol. 116:12a-13a
72. Halstead BW. 1988. Poisonous and Venomous Marine Animals of the World. Princeton, NJ: Darwin Press. 2nd rev. ed.
73. Elliott EJ, Raftery MA. 1979. Venom of marine snail Conus californicus: Biochemical studies of a cholinomimetic component. Toxicon 17:259-68
74. Elliott EJ, Kehoe J. 1978. Cholinergic receptor in Aplysia neurons: Activation by a venom component from the marine snail Conus californicus. Brain Res. 156:387-90
75. Cottrell GA, Twarog BM. 1972. Proceedings: Active factors in the venom duct of Conus californicus. Br. J. Pharmacol. 44:365P-66P
76. Whysner JA, Saunders PR. 1963. Studies on the venom of the marine snail Conus californicus. Toxicon 1:113-22
77. Hinegardner RT. 1958. The venom apparatus of the cone shell. Hawaii Med. J. 17:533-36
78. Whysner JA, Saunders PR. 1966. Purification of the lethal fraction of the venom of the marine snail Conus californicus. Toxicon 4:177-78
79. Stewart J, Gilly WF. 2005. Piscivorous behavior of a temperate cone snail, Conus californicus. Biol. Bull. 209:146-53
80. Miller BA. 1970. Studies on the biology of Indo-Pacific Terebra. PhD diss., Univ. N.H., Durham, NH
81. HeraldeFM III, Kantor Y, Astilla MA, Lluisma AO, Geronimo R, et al. 2010. The Indo-Pacific Gemmula species in the subfamily Turrinae: Aspects of field distribution, molecular phylogeny, radular anatomy and feeding ecology. Philipp. Sci. Lett. 3:21-34
82. Powell AWB. 1964. The family Turridae in the Indo-Pacific. Part 1. The subfamily Turrinae. Indo-Pac. Mollusca 1:227-346
83. Aguilar MB, Chan de la Rosa RA, Falcón A, Olivera BM, Heimer de la Cotera EP. 2009. Peptide pal9a from the venom of the turrid snail Polystira albida from the Gulf of Mexico: Purification, characterization, and comparison with P-conotoxin-like (framework IX) conoidean peptides. Peptides 30:467-76
84. HeraldeFMIII, Imperial J, Bandyopadhyay PK, Olivera BM, Concepcion GP, Santos AD. 2008.Arapidly diverging superfamily of peptide toxins in venomous Gemmula species. Toxicon 51:890-97
85. López-Vera E, Heimer de la Cotera EP, Maillo M, Riesgo-Escovar JR, Olivera BM, Aguilar MB. 2004. A novel structural class of toxins: The methionine-rich peptides from the venoms of turrid marine snails (Mollusca, Conoidea). Toxicon 43:365-74
86. Watkins M, Hillyard DR, Olivera BM. 2006. Genes expressed in a turrid venom duct: Divergence and similarity to conotoxins. J. Mol. Evol. 62:247-56
87. Lluisma AO, Milash BA, Moore B, Olivera BM, Bandyopadhyay P. 2012. Novel venom peptides from the cone snail Conus pulicarius discovered through next-generation sequencing of its venom duct transcriptome. Mar. Genomics 5:43-51
88. Miljanich GP. 2004. Ziconotide: Neuronal calcium channel blocker for treating severe chronic pain. Curr. Med. Chem. 11:3029-40
89. Flecker H. 1936. Cone shell mollusc poisoning, with report of a fatal case. Med. J. Aust. 1:464-66