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Differentiation of Venoms of Predatory Marine Gastropods: Divergence of Orthologous Toxin Genes of Closely Related Conus Species with Different Dietary Specializations

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Abstract

Venoms of Conus are remarkably diverse among species and the genes that encode conotoxins show high rates of evolution. Yet no prior studies have specifically explored how conotoxin gene evolution contributes to the differentiation of venoms of closely related Conus species. Previous investigations of four-loop conotoxin expression patterns of six closely related Conus species identified 12 sets of putative orthologous loci from these species, including eight pairs of loci that are coexpressed by two of these six species, C. abbreviatus and C. miliaris. Here I analyze the molecular evolution of orthologous conotoxin loci of these species and specifically examine the divergence of the eight orthologous counterparts of C. abbreviatus and C. miliaris. Tree and maximum likelihood-based analyses of these sequences reveal that positive selection promotes the divergence of orthologous genes among species and that the evolution of orthologues of C. abbreviatus and C. miliaris is asymmetric among species. The asymmetric evolution of conotoxin loci among species may result from lineage-specific dietary shifts or interspecific differences in the impact of selection from predator-prey interactions on conotoxin loci.

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References

  • Conticello SG, Gilad Y, Avidan N et al (2001) Mechanisms for evolving hypervariability: the case of conopeptides. Mol Biol Evol 18:120–131

    PubMed  CAS  Google Scholar 

  • Duda TF Jr, Kohn AJ (2005) Species-level phylogeography and evolutionary history of the hyperdiverse marine gastropod genus Conus. Mol Phylogenet Evol 34:257–272

    Article  PubMed  Google Scholar 

  • Duda TF Jr, Palumbi SR (1999a) Molecular genetics of ecological diversification: duplication and rapid evolution of toxin genes of the venomous gastropod Conus. Proc Natl Acad Sci USA 96:6820–6823

    Article  PubMed  CAS  Google Scholar 

  • Duda TF Jr, Palumbi SR (1999b) Developmental shifts and species selection in gastropods. Proc Natl Acad Sci USA 96:10272–10277

    Article  PubMed  CAS  Google Scholar 

  • Duda TF Jr, Palumbi SR (2000) Evolutionary diversification of multigene families: allelic selection of toxins in predatory cone snails. Mol Biol Evol 17:1286–1293

    PubMed  CAS  Google Scholar 

  • Duda TF Jr, Palumbi SR (2004) Gene expression and feeding ecology: evolution of piscivory in the venomous gastropod genus Conus. Proc Roy Soc Lond Ser B Biol Scis 271:1165–1174

    Article  CAS  Google Scholar 

  • Duda TF Jr, Remigio EA (2008) Variation and evolution of toxin gene expression patterns of six closely related venomous marine snails. Mol Ecol 17:3018–3032

    Article  PubMed  CAS  Google Scholar 

  • Duda TF Jr, Rolán E (2005) Explosive radiation of Cape Verde Conus, a marine species flock. Mol Ecol 14:267–272

    Article  PubMed  Google Scholar 

  • Duda TF Jr, Kohn AJ, Palumbi SR (2001) Origins of diverse feeding ecologies within Conus, a genus of venomous marine gastropods. Biol J Linn Soc 73:391–409

    Article  Google Scholar 

  • Espiritu DJ, Watkins M, Monje VD, Cartier GE, Cruz LJ, Olivera BM (2001) Venomous cone snails: molecular phylogeny and the generation of toxin diversity. Toxicon 39:1899–1916

    Article  PubMed  CAS  Google Scholar 

  • Gibbs HL, Rossiter W (2008) Rapid evolution by positive selection and gene gain and loss: PLA2 venom genes in closely related Sistrurus rattlesnakes with divergent diets. J Mol Evol 66:151–166

    Article  PubMed  CAS  Google Scholar 

  • Ina Y (1995) New methods for estimating the numbers of synonymous and nonsynonymous substitutions. J Mol Evol 40:190–226

    Article  PubMed  CAS  Google Scholar 

  • Kohn AJ (1959) The ecology of Conus in Hawaii. Ecol Monogr 29(1):47–90

    Article  Google Scholar 

  • Kohn AJ (1966) Food specialization in Conus in Hawaii and California. Ecology 47:1041–1043

    Article  Google Scholar 

  • Kohn AJ (1968) Microhabitats, abundance and food of Conus on atoll reefs in the Maldive and Chagos islands. Ecology 49:1046–1062

    Article  Google Scholar 

  • Kohn AJ (1978) Ecological Shift and release in an isolated population: Conus miliaris at Easter Island. Ecol Monogr 48(3):323–336

    Article  Google Scholar 

  • Kohn AJ (1980) Abundance, diversity, and resource use in an assemblage of Conus species in Enewetak Lagoon. Pacif Sci 34(4):359–369

    Google Scholar 

  • Kohn AJ (2001) Maximal species richness in Conus: diversity, diet and habitat on reefs of northeast Papua New Guinea. Coral Reefs 20:25–38

    Article  Google Scholar 

  • Kohn AJ, Almasi KN (1993) Comparative ecology of a biogeographically heterogeneous Conus assemblage. In: Wells FE, Walker DI, Kirkman H, Lethbridge R (eds) Proceedings of the Fifth International Marine Biological Workshop: The Marine Flora and Fauna of Rottnest Island. Western Australia. Western Australia Museum, Perth, pp 509–521

    Google Scholar 

  • Kohn AJ, Nybakken JW (1975) Ecology of Conus on eastern Indian Ocean fringing reefs: diversity of species and resource utilization. Mar Biol 29:211–234

    Article  Google Scholar 

  • Kohn AJ, Orians GH (1962) Ecological data and the classification of closely related species. Syst Zool 11:119–127

    Article  Google Scholar 

  • Leviten PJ (1980) The foraging strategy of vermivorous conid gastropods. Ecol Monogr 46:157–178

    Article  Google Scholar 

  • Lewis RJ, Nielsen KJ, Craik DJ, Loughnan ML, Adams DA, Sharpe IA, Luchian T, Adams DJ, Bond T, Thomas L, Jones A, Matheson JL, Drinkwater R, Andrews PR, Alewood PF (2000) Novel omega-conotoxins from Conus catus discriminate among neuronal calcium channel subtypes. J Biol Chem 275:35335–35344

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Conery JS (2003) The evolutionary demongraphy of duplicate genes. J Struct Funct Genomics 3(1):35–44

    Article  PubMed  CAS  Google Scholar 

  • Lynch VJ (2007) Inventing an arsenal: adaptive evolution and neofunctionalization of snake venom phospholipase A2 genes. BMC Evol Biol 7:2

    Article  PubMed  CAS  Google Scholar 

  • Marsh H (1971) Observations on the food and feeding of some vermivorous Conus on the Great Barrier Reef. Veliger 14(1):45–53

    Google Scholar 

  • Olivera BM, Walker C, Cartier GE, Hooper Dm Santos AD, Schoenfeld R, Shetty Rm Watkins M, Bandyopadhyay P, Hillyard DR (1999) Speciation of cone snails and interspecific hyperdivergence of their venom peptides. Ann NY Acad Sci 870:223–237

    Article  PubMed  CAS  Google Scholar 

  • Reichelt RE, Kohn AJ (1985) Feeding and distribution of predatory gastropods on some Great Barrier Reef platforms. Proc Fifth Int Coral Reef Congr 5:191–196

    Google Scholar 

  • Rodriquez MA, Vermaak D, Bayes JJ, Malik HS (2007) Species-specific positive selection of the male-specific lethal complex that participates in dosage compensation in Drosophila. Proc Natl Acad Sci USA 104:15412–15417

    Article  Google Scholar 

  • Steinke D, Salzburger W, Braasch I, Meyer A (2006) Many genes in fish have species-specific asymmetric rates of molecular evolution. BioMed Central Genomics 7:20

    PubMed  Google Scholar 

  • Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556

    PubMed  CAS  Google Scholar 

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Acknowledgments

I thank H. A. Lessios, E. A. Remigio, M. B. Bolin, and several anonymous reviewers for comments on previous versions of the manuscript. This work was supported by funds from the Department of Ecology and Evolutionary Biology of the University of Michigan and the University of Michigan Museum of Zoology and the National Science Foundation (IOS 0718370). This project was initiated in H. A. Lessios’ laboratory at the Smithsonian Tropical Research Institute while T.F.D. was a Tupper Fellow.

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  1. University of Michigan Museum of Zoology, 1109 Geddes Avenue, Ann Arbor, MI, 48109, USA

    Thomas F. Duda Jr.

  2. Smithsonian Tropical Research Institute, Apartado 0843-03092, Balboa, Ancón, Republic of Panama

    Thomas F. Duda Jr.

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  1. Thomas F. Duda Jr.
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Correspondence to Thomas F. Duda Jr..

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Duda, T.F. Differentiation of Venoms of Predatory Marine Gastropods: Divergence of Orthologous Toxin Genes of Closely Related Conus Species with Different Dietary Specializations. J Mol Evol 67, 315–321 (2008). https://doi.org/10.1007/s00239-008-9155-8

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  • DOI: https://doi.org/10.1007/s00239-008-9155-8

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