Journal of Chemical Ecology

, Volume 31, Issue 2, pp 343–356 | Cite as

Parallel Arms Races between Garter Snakes and Newts Involving Tetrodotoxin as the Phenotypic Interface of Coevolution

  • Edmund D. BrodieIII
  • Chris R. Feldman
  • Charles T. Hanifin
  • Jeffrey E. Motychak
  • Daniel G. Mulcahy
  • Becky L. Williams
  • Edmund D. BrodieJr.
Article

Abstract

Parallel “arms races” involving the same or similar phenotypic interfaces allow inference about selective forces driving coevolution, as well as the importance of phylogenetic and phenotypic constraints in coevolution. Here, we report the existence of apparent parallel arms races between species pairs of garter snakes and their toxic newt prey that indicate independent evolutionary origins of a key phenotype in the interface. In at least one area of sympatry, the aquatic garter snake, Thamnophis couchii, has evolved elevated resistance to the neurotoxin tetrodotoxin (TTX), present in the newt Taricha torosa. Previous studies have shown that a distantly related garter snake, Thamnophis sirtalis, has coevolved with another newt species that possesses TTX, Taricha granulosa. Patterns of within population variation and phenotypic tradeoffs between TTX resistance and sprint speed suggest that the mechanism of resistance is similar in both species of snake, yet phylogenetic evidence indicates the independent origins of elevated resistance to TTX.

Keywords

Coevolution parallel evolution resistance Taricha tetrodotoxin TTX Thamnophis toxicity 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Berenbaum, M. R. and Zangerl, A. R. 1992. Quantification of chemical coevolution, pp. 69–87, in R. S. Fritz and E. L. Simms (eds.). Plant Resistance to Herbivores and Pathogens: Ecology, Evolution, and Genetics. University of Chicago Press, Chicago.Google Scholar
  2. Brodie, E. D., Jr. 1968. Investigations on the skin toxin of the adult roughskinned newt, Taricha granulosa. Copeia 1968:307–313.Google Scholar
  3. Brodie, E. D., III and Brodie, E. D. Jr. 1990. Tetrodotoxin resistance in garter snakes: An evolutionary response of predators to dangerous prey. Evolution 44:651–659.Google Scholar
  4. Brodie, E. D., III and Brodie, E. D. Jr. 1999a. The cost of exploiting poisonous prey: Tradeoffs in a predator–prey arms race. Evolution 53:626–631.Google Scholar
  5. Brodie, E. D., III and Brodie, E. D. Jr. 1999b. Predator–prey arms races. Bioscience 49:557–568.Google Scholar
  6. Brodie, E. D., III and Ridenhour, B. J. 2003. Reciprocal selection at the phenotypic interface of coevolution. Integr. Comp. Biol. 43:408–418.Google Scholar
  7. Brodie, E. D., Jr., Hensel, J. L., Jr., and Johnson, J. A. 1974. Toxicity of the urodele amphibians Taricha, Notophthalmus, Cynops and Paramesotriton (Salamandridae). Copeia 1974:506– 511.Google Scholar
  8. Brodie, E. D., Jr., Ridenhour, B. J., and Brodie, E. D., III. 2002. The evolutionary response of predators to dangerous prey: Hotspots and coldspots in the geographic mosaic of coevolution between newts and snakes. Evolution 56:2067–2082.Google Scholar
  9. Brown, M. S. and Mosher, H. S. 1963. Tarichatoxin: Isolation and purification. Science 140:295–296.Google Scholar
  10. Cardall, B. L., Brodie, E. D., III, Brodie, E. D., Jr., and Hanifin, C. T. 2004. Secretion and regeneration of tetrodotoxin in the rough-skin newt (Taricha granulosa). Toxicon, 44:933-938.Google Scholar
  11. De Queiroz, A., Lawson, R., and Lemos-Espinal, J. A. 2002. Phylogenetics relationships of North American garter snakes (Thamnophis) based on four mitochondrial genes: How much DNA sequence is enough? Mol. Phylogenet. Evol. 22:315–329.Google Scholar
  12. Denholm, I., Pickett, J. A., and Devonshire, A. L. 1999. Insecticide Resistance from Mechanisms to Management. CABI Publishing, New York, 123 pp.Google Scholar
  13. ffrench-Constant, R. H., Anthony, N., Aronstein, K., Rocheleau, T., and Stilwell, G. 2000. Cyclodiene insecticide resistance: From molecular to population genetics. Annu. Rev. Entomol. 48:449–466.Google Scholar
  14. Geffeney, S., Ruben, P. C., Brodie, E. D., Jr., and Brodie, E. D., III. 2002. Mechanisms of adaptation in a predator–prey arms race: TTX resistant sodium channels. Science 297:1336-1339.Google Scholar
  15. Hanifin, C. T., Yotsu-Yamashita, M., Yasumoto, T., Brodie, E. D., III, and Brodie, E. D., Jr. 1999. Toxicity of dangerous prey: Variation of tetrodotoxin levels within and among populations of the newt Taricha granulosa. J. Chem. Ecol. 25:2161–2175.Google Scholar
  16. Hanifin, C. T., Brodie, E. D., III, and Brodie, E. D., Jr. 2002. Tetrodotoxin levels of the rough-skin newt, Taricha granulosa, increase in long-term captivity. Toxicon 40:1149–1153.Google Scholar
  17. Hanifin, C. T., Brodie, E. D., III, and Brodie, E. D., Jr. 2004. A predictive model to estimate total skin tetrodotoxin in the newt Taricha granulosa. Toxicon 43:243–249. (doi:10.1016/j.toxicon. 2003.11.025).Google Scholar
  18. Hille, B. 1992. Ionic Channels of Excitable Membranes. Sinauer, Sunderland, MA.Google Scholar
  19. JMP v 5.01, 5.01. 1989–2002. SAS Institute, Cary, NC.Google Scholar
  20. Kao, C. Y. and Fuhrman, F. A. 1967. Differentiation of the actions of tetrodotoxin and saxitoxin. Toxicon 5:24–34.Google Scholar
  21. Kidokoro, Y., Grinnell, A. D., and Eaton, D. C. 1974. Tetrodotoxin sensitivity of muscle action potentials in pufferfishes and related fishes. J. Comp. Phsyiol. 89:59–72.Google Scholar
  22. Lehman, E., Brodie, E. D., Jr., and Brodie, E. D., III. 2004. No evidence for an endosymbiotic bacterial origin of tetrodotoxin in the newt Taricha granulosa. Toxicon 44:243–249.Google Scholar
  23. Mallet, J. 1989. The evolution of insecticide resistance: Have the insects won? Trends Ecol. Evol. 4:336–339.Google Scholar
  24. McKenzie, J. A. and Batterham, P. 1994. The genetic, molecular and phenotypic consequences of selection for insecticide resistance. Trends Ecol. Evol. 9:166–169.Google Scholar
  25. Miyazawa, K. and Noguchi, T. 2001. Distribution and origin of tetrodotoxin. J. Toxicol. Toxin Rev. 20:11–33.Google Scholar
  26. Mosher, H. S., Fuhrman, F. A., Buchwald, H. D., and Fischer, H. G. 1964. Tarichatoxin–tetrodotoxin: A potent neurotoxin. Science 144:1100–1110.Google Scholar
  27. Motychak, J. E., Brodie, E. D., Jr., and Brodie, E. D., III. 1999. Evolutionary response of predators to dangerous prey: Preadaptation and the evolution of tetrodotoxin resistance in garter snakes. Evolution 53:1528–1535.Google Scholar
  28. Narahashi, T. 2001. Pharmacology of tetrodotoxin. J. Toxicol. Toxin Rev. 20:67–84.Google Scholar
  29. Ridenhour, B. J., Brodie, E. D., Jr., and Brodie, E. D., III. 2004. Neonate and field-collected garter snake (Thamnophis spp.) resistance to tetrodotoxin. J. Chem. Ecol. 30:143–154.Google Scholar
  30. Shimizu, Y. 2002. Biosynthesis of important marine toxins of microorganism origins, pp. 257–268, in E. J. Massaro (ed.). Handbook of Neurotoxicology. Humana Press, New Jersey.Google Scholar
  31. Tan, A. M. and Wake, D. B. 1995. MtDNA phylogeography of the California Newt, Taricha torosa (Caudata, Salamandridae). Mol. Phylogenet. Evol. 4:383–394.Google Scholar
  32. Williams, B. L., Brodie, E. D., Jr., and Brodie, E. D., III. 2001. Comparisons between toxic effects of tetrodotoxin administered orally and by intraperitoneal injection to the garter snake Thamnophis sirtalis. J. Herp. 36:112–115.Google Scholar
  33. Yasumoto, T. and Michishita, T. 1985. Flourometric determination of tetrodtoxin by high performance liquid chromatography. Agric. Biol. Chem. 49:3077–3080.Google Scholar
  34. Yasumoto, T., Yotsu, M., Murata, M., and Naoki, H. 1988. New tetrodotoxin analogues from the newt Cynops ensicauda. J. Am. Chem. Soc. 110:2344–2345.Google Scholar
  35. Yotsu, M., Endo, A., and Yasumoto, T. 1990. Distribution of tetrodotoxin, 6-epitetrodotoxin, and 11-deoxytetrodotoxin in newts. Toxicon 28:238–241.Google Scholar
  36. Yotsu-Yamashita, M. 2001. The levels of tetrodotoxin and its analogue 6-epitetrodotoxin in the red-spotted newt, Notophthalmus viridescens. Toxicon 38:1261–1263.Google Scholar
  37. Yotsu-Yamashita, M., Nishimori, K., Nitanai, Y., Isemura, M., Sugimoto, A., and Yasumoto, T. 2000. Binding properties of 3H-PbTx-3 and 3H-Saxitoxin to brain membranes and to skeletal muscle membranes of puffer fish Fugu pardalis and the primary structure of a voltage gated Na+ channel α-subunit (fMNa1) from skeletal muscle of F. pardalis. Biochem. Biophys. Res. Commun. 267:403–412.Google Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • Edmund D. BrodieIII
    • 1
  • Chris R. Feldman
    • 2
  • Charles T. Hanifin
    • 2
  • Jeffrey E. Motychak
    • 2
  • Daniel G. Mulcahy
    • 2
  • Becky L. Williams
    • 2
    • 3
  • Edmund D. BrodieJr.
    • 2
  1. 1.Department of BiologyIndiana UniversityBloomingtonUSA
  2. 2.Department of BiologyUtah State UniversityLoganUSA
  3. 3.Department of IntegrativeBiology University of CaliforniaUSA

Personalised recommendations