Abstract
The ability to identify and accurately measure traits at the phenotypic interface of potential coevolutionary interactions is critical in documenting reciprocal evolutionary change between species. We quantify the defensive chemical trait of a prey species, the newt Taricha granulosa, thought to be part of a coevolutionary arms race. Variation in newt toxicity among populations results from variation in levels of the neurotoxin tetrodotoxin (TTX). Individual variation in TTX levels occurs within populations. Although TTX exists as a family of stereoisomers, only two of these (TTX and 6-epi-TTX) are likely to be sufficiently toxic and abundant to play a role in the defensive ecology of the newt.
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REFERENCES
Becker, W. A. 1992. Manual of Quantitative Genetics, 5th ed. Academic Enterprises, Pullman, Washington.
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.
Berenbaum, M. R., and Zangerl, A. R. 1998. Chemical phenotype matching between a plant and its insect herbivore. Proc. Natl. Acad. Sci. U.S.A. 95:13743-13748.
Bernays, E. A., and Chapman, R. F. 1994. Host-Plant Selection by Phytophagous Insects. Chapman Hall, New York.
Brandon, R. A., and Huheey, J. E. 1981. Toxicity in the plethodontid salamanders Pseudotriton ruber and Pseudotriton montanus (Amphibia, Caudata). Toxicon 19:25-31.
Brandon, R. A., and Huheey, J. E. 1985. Salamander skin toxins, with special reference to Necturus lewisi. Brimleyana 10:75-82.
Brodie, E. D., Jr. 1968. Investigations on the skin toxin of the adult rough-skinned newt, Taricha granulosa. Copeia 1968:307-313.
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.
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.
Brodie, E. D., III, and Brodie, E. D., Jr. 1991. Evolutionary response of predators to dangerous prey: Reduction of toxicity of newts and resistance of garter snakes in island populations. Evolution 45:221-224.
Brodie, E. D., III, and Brodie, E. D., Jr. 1999. Predator-prey arms races. Bioscience 49:357-368.
Daly, J. W., Highet, R. J., and Meyers, C. W. 1984. Occurrence of skin alkaloids in non-dendrobatid frogs from Brazil (Bufonidae), Australia (Myobatrachidae), and Madagascar (Mantellinae). Toxicon 25:279-285.
Daly, J. W., Meyers, C. W., and Whittaker, N. 1987. Further classification of skin alkaloids from neotropical poison frogs (Dendrobatidae), with a general survey of toxic, noxious substances in the Amphibia. Toxicon 25:1021-1095.
Daly, J. W., Meyers, C. W., Yotsu-Yamashita, M., and Yasumoto, T. 1994. First occurrence of tetrodotoxin in a dendrobatid frog (Colostethus inguinalis), with further reports for the bufonid genus Atelopus. Toxicon 32:279-285.
Daly, J. W., Padgett, W. L., Saunders, R. L., and Cover, J. F., Jr. 1997. Absence of tetrodotoxin in a captive-raised riparian frog, Atelopus varius. Toxicon. 35:705-709.
Fuhrman, F. A., 1986. Tetrodotoxin, tarichatoxin, and chiriquitoxin: Historical perspectives. Ann. N.Y. Acad. Sci. 479:1-14.
Futuyma, D. J., and Slatkin, M. 1983. Coevolution. Sinauer, Sunderland, Massachusetts.
Groves, J. D. 1980. Mass predation on a population of the American toad Bufo americanus. Am. Mid. Nat. 103:202-203.
Janzen, D. H. 1980. When is it coevolution? Evolution 34:611-612.
Kao, C. Y., and Walker, S. E. 1982. Active groups of saxitoxin and tetrodotoxin as deduced from actions of saxitoxin analogues in frog muscle and squid axon. J. Physiol. (London) 323:619-637.
Kao, C. Y., and Yasumoto, T. 1985. Actions of 4-epitetrodotoxin and anhydrotetrodotoxin on the squid axon. Toxicon 23:729-735.
Kotaki, Y., and Shimizu, Y. 1993. 1-Hydroxy-5,11-dideoxytetrodotoxin, the first N-hydroxy and ring-deoxy derivative of tetrodotoxin found in the newt Taricha granulosa. J. Am. Chem. Soc. 115:827-830.
Martin, J. S., and Martin, M. M. 1982. Tannin assays in ecological studies: Lack of correlation between phenolics, proanthocyanidines, and protein-precipitating constituents in mature foliage of six oak species. Oecologia 61:342-345.
Matsumura, K. 1995. Reexamination of tetrodotoxin production by bacteria. Appl. Environ. Microbiol. 61:3468-3470.
Mebs, D., Yotsu-Yamashita, M., Yasumoto, T., Lotters, S., and Schluter, A. 1995. Further report of the occurrence of tetrodotoxin in Atelopus species (Family: Bufonidae). Toxicon 33:246-249.
Mosher, H. S., Fuhrman, F. A., Buchwald, H. D., and Fischer, H. G. 1964. Tarichatoxin-tetrodotoxin: A potent neurotoxin. Science 144:1100-1110.
Nakamura, M., and Yasumoto, T. 1985. Tetrodotoxin derivatives in puffer fish. Toxicon 23:271-276.
Rosenthal, G. A., and Berenbaum, M. R. (eds.). 1991. Herbivores, Their Interactions with Secondary Plant Metabolites, 2nd ed. Academic Press, San Diego.
Shimizu, Y., and Kobayashi, M. 1983. Apparent lack of tetrodotoxin biosynthesis in captured Taricha torosa and Taricha granulosa. Chem. Pharm. Bull. 31:3625-3631.
Spencer, K. C. 1988. Introduction: chemistry and coevolution, pp. 1-11, in K. C. Spencer (ed.). Chemical Mediation of Coevolution. Academic Press, San Diego.
Thompson, J. N. 1994. The Coevolutionary Process. University of Chicago Press, Chicago.
Vermeij, G. J. 1994. The evolutionary interaction among species: Selection, escalation, and coevolution. Annu. Rev. Ecol. Syst. 25:219-236.
Wakely, J. F., Fuhrman, G. J., Fuhrman, F. A., Fischer, H. G., and Mosher, H. S. 1966. The occurrence of tetrodotoxin (tarichatoxin) in Amphibia and the distribution of the toxin in the organs of newts (Taricha). Toxicon 3:195-203.
Wu, B. Q., Yang, L., Kao, C. Y., Levinson, S. R., Yotsu-Yamashita, M., and Yasumoto, T. 1996. 11-oxo-tetrodotoxin and a specifically labeled 3H-tetrodotoxin. Toxicon. 34:407-416.
Yang, L., Kao, C. Y., and Yasumoto, T. 1992. Actions of 6-epitetrodotoxin and 11-deoxytetrodotoxin on the frog skeletal muscle fiber. Toxicon 30:635-643.
Yasumoto, T., and Michishita, T. 1985. Fluorometric determination of tetrodotoxin by High Performance Liquid Chromatography. Agric. Biol. Chem. 49:3077-3080.
Yasumoto, T., and Yotsu-Yamashita, M. 1996. Chemical and etiological studies on tetrodotoxin and its analogs. J. Toxicol. Toxin Rev. 15:81-90.
Yasumoto, T., Yotsu, M., Murata, M., and Naoki, H. 1988. New tetrodotoxin analogs from the newt Cynops ensicauda. J. Am. Chem. Soc. 110:2344-2345.
Yosef, R., and Whitman, D. W. 1992. Predator exaptations and defensive adaptations in evolutionary balance: No defense is perfect. Evol. Ecol. 6:527-536.
Yotsu, M., Yamazaki, T., Meguro, Y., Endo, A., Murata, M., Naoki, H., and Yasumoto, T. 1987. Production of tetrodotoxin and its derivatives by Pseudomonas sp. isolated from the skin of a pufferfish. Toxicon 25:225-228.
Yotsu, M., Endo, A., and Yasumoto, T. 1989. An improved tetrodotoxin analyser. Agric. Biol. Chem. 53:893-895.
Yotsu, M., Endo, A., and Yasumoto, T. 1990. Distribution of tetrodotoxin, 6-epitetrodotoxin, and 11-deoxytetrodotoxin in newts. Toxicon 28:238-241.
Yotsu-Yamashita, M., Mebs, D., and Yasumoto, T. 1992. Tetrodotoxin and its analogues in extracts from the toad Atelopus oxyhyns (Family: Bufonidae). Toxicon 30:1489-1492.
Zar, J. H. 1984. Biostatistical Analysis, 2nd ed. Prentice Hall, Englewood Cliffs, New Jersey.
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Hanifin, C.T., Yotsu-Yamashita, M., Yasumoto, T. et al. Toxicity of Dangerous Prey: Variation of Tetrodotoxin Levels Within and Among Populations of the Newt Taricha granulosa . J Chem Ecol 25, 2161–2175 (1999). https://doi.org/10.1023/A:1021049125805
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DOI: https://doi.org/10.1023/A:1021049125805