Isolation breeds naivety: Island living robs Australian varanid lizards of toad-toxin immunity via four-base-pair mutation

Evolution

Volumn 67, Issue 1, 2013, Pages 289-294

  Ujvari, Beata ^a   Mun, Hee Chang ^a   Conigrave, Arthur D ^a   Bray, Alessandra ^a   Osterkamp, Jens ^b   Halling, Petter ^b   Madsen, Thomas ^a,c,d  

^a UNIVERSITY OF SYDNEY   (Australia)

^b LUND UNIVERSITY   (Sweden)

^c DEPARTMENT OF ZOOLOGY   (Hungary)

^d UNIVERSITY OF WOLLONGONG   (Australia)

Author keywords

Cane toads; Coevolution; Sodium potassium ATPase enzyme; Toxic prey; Varanid lizards

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); BUFADIENOLIDE DERIVATIVE; BUFALIN; CARDIOTONIC AGENT;

AMINO ACID; COEVOLUTION; ENZYME ACTIVITY; IMMUNITY; LIZARD; MUTATION; PHENOTYPIC PLASTICITY; POTASSIUM; REPRODUCTIVE ISOLATION; ROBBING; SODIUM; TOAD; TOXIC ORGANISM; TOXIN;

AMINO ACID SUBSTITUTION; ANIMAL; ARTICLE; AUSTRALIA; BUFONIDAE; CELL STRAIN HEK293; CHEMISTRY; DRUG ANTAGONISM; ECOSYSTEM; GENETICS; HUMAN; ISLAND (GEOLOGICAL); LIZARD; MOLECULAR EVOLUTION; MUTATION; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SUBSTITUTION; ANIMALS; AUSTRALIA; BUFANOLIDES; BUFONIDAE; CARDIOTONIC AGENTS; ECOSYSTEM; EVOLUTION, MOLECULAR; HEK293 CELLS; HUMANS; ISLANDS; LIZARDS; MUTATION; PROTEIN STRUCTURE, TERTIARY; SODIUM-POTASSIUM-EXCHANGING ATPASE;

AMPHIBIA; ANURA; BUFO MARINUS; SQUAMATA; VARANIDAE;

EID: 84871945658     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2012.01751.x     Document Type: Article

References (44)

1. Aubret, F., G.M. Burghardt, S. Maumelat, X. Bonnet, and D. Bradshaw. 2006. Feeding preferences in 2 disjunct populations of tiger snakes, Notechis scutatus (Elapidae). Behav. Ecol. 17:716-725.
2. Baverstock, P. R., D. King, M. King, J. Birrell, and M. Krieg. 1993. The evolution of species of the Varanidae: Microcomplement fixation analysis of serum albumins. Aust. J. Zool. 41:621-638.
3. Blumstein D. T., and J. C. Daniel. 2005. The loss of anti-predator behaviour following isolation on islands. Proc. R. Soc. Lond. B 272:1663-1668.
4. Brodie, Jr., E. D., B. J. Ridenhour, and E. D. Brodie III. 2002. The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts. Evolution 56:2067-2082.
5. Calsbeek, R., W. Buerman, and T. B. Smith. 2009. Parallel shifts in ecology and natural selection in an island lizard. BMC Evol. Biol. 9:3. doi: 10.1186/1471-2148-9-3.
6. Clarke, B. T. 1997. The natural history of amphibian skin secretions, their normal functioning and potential medical applications. Biol. Rev. Camb. Philos. Soc. 72:365-379.
7. Cogger, H. G. 2000. Reptiles and amphibians of Australia. Reed Books, Melbourne, Australia.
8. Doody, J. S., B. Green, R. Sims, D. Rhind, P. West, and D. Steer 2006. Indirect impacts of invasive cane toads Bufo marinus on nest predation in pig-nosed turtles Carettochelys insulpta. Wildl. Res. 33:349-354.
9. Falconer, D. S., and T. F. C. Mackay. 1996. Introduction to quantitative genetics. Addison-Wesley Longman, Harlow, U.K.
10. Flannery, T. 1994. The future eaters: an ecological history of the Australasian lands and people. Reed New Holland, Sydney, Australia.
11. +-ATPase. Science 208:503-505.
12. Fuller, S., P. Baverstock, and D. King. 1998. Biogeographic origins of goannas Varanidae: a molecular perspective. Mol. Phylogenet. Evol. 9:294-307.
13. Geffeney, S.L., E. Fujimoto, E.D. Brodie III, E.D. Brodie, Jr., and P.C. Ruben. 2005. Evolutionary diversification of TTX-resistant sodium channels in a predator-prey interaction. Nature 434:759-763.
14. Grant, P. 1998. Evolution on islands. Oxford Univ. Press, Oxford, U.K.
15. Hasenfuss, G., and J. R. Teerlink. 2011. Cardiac inotropes: current agents and future directions. Eur. Heart J. 33:1838-1845.
16. Holzinger, F., C. Frick, and M. Wink. 1992. Molecular basis for the insensitivity of the Monarch Danaus plexippus to cardiac glycosides. FEBS Lett. 314:477-480.
17. Jaisser, F., C. M. Canessa, J. D. Horisberger, and B. C. Rossier. 1992. Primary sequence and functional expression of a novel ouabain-resistant Na, K-ATPase. J. Biol. Chem. 267:16895-16903.
18. Lande, R. 1983. The response to selection on major and minor mutations affecting a metrical trait. Heredity 50:47-66.
19. Lingrel, J. B. 2010. The physiological significance of the cardiotonic steroid/ouabain-binding site of the Na, K-ATPase. Annu. Rev. Physiol. 72:395-412.
20. Losos, J. B., and H. W. Greene. 1988. Ecological and evolutionary implications of diet in monitor lizards. Biol. J. Linn. Soc. 35:379-407.
21. Losos, J. B., and R. E. Ricklefs. 2009. Adaptation and diversification on islands. Nature 457: 830-836.
22. Low, T. 2001. Feral future. The untold story of Australia's exotic invaders. Penguin Books, Victoria, Australia.
23. +-ATPase inhibitors down-regulate gene expression of the intracellular signaling protein 14-3-3 in rat lens. J. Pharmacol. Exp. Ther. 289:1559-1563.
24. 2+-sensing receptor's Venus fly trap domain that selectively disables L-amino acid sensing. J. Biol. Chem. 280:29067-29072.
25. Pamnani, M. B., S. Chen, C. M. Yuan, and F.J. Haddy. 1994. Chronic blood pressure effects of bufalin, a sodium-potassium ATPase inhibitor, in rats. Hypertension 23(Suppl I):I106-I109.
26. Pettit, G., and Y. Kamano. 1972. The structure of the steroid toad venom constituent bufotoxin. J. Chem. Soc., Chem. Commun. 1972:45.
27. Phillips, B. L., G. P. Brown, and R. Shine. 2003. Assessing the potential impact of cane toads on Australian snakes. Conserv. Biol. 17:1738-1747.
28. Pianka, E. R. 1995. Evolution of body size: varanid lizards as a model system. Am. Nat. 146:398-414.
29. Pimm, S. L., M. P. Moulton, and L. J. Justice. 1994. Bird extinctions in the central Pacific. Philos. Trans. R. Soc. Lond. B 344:27-33.
30. Price, E. M., D. A. Rice, and J. B. Lingrel. 1990. Structure-function studies of Na, K-ATPase. J. Biol. Chem. 265:6638-6641.
31. Primack, R.B. 1995. A primer of conservation biology. Sinauer Associates, Sunderland, MA.
32. Rohrer, D. C., D. S. Fullerton, E. Kitatsuji, T. Nambara, and E. Yoshi. 1982. Bufalin. Acta Cryst. B38:1865-1868.
33. Shimada, K., and T. Nambara. 1980. Isolation and characterization of a new type of bufotoxin from the skin of Bufo americanus. Chem. Pharm. Bull. 28:1559-1562.
34. Shimada, K., K. Ohishi, and T. Nambara. 1984. Isolation and characterization of new bufotoxins from the skin of Bufo melanostictus. Chem. Pharm. Bull. 32:4396-4401.
35. +-adenosine triphosphatase. J. Pharmacobiodyn 8:1054-1059.
36. Shimada, K., J. S. Ro, K. Ohishi, and T. Nambara. 1985b. Isolation and characterization of cinobufagin 3-glutaroyl-L-arginine ester from Bufo bufo gargarizans. Chem. Pharm. Bull 33:2767-2771.
37. Storz, J. F., A. M. Runcka, S. J. Sabatinoa, J. K. Kellyb, N. Ferrand, H. Moriyamaa, R. E. Webere, and A. Fagoe. 2009. Evolutionary and functional insights into the mechanism underlying high-altitude adaptation of deer mouse hemoglobin. Proc. Natl. Acad. Sci. USA 106:14450-14455.
38. Sutter, N. B., C. D. Bustamante, K. Chase, M. M. Gray, K. Zhao, L. Zhu, B. Padhukasahasram, E. Karlins, S. Davis, P. G. Jones et al. 2007. A single IGF1 allele is a major determinant of small size in dogs. Science 316:112-115.
39. Tashmukhamedov, M. S., S. Y. Mirzaakhmedov, B. T. Ibragimov, F. G. Kamaev, K. M. Beketov, Z. A. Khushbaktova, and S. I. Salikhov. 1995. Arenobufagin and gamabufotalin from the venom of Central Asian green toad Bufo viridis. Introduction, structural-functional features. Chem. Nat. Comp. 31:214-220.
40. Thompson, J. N. 1999. The evolution of species interactions. Science 284:2116-2118.
41. Ujvari, B., and T. Madsen. 2009. Increased mortality of naïve varanid lizards after the invasion of non-native cane toads Bufo marinus. Herp. Conserv. Biol. 4:248-251.
42. Whittaker, R. J., and J. M. Fernández-Palacios. 2007. Island biogeography: ecology, evolution, and conservation. Oxford Univ. Press, Oxford, U.K.
43. Wiles, G. J., J. Bart, R. Beck, Jr., and C. F. Agoun. 2003. Impacts of the brown tree snakes: patterns of decline and species persistence in Guam's avifauna. Conserv. Biol. 17:1350-1360.
44. Zug G. R., and P. B. Zug. 1979. The marine toad, Bufo marinus: a natural history resumé of native populations. Smithsonian Contribut. Zool. 284:1-58.