Abstract
Evolution typically arrives at convergent phenotypic solutions to common challenges of natural selection. However, diverse molecular and physiological mechanisms may generate phenotypes that appear similar at the organismal level. How predictable are the molecular mechanisms of adaptation that underlie adaptive convergence? Interactions between toxic prey and their predators provide an excellent avenue to investigate the question of predictability because both taxa must adapt to the presence of defensive poisons. The evolution of resistance to tetrodotoxin (TTX), which binds to and blocks voltage-gated sodium channels (NaV1) in nerves and muscle, has been remarkably parallel across deep phylogenetic divides. In both predators and prey, representing three major vertebrate groups, TTX resistance has arisen through structural changes in NaV1 proteins. Fish, amphibians and reptiles, though they differ in the total number of NaV1 paralogs in their genomes, have each evolved common amino acid substitutions in the orthologous skeletal muscle NaV1.4. Many of these substitutions involve not only the same positions in the protein, but also the identical amino acid residues. Similarly, predictable convergence is observed across the family of sodium channel genes expressed in different tissues in puffer fish and in garter snakes. Trade-offs between the fundamental role of NaV1 proteins in selective permeability of Na+ and their ability to resist binding by TTX generate a highly constrained adaptive landscape at the level of the protein.
References
1.
Arendt J, Reznick D (2008): Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol Evol 23:26-32.
2.
Arnegard ME, Zwickl DJ, Lu Y, Zakon HH (2010): Old gene duplication facilitates origin and diversification of an innovative communication system - twice. Proc Natl Acad Sci USA 107:22172-22177.
3.
Brodie ED III, Brodie ED 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.
4.
Brodie ED III, Feldman C, Hanifin C, Motychak J, Mulcahy D, Williams B, Brodie ED Jr (2005): Parallel arms races between garter snakes and newts involving tetrodotoxin as the phenotypic interface of coevolution. J Chem Ecol 31:343-356.
5.
Brodie ED Jr (1968): Investigations on the skin toxin of the adult rough-skinned newt, Taricha granulosa. Copeia 1968:307-313.
6.
Brodie ED Jr, Ducey PK, Baness EA (1991): Antipredator skin secretions of some tropical salamanders (Bolitoglossa) are toxic to snake predators. Biotropica 23:58-62.
7.
Brodie ED Jr, Ridenhour BJ, Brodie ED 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.
8.
Catterall WA, Cestèle S, Yarov-Yarovoy V, Yu FH, Konoki K, Scheuer T (2007): Voltage-gated ion channels and gating modifier toxins. Toxicon 49:124-141.
9.
Catterall WA, Goldin A, Waxman S (2005): International Union of Pharmacology. XLVII. Nomenclature and structure-function relationships of voltage-gated sodium channels. Pharmacol Rev 57:397-409.
10.
Christin P-A, Weinreich DM, Besnard G (2010): Causes and evolutionary significance of genetic convergence. Trends Genet 26:400-405.
11.
Conte GL, Arnegard ME, Peichel CL, Schluter D (2012): The probability of genetic parallelism and convergence in natural populations. Proc Biol Sci 279:5039-5047.
12.
DePristo MA, Weinreich DM, Hartl D (2005): Missense meanderings in sequence space: a biophysical view of protein evolution. Nat Rev Genet 6:678-687.
13.
Dobler S, Dalla S, Wagschal V, Agrawal AA (2012): Community-wide convergent evolution in insect adaptation to toxic cardenolides by substitutions in the Na, K-ATPase. Proc Natl Acad Sci USA 109:13040-13045.
14.
Dong K (2007): Insect sodium channels and insecticide resistance. Invert Neurosci 7:17-30.
15.
Feldman CR, Brodie ED Jr, Brodie ED III, Pfrender ME (2012): Constraint shapes convergence in tetrodotoxin-resistant sodium channels of snakes. Proc Natl Acad Sci USA 109:4556-4561.
16.
Fozzard HA, Lipkind GM (2010): The tetrodotoxin binding site is within the outer vestibule of the sodium channel. Mar Drugs 8:219-234.
17.
Geffeney S, Brodie ED Jr, Ruben P, Brodie ED III (2002): Mechanisms of adaptation in a predator-prey arms race: TTX-resistant sodium channels. Science 297:1336-1339.
18.
Geffeney S, Fujimoto E, Brodie ED III, Brodie ED Jr, Ruben P (2005): Evolutionary diversification of TTX-resistant sodium channels in a predator-prey interaction. Nature 434:759-763.
19.
Goldin A (2001): Resurgence of sodium channel research. Annu Rev Physiol 63:871-894.
20.
Goldin A (2002): Evolution of voltage-gated Na+ channels. J Exp Biol 205:575-584.
21.
Hanifin CT (2010): The chemical and evolutionary ecology of tetrodotoxin (TTX) toxicity in terrestrial vertebrates. Mar Drugs 8:577-593.
22.
Hanifin CT, Brodie ED Jr, Brodie ED III (2008): Phenotypic mismatches reveal escape from arms-race coevolution. PLoS Biol 6:471-482.
23.
Hanifin CT, Gilly WF (2015): Evolutionary history of a complex adaptation: tetrodotoxin resistance in salamanders. Evolution 69:232-244.
24.
Hille B (2001): Ion Channels of Excitable Membranes, ed 3. Sunderland, Sinauer.
25.
Huey RB, Moody WJ (2002): Neuroscience and evolution. Snake sodium channels resist TTX arrest. Science 297:1289-1290.
26.
Joron M, Papa R, Beltran M, Chamberlain N, Mavarez J, Baxter S, Abanto M, Bermingham E, Humphray SJ, Rogers J, Beasley H, Barlow K, Ffrench-Constant RH, Mallet J, McMillan WO, Jiggins CD (2006): A conserved supergene locus controls colour pattern diversity in Heliconius butterflies. PLoS Biol 4:e303.
27.
Jost MC, Hillis DM, Lu Y, Kyle JW, Fozzard HA, Zakon HH (2008): Toxin-resistant sodium channels: parallel adaptive evolution across a complete gene family. Mol Biol Evol 25:1016-1024.
28.
Liu Z, Song W, Dong K (2004): Persistent tetrodotoxin-sensitive sodium current resulting from U-to-C RNA editing of an insect sodium channel. Proc Natl Acad Sci USA 101:11862-11867.
29.
Llewellyn LE (1997): Haemolymph protein in xanthid crabs: its selective binding of saxitoxin and possible role in toxin bioaccumulation. Mar Biol 128:599-606.
30.
Lopreato G, Lu Y, Southwell A, Atkinson N, Hillis D, Wilcox T, Zakon H (2001): Evolution and divergence of sodium channel genes in vertebrates. Proc Natl Acad Sci USA 98:7588-7592.
31.
Losos JB (1992): The evolution of convergent structure in Caribbean Anolis communities. Syst Biol 41:403-420.
32.
Manceau M, Domingues VS, Linnen CR, Rosenblum EB, Hoekstra HE (2010): Convergence in pigmentation at multiple levels: mutations, genes and function. Philos Trans R Soc Lond B Biol Sci 365:2439-2450.
33.
Matsui T, Yamamori K, Furukawa K, Kono M (2000): Purification and some properties of a tetrodotoxin binding protein from the blood plasma of kusafugu, Takifugu niphobles. Toxicon 38:463-468.
34.
McGlothlin JW, Chuckalovcak JP, Janes DE, Edwards SV, Feldman CR, Brodie ED Jr, Pfrender ME, Brodie ED III (2014): Parallel evolution of tetrodotoxin resistance in three voltage-gated sodium channel genes in the garter snake Thamnophis sirtalis. Mol Biol Evol 31:2836-2846.
35.
Mohammadi S, McCoy KA, Hutchinson DA, Gauthier DT, Savitzky AH (2013): Independently evolved toad-eating snakes exhibit sexually dimorphic enlargement of adrenal glands. J Zool 290:237-245.
36.
Moody WJ, Huey RB (2002): Snake sodium channels resist TTX arrest. Science 297:1289-1290.
37.
Nagashima Y, Yamamoto K, Shimakura K, Shiomi K (2002): A tetrodotoxin-binding protein in the hemolymph of shore crab Hemigrapsus sanguineus: purification and properties. Toxicon 40:753-760.
38.
Narahashi T (2008): Tetrodotoxin: a brief history. Proc Jpn Acad Ser B Phys Biol Sci 84:147-154.
39.
Payandeh J, Scheuer T, Zheng N, Catterall WA (2011): The crystal structure of a voltage-gated sodium channel. Nature 475:353-358.
40.
Penzotti JL, Fozzard HA, Lipkind GM, Dudley SC Jr (1998): Differences in saxitoxin and tetrodotoxin binding revealed by mutagenesis of the Na+ channel outer vestibule. Biophys J 75:2647-2657.
41.
Rosenblum EB, Rompler H, Schoneberg T, Hoekstra HE (2010): Molecular and functional basis of phenotypic convergence in white lizards at White Sands. Proc Natl Acad Sci USA 107:2113-2117.
42.
Smith HM, White FN (1955): Adrenal enlargement and its significance in the hognose snakes (Heterodon). Herpetologica 11:137-144.
43.
Stern DL, Orgogozo V (2008): The loci of evolution: how predictable is genetic evolution? Evolution 62:2155-2177.
44.
Stern DL, Orgogozo V (2009): Is genetic evolution predictable? Science 323:746-751.
45.
Stokes AN, Ray AN, Buktenica MW, Gall BG, Paulson E, Paulson D, French SS, Brodie ED III, Brodie ED Jr (2015): Otter predation on Taricha granulosa and variation in tetrodotoxin levels with elevation. Northwestern Naturalist 96:13-21.
46.
Terlau H, Heinemann SH, Stühmer W, Pusch M, Conti F, Imoto K, Numa S (1991): Mapping the site of block by tetrodotoxin and saxitoxin of sodium channel II. FEBS Lett 293:93-96.
47.
Tikhonov DB, Zhorov BS (2011): Possible roles of exceptionally conserved residues around the selectivity filters of sodium and calcium channels. J Biol Chem 286:2998-3006.
48.
Tikhonov DB, Zhorov BS (2012): Architecture and pore block of eukaryotic voltage-gated sodium channels in view of NavAb bacterial sodium channel structure. Mol Pharmacol 82:97-104.
49.
Ujvari B, Mun H-C, Conigrave AD, Bray A, Osterkamp J, Halling P, Madsen T (2012): Isolation breeds naivety: island living robs Australian varanid lizards of toad-toxin immunity via four-base-pair mutation. Evolution 67:289-294.
50.
Vornanen M, Hassinen M, Haverin J (2011): Tetrodotoxin sensitivity of vertebrate cardiac Na+ current. Mar Drugs 9:2409-2422.
51.
Weinreich D, Delaney N, DePristo M, Hartl D (2006): Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312:111-114.
52.
Zakon HH (2002): Convergent evolution on the molecular level. Brain Behav Evol 59:250-261.
53.
Zakon HH (2012): Adaptive evolution of voltage-gated sodium channels: the first 800 million years. Proc Natl Acad Sci USA 109:10619-10625.
54.
Zakon HH, Jost MC, Lu Y (2011): Expansion of voltage-dependent Na+ channel gene family in early tetrapods coincided with the emergence of terrestriality and increased brain complexity. Mol Biol Evol 28:1415-1424.
55.
Zakon HH, Jost MC, Zwickl DJ, Lu Y, Hillis DM (2009): Molecular evolution of Na+ channels in teleost fishes. Integr Zool 4:64-74.
56.
Zhang P, Papenfuss TJ, Wake MH, Qu L, Wake DB (2008): Phylogeny and biogeography of the family Salamandridae (Amphibia: Caudata) inferred from complete mitochondrial genomes. Mol Phylogenet Evol 49:586-597.
57.
Zimmer T (2010): Effects of tetrodotoxin on the mammalian cardiovascular system. Mar Drugs 8:741-762.
© 2015 S. Karger AG, Basel
2015
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.
