1932

Abstract

Toxin evolution in animals is one of the most fascinating and complex subjects of scientific inquiry today. Gaining an understanding of toxins poses a multifaceted challenge given the diverse modes of acquisition, evolutionary adaptations, and abiotic components that affect toxin phenotypes. Here, we highlight some of the main genetic and ecological factors that influence toxin evolution and discuss the role of antagonistic interactions and coevolutionary dynamics in shaping the direction and extent of toxicity and resistance in animals. We focus on toxic Pacific newts (family Salamandridae, genus ) as a system to investigate and better evaluate the widely distributed toxin they possess, tetrodotoxin (TTX), and the hypothesized model of arms-race coevolution with snake predators that is used to explain phenotypic patterns of newt toxicity. Finally, we propose an alternative coevolutionary model that incorporates TTX-producing bacteria and draws from an elicitor–receptor concept to explain TTX evolution and ecology.

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2022-02-15
2024-04-22
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Literature Cited

  1. 1. 
    Mebs D. 2001. Toxicity in animals. Trends in evolution?. Toxicon 39:87–96
    [Google Scholar]
  2. 2. 
    Nelsen DR, Nisani Z, Cooper AM, Fox GA, Gren EC et al. 2014. Poisons, toxungens, and venoms: redefining and classifying toxic biological secretions and the organisms that employ them. Biol. Rev. 89:2450–65
    [Google Scholar]
  3. 3. 
    Shaari CM, Sanders I. 1993. Quantifying how location and dose of botulinum toxin injections affect muscle paralysis. Muscle Nerve 16:9964–69
    [Google Scholar]
  4. 4. 
    Malli H, Imboden H, Kuhn-Nentwig L. 1998. Quantifying the venom dose of the spider Cupiennius salei using monoclonal antibodies. Toxicon 36:121959–69
    [Google Scholar]
  5. 5. 
    Li M, Fry BG, Kini RM. 2005. Eggs-only diet: its implications for the toxin profile changes and ecology of the marbled sea snake (Aipysurus eydouxii). J. Mol. Evol. 60:181–89
    [Google Scholar]
  6. 6. 
    Casewell NR, Wagstaff SC, Wüster W, Cook DAN, Bolton FMS et al. 2014. Medically important differences in snake venom composition are dictated by distinct postgenomic mechanisms. PNAS 111:259205–10
    [Google Scholar]
  7. 7. 
    Moreau SJM, Asgari S. 2015. Venom proteins from parasitoid wasps and their biological functions. Toxins 7:72385–412
    [Google Scholar]
  8. 8. 
    Wong ES, Belov K. 2012. Venom evolution through gene duplications. Gene 496:11–7
    [Google Scholar]
  9. 9. 
    Chen N, Xu S, Zhang Y, Wang F. 2018. Animal protein toxins: origins and therapeutic applications. Biophys. Rep. 4:5233–42
    [Google Scholar]
  10. 10. 
    Stephens JS, Johnson RK Jr., Key GS, McCosker JE 1970. The comparative ecology of three sympatric species of California blennies of the genus Hypsoblennius Gill (Teleostomi, Blenniidae). Ecol. Monogr. 40:213–33
    [Google Scholar]
  11. 11. 
    Buchheim JR, Hixon MA. 1992. Competition for shelter holes in the coral-reef fish Acanthemblemaria spinosa Metzelaar. J. Exp. Mar. Biol. Ecol. 164:45–54
    [Google Scholar]
  12. 12. 
    Harris RJ, Jenner RA. 2019. Evolutionary ecology of fish venom: adaptations and consequences of evolving a venom system. Toxins 11:260
    [Google Scholar]
  13. 13. 
    Casewell NR, Visser JC, Baumann K, Dobson J, Han H et al. 2017. The evolution of fangs, venom, and mimicry systems in blenny fishes. Curr. Biol. 27:1184–91
    [Google Scholar]
  14. 14. 
    Morea SJM, Vinchon S, Cherqui A, Prévost G 2009. Components of Asobara venoms and their effects on hosts. Adv. Parasitol. 70:217–32
    [Google Scholar]
  15. 15. 
    Moreau SJM, Guillot S. 2005. Advances and prospects on biosynthesis, structures and functions of venom proteins from parasitic wasps. Insect Biochem. Mol. Biol. 35:1209–23
    [Google Scholar]
  16. 16. 
    LeBrun EG, Jones NT, Gilbert LE. 2014. Chemical warfare among invaders: A detoxification interaction facilitates an ant invasion. Science 343:61741014–17
    [Google Scholar]
  17. 17. 
    Barlow A, Pook CE, Harrison RA, Wüster W. 2009. Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution. Proc. R. Soc. B 276:16662443–49
    [Google Scholar]
  18. 18. 
    Richards DP, Barlow A, Wüster W. 2012. Venom lethality and diet: differential responses of natural prey and model organisms to the venom of the saw-scaled vipers (Echis). Toxicon 59:1110–16
    [Google Scholar]
  19. 19. 
    Starkov VG, Osipov AV, Utkin YN. 2007. Toxicity of venoms from vipers of Pelias group to crickets Gryllus assimilis and its relation to snake entomophagy. Toxicon 49:7995–1001
    [Google Scholar]
  20. 20. 
    Pucca MB, Amorim FG, Cerni FA, Bordon KDCF, Cardoso IA et al. 2014. Influence of post-starvation extraction time and prey-specific diet in Tityus serrulatus scorpion venom composition and hyaluronidase activity. Toxicon 90:326–36
    [Google Scholar]
  21. 21. 
    Remigio EA, Duda TF Jr 2008. Evolution of ecological specialization and venom of a predatory marine gastropod. Mol. Ecol. 17:41156–62
    [Google Scholar]
  22. 22. 
    Yoshida T, Ujiie R, Savitzky AH, Jono T, Inoue T et al. 2020. Dramatic dietary shift maintains sequestered toxins in chemically defended snakes. PNAS 117:115964–69
    [Google Scholar]
  23. 23. 
    Santos JC, Coloma LA, Cannatella DC. 2003. Multiple, recurring origins of aposematism and diet specialization in poison frogs. PNAS 100:12792–97
    [Google Scholar]
  24. 24. 
    Tarvin RD, Santos JC, O'Connell LA, Zakon HH, Cannatella DC 2016. Convergent substitutions in a sodium channel suggest multiple origins of toxin resistance in poison frogs. Mol. Biol. Evol. 33:1068–81
    [Google Scholar]
  25. 25. 
    Underwood AH, Seymour JE. 2007. Venom ontogeny, diet and morphology in Carukia barnesi, a species of Australian box jellyfish that causes Irukandji syndrome. Toxicon 49:81073–82
    [Google Scholar]
  26. 26. 
    Zelanis A, Travaglia-Cardoso SR, De Fátima Domingues Furtado M. 2008. Ontogenetic changes in the venom of Bothrops insularis (Serpentes: Viperidae)and its biological implication. S. Am. J. Herpetol. 3:143–50
    [Google Scholar]
  27. 27. 
    Modahl CM, Mukherjee AK, Mackessy SP. 2016. An analysis of venom ontogeny and prey-specific toxicity in the monocled cobra (Naja kaouthia). Toxicon 119:8–20
    [Google Scholar]
  28. 28. 
    Mackessy SP. 1988. Venom ontogeny in the Pacific rattlesnakes Crotalus viridis helleri and C. v. oreganus. Copeia 1988:192–101
    [Google Scholar]
  29. 29. 
    Mackessy SP. 1993. Fibrinogenolytic proteases from the venoms of juvenile and adult northern Pacific rattlesnakes (Crotalus viridis oreganus). Comp. Biochem. Physiol. B 106:1181–89
    [Google Scholar]
  30. 30. 
    Gibbs HL, Mackessy SP. 2009. Functional basis of a molecular adaptation: prey-specific toxic effects of venom from Sistrurus rattlesnakes. Toxicon 53:6672–79
    [Google Scholar]
  31. 31. 
    Daltry JC, Wüster W, Thorpe RS. 1996. Diet and snake venom evolution. Nature 379:6565537–40
    [Google Scholar]
  32. 32. 
    Creer S, Malhotra A, Thorpe RS, Stöcklin RS, Favreau PS, Chou WSH. 2003. Genetic and ecological correlates of intraspecific variation in pitviper venom composition detected using matrix-assisted laser desorption time-of-flight mass spectrometry (MALDI-TOF-MS) and isoelectric focusing. J. Mol. Evol. 56:3317–29
    [Google Scholar]
  33. 33. 
    Mackessy SP, Williams K, Ashton KG 2003. Ontogenetic variation in venom composition and diet of Crotalus oreganus concolor: A case of venom paedomorphosis?. Copeia 2003 4769–82
    [Google Scholar]
  34. 34. 
    Strickland JL, Smith CF, Mason AJ, Schield DR, Borja M et al. 2018. Evidence for divergent patterns of local selection driving venom variation in Mojave rattlesnakes (Crotalus scutulatus). Sci. Rep. 8:17622
    [Google Scholar]
  35. 35. 
    Pasteels JM, Grégoire JC, Rowell-Rahier M. 1983. The chemical ecology of defense in arthropods. Annu. Rev. Entomol. 28:263–89
    [Google Scholar]
  36. 36. 
    Speed MP, Ruxton GD, Mappes J, Sherratt TN. 2012. Why are defensive toxins so variable? An evolutionary perspective. Biol. Rev. 87:4874–84
    [Google Scholar]
  37. 37. 
    Bókony V, Móricz ÁM, Tóth Z, Gál Z, Kurali A et al. 2016. Variation in chemical defense among natural populations of common toad, Bufo bufo, tadpoles: the role of environmental factors. J. Chem. Ecol. 42:4329–38
    [Google Scholar]
  38. 38. 
    Dumbacher JP, Wako A, Derrickson SR, Samuelson A, Spande TF, Daly JW. 2004. Melyrid beetles (Choresine): a putative source for the batrachotoxin alkaloids found in poison-dart frogs and toxic passerine birds. PNAS 101:4515857–60
    [Google Scholar]
  39. 39. 
    Bartram S, Boland W. 2001. Chemistry and ecology of toxic birds. ChemBioChem 2:11809–11
    [Google Scholar]
  40. 40. 
    Dumbacher JP, Menon GK, Daly JW. 2009. Skin as a toxin storage organ in the endemic New Guinean genus Pitohui. Auk 126:3520–30
    [Google Scholar]
  41. 41. 
    Dumbacher JP, Spande TF, Daly JW. 2000. Batrachotoxin alkaloids from passerine birds: a second toxic bird genus (Ifrita kowaldi) from New Guinea. PNAS 97:2412970–75
    [Google Scholar]
  42. 42. 
    Dutertre S, Jin AH, Vetter I, Hamilton B, Sunagar K et al. 2014. Evolution of separate predation- and defence-evoked venoms in carnivorous cone snails. Nat. Commun. 5:3521
    [Google Scholar]
  43. 43. 
    Heatwole H, Poran NS. 1995. Resistances of sympatric and allopatric eels to sea snake venoms. Copeia 1995:1136–47
    [Google Scholar]
  44. 44. 
    Heatwole H, Powell J. 1998. Resistance of eels (Gymnothorax) to the venom of sea kraits (Laticauda colubrina): a test of coevolution. Toxicon 36:4619–25
    [Google Scholar]
  45. 45. 
    Biardi JE, Coss RG. 2011. Rock squirrel (Spermophilus variegatus) blood sera affects proteolytic and hemolytic activities of rattlesnake venoms. Toxicon 57:2323–31
    [Google Scholar]
  46. 46. 
    Rowe AH, Rowe MP. 2008. Physiological resistance of grasshopper mice (Onychomys spp.) to Arizona bark scorpion (Centruroides exilicauda) venom. Toxicon 52:5597–605
    [Google Scholar]
  47. 47. 
    Rowe AH, Xiao Y, Rowe MP, Cummins TR, Zakon HH. 2013. Voltage-gated sodium channel in grasshopper mice defends against bark scorpion toxin. Science 342:6157441–46
    [Google Scholar]
  48. 48. 
    Drabeck DH, Dean AM, Jansa SA. 2015. Why the honey badger don't care: convergent evolution of venom-targeted nicotinic acetylcholine receptors in mammals that survive venomous snake bites. Toxicon 99:68–72
    [Google Scholar]
  49. 49. 
    Asher O, Lupu-Meiri M, Jensen BS, Paperna T, Fuchs S, Oron Y. 1998. Functional characterization of mongoose nicotinic acetylcholine receptor α-subunit: resistance to α-bungarotoxin and high sensitivity to acetylcholine. FEBS Lett 431:3411–14
    [Google Scholar]
  50. 50. 
    Jansa SA, Voss RS. 2011. Adaptive evolution of the venom-targeted vWF protein in opossums that eat pitvipers. PLOS ONE 6:6e20997
    [Google Scholar]
  51. 51. 
    Anderson B, Johnson SD 2008. The geographical mosaic of coevolution in a plant-pollinator mutualism. Evolution 62:1220–25
    [Google Scholar]
  52. 52. 
    Heithaus ER, Opler PA, Baker HG. 1974. Bat activity and pollination of Bauhinia pauletia: plant-pollinator coevolution. Ecology 55:2412–19
    [Google Scholar]
  53. 53. 
    Bawa KS. 1990. Plant-pollinator interactions in tropical rain forests. Annu. Rev. Ecol. Syst. 1:399–422
    [Google Scholar]
  54. 54. 
    Janzen DH. 1966. Coevolution of mutualism between ants and acacias in Central America. Evolution 20:3249–75
    [Google Scholar]
  55. 55. 
    Brouat C, Garcia N, Andary C, McKey D. 2001. Plant lock and ant key: pairwise coevolution of an exclusion filter in an ant-plant mutualism. Proc. R. Soc. Lond. B 268:14812131–41
    [Google Scholar]
  56. 56. 
    Ehrlich PR, Raven PH. 1964. Butterflies and plants: a study in coevolution. Evolution 1:586–608
    [Google Scholar]
  57. 57. 
    Dawkins R, Krebs JR. 1979. Arms races between and within species. Proc. R. Soc. Lond. B 205:1161489–511
    [Google Scholar]
  58. 58. 
    Arnqvist G, Rowe L. 2002. Antagonistic coevolution between the sexes in a group of insects. Nature 415:6873787–89
    [Google Scholar]
  59. 59. 
    Langmore NE, Hunt S, Kilner RM 2003. Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 422:6928157–60
    [Google Scholar]
  60. 60. 
    Kuntner M, Coddington JA, Schneider JM. 2009. Intersexual arms race? Genital coevolution in nephilid spiders (Araneae, Nephilidae). Evolution 63:61451–63
    [Google Scholar]
  61. 61. 
    Benkman CW, Parchman TL, Favis A, Siepielski AM 2003. Reciprocal selection causes a coevolutionary arms race between crossbills and lodgepole pine. Am. Nat. 162:2182–94
    [Google Scholar]
  62. 62. 
    Berenbaum M, Feeny P. 1981. Toxicity of angular furanocoumarins to swallowtail butterflies: Escalation in a coevolutionary arms race?. Science 212:4497927–29
    [Google Scholar]
  63. 63. 
    Brodie ED III, Brodie ED Jr. 1990. Tetrodotoxin resistance in garter snakes: an evolutionary response of predators to dangerous prey. Evolution 44:3651–59
    [Google Scholar]
  64. 64. 
    Brodie ED III, Brodie ED Jr. 1999. Predator-prey arms races: Asymmetrical selection on predators and prey may be reduced when prey are dangerous. Bioscience 49:7557–68
    [Google Scholar]
  65. 65. 
    Geffeney SL, Fujimoto E, Brodie ED, Ruben PC 2005. Evolutionary diversification of TTX-resistant sodium channels in a predator-prey interaction. Nature 434:7034759–63
    [Google Scholar]
  66. 66. 
    Saporito RA, Donnelly MA, Norton RA, Garraffo HM, Spande TF, Daly JW. 2007. Oribatid mites as a major dietary source for alkaloids in poison frogs. PNAS 104:218885–90
    [Google Scholar]
  67. 67. 
    Saporito RA, Garraffo HM, Donnelly MA, Edwards AL, Longino JT, Daly JW. 2004. Formicine ants: an arthropod source for the pumiliotoxin alkaloids of dendrobatid poison frogs. PNAS 101:218045–50
    [Google Scholar]
  68. 68. 
    Chau R, Kalaitzis JA, Neilan BA. 2011. On the origins and biosynthesis of tetrodotoxin. Aquat. Toxicol. 104:1–261–72
    [Google Scholar]
  69. 69. 
    Bucciarelli GM, Green DB, Shaffer HB, Kats LB. 2016. Individual fluctuations in toxin levels affect breeding site fidelity in a chemically defended amphibian. Proc. R. Soc. Lond. B 283:183120160468
    [Google Scholar]
  70. 70. 
    Bucciarelli GM, Li A, Kats LB, Green DB. 2014. Quantifying tetrodotoxin levels in the California newt using a non-destructive sampling method. Toxicon 80:87–93
    [Google Scholar]
  71. 71. 
    Bucciarelli GM, Shaffer HB, Green DB, Kats LB. 2017. An amphibian chemical defense phenotype is inducible across life history stages. Sci. Rep. 7:8185
    [Google Scholar]
  72. 72. 
    Hanifin CT, Brodie ED III, Brodie ED Jr. 2004. A predictive model to estimate total skin tetrodotoxin in the newt Taricha granulosa. Toxicon 43:3243–49
    [Google Scholar]
  73. 73. 
    Arakawa O, Takatani T, Taniyama S, Tatsuno R 2017. Toxins of pufferfish—distribution, accumulation mechanism, and physiologic functions. Aqua-Biosci. Monogr. 10:41–80
    [Google Scholar]
  74. 74. 
    Hanifin CT, Brodie ED III, Brodie ED Jr. 2002. Tetrodotoxin levels of the rough-skin newt, Taricha granulosa, increase in long-term captivity. Toxicon 40:81149–53
    [Google Scholar]
  75. 75. 
    Yotsu-Yamashita M, Gilhen J, Russell RW, Krysko KL, Melaun C et al. 2012. Variability of tetrodotoxin and of its analogues in the red-spotted newt, Notophthalmus viridescens (Amphibia: Urodela: Salamandridae). Toxicon 59:2257–64
    [Google Scholar]
  76. 76. 
    Hanifin CT, Brodie ED Jr., Brodie ED III 2008. Phenotypic mismatches reveal escape from arms-race coevolution. PLOS Biol 6:3e60
    [Google Scholar]
  77. 77. 
    Vaelli PM, Theis KR, Williams JE, O'Connell LA, Foster JA, Eisthen HL 2020. The skin microbiome facilitates adaptive tetrodotoxin production in poisonous newts. eLife 9:e53898
    [Google Scholar]
  78. 78. 
    Lago J, Rodríguez LP, Blanco L, Vieites JM, Cabado AG. 2015. Tetrodotoxin, an extremely potent marine neurotoxin: distribution, toxicity, origin and therapeutical uses. Mar. Drugs 13:106384–406
    [Google Scholar]
  79. 79. 
    Lehman EM, Brodie ED Jr., Brodie ED III 2004. No evidence for an endosymbiotic bacterial origin of tetrodotoxin in the newt Taricha granulosa. Toxicon 44:3243–49
    [Google Scholar]
  80. 80. 
    Kniskern J, Rausher MD. 2001. Two modes of host-enemy coevolution. Popul. Ecol. 43:3–14
    [Google Scholar]
  81. 81. 
    Elliott SA, Kats LB, Breeding JA. 1993. The use of conspecific chemical cues for cannibal avoidance in California newts (Taricha torosa). Ethology 95:3186–92
    [Google Scholar]
  82. 82. 
    Zimmer RK, Schar DW, Ferrer RP, Krug PJ, Kats LB, Michel WC. 2006. The scent of danger: tetrodotoxin (TTX) as an olfactory cue of predation risk. Ecol. Monogr. 76:4585–600
    [Google Scholar]
  83. 83. 
    Bucciarelli GM, Kats LB. 2015. Effects of newt chemical cues on the distribution and foraging behavior of stream macroinvertebrates. Hydrobiologia 749:169–81
    [Google Scholar]
  84. 84. 
    Ota WM, Olsen B, Bucciarelli GM, Kats LB. 2018. The effect of newt toxin on an invasive snail. Hydrobiologia 817:1341–48
    [Google Scholar]
  85. 85. 
    Matsumura K. 1995. Tetrodotoxin as a pheromone. Nature 378:563–64
    [Google Scholar]
  86. 86. 
    Hwang P, Noguchi T, Hwang DF. 2004. Neurotoxin tetrodotoxin as attractant for toxic snails. Fish. Sci. 70:61106–12
    [Google Scholar]
  87. 87. 
    Hillman K, Goodrich-Blair H. 2016. Are you my symbiont? Microbial polymorphic toxins and antimicrobial compounds as honest signals of beneficial symbiotic defensive traits. Curr. Opin. Microbiol. 31:184–90
    [Google Scholar]
  88. 88. 
    Yotsu-Yamashita M, Yamaki H, Okoshi N, Araki N 2010. Distribution of homologous proteins to puffer fish saxitoxin and tetrodotoxin binding protein in the plasma of puffer fish and among the tissues of Fugu pardalis examined by Western blot analysis. Toxicon 55:1119–24
    [Google Scholar]
  89. 89. 
    Matsui T, Yamamori K, Furukawa M, Kono M. 2000. Purification and some properties of tetrodotoxin binding protein from the blood plasma of kusafugu. Takifugu niphobles. Toxicon 38:463–68
    [Google Scholar]
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