1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Ecology, Evolution, and Systematics
  4. Volume 54, 2023
  5. Article

Annual Review of Ecology, Evolution, and Systematics

Volume 54, 2023

The Diverse Mechanisms that Animals Use to Resist Toxins

Abstract

Biological toxins are entrenched within ecosystems. Thus, animals are often exposed to such toxins, and how they adapt can be a key determinant of their evolutionary trajectories. In this review, we provide an overview of the diversity of toxin resistance mechanisms, with a focus on animals that sequester toxins from their diet and their natural predators and parasites. We propose a structured framework in which to study toxin resistance by recategorizing and reorganizing known mechanisms into avoidance, metabolism, and target categories. Then, using this framework, we review evidence regarding how animals resist four widely studied compounds: tetrodotoxin, batrachotoxin, cardiotonic steroids, and pyrrolizidine alkaloids. Based on the available data, we conclude that toxin resistance and sequestration are interrelated from both ecological and evolutionary perspectives. To conclude, we highlight open questions regarding toxin resistance and review its importance as a field.

En los ecosistemas las toxinas de origen biológico son componentes intrínsecos. Por esta razón, los animales se ven expuestos frecuenciamente a dichas toxinas y la forma en que se adaptan puede ser un factor que determina su trayectoria evolutiva. Esta revisión ofrece una visión general de la diversidad de mecanismos de resistencia a toxinas, centrándose en animales que secuestran toxinas de su dieta y en sus depredadores y parásitos naturales. En este texto se propone un marco estructural para estudiar la resistencia a toxinas mediante la recategorización y reorganización de mecanismos conocidos en categorías de: evación, metabolismo y moléculas diana. A continuación, utilizando este marco, revisamos la literatura científica en busca de evidencia sobre cómo los animales resisten a cuatro compuestos ampliamente estudiados: tetrodotoxina, batracotoxina, esteroides cardiotónicos y alcaloides de pirrolizidina. A partir de los datos disponibles, llegamos a la conclusión de que la resistencia y la retención de toxinas están interrelacionadas tanto desde el punto de vista ecológico como evolutivo. Por último, destacamos algunas preguntas abiertas en torno a la resistencia a las toxinas y resaltamos su importancia como campo de estudio en el futuro.

Keyword(s): batrachotoxin, cardiotonic steroids, chemical defense, pyrrolizidine alkaloids, tetrodotoxin, toxin resistance
Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-102320-102117
2023-11-02
2024-04-29
Loading full text...

Full text loading...

/deliver/fulltext/ecolsys/54/1/annurev-ecolsys-102320-102117.html?itemId=/content/journals/10.1146/annurev-ecolsys-102320-102117&mimeType=html&fmt=ahah

Literature Cited

  1. Abderemane-Ali F, Rossen ND, Kobiela ME, Craig RA, Garrison CE et al. 2021. Evidence that toxin resistance in poison birds and frogs is not rooted in sodium channel mutations and may rely on “toxin sponge” proteins. J. Gen. Physiol. 153:9e202112872
     [Google Scholar]
  2. Agrawal AA. 2011. Current trends in the evolutionary ecology of plant defence. Funct. Ecol. 25:2420–32
     [Google Scholar]
  3. Agrawal AA, Böröczky K, Haribal M, Hastings AP, White RA et al. 2021. Cardenolides, toxicity, and the costs of sequestration in the coevolutionary interaction between monarchs and milkweeds. PNAS 118:16e2024463118
     [Google Scholar]
  4. Agrawal AA, Petschenka G, Bingham RA, Weber MG, Rasmann S. 2012. Toxic cardenolides: chemical ecology and coevolution of specialized plant–herbivore interactions. New Phytol 194:128–45
     [Google Scholar]
  5. Alvarez-Buylla A, Garzón MDM, Rangel AE, Tapia EE, Soh HT et al. 2022. Binding and sequestration of poison frog alkaloids by a plasma globulin. BioRxiv 2022.11.22.517437 https://doi.org/10.1101/2022.11.22.517437
    [Crossref] [Google Scholar]
  6. Amano M, Amiya N, Takaoka M, Sato H, Takatani T et al. 2019. Tetrodotoxin functions as a stress relieving substance in juvenile tiger puffer Takifugu rubripes. Toxicon 171:54–61
     [Google Scholar]
  7. Amano M, Takatani T, Sakayauchi F, Oi R, Sakakura Y. 2022. The brain of the wild toxic marine pufferfishes accumulates tetrodotoxin. Toxicon 218:1–7
     [Google Scholar]
  8. Ames PL. 1966. DDT residues in the eggs of the osprey in the north-eastern United States and their relation to nesting success. J. Appl. Ecol. 3:87–97
     [Google Scholar]
  9. Arbuckle K, Rodríguez de la Vega RC, Casewell NR 2017. Coevolution takes the sting out of it: evolutionary biology and mechanisms of toxin resistance in animals. Toxicon 140:118–31
     [Google Scholar]
  10. Baggot JD, Davis LE. 1973. Plasma protein binding of digitoxin and digoxin in several mammalian species. Res. Vet. Sci. 15:181–87
     [Google Scholar]
  11. Barnett CA, Bateson M, Rowe C. 2007. State-dependent decision making: educated predators strategically trade off the costs and benefits of consuming aposematic prey. Behav. Ecol. 18:4645–51
     [Google Scholar]
  12. Berenbaum M. 1983. Coumarins and caterpillars: a case for coevolution. Evolution 37:1163–79
     [Google Scholar]
  13. Bernays E, Graham M. 1988. On the evolution of host specificity in phytophagous arthropods. Ecology 69:4886–92
     [Google Scholar]
  14. Boppré M, Schneider D. 1989. The biology of Creatonotos (Lepidoptera: Arctiidae) with special reference to the androconial system. Zool. J. Linn. Soc. 96:4339–56
     [Google Scholar]
  15. Bringsøe H, Holden J. 2021. Yet another kukri snake piercing an anuran abdomen: Oligodon ocellatus (Morice, 1875) eats Duttaphrynus melanostictus (Schneider, 1799) in Vietnam. Herpetozoa 34:57–59
     [Google Scholar]
  16. Cabrera-Guzmán E, Crossland MR, Pearson D, Webb JK, Shine R. 2015. Predation on invasive cane toads (Rhinella marina) by native Australian rodents. J. Pest Sci. 88:1143–53
     [Google Scholar]
  17. Carpenter GDH. 1942. Observations and experiments in Africa by the late C.F.M. Swynnerton on wild birds eating butterflies and the preference shown. Proc. Linn. Soc. 154:110–46
     [Google Scholar]
  18. Ceja-Navarro JA, Vega FE, Karaoz U, Hao Z, Jenkins S et al. 2015. Gut microbiota mediate caffeine detoxification in the primary insect pest of coffee. Nat. Commun. 6:7618
     [Google Scholar]
  19. Chakraborty M, Emerson JJ, Macdonald SJ, Long AD. 2019. Structural variants exhibit widespread allelic heterogeneity and shape variation in complex traits. Nat. Commun. 10:14872
     [Google Scholar]
  20. Chung H, Carroll SB. 2015. Wax, sex and the origin of species: dual roles of insect cuticular hydrocarbons in adaptation and mating. Bioessays 37:7822–30
     [Google Scholar]
  21. Crossland MR, Salim AA, Capon RJ, Shine R. 2021. Chemical cues that attract cannibalistic cane toad (Rhinella marina) larvae to vulnerable embryos. Sci. Rep. 11:112527
     [Google Scholar]
  22. del Campo ML, Possner ST, Eisner T. 2007. Corematal function in Utetheisa ornatrix (Lepidoptera: Arctiidae): Hydroxydanaidal is devoid of intrinsic defensive potency. Chemoecology 17:119–22
     [Google Scholar]
  23. Després L, David J-P, Gallet C. 2007. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22:6298–307
     [Google Scholar]
  24. 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. PNAS 109:3213040–45
     [Google Scholar]
  25. Douglas TE, Beskid SG, Gernand CE, Nirtaut BE, Tamsil KE et al. 2022. Trade-offs between cost of ingestion and rate of intake drive defensive toxin use. Biol. Lett. 18:220210579
     [Google Scholar]
  26. Dreisbach D, Bhandari DR, Betz A, Tenbusch L, Vilcinskas A et al. 2023. Spatial metabolomics reveal divergent cardenolide processing in the monarch (Danaus plexippus) and the common crow butterfly (Euploea core). Mol. Ecol. Resour. 23:61195–210
     [Google Scholar]
  27. Durso AM, Neuman-Lee LA, Hopkins GR, Brodie ED Jr. 2021. Stable isotope analysis suggests that tetrodotoxin-resistant Common Gartersnakes (Thamnophis sirtalis) rarely feed on newts in the wild. Can. J. Zool. 99:5331–38
     [Google Scholar]
  28. Egelhaaf A, Rick-Wagner S, Schneider D. 1992. Development of the male scent organ of Creatonotos transiens (Lepidoptera, Arctiidae) during metamorphosis. Zoomorphology 111:3125–39
     [Google Scholar]
  29. Ehmke A, von Borstel K, Hartmann T. 1988. Alkaloid N-oxides as transport and vacuolar storage compounds of pyrrolizidine alkaloids in Senecio vulgaris L. Planta 176:183–90
     [Google Scholar]
  30. Ehrlich PR, Raven PH. 1964. Butterflies and plants: a study in coevolution. Evolution 18:4586–608
     [Google Scholar]
  31. Feyereisen R. 1995. Molecular biology of insecticide resistance. Toxicol. Lett. 82–83:83–90
     [Google Scholar]
  32. Flier J, Edwards MW, Daly JW, Myers CW. 1980. Widespread occurrence in frogs and toads of skin compounds interacting with the ouabain site of Na+, K+-ATPase. Science 208:4443503–5
     [Google Scholar]
  33. FAO (Food Agric. Organ U. N.) 2012. Guidelines on Prevention and Management of Pesticide Resistance Rome: FAO. https://www.fao.org/3/bt561e/bt561e.pdf
  34. Freitas JC, Sato S, Ogata T, Kodama M. 1995. Guanidine neurotoxins are released with the digestive fluid of crabs (Crustacea, Brachyura). Toxicon 33:2201–8
     [Google Scholar]
  35. Frick C, Wink M. 1995. Uptake and sequestration of ouabain and other cardiac glycosides in Danaus plexippus (Lepidoptera: Danaidae): evidence for a carrier-mediated process. J. Chem. Ecol. 21:5557–75
     [Google Scholar]
  36. Geffeney SL, Fujimoto E, Brodie ED III, Brodie ED Jr., Ruben PC 2005. Evolutionary diversification of TTX-resistant sodium channels in a predator–prey interaction. Nature 434:759–63
     [Google Scholar]
  37. Georghiou GP. 1972. The evolution of resistance to pesticides. Annu. Rev. Ecol. Syst. 3:133–68
     [Google Scholar]
  38. Gibbs HL, Sanz L, Pérez A, Ochoa A, Hassinger ATB et al. 2020. The molecular basis of venom resistance in a rattlesnake-squirrel predator-prey system. Mol. Ecol. 29:152871–88
     [Google Scholar]
  39. Glendinning JI. 1994. Is the bitter rejection response always adaptive?. Physiol. Behav. 56:61217–27
     [Google Scholar]
  40. Groen SC, LaPlante ER, Alexandre NM, Agrawal AA, Dobler S, Whiteman NK. 2017. Multidrug transporters and organic anion transporting polypeptides protect insects against the toxic effects of cardenolides. Insect Biochem. Mol. Biol. 81:51–61
     [Google Scholar]
  41. Hague MTJ, Toledo G, Geffeney SL, Hanifin CT, Brodie ED Jr., Brodie ED III 2018. Large-effect mutations generate trade-off between predatory and locomotor ability during arms race coevolution with deadly prey. Evol. Lett. 2:4406–16
     [Google Scholar]
  42. Hanifin CT, Gilly WF. 2015. Evolutionary history of a complex adaptation: tetrodotoxin resistance in salamanders. Evolution 69:1232–44
     [Google Scholar]
  43. Hartmann T, Theuring C, Schmidt J, Rahier M, Pasteels JM. 1999. Biochemical strategy of sequestration of pyrrolizidine alkaloids by adults and larvae of chrysomelid leaf beetles. J. Insect Physiol. 45:1085–95
     [Google Scholar]
  44. Hartmann T, Theuring C, Witte L, Pasteels JM. 2001. Sequestration, metabolism and partial synthesis of tertiary pyrrolizidine alkaloids by the neotropical leaf-beetle Platyphora boucardi. Insect Biochem. Mol. Biol. 31:111041–56
     [Google Scholar]
  45. Heidel-Fischer HM, Vogel H. 2015. Molecular mechanisms of insect adaptation to plant secondary compounds. Curr. Opin. Insect. Sci. 8:8–14
     [Google Scholar]
  46. Helmus MR, Dussourd DE. 2005. Glues or poisons: Which triggers vein cutting by monarch caterpillars?. Chemoecology 15:145–49
     [Google Scholar]
  47. Holding ML, Drabeck DH, Jansa SA, Gibbs HL. 2016. Venom resistance as a model for understanding the molecular basis of complex coevolutionary adaptations. Integr. Comp. Biol. 56:51032–43
     [Google Scholar]
  48. Hurlbert SH. 1970. Predator responses to the vermilion-spotted newt (Notophthalmus viridescens). J. Herpetol. 4:1/247–55
     [Google Scholar]
  49. Imai H, Suzuki N, Ishimaru Y. 2012. Functional diversity of bitter taste receptor TAS2R16 in primates. Biol. Lett. 8:652–56
     [Google Scholar]
  50. Jeckel AM, Bolton SK, Waters KR, Antoniazzi MM, Jared C et al. 2022. Dose-dependent alkaloid sequestration and N-methylation of decahydroquinoline in poison frogs. J. Exp. Zool. A Ecol. Integr. Physiol. 337:5537–46
     [Google Scholar]
  51. Jeckel AM, Matsumura K, Nishikawa K, Morimoto Y, Saporito RA et al. 2020. Use of whole-body cryosectioning and desorption electrospray ionization mass spectrometry imaging to visualize alkaloid distribution in poison frogs. J. Mass Spectrom. 55:6e4520
     [Google Scholar]
  52. Jones TH, Blum MS, Fales HM, Brandão CR, Lattke J. 1991. Chemistry of venom alkaloids in the ant genus Megalomyrmex. J. Chem. Ecol. 17:91897–908
     [Google Scholar]
  53. Kajimura S, Hirano T, Moriyama S, Vakkuri O, Leppäluoto J, Grau EG. 2004. Changes in plasma concentrations of immunoreactive ouabain in the tilapia in response to changing salinity: Is ouabain a hormone in fish?. Gen. Comp. Endocrinol. 135:190–99
     [Google Scholar]
  54. Karageorgi M, Groen SC, Sumbul F, Pelaez JN, Verster KI et al. 2019. Genome editing retraces the evolution of toxin resistance in the monarch butterfly. Nature 574:7778409–12
     [Google Scholar]
  55. Kato-Unoki Y, Takai Y, Kinoshita M, Mochizuki T, Tatsuno R et al. 2018. Genome editing of pufferfish saxitoxin- and tetrodotoxin-binding protein type 2 in Takifugu rubripes. Toxicon 153:58–61
     [Google Scholar]
  56. Kowalski P, Baum M, Körten M, Donath A, Dobler S. 2020. ABCB transporters in a leaf beetle respond to sequestered plant toxins. Proc. Biol. Sci. 2871934:20201311
     [Google Scholar]
  57. Kristensen C, Morant M, Olsen CE, Ekstrøm CT, Galbraith DW et al. 2005. Metabolic engineering of dhurrin in transgenic Arabidopsis plants with marginal inadvertent effects on the metabolome and transcriptome. PNAS 102:51779–84
     [Google Scholar]
  58. Labbé P, Alout H, Djogbénou L, Pasteur N, Weill M. 2011. Evolution of resistance to insecticide in disease vectors. Genetics and Evolution of Infectious Disease M Tibayrenc 363–409. London: Elsevier
     [Google Scholar]
  59. Lawrence JP, Rojas B, Blanchette A, Saporito RA, Mappes J et al. 2023. Linking predator responses to alkaloid variability in poison frogs. J. Chem. Ecol. 49:3–4195–204
     [Google Scholar]
  60. Lee JH, Kondo H, Sato S, Akimoto S, Saito T et al. 2007. Identification of novel genes related to tetrodotoxin intoxication in pufferfish. Toxicon 49:7939–53
     [Google Scholar]
  61. Li X, Schuler MA, Berenbaum MR. 2007. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol. 52:231–53
     [Google Scholar]
  62. Lichtstein D, Gati I, Babila T, Haver E, Katz U. 1991. Effect of salt acclimation on digitalis-like compounds in the toad. Biochim. Biophys. Acta Gen. Subj. 1073:165–68
     [Google Scholar]
  63. Lohr JN, Meinzer F, Dalla S, Romey-Glüsing R, Dobler S. 2017. The function and evolutionary significance of a triplicated Na,K-ATPase gene in a toxin-specialized insect. BMC Evol. Biol. 17:1256
     [Google Scholar]
  64. Lunceford BE, Kubanek J. 2015. Reception of aversive taste. Integr. Comp. Biol. 55:3507–17
     [Google Scholar]
  65. Mahon AR. 1999. An investigation of the roles of toxins in arrow worms (Phylum Chaetognatha). Master of Science thesis Truman State University Kirksville, MO:
     [Google Scholar]
  66. Malcolm SB. 1986. Aposematism in a soft-bodied insect: a case for kin selection. Behav. Ecol. Sociobiol. 18:5387–93
     [Google Scholar]
  67. Malcolm SB. 1989. Disruption of web structure and predatory behavior of a spider by plant-derived chemical defenses of an aposematic aphid. J. Chem. Ecol. 15:61699–716
     [Google Scholar]
  68. Malykin GV, Chernyshev AV, Magarlamov TY. 2021. Intrabody tetrodotoxin distribution and possible hypothesis for its migration in ribbon worms Cephalothrix cf. simula (Palaeonemertea, Nemertea). Mar. Drugs 19:9494
     [Google Scholar]
  69. Manunta P, Ferrandi M, Bianchi G, Hamlyn JM. 2009. Endogenous ouabain in cardiovascular function and disease. J. Hypertens. 27:19–18
     [Google Scholar]
  70. McGlothlin JW, Kobiela ME, Feldman CR, Castoe TA, Geffeney SL et al. 2016. Historical contingency in a multigene family facilitates adaptive evolution of toxin resistance. Curr. Biol. 26:121616–21
     [Google Scholar]
  71. Mebs D, Wunder C, Pogoda W, Toennes SW. 2017. Feeding on toxic prey. The praying mantis (Mantodea) as predator of poisonous butterfly and moth (Lepidoptera) caterpillars. Toxicon 131:16–19
     [Google Scholar]
  72. Mebs D, Yotsu-Yamashita M, Arakawa O. 2016. The praying mantis (Mantodea) as predator of the poisonous red-spotted newt Notophthalmus viridescens (Amphibia: Urodela: Salamandridae). Chemoecology 26:3121–26
     [Google Scholar]
  73. Melnikova DI, Magarlamov TY. 2022. An overview of the anatomical distribution of tetrodotoxin in animals. Toxins 14:8576
     [Google Scholar]
  74. Milani R. 1963. Genetical aspects of insecticide resistance. Bull. World Health Organ. 29:77–87
     [Google Scholar]
  75. Mitchell C, Brennan RM, Graham J, Karley AJ. 2016. Plant defense against herbivorous pests: exploiting resistance and tolerance traits for sustainable crop protection. Front. Plant Sci. 7:1132
     [Google Scholar]
  76. Mohammadi S, Gompert Z, Gonzalez J, Takeuchi H, Mori A, Savitzky AH. 2016. Toxin-resistant isoforms of Na+/K+-ATPase in snakes do not closely track dietary specialization on toads. Proc. R. Soc. B 283:184220162111
     [Google Scholar]
  77. Mohammadi S, Yang L, Bulbert M, Rowland HM. 2022. Defence mitigation by predators of chemically defended prey integrated over the predation sequence and across biological levels with a focus on cardiotonic steroids. R. Soc. Open Sci. 9:9220363
     [Google Scholar]
  78. Mohammadi S, Yang L, Harpak A, Herrera-Álvarez S, del Pilar Rodríguez-Ordoñez M et al. 2021. Concerted evolution reveals co-adapted amino acid substitutions in Na+K+-ATPase of frogs that prey on toxic toads. Curr. Biol. 31:122530–38.e10
     [Google Scholar]
  79. Morabito MA. 1994. Molecular cloning of bullfrog saxiphilin: a unique relative of the transferrin family that binds saxitoxin. PNAS 91:72478–82
     [Google Scholar]
  80. Morris JF, Ismail-Beigi F, Butler VP, Gati I, Lichtstein D. 1997. Ouabain-sensitive Na+,K+-ATPase activity in toad brain. Comp. Biochem. Physiol. A Physiol. 118:3599–606
     [Google Scholar]
  81. Nakata K, Tanaka Y, Nakano T, Adachi T, Tanaka H et al. 2006. Nuclear receptor-mediated transcriptional regulation in phase I, II, and III xenobiotic metabolizing systems. Drug Metab. Pharmacokinet. 21:6437–57
     [Google Scholar]
  82. Narberhaus I, Papke U, Theuring C, Beuerle T, Hartmann T, Dobler S. 2004. Direct evidence for membrane transport of host-plant-derived pyrrolizidine alkaloid N-oxides in two leaf beetle genera. J. Chem. Ecol. 30:102003–22
     [Google Scholar]
  83. Noguchi Y, Suzuki T, Matsutani K, Sakakibara R, Nakahigashi R et al. 2022. An almost nontoxic tetrodotoxin analog, 5,6,11-trideoxytetrodotoxin, as an odorant for the grass puffer. Sci. Rep. 12:115087
     [Google Scholar]
  84. O'Connell LA, LS50: Int. Sci. Lab. Course, O'Connell JD, Paulo JA, Trauger SA et al. 2021. Rapid toxin sequestration modifies poison frog physiology. J. Exp. Biol. 224:Part 3jeb230342
     [Google Scholar]
  85. Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P et al. 2022. vegan: Community Ecology Package. Statistical software https://cran.r-project.org/web/packages/vegan/vegan.pdf
    [Google Scholar]
  86. Olsen JD, Ralphs MH. 1986. Feed aversion induced by intraruminal infusion with larkspur extract in cattle. Am. J. Vet. Res. 47:81829–33
     [Google Scholar]
  87. Petschenka G, Agrawal AA. 2015. Milkweed butterfly resistance to plant toxins is linked to sequestration, not coping with a toxic diet. Proc. R. Soc. B 282:181820151865
     [Google Scholar]
  88. Petschenka G, Pick C, Wagschal V, Dobler S. 2013. Functional evidence for physiological mechanisms to circumvent neurotoxicity of cardenolides in an adapted and a non-adapted hawk-moth species. Proc. R. Soc. B 280:20123089
     [Google Scholar]
  89. Phillips B, Shine R. 2007. When dinner is dangerous: Toxic frogs elicit species-specific responses from a generalist snake predator. Am. Nat. 170:6936–42
     [Google Scholar]
  90. Phillips JM, Bricelj VM, Mitch M, Cerrato RM, MacQuarrie S, Connell LB. 2018. Biogeography of resistance to paralytic shellfish toxins in softshell clam, Mya arenaria (L.), populations along the Atlantic coast of North America. Aquat. Toxicol. 202:196–206
     [Google Scholar]
  91. Poulton EB. 1887. The experimental proof of the protective value of colour and markings in insects in reference to their vertebrate enemies. Proc. Zool. Soc. Lond. 55:2191–274
     [Google Scholar]
  92. Price-Rees SJ, Brown GP, Shine R. 2012. Interacting impacts of invasive plants and invasive toads on native lizards. Am. Nat. 179:3413–22
     [Google Scholar]
  93. Pugalenthi P, Livingstone D. 1995. Cardenolides (heart poisons) in the painted grasshopper Poecilocerus pictus F. (Orthoptera: Pyrgomorphidae) feeding on the milkweed Calotropis gigantea L. (Asclepiadaceae). J. New York Entomol. Soc. 103:2191–96
     [Google Scholar]
  94. R Core Team 2021. R: A Language and Environment for Statistical Computing Vienna: R Found. Stat. Comput.
  95. Ramírez-Castañeda V. 2017. Origin of mutations in the voltage-gated sodium channel family associated with neurotoxin resistance in Erythrolamprus sp. snake predators of the Dendrobatidae poison frogs. Master of Science thesis Universidad de Los Andes Bogotá, Colombia:
     [Google Scholar]
  96. Reid ML, Ahn S. 2020. Realised toxicity of plant defences to an insect herbivore depends more on insect dehydration than on energy reserves. Ecol. Entomol. 45:4771–82
     [Google Scholar]
  97. Reimche JS, Del Carlo RE, Brodie ED Jr., McGlothlin JW, Schlauch K et al. 2022. The road not taken: evolution of tetrodotoxin resistance in the Sierra garter snake (Thamnophis couchii) by a path less travelled. Mol. Ecol. 31:143827–43
     [Google Scholar]
  98. Revell L. 2012. Phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3:217–23
     [Google Scholar]
  99. Rosenkranz V, Wink M. 2007. Induction of apoptosis by alkaloids, non-protein amino acids, and cardiac glycosides in human promyelotic HL-60 cells. Z. Naturforsch. C 62:5–6458–66
     [Google Scholar]
  100. 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]
  101. Santos JC, Tarvin RD, O'Connell LA 2016. A review of chemical defense in poison frogs (Dendrobatidae): ecology, pharmacokinetics, and autoresistance. Chemical Signals in Vertebrates 13, eds. BA Schulte, TE Goodwin, MH Ferkin 305–37. Cham, Switz: Springer Int. Publ.
     [Google Scholar]
  102. Scudder GGE, Moore LV, Isman MB. 1986. Sequestration of cardenolides in Oncopeltus fasciatus: morphological and physiological adaptations. J. Chem. Ecol. 12:51171–87
     [Google Scholar]
  103. Singer MS. 2008. Evolutionary ecology of polyphagy. Specialization, Speciation, and Radiation: The Evolutionary Biology of Herbivorous Insects K Tilmon Berkeley: University of California Press
     [Google Scholar]
  104. Smith JG, Phillips BL. 2006. Toxic tucker: the potential impact of cane toads on Australian reptiles. Pac. Conserv. Biol. 12:140–49
     [Google Scholar]
  105. Snyder MJ, Glendinning JI. 1996. Causal connection between detoxification enzyme activity and consumption of a toxic plant compound. J. Comp. Physiol. A 179:2255–61
     [Google Scholar]
  106. Stermitz FR, Harris GH. 1987. Transfer of pyrrolizidine and quinolizidine alkaloids to Castilleja (Scrophulariaceae) hemiparasites from composite and legume host plants. J. Chem. Ecol. 13:81917–25
     [Google Scholar]
  107. Stevens M, Peigneur S, Tytgat J. 2011. Neurotoxins and their binding areas on voltage-gated sodium channels. Front. Pharmacol. 2:71
     [Google Scholar]
  108. Strauss AS, Peters S, Boland W, Burse A. 2013. ABC transporter functions as a pacemaker for sequestration of plant glucosides in leaf beetles. eLife 2:e01096
     [Google Scholar]
  109. Tarvin RD, Borghese CM, Sachs W, Santos JC, Lu Y et al. 2017. Interacting amino acid replacements allow poison frogs to evolve epibatidine resistance. Science 357:63571261–66
     [Google Scholar]
  110. Trigo JR, Motta PC. 1990. Evolutionary implications of pyrrolizidine alkaloid assimilation by danaine and ithomiine larvae (Lepidoptera: Nymphalidae). Experientia 46:3332–34
     [Google Scholar]
  111. Tsai YH, Hwang DF, Chai TJ, Jeng SS. 1997. Toxicity and toxic components of two xanthid crabs, Atergatis floridus and Demania reynaudi, in Taiwan. Toxicon 35:81327–35
     [Google Scholar]
  112. van Thiel J, Khan MA, Wouters RM, Harris RJ, Casewell NR et al. 2022. Convergent evolution of toxin resistance in animals. Biol. Rev. Camb. Philos. Soc. 97:51823–43
     [Google Scholar]
  113. Wei JS, Cheng HC, Tsai KJ, Liu DH, Lee HH et al. 1996. Purification and characterization of endogenous digoxin-like immunoreactive factors in chicken blood. Life Sci 59:191617–29
     [Google Scholar]
  114. Wilson TG. 2001. Resistance of Drosophila to toxins. Annu. Rev. Entomol. 46:545–71
     [Google Scholar]
  115. Windecker W. 1939. Euchelia (hypocrita) jacobaeae L. und das Schutztrachtenproblem. Z. Morphol. Ökologie der Tiere 35:184–138
     [Google Scholar]
  116. Yotsu-Yamashita M, Sugimoto A, Terakawa T, Shoji Y, Miyazawa T, Yasumoto T. 2001. Purification, characterization, and cDNA cloning of a novel soluble saxitoxin and tetrodotoxin binding protein from plasma of the puffer fish, Fugu pardalis. Eur. J. Biochem. 268:225937–46
     [Google Scholar]
  117. Zdenek CN, Harris RJ, Kuruppu S, Youngman NJ, Dobson JS et al. 2019. A taxon-specific and high-throughput method for measuring ligand binding to nicotinic acetylcholine receptors. Toxins 11:10600
     [Google Scholar]
  118. Zeino M, Paulsen MS, Zehl M, Urban E, Kopp B, Efferth T. 2015. Identification of new P-glycoprotein inhibitors derived from cardiotonic steroids. Biochem. Pharmacol. 93:111–24
     [Google Scholar]
  119. Zhang H, Li P, Wu B, Hou J, Ren J et al. 2022. Transcriptomic analysis reveals the genes involved in tetrodotoxin (TTX) accumulation, translocation, and detoxification in the pufferfish Takifugu rubripes. Chemosphere 303:134962
     [Google Scholar]
  120. Zhang X, Zong J, Chen S, Li M, Lu Y et al. 2020. Accumulation and elimination of Tetrodotoxin in the pufferfish Takifugu obscurus by dietary administration of the wild toxic gastropod Nassarius semiplicata. Toxins 12:5278
     [Google Scholar]
  121. Zimmer RK, Ferrer RP. 2007. Neuroecology, chemical defense, and the keystone species concept. Biol. Bull. 213:208–25
     [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-102320-102117
Loading
The Diverse Mechanisms that Animals Use to Resist Toxins
Annual Review of Ecology, Evolution, and Systematics 54, 283 (2023); https://doi.org/10.1146/annurev-ecolsys-102320-102117
/content/journals/10.1146/annurev-ecolsys-102320-102117
/content/journals/10.1146/annurev-ecolsys-102320-102117
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error