Prey specificity of predatory venoms.

Publisher: Cambridge University Press Country of Publication: England NLM ID: 0414576 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1469-185X (Electronic) Linking ISSN: 00063231 NLM ISO Abbreviation: Biol Rev Camb Philos Soc Subsets: MEDLINE

Original Publication: London, Cambridge University Press.

Predatory Behavior*/physiology ; Venoms*; Animals ; Biological Evolution ; Species Specificity

Venom represents a key adaptation of many venomous predators, allowing them to immobilise prey quickly through chemical rather than physical warfare. Evolutionary arms races between prey and a predator are believed to be the main factor influencing the potency and composition of predatory venoms. Predators with narrowly restricted diets are expected to evolve specifically potent venom towards their focal prey, with lower efficacy on alternative prey. Here, we evaluate hypotheses on the evolution of prey-specific venom, focusing on the effect of restricted diet, prey defences, and prey resistance. Prey specificity as a potential evolutionary dead end is also discussed. We then provide an overview of the current knowledge on venom prey specificity, with emphasis on snakes, cone snails, and spiders. As the current evidence for venom prey specificity is still quite limited, we also overview the best approaches and methods for its investigation and provide a brief summary of potential model groups. Finally, possible applications of prey-specific toxins are discussed.
(© 2024 The Author(s). Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.)

Abd El‐Aziz, T. M., Soares, A. G. & Stockand, J. D. (2020). Advances in venomics: modern separation techniques and mass spectrometry. Journal of Chromatography B 1160, 122352.
Ahmadi, S., Valle, M. B., Boddum, K., Cardoso, F. C., King, G. F., Laustsen, A. H. & Ljungars, A. (2023). From squid giant axon to automated patch‐clamp: electrophysiology in venom and antivenom research. Frontiers in Pharmacology 14, 1249336.
Aili, S. R., Touchard, A., Escoubas, P., Padula, M. P., Orivel, J., Dejean, A. & Nicholson, G. M. (2014). Diversity of peptide toxins from stinging ant venoms. Toxicon 92, 166–178.
Aman, J. W., Imperial, J. S., Ueberheide, B., Zhang, M. M., Aguilar, M., Taylor, D., Watkins, M., Yoshikami, D., Showers‐Corneli, P., Safavi‐Hemami, H., Biggs, J., Teichert, R. W. & Olivera, B. M. (2015). Insights into the origins of fish hunting in venomous cone snails from studies of Conus tessulatus. Proceedings of the National Academy of Sciences USA 112(16), 5087–5092.
Barchan, D., Kachalsky, S., Neumann, D., Vogel, Z., Ovadia, M., Kochva, E. & Fuchs, S. (1992). How the mongoose can fight the snake: the binding site of the mongoose acetylcholine receptor. Proceedings of the National Academy of Sciences USA 89(16), 7717–7721.
Barlow, A., Pook, C. E., Harrison, R. A. & Wüster, W. (2009). Coevolution of diet and prey‐specific venom activity supports the role of selection in snake venom evolution. Proceedings of the Royal Society B: Biological Sciences 276(1666), 2443–2449.
Begon, M. & Townsend, C. R. (2021). Ecology: From Individuals to Ecosystems, 5th Edition (). John Wiley & Sons, Hoboken.
Brodie, E. D. & Brodie, E. D. Jr. (1999). Predator‐prey arms races: asymmetrical selection on predators and prey may be reduced when prey are dangerous. Bioscience 49(7), 557–568.
Bruce, C., Fitches, E. C., Chougule, N., Bell, H. A. & Gatehouse, J. A. (2011). Recombinant conotoxin, TxVIA, produced in yeast has insecticidal activity. Toxicon 58(1), 93–100.
Calvete, J. J., Ghezellou, P., Paiva, O., Matainaho, T., Ghassempour, A., Goudarzi, H., Kraus, F., Sanz, L. & Williams, D. J. (2012). Snake venomics of two poorly known Hydrophiinae: comparative proteomics of the venoms of terrestrial Toxicocalamus longissimus and marine Hydrophis cyanocinctus. Journal of Proteomics 75(13), 4091–4101.
Casewell, N. R., Petras, D., Card, D. C., Suranse, V., Mychajliw, A. M., Richards, D., Koludarov, I., Albulescu, L.‐O., Slagboom, J., Hempel, B.‐F., Ngum, N. M., Kennerley, R. J., Brocca, J. L., Whiteley, G., Harrison, R. A., et al. (2019). Solenodon genome reveals convergent evolution of venom in eulipotyphlan mammals. Proceedings of the National Academy of Sciences 116(51), 25745–25755.
Casewell, N. R., Wüster, W., Vonk, F. J., Harrison, R. A. & Fry, B. G. (2013). Complex cocktails: the evolutionary novelty of venoms. Trends in Ecology & Evolution 28(4), 219–229.
Chang, C. C. & Lee, J. D. (1977). Crotoxin, the neurotoxin of South American rattlesnake venom, is a presynaptic toxin acting like β‐bungarotoxin. Naunyn‐Schmiedeberg's Archives of Pharmacology 296, 159–168.
Chang, C. C., Lee, J. D., Eaker, D. & Fohlman, J. (1977). The presynaptic neuromuscular blocking action of taipoxin. A comparison with β‐bungarotoxin and crotoxin. Toxicon 15(6), 571–576.
Chapman, A. D. (2009). Number of Living Species in Australia and the World, 2nd Edition (). Department of the Environment, Water, Heritage and the Arts, Australian Government, Canberra.
Chen, J., Zhang, X., Lin, C. & Gao, B. (2023). Synthesis and insecticidal activity of cysteine‐free conopeptides from Conus betulinus. Toxicon 233, 107253.
Church, J. E. & Hodgson, W. C. (2002). The pharmacological activity of fish venoms. Toxicon 40, 1083–1093.
Coin, I., Beyermann, M. & Bienert, M. (2007). Solid‐phase peptide synthesis: from standard procedures to the synthesis of difficult sequences. Nature Protocols 2(12), 3247–3256.
Cruz, L. J., Ramilo, C. A., Corpuz, G. P. & Olivera, B. M. (1992). Conus peptides: phylogenetic range of biological activity. The Biological Bulletin 183(1), 159–164.
da Silva Jr, N. J. & Aird, S. D. (2001). Prey specificity, comparative lethality and compositional differences of coral snake venoms. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 128(3), 425–456.
Davies, E. L. & Arbuckle, K. (2019). Coevolution of snake venom toxic activities and diet: evidence that ecological generalism favours toxicological diversity. Toxins 11(12), 711.
Dawkins, R. & Krebs, J. R. (1979). Arms races between and within species. Proceedings of the Royal Society of London. Series B. Biological Sciences 205(1161), 489–511.
De Graaf, D. C., Aerts, M., Danneels, E. & Devreese, B. (2009). Bee, wasp and ant venomics pave the way for a component‐resolved diagnosis of sting allergy. Journal of Proteomics 72(2), 145–154.
DePass, L. R. (1989). Alternative approaches in median lethality (LD50) and acute toxicity testing. Toxicology Letters 49(2–3), 159–170.
de Wit, C. A. (1982). Resistance of the prairie vole (Microtus ochrogaster) and the woodrat (Neotoma floridana), in Kansas, to venom of the Osage copperhead (Agkistrodon contortrix phaeogaster). Toxicon 20(4), 709–714.
Duda, T. F. Jr. (2008). Differentiation of venoms of predatory marine gastropods: divergence of orthologous toxin genes of closely related Conus species with different dietary specializations. Journal of Molecular Evolution 67, 315–321.
Duggan, N. M., Saez, N. J., Clayton, D., Budusan, E., Watson, E. E., Tucker, I. J., Rash, L. D., King, G. F. & Payne, R. J. (2021). Total synthesis of the spider‐venom peptide Hi1a. Organic Letters 23(21), 8375–8379.
Dutertre, S., Jin, A. H., Vetter, I., Hamilton, B., Sunagar, K., Lavergne, V., Dutertre, V., Fry, B. G., Antunes, A., Venter, D. J., Alewood, P. F. & Lewis, R. J. (2014). Evolution of separate predation‐and defence‐evoked venoms in carnivorous cone snails. Nature Communications 5(1), 3521.
Endean, R. & Rudkin, C. (1963). Studies of the venoms of some Conidae. Toxicon 1(2), 49–64.
Endean, R. & Rudkin, C. (1965). Further studies of the venoms of Conidae. Toxicon 2(4), 225–249.
Escoubas, P., Palma, M. F. & Nakajima, T. (1995). A microinjection technique using Drosophila melanogaster for bioassay‐guided isolation of neurotoxins in arthropod venoms. Toxicon 33(12), 1549–1555.
Fainzilber, M., Gordon, D., Hasson, A., Spira, M. E. & Zlotkin, E. (1991). Mollusc‐specific toxins from the venom of Conus textile neovicarius. European Journal of Biochemistry 202(2), 589–595.
Fainzilber, M., Hasson, A., Oren, R., Burlingame, A. L., Gordon, D., Spira, M. E. & Zlotkin, E. (1994). New mollusk‐specific alpha‐conotoxins block Aplysia neuronal acetylcholine receptors. Biochemistry 33(32), 9523–9529.
Fainzilber, M. & Zlotkin, E. (1992). A new bioassay reveals mollusc‐specific toxicity in molluscivorous Conus venoms. Toxicon 30(4), 465–469.
Forsyth, P., Sevcik, C., Martínez, R., Castillo, C. & D'Suze, G. (2012). Bactridine's effects on DUM cricket neurons under voltage clamp conditions. Journal of Insect Physiology 58(12), 1676–1685.
Fry, B. G., Roelants, K., Champagne, D. E., Scheib, H., Tyndall, J. D. A., King, G. F., Nevalainen, T. J., Norman, J. A., Lewis, R. J., Norton, R. S., Renjifo, C. & de la Vega, R. C. (2009). The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annual Review of Genomics and Human Genetics 10, 483–511.
Gangur, A. N., Smout, M., Liddell, M. J., Seymour, J. E., Wilson, D. & Northfield, T. D. (2017). Changes in predator exposure, but not in diet, induce phenotypic plasticity in scorpion venom. Proceedings of the Royal Society B: Biological Sciences 284(1863), 20171364.
Gasanov, S. E., Dagda, R. K. & Rael, E. D. (2014). Snake venom cytotoxins, phospholipase A2s, and Zn2+‐dependent metalloproteinases: mechanisms of action and pharmacological relevance. Journal of Clinical Toxicology 4(1), 1000181.
Gibbs, H. L. & Mackessy, S. P. (2009). Functional basis of a molecular adaptation: prey‐specific toxic effects of venom from Sistrurus rattlesnakes. Toxicon 53(6), 672–679.
Gibbs, H. L., Sanz, L., Pérez, A., Ochoa, A., Hassinger, A. T., Holding, M. L. & Calvete, J. J. (2020). The molecular basis of venom resistance in a rattlesnake‐squirrel predator‐prey system. Molecular Ecology 29(15), 2871–2888.
Giribaldi, J., Wilson, D., Nicke, A., El Hamdaoui, Y., Laconde, G., Faucherre, A., Moha Ou Maati, H., Daly, N., Enjalbal, C. & Dutertre, S. (2018). Synthesis, structure and biological activity of CIA and CIB, two α‐conotoxins from the predation‐evoked venom of Conus catus. Toxins 10(6), 222.
Govorushko, S. (2019). Economic and ecological importance of termites: a global review. Entomological Science 22(1), 21–35.
Grimm, A., Ramírez, A. M. P., Moulherat, S., Reynaud, J. & Henle, K. (2014). Life‐history trait database of European reptile species. Nature Conservation 9, 45–67.
Grundler, M. C. (2020). SquamataBase: a natural history database and R package for comparative biology of snake feeding habits. Biodiversity Data Journal 8, e49943.
Guo, S., Herzig, V. & King, G. F. (2018). Dipteran toxicity assays for determining the oral insecticidal activity of venoms and toxins. Toxicon 150, 297–303.
Guruacharya, A. (2023). Co‐evolution of ion channels and neurotoxins in cnidarians leads to diversification of ion channel genes. bioRxiv 2023.03.11.532225.
Harris, R. J., Zdenek, C. N., Harrich, D., Frank, N. & Fry, B. G. (2020). An appetite for destruction: detecting prey‐selective binding of α‐neurotoxins in the venom of Afro‐Asian elapids. Toxins 12(3), 205.
Harris, R. J., Nekaris, K. A. I. & Fry, B. G. (2021). Monkeying around with venom: an increased resistance to α‐neurotoxins supports an evolutionary arms race between Afro‐Asian primates and sympatric cobras. BMC Biology 19, 1–13.
Hart, A. J., Isbister, G. K., O'Donnell, P., Williamson, N. A. & Hodgson, W. C. (2013). Species differences in the neuromuscular activity of post‐synaptic neurotoxins from two Australian black snakes (Pseudechis porphyriacus and Pseudechis colletti). Toxicology Letters 219(3), 262–268.
Healy, K., Carbone, C. & Jackson, A. L. (2019). Snake venom potency and yield are associated with prey‐evolution, predator metabolism and habitat structure. Ecology Letters 22(3), 527–537.
Herzig, V., King, G. F. & Undheim, E. A. (2019). Can we resolve the taxonomic bias in spider venom research? Toxicon: X 1, 100005.
Heyborne, W. H. & Mackessy, S. P. (2013). Identification and characterization of a taxon‐specific three‐finger toxin from the venom of the Green Vinesnake (Oxybelis fulgidus; family Colubridae). Biochimie 95(10), 1923–1932.
Hillyard, D. R., Olivera, B. M., Woodward, S., Corpuz, G. P., Gray, W. R., Ramilo, C. A. & Cruz, L. J. (1989). A molluskivorous Conus toxin: conserved frameworks in conotoxins. Biochemistry 28(1), 358–361.
Himaya, S. W. A. & Lewis, R. J. (2018). Venomics‐accelerated cone snail venom peptide discovery. International Journal of Molecular Sciences 19(3), 788.
Holding, M. L., Biardi, J. E. & Gibbs, H. L. (2016a). Coevolution of venom function and venom resistance in a rattlesnake predator and its squirrel prey. Proceedings of the Royal Society B: Biological Sciences 283(1829), 20152841.
Holding, M. L., Drabeck, D. H., Jansa, S. A. & Gibbs, H. L. (2016b). Venom resistance as a model for understanding the molecular basis of complex coevolutionary adaptations. Integrative and Comparative Biology 56(5), 1032–1043.
Holding, M. L., Strickland, J. L., Rautsaw, R. M., Hofmann, E. P., Mason, A. J., Hogan, M. P., Nystrom, G. S., Ellsworth, S. A., Colston, T. J., Borja, M., Castañeda‐Gaytán, G., Grünwald, C. I., Jones, J. M., Freitas‐de‐Sousa, L. A., Viala, V. L., et al. (2021). Phylogenetically diverse diets favor more complex venoms in North American pitvipers. Proceedings of the National Academy of Sciences USA 118(17), e2015579118.
Hoso, M., Asami, T. & Hori, M. (2007). Right‐handed snakes: convergent evolution of asymmetry for functional specialization. Biology Letters 3(2), 169–173.
Hu, H. Z. & Li, Z. W. (1996). Substance P potentiates ATP‐activated currents in rat primary sensory neurons. Brain Research 739(1–2), 163–168.
Jackson, R. R. (1992). Eight‐legged tricksters. Bioscience 42(8), 590–598.
Jackson, T. N., Jouanne, H. & Vidal, N. (2019). Snake venom in context: neglected clades and concepts. Frontiers in Ecology and Evolution 7, 332.
Jackson, T. N. & Koludarov, I. (2020). How the toxin got its toxicity. Frontiers in Pharmacology 11, 574925.
Jaiteh, M., Taly, A. & Hénin, J. (2016). Evolution of pentameric ligand‐gated ion channels: pro‐loop receptors. PLoS One 11(3), e0151934.
Jin, J., Agwa, A. J., Szanto, T. G., Csóti, A., Panyi, G., Schroeder, C. I., Walker, A. A. & King, G. F. (2020). Weaponisation ‘on the fly’: convergent recruitment of knottin and defensin peptide scaffolds into the venom of predatory assassin flies. Insect Biochemistry and Molecular Biology 118, 103310.
Jones, L., Harris, R. J. & Fry, B. G. (2021). Not goanna get me: mutations in the savannah monitor lizard (Varanus exanthematicus) nicotinic acetylcholine receptor confer reduced susceptibility to sympatric cobra venoms. Neurotoxicity Research 39, 1116–1122.
Kaas, Q., Westermann, J. C., Halai, R., Wang, C. K. & Craik, D. J. (2008). ConoServer, a database for conopeptide sequences and structures. Bioinformatics 24(3), 445–446.
King, G. F. & Hardy, M. C. (2013). Spider‐venom peptides: structure, pharmacology, and potential for control of insect pests. Annual Review of Entomology 58, 475–496.
King, G. F. (2019). Tying pest insects in knots: the deployment of spider‐venom‐derived knottins as bioinsecticides. Pest Management Science 75(9), 2437–2445.
Kini, R. M. & Doley, R. (2010). Structure, function and evolution of three‐finger toxins: mini proteins with multiple targets. Toxicon 56(6), 855–867.
Kita, M., Nakamura, Y., Okumura, Y., Ohdachi, S. D., Oba, Y., Yoshikuni, M., Kido, H. & Uemura, D. (2004). Blarina toxin, a mammalian lethal venom from the short‐tailed shrew Blarina brevicauda: isolation and characterization. Proceedings of the National Academy of Sciences 101(20), 7542–7547.
Klint, J. K., Senff, S., Saez, N. J., Seshadri, R., Lau, H. Y., Bende, N. S., Undheim, E. A. B., Rash, L. D., Mobli, M. & King, G. F. (2013). Production of recombinant disulfide‐rich venom peptides for structural and functional analysis via expression in the periplasm of E. coli. PLoS One 8(5), e63865.
Kordiš, D. & Gubenšek, F. (2000). Adaptive evolution of animal toxin multigene families. Gene 261(1), 43–52.
Kowalski, K., Marciniak, P., Rosiński, G. & Rychlik, L. (2017). Evaluation of the physiological activity of venom from the Eurasian water shrew Neomys fodiens. Frontiers in Zoology 14, 1–13.
Kowalski, K. & Rychlik, L. (2021). Venom use in eulipotyphlans: an evolutionary and ecological approach. Toxins 13(3), 231.
Kuhn‐Nentwig, L., Schaller, J. & Nentwig, W. (2004). Biochemistry, toxicology and ecology of the venom of the spider Cupiennius salei (Ctenidae). Toxicon 43(5), 543–553.
Kuntner, M. (2022). The seven grand challenges in arachnid science. Frontiers in Arachnid Science 1, 1082700.
LeBrun, E. G., Jones, N. T. & Gilbert, L. E. (2014). Chemical warfare among invaders: a detoxification interaction facilitates an ant invasion. Science 343(6174), 1014–1017.
Lee, C. Y. & Tseng, L. F. (1969). Species differences in susceptibility to elapid venoms. Toxicon 7(2), 89–93.
Liu, L., Chew, G., Hawrot, E., Chi, C. & Wang, C. (2007). Two potent α3/5 conotoxins from piscivorous Conus achatinus. Acta Biochimica et Biophysica Sinica 39(6), 438–444.
Lofgren, C. S. (ed.) (2019). Fire Ants and Leaf‐Cutting Ants: Biology and Management. CRC Press, Boca Raton.
Luna‐Ramírez, K. S., Aguilar, M. B., Falcón, A., de la Cotera, E. P. H., Olivera, B. M. & Maillo, M. (2007). An O‐conotoxin from the vermivorous Conus spurius active on mice and mollusks. Peptides 28(1), 24–30.
Lyons, K., Dugon, M. M. & Healy, K. (2020). Diet breadth mediates the prey specificity of venom potency in snakes. Toxins 12(2), 74.
Mackessy, S. P. (2008). Venom composition in rattlesnakes: trends and biological significance. In The Biology of Rattlesnakes (ed. W. K. Hayes), pp. 495–510. Loma Linda University Press, Loma Linda.
Mancuso, M., Zaman, S., Maddock, S. T., Kamei, R. G., Salazar‐Valenzuela, D., Wilkinson, M., Roelants, K. & Fry, B. G. (2023). Resistance is not futile: widespread convergent evolution of resistance to alpha‐neurotoxic snake venoms in caecilians (Amphibia: Gymnophiona). International Journal of Molecular Sciences 24(14), 11353.
Manzoli‐Palma, M. F., Gobbi, N. & Palma, M. S. (2003). Insects as biological models to assay spider and scorpion venom toxicity. Journal of Venomous Animals and Toxins Including Tropical Diseases 9, 174–185.
Martin, I. G. (1981). Venom of the short‐tailed shrew (Blarina brevicauda) as an insect immobilizing agent. Journal of Mammalogy 62(1), 189–192.
Michálek, O., Kuhn‐Nentwig, L. & Pekár, S. (2019a). High specific efficiency of venom of two prey‐specialized spiders. Toxins 11(12), 687.
Michálek, O., Řezáč, M., Líznarová, E., Symondson, W. O. & Pekár, S. (2019b). Silk versus venom: alternative capture strategies employed by closely related myrmecophagous spiders. Biological Journal of the Linnean Society 126(3), 545–554.
Michálek, O., Walker, A. A., Šedo, O., Zdráhal, Z., King, G. F. & Pekár, S. (2022). Composition and toxicity of venom produced by araneophagous white‐tailed spiders (Lamponidae: Lampona sp.). Scientific Reports 12(1), 21597.
Modahl, C. M., Mrinalini, Frietze, S. & Mackessy, S. P. (2018). Adaptive evolution of distinct prey‐specific toxin genes in rear‐fanged snake venom. Proceedings of the Royal Society B 285(1884), 20181003.
Morgenstern, D. & King, G. F. (2013). The venom optimization hypothesis revisited. Toxicon 63, 120–128.
Mukherjee, S. & Heithaus, M. R. (2013). Dangerous prey and daring predators: a review. Biological Reviews 88(3), 550–563.
Nakamura, T., Yu, Z., Fainzilber, M. & Burlingame, A. L. (1996). Mass spectrometric‐based revision of the structure of a cysteine‐rich peptide toxin with γ‐carboxyglutamic acid, TxVIIA, from the sea snail, Conus textile. Protein Science 5(3), 524–530.
Naples, V. L. (1999). Morphology, evolution and function of feeding in the giant anteater (Myrmecophaga tridactyla). Journal of Zoology 249(1), 19–41.
Neves‐Ferreira, A. G., Perales, J., Ovadia, M., Moussatché, H. & Domont, G. B. (1997). Inhibitory properties of the antibothropic complex from the South American opossum (Didelphis marsupialis) serum. Toxicon 35(6), 849–863.
Nicholson, G. M. (2007). Insect‐selective spider toxins targeting voltage‐gated sodium channels. Toxicon 49(4), 490–512.
Nyffeler, M. & Birkhofer, K. (2017). An estimated 400–800 million tons of prey are annually killed by the global spider community. The Science of Nature 104(3), 1–12.
Oliveira, A. L., Viegas, M. F., da Silva, S. L., Soares, A. M., Ramos, M. J. & Fernandes, P. A. (2022). The chemistry of snake venom and its medicinal potential. Nature Reviews Chemistry 6(7), 451–469.
Olivera, B. M. (1999). Conus venom peptides: correlating chemistry and behavior. Journal of Comparative Physiology 185(4), 353359.
Olivera, B. M. (2002). Conus venom peptides: reflections from the biology of clades and species. Annual Review of Ecology and Systematics 33(1), 25–47.
Olivera, B. M., Seger, J., Horvath, M. P. & Fedosov, A. E. (2015). Prey‐capture strategies of fish‐hunting cone snails: behavior, neurobiology and evolution. Brain Behavior and Evolution 86(1), 58–74.
Olivera, B. M., Showers Corneli, P., Watkins, M. & Fedosov, A. (2014). Biodiversity of cone snails and other venomous marine gastropods: evolutionary success through neuropharmacology. Annual Review of Animal Biosciences 2(1), 487–513.
Oukkache, N., Jaoudi, R. E., Ghalim, N., Chgoury, F., Bouhaouala, B., Mdaghri, N. E. & Sabatier, J. M. (2014). Evaluation of the lethal potency of scorpion and snake venoms and comparison between intraperitoneal and intravenous injection routes. Toxins 6(6), 1873–1881.
Pawlak, J., Mackessy, S. P., Fry, B. G., Bhatia, M., Mourier, G., Fruchart‐Gaillard, C., Servent, D., Ménez, R., Stura, E., Ménez, A. & Kini, R. M. (2006). Denmotoxin, a three‐finger toxin from the colubrid snake Boiga dendrophila (Mangrove Catsnake) with bird‐specific activity. Journal of Biological Chemistry 281(39), 29030–29041.
Pawlak, J., Mackessy, S. P., Sixberry, N. M., Stura, E. A., Le Du, M. H., Ménez, R., Foo, C. S., Ménez, A., Nirthanan, S. & Kini, R. M. (2009). Irditoxin, a novel covalently linked heterodimeric three‐finger toxin with high taxon‐specific neurotoxicity. The FASEB Journal 23(2), 534–545.
Pearce, L. B., Borodic, G. E., Johnson, E. A., First, E. R. & Maccallum, R. (1995). The median paralysis unit: a more pharmacologically relevant unit of biologic activity for botulinum toxin. Toxicon 33(2), 217–227.
Peiren, N., Vanrobaeys, F., de Graaf, D. C., Devreese, B., Van Beeumen, J. & Jacobs, F. J. (2005). The protein composition of honeybee venom reconsidered by a proteomic approach. Biochimica et Biophysica Acta (BBA) ‐ Proteins and Proteomics 1752(1), 1–5.
Pekár, S., Bočánek, O., Michálek, O., Petráková, L., Haddad, C. R., Šedo, O. & Zdráhal, Z. (2018a). Venom gland size and venom complexity—essential trophic adaptations of venomous predators: a case study using spiders. Molecular Ecology 27(21), 4257–4269.
Pekár, S., Coddington, J. A. & Blackledge, T. A. (2012a). Evolution of stenophagy in spiders (Araneae): evidence based on the comparative analysis of spider diets. Evolution 66(3), 776–806.
Pekár, S., García, L. F. & Viera, C. (2017). Trophic niches and trophic adaptations of prey‐specialized spiders from the Neotropics: a guide. In Behaviour and Ecology of Spiders: Contributions from the Neotropical Region (eds C. Viera and M. O. Gonzaga), pp. 247–274. Springer, Cham.
Pekár, S., Líznarová, E., Bočánek, O. & Zdráhal, Z. (2018b). Venom of prey‐specialized spiders is more toxic to their preferred prey: a result of prey‐specific toxins. Journal of Animal Ecology 87(6), 1639–1652.
Pekár, S., Ortiz, D., Sentenská, L. & Šedo, O. (2022). Ecological specialization and reproductive isolation among closely related sympatric ant‐eating spiders. Journal of Animal Ecology 91(9), 1855–1868.
Pekár, S., Petráková, L., Šedo, O., Korenko, S. & Zdráhal, Z. (2018c). Trophic niche, capture efficiency and venom profiles of six sympatric ant‐eating spider species (Araneae: Zodariidae). Molecular Ecology 27(4), 1053–1064.
Pekár, S., Šmerda, J., Hrušková, M., Šedo, O., Muster, C., Cardoso, P., Zdráhal, Z., Korenko, S., Bureš, P., Líznarová, E. & Sentenská, L. (2012b). Prey‐race drives differentiation of biotypes in ant‐eating spiders. Journal of Animal Ecology 81(4), 838–848.
Pekár, S. & Toft, S. (2015). Trophic specialisation in a predatory group: the case of prey‐specialised spiders (Araneae). Biological Reviews 90(3), 744–761.
Pekár, S., Wolff, J. O., Černecká, Ľ., Birkhofer, K., Mammola, S., Lowe, E. C., Fukushima, C. S., Herberstein, M. E., Kučera, A., Buzatto, B. A., Djoudi, E. A., Domenech, M., Enciso, A. V., Piñanez Espejo, Y. M. G., Febles, S., et al. (2021). The World Spider Trait database: a centralized global open repository for curated data on spider traits. Database 2021, baab064.
Pennington, M. W., Czerwinski, A. & Norton, R. S. (2018). Peptide therapeutics from venom: current status and potential. Bioorganic & Medicinal Chemistry 26(10), 2738–2758.
Perez, J. C., Haws, W. C. & Hatch, C. H. (1978). Resistance of woodrats (Neotoma micropus) to Crotalus atrox venom. Toxicon 16(2), 198–200.
Phuong, M. A., Mahardika, G. N. & Alfaro, M. E. (2016). Dietary breadth is positively correlated with venom complexity in cone snails. BMC Genomics 17(1), 1–15.
Pineda, S. S., Chaumeil, P. A., Kunert, A., Kaas, Q., Thang, M. W., Le, L., Nuhn, M., Herzig, V., Saez, N., Cristofori‐Armstrong, B., Anangi, R., Senff, S., Gorse, D. & King, G. F. (2018). ArachnoServer 3.0: an online resource for automated discovery, analysis and annotation of spider toxins. Bioinformatics 34(6), 1074–1076.
Pineda, S. S., Chin, Y. K. Y., Undheim, E. A., Senff, S., Mobli, M., Dauly, C., Escoubas, P., Nicholson, G. M., Kaas, Q., Guo, S., Herzig, V., Mattick, J. S. & King, G. F. (2020). Structural venomics reveals evolution of a complex venom by duplication and diversification of an ancient peptide‐encoding gene. Proceedings of the National Academy of Sciences 117(21), 11399–11408.
Pozdnyakov, I., Matantseva, O. & Skarlato, S. (2018). Diversity and evolution of four‐domain voltage‐gated cation channels of eukaryotes and their ancestral functional determinants. Scientific Reports 8(1), 3539.
Prashanth, J. R., Brust, A., Jin, A. H., Alewood, P. F., Dutertre, S. & Lewis, R. J. (2014). Cone snail venomics: from novel biology to novel therapeutics. Future Medicinal Chemistry 6(15), 1659–1675.
Prashanth, J. R., Hasaballah, N. & Vetter, I. (2017). Pharmacological screening technologies for venom peptide discovery. Neuropharmacology 127, 4–19.
Qu, Y., Walker, A. A., Meng, L., Herzig, V. & Li, B. (2023). The predatory stink bug Arma custos (Hemiptera: Pentatomidae) produces a complex proteinaceous venom to overcome caterpillar prey. Biology 12(5), 691.
Rash, L. D. & Hodgson, W. C. (2002). Pharmacology and biochemistry of spider venoms. Toxicon 40(3), 225–254.
Remigio, E. A. & Duda, T. F. Jr. (2008). Evolution of ecological specialization and venom of a predatory marine gastropod. Molecular Ecology 17(4), 1156–1162.
Reyes‐Velasco, J., Card, D. C., Andrew, A. L., Shaney, K. J., Adams, R. H., Schield, D. R., Casewell, N. R., Mackessy, S. P. & Castoe, T. A. (2015). Expression of venom gene homologs in diverse python tissues suggests a new model for the evolution of snake venom. Molecular Biology and Evolution 32(1), 173–183.
Řezáč, M., Pekár, S. & Lubin, Y. (2008). How oniscophagous spiders overcome woodlouse armour. Journal of Zoology 275(1), 64–71.
Richards, D. P., 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(1), 110–116.
Robinson, S. D. & Norton, R. S. (2014). Conotoxin gene superfamilies. Marine Drugs 12(12), 6058–6101.
Robinson, K. E., Holding, M. L., Whitford, M. D., Saviola, A. J., Yates, J. R. III & Clark, R. W. (2021). Phenotypic and functional variation in venom and venom resistance of two sympatric rattlesnakes and their prey. Journal of Evolutionary Biology 34(9), 1447–1465.
Rode‐Margono, J. E. & Nekaris, K. A. I. (2015). Cabinet of curiosities: venom systems and their ecological function in mammals, with a focus on primates. Toxins 7(7), 2639–2658.
Rodrigues, C. F. B., Zdenek, C. N., Serino‐Silva, C., de Morais‐Zani, K., Grego, K. F., Bénard‐Valle, M., Neri‐Castro, E., Alagón, A., Tanaka‐Azevedo, A. M. & Fry, B. G. (2021). BoaγPLI from Boa constrictor blood is a broad‐spectrum inhibitor of venom PLA2 pathophysiological actions. Journal of Chemical Ecology 47(10–11), 907–914.
Rogalski, A., Himaya, S. W. A. & Lewis, R. J. (2023). Coordinated adaptations define the ontogenetic shift from worm‐to fish‐hunting in a venomous cone snail. Nature Communications 14(1), 3287.
Rohou, A., Nield, J. & Ushkaryov, Y. A. (2007). Insecticidal toxins from black widow spider venom. Toxicon 49(4), 531–549.
Rouland‐Lefèvre, C. (2011). Termites as pests of agriculture. In Biology of Termites: A Modern Synthesis (eds D. E. Bignell, Y. Roisin and N. Lo), pp. 499–517. Springer, Dordrecht.
Saez, N. J., Cristofori‐Armstrong, B., Anangi, R. & King, G. F. (2017). A strategy for production of correctly folded disulfide‐rich peptides in the periplasm of E. coli. Methods in Molecular Biology 1586, 155–180.
Safavi‐Hemami, H., Brogan, S. E. & Olivera, B. M. (2019). Pain therapeutics from cone snail venoms: from Ziconotide to novel non‐opioid pathways. Journal of Proteomics 190, 12–20.
Schendel, V., Rash, L. D., Jenner, R. A. & Undheim, E. A. (2019). The diversity of venom: the importance of behavior and venom system morphology in understanding its ecology and evolution. Toxins 11(11), 666.
Schaeffer, R., Pascolutti, V. J., Jackson, T. N. & Arbuckle, K. (2023). Diversity begets diversity when diet drives snake venom evolution, but evenness rather than richness is what counts. Toxins 15(4), 251.
Shaikh, N. Y. & Sunagar, K. (2023). The deep‐rooted origin of disulfide‐rich spider venom toxins. eLife 12, e83761.
Smiley‐Walters, S. A., Farrell, T. M. & Gibbs, H. L. (2018). The importance of species: pygmy rattlesnake venom toxicity differs between native prey and related non‐native species. Toxicon 144, 42–47.
Smith, E. G., Surm, J. M., Macrander, J., Simhi, A., Amir, G., Sachkova, M. Y., Lewandowska, M., Reitzel, A. M. & Moran, Y. (2023). Micro and macroevolution of sea anemone venom phenotype. Nature Communications 14(1), 249.
Sousa, L. F., Zdenek, C. N., Dobson, J. S., Op den Brouw, B., Coimbra, F. C., Gillett, A., Del‐Rei, T. H. M., Chalkidis, H. d. M., Sant'Anna, S., Teixeira‐da‐Rocha, M. M., Grego, K., Travaglia Cardoso, S. R., Moura da Silva, A. M. & Fry, B. G. (2018). Coagulotoxicity of Bothrops (lancehead pit‐vipers) venoms from Brazil: differential biochemistry and antivenom efficacy resulting from prey‐driven venom variation. Toxins 10(10), 411.
Sousa, L. F., Holding, M. L., Del‐Rei, T. H., Rocha, M. M., Mourão, R. H., Chalkidis, H. M., Prezoto, B., Lisle Gibbs, H. & Moura‐da‐Silva, A. M. (2021). Individual variability in Bothrops atrox snakes collected from different habitats in the Brazilian Amazon: new findings on venom composition and functionality. Toxins 13(11), 814.
Su, N.‐Y. & Scheffrahn, R. H. (2000). Termites as pests of buildings. In Termites: Evolution, Sociality, Symbioses, Ecology (eds T. Abe, D. E. Bignell and M. Higashi), pp. 437–453. Springer, Dordrecht.
Sunagar, K. & Moran, Y. (2015). The rise and fall of an evolutionary innovation: contrasting strategies of venom evolution in ancient and young animals. PLoS Genetics 11(10), e1005596.
Torres, J. P., Lin, Z., Watkins, M., Salcedo, P. F., Baskin, R. P., Elhabian, S., Safavi‐Hemami, H., Taylor, D., Tun, J., Conception, G. P., Saguil, N., Yanagihara, A. A., Fang, Y., McArthur, J. R., Tae, H., et al. (2021). Small‐molecule mimicry hunting strategy in the imperial cone snail, Conus imperialis. Science Advances 7(11), eabf2704.
Touchard, A., Aili, S. R., Fox, E. G. P., Escoubas, P., Orivel, J., Nicholson, G. M. & Dejean, A. (2016). The biochemical toxin arsenal from ant venoms. Toxins 8(1), 30.
Utkin, Y. N. (2013). Three‐finger toxins, a deadly weapon of elapid venom–milestones of discovery. Toxicon 62, 50–55.
Valenzuela‐Rojas, J. C., González‐Gómez, J. C., Van der Meijden, A., Cortés, J. N., Guevara, G., Franco, L. M., Pekár, S. & García, L. F. (2019). Prey and venom efficacy of male and female wandering spider, Phoneutria boliviensis (Araneae: Ctenidae). Toxins 11(11), 622.
Van Valen, L. (1973). A new evolutionary law. Evolutionary Theory 1, 1–30.
Verdes, A., Taboada, S., Hamilton, B. R., Undheim, E. A., Sonoda, G. G., Andrade, S. C., Morato, E., Marina, A. I., Cárdenas, C. A. & Riesgo, A. (2022). Evolution, expression patterns, and distribution of novel ribbon worm predatory and defensive toxins. Molecular Biology and Evolution 39(5), msac096.
von Reumont, B. M., Anderluh, G., Antunes, A., Ayvazyan, N., Beis, D., Caliskan, F., Crnković, A., Damm, M., Dutertre, S., Ellgaard, L., Gajski, G., German, H., Halassy, B., Hempel, B.‐F., Hucho, T., et al. (2022). Modern venomics—current insights, novel methods, and future perspectives in biological and applied animal venom research. GigaScience 2022(11), giac048.
Walker, A. A., Hernández‐Vargas, M. J., Corzo, G., Fry, B. G. & King, G. F. (2018a). Giant fish‐killing water bug reveals ancient and dynamic venom evolution in Heteroptera. Cellular and Molecular Life Sciences 75, 3215–3229.
Walker, A. A., Mayhew, M. L., Jin, J., Herzig, V., Undheim, E. A., Sombke, A., Fry, B. G., Merrit, D. J. & King, G. F. (2018b). The assassin bug Pristhesancus plagipennis produces two distinct venoms in separate gland lumens. Nature Communications 9(1), 755.
Walker, A. A., Robinson, S. D., Undheim, E. A., Jin, J., Han, X., Fry, B. G., Vetter, I. & King, G. F. (2019). Missiles of mass disruption: composition and glandular origin of venom used as a projectile defensive weapon by the assassin bug Platymeris rhadamanthus. Toxins 11(11), 673.
Walker, A. A., Robinson, S. D., Yeates, D. K., Jin, J., Baumann, K., Dobson, J., Fry, B. G. & King, G. F. (2018c). Entomo‐venomics: the evolution, biology and biochemistry of insect venoms. Toxicon 154, 15–27.
Walker, A. A., Robinson, S. D., Hamilton, B. F., Undheim, E. A. & King, G. F. (2020). Deadly proteomes: a practical guide to proteotranscriptomics of animal venoms. Proteomics 20(17–18), 1900324.
Williams, D. J., Faiz, M. A., Abela‐Ridder, B., Ainsworth, S., Bulfone, T. C., Nickerson, A. D., Habib, A. G., Junghanss, T., Fan, H. W., Turner, M., Harrison, R. A. & Warrell, D. A. (2019). Strategy for a globally coordinated response to a priority neglected tropical disease: snakebite envenoming. PLoS Neglected Tropical Diseases 13(2), e0007059.
Windley, M. J., Herzig, V., Dziemborowicz, S. A., Hardy, M. C., King, G. F. & Nicholson, G. M. (2012). Spider‐venom peptides as bioinsecticides. Toxins 4(3), 191–227.
Wirsing, A. J., Cameron, K. E. & Heithaus, M. R. (2010). Spatial responses to predators vary with prey escape mode. Animal Behaviour 79(3), 531–537.
World Spider Catalog (2023). World Spider Catalog. Version 24.5. Natural History Museum Bern, online at http://wsc.nmbe.ch, accessed on 12 December 2023.
Wullschleger, B. & Nentwig, W. (2002). Influence of venom availability on a spider's prey‐choice behaviour. Functional Ecology 16(6), 802–807.
Yamada, S. B. & Boulding, E. G. (1998). Claw morphology, prey size selection and foraging efficiency in generalist and specialist shell‐breaking crabs. Journal of Experimental Marine Biology and Ecology 220(2), 191–211.
Yang, S., Liu, Z., Xiao, Y., Li, Y., Rong, M., Liang, S., Zhang, Z., Yu, H., King, G. F. & Lai, R. (2012). Chemical punch packed in venoms makes centipedes excellent predators. Molecular & Cellular Proteomics 11(9), 640–650.
Youngman, N. J., Zdenek, C. N., Dobson, J. S., Bittenbinder, M. A., Gillett, A., Hamilton, B., Dunstan, N., Allen, L., Veary, A., Veary, E. & Fry, B. G. (2019). Mud in the blood: novel potent anticoagulant coagulotoxicity in the venoms of the Australian elapid snake genus Denisonia (mud adders) and relative antivenom efficacy. Toxicology Letters 302, 1–6.
Youngman, N. J., Llinas, J. & Fry, B. G. (2021). Evidence for resistance to coagulotoxic effects of Australian elapid snake venoms by sympatric prey (blue tongue skinks) but not by predators (monitor lizards). Toxins 13(9), 590.
Zhang, R. Y. (2020). Structural Characterization and Biological Potency of Novel Conotoxin MIIIB from Conus Magus. (Doctoral dissertation, University of Hawai'i at Manoa).
Zheng, H., Wang, J., Fan, H., Wang, S., Ye, R., Li, L., Wang, S., Li, A. & Lu, Y. (2023). Comparative venom multi‐omics reveal the molecular mechanisms driving adaptation to diverse predator‐prey ecosystems in closely related sea snakes. Molecular Biology and Evolution 40, msad125.
Zugasti‐Cruz, A., Maillo, M., López‐Vera, E., Falcón, A., de la Cotera, E. P. H., Olivera, B. M. & Aguilar, M. B. (2006). Amino acid sequence and biological activity of a γ‐conotoxin‐like peptide from the worm‐hunting snail Conus austini. Peptides 27(3), 506–511.

101031131 H2020 Marie Skłodowska-Curie Actions

Keywords: adaptation; cone snails; ecology; prey; snakes; specialisation; spiders; venom composition; venom potency

0 (Venoms)

Date Created: 20240711 Date Completed: 20241105 Latest Revision: 20241105

20241105

10.1111/brv.13120

38991997