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Venom Use in Mammals: Evolutionary Aspects

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Evolution of Venomous Animals and Their Toxins

Part of the book series: Toxinology ((TOXI))

Abstract

Mammals are recently accepted as venomous animals, with four orders having venomous representatives. These are Eulipotyphla (solenodons and some shrews), Monotremata (platypus), Chiroptera (vampire bats), and Primates (slow and pygmy slow lorises). Each of them has different strategies for using very diverse mixtures of toxic molecules. Venomous saliva is used by eulipotyphlans to paralyze and cache prey, and by chiropterans to avoid blood clotting in suitable prey, allowing continuous feeding. Monotremata use crural spurs to inject a highly painful secretion as a tool in sexual selection, while Primates lick an elbow gland, loading modified teeth with anaphylaxis-inducing venom. There is no homology between venomous systems in these different orders, making a common origin for all venom in Mammalia unlikely, even considering gaps in the fossil record. An emerging picture of complex interactions between cost of venom producing, specialized teeth for feeding and possible lack of benefits for venom in larger, stronger mammals may be able to justify the rarity of venom in this group. Both basic science and biotechnology are benefited as more knowledge accumulates about mammalian venoms.

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References

  • Aminetzach YT, Srouji JR, Kong CY, Hoekstra HE. Convergent evolution of novel protein function in shrew and lizard venom. Curr Biol. 2009;19(22):1925–31.

    Article  CAS  PubMed  Google Scholar 

  • Brodie 3rd ED. Toxins and venoms. Curr Biol. 2009;19(20):R931–5.

    Article  CAS  PubMed  Google Scholar 

  • Calvete JJ. Venomics: digging into the evolution of venomous systems and learning to twist nature to fight pathology. J Proteome. 2009;72(2):121–6.

    Article  CAS  Google Scholar 

  • Cuenca-Bescós G, Rofes J. First evidence of poisonous shrews with an envenomation apparatus. Naturwissenschaften. 2007;94(2):113–6.

    Article  PubMed  Google Scholar 

  • Delpietro HA, Russo RG. Acquired resistance to saliva anticoagulants by prey previously fed upon by vampire bats (Desmodus rotundus): evidence for immune response. J Mammal. 2009;90:1132–8.

    Article  Google Scholar 

  • Dufton MJ. Venomous mammals. Pharmacol Ther. 1992;53(2):199–215.

    Article  CAS  PubMed  Google Scholar 

  • Folinsbee KE. Evolution of venom across extant and extinct eulipotyphlans. C R Palevol. 2013;12(7–8):531–42.

    Article  Google Scholar 

  • Folinsbee KE, Müller J, Reisz RR. Canine grooves: morphology, function, and relevance to venom. J Vertebr Paleontol. 2007;27:547–51.

    Article  Google Scholar 

  • Fox RC, Scott CS. First evidence of a venom delivery apparatus in extinct mammals. Nature. 2005;435:1091–3.

    Article  CAS  PubMed  Google Scholar 

  • Francischetti IM, Assumpção TC, Ma D, Li Y, Vicente EC, Uieda W, Ribeiro JM. The “Vampirome”: transcriptome and proteome analysis of the principal and accessory submaxillary glands of the vampire bat Desmodus rotundus, a vector of human rabies. J Proteome. 2013;82:288–319.

    Article  CAS  Google Scholar 

  • Fry BG, Roelants K, Champagne DE, Scheib H, Tyndall JD, King GF, Nevalainen TJ, Norman JA, Lewis RJ, Norton RS, Renjifo C, de la Vega RC. The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet. 2009;10:483–511.

    Article  CAS  PubMed  Google Scholar 

  • Furió M, Agustí J, Mouskhelishvili A, Sanisidro Ó, Santos-Cubedo A. The paleobiology of the extinct venomous shrew Beremendia (Soricidae, Insectivora, Mammalia) in relation to the geology and paleoenvironment of Dmanisi (Early Pleistocene, Georgia). J Vertebr Paleontol. 2010;30:928–42.

    Article  Google Scholar 

  • Grant TR, Temple-Smith PD. Field biology of the platypus (Ornithorhynchus anatinus): historical and current perspectives. Philos Trans R Soc Lond B Biol Sci. 1998;353(1372):1081–91.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grow NB, Wirdateti NB, Nekaris KA. Does toxic defence in Nycticebus spp. relate to ectoparasites? The lethal effects of slow loris venom on arthropods. Toxicon. 2015;95:1–5.

    Article  CAS  PubMed  Google Scholar 

  • Hagey LR, Fry BG, Fitch-Snyder H. Talking defensively: a dual use for the brachial gland exudate of slow and pygmy lorises. In: Gurski S, Nekaris KAI, editors. Primate anti-predatory strategies, vol. 2. New York: Springer; 2007. p. 253–72.

    Chapter  Google Scholar 

  • Harris RJ, Arbuckle K. Tempo and mode of the evolution of venom and poison in tetrapods. Toxins. 2016;8(7):193.

    Article  PubMed Central  Google Scholar 

  • Hurum JH, Luo Z-X, Kielan-Jaworowska Z. Were mammals originally venomous? Acta Palaeontol Pol. 2006;51:1–11.

    Google Scholar 

  • Kaiser L, Velickovic TC, Badia-Martinez D, Adedoyin J, Thunberg S, Hallén D, Berndt K, Grönlund H, Gafvelin G, van Hage M, Achour A. Structural characterization of the tetrameric form of the major cat allergen Fel d 1. J Mol Biol. 2007;370(4):714–27.

    Article  CAS  PubMed  Google Scholar 

  • Kielan-Jaworowska Z, Hurum JH. Limb posture in early mammals: sprawling or parasagittal. Acta Palaeontol Pol. 2006;51:393–406.

    Google Scholar 

  • Kita M, Nakamura Y, Okumura Y, Ohdachi SD, Oba Y, Yoshikuni M, Kido H, Uemura D. Blarina toxin, a mammalian lethal venom from the short-tailed shrew Blarina brevicauda: isolation and characterization. Proc Natl Acad Sci U S A. 2004;101(20):7542–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krane S, Itagaki Y, Nakanishi K, Weldon PJ. “Venom” of the slow loris: sequence similarity of prosimian skin gland protein and Fel d 1 cat allergen. Naturwissenschaften. 2003;90(2):60–2.

    CAS  PubMed  Google Scholar 

  • Krause WJ. Morphological and histochemical observations on the crural gland-spur apparatus of the echidna (Tachyglossus aculeatus) together with comparative observations on the femoral gland-spur apparatus of the duckbilled platypus (Ornithorhyncus anatinus). Cells Tissues Organs. 2009;191:336–54.

    Article  PubMed  Google Scholar 

  • Law RH, Caradoc-Davies T, Cowieson N, Horvath AJ, Quek AJ, Encarnacao JA, Steer D, Cowan A, Zhang Q, Lu BG, Pike RN, Smith AI, Coughlin PB, Whisstock JC. The X-ray crystal structure of full-length human plasminogen. Cell Rep. 2012;1(3):185–90.

    Article  CAS  PubMed  Google Scholar 

  • Lawrence B. Brief comparison of short-tailed shrew and reptile poisons. J Mammal. 1945;26:393–6.

    Article  CAS  PubMed  Google Scholar 

  • Ligabue-Braun R, Carlini CR. Poisonous birds: a timely review. Toxicon. 2015;99:102–8.

    Article  CAS  PubMed  Google Scholar 

  • Ligabue-Braun R, Verli H, Carlini CR. Venomous mammals: a review. Toxicon. 2012;59(7–8):680–95.

    Article  CAS  PubMed  Google Scholar 

  • Ligabue-Braun R, Sachett LG, Pol-Fachin L, Verli H. The calcium goes meow: effects of ions and glycosylation on Fel d 1, the major cat allergen. PLoS One. 2015;10(7):e0132311.

    Article  PubMed  PubMed Central  Google Scholar 

  • Low DH, Sunagar K, Undheim EA, Ali SA, Alagon AC, Ruder T, Jackson TN, Pineda Gonzalez S, King GF, Jones A, Antunes A, Fry BG. Dracula’s children: molecular evolution of vampire bat venom. J Proteome. 2013;89:95–111.

    Article  CAS  Google Scholar 

  • Ma D, Mizurini DM, Assumpção TC, Li Y, Qi Y, Kotsyfakis M, Ribeiro JM, Monteiro RQ, Francischetti IM. Desmolaris, a novel factor XIa anticoagulant from the salivary gland of the vampire bat (Desmodus rotundus) inhibits inflammation and thrombosis in vivo. Blood. 2013;122(25):4094–106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Madani G, Nekaris KA. Anaphylactic shock following the bite of a wild Kayan slow loris (Nycticebus kayan): implications for slow loris conservation. J Venomous Anim Toxins Incl Trop Dis. 2014;20(1):43.

    Article  Google Scholar 

  • Ménez R, Michel S, Muller BH, Bossus M, Ducancel F, Jolivet-Reynaud C, Stura EA. Crystal structure of a ternary complex between human prostate-specific antigen, its substrate acyl intermediate and an activating antibody. J Mol Biol. 2008;376(4):1021–33.

    Article  PubMed  Google Scholar 

  • Morgenstern D, King GF. The venom optimization hypothesis revisited. Toxicon. 2013;63:120–8.

    Article  CAS  PubMed  Google Scholar 

  • Nekaris KA, Moore RS, Rode EJ, Fry BG. Mad, bad and dangerous to know: the biochemistry, ecology and evolution of slow loris venom. J Venomous Anim Toxins Incl Trop Dis. 2013;19(1):21.

    Article  Google Scholar 

  • Orr CM, Delezene LK, Scott JM, Tocheri MW, Schwartz GT. The comparative method and the inference of venom-delivery systems in fossil mammals. J Vertebr Paleontol. 2007;27:541–6.

    Article  Google Scholar 

  • Rode-Margono JE, Nekaris KA. Cabinet of curiosities: venom systems and their ecological function in mammals, with a focus on primates. Toxins. 2015;7(7):2639–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schondube JE, Herrera-M LG, Martínez del Rio C. Diet and the evolution of digestion and renal function in phyllostomid bats. Zoology. 2001;104:59–73.

    Article  CAS  PubMed  Google Scholar 

  • Springer MS, Stanhope MJ, Madsen O, de Jong WW. Molecules consolidate the placental mammal tree. Trends Ecol Evol. 2004;19(8):430–8.

    Article  PubMed  Google Scholar 

  • Tellgren-Roth A, Dittmar K, Massey SE, Kemi C, Tellgren-Roth C, Savolainen P, Lyons LA, Liberles DA. Keeping the blood flowing-plasminogen activator genes and feeding behavior in vampire bats. Naturwissenschaften. 2009;96(1):39–47.

    Article  CAS  PubMed  Google Scholar 

  • Torres AM, Tsampazi C, Geraghty DP, Bansal PS, Alewood PF, Kuchel PW. D-amino acid residue in a defensin-like peptide from platypus venom: effect on structure and chromatographic properties. Biochem J. 2005;391(Pt 2):215–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warren WC, Hillier LW, Marshall Graves JA, Birney E, Ponting CP, Grützner F, Belov K, Miller W, Clarke L, Chinwalla AT, Yang SP, Heger A, Locke DP, Miethke P, Waters PD, et al. Genome analysis of the platypus reveals unique signatures of evolution. Nature. 2008;453(7192):175–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whittington CM, Belov K. Platypus venom: a review. Aust Mammal. 2007;29:57–62.

    Article  Google Scholar 

  • Whittington CM, Belov K. Platypus venom genes expressed in non-venom tissues. Aust J Zool. 2009;57:199–202.

    Article  Google Scholar 

  • Whittington CM, Belov K. The platypus: a venomous mammal. In: Gopalakrishnakone P, Calvete JJ, editors. Venom genomics and proteomics. New York: Springer; 2016. p. 169–83.

    Chapter  Google Scholar 

  • Whittington CM, Papenfuss AT, Bansal P, Torres AM, Wong ES, Deakin JE, Graves T, Alsop A, Schatzkamer K, Kremitzki C, Ponting CP, Temple-Smith P, Warren WC, Kuchel PW, Belov K. Defensins and the convergent evolution of platypus and reptile venom genes. Genome Res. 2008;18:986–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whittington CM, Papenfuss AT, Locke DP, Mardis ER, Wilson RK, Abubucker S, Mitreva M, Wong ES, Hsu AL, Kuchel PW, Belov K, Warren WC. Novel venom gene discovery in the platypus. Genome Biol. 2010;11:R95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Graduate Program in Cellular and Molecular Biology, Center for Biotechnology, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves, 9500 Prédio 43421/43431, Setor IV, Campus do Vale, 91501-970, Porto Alegre, Rio Grande do Sul, Brazil

    Rodrigo Ligabue-Braun

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  1. Rodrigo Ligabue-Braun
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Correspondence to Rodrigo Ligabue-Braun .

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Editors and Affiliations

  1. School of Biological Sciences, Bangor University, Bangor, Gwynedd, United Kingdom

    Anita Malhotra

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Ligabue-Braun, R. (2017). Venom Use in Mammals: Evolutionary Aspects. In: Malhotra, A. (eds) Evolution of Venomous Animals and Their Toxins. Toxinology. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6458-3_20

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