Venom exaptation and adaptation during the trophic switch to blood-feeding by kissing bugs
Christina N. Zdenek,
Fernanda C. Cardoso,
Samuel D. Robinson,
Raine S. Mercedes,
Enriko R. Raidjõe,
María José Hernandez-Vargas,
Jiayi Jin,
Gerardo Corzo,
Irina Vetter,
Glenn F. King,
Bryan G. Fry,
Andrew A. Walker
Affiliations
Christina N. Zdenek
Corresponding author; Australian Reptile Academy, Whiterock, QLD 4306, Australia; Venom Evolution Lab, School of the Environment, The University of Queensland, St. Lucia, QLD 4072, Australia; Institute for Molecular Bioscience, The University of Queensland, St Lucia, QLD 4072, Australia; Australian Research Council Centre of Excellence for Innovations in Peptide and Protein Science, The University of Queensland, St. Lucia, QLD 4072, Australia; University of Tartu, 50090 Tartu, Estonia; Departamento de Medicina Molecular y Bioprocesos, Instituto de Biotecnologia, Universidad Nacional Autónoma de México, Apartado Postal 510-3, Cuernavaca 62210, Morelos, Mexico; School of Pharmacy, The University of Queensland, Woolloongabba, QLD 4102, Australia
Fernanda C. Cardoso
Institute for Molecular Bioscience, The University of Queensland, St Lucia, QLD 4072, Australia; Australian Research Council Centre of Excellence for Innovations in Peptide and Protein Science, The University of Queensland, St. Lucia, QLD 4072, Australia
Samuel D. Robinson
Institute for Molecular Bioscience, The University of Queensland, St Lucia, QLD 4072, Australia
Raine S. Mercedes
Institute for Molecular Bioscience, The University of Queensland, St Lucia, QLD 4072, Australia; Australian Research Council Centre of Excellence for Innovations in Peptide and Protein Science, The University of Queensland, St. Lucia, QLD 4072, Australia
Enriko R. Raidjõe
University of Tartu, 50090 Tartu, Estonia
María José Hernandez-Vargas
Departamento de Medicina Molecular y Bioprocesos, Instituto de Biotecnologia, Universidad Nacional Autónoma de México, Apartado Postal 510-3, Cuernavaca 62210, Morelos, Mexico
Jiayi Jin
Institute for Molecular Bioscience, The University of Queensland, St Lucia, QLD 4072, Australia
Gerardo Corzo
Departamento de Medicina Molecular y Bioprocesos, Instituto de Biotecnologia, Universidad Nacional Autónoma de México, Apartado Postal 510-3, Cuernavaca 62210, Morelos, Mexico
Irina Vetter
Institute for Molecular Bioscience, The University of Queensland, St Lucia, QLD 4072, Australia; School of Pharmacy, The University of Queensland, Woolloongabba, QLD 4102, Australia
Glenn F. King
Institute for Molecular Bioscience, The University of Queensland, St Lucia, QLD 4072, Australia; Australian Research Council Centre of Excellence for Innovations in Peptide and Protein Science, The University of Queensland, St. Lucia, QLD 4072, Australia
Bryan G. Fry
Venom Evolution Lab, School of the Environment, The University of Queensland, St. Lucia, QLD 4072, Australia
Andrew A. Walker
Institute for Molecular Bioscience, The University of Queensland, St Lucia, QLD 4072, Australia; Australian Research Council Centre of Excellence for Innovations in Peptide and Protein Science, The University of Queensland, St. Lucia, QLD 4072, Australia; Corresponding author
Summary: Kissing bugs are known to produce anticoagulant venom that facilitates blood-feeding. However, it is unknown how this saliva evolved and if the venom produced by the entomophagous ancestors of kissing bugs would have helped or hindered the trophic shift. In this study, we show that venoms produced by extant predatory assassin bugs have strong anticoagulant properties mediated chiefly by proteolytic degradation of fibrinogen, and additionally contain anticoagulant disulfide-rich peptides. However, venom produced by predatory species also has pain-inducing and membrane-permeabilizing activities that would be maladaptive for blood-feeding, and which venom of the blood-feeding species lack. This study demonstrates that venom produced by the predatory ancestors of kissing bugs was exapted for the trophic switch to blood-feeding by virtue of its anticoagulant properties. Further adaptation to blood-feeding occurred by downregulation of venom toxins with proteolytic, cytolytic, and pain-inducing activities, and upregulation and neofunctionalization of toxins with anticoagulant activity independent of proteolysis.
