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The evolution and ecology of multiple antipredator defences
Authors:David W. Kikuchi  William L. Allen  Kevin Arbuckle  Thomas G. Aubier  Emmanuelle S. Briolat  Emily R. Burdfield-Steel  Karen L. Cheney  Klára Daňková  Marianne Elias  Liisa Hämäläinen  Marie E. Herberstein  Thomas J. Hossie  Mathieu Joron  Krushnamegh Kunte  Brian C. Leavell  Carita Lindstedt  Ugo Lorioux-Chevalier  Melanie McClure  Callum F. McLellan  Iliana Medina  Viraj Nawge  Erika Páez  Arka Pal  Stano Pekár  Olivier Penacchio  Jan Raška  Tom Reader  Bibiana Rojas  Katja H. Rönkä  Daniela C. Rößler  Candy Rowe  Hannah M. Rowland  Arlety Roy  Kaitlin A. Schaal  Thomas N. Sherratt  John Skelhorn  Hannah R. Smart  Ted Stankowich  Amanda M. Stefan  Kyle Summers  Christopher H. Taylor  Rose Thorogood  Kate Umbers  Anne E. Winters  Justin Yeager  Alice Exnerová
Affiliation:1. Department of Integrative Biology, Oregon State University, Corvallis, Oregon, USA;2. Department of Biosciences, Swansea University, Swansea, UK;3. Department of Biology, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA;4. Centre for Ecology and Conservation, University of Exeter, Penryn, UK;5. Institute of Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands;6. School of Biological Sciences, The University of Queensland, St Lucia, Queensland, Australia;7. Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic;8. Institut de Systématique, Evolution, Biodiversité, CNRS, MNHN, Sorbonne Université, EPHE, Université des Antilles, Paris, France

Smithsonian Tropical Research Institute, Gamboa, Panama;9. School of Natural Sciences, Macquarie University, Sydney, New South Wales, Australia;10. Department of Biology, Trent University, Peterborough, Ontario, Canada;11. CEFE, Université de Montpellier, CNRS, EPHE, IRD, Montpellier, France;12. National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bengaluru, India;13. Department of Biological Sciences, Purdue University, West Lafayette, Indiana, USA;14. Department of Forest Sciences, University of Helsinki, Helsinki, Finland;15. Laboratoire Écologie, Évolution, Interactions des Systèmes Amazoniens (LEEISA), Université de Guyane, CNRS, IFREMER, Cayenne, France;16. School of Biological Sciences, University of Bristol, Bristol, UK;17. School of BioSciences, University of Melbourne, Melbourne, Victoria, Australia;18. Institut de Systématique, Evolution, Biodiversité, CNRS, MNHN, Sorbonne Université, EPHE, Université des Antilles, Paris, France;19. Department of Botany and Zoology, Faculty of Science, Masaryk University, Brno, Czech Republic;20. School of Psychology and Neuroscience, University of St Andrews, St Andrews, UK

Computer Vision Center, Computer Science Department, Universitat Autònoma de Barcelona, Barcelona, Spain;21. School of Life Sciences, University of Nottingham, Nottingham, UK;22. Department of Interdisciplinary Life Sciences, Konrad Lorenz Institute of Ethology, University of Veterinary Medicine, Vienna, Austria;23. HiLIFE Helsinki Institute of Life Sciences, University of Helsinki, Helsinki, Finland

Research Programme in Organismal & Evolutionary Biology, Faculty of Biological and Environmental Sciences, University of Helsinki, Helsinki, Finland;24. Zukunftskolleg, University of Konstanz, Konstanz, Germany

Department of Collective Behavior, Max Planck Institute of Animal Behavior, Konstanz, Germany;25. Institute of Biosciences, Faculty of Medical Sciences, Newcastle University, Newcastle upon Tyne, UK;26. Max Planck Research Group Predators and Toxic Prey, Max Planck Institute for Chemical Ecology, Jena, Germany;27. Institute of Integrative Biology, ETH Zurich, Zurich, Switzerland;28. Department of Biology, Carleton University, Ottawa, Ontario, Canada;29. Hawkesbury Institute of the Environment, Western Sydney University, Penrith, New South Wales, Australia;30. Department of Biological Sciences, California State University, Long Beach, California, USA;31. Department of Biology, East Carolina University, Greenville, North Carolina, USA;32. Hawkesbury Institute of the Environment, Western Sydney University, Penrith, New South Wales, Australia

School of Science Western Sydney University, Penrith, New South Wales, Australia;33. Grupo de Biodiversidad Medio Ambiente y Salud, Universidad de Las Américas, Quito, Ecuador

Abstract:Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such “defence portfolios” that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.
Keywords:antergy  defence portfolio  defence syndrome  intraspecific variation  predation sequence  predator cognition  secondary defences  synergy  trade-offs
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