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The evolution and ecology of multiple antipredator defences

David W. Kikuchi Orcid Logo, William Allen Orcid Logo, Kevin Arbuckle Orcid Logo, Thomas G. Aubier Orcid Logo, Emmanuelle S. Briolat Orcid Logo, Emily R. Burdfield‐Steel, Karen L. Cheney, Klára Daňková, Marianne Elias, Liisa Hämäläinen, Marie E. Herberstein, Thomas J. Hossie, Mathieu Joron, Krushnamegh Kunte Orcid Logo, Brian C. Leavell, Carita Lindstedt, Ugo Lorioux‐Chevalier Orcid Logo, Melanie McClure, Callum F. McLellan, Iliana Medina Orcid Logo, Viraj Nawge, Erika Páez, Arka Pal, Stano Pekár, Olivier Penacchio, Jan Raška Orcid Logo, Tom Reader, Bibiana Rojas Orcid Logo, 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 Orcid Logo, Amanda M. Stefan, Kyle Summers, Christopher H. Taylor Orcid Logo, Rose Thorogood, Kate Umbers, Anne E. Winters, Justin Yeager Orcid Logo, Alice Exnerová Orcid Logo

Journal of Evolutionary Biology, Pages: 1 - 17

Swansea University Authors: William Allen Orcid Logo, Kevin Arbuckle Orcid Logo

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DOI (Published version): 10.1111/jeb.14192

Abstract

Prey seldom rely on a single type of antipredator defence, often using multiple de-fences 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 de-fences to protect itself during a single predator...

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Published in: Journal of Evolutionary Biology
ISSN: 1010-061X 1420-9101
Published: Wiley 2023
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URI: https://cronfa.swan.ac.uk/Record/cronfa63728
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In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple de-fences 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, identifica-tion, 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 comprehen-sive framework for conceptualizing the evolution of multiple prey defences, begin-ning 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 ge-ography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. 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S.</firstname><surname>Briolat</surname><orcid>0000-0001-5695-1065</orcid><order>5</order></author><author><firstname>Emily R.</firstname><surname>Burdfield‐Steel</surname><order>6</order></author><author><firstname>Karen L.</firstname><surname>Cheney</surname><order>7</order></author><author><firstname>Klára</firstname><surname>Daňková</surname><order>8</order></author><author><firstname>Marianne</firstname><surname>Elias</surname><order>9</order></author><author><firstname>Liisa</firstname><surname>Hämäläinen</surname><order>10</order></author><author><firstname>Marie E.</firstname><surname>Herberstein</surname><order>11</order></author><author><firstname>Thomas J.</firstname><surname>Hossie</surname><order>12</order></author><author><firstname>Mathieu</firstname><surname>Joron</surname><order>13</order></author><author><firstname>Krushnamegh</firstname><surname>Kunte</surname><orcid>0000-0002-3860-6118</orcid><order>14</order></author><author><firstname>Brian 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H.</firstname><surname>Rönkä</surname><order>29</order></author><author><firstname>Daniela C.</firstname><surname>Rößler</surname><order>30</order></author><author><firstname>Candy</firstname><surname>Rowe</surname><order>31</order></author><author><firstname>Hannah M.</firstname><surname>Rowland</surname><order>32</order></author><author><firstname>Arlety</firstname><surname>Roy</surname><order>33</order></author><author><firstname>Kaitlin A.</firstname><surname>Schaal</surname><order>34</order></author><author><firstname>Thomas N.</firstname><surname>Sherratt</surname><order>35</order></author><author><firstname>John</firstname><surname>Skelhorn</surname><order>36</order></author><author><firstname>Hannah R.</firstname><surname>Smart</surname><order>37</order></author><author><firstname>Ted</firstname><surname>Stankowich</surname><orcid>0000-0002-6579-7765</orcid><order>38</order></author><author><firstname>Amanda 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spelling v2 63728 2023-06-28 The evolution and ecology of multiple antipredator defences d6f01dd06d25fa8804daad86e251b8a5 0000-0003-2654-0438 William Allen William Allen true false d1775d20b12e430869cc7be5d7d4a27e 0000-0002-9171-5874 Kevin Arbuckle Kevin Arbuckle true false 2023-06-28 SBI Prey seldom rely on a single type of antipredator defence, often using multiple de-fences 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 de-fences 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, identifica-tion, 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 comprehen-sive framework for conceptualizing the evolution of multiple prey defences, begin-ning 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 ge-ography, 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. Journal Article Journal of Evolutionary Biology 1 17 Wiley 1010-061X 1420-9101 antergy, defence portfolio, defence syndrome, intraspecific variation, predation sequence, predator cognition, secondary defences, synergy, trade-offs 1 7 2023 2023-07-01 10.1111/jeb.14192 http://dx.doi.org/10.1111/jeb.14192 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University Another institution paid the OA fee Deutsche Forschungsgemeinschaft Grant/Award Number: 316099922 2023-07-12T15:03:19.1727999 2023-06-28T08:58:50.6297720 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences David W. Kikuchi 0000-0002-7379-2788 1 William Allen 0000-0003-2654-0438 2 Kevin Arbuckle 0000-0002-9171-5874 3 Thomas G. Aubier 0000-0001-8543-5596 4 Emmanuelle S. Briolat 0000-0001-5695-1065 5 Emily R. Burdfield‐Steel 6 Karen L. Cheney 7 Klára Daňková 8 Marianne Elias 9 Liisa Hämäläinen 10 Marie E. Herberstein 11 Thomas J. Hossie 12 Mathieu Joron 13 Krushnamegh Kunte 0000-0002-3860-6118 14 Brian C. Leavell 15 Carita Lindstedt 16 Ugo Lorioux‐Chevalier 0009-0006-1662-8603 17 Melanie McClure 18 Callum F. McLellan 19 Iliana Medina 0000-0002-1021-5035 20 Viraj Nawge 21 Erika Páez 22 Arka Pal 23 Stano Pekár 24 Olivier Penacchio 25 Jan Raška 0000-0003-4768-2507 26 Tom Reader 27 Bibiana Rojas 0000-0002-6715-7294 28 Katja H. Rönkä 29 Daniela C. Rößler 30 Candy Rowe 31 Hannah M. Rowland 32 Arlety Roy 33 Kaitlin A. Schaal 34 Thomas N. Sherratt 35 John Skelhorn 36 Hannah R. Smart 37 Ted Stankowich 0000-0002-6579-7765 38 Amanda M. Stefan 39 Kyle Summers 40 Christopher H. Taylor 0000-0003-4299-7104 41 Rose Thorogood 42 Kate Umbers 43 Anne E. Winters 44 Justin Yeager 0000-0001-8692-6311 45 Alice Exnerová 0000-0001-7937-1477 46 63728__27993__2fd20b16cd174facb97b05e5d659dbd5.pdf Kikuchi et al 2023 The evolution and ecology of multiple antipredator defences.pdf 2023-06-28T09:01:58.6747178 Output 1663674 application/pdf Version of Record true This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. true eng http://creativecommons.org/licenses/by-nc-nd/4.0/
title The evolution and ecology of multiple antipredator defences
spellingShingle The evolution and ecology of multiple antipredator defences
William Allen
Kevin Arbuckle
title_short The evolution and ecology of multiple antipredator defences
title_full The evolution and ecology of multiple antipredator defences
title_fullStr The evolution and ecology of multiple antipredator defences
title_full_unstemmed The evolution and ecology of multiple antipredator defences
title_sort The evolution and ecology of multiple antipredator defences
author_id_str_mv d6f01dd06d25fa8804daad86e251b8a5
d1775d20b12e430869cc7be5d7d4a27e
author_id_fullname_str_mv d6f01dd06d25fa8804daad86e251b8a5_***_William Allen
d1775d20b12e430869cc7be5d7d4a27e_***_Kevin Arbuckle
author William Allen
Kevin Arbuckle
author2 David W. Kikuchi
William 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
format Journal article
container_title Journal of Evolutionary Biology
container_start_page 1
publishDate 2023
institution Swansea University
issn 1010-061X
1420-9101
doi_str_mv 10.1111/jeb.14192
publisher Wiley
college_str Faculty of Science and Engineering
hierarchytype
hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
url http://dx.doi.org/10.1111/jeb.14192
document_store_str 1
active_str 0
description Prey seldom rely on a single type of antipredator defence, often using multiple de-fences 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 de-fences 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, identifica-tion, 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 comprehen-sive framework for conceptualizing the evolution of multiple prey defences, begin-ning 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 ge-ography, 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.
published_date 2023-07-01T15:03:15Z
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score 11.012678

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