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Evolution of Signal Diversity: Predator-Prey Interactions and The JYVÄSKYLÄ STUDIES IN BIOLOGICAL AND ENVIRONMENTAL SCIENCE 339 Katja Rönkä Evolution of Signal Diversity: Predator-Prey Interactions and the Maintenance of Warning Colour Polymorphism in the Wood Tiger Moth Arctia plantaginis JYVÄSKYLÄ STUDIES IN BIOLOGICAL AND ENVIRONMENTAL SCIENCE 339 Katja Rönkä Evolution of Signal Diversity: Predator-Prey Interactions and the Maintenance of Warning Colour Polymorphism in the Wood Tiger Moth Arctia plantaginis Esitetään Jyväskylän yliopiston matemaattis-luonnontieteellisen tiedekunnan suostumuksella julkisesti tarkastettavaksi yliopiston vanhassa juhlasalissa S212 joulukuun 16. päivänä 2017 kello 12. Academic dissertation to be publicly discussed, by permission of the Faculty of Mathematics and Science of the University of Jyväskylä, in building Seminarium, auditorium S212, on December 16, 2017 at 12 o’clock noon. UNIVERSITY OF JYVÄSKYLÄ JYVÄSKYLÄ 2017 Evolution of Signal Diversity: Predator-Prey Interactions and the Maintenance of Warning Colour Polymorphism in the Wood Tiger Moth Arctia plantaginis JYVÄSKYLÄ STUDIES IN BIOLOGICAL AND ENVIRONMENTAL SCIENCE 339 Katja Rönkä Evolution of Signal Diversity: Predator-Prey Interactions and the Maintenance of Warning Colour Polymorphism in the Wood Tiger Moth Arctia plantaginis UNIVERSITY OF JYVÄSKYLÄ JYVÄSKYLÄ 2017 Editors Jari Haimi Department of Biological and Environmental Science, University of Jyväskylä Pekka Olsbo, Ville Korkiakangas Publishing Unit, University Library of Jyväskylä Jyväskylä Studies in Biological and Environmental Science Editorial Board Jari Haimi, Anssi Lensu, Timo Marjomäki, Varpu Marjomäki Department of Biological and Environmental Science, University of Jyväskylä Cover drawings by Helena Rönkä. Permanent link to this publication: http://urn.fi/URN:ISBN:978-951-39-7281-3 URN:ISBN:978-951-39-7281-3 ISBN 978-951-39-7281-3 (PDF) ISBN 978-951-39-7280-6 (nid.) ISSN 1456-9701 Copyright © 2017, by University of Jyväskylä Jyväskylä University Printing House, Jyväskylä 2017 “Nothing in biology makes sense except in the light of evolution” - Theodosius Dobzhansky, 1973 “Look deep into nature and then you will understand everything better” - Albert Einstein “ …or not” - Katja Rönkä ABSTRACT Rönkä, Katja Evolution of signal diversity: predator-prey interactions and the maintenance of warning colour polymorphism in the wood tiger moth Arctia plantaginis Jyväskylä: University of Jyväskylä, 2017, 66 p. (Jyväskylä Studies in Biological and Environmental Science ISSN 1456-9701; 339) ISBN 978-951-39-7280-6 (nid.) ISBN 978-951-39-7281-3 (PDF) Yhteenveto: Peto-saalissuhteet ja paikallisen värimuuntelun evoluutio aposemaattisen täpläsiilikkään (Arctia plantaginis) populaatioissa Diss. Aposematic organisms avoid predation by advertising defences with warning signals. The theory of aposematism predicts warning signal uniformity, yet variation in warning coloration is widespread. The chemically defended wood tiger moth Arctia plantaginis shows both geographic variation and local polymorphism in warning coloration. In this thesis, I studied whether predation by local avian predators is driving the evolution of wood tiger moth warning colours. The close relatives of the wood tiger moth designated here to genus Arctia do not show similar colour polymorphism. The wood tiger moth is thus apparently under evolutionary radiation and provides a natural laboratory for observing current selection and studying the mechanisms leading to population divergence. We found evidence of positive frequency-dependent selection as predicted by aposematic theory, but the direction and strength of selection varied geographically. Variation in predator behaviour and the quality and abundance of alternative prey affected selection on wood tiger moth warning colour. Experiments with wild-caught blue tits (Cyanistes caeruleus) and great tits (Parus major) indicate, that colour is of foremost importance in prey discrimination and avoidance generalization. Birds did not generalize their learned avoidance among morphs, but could generalize between vaguely similar prey species showing similar warning colours. I conclude, that a) the evolution of wood tiger moth warning coloration is driven by predation of local avian predators, b) the direction of selection is affected by variation in predator and prey qualities at different levels (from individuals to communities), which can contribute to the maintenance of polymorphism, and that c) the strength of selection can vary spatially and temporally, and be counterbalanced or overruled by other evolutionary processes, promoting variation in warning colour. Keywords: Aposematism; generalization; mimicry; polymorphism; predator- prey interactions; warning signal evolution. Katja Rönkä, University of Jyväskylä, Department of Biological and Environmental Science, P.O. Box 35, FI-40014 University of Jyväskylä, Finland Author’s address Katja Rönkä Department of Biological and Environmental Science P.O. Box 35 FI-40014 University of Jyväskylä Finland [email protected] Supervisors Professor Johanna Mappes Department of Biological and Environmental Science P.O. Box 35 FI-40014 University of Jyväskylä Finland Dr. Bibiana Rojas Department of Biological and Environmental Science P.O. Box 35 FI-40014 University of Jyväskylä Finland Professor Niklas Wahlberg Department of Biology Lund University Sölvegatan 37 223 62 Lund Sweden Reviewers Associate professor Brice Noonan Department of Biology University of Mississippi Post Office Box 1848” University, MS 38677-1848” USA Dr. Mathieu Joron CEFE CNRS UMR 5175 1919 Route de Mende 34293 Montpellier Cedex 5 France Opponent Professor Chris Jiggins Department of Zoology University of Cambridge Downing Street Cambridge CB2 3EJ UK CONTENTS LIST OF ORIGINAL PUBLICATIONS 1 INTRODUCTION ....................................................................................................... 7 1.1 Prelude: Why are not all wood tiger moths red and why is it worth studying? ............................................................................................................ 7 1.2 Selection on warning colour ............................................................................ 9 1.2.1 Predation and aposematism ................................................................. 9 1.2.2 Density- and frequency-dependence ................................................ 12 1.2.3 Mimicry and alternative prey ............................................................ 13 1.2.4 Generalization and the adaptive landscape..................................... 15 1.3 The maintenance of aposematic polymorphism ........................................ 15 1.4 Evolutionary history constraints .................................................................. 18 1.5 Aims of the thesis ........................................................................................... 19 2 METHODS ................................................................................................................. 21 2.1 Study sites ........................................................................................................ 21 2.2 Observing predator and prey communities ............................................... 22 2.3 Sample collection ............................................................................................ 23 2.3.1 Field survey and moth sampling....................................................... 23 2.3.2 Laboratory stock and rearing of moths ............................................ 23 2.4 Molecular methods ......................................................................................... 24 2.5 Experiments with avian predators ............................................................... 25 2.5.1 Artificial moth models ........................................................................ 25 2.5.2 Field predation experiments (II) ........................................................ 26 2.5.3 Laboratory feeding assays (III, IV) .................................................... 27 2.6 Image analysis with avian vision model (IV) ............................................. 28 3 RESULTS AND DISCUSSION ................................................................................ 30 3.1 Putting Parasemia in its phylogenetic place (I) ........................................... 30 3.2 The role of predation in explaining warning colour variation ................ 32 3.2.1 Geographic differences in predation (II) .......................................... 32 3.2.2 Generalization based on colour and potential for mimicry .......... 34 3.2.3 Variable bird responses towards wood tiger moth morphs ......... 37 3.3 Multiple strategies in multi-predator world .............................................. 39 3.4 The spread of a new morph .......................................................................... 42 4 CONCLUSIONS ....................................................................................................... 44 Postscript: so, why are not all wood tiger moths red and does it matter? ......................... 46 Acknowledgements ............................................................................................................ 49 YHTEENVETO (RÉSUMÉ IN FINNISH) .................................................................... 52 REFERENCES .................................................................................................................. 55 LIST OF ORIGINAL PUBLICATIONS The thesis is based on the following original papers, which
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