Host Manipulation by Parasites This page intentionally left blank Host Manipulation by Parasites EDITED BY David P. Hughes Department of Entomology and Biology, Penn State University, USA J acques B rodeur Department of Biological Sciences, University of Montreal, Canada F rédéric T homas Centre National de la Recherche Scientifi que (CNRS) and Institut de Recherche pour le Développement (IRD), France 1 3 Great Clarendon Street, Oxford OX2 6DP, United Kingdom Oxford University Press is a department of the University of Oxford. It furthers the University’s objective of excellence in research, scholarship, and education by publishing worldwide. Oxford is a registered trade mark of Oxford University Press in the UK and in certain other countries © Oxford University Press 2012 The moral rights of the authors have been asserted First Edition published in 2012 Impression: 1 All rights reserved. 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Contents List of contributors ix Foreword xi Richard Dawkins 1 A history of parasites and hosts, science and fashion 1 Janice Moore 1.1 Introduction 1 1.2 The days before cool 1 1.3 Becoming cool 6 1.4 Beyond manipulation 9 1.5 Conclusion 10 Afterword 14 John Alcock 2 E volutionary routes leading to host manipulation by parasites 16 Frédéric Thomas , Thierry Rigaud , and Jacques Brodeur 2.1 Introduction 16 2.2 The origins of host manipulation 16 2.2.1 Manipulation s ensu stricto 16 2.2.2 Complex parasitic cycles: the cause or the consequence of parasite manipulation? 17 2.2.3 Host-driven scenarios of manipulation 17 2.2.4 Exaptation? 20 2.3 The evolution of manipulation after its emergence 20 2.3.1 Genetically based variation in phenotypic alterations 21 2.3.2 Other sources of variation 22 2.4 Multidimensional manipulations: evidence of evolution or a syndrome? 27 2.4.1 Why do multidimensional manipulations evolve? 27 2.4.2 Simultaneous versus sequential multidimensional manipulations 27 2.4.3 How did multidimensional manipulations evolve? 28 2.4.4 Proximate aspects of multidimensionality 29 2.5 Concluding remarks 29 Afterword 34 Stephen C. Stearns v vi CONTENTS 3 T he strings of the puppet master: how parasites change host behavior 36 Shelley A. Adamo 3.1 Introduction 36 3.2 How do parasites alter host behavior? Vertebrate examples 36 3.2.1 Toxoplasma gondii 36 3.2.2 Neuroviruses 41 3.3 Invertebrate examples 41 3.3.1 Gammarids—don’t go into the light! 42 3.3.2 Suicidal crickets 43 3.4 How might parasites manipulate host behavior? 45 3.5 How can parasitic infections produce specifi c changes in host behavior without neuroanatomical specifi city? 46 Afterword 52 Gene Robinson 4 P arasites discover behavioral ecology: how to manage one’s host in a complex world 54 Bernard D. Roitberg 4.1 Introduction 54 4.2 The problem 55 4.2.1 A healthy caterpillar 56 4.2.2 A parasitized caterpillar 61 4.3 Discussion 67 Afterword 71 Frédérique Dubois 5 M anipulation of plant phenotypes by insects and insect-borne pathogens 73 Mark C. Mescher 5.1 Introduction 73 5.2 Plant manipulation by insect herbivores 74 5.2.1 Gall-inducing insects 75 5.2.2 Structural modifi cation of host plants 78 5.2.3 Green islands 80 5.2.4 Manipulation of phytohormones 81 5.3 Plant manipulation by insect-borne pathogens 82 5.3.1 Manipulation of plant–pollinator interactions by fungal parasites 82 5.3.2 Pathogen manipulation of plant–herbivore interactions 85 5.4 Conclusion 86 Afterword 93 Pedro Jordano 6 V isual trickery in avian brood parasites 95 Naomi E. Langmore and Claire N. Spottiswoode 6.1 Introduction 95 6.2 Accessing host nests 96 CONTENTS vii 6.3 The egg stage 96 6.4 The nestling stage 104 6.5 Visual trickery to elicit parental care 107 6.6 Mimicry in generalist versus specialist parasites 109 6.7 Conclusions 110 Afterword 116 Scott V. Edwards 7 Endosymbiotic microbes as adaptive manipulators of arthropod behavior and natural driving sources of host speciation 119 Wolfgang J. Miller and Daniela Schneider 7.1 Introduction 119 7.2 Wolbachia : the multidimensional manipulator of arthropods 119 7.2.1 Reproductive parasitism triggered by W olbachia 121 7.2.2 Wolbachia ´s repertoire of inducing non-reproductive, adaptive phenotypes 123 7.3 Symbiont-directed adaptive manipulation of host sexual behavior 124 7.3.1 Feminization—the transformation of genetic males into functional females 124 7.3.2 Manipulating sexual mating behavior 127 7.4 Conclusions 131 Afterword 138 Lee Ehrman 8 P arasites and the superorganism 140 David P. Hughes 8.1 Introduction 140 8.2 The extended phenotype and the unitary organism 140 8.3 The behavior of social insects 141 8.4 Behavior of the superorganism 143 8.5 Parasites divide the interests of superorganism 144 8.6 Behaviorally modifying parasites of social insects 144 8.7 Manipulating the whole colony 147 8.7.1 Parasitizing social resources 147 8.7.2 Cheating the mutualism 147 8.7.3 Panicking the crowd 148 8.7.4 Shifting foraging ecology 149 8.8 Future directions and tests 150 Afterword 155 Bert Hölldobler 9 E cological consequences of manipulative parasites 158 Kevin D. Lafferty and Armand M. Kuris 9.1 Introduction 158 9.2 What makes a manipulator important ecologically? 159 viii CONTENTS 9.3 Parasitic castrators and parasitoids as host behavior manipulators 160 9.3.1 Nematomorphs, endangered charr, and crickets in Japanese streams 161 9.4 Trophically transmitted parasites as host behavior manipulators 162 9.4.1 Tapeworms, wolves, moose, and forests on Isle Royale 162 9.4.2 Trematodes, cockles, limpets and anemones in New Zealand mudfl ats 164 9.5 The ecological reach of host behavior manipulators 165 9.6 Testing for the ecological effects of manipulative parasites 165 9.7 Conclusions 166 Afterword 169 Michel Loreau 10 A pplied aspects of host manipulation by parasites 172 Robert Poulin and Edward P. Levri 10.1 Introduction 172 10.2 Manipulative parasites, biological invasions, and conservation 172 10.3 Manipulative parasites in agriculture and aquaculture 175 10.4 Parasite manipulation of disease vectors 177 10.4.1 Leishmaniasis 179 10.4.2 African sleeping sickness 180 10.4.3 Malaria 180 10.5 Parasite manipulation in humans: the case of Toxoplasma gondii 181 10.6 Conclusion 187 Afterword 195 Andrew Read and Victoria Braithwaite 11 B ehavioral manipulation outside the world of parasites 1 98 Frank Cézilly and Frédéric Thomas 11.1 Introduction 198 11.2 A categorization of manipulation 198 11.2.1 Deceit through sensory exploitation 199 11.2.2 Exploitation of compensatory mechanisms 200 11.2.3 Coercive exploitation 201 11.2.4 Manipulation of information 202 11.2.5 Neuroendocrine manipulation 204 11.3 A brief critique of the “manipulation” concept 205 11.4 Manipulation inside and outside the world of parasites: convergence and divergence 205 Afterword 213 Alex Kacelnik Index 215 List of contributors Shelley A. Adamo , Department of Psychology/ Bert Hölldobler , School of Life Sciences, Arizona State Neuroscience Institute, Dalhousie University, University, PO Box 874501, Tempe, AZ 85287, USA Halifax, NS, B3H 3X5, Canada and University of Würzburg, Biozentrum, Zoologie [email protected] II, Am Hubland, D-97074 Würzburg, Germany John Alcock , School of Life Sciences, PO Box 874501, [email protected] Arizona State University, Tempe, AZ 85287-4501, David P. Hughes , Centre for Infectious Disease USA Dynamics, MSC, University Park, Penn State [email protected] University, PA 16802, USA Victoria Braithwaite , School of Forest Resources, [email protected] University Park, Penn State University, PA 16802, Pedro Jordano , Integrative Ecology Group, Estación USA Biológica de Doñana, CSIC, Sevilla, Spain [email protected] [email protected] Jacques Brodeur , Département de Sciences Alex Kacelnik , Behavioural Ecology Research Biologiques, Université de Montréal, 4101, rue Group, Department of Zoology, Oxford Sherbrooke Est, Montréal (Québec), H1X 2B2, University, Oxford, OX1 3PS, UK Canada [email protected] [email protected] Armand M. Kuris , Ecology, Evolution & Marine Frank Cézilly , Université de Bourgogne, Equipe Biology, University of California, Santa Barbara, Ecologie Evolutive, UMR CNRS 5561 Biogéo- Santa Barbara, CA 93106-9620, USA sciences, 6 blvd. Gabriel, 21000 Dijon, France [email protected] [email protected] Kevin D. Lafferty , United States Geological Survey, Richard Dawkins , New College, University of Western Ecological Research Center and Marine Oxford, Oxford, UK. Science Institute, University of California, Santa [email protected] Barbara, California 93106, USA Frédérique Dubois , Université de Montréal, [email protected] Département de Sciences Biologiques, CP 6128, Naomi E. Langmore , Research School of Biology, Succursale Centre-ville, Montréal (Québec), H3C Australian National University, Canberra 0200, 3J7, Canada Australia [email protected] [email protected] Scott V. Edwards , Department of Organismic and Edward P. Levri , Department of Biology, Penn State Evolutionary Biology, Harvard University, 26 Altoona, 3000 Ivyside Park, Altoona, PA 16601, Oxford Street, Cambridge, MA 02138, USA USA [email protected] [email protected] Lee Ehrman , Natural Sciences, State University of Michel Loreau , McGill University, Department of New York, Purchase College, Purchase, New Biology, 1205 ave Docteur Penfi eld, Montréal York, USA (Québec), H3A 1B1, Canada [email protected] [email protected] ix