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Evolution of Cooperation in Ambrosia Beetles

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Evolution of Cooperation in Ambrosia Beetles Evolution of Cooperation in Ambrosia Beetles Inauguraldissertation der Philosophisch-naturwissenschaftlichen Fakultät der Universität Bern vorgelegt von Peter Hans Wilhelm Biedermann von Trofaiach / Österreich Leiter der Arbeit: Prof. Dr. Michael Taborsky Institut für Ökologie und Evolution Abteilung Verhaltensökologie Universität Bern Evolution of Cooperation in Ambrosia Beetles Inauguraldissertation der Philosophisch-naturwissenschaftlichen Fakultät der Universität Bern vorgelegt von Peter Hans Wilhelm Biedermann von Trofaiach / Österreich Leiter der Arbeit: Prof. Dr. Michael Taborsky Institut für Ökologie und Evolution Abteilung Verhaltensökologie Universität Bern Von der Philosophisch-naturwissenschaftlichen Fakultät angenommen. Der Dekan: Bern, 20. März 2012 Prof. Dr. Silvio Decurtins Supervised by: Prof. Dr. Michael Taborsky Department of Behavioural Ecology Institute of Ecology and Evolution University of Bern Wohlenstrasse 50a CH-3032 Hinterkappelen Switzerland Reviewed by: Prof. Dr. Jacobus J. Boomsma Section for Ecology and Evolution Institute of Biology University of Copenhagen Universitetsparken 15 2100 Copenhagen Denmark Examined by: Prof. Dr. Heinz Richner, University of Bern (Chair) Prof. Dr. Michael Taborsky, University of Bern Prof. Dr. Jacobus J. Boosma, University of Copenhagen Copyright Chapter 1 © PNAS 2011 by the National Academy of Sciences of the United States of America, Washington, USA Chapter 2 © Mitt. Dtsch. Ges. allg. angew. Ent. 2011 by the DGaaE, Müncheberg, Gernany Chapter 4 © Zookeys 2010 by Pensoft Publishers, Sofia, Bulgaria Chapter 5 © Behav. Ecol. & Sociobiol. by Springer-Verlag GmbH, Heidelberg, Germany Chapter 9 © J. Bacteriol. by the American Society for Microbiology, Washington, USA General Introduction, Chapter 3, 6, 7, 8, Appendix 1,2, and Summary & Conclusion © Peter H.W. Biedermann Cover drawing © by Barrett Anthony Klein, Entomoartist, Department of Biology, University of Konstanz, Germany. http://www.pupating.org Layout by Peter H. W. Biedermann Printed in Bern, Switzerland by Kopierzentrale der Universität Bern Für meine Eltern die meine Begeisterung für die Natur erkannt haben Für Tabea die mich bedingungslos unterstützt Und Helene Francke-Grosmann, Karl E. Schedl, Dale M. Norris und Richard A. Roeper für ihre Pionierarbeiten auf dem Gebiet der Ambrosiakäfer-Forschung “There is grandeur in this view of life, with its several powers, having been originally breathed into a few forms or into one; and that, whilst this planet has gone cycling on according to the fixed law of gravity, from so simple a beginning endless forms most beautiful and most wonderful have been, and are being, evolved.” C. Darwin, Origin of Species 1859 “Ich habe ihm nun geraten, künftig in der Natur nie einen einzelnen Gegenstand alleine herauszuzeichnen, nie einen einzelnen Baum, einen einzelnen Steinhaufen, eine einzelne Hütte, sondern immer zugleich einigen Hintergrund und einige Umgebung mit. Und zwar aus folgenden Ursachen: Wir sehen in der Natur nie etwas als Einzelheit, sondern wir sehen alles in Verbindung mit etwas anderem, das vor ihm, neben ihm, hinter ihm, unter ihm und über ihm sich befindet. Auch fällt uns wohl ein einzelner Gegenstand als besonders schön und malerisch auf; es ist aber nicht der Gegenstand allein, der diese Wirkung hervorbringt, sondern es ist die Verbindung, in der wir ihn sehen.“ Johann Wolfgang von Goethe, zu Eckermann, 5. Juni 1826 Contents 3 General Introduction 11 Chapter 1 Biedermann PHW and M Taborsky (2011): Larval helpers and age polyethism in ambrosia beetles. Proceedings of the National Academy of Science, USA 108(41): 17064-17069. 27 Chapter 2 Biedermann PHW, K Peer and M Taborsky (2011) Female dispersal and reproduction in the ambrosia beetle Xyleborinus saxesenii Ratzeburg (Coleoptera; Scolytinae). Mitteilungen der deutschen Gesellschaft für allgemeine und angewandte Entomologie 18: in press. 33 Chapter 3 Biedermann PHW and M Taborsky (manuscript in work) Responses to artificial selection on dispersal in a primitively eusocial beetle. 53 Chapter 4 Biedermann PHW (2010) Observations on sex ratio and behavior of males in Xyleborinus saxesenii Ratzeburg (Scolytinae, Coleoptera). In: Cognato AI, Knížek M (Eds) Sixty years of discovering scolytine and platypodine diversity: A tribute to Stephen L. Wood. Zookeys 56: 253-267. 69 Chapter 5 Biedermann PHW, KD Klepzig and M Taborsky (2011) Costs of delayed dispersal and alloparental care in the fungus-cultivating ambrosia beetle Xyleborus affinis Eichhoff (Scolytinae: Curculionidae). Behavioral Ecology and Sociobiology 65:1753–1761. 79 Chapter 6 Biedermann PHW and M Taborsky (manuscript in work) Social fungus farming varies among ambrosia beetles. 101 Chapter 7 Biedermann PHW, KD Klepzig, M Taborsky and DL Six (manuscript in work) Dynamics of filamentous fungi in the complex ambrosia gardens of the primitively eusocial beetle Xyleborinus saxesenii Ratzeburg (Scolytinae; Curculionidae). 123 Chapter 8 De Fine Licht HH and PHW Biedermann (in review) Patterns of functional enzyme activity show that larvae are the key to successful fungus farming by ambrosia beetles. Frontiers in Zoology, submitted 143 Chapter 9 Grubbs KJ, Biedermann PHW, Suen G, Adams SM, Moeller JA, Klassen JL, Goodwinm LA, Woyke T, Munk AC, Bruce D, Detter C, Tapia R, Han CS & CR Currie (2011) The complete genome sequence of Streptomyces cf. griseus (XyelbKG-1 1), an ambrosia beetle-associated actinomycete. Journal of Bacteriology 193(11): 2890-91. 145 Appendix 1 Biedermann PHW, M Taborsky M and DL Six (manuscript in work) Fungal associates and their effect on the behaviours and success of the ambrosia beetle Xyleborus affinis Eichhoff (Scolytinae: Curculionidae). 167 Appendix 2 Biedermann PHW, M Taborsky and CR Currie (manuscript in work) Mechanisms of fungus gardening in ambrosia beetles. 175 Summary & Conclusion 183 Acknowledgements 185 Contributions & Funding 189 Curriculum Vitae © 2000 G. Larson, The Far Side Curriculum Vitae General Introduction “Again as in the case of corporeal structure, and conformably with my theory, the instinct for each species is good for itself, but has never, as far as we can judge, been produced for the exclusive good of others” C. Darwin, Origin of Species 1859. Since I got familiar with Darwin’s concept of the survival of the fittest, I am very much fascinated by the question how a behaviour can persist in nature that obviously reduces the direct success (fitness) of an actor, but instead greatly benefits others. We are surrounded by such examples of the success of cooperation: packs of cooperatively hunting carnivores, helpers at bird nests that support the breeding pair in protection and food provisioning, the great success of social insects, where some individuals even refrain from reproduction, and the incredible diverse examples of symbioses, from gut microbes that help humans to digest their food, to pollination of flowers by bees and the fascinating fungus garden that provide nutrients for their insects farmers for getting tended, weeded and provisioned with new substrate. Perhaps less obvious, cooperation can not only be found among selfish biological entities, but is also the foundation of the major evolutionary transitions to stages of higher complexity. The evolution of chromosomes from independent genes, of multicellular organisms from individual cells and of societies from individuals involves a transition such that “entities that were capable of independent replication before the transition can replicate only as part of a larger whole after it” (Maynard-Smith and Szathmáry 1995). The transition from egoistic individuals to symbioses and to animal societies was already noticed by Darwin as a challenge for his theory of natural selection (Darwin 1859), and has puzzled generations of evolutionary biologists ever since. After the concept of cooperation among animals as “good for the species” has been rejected, W.D. Hamilton’s inclusive fitness theory (also known as kin selection theory; Hamilton 1964) has prevailed as the currently best and most widely accepted theory for understanding the evolution of cooperation. Even though it is perhaps difficult to accept on first sight, there is tremendous evidence that selection acts on the gene level of individuals, meaning that in evolutionary times organisms persist that do not behave for the benefit of themselves, but instead for the highest possible success of the genes they carry. Thus, individuals are expected to maximize the success of their own genes (direct fitness) plus the success of the same genes in other (related) organisms (indirect fitness). This thesis illustrates the power and validity of Hamilton’s inclusive fitness theory by critically testing its predictions with the social life of ambrosia beetles and their symbioses with fungi. My thesis is a first step for explaining the evolution of sociality and fungus farming in a lineage of beetles, which ancestors are solitary living and feeding on plants. On the next few pages, I will briefly introduce the inclusive fitness concept in more detail and present ecological and genetic factors that promote the evolution of cooperation in nature. 1 General Introduction Hamilton’s inclusive fitness theory „Die Theorie bestimmt was wir beobachten können.“ Albert Einstein. Modern evolutionary theory on cooperation1 originated with Hamilton’s inclusive fitness theory and his ground-breaking article on the genetic evolution of social behaviour (Hamilton 1963; 1964). This led biologists to realize that altruistic
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