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School of Doctoral Studies in Biological Sciences School of Doctoral Studies in Biological Sciences University of South Bohemia in České Budějovice Faculty of Science Specificity of insect-plant associations and their role in the formation of plant defenses and speciation Ph.D. Thesis RNDr. Martin Volf Supervisor: Prof. RNDr. Vojtěch Novotný, CSc. Institute of Entomology, Biology Centre, Czech Academy of Sciences, České Budějovice, CZ Department of Zoology, Faculty of Science, University of South Bohemia, České Budějovice, CZ České Budějovice 2016 This thesis should be cited as: Volf, M., 2016: Specificity of insect-plant associations and their role in the formation of plant defenses and speciation. Ph.D. Thesis Series, No. 9. University of South Bohemia, Faculty of Science, School of Doctoral Studies in Biological Sciences, České Budějovice, Czech Republic, 183 pp. Annotation The aim of this dissertation is to investigate what role insect-plant interactions play in the formation of host-plant defenses and in the diversification of both groups. We show that various groups of herbivore respond differently to host-plant defenses. Therefore plant defenses diversify into suites of complementary traits, as individual traits fail to provide protection against specialized herbivores. Further, we identify what levels of host-phylogeny shape the food- web structure of insect herbivores. We show that specialized herbivores are affected mainly by the terminal parts of the host- phylogeny. In contrast, more polyphagous guilds are affected mainly by the mid-levels of the host phylogeny because the effects of terminal or deeper phylogeny seem to be surpassed by other factors in more generalist insect species. In the last chapter, we show how specialized insect-plant interactions generated by tight insect-plant coevolution can influence the speciation in plants over environmental gradients. Declaration [in Czech] Prohlašuji, že svoji disertační práci jsem vypracoval samostatně pouze s použitím pramenů a literatury uvedených v seznamu citované literatury. Prohlašuji, že v souladu s § 47b zákona č. 111/1998 Sb. v platném znění souhlasím se zveřejněním své disertační práce, a to v úpravě vzniklé vypuštěním vyznačených částí archivovaných Přírodovědeckou fakultou elektronickou cestou ve veřejně přístupné části databáze STAG provozované Jihočeskou univerzitou v Českých Budějovicích na jejích internetových stránkách, a to se zachováním mého autorského práva k odevzdanému textu této kvalifikační práce. Souhlasím dále s tím, aby toutéž elektronickou cestou byly v souladu s uvedeným ustanovením zákona č. 111/1998 Sb. zveřejněny posudky školitele a oponentů práce i záznam o průběhu a výsledku obhajoby kvalifikační práce. Rovněž souhlasím s porovnáním textu mé kvalifikační práce s databází kvalifikačních prací Theses.cz provozovanou Národním registrem vysokoškolských kvalifikačních prací a systémem na odhalování plagiátů. České Budějovice, 1.8. 2016 .............................................. Martin Volf This thesis originated from a partnership of Faculty of Science, University of South Bohemia, and Institute of Entomology, Biology Centre of the ASCR, supporting doctoral studies in the Entomology study programme. Financial support The projects in this thesis were supported by Grant Agency of the Czech Republic (14-04258S, 15-24571S, and 206/09/0115), European Research Council (GA669609), Czech Ministry of Education and European Commission (CZ.1.07/2.3.00/20.0064), the Grant Agency of the University of South Bohemia (156/2013/P and 103-016/2015/P), US National Science Foundation (DEB-0841885), and the Academy of Finland (128652). Acknowledgements I would like to give special thanks to my supervisor Vojtěch Novotný. His support and insight have been invaluable for me when exploring the fascinating world of insect-plant interactions. He gave me this amazing opportunity of spending my studies by pursuing insect herbivores in forest canopies around the world. I am very grateful to my colleagues and friends. Especially to Tomokazu Abe, Philip Butterill, Lukáš Čížek, Pavel Drozd, Jan Hrček, Petr Klimeš, Martin Libra, Simon Segar, František Sládeček, and Tomáš Zítek for all their help, fruitful debates over countless beers, and fun we had. Special thanks go to Klára Aurová, Michaela Borovanská a Eva Chocholová who kept this department going. My huge gratitude belongs to my family for their ever present love and support. Especially, I would like to thank my mother Věra and father Petr who always supported me in my love to biology and in my intention to become an entomologist. Further, I thank my grandmother Věra for her huge support and help with feeding the caterpillars during my first rearing experiments and feeding Percy the parrot during my abroad stays. Many thanks go to my grandmother Olga and grandfather Jiří, who always supported my enthusiasm for biology, entomology and beetle collecting. Last but not least, I would like to thank Tereza for her love, support and accompanying me on my insect-sampling journeys. p.s. I would also like to thank all the caterpillars which were reared to adults or provided tissue for DNA barcoding, making their identification much easier. List of papers, manuscripts, and author’s contribution The thesis is based on the following papers (listed chronologically): I. Volf, Martin*, Jan Hrcek, Riitta Julkunen‐Tiitto, and Vojtech Novotny. "To each its own: differential response of specialist and generalist herbivores to plant defence in willows". Journal of Animal Ecology 84, no. 4 (2015): 1123-1132. (IF= 4.827) Martin Volf sampled the insect and plant data, participated in the secondary metabolite analysis, measured the physical traits, did the molecular analysis, reconstructed the host-plant phylogeny, did the statistical analysis of the data, formulated the hypotheses, wrote the first draft of the manuscript. II. Volf, Martin*, Riitta Julkunen‐Tiitto, Jan Hrcek, and Vojtech Novotny. "Insect herbivores drive the loss of unique chemical defense in willows". Entomologia Experimentalis et Applicata 156, no. 1 (2015): 88-98. (IF= 1.442) Martin Volf sampled the insect and plant data, participated in the secondary metabolite analysis, measured the physical traits, did the molecular analysis, reconstructed the host-plant phylogeny, did the statistical analysis of the data, formulated the hypotheses, wrote the first draft of the manuscript. III. Volf*+, Martin, Simon T Segar+, Scott E Miller, Brus Isua, Mentap Sisol, Gibson Aubona, Legi Sam, Petr Šimek, Martin Moos, Juha-Pekka Salminen, Jan Zima, George D Weiblen and Vojtech Novotny. "Dynamic plant defenses of sympatric Ficus species structure local larval leaf-chewer communities". (Manuscript) Martin Volf participated in the secondary metabolite analysis, measured part of the physical traits, did part of the molecular analysis, reconstructed the host-plant phylogeny, did part of the statistical analysis of the data, helped to formulate the hypotheses, wrote the first draft of the manuscript together with Simon T Segar. IV. Volf*, Martin, Petr Pyszko, Tomolazu Abe, Martin Libra, Nela Kotásková, Martin Šigut, Rajesh Kumar, Ondřej Kaman, Philip T Butterill, Jan Šipoš, Haruka Abe, Hiroaki Fukushima, Pavel Drozd, Naoto Kamata, Masashi Murakami and Vojtech Novotny. "Phylogenetic diversity of host plants drives insect- plant food web structure". (Manuscript) Martin Volf sampled part of the insect and plant data, did the molecular analysis, reconstructed the host-plant phylogeny, did the statistical analysis of the data, formulated the hypotheses, wrote the first draft of the manuscript. V. Segar*+, T Simon, Martin Volf +, Jan Zima Jnr., Brus Isua, Mentap Sisol, Legi Sam, Katerina Sam, Daniel Souto-Vilarós and Vojtech Novotny. "Speciation in a keystone plant genus is driven by elevation: a case study in New Guinean Ficus". (Manuscript) Martin Volf did part of the molecular analysis, , did part of the statistical analysis of the data, helped to formulate the hypotheses, wrote the first draft of the manuscript together with Simon T Segar. * corresponding author + shared first authorship Co-author agreement: Vojtěch Novotný, the supervisor of Ph.D. thesis and co-author of all presented papers and manuscripts, fully acknowledges the major contribution of Martin Volf in all presented papers. …………………………………….. Prof. RNDr. Vojtěch Novotný, CSc. Simon T. Segar, the corresponding author of "Speciation in a keystone plant genus is driven by elevation: a case study in New Guinean Ficus" presented in Chapter IV, acknowledges the major contribution of Martin Volf in the presented manuscript. …………………………………….. Simon T. Segar, Ph.D. Contents Introduction…………………………………………………………..1 Chapter I………………………………………………………….…23 Volf, Martin*, Jan Hrcek, Riitta Julkunen‐Tiitto, and Vojtech Novotny. "To each its own: differential response of specialist and generalist herbivores to plant defence in willows". Journal of Animal Ecology 84, no. 4 (2015): 1123-1132. Chapter II………………………………………………………...…53 Volf, Martin*, Riitta Julkunen‐Tiitto, Jan Hrcek, and Vojtech Novotny. "Insect herbivores drive the loss of unique chemical defense in willows". Entomologia Experimentalis et Applicata 156, no. 1 (2015): 88-98. Chapter III……………………………………………...………...…77 Volf*+, Martin, Simon T Segar+, Scott E Miller, Brus Isua, Mentap Sisol, Gibson Aubona, Legi Sam, Petr Šimek, Martin Moos, Juha-Pekka Salminen, Jan Zima, George D Weiblen and Vojtech Novotny. "Dynamic plant defenses of sympatric Ficus species structure local larval leaf-chewer communities". Chapter IV……………………………………………...………...109
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