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ANNÉE 2014 THÈSE / UNIVERSITÉ DE RENNES 1 sous le sceau de l’Université Européenne de Bretagne pour le grade de DOCTEUR DE L’UNIVERSITÉ DE RENNES 1 Mention : Biologie École doctorale Vie – Agro – Santé présentée par Maxime HERVÉ Préparée à l’unité de recherche 1349 IGEPP Institut de Génétique, Environnement et Protection des Plantes UFR Sciences de la Vie et de l’Environnement Thèse soutenue à Rennes Écologie chimique de le 15 octobre 2014 l'interaction colza – devant le jury composé de : Samantha COOK Senior Research Scientist, Rothamsted Research méligèthe : vers de (United Kingdom) / rapporteuse Martine HOSSAERT-McKEY nouvelles stratégies Directrice de Recherche CNRS / rapporteuse Alain BOUCHEREAU de contrôle des Professeur Université Rennes 1 / examinateur Erik POELMAN insectes ravageurs ? Assistant Professor, Wageningen University (the Netherlands) / examinateur Anne Marie CORTESERO Professeure Université Rennes 1 / directrice de thèse Régine DELOURME Directrice de Recherche INRA / co-directrice de thèse PhD thesis Maxime HERVÉ Chemical ecology of the oilseed rape – pollen beetle interaction: towards new control strategies for insect pests? Defended October 15th 2014 Supervised by Anne Marie CORTESERO and Régine DELOURME University of Rennes 1 Institute for Genetics, Environment and Plant Protection – Table of contents – INTRODUCTION Scientific and agronomical context ............................................................................................... 19 Study system ................................................................................................................................... 25 Objectives and organization of the manuscript ........................................................................... 31 General approach Article 1 – Protecting crops against insect pests by selecting for increased plant resistance: barriers to success and an alternative approach (in prep. for Pest Management Science) ........................... 35 CHAPTER 1: Attraction Article 2 – Attractiveness of oilseed rape (Brassica napus) for the pollen beetle (Meligethes aeneus) varies with plant genotype but preference does not match performance (in prep. for Ecological Entomology) ............................................................................................................................ 47 CHAPTER 2: Feeding intensity Article 3 – Manipulating feeding stimulation to protect crops against insect pests? (under revision for Journal of Chemical Ecology) ................................................................................................... 59 CHAPTER 3: Egg production and oviposition Article 4 – How oilseed rape (Brassica napus) genotype influences pollen beetle (Meligethes aeneus) oviposition (published in Arthropod-Plant Interactions) ............................................................ 79 Article 5 – Oviposition behavior of the pollen beetle (Meligethes aeneus): a functional study (under revision for Journal of Insect Behavior) ..................................................................................... 91 CHAPTER 4: Larval development Article 6 – Plant genotype affects nutritional quality of oilseed rape (Brassica napus) for adults and larvae of the pollen beetle (Meligethes aeneus) (in prep. for Journal of Insect Physiology) .... 105 GENERAL DISCUSSION ....................................................................................... 117 FRENCH SUMMARY ............................................................................................. 135 SCIENTIFIC COMMUNICATIONS..................................................................... 143 15 16 – INTRODUCTION – INTRODUCTION Scientific and agronomical context – Scientific and agronomical context – THE PLANT – PHYTOPHAGOUS kingdom is one of the main factors explaining the INSECTS ARMS RACE ecological specialization of the majority of herbivorous insects, for either feeding or oviposition resources In all ecosystems taken together, phytophagous (Fraenkel 1959; Ehrlich & Raven 1964; Jaenike 1990; insects are considered to consume around 20 % of the Hartmann 2007). Indeed, species feeding on more than biomass produced annually by plants (Agrawal 2011). three plant families (i.e. generalists) are thought to During the 415 million years of coevolutionary history represent less than 10 % of all phytophagous insects shared by these two taxa (Ehrlich & Raven 1964; (Bernays & Graham 1988). According to the well- Labandeira 2007), plants have evolved complex and accepted theory specialists should be more efficient than multiple defense strategies against these enemies while generalists in tolerating specific defense compounds insects evolved sophisticated counteradaptations (those of the plant family on which they are specialized), (Gatehouse 2002; Mello & Silva-Filho 2002). but on the other hand should tolerate a smaller diversity of toxic metabolites (Krieger et al. 1971; Whittaker & Plant defenses against insects Feeny 1971). These specific substances should even Apart from a few gene-for-gene resistances (Flor attract specialists toward their host plant and possibly act 1942, 1945) known especially in plant – aphid systems as feeding and/or oviposition stimulants, whereas the (Smith & Boyko 2007), plant resistance to insects is effect on generalists should be at the opposite (Bruce et often complex, involving many different traits (Walling al. 2005; Hartmann 2007; Ali & Agrawal 2012). 2000; Mello & Silva-Filho 2002; Agrawal & Fishbein However, the ‘generalist – specialist’ paradigm, 2006; Agrawal 2011). It is often more appropriate to although practical as a first approximation, has to be put speak about ‘defense syndromes’ than singleton into perspective for at least two reasons. Firstly because strategies (Agrawal & Fishbein 2006). Defense traits can ‘generalist species’ often hide complexes of specialized be either physical or chemical, but can also be related to but still opportunistic populations, or even complexes of plant phenology or growth rate (Mello & Silva-Filho cryptic species (Loxdale et al. 2011). Secondly because 2002; Carmona et al. 2011). examples are known of specialist species being Since the founding paper of Fraenkel (1959), plant negatively affected by secondary metabolites produced resistance to insects is mainly seen through the prism of by their host plant (Ali & Agrawal 2012). Furthermore, so-called secondary metabolites, those compounds not the same species can be considered either as generalist or involved in primary physiological functions such as as specialist depending of its life stage. Many growth and reproduction (Berenbaum & Zangerl 2008; phytophagous insects (especially lepidopteran species) Hartmann 2008). Secondary substances can act as are generalist pollen or nectar feeders as adults, whereas repellents, antifeedants, digestibility reducers or toxins larvae are specialists of a certain plant family. (Mello & Silva-Filho 2002; Hartmann 2007). Many of If secondary metabolites proved to be an important them are typical of one or a few plant families, e.g. part of the plant – insect interaction puzzle, primary cardenolides (Agrawal et al. 2012), furanocoumarins compounds were probably too neglected (Berenbaum (Murray et al. 1982), glucosinolates (Fahey et al. 2001) 1995). Low nutritional quality is a selected direct defense or pyrrolizidine alkaloids (Hartmann 1991). This strategy in some plant species (Agrawal & Fishbein irregular distribution of defensive compounds in the plant 19 INTRODUCTION Scientific and agronomical context 2006). Clancy & Price (1987) suggested that it could also patterns (MAMPs, PAMPs and DAMPs, respectively), be an indirect defense, by lengthening insect elicitors that are often present in insect oral secretions or development time and so extending the vulnerability oviposition fluids (Howe & Jander 2008; Wu & Baldwin window to natural enemies (the ‘slow growth – high 2010; Hilker & Meiners 2011; Bonaventure 2012; Erb et mortality’ hypothesis). Primary metabolites play a major al. 2012). Through a cascade of transcriptomic, role in determining plant nutritional quality (Awmack & metabolomic and proteomic rearrangements regulated Leather 2002). Hence, concentration in some of these essentially by the phytohormones jasmonic acid, salicylic compounds might be under selection due to herbivore acid and ethylene, novel or higher-intensity defenses are pressure (Berenbaum 1995). Certain primary substances then expressed, locally or systemically (Howe & Jander are also important phagostimulant compounds, especially 2008; Wu & Baldwin 2010; Erb et al. 2012). Part of sugars (Chapman 2003). Even if insects are to some these defenses are indirect; they attract herbivore natural extent able to adjust their dietary intake depending on the enemies (especially parasitoids but also invertebrate nutritional value of their food (Behmer 2009), predators and birds) by means of modified and specific appetability (i.e. ability to chemically stimulate feeding) odor bouquets (Dicke & van Loon 2000; Holopainen of plant tissues may partly explain patterns of food 2004; Howe & Jander 2008; Unsicker et al. 2009; consumption. Karban 2011). Even without being attacked, plant However, plant chemistry may not be the sole key to defenses can be primed by volatile methylated understand the ecology and evolution of plant – insect phytohormones (methyl-jasmonate and methyl- interactions. In a recent meta-analysis, Carmona et al. salicylate) emitted by conspecifics (Holopainen 2004; (2011)

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