The key to success: host plant adaptations in the root herbivore 'Diabrotica virgifera virgifera'

<br> Antagonistic interactions between plants and insects are likely the drivers of a fascinating coevolutionary arms race between the two trophic levels. Plants- and plant breeders- are continuously developing traits that allow them to fend-off herbivores, while phytophagous insect keep inventing counter-adaptations to withstand plant defenses. <i>Diabrotica virgifera virgifera</i> LeConte (Coleoptera: Chrysomelidae) is a specialist root herbivore of maize, <i>Zea mays</i>. Known as the billion dollar bug in the USA, the rootworm causes important crop damage annually, and no pest management strategy seems to effectively restrain its spread and voracity. <br><br> This thesis aimed at investigating the interactions of <i>D. virgifera</i> larvae with their plant host to underpin the mechanisms of their remarkable ecological success. <br><br> My results show that the root herbivore is able to exploit plant volatiles such as (<i>E</i>)--caryophyllene and ethylene, to assess the host plant quality at a distance and to orient towards optimal hosts (Chapter 1). I also found that <i>D. virgifera</i> can exploit direct plant defenses: The herbivore is able to detect the most nutritious root tissues using differences in 1,4-benzoxazin-3-one profiles (Chapter 3). Furthermore, I show that <i>D. virgifera</i> induces a reconfiguration of the plant primary metabolism and an attenuation of its defensive inducibility, resulting in induced susceptibility (Chapter 4). Induced susceptibility may explain the benefits for the larvae to aggregate in field. By investigating the aggregative behavior of the larvae, I found that <i>D. virgifera</i> uses (<i>E</i>)--caryophyllene in a dosedependent manner to evaluate the density of conspecifics feeding on a plant. The perception of the sesquiterpene allows the insect to aggregate on plants infested with optimal densities of conspecifics, thereby avoiding intraspecific competition and overexploitation (Chapter 4). <br><br> Maize plants seem to be maladapted to <i>D. virgifera</i>. Yet, plant breeders have grown maize plants in the presence of <i>D. virgifera</i> for almost 10 000 years now. It is therefore hardly conceivable that breeding would not have led to selection of resistant germplasm. For instance, the emissions of (<i>E</i>)--caryophyllene was altered and lost in American maize varieties, possibly to reduce the capacity of <i>D. virgifera</i> to aggregate. My work highlights the ecological and physiological costs associated with the emission of this compound, and proposes a novel scenario to explain the evolution of (<i>E</i>)--caryophyllene (Chapter 2). Finally, one resistance trait that would not exert any pressure on the pest that would cause to adapt is herbivore-induced tolerance. I investigated this trait in maize plant and highlight an unexpected role of stems as storage organs for plants under attack (Chapter 5). Focusing on tolerance mechanisms rather than resistance may be a promising avenue to reduce the impact of <i>D. virgifera</i> on maize yield and food production.

Thèse de doctorat : Université de Neuchâtel, 2012 ; 2248