The making of a pest - Understanding evolutionary mechanisms that underlie host plant specialization in gall midges

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Gall midges, small flies in the Cecidomyiidae family, are considered natures most specialized and sophisticated herbivores, due to their ability to manipulate plant development to form galls. Galls are plant structures formed in response to stimuli produced by the gall-inducer, which can vary from inconspicuous nutritive tissues to elaborate swollen structures that resemble thorns or fruits. This ability to manipulate plant growth has fascinated philosophers and scientists for hundreds of years and spurred investigations on a wide array of subjects including speciation, host selection and manipulation. However, there are still major gaps in our understanding of the underlying mechanisms involved in these events. Given the herbivorous and specialized nature of gall midges, many are destructive agricultural and forestry pests. The swede midge, Contarinia nasturtii, and the canola flower midge, C. brassicola, are two such examples, capable of causing significant damage to Brassicaceae crops (e.g. broccoli, cauliflower, cabbage, canola). Contarinia brassicola is new-to-science, only being formally described in 2019. Whereas C. nasturtii is native to Eurasia, and can infest multiple plant species and tissues within the Brassicaceae, C. brassicola is hypothesized to be native to North America, and is only known to infest developing flower buds of canola (Brassica napus). Phylogenetic evidence also indicates that although they are in the same genus, the two species are distantly related and each have closer relatives that are non-Brassicaceae specialists. This suggests C. nasturtii and C. brassicola may have undergone parallel evolution to use the same host plants. Given their ability to form galls as well as differences in their native ranges, host plants/tissues infested, and pest status, C. nasturtii and C. brassicola represent a unique model system to investigate the mechanisms of host plant shifts, selection and manipulation, which may ultimately underlie the making of a pest. The long-term objective of this NSERC Discovery-based research program is to develop a comprehensive understanding of the evolution of pestiferous Brassicaceae-specialist Contarinia gall midges. To achieve this objective my proposed research will: 1) Annotate the genome of C. brassicola to create a resource for further transcriptomic and population genetic analyses; 2) Compare the geographic range and host selection behaviour of C. brassicola and C. nasturtii to examine possible mechanisms of parallel evolution; 3) Characterize and compare effectors in salivary glands of C. nasturtii and C. brassicola involved in host plant manipulation; and 4) Develop a C. nasturtii-Arabidopsis model system to explore the plant signaling pathways and defense responses which are manipulated by the midge. Ultimately, the knowledge gained through this research program may enable the development of novel strategies to manage these pests.