Adaptation of organisms to contrasting environmental conditions is a major driver of species diversification. However we know very little on the genetic basis underlying ecologically-relevant traits, and on how and at what speed adaptive divergence leads to genetic differentiation. Here, we will use the pea aphid, a well-suited system for adaptive genomics, which conveniently shows a complex of plant-specialized biotypes, ranging from sympatric host races to incipient species, and resulting from a recent adaptive radiation. By combining novel phylogenetic and population genetic analyses of massive genomic dataset, innovative tools for functional analysis and unique biological resources, we will 1) reconstruct the evolutionary history of plant specialization and biotype formation, 2) identify genomic regions under divergent selection and characterize the genomic architecture underlying plant-based differentiation, and 3) identify genes and functions involved in plant specialization in the pea aphid complex. This project relies on a consortium of 3 French partners and 2 associate partners from other European countries who will bring complementary skills and know-how for the development of multidisciplinary approaches and combination of methods needed to reach project's objectives. This project will allow testing whether multiple independent events of adaptation to different environments involve the same genomic regions and the same set of genes and how genetic divergence accumulates along the genome through time in reproductive isolation. It will also increase knowledge on how insects overcome plant defenses and acquire new hosts on which they may become adapted, paving the way for the development of sustainable control strategies against aphids as important crop pests, based on enhanced plant defenses.

Aphids are serious pests of many cultivated crops and mainly managed by application of pesticides. Pesticides can be harmful to the environment and human health, and many aphid species have developed resistance mechanisms against insecticides; therefore, alternative methods for aphid control are required. To develop durable aphid control strategies while reducing pesticide use, it is necessary to create more knowledge on plant-aphid interactions and select or construct aphid resistant crops efficiently. This project takes advantage of well-developed pea aphid (Acyrthosiphon pisum) system to study plant-aphid interactions at a molecular level. More specifically, we will examine A. pisum biotypes and host legume interactions to identify and characterize the compatibility and incompatibility factors in both aphids and plants and examine the plant signaling pathways involved in the interactions. A. pisum biotypes are specialized to feed on one or a few legume species only (compatible hosts) and cannot perform well on the other legumes (incompatible hosts). We hypothesize that plant-aphid interactions are analogous to plant-microbial pathogen interactions: aphid salivary proteins might function like effectors with virulence and avirulence functions, and their interactions with certain plant proteins determine the success of the aphids. We further hypothesize that aphid salivary proteins with biotype specific expression pattern or amino acid sequence can be the effectors involved in the determination of compatibility with specific plants. Based on the analyses of genome re-sequencing and transcriptomic analyses, we have already identified some candidate salivary effector genes that may be involved in the aphid adaptation to their specific host plants. We would like to characterize those genes and envisage identifying their plant targets using protein-protein interactions. To directly identify the plant factors involved in aphid interactions, we have screened 240 re-sequenced Pisum sativum accessions with pea adapted and non-adapted A. pisum lines and observed a range of resistance and susceptibility. In this project, based on the already acquired data, we would like to conduct genome wide association study (GWAS) and identify the loci involved in plant resistance or susceptibility. We will also select accessions with extreme resistance/susceptible phenotype and conduct metabolomics and transcriptomics to identify the signaling pathways involved in the interactions with aphids. Furthermore, we aim to screen P. sativum mutants by TILLING to find the mutants of key resistance pathways, effector targets and resistant genes. We will test their interactions with A. pisum biotypes and examine the induction of genes and accumulation of metabolites. By the end of the project, we will produce valuable data and materials useful for both fundamental and applied researches and create the knowledge that can contribute to select or create aphid resistant crops.