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Molecular genetics of host specialisation in pea aphids

Final Activity Report Summary - APHID GENOMICS (Molecular genetics of host specialisation in pea aphids)

Aphids are model organisms in both applied and evolutionary biology and this status of these small insects is mainly related to several features of their biology that enable them to locate and exploit their host plants. Of course these phytophagous insects are primarily known as a perennial source of frustration to farmers and gardeners as they damage cultures through direct impact on plant tissues or virus transmission while feeding on their host plants. In a completely different context though, host plant use and selection in aphids are also the focus of evolutionary biologists as species and host races of aphids that are specialised on different plants are model organisms in the analysis of population differentiation in sympatry and ecological speciation. The genome of the pea aphid, namely acyrthosiphon pisum, has been recently sequenced, offering a great opportunity to identify key genes involved in the chemical recognition between aphids and their host plants, i.e. the odorant (Or) and gustatory (Gr) receptor genes.

Using available information on the sequence and the structure of chemoreceptors in other insect species and bioinformatics tools, we searched these genes in the pea aphid genome. Our results showed that there were at least 77 Grs and 79 Ors in this genome. Some of them were clustered in the same region of the genome. While we found a few aphid genes showing some degree of homology with other insect sequences, most genes clustered in recently duplicated aphid-specific expansions. Therefore, the Gr and Or gene families appeared to be undergoing rapid and recent expansion in this aphid genome. As we found a signature of evolution under selection in some chemoreceptor genes, their recent diversification might have been related to adaptive events. We proposed that some of these genes were actually involved in the striking host plant specialisation that was observed in the pea aphid as host plant acceptance was known to rely on chemosensory processes in this phytophagous insect.

The identification of chemoreceptor genes in the pea aphid had very important implications for both applied and fundamental research. Firstly, it provided new insights into the evolution of genes involved in smell and taste, which were extensively studied in a wide range of organisms from insects to humans. It was also a crucial step towards understanding the mechanisms of host plant specialisation and host race formation in phytophagous insects. This, in turn, promised new developments in the definition of new pest control strategies based on the manipulation of the attraction of aphids to specific agricultural cultures. More related to our research, the molecular characterisation of chemoreceptor genes in the pea aphid offered the unique opportunity to test the involvement of these candidate loci in the mechanisms leading to speciation among host races.