Abstract
BackgroundThe prevailing paradigm of host-parasite evolution is that arms races lead to increasing specialisation via genetic adaptation. Insect herbivores are no exception and the majority have evolved to colonise a small number of closely related host species. Remarkably, the green peach aphid, Myzus persicae, colonises plant species across 40 families and single M. persicae clonal lineages can colonise distantly related plants. This remarkable ability makes M. persicae a highly destructive pest of many important crop species.ResultsTo investigate the exceptional phenotypic plasticity of M. persicae, we sequenced the M. persicae genome and assessed how one clonal lineage responds to host plant species of different families. We show that genetically identical individuals are able to colonise distantly related host species through the differential regulation of genes belonging to aphid-expanded gene families. Multigene clusters collectively upregulate in single aphids within two days upon host switch. Furthermore, we demonstrate the functional significance of this rapid transcriptional change using RNA interference (RNAi)-mediated knock-down of genes belonging to the cathepsin B gene family. Knock-down of cathepsin B genes reduced aphid fitness, but only on the host that induced upregulation of these genes.ConclusionsPrevious research has focused on the role of genetic adaptation of parasites to their hosts. Here we show that the generalist aphid pest M. persicae is able to colonise diverse host plant species in the absence of genetic specialisation. This is achieved through rapid transcriptional plasticity of genes that have duplicated during aphid evolution.
Highlights
The prevailing paradigm of host-parasite evolution is that arms races lead to increasing specialisation via genetic adaptation
The clone O genome was independently assembled to a size of 355 Mb with 18,433 protein-coding genes (30,247 isoforms) annotated, validating the genome size and number genes identified in the G006 assembly (Table 1)
Gene expression changes upon host transfer occur rapidly To further investigate gene expression plasticity in M. persicae upon transfer to diverged hosts, we investigated differential gene expression of aphids transferred from B. rapa to N. benthamiana and allowed adjustment on their new hosts for seven weeks, this time including a transfer from B. rapa to Arabidopsis thaliana
Summary
The prevailing paradigm of host-parasite evolution is that arms races lead to increasing specialisation via genetic adaptation. Parasites often exhibit a high degree of specialisation to a single or reduced range of host species [1, 2] This is especially true for insect herbivores, of which there are around 450,000 described species living on around 300,000 species of vascular plants, the majority of which are monophagous or oligophagous, being able to colonise only one or a few closely related plant species [3]. The pea aphid Acyrthosiphon pisum is considered polyphagous, being found on most plants of the Fabaceae, but consists of different biotypes on a continuum of differentiation that colonise specific species of this plant family [13] In another example, phylogenetic analysis of Aphidiinae parasitoid wasps showed that most species previously categorised as generalists were cryptic, host specialised, species complexes [14]. Genuine generalists remain rare and how such parasites manage to keep up in multilateral co-evolutionary arms races remains an evolutionary enigma
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