Abstract

The aphid Myzus persicae is a destructive agricultural pest that displays an exceptional ability to develop resistance to both natural and synthetic insecticides. To investigate the evolution of resistance in this species we generated a chromosome-scale genome assembly and living panel of >110 fully sequenced globally sampled clonal lines. Our analyses reveal a remarkable diversity of resistance mutations segregating in global populations of M. persicae. We show that the emergence and spread of these mechanisms is influenced by host–plant associations, uncovering the widespread co‐option of a host-plant adaptation that also offers resistance against synthetic insecticides. We identify both the repeated evolution of independent resistance mutations at the same locus, and multiple instances of the evolution of novel resistance mechanisms against key insecticides. Our findings provide fundamental insights into the genomic responses of global insect populations to strong selective forces, and hold practical relevance for the control of pests and parasites.

Highlights

  • The aphid Myzus persicae is a destructive agricultural pest that displays an exceptional ability to develop resistance to both natural and synthetic insecticides

  • These contigs were categorized and ordered into six chromosomescale scaffolds, corresponding to the haploid chromosome number of this species[21], using in vivo chromatin conformation capture (HiC) data (Fig. 1a). This resulted in a final assembly of 391 Mb, with 95.7% of assembled content contained in the six scaffolds, and a scaffold N50 of 69.9 Mb (Supplementary Table 1)

  • The completeness of the gene space in the assembled genome was assessed using the Benchmarking Universal SingleCopy Orthologues (BUSCO) pipeline[22], with 97.3% of the Arthropoda test gene set found to be present as complete single copies (Supplementary Table 1)

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Summary

Introduction

The aphid Myzus persicae is a destructive agricultural pest that displays an exceptional ability to develop resistance to both natural and synthetic insecticides. Aphids are exceptional models for the study of a range of fundamental ecological and evolutionary topics, including reproductive mode variation, insect-plant interactions, virus transmission, phenotypic plasticity, symbiosis, and insecticide resistance[2,7] Research on this important group of insects has been greatly facilitated by the publication of draft genome sequence assemblies for a number of aphid species[7,8,9,10,11]. One of the most economically important aphid crop pests worldwide, and an emerging insect research model, is the peach potato aphid, Myzus persicae (Sulzer) The status of this species as a pest is enhanced by its global distribution, remarkable efficiency as a vector of more than 100 different plant viruses, and its extremely broad host range[14]. To date, the frequency of these secondary symbionts in populations of M. persicae worldwide remains unknown

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