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.

Abstract. 1. Phenotypic diversity is the fuel that powers evolution.2. Asexual organisms rely on mutation whereas sexual organisms combine mutation with recombination.3. Few organisms provide examples of species that are both sexual and asexual, but aphids do.4. To examine evolution on perceptible timescales requires strong evolutionary forces and, as Darwin noted, agricultural practices provide strong selection. In the case of aphids, insecticides provide a considerable force in the elimination of genotypes.5. Insecticide resistance in Myzus persicae (Sulzer) has arisen independently through point mutation and gene amplification on a number of occasions and at different times. Resistance to organophosphates, pyrethroids, and pirimicarb (a dimethyl carbamate) is now widespread.6. In this paper, we examine these three elements: sexual recombination, clonal expansion, and insecticide selection in the peach-potato aphid M. persicae in relation to the evolution of insecticide resistance and survival of the fittest clone.

In many parts of the world, the tobacco specialist Myzus persicae nicotianae is isolated from the generalist Myzus persicae s . s . because either or both taxa reproduce parthenogenetically. Here we investigated how the genomic integrity of the tobacco specialist is maintained in Greece, where both taxa have a bisexual generation on peach. Microsatellite DNA analysis revealed greatest genetic divergence between populations in tobacco-growing regions and those in a region where tobacco is not cultivated. This was irrespective of reproductive mode, which has an important effect on population structure. Bayesian clustering and admixture analyses split the aphid genotypes into three groups, corresponding with persicae , bisexual nicotianae and unisexual nicotianae , respectively. Genetic distance parameters showed strong regional differentiation but marked year-on-year stability, indicating low interpopulation migration. Assortative mating between taxa is promoted by differences in the daily rhythm of female signalling behaviour, with peak activity coinciding with periods of consubspecific male searching activity. Males showed greater attraction to the sex pheromone of their own subspecies. Thus, despite relatively low overall genetic differentiation, processes are in place facilitating further genomic divergence and eventual speciation.

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Microsatellite genotyping was used to identify common clones in populations of the Myzus persicae group from various hosts and regions in mainland Greece and southern Italy and to compare their distribution and occurrence on tobacco and other crops. Common clones were defined as genotypes collected at more than one time or in more than one population; and, therefore, unlikely to be participating in the annual sexual phase on peach. Sixteen common genotypes were found, accounting for 49.0% of the 482 clonal lineages examined. Eight of these genotypes were subjected, in the laboratory, to short days and found to continue parthenogenetic reproduction, i.e. they were anholocyclic. Four of the six commonest genotypes were red, and one of these accounted for 29.6% of the samples from tobacco and 29.4% of those from overwintering populations on weeds. All six commonest genotypes were found on weeds and five of them both on tobacco and on other field crops. In mainland Greece, the distribution of common clones corresponded closely with that of anholocyclic lineages reported in a previous study of life cycle variation. Common genotypes were in the minority in the commercial peach-growing areas in the north, except on weeds in winter and in tobacco seedbeds in early spring, but predominated further south, away from peach trees. This contrasts with the situation in southern Italy, reported in a previous paper, where peaches were available for the sexual phase, yet all samples from tobacco were of common genotypes.