Spread of a single superclone drives insecticide resistance inAcyrthosiphon kondoiacross an invasive range

Abstract

Populations under similar selection pressures may adapt via parallel evolution or dispersal of advantageous alleles. Here, we investigated insecticide resistance in the invasive blue-green aphid, Acyrthosiphon kondoi, which reproduces clonally in Australia and has rapidly developed resistance across geographic locations. Using genomic, transcriptomic, and experimental approaches, we explored the evolutionary origins and molecular mechanisms of resistance. We developed the first reference genome for A. kondoi (443.8 Mb, 28,405 annotated genes, BUSCO score 97.5%) and established isofemale strains from southern Australia with varying resistance statuses. All resistant strains shared a common ancestor, supporting the spread of a resistant 'superclone' distinct from susceptible strains. Resistance was associated with overexpression of an esterase gene homologous to the E4/FE4 esterases linked to multi-chemical resistance in other aphid pests. Functional experiments in Drosophila melanogaster confirmed the causal role of this E4-like esterase in resistance to organophosphates, carbamates, and pyrethroids. These findings highlight how clonal dispersal and insecticide overuse can transform local adaptation into a widespread pest management issue. Our results suggest a parallel macroevolutionary response to insecticide selection in A. kondoi and other aphid species at the gene family level, but with a distinct regulatory mechanism in A. kondoi. Given the rapid spread of the resistant superclone, alternative management strategies, including expanded chemical control options and enhanced biological control, are urgently needed to mitigate this growing pest problem.