Spread of a single superclone drives insecticide resistance in Acyrthosiphon kondoi across 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 nuclear genome assembly for A. kondoi (443.8 Mb, 28,405 annotated genes, BUSCO score 97.5%) and a partial mitochondrial assembly (11,598 bp). All resistant strains shared a common ancestor, supporting the spread of a resistant superclone lineage that is distinct from susceptible strains. Resistance was associated with over-expression of an esterase gene that was homologous to E4/FE4 esterases in other aphid pests that are linked to resistance. Functional experiments in Drosophila melanogaster confirmed a 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.