Selection-Induced Spinosad Resistance and Associated Fitness Costs in Tuta absoluta: A Key Invasive Tomato Pest

The South American tomato pinworm, Tuta absoluta (Meyrick), is one of the major invasive pests that causes severe economic damage to several hosts, especially tomato plants, globally. Spinosad, a biopesticide widely used against several insect pests, also shows promising results against T. absoluta. Here, we investigated the evolution of spinosad resistance and its effects on biological traits and related gene effects to fully understand the relationship between resistance degree and associated fitness costs. The spinosad-resistant strain (SpRS) with a moderate level of resistance (14.40-fold) was developed following continuous selection of the susceptible strain (SS) against spinosad for eight generations. Fitness analysis showed that the larval and pupal developmental durations were significantly increased, while the adult emergence was substantially reduced in the SpRS compared to SS. Adult longevity (male and female), fecundity, and hatching rates significantly decreased in the SpRS T. absoluta compared to SS. Additionally, the gene expression analyses indicated the down-regulation of development and reproduction-related genes (Vg, VgR, JHBP, JHAMT, JHE, and JHDK) in the SpRS population. Further, the mRNA expression level of the resistance-related cytochrome P450 gene CYP321C40, followed by CYP4M116, CYP6AW1, CYP339A1, and CYP6AB327, were significantly increased in the SpRS T. absoluta. Taken together, these results indicated that although T. absoluta developed a moderate level of spinosad resistance accompanied by fitness costs, continuous and indiscriminate use might elevate the resistance level. Overall, these findings provide important information about the trade-off between resistance degree and fitness cost that might be crucial to designing resistance management strategies against this key invasive herbivore.