Germline mutation rates are fundamental to evolution, yet they remain unquantified for beetles (Coleoptera), the most speciose order including major pests. We sequenced genomes from 16 trios of the Colorado potato beetle (Leptinotarsa decemlineata, CPB)—a pest that has evolved resistance to many insecticides. We estimated a germline mutation rate of 5.8 × 10−9 (95% CI: 4.7 × 10−9, 7.2 × 10−9) per site per generation in CPB, a rate 2-fold higher than the median for other insects. Across 13 insect species, mutation rate was positively associated with genome-wide GC content (PGLS). The increased mutation rate in CPB is also consistent with drift-barrier expectations. Based on this mutation rate and the beetle’s fecundity, we estimate that the brood from just one CPB female can introduce nearly 141 new mutations into the coding regions each generation. These findings inform CPB’s rapid pesticide resistance evolution and fill a key gap in arthropod genomics and evolution
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