Adaptive Evolution and Transcriptomic Specialization of P450 Detoxification Genes in the Colorado Potato Beetle Across Developmental Stages and Tissues.

The Colorado potato beetle is a notorious agricultural pest with remarkable adaptability and insecticide resistance. This study conducted comprehensive transcriptome analysis across multiple developmental stages and tissues, focusing on the cytochrome P450 monooxygenase gene family. Using RNA-seq data from 65 datasets, we identified significant transcriptional reprogramming during key developmental transitions, particularly from egg to first instar larva and from third instar larva to adult, reflecting critical biological processes, including feeding initiation and metamorphosis. We identified 3616 tissue-specific genes, with the testis exhibiting the highest transcriptional specialization (1182 genes). Genome-wide screening revealed 78 P450 genes distributed across four major clans with an uneven chromosomal distribution. Expression analysis demonstrated six distinct clusters with tissue and developmental stage-specific patterns. Evolutionary analysis identified five P450 genes under strong positive selection. Analysis of mRNA sequence polymorphisms revealed developmental stage and tissue-dependent patterns, with elevated mutation frequencies in early developmental stages and specific tissues. These distinct tissue and developmental stage-specific mutation patterns in P450 transcripts highlight the dynamic regulation of detoxification genes. Our findings advance the understanding of the molecular mechanisms underlying the beetle's ecological success and provide valuable targets for developing novel pest management strategies.