Genomic architecture and transposable element dynamics drive the divergent evolution of tandemly arrayed P450 clusters in noctuid moths

Gene duplication and transposable element (TE) dynamics are primary contributors to genomic innovation, yet their joint role in the metabolic adaptation of polyphagous insect pests remains insufficiently characterized. We conducted a comparative genomic analysis across 12 lepidopteran species, including eight polyphagous noctuids and four oligophagous models, to examine the evolutionary mechanisms of the cytochrome P450 superfamily. Our results reveal a significant lineage-specific expansion of P450 genes in noctuids, primarily within the CYP3 and CYP4 clans. These expansions are localized within two evolutionarily conserved genomic regions (Locus 1 and Locus 2) that harbor exceptionally large tandem arrays. Integrated analysis of TE distribution identified divergent evolutionary trajectories for these loci. At Locus 1, a robust positive correlation exists between local TE density and P450 copy number, supporting a model of TE-mediated non-allelic homologous recombination. In contrast, Locus 2 exhibits reduced repetitive content despite its expanded repertoire, suggesting structural stabilization under purifying selection following initial duplication bursts. Molecular evolution analyses identified widespread signatures of episodic diversifying selection across both loci. Combined with transcriptomic profiling under insecticide stress, these selection regimes reflect distinct adaptive strategies: Locus 2 paralogs display highly coordinated expression patterns and stable selection intensity, consistent with a gene dosage effect. Conversely, Locus 1 exhibits significant transcriptional heterogeneity and intensified selection, indicating functional subfunctionalization or specialization. Collectively, our findings demonstrate that the divergent genomic architecture and locus-specific regulatory dynamics of conserved P450 clusters underpin the superior metabolic plasticity of noctuid moths, providing a mechanistic framework for the evolution of environmental resilience in agricultural pests.