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.

基因重复与转座因子（transposable element, TE）动态变化是基因组创新的核心驱动因素，但二者在多食性农业害虫的代谢适应性中的协同作用仍未得到充分解析。本研究针对12种鳞翅目物种开展比较基因组分析，其中包括8种多食性夜蛾科昆虫与4种寡食性模式物种，旨在探究细胞色素P450超家族（cytochrome P450 superfamily）的进化机制。研究结果显示，夜蛾科昆虫的P450基因存在显著的谱系特异性扩张，且扩张主要集中于CYP3和CYP4家族簇。此类扩张定位于两个进化保守的基因组区域（位点1与位点2），这两个区域均包含超大尺寸的串联重复阵列。整合转座因子分布的分析结果表明，这两个位点呈现出截然不同的进化轨迹。在位点1中，局部转座因子密度与P450基因拷贝数之间存在显著正相关，这支持了转座因子介导的非等位同源重组模型。与之相反，位点2的重复序列含量虽低，但基因家族却发生了扩张，这暗示其在初始重复爆发后，经历了纯化选择下的结构稳定化过程。分子进化分析揭示，两个位点均广泛存在间歇性多样化选择的特征。结合杀虫剂胁迫下的转录组分析结果，此类选择模式反映出两种不同的适应性策略：位点2的旁系同源基因呈现高度协同的表达模式与稳定的选择强度，符合基因剂量效应（gene dosage effect）的特征。反之，位点1则表现出显著的转录异质性与强化的选择压力，提示其发生了功能亚功能化或特化。综上，本研究结果表明，保守P450基因簇的不同基因组架构与位点特异性调控动态，共同支撑了夜蛾科昆虫优异的代谢可塑性，为农业害虫的环境适应性进化提供了一套机制性框架。