The landscape and evolutionary dynamics of derived lncRNAs in insects

Long noncoding RNAs (lncRNAs) function as crucial regulatory elements in eukaryotes, yet have remained largely unexplored across diverse insect lineages. We present a comprehensive analysis of lncRNA atlases across 115 insect species, identifying 647,691 multi-exonic lncRNAs with substantial variation (1119 to 40,850 per species). Our analysis reveals that lncRNA abundance correlates positively with both genome size and transposable element (TE) content. Approximately 500 diverse transcriptomes were found to represent the minimum threshold for comprehensive lncRNA identification. While most lncRNAs show limited sequence conservation, we identified 4806 derived lncRNAs that maintain syntenic relationships with protein-coding genes. These derived lncRNAs, which are significantly shaped by TE insertions, exhibit higher expression levels, greater regulatory complexity, and stronger functional conservation compared to conventional lncRNAs. They are primarily involved in regulating development and insect behavior. One such example is Msex-lnc-001918, which is derived from a conserved Lepidoptera orthogroup and retains ancestral functions in regulating spermatogenesis. This study provides fundamental insights into insect lncRNA evolution and demonstrates how the transformation of protein-coding genes can drive novel regulatory mechanisms in insect genomes.