Audible Sound Stress Alters Behavior and Gene Transcription, and Negatively Impacts Development, Survival and Reproductive Fitness in Spodoptera frugiperda

Moth auditory systems, evolutionarily adapted and structurally diverse with ultrasonic sensitivity, underpin the development of acoustic-based pest management strategies. Here, based on hypotheses derived from previous findings, we tested whether and how audible sounds (music, bird chirp, noise; 0.25–1 kHz, 80/120 dB) affect the development, survival, behavior and fecundity, as well as the molecular responses, using both short-term and long-term exposure (three successive generations) experimental designs. Behavioral assays showed dose-specific responses: high-intensity (120 dB) bird chirp and noise suppressed larval and adult activity, while low-intensity (80 dB) counterparts promoted larval crawling. Long-term exposure revealed that bird chirp and noise significantly impaired fitness, reducing larval/pupal body weight, pupation/eclosion rates, and egg hatching rate, with 120 dB noise exerting the strongest effects; 80 dB music showed neutral or positive impacts. Transcriptomic analysis identified 71–235 differentially expressed genes (DEGs) across treatment groups, with bird chirp and noise inducing more downregulated DEGs related to metabolism, immunity, and development. Notably, all cuticle-related DEGs in the 80 dB noise group and 53.2% in the 120 dB noise group were upregulated, suggesting stress-induced cuticular remodeling. GO/KEGG enrichment indicated distinct patterns: 80 dB music, bird chirp and 120 dB noise groups only had downregulated DEGs enriched in certain terms/pathways, mainly associated with cellular components; the 80 dB noise group had upregulated DEGs enriched in sensory, cuticle, metabolism and longevity-related terms/pathways, and downregulated DEGs in metabolism and human disease-related terms/pathways. Analysis of the expression patterns of all the longevity pathway-related genes suggested that sound stress induces lifespan regulation in this insect. These findings clarify S. frugiperda’s multidimensional responses to audible sound, providing a foundation for sound-based pest management.