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Although the importance of transposable elements (TEs) in epigenetic research is well recognized, their specific role in honeybee caste differentiation has not been fully explored. This study reveals a novel regulatory mechanism where the microRNA (miRNA) ame-mir-3721-3p, derived from ApME (Apis miniature inverted-repeat TEs), suppresses DNA methyltransferase gene DNMT3, promoting queen-like development in honeybee larvae. Genome-wide analysis identified 43 ApME elements in Apis, with ApMETm15 being particularly abundant and species-specific. These elements gave rise to 6 miRNAs, including ame-mir-3721-3p which showed notable regulatory potential. Target gene prediction and luciferase reporter assays confirmed that ame-mir-3721-3p binds to and suppresses DNMT3 expression. Spatiotemporal expression analysis indicated that ame-mir-3721-3p is significantly upregulated during the critical L3 larval stage, exhibiting a similar expression pattern to DNMT3. Larval feeding experiments with agomir demonstrated that ame-mir-3721-3p suppresses DNMT3 expression and significantly impacts the expression of genes related to the juvenile hormone and ecdysone pathways. Further physiological evidence showed that when larvae were treated with agomir-3721 during the critical caste differentiation window (L3-L4 stage), the emerging adult bees exhibited increased body size, doubled ovarian area, and significantly higher frequency of ovary development, with significant upregulation of ovarian-specific marker genes. These findings provide direct evidence for ame-mir-3721-3p's role in promoting queen-like developmental trajectories during caste differentiation, uncovering a new regulatory pathway in honeybee development and offering insights into epigenetic mechanisms in social insects.<\/jats:p>","DOI":"10.1093\/molbev\/msaf074","type":"journal-article","created":{"date-parts":[[2025,4,19]],"date-time":"2025-04-19T10:26:36Z","timestamp":1745058396000},"source":"Crossref","is-referenced-by-count":9,"title":["Comprehensive Genomic Analysis Reveals Novel Transposable Element-Derived MicroRNA Regulating Caste Differentiation in Honeybees"],"prefix":"10.1093","volume":"42","author":[{"ORCID":"https:\/\/orcid.org\/0009-0009-3975-8648","authenticated-orcid":false,"given":"Yan","family":"Jiang","sequence":"first","affiliation":[{"name":"College of Life Sciences, Chongqing Normal University , Chongqing ,","place":["China"]},{"name":"Key Laboratory of Pollinator Resources Conservation and Utilization of the 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