Seasonal switches in testicular gene programs underlie spermatogenic plasticity in the large Japanese field mouse (Apodemus speciosus)

Seasonally bred mammals undergo cyclical changes in spermatogenesis to align their reproductive functions with the environmental conditions. The large Japanese field mouse ( Apodemus speciosus ), a rodent endemic to Japan, exhibits pronounced seasonal plasticity in its testicular activity, alternating between active spermatogenesis and testicular regression during the breeding and non-breeding seasons, respectively. However, the molecular mechanisms underlying this seasonal regulation are poorly understood. In this study, we conducted RNA sequencing of testicular tissues collected from wild A. speciosus during breeding and non-breeding seasons. Differential gene expression analysis identified 2,000 transcripts showing significant seasonal variations. Genes upregulated during the non-breeding season were associated with immune regulation, the oxidative stress response, and transcriptional repression. Gene Ontology enrichment analyses confirmed season-specific transitions in biological processes, such as gamete generation, hormone signaling, and immune homeostasis. These results suggest that A. speciosus employs a reversible and highly coordinated transcriptional program to toggle between the reproductively active and quiescent testicular states. This study represents the first testis-specific transcriptomic study of A. speciosus and provides novel insights into the molecular regulation of seasonal spermatogenesis in wild mammals. Our findings establish a valuable framework for future research on reproductive seasonality and contribute to a broader understanding of fertility adaptations under natural ecological conditions.