Functional regulation of testosterone underlying state transition in seasonal spermatogenesis of Plateau Pika (Ochotona curzoniae)

• Published in: Journal of mammalogy 2024-09, Vol.105 (5), p.1105-1116
• Main Authors: Wang, Yujun, Duo, Hairui, Li, Shuang, Zhang, Xiaoqian, Tao, Haiping, Fang, Yougui, Jia, Gongxue, Yang, Qien
• Format: Article
• Language: English
• ISSN: 0022-2372; 1545-1542
• DOI: 10.1093/jmammal/gyae053

Abstract Seasonal reproduction is an adaptive strategy that benefits the survival and growth of offspring. However, the regulatory mechanisms affecting spermatogenesis in male seasonal breeders are not well understood. We examined the actions of testosterone on seasonal spermatogenesis of Plateau Pika (Ochotona curzoniae), a typical long-day breeder living on the Qinghai–Tibetan Plateau. The annual dynamics of germ cell development and steroid hormone synthesis were confirmed and were consistent with testicular morphology. Furthermore, a testosterone regulation experiment showed that elevated testosterone stimulated proliferation of spermatogonia and regeneration of advanced spermatogenic cells in reproductively dormant pika, while testosterone suppression induced cell apoptosis both in reproductively active and dormant pikas. Transcriptomic analyses indicated that testosterone-regulated genes related to spermatogonial fate determination by binding to androgen receptors and inducing the production of retinoic acid, which was responsible for the initiation of spermatogonial differentiation. We show that testosterone orchestrates downstream signaling pathways to balance spermatogonial self-renewal and development. These findings provide a new perspective on seasonal regulation of mammalian spermatogenesis. In this paper, we show testosterone serves double duty on the transition of spermatogonial development in Plateau Pika through orchestrating gene expression related with retinoic acid signaling and response to androgen receptor, providing insight into regulation of seasonal spermatogenesis in male breeders.