Abstract

The wild ground squirrel ( Spermophilus dauricus ) is a typical seasonal breeder with distinct cyclical changes in ovarian function and follicular development. During the breeding season (BS), its ovaries contain primary follicles, secondary follicles, antral follicles, Graafian follicles, and corpora lutea; in contrast, only a small number of early-stage follicles exist in the non-breeding season (NBS), with no Graafian follicles or corpora lutea. This pronounced seasonal contrast reflects precise temporal regulation of follicular development and ovulatory activity. Folliculogenesis relies on adequate glucose metabolism (providing energy and essential substrates for follicular growth and oocyte maturation) and steroid hormones (regulating follicular maturation and ovulation). Using integrated multi-omics analyses and experimental validation, our study is the first to reveal that enhanced ovarian glucose metabolism is tightly coupled with elevated steroidogenesis during the BS, synergistically promoting follicular development and ovulatory competence. Conversely, glycogen synthase kinase-3β (GSK-3β)—a negative regulator of glucose metabolism—is upregulated in the NBS, acting as a novel regulatory target to maintain ovarian metabolic quiescence. These findings elucidate the coordinated dynamics of glucose metabolism and steroid hormone synthesis across the seasonal reproductive cycle, providing novel insights into the metabolic–endocrine crosstalk underlying seasonal follicular development in this species and the physiological mechanisms of periodic reproduction. Precise regulation of ovarian glucose metabolism and steroidogenesis is pivotal for the reproductive success of seasonal breeders. This study investigated seasonal variations in ovarian glucose metabolism and its association with follicular development and steroidogenesis in wild ground squirrels ( Spermophilus dauricus ). Results showed that ovarian weight and volume, and serum levels of luteinizing hormon