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Seasonal Change in Glucose Metabolism and Steroidogenesis in the Ovaries of Wild Ground Squirrels (Spermophilus dauricus)
by
, , and
Zhaomei Dong
,
Qingjing Gao
,
Pengyu Chen
,
Xi Wang
,
Yuning Liu
,
Haolin Zhang
,
Zhengrong Yuan
,
Yingying Han
* and
Qiang Weng
* Laboratory of Animal Physiology, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China
*
Authors to whom correspondence should be addressed.
Animals 2026, 16(3), 521; https://doi.org/10.3390/ani16030521 (registering DOI)
Submission received: 6 January 2026
/
Revised: 1 February 2026
/
Accepted: 5 February 2026
/
Published: 6 February 2026
(This article belongs to the Special Issue Advances in the Reproduction of Wild and Exotic Animals)
Simple Summary
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.
Abstract
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 hormone (LH), follicle-stimulating hormone (FSH), 17β-estradiol, and progesterone were significantly higher in the breeding season (BS) than in the non-breeding season (NBS). Ovarian glycogen content was elevated in the BS, whereas circulating glucose levels decreased remarkably. Histologically, the BS ovaries contained follicles at all developmental stages (primary to Graafian) and corpora lutea, while corpora lutea were absent in the NBS. Integrated transcriptomic and metabolomic analyses revealed upregulated glycogen synthesis, glycolytic pathways, and altered steroidogenic metabolites in the BS. Quantitative real-time PCR (qRT-PCR) confirmed higher expression of glucose transporter 1 (GLUT1), glucose metabolism-related enzymes (G6PD, PFKFB3, PFKM), glycogen synthase (GYS), and steroidogenic factors (StAR, P450scc, P450c17, 3β-HSD, P450arom) in the BS, whereas glycogen synthase kinase-3β (Gsk-3β) was upregulated in the NBS. Immunohistochemistry demonstrated colocalization of steroidogenic and glucose-metabolizing enzymes in granulosa and theca cells, and correlation analyses confirmed positive associations between glucose metabolism, steroidogenesis, and ovarian weight. Collectively, these findings indicate that enhanced ovarian glucose metabolism in the BS is tightly coupled with elevated steroidogenesis, synergistically promoting seasonal follicular development and ovulatory competence in this species.
