Reproductive K-strategy in a subterranean rodent: Delayed ovarian development and restricted ovulation in Rhizomys pruinosus

Subterranean rodents have evolved a suite of traits that are adapted to hypoxic and energy-limited environments. Among these, reduced fertility is a hallmark. The hoary bamboo rat (Rhizomys pruinosus) has a remarkably low litter size (2-4). We compare ovarian development in hoary bamboo rat with a representative of an above-ground highly fertile rat, the Sprague-Dawley (SD) rat, by way of combined histological, physiological, and molecular analyses. Compared with SD rats, hoary bamboo rats have delayed ovarian development, extensive atresia of dominant follicles, and restricted ovulation (reflected by a lower proportion of mature follicles and corpora lutea). Physiologically, they have markedly lower levels of luteinizing hormone, follicle-stimulating hormone, testosterone, and estrogen, and significantly downregulated positive follicular regulators and upregulated negative regulators promoting atresia across developmental stages. Transcriptomic analysis reveals a global shift in transcriptional regulation in them during ovarian development, with hub gene modules correlating positively with age being enriched in pathways related to autophagy, apoptosis, lysosome, and cell cycle arrest. We posit that low fecundity in subterranean rodents is both a passive consequence of environmental constraints and an actively reinforced and maintained adaptive strategy. This is manifested in delayed ovarian development and restricted ovulation, driven by attenuated hormonal stimulation and enhanced negative regulation of follicular survival, and is closely associated with enrichment of pro-apoptotic and growth-suppressive pathways. These “delayed ovarian maturation and constrained ovulation” characteristics represent a “K-strategy”, enabling energy balance and population stability in closed underground ecosystems by reducing reproductive costs and slowing population growth.