Ground squirrels initiate sexual maturation during hibernation

Rafael Dai Pra; Sarah M Mohr; Dana K Merriman; Sviatoslav N Bagriantsev; Elena O Gracheva

doi:10.1016/j.cub.2022.02.032

Ground squirrels initiate sexual maturation during hibernation

Curr Biol. 2022 Apr 25;32(8):1822-1828.e4. doi: 10.1016/j.cub.2022.02.032. Epub 2022 Mar 3.

Authors

Rafael Dai Pra¹, Sarah M Mohr¹, Dana K Merriman², Sviatoslav N Bagriantsev³, Elena O Gracheva⁴

Affiliations

¹ Department of Cellular and Molecular Physiology, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510, USA; Department of Neuroscience, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510, USA; Program in Cellular Neuroscience, Neurodegeneration and Repair, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510, USA.
² Department of Biology, University of Wisconsin-Oshkosh, 800 Algoma Boulevard, Oshkosh, WI 54901, USA.
³ Department of Cellular and Molecular Physiology, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510, USA. Electronic address: slav.bagriantsev@yale.edu.
⁴ Department of Cellular and Molecular Physiology, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510, USA; Department of Neuroscience, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510, USA; Program in Cellular Neuroscience, Neurodegeneration and Repair, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510, USA. Electronic address: elena.gracheva@yale.edu.

PMID: 35245461
DOI: 10.1016/j.cub.2022.02.032

Abstract

Adequate nutrition is essential for normal reproductive function, which is vital for species to survive. In humans and other mammals, starvation and undernutrition deplete fat reserves and cause weight loss, attenuating the function of the reproductive axis and causing hypogonadism.^1-4 Thirteen-lined ground squirrels (Ictidomys tridecemlineatus) spend 7 months of every year in hibernation without food and water. Hibernating squirrels alternate between periods of torpor and interbout arousal (IBA), when animals temporarily return to an active-like state.⁵ The physiological significance of IBA is unclear, but it is thought to be essential for hibernation in animals that drop their body temperature to 2°C-4°C during torpor. Here, we report that juvenile male ground squirrels initiate reproductive maturation during their first hibernation season, despite prolonged undernutrition and profound weight loss. We show that the hypothalamic reproductive axis undergoes activation during interbout arousals in the middle of hibernation, triggering production of luteinizing hormone and testosterone, and promoting testicular growth. Initiation of sexual maturation is circannually entrained and is independent of physiological state, ambient temperature, and food availability. Our study suggests a role for interbout arousals during hibernation and uncovers the neurophysiological mechanism of reproductive axis activation during conditions of extreme negative energy balance. VIDEO ABSTRACT.

Keywords: energy balance; ground squirrel; hibernation; hypothalamic reproductive axis; sexual maturation.

Publication types

Video-Audio Media
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural

MeSH terms

Animals
Hibernation* / physiology
Male
Malnutrition*
Sciuridae / physiology
Sexual Maturation
Weight Loss

Grants and funding

R24 HD102061/HD/NICHD NIH HHS/United States