Torpor expression is associated with differential spermatogenesis in hibernating eastern chipmunks

Hibernators suppress physiological processes when expressing torpor, yet little is known about the effects of torpor on male reproductive physiology. Studies of hibernating mammals suggest that deep torpor negatively impacts spermatogenesis and that transitions between torpor and euthermic arousals increase cellular oxidative stress, with potentially damaging effects on sperm. Here, we hypothesize that variation in torpor expression affects the reproductive readiness of hibernators by impacting their sperm production. To test this, we examined the relationship between torpor expression and spermatogenesis in captive eastern chipmunks (Tamias striatus). We determined torpor depth with temperature data loggers and assessed its relationship with spermatogenesis by examining spermatogenic progression, cell division, sperm counts, sperm maturity, and DNA damage. We show that deep hibernators (high levels of torpor) largely halted spermatogenesis in late hibernation in comparison with shallow hibernators (low levels of torpor), where ongoing spermatogenesis was observed. Despite these differences in spermatogenic state during hibernation, spermatogenic progression, sperm numbers, and maturity did not differ in spring, potentially reflecting similar degrees of reproductive readiness. Interestingly, shallow hibernators exhibited higher rates of DNA damage in spermatogenic cells during hibernation, with this trend reversing in spring. Our results thus indicate that once heterothermy is terminated, deep hibernators resume spermatogenesis but are characterized by higher rates of DNA damage in spermatogenic cells at the seasonal stage when spring mating commences. Therefore, our study confirmed posthibernation recovery of sperm production but also a potential impact of deep torpor expression during winter on DNA damage in spring.