Photo-refractoriness reflects bet-hedging strategies deployed in unpredictable environments in male Brandt’s voles

Day length, also known as photoperiod, is an important reproductive regulatory factor in most seasonal breeders. Brandt's vole, a long-day breeder, exhibits significant differentces in reproductive development depending on the photoperiod of the season of birth, as is seen in other rodent seasonal breeders. However, there is a lack of comprehensive studies on the effects of photoperiod across different seasons. In the present study, we investigated the impact of long (LP) and short photoperiod (SP) on postnatal development in male voles. We measured somatic and testicular parameters from weaning at three postnatal weeks (PNW3) to PNW19, weighed testis mass from birth, and confirmed the status of testicular development by observing the histological features of the seminiferous epithelium. The results showed no difference in testis mass between LP and SP males up to PNW3, with normal initiation of intratubular meiosis and the presence of leptotene/zygotene spermatocytes in both groups. From PNW4 to PNW10, SP males displayed slower growth in both somatic and testicular parameters and showed suppressed development of primary spermatocytes and Leydig cells compared to LP males. After PNW10, both groups experienced photo-refractoriness, characterized by a reversal of gonadal activity. During this stage, SP voles spontaneously initiated gonadal development and resumed the meiotic process, while LP males showed testicular degeneration accompanied by a progressive loss of germ cells ranging from spermatids to primary spermatocytes. Until PNW19, both groups reached similar testis size and mass. Interestingly, this refractoriness was observed in only half of the males in each group, suggesting a bet-hedging survival strategy that allows populations to cope with unpredictable environmental changes, such as fluctuations in temperature and food. These findings highlight the importance of photoperiod as a key environmental factor in influencing sexual maturation in young Brandt's voles, and indicate that the impact of photoperiod in adult voles can be flexible in vole adulthood, varying according to their natural life cycle. This suggests a bet-hedging survival strategy of photo-refractoriness with complex interactions between environmental cues and life history traits.