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

Abstract 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 s...

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Main Authors: Lewen Wang, Yaqi Ying, Ying Song, Ning Li, Xiao-Hui Liu, Dawei Wang
Format: Article
Language:English
Published: BMC 2025-04-01
Series:Zoological Letters
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Online Access:https://doi.org/10.1186/s40851-025-00251-6
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author Lewen Wang
Yaqi Ying
Ying Song
Ning Li
Xiao-Hui Liu
Dawei Wang
author_facet Lewen Wang
Yaqi Ying
Ying Song
Ning Li
Xiao-Hui Liu
Dawei Wang
author_sort Lewen Wang
collection DOAJ
description Abstract 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.
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issn 2056-306X
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spelling doaj-art-991bf833625f40b484c55a5310f999912025-08-20T02:55:24ZengBMCZoological Letters2056-306X2025-04-0111111510.1186/s40851-025-00251-6Photo-refractoriness reflects bet-hedging strategies deployed in unpredictable environments in male Brandt’s volesLewen Wang0Yaqi Ying1Ying Song2Ning Li3Xiao-Hui Liu4Dawei Wang5State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesState Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural SciencesAbstract 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.https://doi.org/10.1186/s40851-025-00251-6PhotoperiodismBrandt’s voleTesticular developmentPhoto-refractorinessBet-hedging
spellingShingle Lewen Wang
Yaqi Ying
Ying Song
Ning Li
Xiao-Hui Liu
Dawei Wang
Photo-refractoriness reflects bet-hedging strategies deployed in unpredictable environments in male Brandt’s voles
Zoological Letters
Photoperiodism
Brandt’s vole
Testicular development
Photo-refractoriness
Bet-hedging
title Photo-refractoriness reflects bet-hedging strategies deployed in unpredictable environments in male Brandt’s voles
title_full Photo-refractoriness reflects bet-hedging strategies deployed in unpredictable environments in male Brandt’s voles
title_fullStr Photo-refractoriness reflects bet-hedging strategies deployed in unpredictable environments in male Brandt’s voles
title_full_unstemmed Photo-refractoriness reflects bet-hedging strategies deployed in unpredictable environments in male Brandt’s voles
title_short Photo-refractoriness reflects bet-hedging strategies deployed in unpredictable environments in male Brandt’s voles
title_sort photo refractoriness reflects bet hedging strategies deployed in unpredictable environments in male brandt s voles
topic Photoperiodism
Brandt’s vole
Testicular development
Photo-refractoriness
Bet-hedging
url https://doi.org/10.1186/s40851-025-00251-6
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