研究论文

捕食风险应激对雄性布氏田鼠及子代繁殖性能的影响

  • 周桃秀 ,
  • 陈琳 ,
  • 吴涌珍 ,
  • 杨生妹 ,
  • 魏万红 ,
  • 武瑞勇
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  • 扬州大学生物科学与技术学院, 扬州 225009
周桃秀(1999-),女,硕士研究生,主要从事动物行为生理生态学研究.E-mail:zhoutaoxiu@163.com

收稿日期: 2024-01-22

  修回日期: 2024-05-06

  网络出版日期: 2024-09-30

基金资助

国家自然科学基金(31770422,31900334);江苏省自然科学基金(BK20190910);中国博士后科学基金(2018M630610,2019T120468)

Effects of predation risk stress on the reproductive characteristics of male Brandt’s voles and their offspring

  • ZHOU Taoxiu ,
  • CHEN Lin ,
  • WU Yongzhen ,
  • YANG Shengmei ,
  • WEI Wanhong ,
  • WU Ruiyong
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  • College of Bioscience and Biotechnology, Yangzhou University, Yangzhou 225009, China

Received date: 2024-01-22

  Revised date: 2024-05-06

  Online published: 2024-09-30

摘要

本研究旨在探讨雄性布氏田鼠暴露于捕食风险应激对自身及后代繁殖性能的影响,以及这种效应的阶段性。青春期是动物生长发育和对外界环境敏感的重要阶段,推测青春期所经历的捕食风险应激对雄鼠和后代繁殖性能的影响更为显著。实验选取90日龄成年期和28日龄青春期雄性布氏田鼠作为亲代,每天分别暴露于蒸馏水、兔尿和猫尿1 h,连续18 d。随后每组随机选取一半田鼠取样检测性腺器官指数、精子质量和数量等参数,另一半与正常雌鼠交配,待后代成年后检测繁殖性能。结果显示,与对照相比,成年期和青春期暴露于猫气味的雄性布氏田鼠精子正常率显著下降,精子畸形率和死亡率显著升高,而暴露于兔气味的雄鼠仅降低了正常精子比例;成年期雄性田鼠暴露于猫气味没有影响繁殖输出,而青春期暴露的雄鼠的后代在出生时雌性比例显著增加;成年期暴露于猫气味和兔气味都没有影响后代的繁殖性能,青春期暴露于猫气味的雄鼠的后代成年后性腺指数、精子密度和精子正常率降低,精子畸形率和死亡率显著升高,而暴露于兔气味仅降低了雄性后代的精子密度和精子正常率。以上结果验证了本研究假设,即捕食风险应激对布氏田鼠亲代和后代的繁殖性能均有一定的抑制作用,且青春期应激的效应更强更持久,存在明显的效应阶段依赖性。

本文引用格式

周桃秀 , 陈琳 , 吴涌珍 , 杨生妹 , 魏万红 , 武瑞勇 . 捕食风险应激对雄性布氏田鼠及子代繁殖性能的影响[J]. 兽类学报, 2024 , 44(5) : 587 -597 . DOI: 10.16829/j.slxb.150904

Abstract

The present study aims to investigate whether predation risk stress can affect the reproductive characteristics of male Brandt’s voles (Lasiopodomys brandtii) and their offspring, and whether this is stage-specific. Adolescence is a crucial period for growth and development, and it is sensitive to external environmental factors. Thus, we speculated that exposure to predation risk stress during adolescence would have a more pronounced impact on the reproductive characteristics of both the males and their offspring. In this study, 90-day-old adult male Brandt’s voles and 28-day-old adolescent male Brandt’s voles were exposed to distilled water, rabbit urine, and cat urine for 1 hour daily for 18 consecutive days. Subsequently, half of each group was randomly selected for sampling to assess reproductive characteristics, including reproductive organ index, sperm quality and quantity. The remaining half was mated with a normal female, and their offspring's reproductive characteristics were evaluated until adulthood. The results indicated that, when compared to the control group, male Brandt’s voles exposed to cat odor during adulthood and adolescence significantly reduced normal sperm rate and increased sperm malformation and mortality rates, while exposure to rabbit odor only reduced the normal sperm rate. Exposure to cat odor during adulthood had no effect on reproductive output, whereas offspring from fathers exposed to cat odor during adolescence showed an increase in the ratio of female offspring at birth. Exposure to cat or rabbit odor during adulthood had no effect on offspring reproductive characteristics, but adult offspring from cat odor-exposed father during adolescence exhibited reduced gonadal index, sperm density, and normal sperm rate, as well as increased sperm deformity and mortality rates, while rabbit odor exposure only reduced sperm density and normal sperm rate in male offspring. These results confirmed our hypothesis that predation risk has a suppressive effect on the repro ductive characteristics of fathers and their offspring, especially during adolescence. The cross-generation transmission induced by paternal predation risk on offspring reproduction is stage-dependent.

参考文献

Azizi N, Roshan-Milani S, MahmoodKhani M, Saboory E, Gholinejad Z, Abdollahzadeh N, Sayyadi H, Chodari L. 2019. Parental pre-conception stress status and risk for anxiety in rat offspring:specific and sex-dependent maternal and paternal effects. Stressthe International Journal on the Biology of Stress, 22 (5):619-631.
Bian J H, Wu Y, Liu J K. 2005. Breeding behavior under temporal risk of predation in male root voles (Microtus oeconomus). Jour nal of Mammalogy, 86 (5):953-960.
Bian J H, Wu Y, Liu J K. 2004. Effects of maternal stress induced by predation risk on postnatal body mass growth and sex ratio in root voles (Microtus oeconomus). Acta Theriologica Sinica, 24 (2):139-144. (in Chinese)
Blas J, Bortolotti G R, Tella J L, Baos R, Marchant T A. 2007. Stress response during development predicts fitness in a wild, long lived vertebrate. Proceedings of the National Academy of Sciences of the United States of America, 104 (21):8880-8884.
Brass K E, Herndon N, Gardner S A, Grindstaff J L, Campbell P. 2020. Intergenerational effects of paternal predator cue exposure on behavior, stress reactivity, and neural gene expression. Hor mones and Behavior, 124:104806.
Castellano J M, Tena-Sempere M. 2016. Animal modeling of early programming and disruption of pubertal maturation. Endocrine Development, 29:87-121.
Clinchy M, Sheriff M J, Zanette L Y. 2013. Predator-induced stress and the ecology of fear. Functional Ecology, 27 (1):56-65.
Curley J P, Mashoodh R, Champagne F A. 2011. Epigenetics and the origins of paternal effects. Hormones and Behavior, 59 (3):306-314.
DeWitt P D, Visscher D R, Schuler M S, Thiel R P. 2019. Predation risks suppress lifetime fitness in a wild mammal. Oikos, 128 (6):790-797.
Dias B G, Ressler K J. 2014. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nature Neuroscience, 17 (1):89-96.
Fang J M, Sun R Y. 1989. Seasonal changes of Brandt's vole and their relation to burrows. Acta Theriologica Sinica, 9 (3):202-209. (in Chinese)
Firman R C, Tedeschi J N, Garcia-Gonzalez F. 2020. Sperm sex ratio adjustment in a mammal:perceived male competition leads to el evated proportions of female-producing sperm. Biology Letters, 16 (6):20190929.
Foufopoulos J, Zhao Y, Brock K M, Pafilis P, Valakos E D. 2023. Pre dation risk, and not shelter or food availability, as the main deter minant of reproduction investment in island lizards. Animals (Ba sel), 13 (23):3689.
Ganz D, Sher L. 2010. Suicidal behavior in adolescents with posttraumatic stress disorder. Minerva Pediatrica, 62 (4):363-370.
Gromov V S. 2023. Ecology and social behavior of the Brandt's vole:a generalized review. Journal of Arid Environments, 214:104994.
Gu C, Liu Y, Huang Y F, Yang S M, Wang A Q, Yin B F, Wei W H. 2020. Effects of predator-induced stress during pregnancy on re productive output and offspring quality in Brandt's voles(Lasiopodomys brandtii). European Journal of Wildlife Research, 66 (1):14.
Gu C, Wang W J, Ding X Q, Yang S M, Wang A Q, Yin B F, Wei W H. 2018. Effects of maternal stress induced by predator odors during gestation on behavioral and physiological responses of offspring in Brandt's vole (Lasiopodomys brandtii). Integrative Zoology, 13 (6):723-734.
Hegab I M, Shang G, Ye M, Jin Y, Wang A, Yin B, Yang S, Wei W. 2014. Defensive responses of Brandt's voles (Lasiopodomys brandtii) to chronic predatory stress. Physiology & Behavior, 126:1-7.
Humphrey E A, Crespi E, Travis J. 2020. Under pressure:Short and long-term response to predation varies in two populations of a live-bearing fish. Ethology, 126 (4):463-475.
Iribarne J, Brachetta V, Kittlein M, Schleich C, Zenuto R. 2023. Ef fects of acute maternal stress induced by predator cues on spatial learning and memory of offspring in the subterranean rodent Cte nomys talarum. Animal Cognition, 26 (6):1997-2008.
Lima S L. 2009. Predators and the breeding bird:behavioral and re productive flexibility under the risk of predation. Biological Re views, 84 (3):485-513.
Lupien S J, McEwen B S, Gunnar M R, Heim C. 2009. Effects of stress throughout the lifespan on the brain, behaviour and cogni tion. Nature Reviews Neuroscience, 10 (6):434-445.
Mahmoodkhani M, Saboory E, Roshan-Milani S, Azizi N, Karimipour M, Sayyadi H, Rasmi Y. 2018. Pre-pregnancy stress suppressed the reproductive systems in parents and changed sex ratio in off spring. Journal of Applied Biomedicine, 16 (4):370-377.
Marshall A D. 2016. Developmental timing of trauma exposure rela tive to puberty and the nature of psychopathology among adoles cent Girls. Journal of the American Academy of Child and Ado lescent Psychiatry, 55 (1):25-32.
Mateo J M. 2007. Ecological and hormonal correlates of antipredator behavior in adult Belding's ground squirrels (Spermophilus beld ingi). Behavioral Ecology and Sociobiology, 62 (1):37-49.
Middlemis M J, Werner E E, Denver R J. 2013. Stress hormones me diate predator-induced phenotypic plasticity in amphibian tad poles. Proceedings of the Royal Society B-Biological Sciences, 280 (1758):20123075.
Monclus R, Palomares F, Tablado Z, Martinez-Fonturbel A, Palme R. 2009. Testing the threat-sensitive predator avoidance hypothesis:physiological responses and predator pressure in wild rabbits. Oecologia, 158 (4):615-623.
Nan Y, Yi S J, Zhu H L, Xiong Y W, Shi X T, Cao X L, Zhang C, Gao L, Zhao L L, Zhang J, Xu D X, Wang H. 2020. Paternal cad mium exposure increases the susceptibility to diet-induced testicu lar injury and spermatogenic disorders in mouse offspring. Che mosphere, 246:125776.
O'Donnell S, Noseworthy M D, Levine B, Dennis M. 2005. Cortical thickness of the frontopolar area in typically developing children and adolescents. Neuroimage, 24 (4):948-954.
Park G, Ryu C, Kim S, Jeong S J, Koo J W, Lee Y S, Kim S J. 2021. Social isolation impairs the prefrontal-nucleus accumbens circuit subserving social recognition in mice. Cell Reports, 35 (6):109104.
Pang J Y, Li S, Liu Y, Yang S M, Wu R Y, Wei W H. 2022. Adolescent predatory risk alters the antipredator behavior and basal HPA axis activity of future offspring in Brandt's voles. Acta Theriologica Sinica, 42 (2):177-188. (in Chinese)
Payo-Payo A, Sanz-Aguilar A, Genovart M, Bertolero A, Piccardo J, Camps D, Ruiz-Olmo J, Oro D. 2018. Predator arrival elicits dif ferential dispersal, change in age structure and reproductive per formance in a prey population. Scientific Reports, 8 (1):1971.
Pellis S M, Hastings E, Shimizu T, Kamitakahara H, Komorowska J, Forgie M L, Kolb B. 2006. The effects of orbital frontal cortex damage on the modulation of defensive responses by rats in playful and nonplayful social contexts. Behavioral Neuroscience, 120(1):72-84.
Preisser E L, Bolnick D I, Benard M F. 2005. Scared to death? The ef fects of intimidation and consumption in predator-prey interac tions. Ecology, 86 (2):501-509.
Romero L M. 2004. Physiological stress in ecology:lessons from bio medical research. Trends in Ecology & Evolution, 19 (5):249-255.
Ruby E, Sher L. 2013. Prevention of suicidal behavior in adolescents with post-traumatic stress disorder. International Journal of Ado lescent Medicine and Health, 25 (3):283-293.
Shang G Z, Yang Y G, Zhu Y H, Wu X Q, Cao Y F, Wu Y, Bian J H. 2020. A complex regulating pattern induced by the effects of pre dation and parasites on root vole (Microtus oeconomus) popula tions during the breeding season. Journal of Mammalogy, 101(5):1345-1355.
Shang G Z, Zhu Y H, Wu Y, Cao Y F, Bian J H. 2019. Synergistic ef fects of predation and parasites on the overwinter survival of root voles. Oecologia, 191 (1):83-96.
Sievert T, Haapakoski M, Palme R, Voipio H, Ylonen H. 2019. Sec ondhand horror:effects of direct and indirect predator cues on be havior and reproduction of the bank vole. Ecosphere, 10 (6):e02765.
St-Cyr S, Abuaish S, Sivanathan S, McGowan P O. 2017. Maternal programming of sex-specific responses to predator odor stress in adult rats. Hormones and Behavior, 94:1-12.
Stein L R, Bell A M. 2014. Paternal programming in sticklebacks. Animal Behaviour, 95:165-171.
Vinterstare J, Hulthen K, Nilsson P A, Nilsson S H, Bronmark C. 2020. Experimental manipulation of perceived predation risk and cortisol generates contrasting trait trajectories in plastic crucian carp. Journal of Experimental Biology, 223 (4):jeb213611.
Voznessenskaya V V, Malanina T V. 2013. Effect of chemical signals from a predator (Felis catus) on the reproduction of Mus muscu lus. Doklady Biological Sciences, 453:362-364.
Wang H Y, Han F, Zhong N Z, Lu Y P. 2017. Research progress of chronic stress on adolescent brain damage and implications for education. Journal of Bio-education, 5 (2):95-100. (in Chinese)
Wang R W, Wang Y Q, He J Z, Li Y T. 2013. Resource elasticity of offspring survival and the optimal evolution of sex ratios. PLoS ONE, 8 (1):e53904.
Wang T L, Zhang X Y, Fu R S, Wang D H. 2015. Trade-off between growth and reproduction in male offspring of Brandt's voles from low body mass parents. Acta Theriologica Sinica, 35 (4):389-397. (in Chinese)
Weterings M J A, Losekoot S, Kuipers H J, Prins H H T, Langevelde F, Wieren S E. 2022. Influence of multiple predators decreases body condition and fecundity of European hares. Ecology and Evolution, 12 (1):e8442.
Wright L D, Muir K E, Perrot T S. 2012. Enhanced stress responses in adolescent versus adult rats exposed to cues of predation threat, and peer interaction as a predictor of adult defensiveness. Devel opmental Psychobiology, 54 (1):47-69. Wu R Y, Huang Y F, Liu Y, Shen Q Y, Han Y X, Yang S M, Wei W H. 2020. Repeated predator odor exposure alters maternal behavior of postpartum Brandt's voles and offspring's locomotor activity. Behavioural Processes, 177:104143.
Wu R Y, Li S, Huang Y F, Pang J Y, Cai Y J, Zhang X Y, Jiang T Y, Yang S M, Wei W H. 2022. Postpartum maternal exposure to predator odor alters offspring antipredator behavior, basal HPA axis activity and immunoglobulin levels in adult Brandt's voles. Behavioural Brain Research, 416:113532.
Wu R Y, Wu X Y, Li S, Li G, Jiang Z Y, Zhong H C, Wang B, Yang S M, Wei W H. 2021. Predator odor exposure increases social con tact in adolescents and parental behavior in adulthood in Brandt's voles. Behavioural Processes, 186:104372.
Yang Y G, Shang G Z, Bian J H. 2021. The effects of coccidian infec tion and predators on reproductive performance of root vole (Alex andromys oeconomus). Acta Theriologica Sinica, 41 (6):676-684. (in Chinese)
Yeshurun S, Rogers J, Short A K, Renoir T, Pang T Y, Hannan A J. 2017a. Elevated paternal glucocorticoid exposure modifies memory retention in female offspring. Psychoneuroendocrinol ogy, 83:9-18.
Yeshurun S, Short A K, Bredy T W, Pang T Y, Hannan A J. 2017b. Pa ternal environmental enrichment transgenerationally alters affec tive behavioral and neuroendocrine phenotypes. Psychoneuroen docrinology, 77:225-235.
Yin B F, Yang S M, Shang G Z, Wei W H. 2017. Effects of predation risk on behavior, hormone levels, and reproductive success of pla teau pikas. Ecosphere, 8 (1):e1643.
Zaidan H, Gaisler-Salomon I. 2015. Prereproductive stress in adoles cent female rats affects behavior and corticosterone levels in second-generation offspring. Psychoneuroendocrinology, 58:120-129.
Zhang H, Shan L D, Aniagu S, Jiang Y, Chen T. 2022. Paternal acryl amide exposure induces transgenerational effects on sperm param eters and learning capability in mice. Food and Chemical Toxicol ogy, 161:112817.
Zhang Z B, Pech R, Davis S, Shi D Z, Wan X R, Zhong W Q. 2003.
Extrinsic and intrinsic factors determine the eruptive dynamics of Brandt's voles Microtus brandti in Inner Mongolia, China. Oikos, 100 (2):299-310.
王同亮, 张学英, 付荣恕, 王德华. 2015. 布氏田鼠双亲低体重导致雄性后代生长和繁殖间的权衡. 兽类学报, 35 (4):389-397.
王慧莹, 韩菲, 钟能政, 鲁亚平. 2017. 慢性应激对青春期大脑损伤的研究进展及教育启示. 教育生物学杂志, 5 (2):95-100
边疆晖, 吴雁, 刘季科. 2004. 根田鼠母体捕食应激效应与Trivers-Willard 模型的关系. 兽类学报, 24 (2):139-144.
杨元罡, 尚国珍, 边疆晖. 2021. 球虫感染与捕食对根田鼠繁殖性能的影响. 兽类学报, 41 (6):676-684.
庞金月, 李陕, 刘园, 杨生妹, 武瑞勇, 魏万红. 2022. 布氏田鼠母体青春期捕食风险应激对后代反捕食行为和 HPA 轴基础活动水平的影响. 兽类学报, 42 (2):177-188.
房继明, 孙儒泳. 1989. 布氏田鼠种群数量的季节动态与鼠洞的关系. 兽类学报, 9 (3):202-209.
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