嗅觉在绵羊母性识别中的作用及信号传导机制

doi:10.13287/j.1001-9332.202501.033

摘要/Abstract

摘要： 家畜母性行为是幼畜出生前后母畜所表现出的与分娩和育幼有关的行为,包括筑窝、分娩、清理仔畜、识别仔畜、授乳、养育和保护等行为,这些行为可为仔畜提供丰富的社交经验和生存技能,对物种的延续及种群的稳定具有重要意义。母性识别是决定母畜授乳、养育和保护等母性行为表达的前提。绵羊在分娩后能迅速且专一地识别自己的羔羊,并与之建立紧密的母子联系,分娩后的4～6 h是母羊识别羔羊的关键时期,且嗅觉是决定母性识别成功与否的重要途径。由嗅黏膜、主嗅球参与构成的主嗅觉系统以及犁鼻器、副嗅球构成的副嗅觉系统介导母羊对羔羊气味的识别和记忆,但其中所涉及的嗅觉信号传导机制尚缺乏系统性总结。生产中,因母性行为差异导致的哺乳期羔羊的高死亡率是困扰养殖业的难题,系统性回顾和总结嗅觉在绵羊母性识别中的作用对改善母性行为、提高羔羊成活率尤为重要。本文综述了嗅觉在绵羊母性识别中的作用、主嗅觉系统和副嗅觉系统参与母性识别的结构和功能,主嗅觉系统通过G蛋白(Golf)-AC3-cAMP介导的cAMP信号通路和催产素受体(OTR)-Gq-PLC-IP₃介导的IP₃信号途径参与嗅觉信号传导,而G_αi2/G_αo-PLC-IP₃/DAG途径介导副嗅觉系统的嗅觉信号传导。本文可为深入了解母性识别的嗅觉信号传导机制以及母性行为改善策略提供参考。

关键词: 母性识别, 主嗅觉系统, 副嗅觉系统, 结构和功能, 信号途径

Abstract: Maternal behavior of domestic animals refers to the behaviors related to delivery and rearing of offspring, including nesting, delivery, grooming, recognition, lactation, rearing and protection of the young. These behaviors can provide rich social experience and survival skills for young, which are important for the continuation of species and population stability. Maternal recognition of the young is the first step in the initiation of maternal behaviors, such as lactation, nurturing, and protection. Ewes can quickly and exclusively recognize their lambs after giving birth and establish a strong mother-young bond. The 4-6 h period after delivery is particularly important because it is the critical period for ewes to recognize their lambs, in which olfaction plays a key role. The main olfactory system, which consists of the olfactory mucosa and the main olfactory bulb, and the accessory olfactory system, which consists of the vomeronasal organ and the accessory olfactory bulb, can mediate ewes’ recognition and memory of lamb odors. A systematic summary of the olfactory signaling mechanisms is lacking. Given that the high mortality rate of lactating lambs due to poor maternal behavior is a challenge in the farming industry, a systematic review and summary of the role of olfaction in maternal recognition in sheep is particularly important for improving maternal behavior and lamb survival. Here, we reviewed the role of olfaction in maternal recognition in sheep, as well as the structures and functions involved in maternal recognition of the main and accessory olfactory systems. The cAMP signaling pathway mediated by G protein (Golf)-AC3-cAMP and the IP₃ signaling pathway mediated by (OTR)-Gq-PLC-IP₃ have been considered as the main pathways involved in olfactory signaling in the main olfactory system. The olfactory signaling function in the accessory olfactory system is mediated by the G_αi2/G_αo -PLC-IP₃/DAG pathway. It would offer a theoretical reference for further understanding of the olfactory signal transduction mechanism of maternal recognition and maternal behavior improvement strategies.

Key words: maternal recognition, main olfactory system, accessory olfactory system, structure and function, signaling

王慧, 王悦尚, 韩成全, 胡希怡, 杨燕, 吕慎金. 嗅觉在绵羊母性识别中的作用及信号传导机制[J]. 应用生态学报, 2025, 36(1): 318-326.

WANG Hui, WANG Yueshang, HAN Chengquan, HU Xiyi, YANG Yan, LYU Shenjin. Progress on the role of olfaction in maternal recognition and its signaling mechanism in sheep[J]. Chinese Journal of Applied Ecology, 2025, 36(1): 318-326.

参考文献

[1] Mier Quesada Z, Portillo W, Paredes RG. Behavioral evidence of the functional interaction between the main and accessory olfactory system suggests a large olfactory system with a high plastic capability. Frontiers in Neuroanatomy, 2023, 17: 1211644
[2] McGann JP. Poor human olfaction is a 19th-century myth. Science, 2017, 356: 6338
[3] 杨瑜, 李鸣, 陈红. 母性应激对母性行为和心理功能的影响. 心理科学进展, 2020, 28(1): 128-140
[4] 韩成全, 王慧, 王健伟, 等. 塑化剂对母性行为干扰效应及其潜在机制的研究进展. 应用生态学报, 2023, 34(11): 3157-3168
[5] 王慧, 王悦尚, 李富宽, 等. 绵羊母性行为及其神经、内分泌、分子机制研究进展. 中国农业大学学报, 2019, 24(5): 67-72
[6] Wang H, Han CQ, Li M, et al. Effects of parity, litter size and lamb sex on maternal behavior of small Tail Han sheep and their neuroendocrine mechanisms. Small Ruminant Research, 2021, 202: 106451
[7] Viviers MZ, Burger BV, Ie Roux NJ, et al. Temporal changes in the neonatal recognition cue of Dohne Merino lambs (Ovis aries). Chemical Senses, 2014, 39: 249-262
[8] Dhaoui A, Chniter M, Lévy F, et al. Does lambing season affect mother-young relationships and lamb vigor in d’Man sheep reared in oases? Animal, 2020, 14: 2363-2371
[9] Medina PM, Trujillo AO, Tirado EA, et al. Sensory factors involved in mother-young bonding in sheep: A review. Veterinarni Medicina, 2016, 61: 595-611
[10] Levy F, Keller M, Poindron P. Olfactory regulation of maternal behavior in mammals. Hormones and Beha-vior, 2004, 46: 284-302
[11] Burger BV, Viviers MZ, Le Roux NJ, et al. Olfactory cue mediated neonatal recognition in sheep, Ovis aries. Journal of Chemical Ecology, 2011, 37: 1150-1163
[12] Mota-Rojas D, Bienboire-Frosini C, Marcet-Rius M, et al. Mother-young bond in non-human mammals: Neonatal communication pathways and neurobiological basis. Frontiers in Psychology, 2022, 13: 1064444
[13] Morgan PD, Boundy CAP, Arnold GW, et al. The roles played by the senses of the ewe in the location and the recognition of lambs. Applied Animal Ethology, 1975, 1: 139-159
[14] Baldwin BA, Shillito EE. The effects of ablation of the olfactory bulbs on parturition and maternal behaviour in Soay sheep. Animal Behaviour, 1974, 22: 220-223
[15] Ferreira G, Terrazas A, Poindron P, et al. Learning of olfactory cues is not necessary for early lamb recognition by the mother. Physiology & Behavior, 2000, 69: 405-412
[16] Riviere S, Challet L, Fluegge D, et al. Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors. Nature, 2009, 459: 574-577
[17] Poindron P, Levy F, Krehbiel D. Genital, olfactory and endocrine interactions in the development of maternal behavior in the parturient ewe. Psychoneuroendocrinology, 1988, 13: 99-125
[18] Corona R, Meurisse M, Cornilleau F, et al. Exposure to young preferentially activates adult-born neurons in the main olfactory bulb of sheep mothers. Brain Structure and Function, 2017, 222: 1219-1229
[19] Poindron P. Mother-young relationships in intact or anosmic ewes at the time of suckling. Biology of Beha-viour, 1976, 2: 161-177
[20] Nowak R, Keller M, Lévy F, et al. Mother-young relationships in sheep: A model for a multidisciplinary approach of the study of attachment in mammals. Journal of Neuroendocrinology, 2011, 23: 1042-1053
[21] Kendrick KM, Lévy F, Keverne EB. Changes in the sensory processing of olfactory signals induced by birth in sheep. Science, 1992, 256: 833-836
[22] Poindron P, Lévy F, Keller M. Maternal responsiveness and maternal selectivity in domestic sheep and goats: The two facet of maternal attachment. Developmental Psychobiology, 2007, 49: 54-70
[23] Wyatt TD. Pheromones and Animal Behaviour: Communication by Smell and Taste. Cambridge: Cambridge University Press, 2003
[24] Wyatt TD. Pheromones and signature mixtures: Defining species-wide signals and variable cues for identity in both invertebrates and vertebrates. Journal of Comparative Physiology A: Neuroethology Sensory Neural and Behavioral Physiology, 2010, 196: 685-700
[25] Poindron P, Otal J, Ferreira G, et al. Amniotic fluid is important for the maintenance of maternal responsiveness and the establishment of maternal selectivity in sheep. Animal, 2010, 4: 2057-2064
[26] Alexander G, Stevens D. Recognition of washed lambs by Merino ewes. Applied Animal Ethology, 1981, 7: 77-86
[27] Poindron P. The behaviour of sheep: Biological principles and implications for production. Livestock Production Science, 1993, 34: 308-309
[28] Burger BV, Marx B, le Roux M, et al. Development of second-generation sample enrichment probe (SEP) for improved sorptive analysis of volatile organic compounds. Journal of Chromatography A, 2011, 1218: 1567-1575
[29] Levy F, Poindron P. The importance of amniotic fluids for the establishment of maternal behavior in experienced and inexperienced ewes. Animal Behaviour, 1987, 35: 1188-1192
[30] Martinez MGR, Gonzalez RS, Massot PP, et al. Maternal behaviour around birth and mother-young recognition in Pelibuey sheep. Veterinaria Mexico, 2011, 42: 27-45
[31] Alexander G, Stevens D, Bradley LR. Washing lambs and confinement as aids to fostering. Applied Animal Ethology, 1983, 10: 251-261
[32] Wysocki CJ, Nyby J, Whitney G, et al. The vomeronasal organ: Primary role in mouse chemosensory gender recognition. Physiology and Behavior, 1982, 29: 315-327
[33] Vazquez R, Orihuela A, Flores-Perez FI, et al. Redu-cing early maternal licking of male lambs (Ovis aries) does not impair their sexual behavior in adulthood. Journal of Veterinary Behavior, 2015, 10: 78-82
[34] Booth KK, Katz LS. Role of the vomeronasal organ in neonatal offspring recognition in sheep. Biology of Reproduction, 2000, 63: 953-958
[35] Levy F, Locatelli A, Piketty V, et al. Involvement of the main but not the accessory olfactory system in maternal behavior of primiparous and multiparous ewes. Phy-siology and Behavior, 1995, 57: 97-104
[36] Romeyer A, Poindron P, Orgeur P. Olfaction mediates the establishment of selective bonding in goats. Physio-logy and Behavior, 1994, 56: 693-700
[37] 王建礼, 邰发道. 哺乳动物嗅觉与母性识别. 动物学杂志, 2010, 45(5): 170-176
[38] Tufo C, Poopalasundaram S, Dorrego-Rivas A, et al. Development of the mammalian main olfactory bulb. Development, 2022, 149: dev200210
[39] Restrepo D, Arellano J, Oliva AM, et al. Emerging views on the distinct but related roles of the main and accessory olfactory systems in responsiveness to chemosensory signals in mice. Hormones and Behavior, 2004, 46: 247-256
[40] Castro AE, Young LJ, Camacho FJ, et al. Effects of mating and social exposure on cell proliferation in the adult male prairie vole (Microtus ochrogaster). Neural Plasticity, 2020, 2020: 8869669
[41] Buck L, Axel R. A novel multigene family may encode odorant receptors: A molecular basis for odor recognition. Cell, 1991, 65: 175-187
[42] Mori K, Takahashi YK, Igarashi KM, et al. Maps of odorant molecular features in the mammalian olfactory bulb. Physiological Reviews, 2006, 86: 409-433
[43] Goldstein BJ, Matsunami H. The Olfactory System. New York: Humana Press, 2023
[44] Wang IH, Murray E, Andrews G, et al. Spatial transcriptomic reconstruction of the mouse olfactory glomerular map suggests principles of odor processing. Nature Neuroscience, 2022, 25: 484-492
[45] Barrios AW, Quinteiro PS, Salazar I. The nasal cavity of the sheep and its olfactory sensory epithelium. Microscopy Research and Technique, 2014, 77: 1052-1059
[46] Nomura T, Takahashi S, Ushiki T. Cytoarchitecture of the normal rat olfactory epithelium: Light and scanning electron microscopic studies. Archives of Histology and Cytology, 2004, 67: 159-170
[47] Herrera LP, Casas CE, Bates ML, et al. Ultrastructural study of the primary olfactory pathway in Macaca fasci-cularis. Journal of Comparative Neurology, 2005, 488: 427-441
[48] Kavoi B, Makanya A, Hassanali J, et al. Comparative functional structure of the olfactory mucosa in the domestic dog and sheep. Annals of Anatomy, 2010, 192: 329-337
[49] Wang ZS, Nudelman A, Storm DR. Are pheromones detected through the main olfactory epithelium? Molecular Neurobiology, 2007, 35: 317-323
[50] Takeuchi H, Kurahashi T. Segregation of Ca²⁺ signaling in olfactory signal transduction. Journal of General Phy-siology, 2023, 155: 20230403
[51] Corey EA, Ukhanov K, Bobkov YV, et al. Inhibitory signaling in mammalian olfactory transduction potentially mediated by Gα_o. Molecular and Cellular Neuroscien-ces, 2021, 110: 103585
[52] Restrepo D, Teeter JH, Schild D. Second messenger signaling in olfactory transduction. Journal of Neurobio-logy, 1996, 30: 37-48
[53] Bigdai EV, Razinova AA. The role of cAMP in topographic organization of the olfactory system. Journal of Evolutionary Biochemistry and Physiology, 2023, 59: 1461-1478
[54] Reisert J, Yau KW, Margolis FL. Olfactory marker protein modulates the cAMP kinetics of the odour-induced response in cilia of mouse olfactory receptor neurons. Journal of Physiology, 2007, 585: 731-740
[55] Yang J, Qiu L, Strobel M, et al. Acid-sensing ion channels contribute to type III adenylyl cyclase-independent acid sensing of mouse olfactory sensory neurons. Mole-cular Neurobiology, 2020, 57: 3042-3056
[56] Boccaccio A, Menini A, Pifferi S. The cyclic AMP signaling pathway in the rodent main olfactory system. Cell and Tissue Research, 2021, 383: 429-443
[57] Ou Y, Ruan Y, Cheng M, et al. Adenylate cyclase re-gulates elongation of mammalian primary cilia. Experimental Cell Research, 2009, 315: 2802-2817
[58] Pun RYK, Kleene SJ. Contribution of cyclic-nucleotide-gated channels to the resting conductance of olfactory receptor neurons. Biophysical Journal, 2003, 84: 3425-3435
[59] Huang L, Zhang WX, Tong DF, et al. Triclosan and triclocarban weaken the olfactory capacity of goldfish by constraining odorant recognition, disrupting olfactory signal transduction, and disturbing olfactory information processing. Water Research, 2023, 233: 119736
[60] Ronnett GV, Moon C. G proteins and olfactory signal transduction. Annual Review of Physiology, 2002, 64: 189-222
[61] Stephan AB, Shum EY, Hirsh S, et al. ANO2 is the cilial calcium-activated chloride channel that may mediate olfactory amplification. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106: 11776-11781
[62] Rasche S, Toetter B, Adler J, et al. Tmem16b is speci-fically expressed in the cilia of olfactory sensory neurons. Chemical Senses, 2010, 35: 239-245
[63] Billig GM, Pál B, Fidzinski P, et al. Ca²⁺-activated Cl^- currents are dispensable for olfaction. Nature Neuroscience, 2011, 14: 763-769
[64] Nakashima N, Nakashima K, Taura A, et al. Olfactory marker protein directly buffers cAMP to avoid depolarization-induced silencing of olfactory receptor neurons. Nature Communications, 2020, 11: 2188
[65] Bönigk W, Bradley J, Müller F, et al. The native rat olfactory cyclic nucleotide-gated channel is composed of three distinct subunits. Journal of Neuroscience, 1999, 19: 5332-5347
[66] Nache V, Zimmer T, Wongsamitkul N, et al. Differen-tial regulation by cyclic nucleotides of the CNGA4 and CNGB1b subunits in olfactory cyclic nucleotide-gated channels. Science Signaling, 2012, 5: ra48
[67] Sautter A, Zong X, Hofmann F, et al. An isoform of the rod photoreceptor cyclic nucleotide-gated channel beta subunit expressed in olfactory neurons. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95: 4696-4701
[68] Kaupp UB, Seifert R. Cyclic nucleotide-gated ion channels. Physiological Reviews, 2002, 82: 769-824
[69] Evans EGB, Morgan JLW, DiMaio F, et al. Allosteric conformational change of a cyclic nucleotide-gated ion channel revealed by deer spectroscopy. Proceedings of the National Academy of Sciences of the United States of America, 2020, 117: 10839-10847
[70] Munger SD, Lane AP, Zhong H, et al. Central role of the CNGA4 channel subunit in Ca²⁺-calmodulin-depen-dent odor adaptation. Science, 2001, 294: 2172-2175
[71] Song Y, Cygnar KD, Sagdullaev B, et al. Olfactory CNG channel desensitization by Ca²⁺/CaM via the B1b subunit affects response termination but not sensitivity to recurring stimulation. Neuron, 2008, 58: 374-386
[72] Pedemonte N, Galietta LJV. Structure and function of TMEM16 proteins (anoctamins). Physiological Reviews, 2014, 94: 419-459
[73] Falzone ME, Malvezzi M, Lee BC, et al. Known structures and unknown mechanisms of TMEM16 scramblases and channels. Journal of General Physiology, 2018, 150: 933-947
[74] Moran O, Tammaro P. Identification of determinants of lipid and ion transport in TMEM16/anoctamin proteins through a Bayesian statistical analysis. Biophysical Chemistry, 2024, 308: 107194
[75] Le SC, Liang PF, Lowry AJ, et al. Gating and regulatory mechanisms of TMEM16 ion channels and scramblases. Frontiers in Physiology, 2021,12: 787773
[76] 袁宏博, 邢成芬, 陈娅斐, 等. 钙激活氯离子通道钙离子依赖性研究进展. 青岛: 中国化学会第三届全国生物物理化学会议(NCBPC3)暨国际华人生物物理化学发展论坛, 2023: 108
[77] Ponissery Saidu S, Stephan AB, Talaga AK, et al. Channel properties of the splicing isoforms of the olfactory calcium-activated chloride channel anoctamin 2. Journal of General Physiology, 2013, 141: 691-703
[78] Pietra G, Dibattista M, Menini A, et al. The Ca²⁺-activated Cl^- channel TMEM16B regulates action potential firing and axonal targeting in olfactory sensory neurons. Journal of General Physiology, 2016, 148: 293-311
[79] Tien J, Peters CJ, Wong XM, et al. A comprehensive search for calcium binding sites critical for TMEM16A calcium-activated chloride channel activity. eLife, 2014, 3: 02772
[80] Fischer T, Scheffler P, Lohr C. Dopamine-induced calcium signaling in olfactory bulb astrocytes. Scientific Reports, 2020, 10: 631
[81] Oettl LL, Kelsch W. Oxytocin and olfaction. Current Topics in Behavioral Neurosciences, 2018, 35: 55-75
[82] Sun C, Yin Z, Li BZ, et al. Oxytocin modulates neural processing of mitral/tufted cells in the olfactory bulb. Acta Physiologica, 2021, 231: e13626
[83] Pekarek BT, Kochukov M, Lozzi B, et al. Oxytocin signaling is necessary for synaptic maturation of adult-born neurons. Genes & Development, 2022, 36: 1100-1118
[84] Mitre M, Marlin BJ, Schiavo JK, et al. A distributed network for social cognition enriched for oxytocin receptors. Journal of Neuroscience, 2016, 36: 2517-2535
[85] Stoop R. Sniffing and oxytocin: Effects on olfactory memories. Neuron, 2016, 90: 431-433
[86] Oettl LL, Ravi N, Schneider M, et al. Oxytocin enhances social recognition by modulating cortical control of early olfactory processing. Neuron, 2016, 90: 609-621
[87] Choe HK, Reed MD, Benavidez N, et al. Oxytocin mediates entrainment of sensory stimuli to social cues of opposing valence. Neuron, 2015, 87: 152-163
[88] Stoyanov GS, Sapundzhiev NR, Tonchev AB. The vomeronasal organ: History, development, morphology, and functional neuroanatomy. Handbook of Clinical Neurology, 2021, 182: 283-291
[89] Amos C, Fox MA, Su JM. Collagen XIX is required for pheromone recognition and glutamatergic synapse formation in mouse accessory olfactory bulb. Frontiers in Cellular Neuroscience, 2023, 17: 1157577
[90] Bargmann CI. Olfactory receptor, vomeronasal receptors, and the organization of olfactory information. Cell, 1997, 90: 585-587
[91] Zuk KE, Cansler HL, Wang JX, et al. Arc-expressing accessory olfactory bulb interneurons support chemosensory social behavioral plasticity. Journal of Neuroscience, 2023, 43: 1178-1190
[92] Kratzing J. The structure of the vomeronasal organ in the sheep. Journal of Anatomy, 1971, 108: 247-260
[93] Mohrhardt J, Nagel M, Fleck D, et al. Signal detection and coding in the accessory olfactory system. Chemical Senses, 2018, 43: 667-695
[94] McCotter RE. The connection of the vomeronasal nerves with the accessory olfactory bulb in the opossum and other mammals. The Anatomical Record, 1912, 6: 299-318
[95] Trouillet AC, Keller M, Weiss J, et al. Central role of G protein Gαi2 and Gαi2 vomeronasal neurons in balancing territorial and infant-directed aggression of male mice. Proceedings of the National Academy of Sciences of the United States of America, 2019,116: 5135-5143
[96] Lee D, Kume M, Holy TE. Sensory coding mechanisms revealed by optical tagging of physiologically defined neuronal types. Science, 2019, 366: 1384-1389
[97] Wong WM, Cao J, Zhang X, et al. Physiology-forward identification of bile acid-sensitive vomeronasal receptors. Science Advances, 2020, 6: 6868
[98] Pérez-Gómez A, Stein B, Leinders-Zufall T, et al. Signaling mechanisms and behavioral function of the mouse basal vomeronasal neuroepithelium. Frontiers in Neuroanatomy, 2014, 8: 135
[99] Liman ER, Corey DP, Dulac C. TRP₂: A candidate transduction channel for mammalian pheromone sensory signaling. Proceedings of the National Academy of Sciences of the United States of America, 1999, 96: 5791-5796
[100] Skinner CB, Upadhya SC, Smith TK, et al. Signal transduction and gene expression in cultured accessory olfactory bulb neurons. Neuroscience, 2008, 157: 340-348
[101] Brennan PA, Hancock D, Keverne EB. The expression of the immediate-early genes c-fos, egr-1 and c-jun in the accessory olfactory bulb during the formation of an olfactory memory in mice. Neuroscience, 1992, 49: 277-284
[102] Hegde AN, Mu J, Godwin D, et al. A novel mechanism of synaptic plasticity underlies pheromone memory in mice. Social Neuroscience, 2005, 31: 503-508
[103] Navarro-Moreno C, Sanchez-Catalan MJ, Barneo-Munoz M, et al. Pregnancy changes the response of the vomeronasal and olfactory systems to pups in mice. Frontiers in Cellular Neuroscience, 2020, 14: 593309
[104] Alexander G, Shillito EE. The importance of odour, appearance and voice in maternal recognition of the young in Merino sheep (Ovis aries). Applied Animal Ethology, 1977, 32: 127-135
[105] Ungerfeld R, Fernández-Werner A, Gökdal Ö, et al. Lambs identify their mothers’ bleats but not a picture of her face. Journal of Veterinary Behavior, 2021, 46: 69-73
[106] Laliotis GP, Papadaki K, Bizelis I. Ovine vocal individuality expression by ewes and lambs at a late (40 days) postpartum time point. Journal of the Acoustical Society of America, 2023, 153: 751
[107] Kuhlmann K, Tschapek A, Wiese H, et al. The membrane proteome of sensory cilia to the depth of olfactory receptors. Molecular & Cellular Proteomics, 2014, 13: 1828-1843