Effects of paternal deprivation in social rodents

Gromov V.S.

P. 123-138

The article concerns the effects of paternal deprivation in social rodents (California mice, Mongolian gerbils, mandarin and prairie voles and degus) whose social organizations are characterized by a family-group lifestyle and biparental care. Paternal deprivation was found to have a dramatic effect on pup survival (e.g. in California mice), as well as negatively affect pair bonding and adult parental behavior in other social rodents. Paternal deprivation resulted in reduction of central expression of some steroid and neuropeptide receptors in offspring. Besides, paternal deprivation was found to alter the regional density as well as the homoeostatic balance of distinct interneuron populations in an age- and brain region-specific manner; it also affects maturation of excitatory spine synapses in prefrontal cortical and limbic regions. The father-deprived individuals showed the behavioral differences resulted from altered brain circuits. As a result, cognitive and emotional competence might be essentially changed in father-deprived animals. These findings indicate the importance of paternal care and paternal bonding as a unique source of sensory and socio-emotional stimuli, which may protect the offspring from developing an increased vulnerability towards stress-related life events.DOI: 10.15298/rusjtheriol.21.2.03

• Ågren G., Zhou Q. & Zhong W. 1989. Ecology and social behaviour of Mongolian gerbils, Meriones unguiculatus, at Xilinhot, Inner Mongolia, China // Animal Behaviour. Vol.37. P.11–27.
• Ahern T.H. & Young L.J. 2009. The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (Microtus ochrogaster) // Frontiers in Behavioral Neuroscience. Vol.3. P.1–18.
• Ahern T.H., Hammock E.A. & Young L.J. 2011. Parental division of labor, coordination, and the effects of family structure on parenting in monogamous prairie voles (Microtus ochrogaster) // Developmental Psychobiology. Vol.53. P.118–131.
• Aragona B.J., Liu Y., Yu Y.J., Curtis J.T., Detwiler J.M., Insel T.R. & Wang Z. 2006. Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds // Nature Neuroscience. Vol.9. P.133–139.
• Bales K.L., Mason W.A., Catana C., Cherry S.R. & Mendoza S.P. 2007. Neural correlates of pair-bonding in a monogamous primate // Brain Research. Vol.1184. P.245–253.
• Bales K.L. & Saltzman W. 2016. Fathering in rodents: Neurobiological substrates and consequences for offspring // Hormones and Behavior. Vol.77. P.249–259.
• Bamshad M., Novak M.A. & de Vries A.C. 1993. Sex and species differences in the vasopressin innervation of sexually naive and parental prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus) // Journal of Neuroendocrinology. Vol.5. P.247–255.
• Braun K., Seidel K., Weigel S., Roski C. & Poeggel G. 2010. Paternal deprivation alters region-and age-specific interneuron expression patterns in the biparental rodent, Octodon degus // Cerebral Cortex. Is.12. P.1–15.
• Bredy T.W., Lee A.W., Meaney M.J. & Brown R.E. 2004. Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse (Peromyscus californicus) // Hormones and behavior. Vol.46. P.30–38.
• Brown R.E. & Moger W.H. 1983. Hormonal correlates of parental behavior in male rats // Hormones and Behavior. Vol.17. P.356–365.
• Cantoni D. & Brown R.E. 1997. Paternal investment and reproductive success in the California mouse, Peromyscus californicus // Animal Behaviour. Vol.54. P.377–386.
• Cao Y., Wu R., Tai F., Zhang X., Yu P., An X., Qiao X. & Hao P. 2014. Neonatal paternal deprivation impairs social recognition and alters levels of oxytocin and estrogen receptor α mRNA expression in the MeA and NAcc, and serum oxytocin in mandarin voles // Hormones and Behavior. Vol.65. P.57–65.
• Carter C.S. & Getz L.L. 1993. Monogamy and the prairie vole // Scientific American. Vol.268. P.100–106.
• Champagne F.A., Weaver I.C.G., Diorio J., Sharma S. & Meaney M J. 2003. Natural variations in maternal care are associated with estrogen receptor alpha expression and estrogen sensitivity in the medial preoptic area // Endocrinology. Vol.144. P.4720–4724.
• Clark M.M., Desousa D., Vonk J. & Galef B.G. 1997. Parenting and potency: Alternative routes to reproductive success in male Mongolian gerbils // Animal Behaviour. Vol.54. P.635–642.
• Cushing B.S. & Kramer K.M. 2005. Mechanisms underlying epigenetic effects of early social experience: The role of neuropeptides and steroids // Neuroscience and Biobehavioral Reviews. Vol.29. P.1089–1105.
• Cushing B.S. & Wynne-Edwards K.E. 2006. Estrogen receptor-alpha distribution in male rodents is associated with social organization // Journal of Comparative Neurology. Vol.494. P.595–605.
• De Jong T.R., Chauke M., Harris B.N. & Saltznan W. 2009. From here to paternity: Neural correlates of the onset of paternal behavior in California mice (Peromyscus californicus) // Hormones and Behavior. Vol.56. P.220–231.
• Deroche V., Marinelli M., Maccari S., Moal M.L., Simon H. & Piazza P.V. 1995. Stress-induced sensitization and glucocorticoids: I. Sensitization of dopamine-dependent locomotor effects of amphetamine and morphine depends on stress-induced corticosterone secretion // Journal of Neuroscience. Vol.15. P.7181–7188.
• De Vries A.C., De Vries M.B., Taymans S.E.& Carter C.S. 1995. Modulation of pair bonding in female prairie voles (Microtus ochrogaster) by corticosterone // Proceedings of the National Academy of Sciences (USA). Vol.92. P.7744–7748.
• De Vries A.C., De Vries M.B., Taymans S.E. & Carter C.S. 1996. The effects of stress on social preferences are sexually dimorphic in prairie voles // Proceedings of the National Academy of Sciences (USA). Vol.93. P.11980–11984.
• De Vries A.C., Guptaa T., Cardillo S., Cho M. & Carter C.S. 2002. Corticotropin-releasing factor induces social preferences in male prairie voles // Psychoneuroendocrinology. Vol.27. P.705–714.
• Dewsbury D.A. 1985. Paternal behavior in rodents // American Zoologist. Vol.25. P.841–852.
• Dudley D. 1974a. Paternal behavior in the California mouse, Peromyscus californicus // Behavioral Biology. Vol.11. P.247–251.
• Dudley D. 1974b. Contributions of paternal care to the growth and development of the young in Peromyscus californicus // Behavioral Biology. Vol.11. P.155–166.
• Ebensperger L.A. & Bozinovic F. 2000. Communal burrowing in the hystricognath rodent, Octodon degus: a benefit of sociality? // Behavioral Ecology and Sociobiology. Vol.47. P.365–369.
• Ebensperger L.A., Hurtado M.J., Soto-Gamboa M., Lacey E.A. & Chang A.T. 2004. Communal nesting and kinship in degus (Octodon degus) // Naturwissenschaften. Bd.91. S.391–395. Eisenberg J.F. 1966. The social organization of mammals // Handbook of Zoology. Vol.10. P.1–192.
• Elwood R.W. 1975. Paternal and maternal behaviour in the Mongolian gerbil // Animal Behaviour. Vol.23. P.766–772. Elwood R.W. 1979. Maternal and paternal behaviour of the Mongolian gerbil: A correlation study // Behavioral and Neural Biology. Vol.25. P.555–562.
• Elwood R.W. & Broom D.M. 1978. The influence of litter size and parental behaviour on the development of Mongolian gerbil pups // Animal Behaviour. Vol.26. P.438–454.
• Feldman R., Braun K. & Champagne F.A. 2019. The neural mechanisms and consequences of paternal caregiving // Nature Reviews: Neuroscience. Vol.20. P.205–224.
• Feng T., An S., Kinden R., Zhang X., Jia R. & Tai F. 2019. Alteration in oxytocin levels induced by early social environment affects maternal behavior and estrogen receptor alpha in mandarin voles (Microtus mandarinus) // Behavioural Brain Research. Vol.365. P.36–47.
• Francis D.D., Champagne F.C. & Meaney M.J. 2000. Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat // Journal of Neuroendocrinology. Vol.12. P.1145.
• Francis D.D., Young L.J., Meaney M.J. & Insel T.R. 2002. Naturally occurring differences in maternal care are as- sociated with the expression of oxytocin and vasopressin (V1a) receptors: Gender differences // Journal of Neuroendocrinology. Vol.14. P.349.
• French J.A. 1994. Alloparents in the Mongolian gerbil: impact on long-term reproductive performance of breeders and opportunities for independent reproduction // Behavioral Ecology. Vol.5. P.273–279.
• Fulk G.W. 1976. Notes on the activity, reproduction and social behavior of Octodon degus // Journal of Mammalogy. Vol.57. P.495–505.
• Fuster J.M. 2002. Frontal lobe and cognitive development // Journal of Neurocytology. Vol.31. P.373–385.
• Getz L.L. & Carter C.S. 1996. Prairie-vole partnerships // American Scientist. Vol.84. P.56–62.
• Getz L.L. & Hofmann J.E. 1986. Social organization in free-living prairie voles, Microtus ochrogaster // Behavioral Ecology and Sociobiology. Vol.18. P.275–282.
• Getz L. L., Carter C. S. & Gavish L. 1981. The mating system of the prairie vole, Microtus ochrogaster: field and laboratory evidence for pair-bonding // Behavioral Ecology and Sociobiology. Vol.8. P.189–194.
• Getz L.L., Hofmann J.E. & Carter C.S. 1987. Mating system and population fluctuations of the prairie vole, Microtus ochrogaster // American Zoologist. Vol.27. P.909–920.
• Getz L.L., McGuire B., Pizzuto T., Hofmann J.E. & Frase B. 1993. Social organization of the prairie vole (Microtus ochrogaster) // Journal of Mammalogy. Vol.74. P.44–58. Gingrich B., Liu Y., Cascio C., Wang Z. & Insel T.R. 2000. Dopamine D2 receptors in the nucleus accumbens are important for social attachment in female prairie voles (Microtus ochrogaster) // Behavioral Neuroscience. Vol.114. P.173–183.
• Gonzalez A., Lovic V., Ward G.R., Wainwright P.E. & Fleming A.S., 2001. Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats // Developmental Psychobiology. Vol.38. P.11–32.
• Gromov V.S. 1981. [Social organization of the family groups of clawed jird Meriones unguiculatus in natural colonies] // Zoologichesky Zhurnal. Vol.60. P.1683–1694 [in Russian with English summary]
• Gromov V.S. 2000. [Ethological mechanisms of population homeostasis in gerbils (Mammalia, Rodentia).] Moscow: Severtsov Institute of Ecology & Evolution. 392 p. [in Russian]
• Gromov V.S. 2009. Interactions of partners in family pairs, care of the offspring, and the role of tactile stimulation in formation of parental behaviour of the Mongolian gerbil (Meriones unguiculatus) under laboratory conditions // Biology Bulletin. Vol.36. P.479–488.
• Gromov V.S. 2011a. Pair-bonding and parental care in cricetid rodents: A comparative study // Acta Theriologica. Vol.56. P.23–33.
• Gromov V.S. 2011b. Biparental care, tactile stimulation, and evolution of sociality in rodents // Journal of Evolutionary Biology Research. Vol.3. P.33–43.
• Gromov V.S. 2013. [Parental care in rodents: Ethological, physiological and evolutionary aspects.] Moscow: KMK Press. 338 p. [in Russian]
• Gromov V.S. 2014. Complicated social structure and the evolution of sociality in rodents: Cooperation as the main promoting factor // Watson P. (ed.). Social Behavior: Evolutionary Pathways, Environmental Influences and Impairments. NY: Nova Science Publ. P.71–119.
• Gromov V.S. 2020. Paternal care in rodents: Ultimate causation and proximate mechanisms // Russian Journal of Theriology. Vol.19. No.1. P.1–20.
• Gruder-Adams S. & Getz L.L. 1985. Comparison of the mating system and paternal behaviour in Microtus ochrogaster and Microtus pennsylvanicus // Journal of Mammalogy. Vol.66. P.165–167.
• Gubernick D.J. & Alberts J.R. 1987. The biparental care system of the California mouse, Peromyscus californicus // Journal of Comparative Psychology. Vol.101. P.169–177.
• Gubernick D.J. & Teferi T. 2000. Adaptive significance of male parental care in a monogamous mammal // Proceedings of Royal Society of London. Ser.B. Vol.267. P.147–150.
• Gubernick D.J., Wright S.L. & Brown R.E. 1993. The significance of the male’s presence for offspring survival in the monogamous California mouse, Peromyscus californicus // Animal Behaviour. Vol.46. P.539–546.
• Hammock E.A. & Young L.J. 2002. Variation in the vasopressin V1a receptor promoter and expression: implications for inter- and intraspecific variation in social behaviour // European Journal of Neuroscience. Vol.16. P.399–402.
• Hartung T.G. & Dewsbury D.A. 1979. Paternal behavior of six species of muroid rodents // Behavioral and Neural Biology. Vol.26. P.446–478.
• Helmeke C., Seidel K., Poeggel G., Bredy T.W., Abraham A. & Braun K. 2009. Paternal deprivation during infancy results in dendrite- and time-specific changes of dendritic development and spine formation in the orbitofrontal cortex of the biparental rodent Octodon degus // Neuroscience. Vol.163. P.790–798.
• Hensch T.K. 2005. Critical period plasticity in local cortical circuits // Nature Reviews: Neuroscience. Vol.6. P.877–888. Insel T.R. & Shapiro L.E. 1992. Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles // Proceedings of the National Academy of Sciences (USA). Vol.89. P.5981–5985.
• Insel T.R. & Young L.J. 2001. The neurobiology of attachment // Nature Reviews: Neuroscience. Vol.2. P.129–135. Insel T.R., Wang Z.X. & Ferris C.F. 1994. Patterns of brain vasopressin receptor distribution associated with social organization in microtine rodents // Journal of Neuroscience. Vol.14. P.5381–5392.
• Jia R., Tai F., An S., Broders H. & Sun R. 2008a. Neonatal manipulation of oxytocin influences the partner preference in mandarin voles (Microtus mandarinus) // Neuropeptides. Vol.42. P.525–533.
• Jia R., Tai F.D., An S.C., Broders H., Ding X.L., Kong Q. et al. 2008b. Effects of neonatal oxytocin treatment on aggression and neural activities in mandarin voles // Physiology & Behavior. Vol.95. P.56–62.
• Jia R., Tai F., An S., Zhang X. & Broders H. 2009. Effects of neonatal paternal deprivation or early deprivation on anxi- ety and social behaviors of the adults in mandarin voles // Behavioural Processes. Vol.82. P.271–278.
• Jia R., Tai F., An S. & Zhang X. 2011. Neonatal paternal deprivation or early deprivation reduces adult parental behavior and central estrogen receptor expression in mandarin voles (Microtus mandarinus) // Behavioural Brain Research. V.224. P.279–289.
• Kang N., Baum M.J. & Cherry J.A. 2009. A direct main olfactory projection to the ‘vomeronasal’ amygdale in female mice selectively responds to volatile pheromones from males // European Journal of Neuroscience. Vol.29. P.624–634.
• Kentner A.C., Abizaid A. & Bielajew C. 2010. Modelling dad: animal models of paternal behaviour // Neuroscience and Biobehavioral Reviews. Vol.34. P.438–451.
• Kirkpatrick B., Kim J.W. & Insel T.R. 1994. Limbic system fos expression associated with paternal behavior // Brain Research. Vol.658. P.112–118.
• Kling A.S. & Brothers L.A. 1992. The amygdale and social behavior // Aggleton J.P. (ed.) The amygdale: Neurobiological aspects of emotion, memory and mental functions. NY: Wiley-Liss. P.353–377.
• Kolb B., Pellis S. & Robinson T.E. 2004. Plasticity and functions of the orbital frontal cortex // Brain Cognition. Vol.55. P.104–115.
• Koob G.F. 1992. Drugs of abuse: anatomy, pharmacology and function of reward pathways // Trends in Pharmacological Science. Vol.13. P.177–184.
• Lacey E.A. & Ebensperger L.A. 2007. Social structure in octodontid and ctenomyid rodents // Wolff J.O. & Sherman P.W. (eds.) Rodent societies: An ecological and evolutionary perspective. Chicago: Univ. Chicago Press. P.403–415.
• Leont’ev A.N. 1954. [About the ecology of the Mongolian gerbil in the BMASSR] // Izvestia Irkutskogo Nauch- no-Issledovatelskogo Protivochumnogo Instituta Sibiri i Dal’nego Vostoka. Vol.12. P.137–149. [in Russian]
• Leont’ev A.N. 1962. [Studying Mongolian gerbils by the method of marking] // Izvestia Irkutskogo Nauchno-Issledovatelskogo Protivochumnogo Instituta Sibiri i Dal’nego Vostoka. Vol.24. P.296–302. [in Russian]
• Lonstein J.S. & De Vries G.J. 1999. Comparison of the parental behavior of pair-bonded female and male prairie voles (Microtus ochrogaster // Physiology & Behavior. Vol.66. P.33–45.
• Lukas M., Bredewold R., Landgraf R., Neumann I.D. & Veenema A.H. 2011. Early life stress impairs social recognition due to ablunted response of vasopressin release within the septum of adult male rats // Psychoneuroendocrinology. Vol.36. P.843–853.
• Martínez A., Arteaga-Silva M., Bonilla-Jaime H., Cárdenas M. & Luis J. 2019. Paternal behavior in the Mongolian gerbil, and its regulation by social factors, T, ERα, and AR // Physiology & Behavior. V.199. P.351–358.
• McGuire B. 1988. Effects of cross-fostering on parental be- haviour of meadow voles (Microtus pennsylvanicus). // Journal of Mammalogy. Vol.69. P.332–341.
• McGuire B. & Novak M. 1984. A comparison of maternal behaviour in the meadow vole (Mictotus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum) // Animal Behaviour. Vol.32. P.1132–1141.
• Meaney M.J., Aitken D.H., van Berkel C., Bhatnagar S. & Sapolsky R.M. 1988. Effect of neonatal handling on age-related impairments associated with the hippocampus // Science. Vol.239. P.766–768.
• Meaney M.J., Aitken D.H., Bhatnagar S. & Sapolsky R.M. 1991. Postnatal handling attenuates certain neuroendocrine, anatomical, and cognitive dysfunctions associated with aging in female rats // Neurobiology of Aging. Vol.12. P.31–38.
• Meserve P.L., Martin R.E. & Rodriguez J.M. 1983. Feeding ecology of two chilean caviomorphs in a central mediterranean savanna // Journal of Mammalogy. Vol.64. P.322–325. Mitra S.W., Hoskin E., Yudkovitz J., Pear L., Wilkinson H.A., Hayashi S., Pfaff W., Ogawa S., Rohrer S.P., Schaeffer J.M., McEwen B.S. & Alves S.E. 2003. Immunolocalization of estrogen receptor b in the mouse brain: comparison with estrogen receptor alpha // Endocrinology. Vol.144. P.2055–2067.
• Mugford R.A. & Nowell N.W. 1972. Paternal stimulation during infancy: Effects upon aggression and open-field performance of mice // Journal of Comparative Physiology and Psychology. Vol.79. P.30–36.
• Numan M. & Insel T. 2003. The Neurobiology of Parental Behavior. New York: Springer. 418 p.
• Oitzl M.S., Workel J.O., Fluttert M., Frosch F. & De Kloet E.R. 2000. Maternal deprivation affects behavior from youth to senescence: amplification of individual differences in spatial learning and memory in senescent brown Norway rats // European Journal of Neuroscience. Vol.12. P.3771–3780.
• Ostermeyer M.C. & Elwood R.W. 1984. Helpers (?) at the nest in the Mongolian gerbil, Meriones unguiculatus // Behaviour. Vol.91. P.61–77.
• O’Connell L.A. & Hofmann H.A. 2011. The vertebrate mesolimbic reward system and social behavior network: A comparative synthesis // Journal of Comparative Neurology. Vol.519. P.3599–3639.
• Pinkernelle J., Abraham A., Seidel K. & Braun K. 2009. Paternal deprivation induces dendritic and synaptic changes and hemispheric asymmetry of pyramidal neurons in the somatosensory cortex // Developmental Neurobiology. Vol.69. P.663–673.
• Pitkänen A. 2000. Connectivity of the rat amygdaloid complex // Aggleton J.P. (ed.) The amygdala: a functional analysis. New York: Oxford University Press. P.31–115.
• Ribble D.O. 1991. The monogamous mating system of Peromyscus californicus as revealed by DNA fingerprinting // Behavioral Ecology and Sociobiology. Vol.29. P.161–166.
• Ribble D.O. 1992. Lifetime reproductive success and its correlates in the monogamous rodent, Peromyscus californicus // Journal of Animal Ecology. Vol.61. P.457–468.
• Ribble D.O. & Salvioni M. 1990. Social organization and nest co-occupancy in Peromyscus californicus, a monogamous rodent // Behavioral Ecology and Sociobiology. Vol.26. P.9–15.
• Roberts R.L., Williams J.R., Wang A.K. & Carter C.S. 1998. Cooperative breeding and monogamy in prairie voles: Influence of the sire and geographic variation // Animal Behaviour. Vol.55. P.1131–1140.
• Rolls E.T. 2004. The functions of the orbitofrontal cortex // Brain Cognition. Vol.55. P.11–29.
• Rosenblatt J.S. & Ceus K. 1998. Estrogen implants in the medial preoptic area stimulate maternal behavior in male rats // Hormones and Behavior. Vol.33. P.23–30.
• Russell P.A. 1971. ‘Infantile stimulation’ in rodents: A consideration of possible mechanisms // Psychology Bulletin. Vol.75. P.192–202.
• Seidel K., Poeggel G., Holetschka R., Helmeke C. & Braun K. 2011. Paternal deprivation affects the development of corticotropin releasing factor (CRF) expressing neurons in prefrontal cortex, amygdala and hippocampus of the biparental Octodon degus // Journal of Neuroendocrinology. Vol.23. P.1166-1176.
• Shepard K.N., Michopoulos V., Toufexis D.J. & Wilson M.E. 2009. Genetic, epigenetic and environmental impact on sex differences in social behavior // Physiology & Behavior. Vol.97. P.157–170.
• Smorkatcheva A.V. 1999. The social organization of the mandarin vole, Lasiopodomys mandarinus, during the reproductive period // Zeitschrift für Säugetierkunde. Bd.64. S.344–355.
• Smorkatcheva A.V. 2003. Parental care in the captive mandarin vole, Lasiopodomys mandarinus // Canadian Journal of Zoology. Vol.81. P.1339–1345.
• Solomon N.G. 1991. Current indirect fitness benefits associated with philopatry in juvenile prairie voles // Behavioral Ecology and Sociobiology. Vol.29. P.277–282.
• Song Z., Tai F., Yu C., Wu R., Zhang X., Broders H. et al. 2010. Sexual or paternal experiences alter alloparental behavior and the central expression of ERα and OT in male mandarin voles (Microtus mandarinus) // Behavioural Brain Research. Vol.214. P.290–300.
• Sullivan R.M., Dufresne M.M. & Waldron J. 2009. Lateralized sex differences in stress-induced dopamine release in the rat // Neuroreport. Vol.20. P.229–232.
• Tai F.D. & Wang T.Z. 2001. Social organization of mandarin voles in burrow system // Acta Theriologica Sinica. Vol.21. P.50–56.
• Tai F.D., Wang T.Z. & Zhao Y.J. 2001. Mating system of mandarin vole (Microtus mandarinus) // Acta Zoologica Sinica. Vol.47. P.260–267.
• Tang A.C. 2001. Neonatal exposure to novel environment enhances hippocampal-dependent memory function during infancy and adulthood // Learning and Memory. Vol.8. P.257–264.
• Thomas J.A. & Birney E.C. 1979. Parental care and mating system of the prairie vole, Microtus ochrogaster // Behavioral Ecology and Sociobiology. Vol.5. P.171–186.
• Trainor B.C. & Marler C.A. 2002. Testosterone promotes paternal behaviour in a monogamous mammal via conversion to oestrogen // Proceedings of Royal Society of London. Ser.B. Vol.269. P.823–829.
• Trainor B.C., Bird I.M., Alday N.A., Schlinger B.A. & Marler C.A. 2003. Variation in aromatase activity in the medial preoptic area and plasma progesterone is associated with the onset of paternal behavior // Neuroendocrinology. Vol.78. P.36–44.
• Wang Z.X. & Novak M.A. 1994. Alloparental care and the influence of father presence on juvenile prairie voles, Mi- crotus ochrogaster // Animal Behaviour. Vol.47. P.281–288.
• Weinandy R. & Gatterman R. 1999. Parental care and time sharing in the Mongolian gerbil // Zeitschrift für Saugetierkunde. Vol.64. P.169–175.
• Willner P. 1995. Dopaminergic mechanisms in depression and mania // Bloom F.E. & Kupfer D.J. (eds.). Psychopharmacology: The Fourth Generation of Progress. New York: Raven Press. P.921–931.
• Wilson S.C. 1982. Contact-promoting behavior, social development, and relationship with parents in sibling juvenile degus (Octodon degus) // Developmental Psychobiology. Vol.15. P.257–268.
• Wright S.L. & Brown R.E. 2002. The importance of paternal care on pup survival and pup growth in Peromyscus californicus when required to work for food // Behavioural Processes. Vol.60. P.41–52.
• Young L.J., Wang Z., Donaldson R. & Rissman E.F. 1998. Estrogen receptor α is essential for induction of oxytocin receptor by estrogen // Neuroreport. Vol.9. P.933–936.
• Yu P., An S., Tai F., Zhang X., He F., Wang J., An X. & Wu R. 2012. The effects of neonatal paternal deprivation on pair bonding, NAcc dopamine receptor mRNA expression and serum corticosterone in mandarin voles // Hormones and Behavior. Vol.61. P.669–677.
• Yu P., Zhang X., Li X., He F. & Tai F. 2015. Early bi-parental separation or neonatal paternal deprivation in mandarin voles reduces adult offspring paternal behavior and alters serum corticosterone levels and neurochemistry // Hormones and Behavior. Vol.73. P.8–14.