Paternal care in rodents: Ultimate causation and proximate mechanisms Gromov V.S. P. 1-20 The evolution of paternal care in rodents has intrigued biologists for over decades. In this paper, both ultimate (adaptive significance, evolution) and proximate (ontogeny, mechanisms) questions related to the emergence and maintenance of male paternal care are reviewed. Paternal care is thought to be a consequence of social monogamy, but no definitive hypothesis adequately explains the evolution of paternal behavior in rodents. The onset, activation and maintenance of paternal care are shown to be governed by complex interactions in neuroendocrine systems that change during ontogeny. Depending on the species, different components of male experience as well as different exogenous cues are likely to be involved in the organization and activation of paternal behavior. Several hormones, including steroids (testosterone, estradiol, progesterone) and neuropeptides (prolactin, vasopressin, oxytocin), are involved in the onset, the maintenance, or both the onset and the maintenance of parental behavior, including direct paternal care. The effect of testosterone was found to be not universal and, moreover, species-specific. As for estrogens and neuropeptides, further investigations are needed to better understand the role of these hormones in activation and maintenance of rodent paternal behavior. Current research shows that male parental care in rodents is, to a great extent, an epigenetic phenomenon, and future studies will focus on the epigenetic modifications that can affect the paternal behavior in rodents.
DOI: 10.15298/rusjtheriol.19.1.01References- 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.118–31.
- Akther S., Fakhrul A.A.K.M. & Higashida H. 2014. Effects of electrical lesions of the medial preoptic area and the ventral pallidum on mate-dependent paternal behavior in mice // Neuroscience Letters. Vol.570. P.21–24.
- Bales K.L. & Saltzman W. 2016. Fathering in rodents: Neurobiological substrates and consequences for offspring // Hormones and Behavior. Vol.77. P.249–59.
- Bales K.L., Kim A.J., Lewis-Reese A.D. & Carter C.S. 2004. Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles // Hormones and Behavior. Vol.45. P.354–361.
- Bales K.L., Boone E., Epperson P., Hoffman G. & Carter C.S. 2011. Are behavioral effects of early experience mediated by oxytocin? // Frontiers of Psychiatry. Vol.2. P.24.
- Bamshad M., Novak M.A. & de Vries G.J. 1994. Cohabitation alters vasopressin innervation and paternal behavior in prairie voles (Microtus ochrogaster) // Physiology & Behavior. Vol.56. P.751–758.
- Barash D.P. 1975. Ecology of paternal behavior in the hoary marmot (Marmota caligata): An evolutionary interpretation // Journal of Mammalogy. Vol.56. P.613–618.
- Bendesky A., Kwon Y.-M., Lassance J.-M., Lewarch C.L., Yao S., Peterson B.K., He M.X., Dulac C. & Hoekstra H.E. 2017. The genetic basis of parental care evolution in monogamous mice // Nature. Vol.544. P.434–439.
- Bester-Meredith J.K. & Marler C.A. 2003. Vasopressin and the transmission of paternal behavior across generations in mated, cross-fostered Peromyscus mice // Behavioral Neuroscience. Vol.117. P.455–463.
- Bester-Meredith J.K., Young L.J. & Marler C.A. 1999. Species differences in paternal behavior and aggression in Peromyscus and their associations with vasopressin immunoreactivity and receptors // Hormones and Behavior. Vol.36. P.25–38.
- Bonthuis P.J., Patteson J.K. & Rissman E.F. 2011. Acquisition of sexual receptivity: roles of chromatin acetylation, estrogen receptor-alpha, and ovarian hormones // Endocrinology. Vol.152. P.3172–3181.
- Brady C.A. & Svendsen G.E. 1981. Social behaviour in a family of beaver, Castor canadensis // Biology of Behaviour. Vol.6. P.99–114.
- Braun K. & Champagne F.A. 2014. Paternal influence son offspring development: behavioural and epigenetic pathways // Journal of Neuroendocrinology. Vol.26. P.697–706.
- 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.
- Bridges R.S. 2015. Neuroendocrine regulation of maternal behavior // Frontiers of Neuroendocrinology. Vol.36. P.178–196.
- Brooks P.L., Vella E.T. & Wynne-Edwards K.E. 2005. Dopamine agonist treatment before and after the birth reduces prolactin concentration but does not impair paternal responsiveness in Djungarian hamsters, Phodopus campbelli // Hormones and Behavior. Vol.47. P.358–366.
- Brown R.E. 1993. Hormonal and experimental factors influencing parental behavior in male rodents: An integrative approach // Behavioural Processes. Vol.30. P.1–28.
- Brown R.E. & Moger W.H. 1983. Hormonal correlates of parental behavior in male rats // Hormones and Behavior. Vol.17. P.356–365.
- Brown R.E., Murdoch T., Murphy P.R. & Moger W.H. 1995. Hormonal responses of male gerbils to stimuli from their mate and pups // Hormones and Behavior. Vol.29. P.474–491.
- Brown K., Seidel K., Holetschka R., Groeger N. & Poeggel G. 2013. Paternal deprivation alters the development of catecholaminergic innervation in the prefrontal cortex and related limbic brain regions // Brain Structure and Functions. Vol.218. P.859–872.
- 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 mPRA expression in the MeA and NAcc, and serum oxytocin in mandarin voles // Hormones and Behavior. Vol.65. P.57–65.
- Carone B.R., Fauquier L., Habib N., Shea J.M., Hart C.E., Li R., Bock C., Li C., Gu H. & Zamore P.D. 2010. Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals // Cell. Vol.143. P.1084–1096.
- Carter C.S., Williams J.R., Witt D.M. & Insel T.R. 1992. Oxytocin and social bonding // Annals New York Academy of Science. Vol.652. P.204–211.
- Castelli F.R., Kelley R.A., Keane B. & Solomon N.G. 2011. Female prairie voles show social and sexual preferences for males with longer avpr1a microsatellite alleles // Animal Behaviour. Vol.82. P.1117–1126.
- Champagne F.A. 2008. Epigenetic mechanisms and the transgenerational effects of maternal care // Frontiers of Neuroendocrinology. Vol.29. P.386–397.
- Champagne F.A. 2011. Maternal imprints and the origins of variation // Hormones and Behavior. Vol.60. P.4–11.
- Champagne F.A. & Curley J.P. 2009. Epigenetic mechanisms mediating the long-term effects of maternal care on development // Neuroscience and Biobehavioral Reviews. Vol.33. P.593–600.
- Champagne F.A. & Rissman E.F. 2011. Behavioral epigenetics: A new frontier in the study of hormones and behavior // Hormones and Behavior. Vol.59. P.277–278.
- 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.
- Champagne F.A., Weaver I.C., Diorio J., Dymov S., Szyf M. & Meaney M.J. 2006. Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring // Endocrinology. Vol.147. P.2909–2915.
- Clark M.M. & Galef B.G. 1999. A testosterone-mediated trade-off between parental and sexual effort in male Mongolian gerbils (Meriones unguiculatus) // Journal of Comparative Psychology. Vol.113. P.388–395.
- Clark M.M. & Galef B.G. 2000. Why some male Mongolian gerbils may help at the nest: testosterone, asexuality and alloparenting // Animal Behaviour. Vol.59. P.801–806.
- Clark M.M., vom Saal F.S. & Galef B.J. Jr. 1992. Intrauterine positions and testosterone levels of adult male gerbils are correlated // Physiology & Behavior. Vol.51. P.957–960.
- Clark M.M., Vonk J.M. & Galef B.G. Jr. 1998. Intrauterine position, parenting, and nest-site attachment in male Mongolian gerbils // Developmental Psychobiology. Vol.32. P.177–181.
- Clutton-Brock T.H. 1989. Mammalian mating systems // Proceedings of the Royal Society of London, Series B. Vol.236. P.339–372.
- Clutton-Brock T.H. 1991. The evolution of parental care. Princeton: Princeton Univ. Press. 365 p.
- Curley J.P., Mashoodh R. & Champagne F.A. 2011. Epigenetics and the origins of paternal effects // Hormones and Behavior. Vol.59. P.306–314.
- 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.
- Cushing B.S., Perry A., Musatov S., Ogawa S. & Papademetriou E. 2008. Estrogen receptors in the medial amygdala inhibit the expression of male prosocial behavior // Journal of Neuroscience. Vol.28. P.10399–10403.
- 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.
- De Vries G.J. & Boyle P.A. 1998. Double duty for sex differences in the brain // Behavioural Brain Research. Vol.92. P.205–213.
- Dewsbury D.A. 1985. Paternal behavior in rodents // American Zoologist. Vol.25. P.841–852.
- Edwards H.E., Reburn C.J. & Wynne-Edwards K.E. 1995. Daily patterns of pituitary prolactin secretion and their role in regulating maternal serum progesterone concentrations across pregnancy in the Djungarian hamster (Phodopus campbelli) // Biology of Reproduction. Vol.52. P.814–823.
- Eisenberg J.F. 1965. The social organization of mammals // Handbook of Zoology. Vol.8. P.1–191.
- Elwood R.W. 1977. Changes in the responses of male and female gerbils (Meriones unguiculatus) towards test pups during the pregnancy of the female // Animal Behaviour. Vol.25. P.46–51.
- Elwood R.W. 1983. Paternal care in rodents // Elwood R.W. (ed.). Parental Behaviour of Rodents. New York: John Wiley & Sons. P.441–455.
- Elwood R.W. 1986. What makes male mice paternal? // Behavioral and Neural Biology. Vol.46. P.54–63.
- Emlen S.T. 1982. The evolution of helping. I. An ecological constraints model // American Naturalist. Vol.119. P.29–39.
- Emlen S.T. & Oring L.W. 1977. Ecology, sexual selection, and the evolution of mating systems // Science. Vol.197. P.215–223.
- Feldman R., Braun K. & Champagne F.A. 2019. The neural mechanisms and consequences of paternal caregiving // Nature Reviews: Neuroscience. Vol.20. P.205–224.
- Fish E.W., Shahrokh D., Bagot R., Caldji C., Bredy T., Szyf M. & Meaney M.J. 2004. Epigenetic programming of stress responses through variations in maternal care // Annals New York Academy of Science. Vol.1036. P.167–180.
- Francis D., Diorio. J., Liu D. & Meany M.J. 1999. Nongenomic transmission across generations of maternal behavior and stress responses in the rat // Science. Vol.286. P.1155–1158.
- Francis D.D., Young L.J., Meaney M.J. & Insel T.R. 2002. Naturally occurring differences in maternal care are associated with the expression of oxytocin and vasopressin (V1a) receptors: gender differences // Journal of Neuroendocrinology. Vol.14. P.349–353.
- Geoghegan J.L. & Spencer H.G. 2012. Population-epigenetic models of selection // Theoretical Population Biology. Vol.81. P.232–242.
- 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.
- Gleason E.D. & Marler C.A. 2013. Non-genomic transmission of paternal behaviour between fathers and sons in the monogamous and biparental California mouse // Proceedings of Biology Sciences. Vol.280. P.20130824.
- Gos T., Schulkin J., Gos A., Bock J., Poeggel G. & Braun K. 2014. Paternal deprivation affects the functional maturation of corticotrophin-releasing hormone (CRH) and calbindin-D28k-expressing neurons in the bed nucleus of the stria terminalis (BNST) of the biparental Octodon degus // Brain Structure and Functions. Vol.219. P.1983–1990.
- Gromov V.S. 2008. [The spatial-and-ethological population structure in rodents.] Moscow: KMK Sci. Press. 582 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 behavior of the Mongolian gerbil (Meriones unguiculatus) under laboratory conditions // Biology Bulletin. Vol.36. No.5. P.479–488.
- Gromov V.S. 2011a. Parental care, tactile stimulation and sociality evolution in rodents: Behavioural, physiological and developmental aspects. LAP LAMBERT Academic Publ. 104 p.
- 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. The early experience of tactile stimulation and its behavioral consequences related to socialization in mammals // Andersen E.L. & Thomas S. (eds.). Socialization: Theories, Processes and Impact. New York: Nova Science Publ. P.1–28.
- 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. New York: Nova Science Publ. P.71–119.
- Gromov V.S. 2017. The spatial-and-ethological population structure, cooperation, and the evolution of sociality in rodents // Behaviour. Vol.154. P.609–649.
- Gromov V.S. 2018. The evolution of sociality in rodents: Environments and selective forces promoting grouping. LAP LAMBERT Academic Publ. 163 p.
- Gromov V.S. & Osadchuk L.V. 2015. Parental care and testosterone secretion in forest rodent males: sensitization and androgenic stimulation of parental behavior // Biology Bulletin. Vol.42. No.4. P.354–360.
- Gromov V.S. & Voznesenskaya V.V. 2013. Care of young, aggressiveness, and secretion of testosterone in male rodents: a correlation analysis // Biology Bulletin. Vol.40. No.5. P.463–470.
- Gubernick D.J. & Alberts J.R. 1989. Postpartum maintenance of paternal behaviour in the biparental California mouse, Peromyscus californicus // Animal Behaviour. Vol.37. P.656–664.
- Gubernick D.J. & Laskin B. 1994. Mechanisms influencing sibling care in the monogamous biparental California mouse, Peromyscus californicus // Animal Behaviour. Vol.48. P.1235–1237.
- Gubernick D.J. & Nelson R.J. 1989. Prolactin and paternal behavior in the biparental California mouse, Peromyscus californicus // Hormones and Behavior. Vol.23. P.203–210.
- Gubernick D.J. & Teferi T. 2000. Adaptive significance of male parental care in a monogamous mammal // Proceedings of the Royal Society of London, Series B. Vol.267. P.147–150.
- Gubernick D.J., Wright S.L. & Brown R.E. 1993. The significance of fathers presence for offspring survival in the monogamous California mouse, Peromyscus californicus // Animal Behaviour. Vol.46. P.539–546.
- Gubernick D.J., Winslow J.T., Jensen P., Jeanotte L. & Bowen J. 1995. Oxytocin changes in males over the reproductive cycle in the monogamous, biparental California mouse, Peromyscus californicus // Hormones and Behavior. Vol.29. P.59–73.
- Hartung T.G. & Dewsbury D.A. 1979. Paternal behavior in six species of muroid rodents // Behavioral and Neural Biology. Vol.26. P.466–478.
- Hashemian F., Shafigh F. & Roohi E. 2016. Regulatory role of prolactin in paternal behavior in male parents: a narrative review // Journal of Postgraduated Medicine. Vol.62. P.182–187.
- 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.
- Hodgdon H.E., Lancia R.A., 1983. Behavior of the North American beaver, Castor canadensis // Acta Zoologica Fennici. Vol.174. P.99–103.
- Holmes W.G. 1984. The ecological basis of monogamy in Alaskan hoary marmots // Murie J.O. & Michener J.R. (eds.). The biology of ground-dwelling squirrels. Lincoln: Univ. Nebraska Press. P.250–274.
- Horner B.E. & Taylor J.M. 1968. Growth and reproductive behavior in the southern grasshopper mouse // Journal of Mammalogy. Vol.49. P.644–660.
- Horrell N.D., Perea-Rodriguez J.P., Harris B.N. & Saltzman W. 2017. Effects of repeated pup exposure on behavioral, neural, and adrenocortical responses to pups in male California mice (Peromyscus californicus) // Hormones and Behavior. Vol.90. P.56–63.
- Huber S., Millesi E. & Dittami J.P. 2002. Paternal effort and its relation to mating success in the European ground squirrel // Animal Behaviour. Vol.63. P.157–164.
- Hume J.M. & Wynne-Edwards K.E. 2005. Castration reduces male testosterone, estradiol, and territorial aggression, but not paternal behavior in biparental dwarf hamsters (Phodopus campbelli) // Hormones and Behavior. Vol.48. P.303–310.
- Hume J.M. & Wynne-Edwards K.E., 2006. Paternal responsiveness in biparental dwarf hamsters (Phodopus campbelli) does not require estradiol // Hormones and Behavior. Vol.49. P.538–544.
- Insel T.R. & Hulihan T.J. 1995. A gender-specific mechanism for pair bonding: Oxytocin and partner preference formation in monogamous voles // Behavioral Neuroscience. Vol.109. P.782–789.
- 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.
- Jablonka E. & Raz G. 2009. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution // Quarterly Review of Biology. Vol.84. P.131–176.
- Jakubowski M. & Terkel J. 1985. Transition from pup killing to parental behavior in male and virgin female albino rats // Physiology & Behavior. Vol.34. P.683–686.
- Jensen P. 2013. Transgenerational epigenetic effects on animal behaviour // Progress in Biophysics and Molecular Biology. Vol.113. P.447–454.
- Jia R., Tai F., An S. & Zhang X. 2011. Neonatal paternal deprivation or early deprivation reduces adult parental behavior and central estrogen receptor α expression in mandarin voles (Microtus mandarinus) // Behavioural Brain Research. Vol.224. P.279–289.
- Johnston T.D. 1987. The persistence of dichotomies in the study of behavioral development // Developmental Review. Vol.7. P.149–182.
- Kalcounis-Rüppel M.C. & Ribble D.O. 2007. A phylogenetic analysis of the breeding systems of neotomine-peromyscine rodents // Wolff J.O. & Sherman P.W. (eds.). Rodent Societies – An Ecological & Evolutionary Perspective. Chicago: Univ. Chicago Press. P.68–85.
- Kelley D.B. 1988. Sexually dimorphic behaviors // Annual Review of Neuroscience. Vol.11. P.225–251.
- Kenkel W.M., Paredes J., Lewis G.F., Yee J.R., Pournajafi-Nazarloo H., Grippo A.J., Porges S.W. & Carter C.S. 2013. Autonomic substrates of the response to pups in male prairie voles // PLoS One. Vol.8. P.69965.
- Kenkel W.M., Suboc G. & Carter C.S. 2014. Autonomic, behavioral and neuroendocrine correlates of paternal behavior in male prairie voles // Physiology & Behavior. Vol.128. P.252–259.
- Kenkel W.M., Perkeybile A.M. & Carter C.S. 2017. The neurobiological causes and effects of alloparenting // Developmental Neurobiology. Vol.77. P.214–232.
- Kenkel W.M., Perkeybile A.M., Yee J.R. & Carter C.S. 2019. Rewritable fidelity: How repeated pairings and age influence subsequent pair-bond formation in male prairie voles // Hormones and Behavior. Vol.113. P.47–54.
- Ketterson E.D. & Nolan V., Jr. 1992. Hormones and life histories: An integrative approach // American Naturalist. Vol.140 (Suppl.). P.S33–S62.
- Kirkpatrick B., Kim J.W. & Insel T.R. 1994. Limbic system fos expression associated with paternal behavior // Brain Research. Vol.658. P.112–118.
- Kleiman D.G. 1977. Monogamy in mammals // Quarterly Review of Biology. Vol.52. P.39–69.
- Kleiman D.G. & Malcolm J.R. 1981. The evolution of male parental investment // Gubernick D.J. & Klopfer P.H. (eds.). Parental care in mammals. New York: Plenum Press. P.347–387.
- Komers P.E. & Brotherton P.N.M. 1997. Female space use is a best predictor of monogamy in mammals // Proceedings of the Royal Society of London, Series B. Vol.264. P.1261–1270.
- Kurland J.A. & Gaulin S.J.C. 1984. The evolution of male parental investment: effects of genetic relatedness and feeding ecology on the allocation of reproductive effort // Taub D.W. (ed.). Primate paternalism. New York: Van Nostrand Reinhold. P.259–308.
- Lambert K.G., Franssen C.L., Hampton J.E., Rzucidlo A.M., Hyer M.M., True M., Kaufman C. & Bardi M. 2013. Modeling paternal attentiveness: Distressed pups evoke differential neurobiological and behavioral responses in paternal and non-paternal mice // Neuroscience. Vol.234. P.1–12.
- Lambin N. & Krebs C.J. 1991. Spatial organization and mating system of Microtus townsendii // Behavioral Ecology and Sociobiology. Vol.28. P.353–363.
- Lee A.W. & Brown R.E. 2002. Medial preoptic lesions disrupt parental behavior in both male and female California mice (Peromyscus californicus) // Behavioral Neuroscience. Vol.116. P.968–975.
- Lehrman D.S. 1970. Semantic and conceptual issues in the nature-nurture problem // Aronson L.R., Tobach E., Lehrman D.S. & Rosenblatt J.S. (eds.). Development and evolution of behavior. San Francisco: Freeman W.H. P.17–52.
- Lei K., Cushing B.S., Musatov S., Ogawa S. & Kramer K.M. 2010. Estrogen receptor-α in the bed nucleus of the stria terminalis regulates social affiliation in male prairie voles (Microtus ochrogaster) // PLos One. Vol.5. P.8931.
- Lim M.M., Murphy A.Z. & Young L.J. 2004. Ventral striatopallidal oxytocin and vasopressin V1a receptors in the monogamous prairie vole (Microtus ochrogaster) // Journal of Comparative Neurology. Vol.468. P.555–570.
- Liu J.W. & Ben-Jonathan N. 1994. Prolactin-releasing activity of neurohypophysial hormones: structure–function relationship // Endocrinology. Vol.134. P.114–118.
- Liu D., Diorio J., Tannenbaum B., Caldji C., Francis D., Freedman A. & Shanna S. 1997. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress // Science. Vol.277. P.1659–1662.
- Lonstein J.S. & De Vries G.J. 1999. Sex differences in the parental behaviour of adult virgin prairie voles: independence from gonadal hormones and vasopressin // Journal of Neuroendocrinology. Vol.11. P.441–449.
- Lonstein J.S. & De Vries G.J. 2000. Sex differences in the parental behavior of rodents // Neuroscience and Biobehavioral Reviews. Vol.24. P.669–686.
- Lonstein J.S., Rood B.D. & De Vries G.J. 2002. Parental responsiveness is feminized after neonatal castration in virgin male prairie voles, but is not masculinized by perinatal testosterone in virgin females // Hormones and Behavior. Vol.41. P.80–87.
- Luis J., Vázquez-Gaytán B., Martínez-Torres M., Carmona A., Ramos-Blancas G. & Ortíz G. 2010. Neither testosterone levels nor aggression decrease when the male Mongolian gerbil (Meriones unguiculatus) displays paternal behavior // Hormones and Behavior. Vol.57. P.271–275.
- Lukas D. & Clutton-Brock T.H. 2013. The evolution of social monogamy in mammals // Science. Vol.341. P.526–530.
- Maher C.R. & Burger J.R. 2016. Diversity of social behavior in caviomorph rodents // Ebensperger L.A. & Hayes L.D. (eds.). Sociobiology of caviomorph rodents: an integrative approach. Chichester: John Wiley & Sons. P.28–58.
- Marinelli L. & Messier F. 1993. Space use and the social system of muskrat (Ondatra zibethicus) // Canadian Journal of Zoology. Vol.71. P.869–875.
- Marinelli L. & Messier F. 1995. Parental care strategies among muskrats in a female-biased population // Canadian Journal of Zoology. Vol.73. P.1503–1510.
- Marler C.A., Bester-Meredith J.K. & Trainor B.C. 2003. Paternal behavior and aggression: Endocrine mechanisms and nongenomic transmission of behavior // Advances in the Study of Behavior. Vol.32. P.263–323.
- Martınez A., Ramos G., Martınez-Torres M., Nicolas L., Carmona A., Cardenas M. & Luis J. 2015. Paternal behavior in the Mongolian gerbil (Meriones unguiculatus): estrogenic and androgenic regulation // Hormones and Behavior. Vol.71. P.91–95.
- 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.
- Mashoodh R. & Champagne F.A. 2019. Paternal epigenetic inheritance // Transgenerational Epigenetics. 2nd ed. P.107–133.
- Mateo J.M. 2007. Ontogeny of adaptive behaviors // Wolff J.O. & Sherman P.W. (eds.). Rodent Societies – An Ecological & Evolutionary Perspective. Chicago: Univ. Chicago Press. P.195–206.
- Maynard-Smith J. 1977. Parental investment: a prospective analysis // Animal Behaviour. Vol.25. P.1–9.
- Maynard-Smith J. 1982. Evolution and the Theory of Games. Cambridge: Cambridge University Press. 265 p.
- McCarty R. & Southwick C.H. 1977. Patterns of parental care in two cricetid rodents, Onychomys torridus and Peromyscus leucopus // Animal Behaviour. Vol.25. P.945–948.
- McGowan P.O., Meaney M.J. & Szyf M. 2008. Diet and the epigenetic (re)programming of phenotypic differences in behavior // Brain Research. Vol.1237. P.12–24.
- McGuire B. 1988. Effects of cross-fostering on parental behavior of meadow voles (Microtus pennsylvanicus) // Journal of Mammalogy. Vol.69. P.332–341.
- McGuire B. 2003. Paternal care and its effect on maternal behavior and pup survival and development in prairie voles (Microtus ochrogaster) // Exploring Animal Behavior in Laboratory and Field. P.167–176.
- McGuire B. & Bemis W.E. 2007. Parental care // Wolff J.O. & Sherman P.W. (eds.). Rodent Societies – An Ecological & Evolutionary Perspective. Chicago: Univ. Chicago Press. P.231–242.
- 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.
- McGuire B. & Novak M. 1986. Parental care and its relation to social organization in the montane vole // Journal of Mammalogy. Vol.67. P.305–311.
- McGuire B., Henyey E., McCue E. & Bemis W.E. 2003. Parental behavior at parturition in prairie voles (Microtus ochrogaster) // Journal of Mammalogy. Vol.84. P.513–523.
- Meaney M.J. 2001. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations // Annual Review of Neuroscience. Vol.24. P.1161–1192.
- Meaney M.J. & Szyf M. 2005. Maternal care as a model for experience-dependent chromatin plasticity? // Trends in Neuroscience. Vol.28. P.456–463.
- Meaney M.J., Szyf M. & Seckl J.R. 2007. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitary-adrenal function and health // Trends in Molecular Medicine. Vol.13. P.269–277.
- Mihok S. 1979. Behavioral structure and demography of subarctic Clethrionomys gapperi and Peromyscus maniculatus // Canadian Journal of Zoology. Vol.57. P.1520–1535.
- Nonneman D.J., Ganjam V.K., Welshons W.V. & vom Saal F.S. 1992. Intrauterine position effects on steroid metabolism and steroid receptors of reproductive organs in male mice // Biology of Reproduction. Vol.47. P.723–729.
- Numan M. & Insel T. 2003. The Neurobiology of Parental Behavior. New York: Springer. 418 p.
- Numan M. & Stolzenberg D.S. 2009. Medial preoptic area interactions with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats // Frontiers in Neuroendocrinology. Vol.30. P.46–64.
- Orians G.H. 1969. On the evolution of mating systems in birds and mammals // The American Naturalist. Vol.103. P.589–604.
- Parker K.J. & Lee T.M. 2001a. Social and environmental factors influence the suppression of pup-directed aggression and development of paternal behavior in captive meadow voles (Microtus pennsylvanicus) // Journal of Comparative Psychology. Vol.115. P.331–336.
- Parker K.J. & Lee T.M. 2001b. Central vasopressin administration regulates the onset of facultative paternal behavior in Microtus pennsylvanicus (meadow voles) // Hormones and Behavior. Vol.39. P.285–294.
- Patris B. & Baudoin C. 2000. A comparative study of parental care between two rodent species: implications for the mating system of the mound-building mouse Mus spicilegus // Behavioural Processes. Vol.51. P.35–43.
- PayneR.B. & Payne L.L. 1993. Breeding dispersal in Indigo buntings: circumstances and consequences for breeding success and population structure // Condor. Vol.95. P.1–24.
- Pei M., Matsuda K.-I., Sakamoto H. & Kawata M. 2006. Intrauterine proximity to male fetuses affects the morphology of the sexually dimorphic nucleus of the preoptic area in the adult rat brain // European Journal of Neuroscience. Vol.23. P.1234–1240.
- Perea-Rodriguez J.P., Takahashi E.Y., Amador T.M., Hao R.C., Saltzman W. & Trainor B.C. 2015. Effects of reproductive experience on central expression of progesterone, estrogen α, oxytocin and vasopressin receptor mRNA in male California mice (Peromyscus californicus) // Journal of Neuroendocrinology. Vol.27. P.245–252.
- Perkeybile A.M., Griffin L.L. & Bales K.L. 2013. Natural variation in early parental care correlates with social behaviors in adolescent prairie voles (Microtus ochrogaster) // Frontiers in Behavioral Neuroscience. Vol.7:21.
- Perkeybile A.M., Delaney-Busch N., Hartman S., Grimm K.J. & Bales K.L. 2015. Intergenerational transmission of alloparental behavior and oxytocin and vasoapressin receptor distribution in the prairie vole // Frontiers in Behavioral Neuroscience. Vol.9:191.
- Perrigo G., Belvin L. & vom Saal F.S. 1991. Individual variation in the neural timing of infanticide and parental behavior in male house mice // Physiology & Behavior. Vol.50. P.287–296.
- Porter R.H., Cavallaro S.A. & Moore J.D. 1980. Developmental parameters on mother-offsping interactions in Acomys cahirinus // Zeitschrift für Tierpsychologie. Bd.53. S.153–170.
- Rakyan V.K. & Beck S. 2006. Epigenetic variation and inheritance in mammals // Current Opinion in General Development. Vol.16. P.573–577.
- Rakyan V. & Whitelaw E. 2003. Transgenerational epigenetic inheritance // Current Biology. Vol.13. P.6.
- Rando O.J. 2012. Daddy issues: Paternal effects on phenotype // Cell. Vol.151. P.702–708.
- Reburn C.J. & Wynne-Edwards K.E. 1999. Hormonal changes in males of a naturally biparental and a uniparental mammal // Hormones and Behavior. Vol.35. P.163–176.
- Reik W. 2001. Epigenetic reprogramming in mammalian development // Science. Vol.293. P.1089–1093.
- Requena G.S. & Alonzo S.H. 2017. Sperm competition games when males invest in paternal care // Proceedings of Biology Sciences. Vol.284:20171266.
- Reynolds J.D., Goodwin N.B. & Freckleton R.P. 2002. Evolutionary transitions in parental care and live bearing in vertebrates // Philosophical Transactions Royal Society of London, Series B. Vol.357. P.269–281.
- Ribble D.O. 2003. The evolution of social and reproductive monogamy in Peromyscus, evidence from Peromyscus californicus (the California mouse) // Reichard U. & Boesh C. (eds.). Monogamy: Mating strategies and partnership in birds, humans, and other mammals. Cambridge: Cambridge Univ. Press. P.81–92.
- 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.
- Ridley P. 1978. Paternal care // Animal Behaviour. Vol.26. P.904–932.
- Rilling J.K. & Mascaro J.S. 2017. The neurobiology of fatherhood // Current Opinion in Psychology. Vol.15. P.26–32.
- 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.
- Roberts R.L., Miller A.K., Taymans S.E. & Carter C.S. 1999. Role of social and endocrine factors in alloparental behavior of prairie voles (Microtus ochrogaster) // Canadian Journal of Zoology. Vol.76. P.1862–1868.
- Romero-Morales L., Martínez-Torres M., Cárdenas M., Álvarez C., Carmona A., Cedillo B., Loya-Zurita E. & Luis J. 2018a. An increase in estradiol facilitates the onset of paternal behavior in the dwarf hamster (Phodopus campbelli) // Hormones and Behavior. Vol.99. P.35–40.
- Romero-Morales L., Cárdenas M., Martínez-Torres M., García-Saucedo B., Carmona A. & Luis J. 2018b. Neuronal activation associated with paternal and aversive interactions toward pups in the Mongolian gerbils (Meriones unguiculatus) // Hormones and Behavior. Vol.105. P.47–57.
- Rosenbaum S. & Getter L.T. 2018. With a little help from her friends (and family) part II: non-maternal care-giving behavior and physiology in mammals // Physiology & Behavior. Vol.193. P.12–24.
- 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.
- Rosenblatt J.S., Hazelwood S. & Poole J. 1996. Maternal behavior in male rats: effects of medial preoptic area lesions and presence of maternal aggression // Hormones and Behavior. Vol.30. P.201–215.
- Royle N.J., Russel A.F. & Wilson A.J. 2014. The evolution of flexible parenting // Science. Vol.345. P.776–781.
- Ryan B.C. & Vandenbergh J.G. 2002. Intrauterine position effects // Neuroscience and Biobehavioral Reviews. Vol.26. P.665.
- Rymer T. & Pillay N. 2011. The influence of the early rearing environment on the development of paternal care in African striped mice // Ethology. Vol.117. P.284–293.
- Rymer T. & Pillay N. 2018. An integrated understanding of paternal care in mammals: Lessons from the rodents // Journal of Zoology. Vol.306. No.2. P.69–76.
- Sakaguchi K., Tanaka M., Ohkubo T., Dohura K., Fujikawa T., Sudo S. & Nakashima K. 1996. Induction of brain prolactin receptor long-form mRNA expression and maternal behavior in pup-contacted male rats: promotion by prolactin administration and suppression by female contact // Neuroendocrinology. Vol.63. P.559–568.
- Saltzman W. & Ziegler T.E. 2014. Functional significance of hormonal changes in mammalian fathers // Journal of Neuroendocrinology. Vol.26. P.685–96.
- Saltzman W., Harris B.N., De Jong T.R., Perea-Rodriguez J.P., Horrell N.D., Zhao M. & Andrew J.R. 2017. Paternal care in biparental rodents: intra- and inter-individual variation // Integrative and Comparative Biology. Vol.57. P.589–602.
- Schneider J.S., Stone M.K., Wynne-Edwards K.E., Horton T.H., Lydon J.P., OMalley B. & Levine J.E. 2003. Progesterone receptors mediate male aggression towards infants // Proceedings of the National Academy of Sciences of USA. Vol.100. P.2951–2956.
- Schradin C. & Anzenberger G. 1999. Prolactin, the hormone of paternity // New Physiological Sciences. Vol.14. P.223–231.
- Schradin C. & Pillay N. 2004. Prolactin levels in paternal striped mouse (Rhabdomys pumilio) fathers // Physiology & Behavior. Vol.81. P.43–50.
- Schubert M., Pillay N. & Schradin C. 2009. Parental and alloparental care in a polygynous mammal // Journal of Mammalogy. Vol.90. P.724–731.
- Schum J.E. & Wynne-Edwards K.E. 2005. Estradiol, progesterone and testosterone in paternal and non-paternal hamsters (Phodopus) becoming fathers: conflict with hypothesized roles. Hormones and Behavior. Vol.47. P.410–418.
- Shen S.F., Emlen S.T., Koenig W.D. & Rubenstein D.R. 2017. The ecology of cooperative breeding behaviour // Ecology Letters. Vol.20. P.708–720.
- Shin S.H. 1996. Vasopressin has a direct effect on prolactin release in male rats // Neuroendocrinology. Vol.34. P.55–58.
- Skinner M., Anway M., Savenkova M. & Gore A. 2008. Transgenerational epigenetic programming of the brain transcriptome and anxiety behavior // PLoS ONE. Vol.3. P.3745.
- Slobodchikoff C.N. 1984. Resources and the evolution of social behavior // Price P.W., Slobodchikoff C.N. & Gaud W.S. (eds.). A New Ecology: Novel Approaches to Interactive Systems. New York: John Wiley & Sons. P.227–251.
- Solomon N.G., Keane B., Knoch L.R. & Hogan P.J. 2004. Multiple paternity in socially monogamous prairie voles (Microtus ochrogaster) // Canadian Journal of Zoology. Vol.82. P.1667–1671.
- Sommer S. 1997. Monogamy in Hypogeomys antimena, an endemic rodent of the deciduous dry forest in western Madagascar // Journal of Zoology. Vol.241. P.301–314.
- Song Z., Tai F., Yu C., Wu R., Zhang X., Broders H., He F. & Guo R. 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.
- Soroker V. & Terkel J. 1988. Changes in incidence of infanticidal and parental responses during the reproductive cycle in male and female wild mice Mus musculus // Animal Behaviour. Vol.36. P.1275–l281.
- Stockley P. & Hobson L. 2016. Paternal care and litter size coevolution in mammals // Proceedings of Royal Society of London, Series B. Vol.283. P.20160140.
- Stolzenberg D.S., Stevens J.S. & Rissman E.F. 2012. Experience-facilitated improvements in pup retrieval; evidence for an epigenetic effect // Hormones and Behavior. Vol.62. P.128–135.
- Storey A.E. & Joyce T.L. 1995. Pup contact promotes paternal responsiveness in male meadow voles // Animal Behaviour. Vol.49. P.1–10.
- Storey A.E. & Snow D.T. 1987. Male identity and enclosure size effect paternal attendance of meadow voles, Microtus pennsilvanicus // Animal Behaviour. Vol.5. P.411–419.
- Storey A.E., Bradbury C.G. & Joyce T.L. 1994. Nest attendance in male meadow voles: the role of the female in regulating male interactions with pups // Animal Behaviour. Vol.47. P.1037–1046.
- Sturgis J.D. & Bridges R.S. 1997. N-methyl-DL-aspartic acid lesions on the medial preoptic area disrupt ongoing parental behavior in male rats // Physiology & Behavior. Vol.62. P.305–310.
- Szyf M. 2015. Nongenetic inheritance and transgenerational epigenetics // Trends in Molecular Medicine. Vol.21. P.134–144.
- Trainor B.C. & Marler C.A. 2001. Testosterone, paternal behav¬ior, and aggression in the monogamous California mouse (Peromyscus californicus) // Hormones and Behavior. Vol.40. P.32–42.
- 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. 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.
- Trivers R.L. 1972. Parental investment and sexual selection // Campbell B. (ed.). Sexual selection and the descent of man. Chicago: Aldine. P.136–179.
- Turner J.D., Kirschner S.A., Molitor A.M., Evdokimov K. & Muller C.P. 2015. Epigenetics // International encyclopedia of the social and behavioral sciences. 2nd ed. P.839–847.
- Vella E.T., Evans C.C., Ng M.W. & Wynne-Edwards K.E. 2005. Ontogeny of the transition from killer to caregiver in dwarf hamsters (Phodopus campbelli) with biparental care // Developmental Psychobiology. Vol.46. P.75–85.
- Vom Saal F.S., Grant W.M., McMullen C.W. & Laves K.S. 1983. High fetal estrogen concentrations: correlation with in¬creased adult sexual activity and decreased aggression in male mice // Science. Vol.220. P.1306–1309.
- Walsh C.J., Fleming A.S., Lee A. & Magnusson J.E. 1996. The effects of olfactory and somatosensory desensitization on fos-like immunoreactivity in the brains of pup-exposed postpartum rats // Behavioral Neuroscience. Vol.110. P.134–153.
- Walton J.M. & Wynne-Edwards K.E., 1997. Paternal care reduces maternal hyperthermia in Djungarian hamsters (Phodopus campbelli) // Physiology & Behavior. Vol.63. P.41–47.
- Wang Z.X. & De Vries G.J. 1993. Testosterone effects on paternal behavior and vasopressin immunoreactive projections in prairie voles (Microtus ochrogaster) // Brain Research. Vol.631. P.156–160.
- Wang Z.X. & Novak M.A. 1994. Alloparental care and the influence of father presence on juvenile prairie voles, Microtus ochrogaster // Animal Behaviour. Vol.47. P.282–288.
- Wang Z., Ferris C.F. & De Vries G.J. 1994. Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster) // Proceedings of National Academy of Sciences of USA. Vol.91. P.400–404.
- Wang Z., Young L.J., De Vries G.J. & Insel T.R. 1999. Voles and vasopressin: A review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors // Progress in Brain Research. Vol.119. P.483–499.
- Wang Z.X., Liu Y. & Insel T.R. 2000. Hypothalamic vasopressin gene expression increases in both males and females postpartum in a biparental rodent // Journal of Neuroendocrinology. Vol.12. P.111–120.
- Wang L., Zhang W., Wu R., Kong L., Feng W., Cao Y., Tai F. & Zhang X. 2014. Neuroendocrine responses to social isolation and paternal deprivation at different postnatal ages in mandarin voles // Developmental Psychobiology. Vol.56. P.1214–1228.
- Wang P., Yang H.-P., Tian S., Wang L., Wang S., Zhang F. & Wang Y.-F. 2015. Oxitocin-secreting system: a major part of the neuroendocrine center regulating immunologic activity // Journal of Neuroimmunology. Vol.289. P.152–161.
- Wang B., Wang L., Wang K. & Tai F. 2018. The effects of fathering experience on paternal behaviors and levels of central expression of oxytocin and dopamine-2 type receptors in mandarin voles // Physiology & Behavior. Vol.193. P.35–42.
- Waterman J. 2007. Male mating strategies in rodents // Wolff J.O. & Sherman P.W. (eds.). Rodent Societies – An Ecological & Evolutionary Perspective. Chicago: Univ. Chicago Press. P.27–41.
- Weaver I.C. 2007. Epigenetic programming by maternal behavior and pharmacological intervention. Nature versus nurture: lets call the whole thing off // Epigenetics. Vol.2. P.22–28.
- Weaver I.C., Cervoni F., Champagne A., DAlessio S., Sharma J., Seckl S., Dymov M., Szyf M. & Meany M. 2004. Epigenetic programming by maternal behavior // Nature Neuroscience. Vol.7. P.847–854.
- Werren J.H., Gross M.R. & Shine R., 1980. Paternity and the evolution of male parental care // Journal of Theoretical Biology. Vol.82. P.619–631.
- West H.E. & Capellini I. 2016. Male care and life history traits in mammals // Nature Communications. Vol.7. P.1–10.
- Westnead D.F. & Sherman P.W. 1993. Parentage and the evolution of parental behavior // Behavioral Ecology. Vol.4. P.66–77.
- Wittenberger J.F. & Tilson R.L. 1980. The evolution of monogamy: Hypotheses and evidence // Annual Review of Ecology and Systematics. Vol.11. P.197–232.
- Wolff J.O. 1985. Social behaviour // Kirkland G.L. & Layne J.N. (eds.) Advances in the Study of Peromyscus (Rodentia). Lubbock: Texas Tech Univ. Press. P.271–291.
- Wolff J.O. 2003. Laboratory studies with rodents: Facts or artifacts // BioScience. Vol.53. P.421–427.
- Wolf J.B., Brodie E.D., Cheverud J.M., Moore A.J. & Wade M.J. 1998. Evolutionary consequences of indirect genetic effects // Trends in Ecology & Evolution. Vol.13. P.64–69.
- Woodroffe R. & Vincent A. 1994. Mothers little helpers: Patterns of male care in mammals // Trends in Ecology & Evolution. Vol.9. P.294–297.
- 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 // Behavioral Processes. Vol.60. P.41–52.
- Wynne-Edwards K.E. 1995. Biparental care in Djungarian but not Siberian dwarf hamsters (Phodopus) // Animal Behaviour. Vol.50. P.1571–1585.
- Wynne-Edwards K. E. 2001. Hormonal changes in mammalian fathers // Hormones and Behavior. Vol.40. P.139–145.
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