How Fathers Evolve: A Functional Analysis of Fathering Behavior

  • Anne Storey
  • Carolyn Walsh
Part of the National Symposium on Family Issues book series (NSFI)


In mammals, paternal care is rarer and more variable in its proximate mechanisms of development and underlying neural mechanisms than is maternal care. Here, we discuss how species differences in these proximate mechanisms reflect ecological pressures that have been selected for biparental care and argue that paternal care is more fixed (i.e., shaped less by social experiences) in those species where it is most important for infant survival. A second theme is that glucocorticoids such as cortisol and corticosterone are associated with both positive (more responsive to infant cues, more domestic work) and negative aspects of parenting (find parenting more difficult) in human fathers, findings that mirror research on maternal behavior. Finally, we discuss an animal model with obligatory biparental care, a seabird, the common murre (Uria aalge) – and show, as in humans, that elevated corticosterone is associated with both positive and negative aspects of parental responses, depending on environmental (foraging) context. We conclude that biparental care contributes to flexibility in reproductive strategies that allow organisms to extend their seasonal or geographic breeding ranges.

Questions about parenting behavior can be examined from at least four different perspectives (as in Tinbergen, 1963). We share this view with Mileva and Fleming (see  Chap. 1), based in part on the common training that Fleming and Storey received from the Institute of Animal Behavior and have shared with students and colleagues. These four perspectives include studies of mechanism and development at the individual level, which has been Fleming’s focus, and studies of why and how the behavior evolved, which has been our emphasis. Studies of mechanism include all components discussed by Mileva and Fleming, including how sensory stimuli from the young initiate the hormonal and neural responses that trigger parental behavior. Mileva and Fleming’s overview of the mechanisms underlying maternal behavior covered the field beautifully, summarizing the seminal contributions of Fleming and her colleagues. In fact, the work by Fleming and colleagues in this area is so comprehensive that there are no gaps.

For this reason, we develop a comparison here with the much smaller literature on the other parent, the father. We are interested in evolutionary/functional questions such as why there are species and individual differences in fathers’ involvement in the care of offspring. We explore how selection for flexibility in the expression of paternal care under different social and environmental conditions has shaped its development and neural mechanisms. In connection with fathers, we develop two other themes from the Mileva and Fleming chapter: the role of glucocorticoids (cortisol and corticosterone), hormones linked to both positive and negative aspects of parenting, and the use of an animal model to understand the ecological context in which biparental care evolves.


Parental Behavior Paternal Care Prairie Vole Meadow Vole Djungarian Hamster 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. Alvergne, A., Faurie, C., & Raymond, M. (2009). Father–offspring resemblance predicts paternal investment in humans. Animal Behavior, 78, 61–69.CrossRefGoogle Scholar
  2. Astheimer, L. B., Buttemer, W. A., & Wingfield, J. C. (1992). Interactions of corticosterone with feeding, activity and metabolism in passerine birds. Ornis Scandinavica, 23, 355–365.CrossRefGoogle Scholar
  3. Barry, H., & Paxson, L. M. (1971). Infancy and early childhood: cross cultural codes 2. Ethnology, 10, 466–508.CrossRefGoogle Scholar
  4. Belsky, J., Steinberg, L., & Draper, P. (1991). Childhood experience, interpersonal development, and reproductive strategy: an evolutionary theory of socialization. Child Development, 62, 647–670.PubMedCrossRefGoogle Scholar
  5. Belthoff, J. R., & Dufty, A. M. (1998). Corticosterone, body condition and locomotor activity: a model for dispersal in screech–owls. Animal Behavior, 55, 405–415.CrossRefGoogle Scholar
  6. Berg, S. J., & Wynne–Edwards, K. E. (2001). Changes in testosterone, cortisol, and estradiol levels in men becoming fathers. Mayo Clinic Proceedings, 76, 582–592.PubMedGoogle Scholar
  7. 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, 47, 358–366.PubMedCrossRefGoogle Scholar
  8. 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, 29, 474–491.PubMedCrossRefGoogle Scholar
  9. Buchan, J.C., Alberts, S.C., Silk, J.B., & Altmann, J. (2003). True paternal care in a multi–male primate society. Nature, 425, 179–181.PubMedCrossRefGoogle Scholar
  10. Carpentier, M. J. E., Van Horn, R. C., Altmann, J., & Alberts, S. C. (2008). Paternal effects of offspring fitness in a multimale primate society. Proceedings of the Royal Society of London, Series B, Biological Science, 105, 1988–1992.Google Scholar
  11. 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, 113, 388–395.PubMedCrossRefGoogle Scholar
  12. 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, 29, 1089–1105.PubMedCrossRefGoogle Scholar
  13. Cushing, B. S., Perry, A., Musatov, S., Ogawa, S., & Papademetriou, E. (2008). Estrogen receptors in the medial amydala inhibit the expression of male prosocial behavior. Journal of Neuroscience, 28, 10399–10403.PubMedCrossRefGoogle Scholar
  14. Cushing, B. S., Razzoli, M., Murphy, A. Z., Epperson, P. M., Le, W–W., & Hoffman, G. E. (2004). Intraspecific variation in estrogen receptor alpha and the expression of male sociosexual behavior in two populations of prairie voles. Brain Research, 1016, 247–254.PubMedCrossRefGoogle Scholar
  15. Cushing, B. S., & Wynne–Edwards, K. E. (2006). Estrogen receptor-a distribution in male rodents is associated with social organization. Journal of Comparative Neurology, 494, 595–605.PubMedCrossRefGoogle Scholar
  16. de Jong, T. R., Chauke, M., Harris, B. N., & Saltzman, W. (2009). From here to paternity: Neural correlates of the onset of paternal behavior in California mice (Peromyscus californicus). Hormones and Behavior, 56, 220–231.PubMedCrossRefGoogle Scholar
  17. Delahunty, K. M, McKay, D. W., Noseworthy, D. E., & Storey, A. E. (2007). Prolactin responses to infant cues in men and women: effects of parental experience and recent infant contact. Hormones and Behavior, 51, 213–220.PubMedCrossRefGoogle Scholar
  18. Doody, L. M., Wilhelm, S. I., McKay, D. W., & Storey, A. E. (2008). The effects of variable foraging conditions on common murre (Uria aalge) parental behavior and corticosterone concentrations. Hormones and Behavior, 53, 140–148.PubMedCrossRefGoogle Scholar
  19. Ehlert, U., Patalla, U., Kirschbaum, C., Piedmont, E., & Hellhammer, D. H. (1990). Postpartum blues: salivary cortisol and psychological factors. Journal of Psychosomatic Medicine, 34, 319–325.CrossRefGoogle Scholar
  20. Fleming, A. S., Corter, C., Stallings, J., & Steiner, M. (2002). Testosterone and prolactin are associated with emotional responses to infant cries in new fathers. Hormones and Behavior, 42, 399–413.PubMedCrossRefGoogle Scholar
  21. Fleming, A. S., Ruble, D., Krieger, H., & Wong, P. Y. (1997). Hormonal and experiential ­correlates of maternal responsiveness during pregnancy and the puerperium in human mothers. Hormones and Behavior, 31, 145–158.PubMedCrossRefGoogle Scholar
  22. Fleming, A. S., Steiner, M., & Corter, C. (1997). Cortisol, hedonics, and maternal responsiveness in human mothers. Hormones and Behavior, 32, 85–98.PubMedCrossRefGoogle Scholar
  23. Gonzales, A., Jenkins, J. M, Steiner, M., & Fleming, A. S. (2009). The relation between early life adversity, cortisol awakening response and diurnal salivary cortisol levels in postpartum women. Psychoneuroendocrinology, 34, 76–86.CrossRefGoogle Scholar
  24. Gray, P. B., Kathlenberg, S. M., Barrett E. S., Lipson S. F., & Ellison P. T. (2002). Marriage and fatherhood are associated with lower testosterone in males. Evolution and Human Behavior, 23, 193–201.CrossRefGoogle Scholar
  25. Groer, M. W., & Morgan, K. (2007). Immune, health and endocrine characteristics of depressed postpartum mothers. Psychoneuroendocrinology, 32, 133–139.PubMedCrossRefGoogle Scholar
  26. Gubernick, D. J., Schneider, K. A., & Jeannotte, L. A. (1994). Individual differences in the mechanisms underlying the onset and maintenance of paternal behavior and the inhibition of ­infanticide in the monogamous biparental California mouse, Peromyscus californicus. Behavioral Ecology and Sociobiology, 34, 225–231.CrossRefGoogle Scholar
  27. Gubernick, D. J., Wright, S. L., & Brown, R. E. (1993). The significance of father’s Presence for offspring survival in the monogamous California mouse, Peromyscus californicus. Animal Behavior, 46, 539–546.CrossRefGoogle Scholar
  28. Han, T. M., & De Vries, G. J. (2003). Organizational effects of testosterone, estradiol, and dihydrotestosterone on vasopressin mRNA expression in the bed nucleus of the stria terminalis. Journal of Neurobiology, 54, 502–510.PubMedCrossRefGoogle Scholar
  29. Hewlett, B. S. (1992). Husband–wife reciprocity and the father–infant relationship among Aka Pygmies. In B. S. Hewlett (Ed.), Father–child Relations: Cultural and biosocial contexts (pp. 31–55). NewYork: Aldine de Gruyter.Google Scholar
  30. Huber, S., Millesi, E., & Dittami, J. P. (2002). Paternal effort and its relation to mating success in the European ground squirrel. Animal Behavior, 63, 157–164.CrossRefGoogle Scholar
  31. Hurtado, A. M., & Hill, K. R. (1992). Paternal effects of offspring survivorship among Ache and Hiwi hunter–gatherers: implications for modeling pair–bond stability. In B. S. Hewlett (Ed.), Father–child relations: Cultural and biosocial contexts (pp. 153–176). New York: Aldine de Gruyter.Google Scholar
  32. Iwaniuk, A. N. (2005). Evolution. In I. Q. Whishaw & B. Kolb (Eds.), The behavior of the laboratory­ rat: A handbook with tests (pp. 3–14). New York: Oxford University Press.Google Scholar
  33. Jia, R., Tai, F., An, S., Zhang, X., & Broders, H. (2009). Effects of neonatal paternal deprivation or early deprivation on anxiety and social behaviors of the adults in maderin voles. Behavioral Processes, 82, 271–278.CrossRefGoogle Scholar
  34. Jones, J. S., & Wynne–Edwards, K. E. (2001). Paternal behavior in biparental hamsters, Phodopus campbelli, does not require contact with the pregnant female. Animal Behavior, 62, 453–464.CrossRefGoogle Scholar
  35. Jones, K.M., Ruxton, G.D., & Monaghan, P. (2002). Model parents: is full compensation for reduced partner nest attendance compatible with stable biparental care? Behavioral Ecology, 13, 838–843.CrossRefGoogle Scholar
  36. Kleiman, D. G., & Malcolm, J. R. (1981). The evolution of male parental investment in mammals. Quarterly Review of Biology, 52, 39–68.Google Scholar
  37. Kramer, K. K., Perry, A. N., Golbin, D., & Cushing, B. S. (2009). Sex steroids are necessary in the second postnatal week for the expression of male alloparental behavior in prairie voles (Microtus ochragaster). Behavioral Neuroscience, 123, 958–963.PubMedCrossRefGoogle Scholar
  38. Luis, J., Ramirez, L., Carmona, A., Ortiz, G., Delgado, J., & Cárdenas, R. (2009). Paternal ­behavior and testosterone plasma levels in the Volcano Mouse Neotomodon alstoni (Rodentia: Muridae). International Journal of Tropical Biology, 57, 433–439.Google Scholar
  39. Madison, D. M., Fitzgerald, R. W., & McShea, W. J. (1984). Dynamics of social nesting in overwintering meadow voles, Microtus pennsylvanicus: possible consequences for population cycling. Behavioral Ecology and Sociobiology, 15, 9–17.CrossRefGoogle Scholar
  40. McEwen, B.S., & Wingfield, J.C. (2003). The concept of allostasis in biology and biomedicine. Hormones and Behavior, 43, 2–15.PubMedCrossRefGoogle Scholar
  41. McGuire, B. (1988). Effects of cross–fostering on parental behavior in the meadow vole (Microtus pennsylvanicus). Journal of Mammalogy, 69, 332–341.CrossRefGoogle Scholar
  42. Oliveras, D., & Novak, M. (1986). A comparison of paternal behavior in the meadow vole (Microtus pennsylvanicus), the pine vole (M. pinetorum) and the prairie vole (M. ochrogaster). Animal Behavior, 34, 519–526.CrossRefGoogle Scholar
  43. Parker, K. J., & Lee, T. M. (2001). Central vasopressin administration regulates the onset of paternal behavior in Microtus pennsylvanicus. Hormones and Behavior, 39, 285–294.PubMedCrossRefGoogle Scholar
  44. Reburn, C.J., & Wynne–Edwards, K.E. (1999). Hormonal changes in males of a naturally ­biparental and a uniparental mammal. Hormones and Behavior, 35, 163–176.PubMedCrossRefGoogle Scholar
  45. Roberts, R. L., Jenkins, K. T., Lawler, T., Jr., Wegner, F. H., & Newman, J. D. (2001). Bromocriptine administration lowers serum prolactin and disrupts parental responsiveness in common marmosets (Callithrix j. jacchus). Hormones and Behavior, 39, 106–112.PubMedCrossRefGoogle Scholar
  46. 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 Behavior, 55, 1131–1140.CrossRefGoogle Scholar
  47. Romero, M., Dickens, M. J., & Cyr, N. E. (2009). The reactive scope model – A new model ­integrating homeostasis, allostasis, and stress. Hormones and Behavior, 55, 375–389.PubMedCrossRefGoogle Scholar
  48. Schradin, C., & Pillay, N. (2004). The influence of the father on offspring development in the striped mouse. Behavioral Ecology, 16, 450–455.CrossRefGoogle Scholar
  49. Seifritz, E., Esposito, F., Neuhoff, J. G., Luthi, A., Mustovic, H., Dammann G., et al. (2003). Differential sex–independent amygdala response to infant crying and laughing in parents versus nonparents. Biological Psychiatry, 54, 1367–1375.PubMedCrossRefGoogle Scholar
  50. 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 Behavior, 47, 1037–1046.CrossRefGoogle Scholar
  51. Storey, A. E., Delahunty, K. M., McKay, D. M., Walsh, C. J., & Wilhelm, S. I. (2006). Social and hormonal bases for individual differences in the parental behavior of bird and mammals. Canadian Journal of Experimental Psychology, 60, 237–245.PubMedCrossRefGoogle Scholar
  52. Storey, A. E., Delahunty, K. M., & McKay, D. W. (2007). Are elevated cortisol levels associated with enhanced or reduced parental responsiveness? Poster presented at the Parental Brain Conference, Boston.Google Scholar
  53. Storey, A. E., & Joyce, T. L. (1995). Pup contact promotes paternal responsiveness in male meadow voles. Animal Behavior, 49, 1–10.CrossRefGoogle Scholar
  54. Storey, A. E., & Snow, D. T. (1987). Male identity and enclosure size affect paternal attendance of meadow voles, Microtus pennsylvanicus. Animal Behavior, 35, 411–419.CrossRefGoogle Scholar
  55. Storey, A. E. & Walsh, C. J. (1994). The role of physical contact from females and pups in the development of paternal responsiveness in meadow voles. Behavior, 131, 139–151.CrossRefGoogle Scholar
  56. Storey, A. E., Walsh, C. J., Quinton, R., & Wynne–Edwards, K. E. (2000). Hormonal correlates of paternal responsiveness in new and expectant fathers. Evolution and Human Behavior, 21, 79–95.PubMedCrossRefGoogle Scholar
  57. Taylor, A., Glover, V., Marks, M., & Kammerer, M. (2009). Diurnal pattern of cortisol output in postnatal depression. Psychoneuronedocrinology, 34, 1184–1188.CrossRefGoogle Scholar
  58. Timonin, M. E., & Wynne–Edwards, K. E. (2008). Aromatase inhibition during adolescence reduces adult sexual and paternal behavior in the biparental dwarf hamster Phodopus ­campbelli. Hormones and Behavior, 54, 748–757.PubMedCrossRefGoogle Scholar
  59. Tinbergen, N. (1963). On aims and methods of ethology. Zeitschrift für Tierpsychology, 20, 410–433.CrossRefGoogle Scholar
  60. Trainor, B. C., & Marler, C. A. (2002). Testosterone promotes paternal behavior in a monogamous mammal via conversion to oestrogen. Proceedings of the Royal Society of London, Series B, 269, 823–829.CrossRefGoogle Scholar
  61. Woodroffe, R., & Vincent, A. (1994). Mother’s little helpers: patterns of male care in mammals. Trends in Ecology and Evolution, 9, 294–297.PubMedCrossRefGoogle Scholar
  62. Wright, H. W. Y. (2006). Paternal den attendance is the best predictor of offspring survival in the socially monogamous bat–eared fox. Animal Behavior, 71, 503–510.CrossRefGoogle Scholar
  63. Wynne–Edwards, K. (1995). Biparental care in Djungarian but not Siberian dwarf hamsters (Phodopus). Animal Behavior, 50, 1571–1585.CrossRefGoogle Scholar
  64. Wynne–Edwards, K. E., & Lisk, R. D. (1989). Differential effects of paternal presence on pup survival in two species of dwarf hamster (Phodopus sungorus and Phodopus campbelli). Physiology and Behavior, 45, 465–469.PubMedCrossRefGoogle Scholar
  65. Wynne–Edwards, K. E., & Timonin, M. E. (2007). Parental care in rodents: weakening support for hormonal regulation of transition to behavioral fatherhood in rodent animal models of biparental care. Hormones and Behavior, 52, 114–121.PubMedCrossRefGoogle Scholar
  66. Yamamoto, Y., Carter, C. S., & Cushing, B. S. (2006). Neonatal manipulation of oxytocin affects expression of estrogen receptor alpha. Neuroscience, 137, 157–164.PubMedCrossRefGoogle Scholar
  67. Young, K. A., Liu, Y., & Wang Z. (2008). The neurobiology of social attachment: A comparative approach to behavioral, neuroanatomical, and neurochemical studies. Comparative Biochemistry and Physiology C, 148, 401–410.Google Scholar

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© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of PsychologyMemorial University of NewfoundlandSt. John’sCanada

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