Abstract
In mammals, the social behaviour of males and females reflects their different lifetime reproductive strategies. Reproductive success in males is determined by the outcome of competition with other males, the dominant males mating with as many females as possible. Hence, males rarely form strong social relationships and male coalitions are typically hierarchical, with emphasis upon aggressive rather than affiliative behaviour. Females have a different strategy. They invest in the production of relatively few offspring, with reproductive success being determined by the quality of care and the ability to enable infant survival beyond the weaning age. Females, therefore, form strong social bonds with their infants and their female-female relationships are affiliative, especially among matrilineal kin who often assist with infant care. In a minority of mammalian populations (less than 5%), a promiscuous male strategy is not an option, owing to the low population density of females. In this situation, males and females form a partner preference (bond), defending their partners against intruders and both parents participating in infant care (Kleiman 1997). The questions addressed in this chapter concern the hormonalmechanisms that underpin these female-bonded social relationships and how the evolutionary development of the neocortex in largebrained primates has impacted on the role of “bonding” as being an integral adjunct of physiological homeostasis.
Access provided by Autonomous University of Puebla. Download to read the full chapter text
Chapter PDF
Similar content being viewed by others
Keywords
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.
References
Amico J, Mantella R, Vollmer R, Li X (2004) Anxiety and stress responses in female oxytocin deficient mice. J Neuroendocrinol 16:319–324
Barton R (1998) Visual specialization and brain evolution in primates. Proc Biol Sci 265:1933–1937
Bergman T, Beehner J, Cheney D, Seyfarth R (2003) Hierarchical classification by rank and kinship in baboons. Science 302:1234–1236
Brennan P (2001) The vomeronasal system. Cell Mol Life Sci 58:546–555
Brennan P, Keverne EB (2004) Something in the air? New insights into mammalian pheromones. Curr Biol 14:R81–R89
Broad KD, Levy F, Evans F, Kimura T, Keverne EB, Kendrick KM (1999) Previous maternal experience potentiates the effects of parturition on oxytocin receptor mRNA expression in the paraventricular nucleus. Eur J Neurosci 11:3725–3737
Broad KD, Curley JP, Keverne EB (2006) Mother-infant bonding and the evolution of mammalian social relationships. Phil Trans Roy Soc B 361:2199–2214
Choleris E, Gustafsson J, Korach K, Muglia L, Pfaff D, Ogawa S (2003) An estrogen-dependent four-gene micronet regulating social recognition: a study with oxytocin and estrogen receptor-α and -β knockout mice. Proc Natl Acad Sci USA 100:6192–6197
Del Punta K, Leinders-Zufall T, Rodriquez I, Jukam D, Wysocki, CJ, Ogawa S, Zufall F, Mombaerts P (2002) Deficient pheromone responses in mice lacking a cluster of vomeronasal receptor genes. Nature 419:70–74
Dluzen D, Muraoka S, Engelmann N, Ebner K, Langraf R (2000) Oxytocin induces preservation of social recognition in male rats by activating α-adrenoceptors of the olfactory bulb. Eur J Neuroci 12:760–766
Dulac C, Axel R (1995) A novel family of genes encoding putative pheromone receptors in mammals. Cell 83:195–206
Dunbar RIM (1992) Neocortex size as a constraint on group six in primates. J Human Evol 20:469–493
Dunbar RIM (1998) Primate social systems. Chapman and Hall, London
Ferguson JN, Young, LJ, Hearn EF, Matzuk MM, Insel TR, Winslow JT (2000) Social amnesia in mice lacking the oxytocin gene. Nat Genet 25:284–288
Ferguson J, Aldag J, Insel T, Young L (2001) Oxytocin in the medial amygdala is essential for social recognition in the mouse. J Neuroci 21:8278–8285
Ghazanfar A, Santos L (2004) Primate brains in the wild: the sensory bases for social interactions. Nat Rev Neurosci 5:603–616
Gilad Y, Man P, Paabo S, Lancet D (2003) Human specific loss of olfactory receptor genes. Proc Natl Acad Sci USA 100:3324–3327
Gilad Y, Wiebe V, Przeworski M, Lancet D, Paabo S (2004) Loss of olfactory receptor genes coincides with the acquisition of full trichromaic vision in primates. PLoS Biol 2:E5
Herrada V, Dulac C (1997) A novel family of putative pheromone receptors in mammals with a topographically organized sexually dimorphic distribution. Cell 90:763–773
Hinde RA, Leighton-Shapiro ME, McGinnis L (1978) Effects of various types of separation experience on rhesus monkeys 5 months later. J Child Psychol Psychiat 19:199–211
Kalin NH, Sheldon SE, Lynn DE (1995) Opiate systems in mother and infant primates coordinate intimate contact during reunion. Psychoneuroendocrinology 7:735–742
Keverne EB (1992) Primate social relationships: Their determinants and consequences. In: Slater PJB, Rosenblatt JS, Beer C, Milinski M (eds) Advances in the study of behaviour. Academic Press, San Diego, pp 1–37
Keverne EB (1999) The vomeronasal organ. Science 286:716–720
Keverne EB (2002) Pheromones, vomeronasal function, and gender-specific behaviour. Cell 108:735–738
Keverne EB (2006) Trophoblast regulation of maternal endocrine function and behaviour. In: Moffett A, Loke C, McLaren A (eds) Biology and pathology of trophoblast. Cambridge University Press, Cambridge, pp 368–411
Keverne EB, Kendrick KM (1992) Oxytocin facilitation of maternal behavior. Ann NY Acad Sci 652:83–101
Keverne EB, Martenz ND, Tuite B (1989) β-endorphin levels in the cerebrospinal fluid of monkeys influenced by grooming relationships. Psychoneuroendocrinology 14:155–161
Kimchi T, Xu J, Dulac C (2007) A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 448:1009–1014
Kippin T, Cain S, Pfaus J (2003) Estrous odors and sexually conditioned neutral odors activate separate neural pathways in the male rat. Neuroscience 117:971–979
Kleiman D (1977) Monogamy in mammals. Q Rev Biol 52:39–69
Kraemer GW, Ebert MH, Schmidt DE, McKinnery WT (1991) Strangers in a strange land: a psychobiological study of infant monkeys before and after separation from real or inanimater mothers. Child Dev 62:548–566
Kudo H, Dunbar R (2001) Neocortex size and social network size in primates. Anim Behav 62:711–722
Liberles SD, Buck LB (2006) A second class of chemosensory receptors in the olfactory epithelium. Nature 442:645–650
Lim MM, Young LJ (2004) Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole. Neuroscience 125:35–45
Lim M, Murphy A, Young L (2004a) Ventral striatopallidal oxytocin and vasopressin V1a receptors in the monogamous prairie vole (Microtus ochragaster). J Comp Neurol 468:555–570
Lim MM, Wang Z, Olazabal DE, Ren X, Terwilliger EF, Young LJ (2004b) Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429:754–757
Liman ER, Innan H (2003) Relaxed selective pressure on an essential component of pheromone transduction in primate evolution. Proc Natl Acad Sci USA 100:3328–3332
Liu Y, Wang Z (2003) Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. Neuroscience 121:537–544
Lyons DM, Schatzberg AF (2003) Early maternal availability and prefrontal correlates of reward-related memory. Neurobiol Learn Mem 80:97–104
Martel FL, Nevison CM, Rayment FD, Simpson MJ, Keverne EB (1993) Opioid receptor blockade reduces maternal affect and social grooming in rhesus monkeys. Psychoneuroendocrinology 18:307–321
Martel FL, Nevison CM, Simpson MDA, Keverne EB (1995) Effects of opioid receptor blockade on the social behaviour of rhesus monkeys living in large family groups. Dev Psychobiol 28:71–84
Matsumoto K, Tanaka K (2004) The role of the medial prefrontal cortex in achieving goals. Curr Opin Neurobiol 14:178–185
Michael RP, Wilson MI (1973) Effects of castration and hormone replacement in fully adult male rhesus monkeys. Endocrinology (Baltimore) 95:150–159
Mitra S, Hoskin E, Yudkovitz J, Pear L, Wilkinson J, Hayuashi S, Pfaff D, Ogawa S, Rohrer S, Schaeffer J et al. (2003) Immunolocalization of estrogen receptor β in the mouse brain: comparison with estrogen receptor. Endocrinology 144:2055–2067
Osaka Y, Otrsuka T, Taniguchi M, Oka T, Kaba H (2001) Oxytocin enhances presynaptic and postsynaptic glutamergic transmission between rat olfactory bulb neurones in culture. Neurosci Lett 299:65–68
Panksepp J, Nelson E Bekkedal M (1997) Brain systems for the mediation of social separation-distress and social reward. Ann NY Acad Sci 807:78–100
Perrett D, Hietanen J, Oram N, Benson P (1992) Organization and functions of cells responsive to faces in the temporal cortex. Philos Trans R Soc Lond B Biol Sci 335:23–30
Pfaus J, Heeb M (1997) Implications of immediate-early gene induction in the brain following sexual stimulation of female and male rodents. Brain Res Bull 44:397–407
Ranote S, Elliott R, Abel, KM, Mitchell R, Deakin JF, Appleby L (2004) The neural basis of maternal responsiveness to infants: an fMRI study. NeuroReport 15:1825–1829
Ridderinkhof KR, van den Wildenbert WP, Segalowitz SJ, Carter CS (2004) Neurocognitive mechanisms of cognitive control: the role of prefrontal cortex in action selection, response inhibition, performance monitoring, and reward-based learning. Brain Cogn 56:129–140
Rogers RD, Ramnani N, Mackay C, Wilson, JL, Jezzard, P, Carter CS, Smith SM (2004) Distinct portions of anterior cingulated cortex and medial prefrontal cortex are activated by reward processing separable phases of decision-making cognition. Biol Psychiat 55:594–602
Silk J, Alberts S, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234
Simpson MJA, Gore MA, Janus M, Rayment FD (1989) Prior experience of risk and individual differences in enterprise shown by rhesus monkey infants in the second half of their first year. Primates 30:493–509
Stephan H, Baron G, Frahm HD (1982) Comparison of brain structure volumes in insectivores and primates. II. Accessory olfactory bulb (AOB). J Hirnforsch 23:575–591
Stowers L, Holy TE, Markus M, Dulac C, Koentges G (2002) Electrophysiological characterization of chemosensory neurons from the mouse vomeronasal organ. J Neurosci 16:4625–4637
Suomi SJ, Harlow HF (1975) Effects of differential removal from group on social development of rhesus monkeys. J Child Psychol Psychiat 16:149–164
Surridge A, Mundy N (2002) Trans-specific evolution of opsin alleles and the maintenance of trichromatic colour vision in Callitrichine primates. Mol Ecol 11:2157–2169
Surridge A, Osorio D, Mundy NI (2003) Evolution and selection of trichromatic vision in primates. Trends Ecol Evol 18:198–205
Van Essen D, Anderson C, Felleman D (1992) Information processing in the primate visual system: an integrated systems perspective. Science 255:419–423
Webb D, Cortes-Ortiz L, Zhang J (2004) Genetic evidence for the coexistence of pheromone perception and full trichromatic vision in howler monkey. Mol Biol Evol 21:697–704
Whinnett A, Mundy N (2003) Isolation of novel olfactory receptor genes in marmosets (Callithrix): Insights into pseudogene formation and evidence of functional degeneracy in non-human primates. Gene 304:87–96
Williams J, Catania K, Carter C (1992) Development of partner preferences in female prairie voles (Microtus ochrogaster): the role of social and sexual experience. Horm Behav 117:339–349
Williams J, Insel T, Harbaugh C, Carter C (1994) Oxytocin centrally administered facilitates formation of a partner preference in female prairie voles (Microtus ochragaster). J Neuroendocrinol 6:247–250
Winslow J, Hearn E, Ferguson J, Young L, Matzuk M, Insel T (2000) Infant vocalization, adult aggression, and fear behaviour of an oxytocin null mutant mouse. Horm Behav 37:145–155
Winslow JT, Noble PL, Lyons CK, Sterk SM, Insel TR (2003) Rearing effects of cerebrospinal fluid oxytocin concentration and social buffering in rhesus monkeys. Neuropsychopharmacology 28:910–918
Wrangham R (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300
Young L, Wang Z, Donaldson R, Rissman E (1998) Estrogen receptor α is essential for induction of oxytocin receptor by estrogen. NeuroReport 9:933–936
Zhang X, Firestein S (2002) The olfactory receptor gene superfamily of the mouse. Nat Neurosci 5:124–133
Zhang J, Webb D (2003) Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates. Proc Natl Acad Sci USA 100:8337–8341
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2008 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Keverne, E. (2008). Impact of Brain Evolution on Hormones and Social Behaviour. In: Pfaff, D., Kordon, C., Chanson, P., Christen, Y. (eds) Hormones and Social Behaviour. Research and Perspectives in Endocrine Interactions. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-79288-8_6
Download citation
DOI: https://doi.org/10.1007/978-3-540-79288-8_6
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-540-79286-4
Online ISBN: 978-3-540-79288-8
eBook Packages: MedicineMedicine (R0)