Mating in the monogamous male: Behavioral consequences
Abstract
In monogamous mammals, males typically show selective affiliation with a single mate, high levels of paternal care, and aggression towards conspecifics to protect male and offspring. We have previously described how selective aggression and affiliation increase after mating in the male prairie vole, Microtus ochrogaster. The current studies further explored the behavioral changes that follow mating in the male of this species. The first set of experiments tested males on several behavioral measures after 24 h of either mating, social (but not sexual) exposure, or no social contact. After 24 h of mating, but not after the other two conditions, aggression and affiliation (partner preference) increased as previously reported. In addition, mated animals showed increased exploration of the open arms of a plus maze, consistent with decreased fearfulness. There were no group differences in paternal behavior (which was high in all three conditions) or analgesia (assessed by tail flick latency). To determine the minimum amount of mating necessary for the induction of aggression, males were tested in a resident-intruder paradigm after 1,6, or 24 h of mating. Although 1 h of mating was associated with a transient increase in the frequency of threats and attacks, the full spectrum of enduring aggression was observed only in the males given 24 h of mating. In a final experiment, the behavioral consequences of mating were studied in males of the closely related montane vole (Microtus montanus) which does not pair bond. Males of this nonmonogamous vole species did not show increased aggression, partner preference, or alterations in plus maze exploration following 24 h of mating. These results demonstrate the importance of prolonged mating for the induction of pair bonding in the monogamous male and they suggest that increases in aggression and affiliation are associated with decreased fearfulness in pair bonded males.
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When male prairie voles have cohabitated with females for two weeks, they develop intense selective aggression toward male and female strangers and not toward their female partners.
“However, when males have cohabitated with females for two weeks, they develop intense selective aggression toward male and female strangers and not toward their female partners (Insel et al 1995; Wang et al 1997b).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Insel et al 1995
Sexually naïve male prairie voles are highly social and show very little aggressive behavior toward novel conspecifics.
“Sexually naïve male prairie voles are highly social and show very little aggressive behavior toward novel conspecifics (Insel et al 1995).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Insel et al 1995
Pair bonding in prairie voles is operationally defined by two observable behaviors: partner preference and selective aggression.
“Pair bonding in prairie voles is operationally defined based on two observable behaviors: preference for the partner over the stranger in a choice test (or “partner preference”); and intense aggression toward prairie voles other than the mate (or “selective aggression”) (Williams et al 1992; Winslow et al 1993; Insel et al 1995; Wang et al 1997b; Ahern et al 2009).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Insel et al 1995
Following successful pair bond formation, male prairie voles (and sometimes females) will actively attack strangers including sexually receptive females.
“following successful pair bond formation, male prairie voles (and sometimes females) will actively attack strangers including sexually receptive females (Aragona et al., 2006, Gobrogge et al., 2007, Insel et al., 1995, Wang et al., 1997, Winslow et al., 1993).”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Insel et al., 1995
Prior to pair bonding, male prairie voles show little aggression toward strangers.
“Prior to pair bonding, male prairie voles show little aggression toward strangers”
From Oxytocin, motivation and the role of dopamine (2014) · cites this paper as Insel et al., 1995
Cites
Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat
Pellow, S., Chopin, P., File, S. E., & Briley, M. (1985) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(85)90031-7 · Cited by 5,822 · see citing works
A METHOD FOR DETERMINING LOSS OF PAIN SENSATION
D'AMOUR, F. E., & Smith, D. L. (1941) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)03823-6 · Cited by 3,238 · see citing works
The use of a plus-maze to measure anxiety in the mouse
Lister, R. G. (1987) · Psychopharmacology · doi:10.1007/bf00177912 · Cited by 2,617 · see citing works
Pellow, S., & File, S. E. (1986) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(86)90552-6 · Cited by 1,534 · see citing works
Kleiman, D. G. (1977) · The Quarterly Review of Biology · doi:10.1086/409721 · Cited by 1,436 · see citing works
Review Lecture: Mammalian mating systems
Clutton-Brock, T. H. (1989) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1989.0027 · Cited by 1,413 · see citing works
A role for central vasopressin in pair bonding in monogamous prairie voles
Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R. (1993) · Nature · doi:10.1038/365545a0 · Cited by 948 · see citing works
Self-citationFile, S. E. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90012-6 · Cited by 820 · see citing works
Keverne, E. B., Martensz, N. D., & Tuite, B. (1989) · Psychoneuroendocrinology · doi:10.1016/0306-4530(89)90065-6 · Cited by 525 · see citing works
WILLIAMS, J. (1992) · Hormones and Behavior · doi:10.1016/0018-506x(92)90004-f · Cited by 471 · see citing works
Getz, L. L., Carter, C. S., & Gavish, L. (1981) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00299829 · Cited by 466 · see citing works
Opioid-Like Analgesia in Defeated Mice
Miczek, K. A., Thompson, M. L., & Shuster, L. (1982) · Science · doi:10.1126/science.7199758 · Cited by 418 · see citing works
Carter, C. S., & Getz, L. L. (1993) · Scientific American · doi:10.1038/scientificamerican0693-100 · Cited by 310 · see citing works
Influence of social isolation, gender, strain, and prior novelty on plus-maze behaviour in mice
Rodgers, R. J., & Cole, J. C. (1993) · Physiology & Behavior · doi:10.1016/0031-9384(93)90084-s · Cited by 294 · see citing works
Social organization in free-living prairie voles, Microtus ochrogaster
Getz, L. L., & Hofmann, J. E. (1986) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00300004 · Cited by 239 · see citing works
Time-contingent change in infanticide and parental behavior induced by ejaculation in male mice
Saal, F. S. V. (1985) · Physiology & Behavior · doi:10.1016/0031-9384(85)90069-1 · Cited by 209 · see citing works
Oliveras, D. M., & Novak, M. A. (1986) · Animal Behaviour · doi:10.1016/s0003-3472(86)80120-8 · Cited by 196 · see citing works
Assessing pain threshold in the rat: Changes with estrus and time of day
Martı́nez–Gómez, M., Cruz, Y., Salas, M., Hudson, R., & Pacheco, P. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90040-x · Cited by 185 · see citing works
Bamshad, M., Novak, M. A., & de Vries, G. J. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90238-0 · Cited by 162 · see citing works
Aggressive behavioral characteristics, hormones, and sexual orientation in men and women
Gladue, B. A. (1991) · Aggressive Behavior · doi:10.1002/1098-2337(1991)17:6 · Cited by 157 · see citing works
Shapiro, L. E., & Insel, T. R. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230502 · Cited by 128 · see citing works
Self-citationRelationships between Social Organization and Behavioral Endocrinology in a Monogamous Mammal
Carter, C. S., Getz, L. L., & Cohen-Parsons, M. (1986) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60189-8 · Cited by 125 · see citing works
Shapiro, L. E., & Dewsbury, D. A. (1990) · Journal of comparative psychology · doi:10.1037/0735-7036.104.3.268 · Cited by 95 · see citing works
Gubernick, D. J., Schneider, K. A., & Jeannotte, L. A. (1994) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00167748 · Cited by 86 · see citing works
Shapiro, L. E., Austin, D., Ward, S. E., et al. (1986) · Animal Behaviour · doi:10.1016/0003-3472(86)90010-2 · Cited by 78 · see citing works
Does copulation inhibit infanticide in male rodents?
Elwood, R. W., & Ostermeyer, M. C. (1984) · Animal Behaviour · doi:10.1016/s0003-3472(84)80350-4 · Cited by 64 · see citing works
Effects of septal lesions on food and water intake and operant responding for food
Lorens, S. A., & Kondo, C. Y. (1969) · Physiology & Behavior · doi:10.1016/0031-9384(69)90107-3 · Cited by 60 · see citing works
Albert, D. J., Dyson, E. M., Walsh, M. L., & Petrovic, D. M. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90054-6 · Cited by 53 · see citing works
Experimental Psychopharmacology
Blackman, D. E. (1987) · Humana Press eBooks · doi:10.1007/978-1-59259-461-0_1 · Cited by 40 · see citing works
The biology of social bonding in a monogamous mammal
Witt, D., Williams, J. F., & Porges, C. C. (1989) · Cited by 30 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The neurobiology of pair bonding.
Young, L. J., & Wang, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1327 · Cited by 1,523 · see citing works
Neuroendocrine perspectives on social attachment and love
Sue Carter, C. (1998) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00055-9 · Cited by 1,425 · see citing works
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
Liu, Y., & Wang, Z. X. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00555-4 · Cited by 580 · see citing works
A neurobiological basis of social attachment.
(1997) · American Journal of Psychiatry · doi:10.1176/ajp.154.6.726 · Cited by 553 · see citing works
Cho, M. M., DeVries, A. C., Williams, J. R., & Carter, C. S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.1071 · Cited by 529 · see citing works
The neurobiology of pair bonding: Insights from a socially monogamous rodent
Young, K. A., Gobrogge, K. L., Liu, Y., & Wang, Z. (2011) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.07.006 · Cited by 389 · see citing works
Oxytocin, motivation and the role of dopamine
Love, T. M. (2014) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2013.06.011 · Cited by 369 · see citing works
A critical role for nucleus accumbens dopamine in partner-preference formation in male prairie voles
Aragona, B. J., Liu, Y., Curtis, J. T., Stephan, F. K., & Wang, Z. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03483.2003 · Cited by 351 · see citing works
Vasopressin-dependent neural circuits underlying pair bond formation in the monogamous prairie vole
Lim, M. M., & Young, L. J. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.12.008 · Cited by 322 · see citing works
Burkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307 · see citing works
“Sexually naïve male prairie voles are highly social and show very little aggressive behavior toward novel conspecifics (Insel et al. 1995).”
Pitkow, L. J., Sharer, C. A., Ren, X., Insel, T. R., Terwilliger, E. F., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07392.2001 · Cited by 295 · see citing works
Self-citationNeuropeptides and the evolution of social behavior
Insel, T. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00146-x · Cited by 264 · see citing works
Bales, K. L., Perkeybile, A. M., Conley, O. G., Lee, M. H., Guoynes, C. D., Downing, G. M., Yun, C. R., Solomon, M., Jacob, S., & Mendoza, S. P. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.08.025 · Cited by 265 · see citing works
Liu, Y., Curtis, J. T., & Wang, Z. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.4.910 · Cited by 282 · see citing works
Smith, A. S., Ågmo, A., Birnie, A. K., & French, J. A. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.12.004 · Cited by 228 · see citing works
Smeltzer, M. D., Curtis, J. T., Aragona, B. J., & Wang, Z. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2005.10.019 · Cited by 222 · see citing works
Bosch, O. J., Nair, H. P., Ahern, T. H., Neumann, I. D., & Young, L. J. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.154 · Cited by 216 · see citing works
Bales, K. L., & Carter, C. S. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00154-5 · Cited by 195 · see citing works
Bales, K. L., van Westerhuyzen, J. A., Lewis-Reese, A. D., Grotte, N. D., Lanter, J. A., & Carter, C. S. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.05.004 · Cited by 192 · see citing works
Wang, Z., Yu, G., Cascio, C., Liu, Y., Gingrich, B., & Insel, T. R. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.3.602 · Cited by 205 · see citing works
Self-citationGobrogge, K. L., Liu, Y., Jia, X., & Wang, Z. (2007) · Journal of Comparative Neurology · doi:10.1002/cne.21364 · Cited by 178 · see citing works
Gobrogge, K. L., Liu, Y., Young, L. J., & Wang, Z. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908620106 · Cited by 178 · see citing works
Young, K. A., Liu, Y., & Wang, Z. (2008) · Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology · doi:10.1016/j.cbpc.2008.02.004 · Cited by 163 · see citing works
Genetics of aggressive behavior: An overview
Veroude, K., Zhang‐James, Y., Fernàndez‐Castillo, N., Bakker, M. J., Cormand, B., & Faraone, S. V. (2016) · American Journal of Medical Genetics Part B: Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32364 · Cited by 147 · see citing works
Beiderbeck, D. I., Neumann, I. D., & Veenema, A. H. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05974.x · Cited by 142 · see citing works
Sun, P., Smith, A. S., Lei, K., Liu, Y., & Wang, Z. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.02.016 · Cited by 141 · see citing works
Bales, K. L., Pfeifer, L. A., & Carter, C. S. (2004) · Developmental Psychobiology · doi:10.1002/dev.10165 · Cited by 107 · see citing works
Oxytocin and same-sex social behavior in female meadow voles
Beery, A. K., & Zucker, I. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.05.023 · Cited by 108 · see citing works
Are behavioral effects of early experience mediated by oxytocin?
Bales, K. L., Boone, E., Epperson, P., Hoffman, G., & Carter, C. S. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00024 · Cited by 99 · see citing works
Curtis, J. T., Liu, Y., Aragona, B. J., & Wang, Z. (2006) · Brain Research · doi:10.1016/j.brainres.2006.07.126 · Cited by 74 · see citing works
INSEL, T. R., YOUNG, L., & WANG, Z. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51928.x · Cited by 56 · see citing works
Self-citationA Neuroscientist’s Guide to the Vole
Kenkel, W. M., Gustison, M. L., & Beery, A. K. (2021) · Current Protocols · doi:10.1002/cpz1.175 · Cited by 52 · see citing works
Odor Communication and Mate Choice in Rodents
Ferkin, M. (2018) · Biology · doi:10.3390/biology7010013 · Cited by 55 · see citing works
Qiao, X., Yan, Y., Wu, R., Tai, F., Hao, P., Cao, Y., & Wang, J. (2014) · Journal of Comparative Physiology A · doi:10.1007/s00359-013-0870-2 · Cited by 40 · see citing works
Behavioral characteristics of pair bonding in the black tufted-ear marmoset (Callithrix penicillata)
Birnie, A. K., Smith, A. S., Ågmo, A., & French, J. A. (2012) · Behaviour · doi:10.1163/156853912x638454 · Cited by 31 · see citing works
Cushing, B. S., Okorie, U., & Young, L. J. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01097.x · Cited by 31 · see citing works
Young, K. A., Liu, Y., Gobrogge, K. L., Dietz, D. M., Wang, H., Kabbaj, M., & Wang, Z. (2011) · Brain Research · doi:10.1016/j.brainres.2010.09.109 · Cited by 27 · see citing works
Curtis, J. T., & Wang, Z. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.07.011 · Cited by 15 · see citing works
Stetzik, L. A., Sullivan, A. W., Patisaul, H. B., & Cushing, B. S. (2018) · BMC Research Notes · doi:10.1186/s13104-018-3934-0 · Cited by 10 · see citing works
- Authors
- Insel, T. R., Preston, S., & Winslow, J. T.
- Affiliations
- National Institute of Mental Health (US)
- Corresponding author
- Insel, Thomas R.
- ORCID
- Insel, Thomas R.
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 1995-04
- Volume
- 57
- Issue
- 4
- Pages
- 615-627
- ISSN
- 0031-9384 (ISSN-L)
- OpenAlex
- W2070780269
- Cited by
- 215
- References
- 30
- Citations by year
- 2026: 3 · 2025: 7 · 2024: 1 · 2023: 5 · 2022: 8 · 2021: 6 · 2020: 3 · 2019: 2 · 2018: 13 · 2017: 10 · 2016: 10 · 2015: 5 · 2014: 9 · 2013: 11 · 2012: 8
- FWCI
- 9.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Physiology & Behavior (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Evolutionary Psychology and Human Behavior
- Keywords
- monogamy, pair bonding, Microtus ochrogaster, montane vole, male aggression, mate preferences, social affiliation, paternal care, fearfulness, analgesia, resident-intruder paradigm, mating duration, social behavior
- MeSH terms
- Aggression, Analgesia, Animals, Anxiety, Arvicolinae, Exploratory Behavior, Female, Male, Paternal Behavior, Sexual Behavior, Animal, Social Behavior
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