Inadvertent social information and the avoidance of parasitized male mice: A role for oxytocin
Abstract
Social information can be acquired either directly or indirectly from cues inadvertently produced by individuals with similar interests and requirements ("inadvertent social information," ISI). These inadvertent cues provide "public information" that other individuals can use to guide their behavior. We show here that female mice use olfactory ISI to determine their choice of, and responses to, males and that the use of this ISI involves the gene for oxytocin (OT). Female mice (OT wild type and CF-1 strain) displayed a significant interest in, and choice of, the odors of uninfected males of varying sexual status that were associated with the odors of an another estrous female. This recognition of, and choices for, specific, individual male odors was evident 24 h later. Female mice also distinguished between males subclinically infected with the gastrointestinal nematode parasite, Heligimosomoides polygyrus, and nonparasitized males, displaying aversive responses (analgesia, increased corticosterone) to, and avoidance of, the odors of infected males. The presence of the odors of another estrous female with that of the infected male, which are indicative of potential mate interests, attenuated these aversive responses and resulted in a choice for the odors of infected male. OT gene-deficient (knockout) females were impaired in their use of this ISI to modulate their responses to either uninfected males of differing sexual states or infected males. These findings suggest that OT genes are necessary for the processing of inadvertent social information and likely the integration of both direct and indirect social information.
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Olfactory cues carry information about sex, strain, social rank, health, and sexual receptivity.
“Olfactory cues carry information about sex, strain, social rank, health, and sexual receptivity [86,87].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [87]
Oxytocin plays an important role in processing olfactory signals involved in assessing partner quality and social recognition.
“OT plays an important role in processing olfactory signals involved in assessing partner quality and social recognition [87].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [87]
Female mice display a preference for odors from healthy males over those with an infection, but this preference is diminished in female mice lacking oxytocin receptors.
“For example, female mice display a preference for odors from healthy males over those with an infection; however, this preference is diminished in female mice lacking OXTRs.”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [87]
Cites
(1990) · Choice Reviews Online · doi:10.5860/choice.27-3338 · Cited by 35,305 · see citing works
Heritable True Fitness and Bright Birds: A Role for Parasites?
Hamilton, W. D., & Zuk, M. (1982) · Science · doi:10.1126/science.7123238 · Cited by 3,733 · see citing works
Oxytocin increases trust in humans
Kosfeld, M., Heinrichs, M., Zak, P. J., Fischbacher, U., & Fehr, E. (2005) · Nature · doi:10.1038/nature03701 · Cited by 3,690 · see citing works
Public Information: From Nosy Neighbors to Cultural Evolution
Danchin, É., Giraldeau, L., Valone, T. J., & Wagner, R. H. (2004) · Science · doi:10.1126/science.1098254 · Cited by 1,513 · 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
Social amnesia in mice lacking the oxytocin gene
Ferguson, J. N., Young, L. J., Hearn, E. F., Matzuk, M. M., Insel, T. R., & Winslow, J. T. (2000) · Nature Genetics · doi:10.1038/77040 · Cited by 1,130 · see citing works
Oxytocin in the Medial Amygdala is Essential for Social Recognition in the Mouse
Ferguson, J. N., Aldag, J. M., Insel, T. R., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-20-08278.2001 · Cited by 1,043 · see citing works
Female sticklebacks use male coloration in mate choice and hence avoid parasitized males
Milinski, M., & Bakker, T. C. M. (1990) · Nature · doi:10.1038/344330a0 · Cited by 861 · see citing works
Social Organization and Parasite Risk in Mammals: Integrating Theory and Empirical Studies
Altizer, S., Nunn, C. L., Thrall, P. H., Gittleman, J. L., Antonovics, J., Cunningham, A. A., Dobson, A. P., Ezenwa, V. O., Jones, K. E., Pedersen, A. B., et al. (2003) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev.ecolsys.34.030102.151725 · Cited by 771 · see citing works
Control of mating preferences in mice by genes in the major histocompatibility complex.
Yamazaki, K., Boyse, E. A., Miké, V., Thaler, H. T., Mathieson, B. J., Abbott, J., Boyse, J., Zayas, Z. A., & Thomas, L. (1976) · The Journal of Experimental Medicine · doi:10.1084/jem.144.5.1324 · Cited by 687 · see citing works
Molecular detection of pheromone signals in mammals: from genes to behaviour
Dulac, C. G., & Torello, A. T. (2003) · Nature reviews. Neuroscience · doi:10.1038/nrn1140 · Cited by 662 · see citing works
Individual recognition in mice mediated by major urinary proteins
Hurst, J. L., Payne, C. E., Nevison, C. M., Marie, A. D., Humphries, R. E., Robertson, D. H. L., Cavaggioni, A., & Beynon, R. J. (2001) · Nature · doi:10.1038/414631a · Cited by 605 · see citing works
HOW THE BRAIN PROCESSES SOCIAL INFORMATION: Searching for the Social Brain
Insel, T. R., & Fernald, R. D. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144148 · Cited by 556 · see citing works
The neuroendocrine basis of social recognition
Ferguson, J. N., Young, L. J., & Insel, T. R. (2002) · Frontiers in Neuroendocrinology · doi:10.1006/frne.2002.0229 · Cited by 494 · see citing works
Measuring female mating preferences
Wagner, W. E. (1998) · Animal Behaviour · doi:10.1006/anbe.1997.0635 · Cited by 448 · see citing works
Public information for the assessment of quality: a widespread social phenomenon
Valone, T. J., & Templeton, J. J. (2002) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1064 · Cited by 419 · see citing works
Scent-marking by male mammals: Cheat-proof signals to competitors and mates
Gosling, L. M., & Roberts, S. C. (2001) · Advances in the Study of Behavior · doi:10.1016/s0065-3454(01)80007-3 · Cited by 411 · see citing works
Chemical signals and parasite-mediated sexual selection
Penn, D. J. (1998) · Trends in Ecology & Evolution · doi:10.1016/s0169-5347(98)01473-6 · Cited by 401 · see citing works
Choleris, E., Gustafsson, J.-Å., Korach, K. S., Muglia, L. J., Pfaff, D. W., & Ogawa, S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0631699100 · Cited by 386 · see citing works
Self-citationIndividual Odors among Mammals: Origins and Functions
Halpin, Z. T. (1986) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60187-4 · Cited by 330 · see citing works
Reversal of female mate choice by copying in the guppy (Poecilia reticulata)
Dugatkin, L. A., & Godin, J. J. (1992) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1992.0101 · Cited by 294 · see citing works
Drickamer, L. C., Gowaty, P. A., & Holmes, C. M. (2000) · Animal Behaviour · doi:10.1006/anbe.1999.1316 · Cited by 273 · see citing works
Dynamic Actin Patterns and Arp2/3 Assembly at the Substrate-Attached Surface of Motile Cells
Bretschneider, T., Diez, S., Anderson, K. I., Heuser, J., Clarke, M., Müller‐Taubenberger, A., Köhler, J., & Gerisch, G. (2004) · Current Biology · doi:10.1016/j.cub.2003.12.005 · Cited by 267 · see citing works
Independent Versus Nonindependent Mate Choice: Do Females Copy Each Other?
Pruett‐Jones, S. (1992) · The American Naturalist · doi:10.1086/285452 · Cited by 266 · see citing works
Volatile signals of the major histocompatibility complex in male mouse urine
Singer, A. G., Beauchamp, G. K., & Yamazaki, K. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.6.2210 · Cited by 248 · see citing works
Opposing actions of prostaglandins and oxytocin determine the onset of murine labor
Gross, G. A., Imamura, T., Luedke, C., Vogt, S. K., Olson, L. M., Nelson, D. M., Sadovsky, Y., & Muglia, L. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.11875 · Cited by 238 · see citing works
Self-citationGibson, R. M., & Höglund, . (1992) · Trends in Ecology & Evolution · doi:10.1016/0169-5347(92)90050-l · Cited by 236 · see citing works
Scent-marking displays provide honest signals of health and infection
Zala, S. M. (2004) · Behavioral Ecology · doi:10.1093/beheco/arh022 · Cited by 209 · see citing works
The major histocompatibility complex and female mating preferences in mice
Egid, K., & Brown, J. L. (1989) · Animal Behaviour · doi:10.1016/s0003-3472(89)80051-x · Cited by 206 · see citing works
Parasites and the Evolution of Host Social Behavior
Møller, A., Dufva, R., & Allander, K. (1993) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60405-2 · Cited by 189 · see citing works
Signaling Health versus Parasites
Getty, T. (2002) · The American Naturalist · doi:10.1086/338992 · Cited by 182 · see citing works
Mate-choice copying in Japanese quail,Coturnix coturnix japonica
GALEF, B. G., & WHITE, D. J. (1998) · Animal Behaviour · doi:10.1006/anbe.1997.0616 · Cited by 175 · see citing works
Alternative mechanisms of nonindependent mate choice
Westneat, D. F., Walters, A., McCarthy, T. M., et al. (2000) · Animal Behaviour · doi:10.1006/anbe.1999.1341 · Cited by 174 · see citing works
Multiple roles of major urinary proteins in the house mouse, Mus domesticus
Beynon, R. J., & Hurst, J. L. (2003) · Biochemical Society Transactions · doi:10.1042/bst0310142 · Cited by 173 · see citing works
Detailed information about parasites revealed by sexual ornamentation
Wedekind, C. (1992) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1992.0024 · Cited by 170 · see citing works
Dugatkin, L. A. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.7.2770 · Cited by 161 · see citing works
Potts, W. K., Manning, C. J., & Wakeland, E. K. (1994) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1994.0154 · Cited by 142 · see citing works
Odours of parasitized males induce aversive responses in female mice
Kavaliers, M., & Colwell, D. D. (1995) · Animal Behaviour · doi:10.1016/0003-3472(95)80032-8 · Cited by 131 · see citing works
Self-citationRecognition of Familiar Individuals in Golden Hamsters: A New Method and Functional Neuroanatomy
Lai, W., Ramiro, L.-L. R., Yu, H. A., & Johnston, R. E. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2124-05.2005 · Cited by 104 · see citing works
Influenza Infection Neutralizes the Attractiveness of Male Odour to Female Mice (Mus musculus)
Penn, D. J., Schneider, G., White, K., Slev, P. R., & Potts, W. K. (1998) · Ethology · doi:10.1111/j.1439-0310.1998.tb00102.x · Cited by 95 · see citing works
Hurst, J. L. (1990) · Animal Behaviour · doi:10.1016/s0003-3472(05)80917-0 · Cited by 95 · see citing works
Swaddle, J. P., Cathey, M. G., Correll, M. D., et al. (2005) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2005.3054 · Cited by 94 · see citing works
Male body length influences mate-choice copying in the sailfin molly Poecilia latipinna
Witte, K., & Ryan, M. J. (1998) · Behavioral Ecology · doi:10.1093/beheco/9.5.534 · Cited by 92 · see citing works
Kavaliers, M., Choleris, E., & Colwell, D. D. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1714 · Cited by 89 · see citing works
Self-citationKavaliers, M., Colwell, D. D., Braun, W. J., & Choleris, E. (2003) · Animal Behaviour · doi:10.1006/anbe.2002.2043 · Cited by 82 · see citing works
Self-citationPedersen, C. A., & Boccia, M. L. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2001.1736 · Cited by 81 · see citing works
Ehman, K. D., & Scott, M. E. (2001) · Animal Behaviour · doi:10.1006/anbe.2001.1805 · Cited by 79 · see citing works
Impaired discrimination of and aversion to parasitized male odors by female oxytocin knockout mice
Kavaliers, M., Colwell, D. D., Choleris, E., Ågmo, A., Muglia, L. J., Ogawa, S., & Pfaff, D. W. (2003) · Genes, Brain and Behavior · doi:10.1034/j.1601-183x.2003.00021.x · Cited by 78 · see citing works
Self-citationFunctional Genomics of Social Recognition
Choleris, E., Kavaliers, M., & Pfaff, D. W. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.0953-8194.2004.01178.x · Cited by 75 · see citing works
Self-citationChemosensation and genetic individuality
Singh, P. B. (2001) · Reproduction · doi:10.1530/rep.0.1210529 · Cited by 68 · see citing works
Mate Choice for Non‐siblings in Wild House Mice: Evidence from a Choice Test and a Reproductive Test
Krackow, S., & Matuschak, B. (1991) · Ethology · doi:10.1111/j.1439-0310.1991.tb00266.x · Cited by 63 · see citing works
Experimental tests of copying and mate choice in fallow deer (Dama dama)
Clutton-Brock, T. H., & McComb, K. (1993) · Behavioral Ecology · doi:10.1093/beheco/4.3.191 · Cited by 61 · see citing works
MARUNIAK, J. A., Owen, K., Bronson, F. H., & Desjardins, C. (1975) · Behavioral Biology · doi:10.1016/s0091-6773(75)91920-3 · Cited by 47 · see citing works
Palanza, P., Parmigiani, S., & Saal, F. S. V. (1994) · Animal Behaviour · doi:10.1006/anbe.1994.1235 · Cited by 35 · see citing works
Barnard, C. J., Behnke, J. M., Gage, A. R., Brown, H. J., & Smithurst, P. R. (1998) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1998.0544 · Cited by 30 · see citing works
Kavaliers, M., Choleris, E., Ågmo, A., Muglia, L. J., Ogawa, S., & Pfaff, D. W. (2005) · Animal Behaviour · doi:10.1016/j.anbehav.2004.12.016 · Cited by 28 · see citing works
Self-citation(1995) · Drug Development Research · doi:10.1002/ddr.430350407 · Cited by 1 · see citing works
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“OT plays an important role in processing olfactory signals involved in assessing partner quality and social recognition [87].”
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- Authors
- Kavaliers, M., Choleris, E., Ågmo, A., Braun, W. J., Colwell, D. D., Muglia, L. J., Ogawa, S., & Pfaff, D. W.
- Affiliations
- Western University (CA)
- University of Guelph (CA)
- UiT The Arctic University of Norway (NO)
- Agriculture and Agri-Food Canada (CA)
- Washington University in St. Louis (US)
- Rockefeller University (US)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2006-03-08
- Volume
- 103
- Issue
- 11
- Pages
- 4293-4298
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- OpenAlex
- W2043569070
- Cited by
- 87
- References
- 57
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1 · 2023: 6 · 2022: 5 · 2021: 6 · 2020: 3 · 2019: 5 · 2018: 8 · 2017: 2 · 2016: 2 · 2015: 4 · 2014: 3 · 2013: 4 · 2012: 7
- FWCI
- 5.61
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH 38273, R01MH038273, MH-62147, R01MH062147)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- oxytocin, mate choice, parasite avoidance, Heligmosomoides polygyrus, gastrointestinal nematode infection, female mice, social information processing, corticosterone, analgesia
- MeSH terms
- Animals, Avoidance Learning, Corticosterone, Female, Male, Nematospiroides dubius, Nociceptors, Odorants, Oxytocin, Sexual Behavior, Animal, Smell, Social Behavior, Strongylida Infections, Mice, Knockout, Mice
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