Estrous phase alters social behavior in a polygynous but not a monogamous Peromyscus species
Abstract
The social organization of rodent species determines behavioral patterns for both affiliative and agonistic encounters. The neuropeptide oxytocin has been implicated in the mediation of social behavior; however, variability in both neuropeptide expression and social behavior within a single species indicates an additional mediating factor. The purpose of the present comparative study was to investigate social behaviors in naïve mixed-sex pairs of monogamous Peromyscus californicus and polygynous Peromyscus leucopus. We identified substantial inter- and intra-specific variability in the expression of affiliative and agonistic behaviors. Although all P. californicus tested engaged in frequent and prolonged intervals of social contact and rarely engaged in aggressive behaviors, P. leucopus exhibited significant variability in both measures of social behaviors. The naturally occurring differences in social behavior displayed by P. leucopus vary across the estrous cycle, and correspond to hypothalamic oxytocin, as well as circulating oxytocin and glucocorticoid concentrations. These results provide evidence for a rhythm in social behavior across the estrous cycle in polygynous, but not monogamous, Peromyscus species.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Experimental studies in nonhuman social species show that isolation has direct harmful physiological effects.
“experimental studies in nonhuman social species indicate that isolation has direct, deleterious physiological effects.”
From Social isolation (2011) · cites this paper as [13]
Social isolation increases infarct size and edema and lowers post-stroke survival in mice after experimentally induced stroke, due to elevated proinflammatory cytokines.
“increases infarct size and edema and decreases the post-stroke survival rate following experimentally induced stroke in mice due to elevated levels of proinflammatorycytokines;13”
From Social isolation (2011) · cites this paper as [13]
Cites
Oxytocin, vasopressin, and the neurogenetics of sociality
Donaldson, Z. R., & Young, L. J. (2008) · Science · doi:10.1126/science.1158668 · Cited by 1,645 · 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
Dendritic peptide release and peptide-dependent behaviours
Ludwig, M., & Leng, G. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1845 · Cited by 945 · see citing works
Pedersen, C. A., & Prange, A. J. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.12.6661 · Cited by 841 · see citing works
Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles
Insel, T. R., & Shapiro, L. E. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.13.5981 · Cited by 833 · see citing works
Goldman, J. M., Murr, A. S., & Cooper, R. L. (2007) · Birth Defects Research Part B Developmental and Reproductive Toxicology · doi:10.1002/bdrb.20106 · Cited by 804 · see citing works
Physiological substrates of mammalian monogamy: The prairie vole model
Sue Carter, C., Courtney Devries, A., & Getz, L. L. (1995) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(94)00070-h · Cited by 615 · 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
Self-citationCellular Mechanisms of Social Attachment
Young, L. J., Lim, M. M., Gingrich, B., & Insel, T. R. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1691 · Cited by 523 · see citing works
Francis, D. D., Young, L. J., Meaney, M. J., & Insel, T. R. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.0007-1331.2002.00776.x · Cited by 415 · see citing works
Motivational systems and the neural circuitry of maternal behavior in the rat
Numan, M. (2007) · Developmental Psychobiology · doi:10.1002/dev.20198 · Cited by 358 · see citing works
Grippo, A. J., Gerena, D., Huang, J., Kumar, N., Shah, M., Ughreja, R., & Sue Carter, C. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.07.004 · Cited by 336 · see citing works
Ross, H. E., Freeman, S. M., Spiegel, L. L., Ren, X., Terwilliger, E. F., & Young, L. J. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5039-08.2009 · Cited by 322 · see citing works
Oxytocin, vasopressin and pair bonding: implications for autism
Hammock, E. A. D., & Young, L. J. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1939 · Cited by 289 · see citing works
Neumann, I. D., Krömer, S. A., Toschi, N., & Ebner, K. (2000) · Regulatory Peptides · doi:10.1016/s0167-0115(00)00197-x · Cited by 285 · see citing works
Bester‐Meredith, J. K., Young, L. J., & Marler, C. A. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1522 · Cited by 285 · see citing works
The biparental care system of the California mouse, Peromyscus californicus.
Gubernick, D. J., & Alberts, J. R. (1987) · Journal of comparative psychology · doi:10.1037/0735-7036.101.2.169 · Cited by 274 · see citing works
Enhanced social interactions in rats following chronic, centrally infused oxytocin
Witt, D. M., Winslow, J. T., & Insel, T. R. (1992) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(92)90418-f · Cited by 244 · see citing works
Tol, H. H. M. V., Bolwerk, E., LlU, B., & Burbach, J. P. H. (1988) · Endocrinology · doi:10.1210/endo-122-3-945 · Cited by 226 · see citing works
Behavioral Effects of Progesterone Associated with Rapid Modulation of Oxytocin Receptors
Schumacher, M., Coirini, H., Pfaff, D. W., & McEwen, B. S. (1990) · Science · doi:10.1126/science.2173139 · Cited by 221 · see citing works
CUSHING, B., & KRAMER, K. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.04.001 · Cited by 209 · see citing works
Choleris, E., Ogawa, S., Kavaliers, M., Gustafsson, J.-Α., Korach, K. S., Muglia, L. J., & Pfaff, D. W. (2006) · Genes Brain & Behavior · doi:10.1111/j.1601-183x.2006.00203.x · Cited by 173 · see citing works
The neurobiology of social recognition, approach, and avoidance
Young, L. J. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01268-9 · Cited by 172 · see citing works
Oxytocin Control of Maternal Behavior Regulation by Sex Steroids and Offspring Stimuli<sup>a</sup>
PEDERSEN, C. A. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51916.x · Cited by 172 · see citing works
Modulation of pair bonding in female prairie voles (Microtus ochrogaster) by corticosterone.
DeVries, A. C., DeVries, M. B., Taymans, S. E., & Carter, C. S. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.17.7744 · Cited by 170 · see citing works
Self-citationWindle, R. J., Shanks, N., Lightman, S. L., & Ingram, C. D. (1997) · Endocrinology · doi:10.1210/en.138.7.2829 · Cited by 170 · see citing works
2006 Curt P. Richter award winner
DeVries, A. C., Craft, T. K. S., Glasper, E. R., Neigh, G. N., & Alexander, J. K. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.04.007 · Cited by 153 · see citing works
Self-citationWILLIAMS, J. R., CARTER, C. S., & INSEL, T. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34393.x · Cited by 147 · see citing works
McCarthy, M. M., Kleopoulos, S. P., Mobbs, C. V., & Pfaff, D. W. (2008) · Neuroendocrinology · doi:10.1159/000126689 · Cited by 142 · see citing works
Larcher, A., Neculcea, J., Breton, C., Arslan, A., Rozen, F., Russo, C., & Zingg, H. H. (1995) · Endocrinology · doi:10.1210/endo.136.12.7588281 · Cited by 140 · see citing works
Taymans, S. E., DeVries, A. C., DeVries, M. B., Nelson, R. J., Friedman, T. C., de Castro, M., Detera‐Wadleigh, S. D., Carter, C. S., & Chrousos, G. P. (1997) · General and Comparative Endocrinology · doi:10.1006/gcen.1996.6849 · Cited by 112 · see citing works
Self-citationSocial structure influences effects of pair-housing on wound healing
Glasper, E. R., & DeVries, A. C. (2004) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2004.03.002 · Cited by 109 · see citing works
Self-citationBlaustein, J. D. (2007) · Annual Review of Psychology · doi:10.1146/annurev.psych.59.103006.093556 · Cited by 101 · see citing works
Interaction among Social Environment, the Hypothalamic–Pituitary–Adrenal Axis, and Behavior
DeVries, A. C. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2002.1780 · Cited by 101 · see citing works
Self-citationOxytocin receptor mRNA expression in the ventromedial hypothalamus during the estrous cycle
Bale, T., Dorsa, D. M., & Johnston, C. I. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-07-05058.1995 · Cited by 98 · 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
Oxytocin Receptor Binding in Female Prairie Voles: Endogenous and Exogenous Oestradiol Stimulation
Witt, D. M., Carter, C. S., & Lnsel, T. R. (1991) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1991.tb00258.x · Cited by 91 · see citing works
Davis, E. S., & Marler, C. A. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.05.034 · Cited by 81 · see citing works
Oxytocin and complex social behavior: species comparisons.
Winslow, J. T., Shapiro, L., Carter, C. S., & Insel, T. R. (1993) · PubMed · Cited by 80 · see citing works
Greer, E. R., Caldwell, J. D., Johnson, M. F., Prange, A. J., & Pedersen, C. A. (1986) · Life Sciences · doi:10.1016/0024-3205(86)90638-7 · Cited by 77 · see citing works
Reproductive behavior of small animals
Kustritz, M. V. R. (2005) · Theriogenology · doi:10.1016/j.theriogenology.2005.05.022 · Cited by 72 · see citing works
Neonatal manipulation of oxytocin affects expression of estrogen receptor alpha
Yamamoto, Y., Carter, C. S., & Cushing, B. S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.065 · Cited by 70 · see citing works
Bester‐Meredith, J. K., MARTIN, P. A., & Marler, C. A. (2005) · Aggressive Behavior · doi:10.1002/ab.20075 · Cited by 57 · see citing works
Dluzen, D. E., & Carter, C. S. (1979) · Physiology & Behavior · doi:10.1016/0031-9384(79)90063-5 · Cited by 56 · see citing works
Cushing, & Carter (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00382.x · Cited by 50 · see citing works
Hormone Effects on Specific and Global Brain Functions
Lee, A. W., & Pfaff, D. W. (2008) · The Journal of Physiological Sciences · doi:10.2170/physiolsci.rv007008 · Cited by 42 · see citing works
WOLF–BISON INTERACTIONS IN YELLOWSTONE NATIONAL PARK
Smith, D. W., Mech, L. D., Meagher, M., Clark, W. E., Jaffe, R., Phillips, M. K., & Mack, J. A. (2000) · Journal of Mammalogy · doi:10.1644/1545-1542(2000)081
Flagged first, then by citations
1 of the 48 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Cacioppo, J. T., Hawkley, L. C., Norman, G. J., & Berntson, G. G. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06028.x · Cited by 554 · see citing works
Self-citationPultorak, J. D., Fuxjager, M. J., Kalcounis‐Rueppell, M. C., & Marler, C. A. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.02.003 · Cited by 55 · see citing works
Pultorak, J. D., Matusinec, K. R., Miller, Z. K., & Marler, C. A. (2017) · Animal Behaviour · doi:10.1016/j.anbehav.2016.12.023 · Cited by 40 · see citing works
Wright, L., Muir, K. E., & Perrot, T. S. (2011) · Developmental Psychobiology · doi:10.1002/dev.20575 · Cited by 31 · see citing works
Harris, B. N., & Wendy Saltzman, A. (2013) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2013.02.010 · Cited by 23 · see citing works
Neuroendocrine regulation of female aggression
Oliveira, V. E. D. M., & Bakker, J. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.957114 · Cited by 22 · see citing works
Oliveira, V. E. D. M. (2023) · Springer eBooks · doi:10.1007/978-3-030-98711-4_144-1 · Cited by 15 · see citing works
Raymond, J. S., Rehn, S., James, M. H., Everett, N. A., & Bowen, M. T. (2024) · Biology of Sex Differences · doi:10.1186/s13293-024-00612-4 · Cited by 12 · see citing works
Social neuroscience: how a multidisciplinary field is uncovering the biology of human interactions.
Cacioppo, J. T., & Ortigue, S. (2011) · Europe PMC (PubMed Central) · Cited by 10 · see citing works
Aksu, B. Ç., & Barış, O. R. A. K. (2021) · International Journal of Management Economics and Business · doi:10.17130/ijmeb.964154 · Cited by 7 · see citing works
Bester‐Meredith, J. K., Burns, J. N., Dang, M. N., Garcia, A. M., Mammarella, G. E., Rowe, M. E., & Spatacean, C. F. (2021) · Aggressive Behavior · doi:10.1002/ab.22004 · Cited by 7 · see citing works
Mackay, M. K. (2011) · University of the Witwatersrand, Johannesburg Institutional Repository on DSpace (University of the Witwatersrand, Johannesburg) · Cited by 6 · see citing works
Pair bonding in monogamously and polygynously kept African striped mice, Rhabdomys pumilio
Garnier, L., & Carsten Schradin, A. (2019) · Animal Behaviour · doi:10.1016/j.anbehav.2019.02.001 · Cited by 5 · see citing works
Characterization of the gut microbiome of wild Peromyscus sonoriensis in New Mexico, USA
Skidmore, A. M., Goodfellow, S. M., Nofchissey, R., Jiang, L.-M., Dunnum, J. L., Cook, J. A., Guo, Y., Mali, I., & Bradfute, S. (2026) · Frontiers in microbiomes · doi:10.3389/frmbi.2026.1672092
Oliveira, V. E. D. M. (2023) · Springer eBooks · doi:10.1007/978-3-031-31547-3_144 · Cited by 1 · see citing works
- Authors
- Karelina, K., Walton, J. C., Weil, Z. M., Norman, G. J., Nelson, R. J., & DeVries, A. C.
- Affiliations
- The Ohio State University (US)
- Corresponding author
- Karelina, Kate
- ORCID
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 2010-07
- Volume
- 58
- Issue
- 2
- Pages
- 193-199
- ISSN
- 0018-506X (ISSN-L)
- OpenAlex
- W2111087557
- Cited by
- 15
- References
- 48
- Citations by year
- 2026: 1 · 2024: 1 · 2023: 2 · 2022: 1 · 2021: 2 · 2019: 1 · 2017: 1 · 2015: 1 · 2013: 1
- FWCI
- 2.19
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hormones and 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 › Social Psychology › Primate Behavior and Ecology
- Keywords
- estrous cycle, social behavior, Peromyscus californicus, white-footed mouse, polygyny, monogamy, affiliative behavior, agonistic behavior, oxytocin, glucocorticoids
- MeSH terms
- Aggression, Analysis of Variance, Animals, Behavior, Animal, Cell Count, Corticosterone, Female, Hypothalamus, Immunohistochemistry, Male, Oxytocin, Paraventricular Hypothalamic Nucleus, Peromyscus, Radioimmunoassay, Sexual Behavior, Animal, Social Behavior, Species Specificity, Supraoptic Nucleus, Time Factors, Estrous Cycle
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review