Dynamic changes in social dominance and mPOA GnRH expression in male mice following social opportunity
Open accessAbstract
Social competence - the ability of animals to dynamically adjust their social behavior dependent on the current social context - is fundamental to the successful establishment and maintenance of social relationships in group-living species. The social opportunity paradigm, where animals rapidly ascend a social hierarchy following the removal of more dominant individuals, is a well-established approach for studying the neural and neuroendocrine mechanisms underlying socially competent behavior. In the current study, we demonstrate that this paradigm can be successfully adapted for studying socially competent behavior in laboratory mice. Replicating our previous reports, we show that male laboratory mice housed in a semi-natural environment form stable linear social hierarchies. Novel to the current study, we find that subdominant male mice immediately respond to the removal of the alpha male from a hierarchy by initiating a dramatic increase in aggressive behavior towards more subordinate individuals. Consequently, subdominants assume the role of the alpha male. Analysis of brain gene expression in individuals 1h following social ascent indicates elevated gonadotropin-releasing hormone (GnRH) mRNA levels in the medial preoptic area (mPOA) of the hypothalamus compared to individuals that do not experience a social opportunity. Moreover, hormonal analyses indicate that subdominant individuals have increased circulating plasma testosterone levels compared to subordinate individuals. Our findings demonstrate that male mice are able to dynamically and rapidly adjust both behavior and neuroendocrine function in response to changes in social context. Further, we establish the social opportunity paradigm as an ethologically relevant approach for studying social competence and behavioral plasticity in mammals.
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?
Male mice show increases in GnRH mRNA in the medial preoptic nucleus one hour following the onset of social ascent.
“Similarly, male mice show increases in GnRH mRNA in the medial preoptic nucleus one hour following the onset of social ascent [12].”
In both cichlid fish and CD-1 mice, ascending males rapidly decrease submissive behavior and increase aggression towards other males following removal of the alpha male.
“In both species, ascending males rapidly decrease submissive behavior and increase aggression towards other males following removal of the alpha male.”
Previous work has demonstrated that mice show large changes in neural gene expression 70 minutes following social challenges.
“Previous work has demonstrated that mice do indeed show large changes in neural gene expression 70 minutes following social challenges [12,30], but it should be noted that many changes in gene expression associated with social status change may take longer to manifest and will not be observable at this time point.”
Social ascent by subordinate males has been well-documented in Burton's mouthbrooder cichlid fish, Astatotilapia burtoni, and outbred CD-1 mice, Mus musculus.
“Experimentally, social ascent by subordinate males has been well-documented in Burton’s mouthbrooder cichlid fish, Astatotilapia burtoni [10,11] and outbred CD-1 mice, Mus musculus [12].”
We have previously demonstrated that beta CD-1 males will rapidly rise to dominant status following the removal of alpha males.
“We have previously demonstrated that beta CD-1 males will rapidly rise to dominant status following the removal of alpha males [12,15].”
The association between social status and corticosterone level in mice is highly inconsistent.
“this is not unexpected as the association between social status and corticosterone level in mice is highly inconsistent [12].”
After removing the alpha mouse, one of the subordinates quickly takes its position.
“After removing the alpha, one of the subordinates quickly takes its position.140”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [140]
Cites
Analyzing real-time PCR data by the comparative CT method
Schmittgen, T. D., & Livak, K. J. (2008) · Nature Protocols · doi:10.1038/nprot.2008.73 · Cited by 26,190 · see citing works
<b>lmerTest</b> Package: Tests in Linear Mixed Effects Models
Kuznetsova, A., Brockhoff, P. B., & Christensen, R. H. B. (2017) · Journal of Statistical Software · doi:10.18637/jss.v082.i13 · Cited by 24,346 · see citing works
The mouse brain in stereotaxic coordinates
Konsman, J. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00088-x · Cited by 16,796 · see citing works
The Mouse Brain in Stereotaxic Coordinates
Paxinos, G. (2001) · Cited by 12,859 · see citing works
Wingfield, J. C., Hegner, R. E., Dufty, & Ball, G. F. (1990) · The American Naturalist · doi:10.1086/285134 · Cited by 2,330 · see citing works
The influence of social hierarchy on primate health
Sapolsky, R. M. (2005) · Science · doi:10.1126/science.1106477 · Cited by 2,113 · cited 2× · see citing works
“…literature on the relationship between circulating testosterone and aggression and social dominancewith higher circulating testosterone levels being commonly observed in the dominants of many species (Gesquiere et al., 2011; Higham et al., 2012; Mendonça-Furtado et al., 2014; Sapolsky, 2005).”
BackgroundNutritional Control of Reproductive Status in Honeybees via DNA Methylation
Kucharski, R., Maleszka, J., Forêt, S., & Maleszka, R. (2008) · Science · doi:10.1126/science.1153069 · Cited by 1,146 · see citing works
An improved test of linearity in dominance hierarchies containing unknown or tied relationships
VRIES, H. D. (1995) · Animal Behaviour · doi:10.1016/0003-3472(95)80053-0 · Cited by 590 · see citing works
Fish can infer social rank by observation alone
Grosenick, L., Clement, T. S., & Fernald, R. D. (2007) · Nature · doi:10.1038/nature05511 · Cited by 556 · see citing works
Bidirectional control of social hierarchy by synaptic efficacy in medial prefrontal cortex
Wang, F., Zhu, J., Zhu, H., Zhang, Q., Lin, Z., & Hu, H. (2011) · Science · doi:10.1126/science.1209951 · Cited by 528 · see citing works
Dominance, aggression and testosterone in wild chimpanzees: a test of the ‘challenge hypothesis’
Muller, M. N., & Wrangham, R. W. (2003) · Animal Behaviour · doi:10.1016/j.anbehav.2003.03.013 · Cited by 478 · see citing works
Social competence: an evolutionary approach
Taborsky, B., & Oliveira, R. F. (2012) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2012.09.003 · Cited by 419 · see citing works
(1994) · Choice Reviews Online · doi:10.5860/choice.31-2688 · Cited by 372 · see citing works
Bernhardt, P. C., Dabbs, J. M., Fielden, J. A., & Lutter, C. D. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00147-4 · Cited by 365 · see citing works
Parameter Estimation in Large Dynamic Paired Comparison Experiments
Glickman, M. E. (1999) · Journal of the Royal Statistical Society Series C (Applied Statistics) · doi:10.1111/1467-9876.00159 · Cited by 364 · see citing works
Nakano, S. (1995) · Journal of Animal Ecology · doi:10.2307/5828 · Cited by 348 · see citing works
Life at the Top: Rank and Stress in Wild Male Baboons
Gesquiere, L. R., Learn, N. H., Simao, M. C., Onyango, P. O., Alberts, S. C., & Jeanne Altmann, A. (2011) · Science · doi:10.1126/science.1207120 · Cited by 343 · see citing works
Influence of amygdalectomy on social behavior in monkeys.
Rosvold, H. E., Mirsky, A. F., & Pribram, K. H. (1954) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0058870 · Cited by 331 · see citing works
Social complexity and transitive inference in corvids
Bond, A. B., Kamil, A. C., & Balda, R. P. (2003) · Animal Behaviour · doi:10.1006/anbe.2003.2101 · Cited by 312 · see citing works
Oyegbile, T. O., & Marler, C. A. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.04.007 · Cited by 303 · see citing works
Rapid Behavioral and Genomic Responses to Social Opportunity
Burmeister, S. S., Jarvis, E. D., & Fernald, R. D. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030363 · Cited by 275 · see citing works
Social behavior in context: Hormonal modulation of behavioral plasticity and social competence
Oliveira, R. F. (2009) · Integrative and Comparative Biology · doi:10.1093/icb/icp055 · Cited by 255 · see citing works
Mating Season Aggression and Fecal Testosterone Levels in Male Ring-Tailed Lemurs (Lemur catta)
Cavigelli, S. A., & Pereira, M. E. (2000) · Hormones and Behavior · doi:10.1006/hbeh.2000.1585 · Cited by 248 · see citing works
Natural Variation in a Testosterone‐Mediated Trade‐Off between Mating Effort and Parental Effort
McGlothlin, J. W., Jawor, J. M., & Ketterson, E. D. (2007) · The American Naturalist · doi:10.1086/522838 · Cited by 246 · see citing works
Endocrine aspects of social instability in the olive baboon (Papio anubis)
Sapolsky, R. M. (1983) · American Journal of Primatology · doi:10.1002/ajp.1350050406 · Cited by 241 · see citing works
Social status in mice: behavioral, endocrine and immune changes are context dependent
Bartolomucci, A., Palanza, P., Gaspani, L., Limiroli, E., Panerai, A. E., Ceresini, G., Poli, M., & Parmigiani, S. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00453-x · Cited by 214 · see citing works
Watching fights raises fish hormone levels
Oliveira, R. F., Lopes, M., Carneiro, L. A., & Canário, A. V. M. (2001) · Nature · doi:10.1038/35054128 · Cited by 208 · see citing works
Dynamics of Hierarchy Formation: the Sequential Development of Dominance Relationships
Chase, I. D. (1982) · Behaviour · doi:10.1163/156853982x00364 · Cited by 204 · see citing works
An evolutionary framework for studying mechanisms of social behavior
Hofmann, H. A., Beery, A. K., Blumstein, D. T., Couzin, I. D., Earley, R. L., Hayes, L. D., Hurd, P. L., Lacey, E. A., Phelps, S. M., Solomon, N. G., et al. (2014) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2014.07.008 · Cited by 200 · see citing works
Social status predicts wound healing in wild baboons
Archie, E. A., Jeanne Altmann, A., & Alberts, S. C. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1206391109 · Cited by 191 · see citing works
Encyclopedia of Human Behavior
(2012) · Elsevier eBooks · doi:10.1016/c2009-1-03753-8 · Cited by 190 · see citing works
Dominance Hierarchy Influences Adult Neurogenesis in the Dentate Gyrus: Figure 1.
Kozorovitskiy, Y., & Gould, E. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0345-04.2004 · Cited by 179 · see citing works
Greenberg, N. L., & Crews, D. P. (1990) · General and Comparative Endocrinology · doi:10.1016/0016-6480(90)90309-a · Cited by 170 · see citing works
Bronson, F. H. (1973) · Physiology & Behavior · doi:10.1016/0031-9384(73)90065-6 · Cited by 168 · see citing works
Haemisch, A., Voss, T., & Gärtner, K. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90341-7 · Cited by 164 · see citing works
Maruska, K. P., & Fernald, R. D. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.03.011 · Cited by 161 · see citing works
Neuroendocrine response patterns in dominant and subordinate mice
Ely, D., & Henry, J. P. (1978) · Hormones and Behavior · doi:10.1016/0018-506x(78)90005-3 · Cited by 154 · see citing works
Dominance hierarchy formation in juvenile crayfish procambarus clarkii
Issa, F. A., Adamson, D. J., & Edwards, D. H. (1999) · Journal of Experimental Biology · doi:10.1242/jeb.202.24.3497 · Cited by 151 · see citing works
Temporal dynamics of social hierarchy formation and maintenance in male mice
Williamson, C. M., Lee, W., & Curley, J. P. (2016) · Animal Behaviour · doi:10.1016/j.anbehav.2016.03.004 · Cited by 150 · see citing works
Self-citationChronic physiological effects of fighting in mice
Bronson, F. H., & Eleftheriou, B. E. (1964) · General and Comparative Endocrinology · doi:10.1016/0016-6480(64)90033-4 · Cited by 144 · see citing works
Dominance, attention, and affiliation in a preschool group: a nine-month longitudinal study
LaFrenière, P. J., & Charlesworth, W. R. (1983) · Ethology and Sociobiology · doi:10.1016/0162-3095(83)90030-4 · Cited by 141 · see citing works
Maruska, K. P., Zhang, A., Neboori, A., & Fernald, R. D. (2012) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2012.02382.x · Cited by 138 · see citing works
Social Regulation of Gene Expression in the Hypothalamic-Pituitary-Gonadal Axis
Maruska, K. P., & Fernald, R. D. (2011) · Physiology · doi:10.1152/physiol.00032.2011 · Cited by 137 · see citing works
So, N., Franks, B., Lim, S., & Curley, J. P. (2015) · PLOS ONE · doi:10.1371/journal.pone.0134509 · Cited by 135 · see citing works
Self-citationSelf-organizing dominance hierarchies in a wild primate population
Franz, M., McLean, E. M., Tung, J., Jeanne Altmann, A., & Alberts, S. C. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2015.1512 · Cited by 125 · see citing works
Seasonal control of gonadotropin-inhibitory hormone (GnIH) in birds and mammals
Kriegsfeld, L. J., Ubuka, T., Bentley, G. E., & Tsutsui, K. (2014) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.12.001 · Cited by 117 · see citing works
Social Context Influences Aggressive and Courtship Behavior in a Cichlid Fish
Desjardins, J. K., Hofmann, H. A., & Fernald, R. D. (2012) · PLoS ONE · doi:10.1371/journal.pone.0032781 · Cited by 111 · see citing works
Self-Structuring Properties of Dominance Hierarchies
Chase, I. D., & Seitz, K. (2011) · Advances in genetics · doi:10.1016/b978-0-12-380858-5.00001-0 · Cited by 105 · see citing works
Social Regulation of Male Reproductive Plasticity in an African Cichlid Fish
Maruska, K. P., & Fernald, R. D. (2013) · Integrative and Comparative Biology · doi:10.1093/icb/ict017 · Cited by 96 · see citing works
Gonadotropin-releasing hormone plasticity: A comparative perspective
Stevenson, T. J., Hahn, T. P., MacDougall‐Shackleton, S. A., & Ball, G. F. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2012.09.001 · Cited by 94 · see citing works
Faulkes, C. G., Abbott, D. H., Jarvis, J. U. M., & Sherriff, F. E. (1990) · Reproduction · doi:10.1530/jrf.0.0890317 · Cited by 91 · see citing works
Higham, J. P., Heistermann, M., & Dario Maestripieri, A. (2012) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-012-1420-6 · Cited by 87 · see citing works
Maruska, K. P., Levavi‐Sivan, B., Biran, J., & Fernald, R. D. (2010) · Endocrinology · doi:10.1210/en.2010-0875 · Cited by 74 · see citing works
Testosterone and competitive ability in male house mice, Mus musculus: laboratory and field studies
Zielinski, W. J., & Vandenbergh, J. G. (1993) · Animal Behaviour · doi:10.1006/anbe.1993.1108 · Cited by 71 · see citing works
Gonadotropin‐releasing hormone: regulation of theGnRHgene
Lee, V. H. Y., Lee, L. T. O., & Chow, B. (2008) · FEBS Journal · doi:10.1111/j.1742-4658.2008.06676.x · Cited by 69 · see citing works
Intermale Stimuli and Testicular Function in Adult and Immature House Mice1
McKinney, T. D., & Desjardins, C. (1973) · Biology of Reproduction · doi:10.1093/biolreprod/9.4.370 · Cited by 69 · see citing works
Mendonça‐Furtado, O., Edaes, M., Palme, R., Rodrigues, A. S., Siqueira, J. D. O., & Izar, P. (2014) · Behavioural Processes · doi:10.1016/j.beproc.2014.09.010 · Cited by 64 · see citing works
Lowered Sperm Motility in Subordinate Social Status of Mice
Koyama, S., & Kamimura, S. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00205-4 · Cited by 55 · see citing works
Serum testosterone, agonistic behavior, and dominance in inbred strains of mice
SELMANOFF, M. K., Goldman, B. D., & Ginsburg, B. E. (1977) · Hormones and Behavior · doi:10.1016/0018-506x(77)90026-5 · Cited by 55 · see citing works
Courtship interactions stimulate rapid changes in GnRH synthesis in male ring doves
Mantei, K. E., RAMAKRISHNAN, S., SHARP, P., et al. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.07.005 · Cited by 46 · see citing works
Conspecific aggression influences food carrying: Studies on a wild population of Rattus norvegicus
Whishaw, I. Q., & Whishaw, G. E. (1996) · Aggressive Behavior · doi:10.1002/(sici)1098-2337(1996)22:1 · Cited by 45 · see citing works
Carpenter, R. E., Maruska, K. P., Becker, L., & Fernald, R. D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0096632 · Cited by 43 · see citing works
Temporal pairwise-correlation analysis provides empirical support for attention hierarchies in mice
Curley, J. P. (2016) · Biology Letters · doi:10.1098/rsbl.2016.0192 · Cited by 43 · see citing works
Self-citationShaking the myth: Body mass, aggression, steroid hormones, and social dominance in wild house mouse
Hiadlovská, Z., Mikula, O., Macholán, M., Hamplová, P., Bímová, B. V., & Daniszová, K. (2015) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.09.033 · Cited by 33 · see citing works
Social instability promotes hormone–behavior associated patterns in a cichlid fish
Almeida, O., Gonçalves‐de‐Freitas, E., Lopes, J. S., & Oliveira, R. F. (2014) · Hormones and Behavior · doi:10.1016/j.yhbeh.2014.05.007 · Cited by 31 · see citing works
Cognitive Skills Needed for Social HierarchiesPreprint
Fernald, R. D. (2014) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.2014.79.024752 · Cited by 26 · see citing works
Gore, A. C., Wersinger, S. R., & Rissman, E. F. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00578.x · Cited by 22 · see citing works
Bradley, A. J., & Stoddart, D. M. (1997) · Journal of Zoology · doi:10.1111/j.1469-7998.1997.tb04849.x · Cited by 13 · see citing works
Jennings, K. J., Chang, J., Cho, H., Piekarski, D. J., Russo, K. A., & Kriegsfeld, L. J. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.10.021 · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Ecological validity of social interaction tests in rats and mice
Kondrakiewicz, K., Kostecki, M., Szadzińska, W., & Knapska, E. (2019) · Genes, Brain and Behavior · doi:10.1111/gbb.12525 · Cited by 136 · see citing works
Advances in understanding neural mechanisms of social dominance
Zhou, T., Sandi, C., & Hu, H. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.01.006 · Cited by 133 · see citing works
Social context-dependent relationships between mouse dominance rank and plasma hormone levels
Williamson, C. M., Lee, W., Romeo, R. D., & Curley, J. P. (2017) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.12.038 · Cited by 120 · see citing works
Self-citationMilewski, T. M., Lee, W., Young, R. L., Hofmann, H. A., & Curley, J. P. (2025) · PLoS Genetics · doi:10.1371/journal.pgen.1011548 · Cited by 7 · see citing works
Self-citation
- Authors
- Williamson, C. M., Romeo, R. D., & Curley, J. P.
- Affiliations
- Columbia University (US)
- Barnard College (US)
- Corresponding author
- Curley, James P.
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 2017-01
- Volume
- 87
- Pages
- 80-88
- ISSN
- 0018-506X (ISSN-L)
- OpenAlex
- W2547587217
- Cited by
- 62
- References
- 69
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 9 · 2023: 5 · 2022: 7 · 2021: 8 · 2020: 6 · 2019: 8 · 2018: 9 · 2017: 3
- FWCI
- 10.50
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Hormones and Behavior (acceptedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (DGE-16-44869)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- social dominance, social hierarchy, social competence, gonadotropin-releasing hormone, medial preoptic area, hypothalamus, testosterone, aggression, social ascent, behavioral plasticity, neuroendocrine regulation, male mice
- MeSH terms
- Aggression, Animals, Behavior, Animal, Brain, Competitive Behavior, Hierarchy, Social, Hypothalamus, Gonadotropin-Releasing Hormone, Male, Preoptic Area, Social Behavior, Social Dominance, Social Environment, Animals, Outbred Strains, Mice
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
