Differential changes in steroid hormones before competition in bonobos and chimpanzees
Open accessAbstract
A large body of research has demonstrated that variation in competitive behavior across species and individuals is linked to variation in physiology. In particular, rapid changes in testosterone and cortisol during competition differ according to an individual's or species’ psychological and behavioral responses to competition. This suggests that among pairs of species in which there are behavioral differences in competition, there should also be differences in the endocrine shifts surrounding competition. We tested this hypothesis by presenting humans’ closest living relatives, chimpanzees ( Pan troglodytes ) and bonobos ( Pan paniscus ), with a dyadic food competition and measuring their salivary testosterone and cortisol levels. Given that chimpanzees and bonobos differ markedly in their food-sharing behavior, we predicted that they would differ in their rapid endocrine shifts. We found that in both species, males showed an anticipatory decrease (relative to baseline) in steroids when placed with a partner in a situation in which the two individuals shared food, and an anticipatory increase when placed with a partner in a situation in which the dominant individual obtained more food. The species differed, however, in terms of which hormone was affected; in bonobo males the shifts occurred in cortisol, whereas in chimpanzee males the shifts occurred in testosterone. Thus, in anticipation of an identical competition, bonobo and chimpanzee males showed differential endocrine shifts, perhaps due to differences in perception of the situation, that is, viewing the event either as a stressor or a dominance contest. In turn, common selection pressures in human evolution may have acted on the psychology and the endocrinology of our competitive behavior.
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The study found an anticipatory increase in urinary oxytocin in wild chimpanzees, similar to the anticipatory testosterone increase previously found in intergroup conflicts and intragroup competition in chimpanzees.
“Our results demonstrate an anticipatory increase in urinary oxytocin in a similar manner to the anticipatory testosterone increase found in intergroup conflicts (28) and intragroup competition (29) in chimpanzees.”
From Oxytocin reactivity during intergroup conflict in wild chimpanzees (2017) · cites this paper as [29]
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Cites
Sapolsky, R. M., Romero, L. M., & Munck, A. U. (2000) · Endocrine Reviews · doi:10.1210/edrv.21.1.0389 · Cited by 7,541 · 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
Sex differences in HPA axis responses to stress: a review
Kudielka, B. M., & Kirschbaum, C. (2005) · Biological Psychology · doi:10.1016/j.biopsycho.2004.11.009 · Cited by 1,624 · see citing works
Testosterone and dominance in men
Mazur, A., & Booth, A. (1998) · Behavioral and Brain Sciences · doi:10.1017/s0140525x98001228 · Cited by 1,447 · see citing works
Reproduction and Resistance to Stress: When and How
Wingfield, J. C., & Sapolsky, R. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01033.x · Cited by 1,131 · see citing works
Kirschbaum, C., Klauer, T., Filipp, S., & Hellhammer, D. H. (1995) · Psychosomatic Medicine · doi:10.1097/00006842-199501000-00004 · Cited by 583 · see citing works
Chimpanzees Recruit the Best Collaborators
Melis, A. P., Hare, B. A., & Tomasello, M. (2006) · Science · doi:10.1126/science.1123007 · Cited by 574 · see citing works
Self-citationThe last ape: pygmy chimpanzee behavior and ecology
(1993) · Choice Reviews Online · doi:10.5860/choice.30-4403 · Cited by 542 · see citing works
Tolerance Allows Bonobos to Outperform Chimpanzees on a Cooperative Task
Hare, B. A., Melis, A. P., Woods, V. E., Hastings, S., & Wrangham, R. W. (2007) · Current Biology · doi:10.1016/j.cub.2007.02.040 · Cited by 526 · see citing works
Self-citationTestosterone, and winning and losing in human competition
Booth, A., Shelley, G., Mazur, A., Tharp, G., & Kittok, R. (1989) · Hormones and Behavior · doi:10.1016/0018-506x(89)90042-1 · Cited by 515 · 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
Self-citationKoolhaas, J. M., de Boer, S. F., Buwalda, B., & van Reenen, K. (2007) · Brain Behavior and Evolution · doi:10.1159/000105485 · Cited by 440 · see citing works
The “trouble” with salivary testosterone
Granger, D. A., Shirtcliff, E. A., Booth, A., Kivlighan, K. T., & Schwartz, E. B. (2004) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2004.02.005 · Cited by 388 · see citing works
Rosati, A. G., Stevens, J. R., Hare, B. A., & HAUSER, M. D. (2007) · Current Biology · doi:10.1016/j.cub.2007.08.033 · Cited by 357 · see citing works
Self-citationOyegbile, T. O., & Marler, C. A. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.04.007 · Cited by 303 · see citing works
Testosterone and Chess Competition
Mazur, A., BOOTH, A. R., & Dabbs, J. M. (1992) · Social Psychology Quarterly · doi:10.2307/2786687 · Cited by 282 · see citing works
Testosterone, cortisol, and women's competition
Bateup, H. S., BOOTH, A. R., Shirtcliff, E. A., & Granger, D. A. (2002) · Evolution and Human Behavior · doi:10.1016/s1090-5138(01)00100-3 · Cited by 266 · see citing works
Effects of competition and its outcome on serum testosterone, cortisol and prolactin
Suay, F., Salvador, A., González‐Bono, E., Sanchı́s, C., Martı́nez, M., Martínez‐Sanchis, S., SIMON, V. M., & Montoro, J. B. (1999) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(99)00011-6 · Cited by 263 · see citing works
Schultheiss, O. C., Wirth, M. M., Torges, C. M., Pang, J. S., Villacorta, M. A., & Welsh, K. M. (2005) · Journal of Personality and Social Psychology · doi:10.1037/0022-3514.88.1.174 · Cited by 248 · see citing works
Agonistic relations among Kanyawara chimpanzees
Muller, M. N. (2002) · Cambridge University Press eBooks · doi:10.1017/cbo9780511606397.012 · Cited by 239 · see citing works
Sexual Coercion in Primates and Humans
(2009) · Harvard University Press eBooks · doi:10.4159/9780674054349 · Cited by 222 · see citing works
Gender differences in testosterone and cortisol response to competition
Kivlighan, K. T., Granger, D. A., & Booth, A. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2004.05.009 · Cited by 215 · see citing works
Bonobos Exhibit Delayed Development of Social Behavior and Cognition Relative to Chimpanzees
Wobber, V., Wrangham, R. W., & Hare, B. A. (2010) · Current Biology · doi:10.1016/j.cub.2009.11.070 · Cited by 213 · see citing works
Self-citationPsychophysiological stress in tennis players during the first single match of a tournament
Filaire, E., Alix, D., Ferrand, C., & Verger, M. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.08.022 · Cited by 199 · see citing works
Hormonal response to competition in human males
Gladue, B. A., Boechler, M., & McCaul, K. D. (1989) · Aggressive Behavior · doi:10.1002/1098-2337(1989)15:6 · Cited by 186 · see citing works
Testosterone and Social Behavior
BOOTH, A. R., Granger, D. A., Mazur, A., & Kivlighan, K. T. (2006) · Social Forces · doi:10.1353/sof.2006.0116 · Cited by 178 · see citing works
Smider, N. A., Essex, M. J., Kalin, N. H., Buss, K. A., Klein, M. H., Davidson, R. J., & Goldsmith, H. H. (2002) · Child Development · doi:10.1111/1467-8624.00393 · Cited by 175 · see citing works
Schultheiss, O. C., Campbell, K. L., & McClelland, D. C. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1542 · Cited by 174 · see citing works
The hormonal correlates of implicit power motivation
Stanton, S. J., & Schultheiss, O. C. (2009) · Journal of Research in Personality · doi:10.1016/j.jrp.2009.04.001 · Cited by 172 · see citing works
Coping with competition: Neuroendocrine responses and cognitive variables
Salvador, A., & Costa, R. (2008) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.09.005 · Cited by 169 · see citing works
Tension regulation and nonreproductive functions of sex in captive bonobos pan paniscus
Waal, D. (1987) · Cited by 165 · see citing works
Wrangham, R. W., & Pilbeam, D. R. (2005) · Kluwer Academic Publishers eBooks · doi:10.1007/0-306-47461-1_2 · Cited by 163 · see citing works
Self-citationBonobos voluntarily share their own food with others
Hare, B. A., & Kwetuenda, S. (2010) · Current Biology · doi:10.1016/j.cub.2009.12.038 · Cited by 155 · see citing works
Self-citationWirth, M. M., Welsh, K. M., & Schultheiss, O. C. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.08.013 · Cited by 150 · see citing works
Dominance and its Behavioral Measures in a Captive Group of Bonobos (Pan paniscus)
Vervaecke, H., de Vries, H. D., & Elsacker, L. V. (2000) · International Journal of Primatology · doi:10.1023/a:1005471512788 · Cited by 131 · see citing works
A geometric morphometric analysis of heterochrony in the cranium of chimpanzees and bonobos
Lieberman, D. E., Carlo, J., de León, M. S. P., & Zollikofer, C. P. E. (2007) · Journal of Human Evolution · doi:10.1016/j.jhevol.2006.12.005 · Cited by 130 · see citing works
Guatelli‐Steinberg, D., & Lukacs, J. R. (1999) · American Journal of Physical Anthropology · doi:10.1002/(sici)1096-8644(1999)110:29+ · Cited by 127 · see citing works
Behavioral and environmental events influencing primate testosterone levels
Bernstein, I. S., Rose, R. M., & Gordon, T. P. (1974) · Journal of Human Evolution · doi:10.1016/0047-2484(74)90012-8 · Cited by 102 · see citing works
Veenema, A. H., Koolhaas, J. M., & de Kloet, E. R. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1296.030 · Cited by 97 · see citing works
Galdikas, B. M. F., Goodall, J., Shapiro, G. L., Sheeran, L. K., & Briggs, N. E. (2001) · Springer eBooks · doi:10.1007/b107546 · Cited by 95 · see citing works
Development of protocols for the application of salivary steroid analysis to field conditions
Lipson, S., & Ellison, P. T. (1989) · American Journal of Human Biology · doi:10.1002/ajhb.1310010304 · Cited by 93 · see citing works
Self-citationIt's not that bad: Error introduced by oral stimulants in salivary cortisol research
Talge, N. M., Donzella, B., Kryzer, E. M., Gierens, A., & Gunnar, M. R. (2005) · Developmental Psychobiology · doi:10.1002/dev.20097 · Cited by 92 · see citing works
How and why the winner effect forms: influences of contest environment and species differences
Fuxjager, M. J., & Marler, C. A. (2009) · Behavioral Ecology · doi:10.1093/beheco/arp148 · Cited by 88 · see citing works
Muehlenbein, M. P., Watts, D. P., & Whitten, P. L. (2004) · American Journal of Primatology · doi:10.1002/ajp.20062 · Cited by 86 · see citing works
How bonobos handle hunts and harvests: why share food?
Fruth, B., & Hohmann, G. (2002) · Cambridge University Press eBooks · doi:10.1017/cbo9780511606397.023 · Cited by 84 · see citing works
Diurnal patterns of urinary steroid excretion in wild chimpanzees
Muller, M. N., & Lipson, S. F. (2003) · American Journal of Primatology · doi:10.1002/ajp.10103 · Cited by 75 · see citing works
Self-citationSannen, A., Elsacker, L. V., Eens, M., Heistermann, M., & Möhle, U. (2003) · Behaviour · doi:10.1163/156853903322149504 · Cited by 73 · see citing works
Hohmann, G., Mundry, R., & Deschner, T. (2008) · American Journal of Primatology · doi:10.1002/ajp.20640 · Cited by 72 · see citing works
Association and social interactions between strangers and residents in bonobos (Pan paniscus)
Hohmann, G. (2001) · Primates · doi:10.1007/bf02640692 · Cited by 65 · see citing works
Effects of ability- and chance-determined competition outcome on testosterone
van Anders, S. M., & Watson, N. V. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.11.017 · Cited by 49 · see citing works
Psychophysiological responses in the pre-competition period in elite soccer players.
Alix, D., Scanff, C. L., & Filaire, E. (2008) · Europe PMC (PubMed Central) · Cited by 45 · see citing works
Marshall, A. J., & Hohmann, G. (2005) · American Journal of Primatology · doi:10.1002/ajp.20099 · Cited by 42 · see citing works
Schanfield, M. S., Giles, E., & Gershowitz, H. (1975) · American Journal of Physical Anthropology · doi:10.1002/ajpa.1330420102 · Cited by 34 · see citing works
Rapid changes in chimpanzee (Pan troglodytes) urinary cortisol excretion
Anestis, S. F., & Bribiescas, R. G. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2003.09.015 · Cited by 32 · see citing works
Children?s competitive peer aggression during reward and punishment
Atkins, M. S., Osborne, M. L., Bennett, D. S., Hess, L. E., & Halperin, J. M. (2001) · Aggressive Behavior · doi:10.1002/1098-2337(20010101/31)27:1 · Cited by 21 · see citing works
Lore, R., & Flannelly, K. J. (1981) · Aggressive Behavior · doi:10.1002/1098-2337(1981)7:3 · Cited by 19 · see citing works
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- Authors
- Wobber, V., Hare, B., Maboto, J., Lipson, S., Wrangham, R., & Ellison, P. T.
- Affiliations
- Harvard University (US)
- Duke University (US)
- Tchimpounga Chimpanzee Sanctuary, BP 1896, Pointe Noire, Republic of Congo
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2010-06-28
- Volume
- 107
- Issue
- 28
- Pages
- 12457-12462
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2906573
- OpenAlex
- W2155178435
- Cited by
- 178
- References
- 56
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 3 · 2023: 47 · 2022: 13 · 2021: 7 · 2020: 8 · 2019: 7 · 2018: 7 · 2017: 9 · 2016: 7 · 2015: 14 · 2014: 12 · 2013: 6 · 2012: 23
- FWCI
- 16.97
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Topics
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Evolutionary Psychology and Human Behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- bonobos, chimpanzees, food competition, testosterone, cortisol, salivary hormones, food sharing, primate social behavior, human evolution, stress response, sex differences
- MeSH terms
- Aggression, Animals, Pan troglodytes, Biological Evolution, Food, Hormones, Male, Social Behavior, Steroids, Hominidae, Pan paniscus
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