Opposite effects of male and female helpers on social tolerance and proactive prosociality in callitrichid family groups
Open accessAbstract
Across a broad variety of primate species (including lemurs, New World monkeys, Old World monkeys, and apes), proactive prosociality and social tolerance are linked to allomaternal care, reaching the highest levels in the cooperatively breeding callitrichid monkeys and humans. However, considerable variation exists within callitrichids, and the aim of this study was to identify factors that explain this variation. Male and female callitrichids pursue different reproductive strategies, leading males to play a more prominent role in allomothering. We thus hypothesised that prosociality and tolerance may be affected by group composition and sex differences. We analysed social tolerance and proactive prosociality data in 49 common marmosets and found that the number of female helpers in a group was negatively correlated with group-level prosociality and tolerance. At the individual level, rearing experience or age enhanced prosociality in male, but not in female helpers. These findings are consistent with the more ambivalent role of female helpers in infant rearing. Adding data from 5 cotton-top and 5 lion tamarins strengthened this pattern. The same factor which explains variation in prosociality and tolerance across primate species, i.e. allomaternal care, is therefore also linked to variation within common marmosets, and presumably callitrichid monkeys in general.
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Marmoset families with more male helpers are more prosocial than marmoset families with more female helpers.
“Furthermore, marmoset families with more male helpers are more prosocial than marmoset families with more female helpers, and infant care experience enhanced prosociality in males but not females (Burkart, 2015).”
From Inequity aversion strategies between marmosets are influenced by partner familiarity and sex but not by oxytocin (2016) · cites this paper as Burkart, 2015
Infant care experience enhanced prosociality in males but not females.
“Furthermore, marmoset families with more male helpers are more prosocial than marmoset families with more female helpers, and infant care experience enhanced prosociality in males but not females (Burkart, 2015).”
From Inequity aversion strategies between marmosets are influenced by partner familiarity and sex but not by oxytocin (2016) · cites this paper as Burkart, 2015
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Cites
Cooperative Breeding and Human Cognitive Evolution
Burkart, J. M., Hrdy, S. B., & Van Schaik, C. P. (2009) · Evolutionary Anthropology: Issues, News, and Reviews · doi:10.1002/evan.20222 · Cited by 646 · see citing works
The evolutionary origin of human hyper-cooperation
Burkart, J. M., Allon, O., Amici, F., Fichtel, C., Finkenwirth, C., Heschl, A., Huber, J., Isler, K., Kosonen, Z. K., Martins, E., et al. (2014) · Nature Communications · doi:10.1038/ncomms5747 · Cited by 396 · see citing works
Other-regarding preferences in a non-human primate: common marmosets provision food altruistically
Burkart, J. M., Fehr, E., Efferson, C., & van Schaik, C. P. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710310104 · Cited by 359 · see citing works
Jaeggi, A. V., Burkart, J. M., & van Schaik, C. P. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2010.0118 · Cited by 250 · see citing works
Goldizen, A. W. (1987) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00572631 · Cited by 228 · see citing works
Prosocial behaviour in animals: the influence of social relationships, communication and rewards
Cronin, K. A. (2012) · Animal Behaviour · doi:10.1016/j.anbehav.2012.08.009 · Cited by 205 · see citing works
Evolutionary foundations of human prosocial sentiments
Silk, J. B., & House, B. R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1100305108 · Cited by 199 · see citing works
A new interpretation of the social organization and mating system of the Callitrichidae
Sussman, R. W., & Garber, P. A. (1987) · International Journal of Primatology · doi:10.1007/bf02737114 · Cited by 193 · see citing works
Lion tamarins : biology and conservation
Kleiman, D. G., & Rylands, A. B. (2002) · Cited by 189 · see citing works
One for all and breeding for one: Cooperation and competition as a tamarin reproductive strategy
Garber, P. A. (1997) · Evolutionary Anthropology Issues News and Reviews · doi:10.1002/(sici)1520-6505(1997)5:6 · Cited by 183 · see citing works
Garber, P. A., Moya, L., & Málaga, C. A. (1984) · Folia Primatologica · doi:10.1159/000156141 · Cited by 167 · see citing works
Behavioural evidence for monopolization of paternity in multi-male groups of golden lion tamarins
Baker, A. J., Dietz, J. M., & Kleiman, D. G. (1993) · Animal Behaviour · doi:10.1006/anbe.1993.1299 · Cited by 150 · see citing works
Begging, Stealing, and Offering: Food Transfer in Nonhuman Primates
Brown, G. R., Almond, R. E. A., & Bergen, Y. V. (2004) · Advances in the Study of Behavior · doi:10.1016/s0065-3454(04)34007-6 · Cited by 144 · see citing works
Madden, J. R., & Clutton-Brock, T. H. (2011) · Proceedings of the Royal Society B: Biological Sciences · doi:10.1098/rspb.2010.1675 · Cited by 144 · see citing works
Tardif, S. D., Richter, C. B., & Carson, R. L. (1984) · American Journal of Primatology · doi:10.1002/ajp.1350060408 · Cited by 129 · see citing works
Effects of Allocare-Givers on Fitness of Infants and Parents in Callitrichid Primates
Bales, K. L., Dietz, J. M., Baker, A., Miller, K. E., & Tardif, S. D. (2000) · Folia Primatologica · doi:10.1159/000021728 · Cited by 114 · see citing works
Infant Care in Cooperatively Breeding Species
Snowdon, C. T. (1996) · Advances in the study of behavior · doi:10.1016/s0065-3454(08)60345-9 · Cited by 110 · see citing works
Demography, group composition, and dispersal in wild cotton-top tamarin (Saguinus oedipus) groups
Savage, A., Giraldo, L. H., Soto, L. H., & Snowdon, C. T. (1996) · American Journal of Primatology · doi:10.1002/(sici)1098-2345(1996)38:1 · Cited by 102 · see citing works
Lazaro-Perea, C., de Castro, C. S. S., Harrison, R., Araújo, A., Arruda, M. F., & Snowdon, C. T. (2000) · Behavioral Ecology and Sociobiology · doi:10.1007/s002650000215 · Cited by 99 · see citing works
The Smallest anthropoids: the marmoset/Callimico radiation
(2010) · Choice Reviews Online · doi:10.5860/choice.47-5654 · Cited by 95 · see citing works
Group size, composition, and reproductive success in wild common marmosets (Callithrix jacchus)
Koenig, A. (1995) · American Journal of Primatology · doi:10.1002/ajp.1350350407 · Cited by 91 · see citing works
Burkart, J. M., & van Schaik, C. P. (2012) · Journal of comparative psychology · doi:10.1037/a0026392 · Cited by 83 · see citing works
Social processes in communication and cognition in callitrichid monkeys: a review
Snowdon, C. T. (2001) · Animal Cognition · doi:10.1007/s100710100094 · Cited by 81 · see citing works
Cooperative breeders do cooperate
Snowdon, C. T., & Cronin, K. A. (2007) · Behavioural Processes · doi:10.1016/j.beproc.2007.01.016 · Cited by 75 · see citing works
Digby, L. J. (1999) · Folia Primatologica · doi:10.1159/000021686 · Cited by 69 · see citing works
Arruda, M. F., Araújo, A., de Sousa, M. B. C., Albuquerque, F. S., Albuquerque, A. C. S. R., & Yamamoto, M. E. (2005) · Folia Primatologica · doi:10.1159/000082451 · Cited by 68 · see citing works
Social determinants of reproductive failure in male common marmosets housed with their natal family
Baker, J. V., Abbott, D. H., & Wendy Saltzman, A. (1999) · Animal Behaviour · doi:10.1006/anbe.1999.1200 · Cited by 63 · see citing works
Poole, T. B., & Evans, R. G. (1982) · Laboratory Animals · doi:10.1258/002367782780908760 · Cited by 62 · see citing works
Marmosets as model species in neuroscience and evolutionary anthropology
Burkart, J. M., & Finkenwirth, C. (2014) · Neuroscience Research · doi:10.1016/j.neures.2014.09.003 · Cited by 60 · see citing works
The Role of Non‐reproductive Helpers in Infant Care in Captive Callithrix jacchus
Yamamoto, M. E., & Box, H. O. (1997) · Ethology · doi:10.1111/j.1439-0310.1997.tb00184.x · Cited by 59 · see citing works
Tardif, S. D., Carson, R. L., & Gangaware, B. L. (1986) · American Journal of Primatology · doi:10.1002/ajp.1350110202 · Cited by 56 · see citing works
The development of infant-caregiver relationships in captive common marmosets (Callithrix jacchus)
Locke-Haydon, J., & Chalmers, N. (1983) · International Journal of Primatology · doi:10.1007/bf02739360 · Cited by 55 · see citing works
Zahed, S. R., Kurian, A. V., & Snowdon, C. T. (2009) · American Journal of Primatology · doi:10.1002/ajp.20782 · Cited by 51 · see citing works
Mating Systems and Female–Female Competition in the Common Marmoset, Callithrix jacchus
Yamamoto, M. E., Arruda, M. D. F., Alencar, A. I., de Sousa, M. B. C., & Araújo, A. (2009) · Springer eBooks · doi:10.1007/978-1-4419-0293-1_6 · Cited by 50 · see citing works
The care of infants in a wild marmoset (Callithrix flaviceps) group
Ferrari, S. F. (1992) · American Journal of Primatology · doi:10.1002/ajp.1350260205 · Cited by 49 · see citing works
Preschool children fail primate prosocial game because of attentional task demands
Burkart, J. M., & Rueth, K. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068440 · Cited by 45 · see citing works
Male and female breeding strategies in a cooperative primate
Yamamoto, M. E., Araujo, A., Arruda, M. D. F., Lima, A. K. M., Siqueira, J. D. O., & Hattori, W. T. (2014) · Behavioural Processes · doi:10.1016/j.beproc.2014.06.009 · Cited by 42 · see citing works
Effect of Removal from the Family Group on Feeding Behavior by Captive Callithrix jacchus
Yamamoto, M. E., & Lopes, F. D. A. (2004) · International Journal of Primatology · doi:10.1023/b:ijop.0000019164.98756.9c · Cited by 40 · see citing works
Koenig, A., & Rothe, H. (1991) · Primates · doi:10.1007/bf02381175 · Cited by 38 · see citing works
Family Feuds: Severe Aggression among Cooperatively Breeding Cotton-Top Tamarins
Snowdon, C. T., & Pickhard, J. J. (1999) · International Journal of Primatology · doi:10.1023/a:1020796517550 · Cited by 34 · see citing works
Individual and group effects on early caregiver-infant relationships in red-bellied tamarin monkeys
Pryce, C. R. (1988) · Animal Behaviour · doi:10.1016/s0003-3472(88)80216-1 · Cited by 28 · see citing works
Price, E. C. (1992) · International Journal of Primatology · doi:10.1007/bf02547838 · Cited by 28 · see citing works
Henry, M. D., Hankerson, S. J., Siani, J. M., French, J. A., & Dietz, J. M. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.02.009 · Cited by 27 · see citing works
Mills, D. A., Windle, C. P., Baker, H. F., & Ridley, R. M. (2004) · Primates · doi:10.1007/s10329-004-0095-7 · Cited by 25 · see citing works
Smith, H. J. (2005) · Harvard University Press eBooks · doi:10.4159/9780674043800 · Cited by 23 · see citing works
Faulkes, C. G., Arruda, M. F., & da Cruz, M. A. O. M. (2009) · Springer eBooks · doi:10.1007/978-1-4419-0293-1_5 · Cited by 22 · see citing works
Barbosa, M. N., & Mota, M. T. D. S. (2012) · American Journal of Primatology · doi:10.1002/ajp.22092 · Cited by 16 · see citing works
Predation rate and future reproductive potential explain home range size in golden lion tamarins
Hankerson, S. J., & Dietz, J. M. (2014) · Animal Behaviour · doi:10.1016/j.anbehav.2014.07.026 · Cited by 14 · see citing works
Gil‐Bürmann, C., Peláez, F., & Sánchez, S. (1998) · Primates · doi:10.1007/bf02557570 · Cited by 14 · see citing works
Gender Differences in Marmosets and Tamarins: Responses to Food Tasks
Box, H. O., Yamamoto, M. E., & Lopes, F. A. (2012) · International Journal of Comparative Psychology · doi:10.46867/c42g67 · Cited by 10 · see citing works
Fathers have higher motivation for parenting than mothers in common marmoset (Callithrix jacchus)
Saito, A., Izumi, A., & Nakamura, K. (2011) · Behaviour · doi:10.1163/000579511x596598 · Cited by 9 · see citing works
Mattle, F. M. E., Pryce, C. R., & Anzenberger, G. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.03.004 · Cited by 9 · see citing works
Cuidado cooperativo à prole em Callithrix jacchus: dinâmica em ambiente natural
Albuquerque, F. D. S., & Otta, E. (1999) · Cited by 7 · see citing works
Food Sharing Behavior in Primates: Another Species Added
Wilson, C. G. (1976) · Journal of the Arkansas Academy of Science · Cited by 6 · see citing works
Flagged first, then by citations
Research works printed but not linked: 7
- Digby L. J., Ferrari S. F. & Saltzman W. in Primates in Perspective (eds Campbell C. J., et al.) 85– 105 (Oxford University Press, 2007).
- Schaffner C. M. & Caine N. G. in Natural Conflict Resolution (eds Aureli F., & de Waal F. B. M., eds.) 155– 169 (University of California Press, 2000).
- Sousa M. B. C., Albuquerque A. C. S. R., Yamamoto M. E., Araújo A. & Arruda M. D. F. in The Smallest Anthropoids 167– 182 (Springer, 2009).
- Yamamoto M. E., de Fátima Arruda M., Alencar A. I., de Sousa M. B. C. & Araújo A. in The Smallest Anthropoids. The Marmoset/Callimico Radiation (eds Ford S. M.,, Porter L. M., & Davis L. C., eds.) 119– 133 (Springer, 2009).
- Goldizen A. W. & Terborgh J. Cooperative polyandry and helping behavior in saddle-backed tamarins (Saguinus fuscicollis). (Canbridge University Press, 1986).
- Hoage R. Parental care in Leontopithecus rosalia rosalia: Sex and age differences in carrying behavior and the role of prior experience. In: The biology and conservation of the Callitrichidae, (ed Kleiman D. G., ed.), 293– 305. Smithsonian Institution Press Washington, DC (1978).
- Pielou E. C. Mathematical Ecology. (Wiley, 1977).
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- Authors
- Burkart, J. M.
- Affiliations
- University of Zurich (CH)
- Corresponding author
- Burkart, Judith M.
- ORCID
- Burkart, Judith M.
- Venue
- Scientific Reports
- Published
- 2015-04-16
- Volume
- 5
- Issue
- 1
- Pages
- 9622-9622
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC4399387
- OpenAlex
- W2012701550
- Cited by
- 24
- References
- 54
- Citations by year
- 2026: 2 · 2025: 1 · 2022: 3 · 2021: 3 · 2020: 1 · 2019: 1 · 2018: 4 · 2017: 6 · 2016: 3
- FWCI
- 7.09
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Topics
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Keywords
- social tolerance, allomaternal care, Callithrix jacchus, cotton-top tamarin, sex differences, cooperative breeding, infant rearing, group composition, rearing experience
- MeSH terms
- Animals, Behavior, Animal, Callithrix, Female, Male, Social Behavior
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