Cover not available
Part of
How the Brain Got Language – Towards a New Road Map
Edited by Michael A. Arbib
[Benjamins Current Topics 112] 2020
► pp. 136–150

From sharing food to sharing information

Cooperative breeding and language evolution

| University of Zurich
| University of Zurich
| University of Zurich
| University of Zurich

Language is a cognitively demanding human trait, but it is also a fundamentally cooperative enterprise that rests on the motivation to share information. Great apes possess many of the cognitive prerequisites for language, but largely lack the motivation to share information. Callitrichids (including marmosets and tamarins) are highly vocal monkeys that are more distantly related to humans than great apes are, but like humans, they are cooperative breeders and all group members help raising offspring. Among primates, this rearing system is correlated with proactive prosociality, which can be expressed as motivation to share information. We therefore propose that the unique coincidence of these two components in humans set the stage for language evolution: The cognitive component inherited from our great ape-like ancestors, and the motivational one added convergently as a result of cooperative breeding. We evaluate this scenario based on a review of callitrichd vocal communication and show that furthermore, they possess many of the mechanistic elements emphasized by the mirror system hypothesis of language evolution. We end by highlighting how more systematic phylogenetic comparisons will enable us to further promote our understanding of the role of cooperative breeding during language evolution.

Keywords: primates, prosociality, marmosets, cooperative breeding, convergence, shared ancestry, information sharing
Article outline
  • 1.Introduction
  • 2.Callitrichid vocal communication
  • 3.Cooperative breeding and vocal complexity?
  • 4.Callitrichid communication and the mirror system hypothesis
  • 5.Towards a new roadmap
  • References
Published online: 11 August 2020
DOI logo
https://doi.org/10.1075/bct.112.10bur
References
Agamaite, J. A., Chang, C. -J., Osmanski, M. S., & Wang, X.
(2015) A quantitative acoustic analysis of the vocal repertoire of the common marmoset (Callithrix jacchus). The Journal of the Acoustical Society of America, 138(5), 2906–2928. DOI logoGoogle Scholar
Arbib, M. A.
(2012) How the brain got language: The mirror system hypothesis (Vol. 16). OUP USA. DOI logoGoogle Scholar
Bardi, M., Petto, A. J., & Lee‐Parritz, D. E.
(2001) Parental failure in captive cotton‐top tamarins (Saguinus Oedipus). American Journal of Primatology, 54(3), 159–169. DOI logoGoogle Scholar
Bezerra, B. M., & Souto, A.
(2008) Structure and usage of the vocal repertoire of Callithrix jacchus . International Journal of Primatolgoy (29), 671–701. DOI logoGoogle Scholar
Borjon, J. I., & Ghazanfar, A. A.
(2014) Convergent evolution of vocal cooperation without convergent evolution of brain size. Brain, Behavior and Evolution, 84(2), 93–102. DOI logoGoogle Scholar
Brown, G. R., Almond, R. E. A., & van Bergen, Y.
(2004) Begging, stealing and offering: food transfer in non-human primates. Advances in the Study of Behaviour, 34, 265–295. DOI logoGoogle Scholar
Burkart, J., Kupferberg, A., Glasauer, S., & van Schaik, C.
(2012) Even simple forms of social learning rely on intention attribution in marmoset monkeys (Callithrix jacchus). Journal of Comparative Psychology, 126(2), 129. DOI logoGoogle Scholar
Burkart, J. M., Allon, O., Amici, F., Fichtel, C., Finkenwirth, C., Heschl, A., … van Schaik, C. P.
(2014) The evolutionary origin of human hyper-cooperation. Nature Communications, 5, 4747.Google Scholar
Burkart, J. M., Hrdy, S. B., & van Schaik, C. P.
(2009) Cooperative breeding and human cognitive evolution. Evolutionary Anthropology, 18, 175–186. DOI logoGoogle Scholar
Burkart, J. M., Schubiger, M. N., & van Schaik, C. P.
(2017) The evolution of general intelligence. Behavioral and Brain Sciences, 1–65.Google Scholar
Burkart, J. M., & van Schaik, C. P.
(2010) Cognitive consequences of cooperative breeding in primates. Animal Cognition, 13, 1–19. DOI logoGoogle Scholar
(2016) The cooperative breeding perspective helps pinning down when uniquely human evolutionary processes are necessary Behavioral and Brain Sciences, 39, e34.Google Scholar
Caine, N. G., Addington, R. L., & Windfelder, T. L.
(1995) Factors affecting the rates of food calls given by red-bellied tamarins. Animal Behaviour, 50(1), 53–60. DOI logoGoogle Scholar
Campbell, M., & Snowdon, C. T.
(2007) Vocal response of captive-reared Saguinus oedipus during mobbing. International Journal of Primatology, 28(2), 257–270. DOI logoGoogle Scholar
Caro, T. M., & Hauser, M. D.
(1992) Is there teaching in nonhuman animals? Quarterly Review of Biology, 67, 151–172. DOI logoGoogle Scholar
Cäsar, C., & Zuberbühler, K.
(2012) Referential alarm calling behaviour in New World primates. Current Zoology, 58(5), 680–697. DOI logoGoogle Scholar
Chisholm, J. S.
(2003) Uncertainty, contingency, and attachment: A life history theory of Theory of Mind. In K. Sterelny & J. Fitness (Eds.), From mating to mentality. Evaluating Evolutionary Psychology. (pp. 125–154). New York: Psychology Press.Google Scholar
Chow, C. P., Mitchell, J. F., & Miller, C. T.
(2015) Vocal turn-taking in a non-human primate is learned during ontogeny. Proc. R. Soc. B, 282(1807), 20150069. DOI logoGoogle Scholar
Clay, Z., Smith, C. L., & Blumstein, D. T.
(2012) Food-associated vocalizations in mammals and birds: what do these calls really mean? Animal Behaviour, 83(2), 323–330. DOI logoGoogle Scholar
Cleveland, J., & Snowdon, C. T.
(1982) The complex vocal repertoire of the adult cotton-top tamarin (Saguinus oedipus oedipus). Zeitschrift für Tierpsychologie, 58, 231–270. DOI logoGoogle Scholar
de la Torre, S., & Snowdon, C. T.
(2009) Dialects in pygmy marmosets? Population variation in call structure. American Journal of Primatology, 71(4), 333–342. DOI logoGoogle Scholar
Dell’Mour, V., Range, F., & Huber, L.
(2009) Social learning and mother’s behavior in manipulative tasks in infant marmosets. American Journal of Primatology, 71(6), 503–509. DOI logoGoogle Scholar
Digby, L. J., Ferrari, S. F., & Saltzman, W.
(2007) Callitrichines: The role of competition in cooperatively breeding species. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. A. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 85–105). New York: Oxford University Press.Google Scholar
Eliades, S. J., & Miller, C. T.
(2016) Marmoset vocal communication: Behavior and neurobiology. Developmental neurobiology.Google Scholar
Elowson, A. M., Snowdon, C. T., & Lazaro-Perea, C.
(1998a) ‘Babbling’ and social context in infant monkeys: parallels to human infants. Trends in Cognitive Sciences, 35–43.Google Scholar
(1998b) Infant ‘babbling’ in a nonhuman primate: complex seqeunces of vocal behavior. Behaviour, 135, 643–664. DOI logoGoogle Scholar
Fitch, W. T.
(2005) The evolution of language: a comparative review. Biology and Philosopy, 20, 193–230. DOI logoGoogle Scholar
Garber, P. A.
(1997) One for all and breeding for one: cooperation and competition as a tamarin reproductive strategy. Evolutionary Anthropology: Issues, News, and Reviews, 5(6), 187–199. DOI logoGoogle Scholar
Grice, H. P.
(1975) Logic and conversation. In P. Cole (Ed.), Syntax and Semantics, Vol 3, (pp. 41–58). New York: Academic Press.Google Scholar
Gros-Louis, J.
(2004) The function of food-associated calls in white-faced capuchin monkeys, Cebus capucinus, from the perspective of the signaller. Animal Behaviour, 67(3), 431–440. DOI logoGoogle Scholar
Guerreiro Martins, E. M., & Burkart, J. M.
(2013) Common marmosets preferentially share difficult to obtain food items. Folia Primatologica, 84(3–5), 281–282.Google Scholar
in prep.). Teaching in marmosets:contingent on age or skill levels of immatures?
Guerreiro Martins, E. M., Moura, A. C., Finkenwirth, C., & Burkart, J. M.
subm). Food sharing in three species of callitrichid monkeys (Callithrix jacchus, Leontopithecus chrysomelas & Sanguinus midas): Individual differences and interspecific variation. Animal Behaviour.
Gultekin, Y. B., & Hage, S. R.
(2017) Limiting parental feedback disrupts vocal development in marmoset monkeys. Nature Communications, 8. DOI logoGoogle Scholar
Hawkes, K.
(2014) Primate sociality to human cooperation. Human Nature, 25(1), 28–48. DOI logoGoogle Scholar
Horn, L., Scheer, C., Bugnyar, T., & Massen, J. J.
(2016) Proactive prosociality in a cooperatively breeding corvid, the azure-winged magpie (Cyanopica cyana). Biology letters, 12(10), 20160649. DOI logoGoogle Scholar
Hrdy, S.
(2005a) Comes the child before the man: how cooperative breeding and prolonged postweaning dependence shaped human potentials. In B. Hewlett & M. Lamb (Eds.), Hunter gatherer childhood. (pp. 65–91). Psicataway: Transactions.Google Scholar
(2005b) Evolutionary context of human development: The cooperative breeding model. In C. S. Carter, L. Ahnert, K. E. Grossmann, S. B. Hrdy, M. E. Lamb, S. W. Porges, & N. Sachser (Eds.), Attachment and Bonding: A New Synthesis; From the 92nd Dahlem Workshop Report (pp. 9–32): MIT Press.Google Scholar
(2009) Mothers & Others: The Evolutionary Origins of Mutual Understanding. Cambridge: Harvard University Press.Google Scholar
Hrdy, S. B.
(2016) Variable postpartum responsiveness among humans and other primates with “cooperative breeding”: A comparative and evolutionary perspective. Hormones and Behavior, 77, 272–283. DOI logoGoogle Scholar
Humle, T., & Snowdon, C. T.
(2008) Socially biased learning in the acquisition of a complex foraging task in juvenile cottontop tamarins (Saguinus oedipus). Animal Behaviour, 27(1), 267–277. DOI logoGoogle Scholar
Jaeggi, A., Burkart, J. M., & van Schaik, C. P.
(2010) On the psychology of cooperation in humans and other primates: The natural history of food sharing and experimental evidence of prosociality. PhilTransB 12(365), 2723–2735.Google Scholar
Kirchhof, J., & Hammerschmidt, K.
(2006) Functionally referential alarm calls in tamarins (Saguinus fuscicollis and Saguinus mystax)–evidence from playback experiments. Ethology, 112(4), 346–354. DOI logoGoogle Scholar
Kitzmann, C. D., & Caine, N. G.
(2009) Marmoset (Callithrix geoffroyi) Food‐Associated Calls are Functionally Referential. Ethology, 115(5), 439–448. DOI logoGoogle Scholar
Kline, M. A.
(2014) How to learn about teaching: An evolutionary framework for the study of teaching behavior in humans and other animals. Behavioral and Brain Sciences, 1–70. DOI logoGoogle Scholar
Kupferberg, A., Glasauer, S., & Burkart, J. M.
(2013) Do robots have goals? How agent cues influence action understanding in non-human primates. Behavioural Brain Research. DOI logoGoogle Scholar
Leighton, G. M.
(2017) Cooperative breeding influences the number and type of vocalizations in avian lineages. Proc. R. Soc. B, 284, 20171508. DOI logoGoogle Scholar
MacLean, E. L., Hare, B., Nunn, C. L., Addessi, E., Amici, F., Anderson, R. C., … Barnard, A. M.
(2014) The evolution of self-control. PNAS, 111(20), E2140–E2148. DOI logoGoogle Scholar
MacLean, E. L., Matthews, L. J., Hare, B., Nunn, C. L., Anderson, R. C., Aureli, F., … Emery, N. J.
(2012) How does cognition evolve? Phylogenetic comparative psychology. Animal Cognition, 15(2), 223–238. DOI logoGoogle Scholar
Masataka, N.
(1982) A field study on the vocalizations of Goeldi’s monkeys (Callimico goeldii). Primates, 23, 206–219. DOI logoGoogle Scholar
McComb, K., & Semple, S.
(2005) Coevolution of vocal communication and sociality in primates. Biology Letters, 1(4), 381–385. DOI logoGoogle Scholar
Melis, A. P., & Warneken, F.
(2016) The psychology of cooperation: Insights from chimpanzees and children. Evolutionary Anthropology, 25(6), 297–305. DOI logoGoogle Scholar
Milward, S. J., Kita, S., & Apperly, I. A.
(2016) Individual differences in children’s co-representation of self and other in joint action. Child Development.Google Scholar
Miss, F. M., & Burkart, J. M.
(2018) Corepresentation During Joint Action in Marmoset Monkeys (Callithrix jacchus). Psychological Science. DOI logo.Google Scholar
Moura, A. C., Nunes, H. G., & Langguth, A.
(2010) Food Sharing in Lion Tamarins (Leontopithecus chrysomelas): Does Foraging Difficulty Affect Investment in Young by Breeders and Helpers? International Journal of Primatology, 31(5), 848–862. DOI logoGoogle Scholar
Noble, J.
(2000) Cooperation, competition and the evolution of prelinguistic communication. The Emergence of Language, 40–61. DOI logoGoogle Scholar
Pistorio, A. L., Vintch, B., & Wang, X.
(2006) Acoustic analysis of vocal development in a New World primate, the common marmoet (Callithrix jacchus). J Aocust Soc Am, 120(3), 1655–1670. DOI logoGoogle Scholar
Pollick, A. S., Gouzoules, H., & de Waal, F. B. M.
(2005) Audience effects on food calls in captive brown capuchin monkeys, Cebus apella . Animal Behaviour, 70, 1273–1281. DOI logoGoogle Scholar
Rapaport, L. G.
(2011) Progressive parenting behavior in wild golden lion tamarins. Behavioral Ecology. DOI logoGoogle Scholar
Roupe, S. L., Pistorio, A., & Wang, X.
(2003) Vocal plasticity induced by auditory deprivation in the common marmoset. Paper presented at the Society for Neuroscience, New Orleans, Nov. 11.
Roy, S., Miller, C. T., Gottsch, D., & Wang, X.
(2011) Vocal control by the common marmoset in the presence of interfering noise. The Journal of Experimental Biology, 214(21), 3619–3629. DOI logoGoogle Scholar
Ruch, H., Zürcher, Y., & Burkart, J. M.
(2018) The function of vocal accommodation in humans and other primates. Biological Reviews, 93(2), 996–1013. DOI logoGoogle Scholar
Rukstalis, M., Fite, J. E., & French, J. A.
(2003) Social Change Affects Vocal Structure in a Callitrichid Primate (Callithrix kuhlii). Ethology, 109(4), 327–340. DOI logoGoogle Scholar
Rukstalis, M., & French, J. A.
(2005) Vocal buffering of the stress response: exposure to conspecific vocalizations moderates urinary cortisol excretion in isolated marmosets. Hormones and Behavior, 47(1), 1–7. DOI logoGoogle Scholar
Shelley, E. L. & Blumstein, D. T.
(2004) The evolution of vocal alarm communication in rodents. Behavioral Ecology, 16(1), 169–77. DOI logoGoogle Scholar
Sebanz, N., Knoblich, G., & Prinz, W.
(2003) Representing others’ actions: just like one’s own? Cognition, 88(3), B11–B21. DOI logoGoogle Scholar
Snowdon, C. T.
(2013) Language parallels in New World primates Animal Models of Speech and Language Disorders (pp. 241–261). New York: Springer. DOI logoGoogle Scholar
(2001) Social processes in communication and cognition in callitrichid monkeys: a review. Animal Cognition, 4, 247–257. DOI logoGoogle Scholar
(2017a) Cultural Phenomena in Cooperatively Breeding Primates. In J. M. Causadias, E. H. Telzer, & N. A. Gonzales (Eds.), The Handbook of Culture and Biology: John Wiley & Sons. DOI logoGoogle Scholar
(2017b) Learning from monkey “talk”. Science, 355(6330), 1120–1122. DOI logoGoogle Scholar
(2017c) Vocal Communication in Family-Living and Pair-Bonded Primates Primate Hearing and Communication (pp. 141–174): Springer. DOI logoGoogle Scholar
Snowdon, C. T., & Cleveland, J.
(1984) “Conversations” among pygmy marmosets. American Journal of Primatology 7, 15–20. DOI logoGoogle Scholar
Snowdon, C. T., & Cronin, K. A.
(2007) Cooperative breeders do cooperate. Behavioural Processes, 76(2), 138–141. DOI logoGoogle Scholar
Snowdon, C. T., & Elowson, A. M.
(2001) ‘Babbling’ in pygmy marmosets: development after infancy. Behaviour, 138(10), 1235–1248. DOI logoGoogle Scholar
Snowdon, C. T., & Roskos, T. R.
(2017) Stick-weaving: Innovative behavior in tamarins (Saguinus oedipus). Journal of Comparative Psychology, 131(2), 174. DOI logoGoogle Scholar
Solomon, N. G., & French, J. A.
(1997) Cooperative Breeding in Mammals. New York: Cambridge University Press.Google Scholar
Suzuki, W., Banno, T., Miyakawa, N., Abe, H., Goda, N., & Ichinohe, N.
(2015) Mirror neurons in a new world monkey, common marmoset. Frontiers in neuroscience, 9. DOI logoGoogle Scholar
Takahashi, D. Y., Fenley, A. R., & Ghazanfar, A. A.
(2016) Early development of turn-taking with parents shapes vocal acoustics in infant marmoset monkeys. Phil. Trans. B, 371(1693), 20150370. DOI logoGoogle Scholar
Takahashi, D. Y., Fenley, A. R., Teramoto, Y., Narayanan, D. Z., Borjon, J. I., Holmes, P., & Ghazanfar, A. A.
(2015) The developmental dynamics of marmoset monkey vocal production. Science, 349(6249), 734–738. DOI logoGoogle Scholar
Takahashi, D. Y., Liao, D. A., & Ghazanfar, A. A.
(2017) Vocal Learning via Social Reinforcement by Infant Marmoset Monkeys. Current Biology. DOI logoGoogle Scholar
Takahashi, D. Y., Narayanan, D. Z., & Ghazanfar, A. A.
(2013) Coupled oscillator dynamics of vocal turn-taking in monkeys. Current Biology, 23(21), 2162–2168. DOI logoGoogle Scholar
Tomasello, M.
(2017) What did we learn from the ape language studies?. In: Hare, B. & Yamamoto, S. (eds.) Bonobos: Unique in Mind, Brain, and Behavior. Oxford: Oxford University Press, 95–105Google Scholar
(2008) Origins of human communication. Cambridge MA: MIT Press. DOI logoGoogle Scholar
Tomasello, M., & Gonzalez-Cabrera, I.
(2017) The role of ontogeny in the evolution of human cooperation. Human Nature, 1–15.Google Scholar
Vitale, A., Zanzoni, M., Queyras, A., & Chiarotti, F.
(2003) Degree of social contact affects the emission of food calls in the common marmoset (Callithrix jacchus) . American Journal of Primatology, 59, 21–28. DOI logoGoogle Scholar
Voelkl, B., & Huber, L.
(2007) Imitation as faithful copying of a novel techinque in marmoset monkeys. PLoS ONE, 2(7), e611. DOI logoGoogle Scholar
Weiss, D. J., Garibaldi, B. T., & Hauser, M. D.
(2001) The production and perception of long calls by cotton-top tamarins (Saguinus oedipus): acoustic analyses and playback experiments. Journal of Comparative Psychology, 115(3), 258. DOI logoGoogle Scholar
Wen, T., & Hsieh, S.
(2015) Neuroimaging of the joint Simon effect with believed biological and non-biological co-actors. Frontiers in human neuroscience, 9. DOI logoGoogle Scholar
Zuberbühler, K.
(2011) Cooperative breeding and the evolution of vocal flexibility. In M. Tallerman & K. Gibson (Eds.), The Oxford Handbook of Language Evolution.Google Scholar
Zürcher, Y., & Burkart, J. M.
(2017) Evidence for dialects in three captive populations of common marmosets (Callithrix jacchus). International Journal of Primatolgoy, 38(4), 780–793. DOI logoGoogle Scholar
in prep). Translocation experiments provide evidence for vocal accommodation learing in marmosets.
Cited by

Cited by 1 other publications

Griebel, Ulrike & D. Kimbrough Oller
2024. From emotional signals to symbols. Frontiers in Psychology 15 DOI logo

This list is based on CrossRef data as of 15 april 2024. Please note that it may not be complete. Sources presented here have been supplied by the respective publishers. Any errors therein should be reported to them.