Policing stabilizes construction of social niches in primates

Abstract

All organisms interact with their environment, and in doing so shape it, modifying resource availability. Termed niche construction, this process has been studied primarily at the ecological level with an emphasis on the consequences of construction across generations1. We focus on the behavioural process of construction within a single generation, identifying the role a robustness mechanism2—conflict management—has in promoting interactions that build social resource networks or social niches. Using ‘knockout’ experiments on a large, captive group of pigtailed macaques (Macaca nemestrina), we show that a policing function, performed infrequently by a small subset of individuals3, significantly contributes to maintaining stable resource networks in the face of chronic perturbations that arise through conflict. When policing is absent, social niches destabilize, with group members building smaller, less diverse, and less integrated grooming, play, proximity and contact-sitting networks. Instability is quantified in terms of reduced mean degree, increased clustering, reduced reach, and increased assortativity. Policing not only controls conflict3,4,5, we find it significantly influences the structure of networks that constitute essential social resources in gregarious primate societies. The structure of such networks plays a critical role in infant survivorship6, emergence and spread of cooperative behaviour7, social learning and cultural traditions8.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Schematic showing putative basins of attraction for pigtailed macaque social networks.
Figure 2: Empirically derived grooming and play networks in three conditions.
Figure 3: Reach and assortativity results.

References

  1. 1

    Odling-Smee, F. J., Laland, K. N. & Feldman, M. W. Niche Construction: The Neglected Process in Evolution (Princeton Univ. Press, Princeton, New Jersey, 2003)

    Google Scholar 

  2. 2

    Flack, J. C., Krakauer, D. C. & de Waal, F. B. M. Robustness mechanisms in primate societies: A perturbation study. Proc. R. Soc. Lond. B 272, 1091–1099 (2005)

    Article  Google Scholar 

  3. 3

    Flack, J. C., de Waal, F. B. M. & Krakauer, D. C. Social structure, robustness, and policing cost in a cognitively sophisticated species. Am. Nat. 165, E126–E139 (2005)

    Article  Google Scholar 

  4. 4

    Frank, S. Repression of competition and the evolution of cooperation. Evolution 57, 693–705 (2003)

    PubMed  Google Scholar 

  5. 5

    Boehm, C. in Primate Behavior and Sociobiology (eds Chiarelli, A. B. & Corruccini, R. S.) 161–182 (Springer, New York, 1981)

    Google Scholar 

  6. 6

    Silk, J., Alberts, S. C. & Altmann, J. Social bonds of female baboons enhance infant survival. Science 302, 1231–1234 (2003)

    ADS  CAS  Article  Google Scholar 

  7. 7

    Watts, D. J. Small Worlds: The Dynamics of Networks Between Order and Randomness 199–222 (Princeton Univ. Press, Princeton, New Jersey, 1999)

    Google Scholar 

  8. 8

    Whiten, A., Horner, V. & de Waal, F. B. M. Conformity to cultural norms of tool use in chimpanzees. Nature 437, 737–740 (2005)

    ADS  CAS  Article  Google Scholar 

  9. 9

    Hutchinson, G. E. Concluding remarks. Coldspring Harbor Symp. Quant. Biol. 22, 415–427 (1957)

    Article  Google Scholar 

  10. 10

    de Waal, F. B. M. Primates—A natural heritage of conflict resolution. Science 289, 586–590 (2000)

    ADS  CAS  Article  Google Scholar 

  11. 11

    Krakauer, D. C. Genetic redundancy. In Encyclopedia of the Human Genome Vol. 2, 892–897 (Nature Publishing Group/Wiley, London, 2003)

    Google Scholar 

  12. 12

    Albert, R., Jeong, H. & Barabasi, A. L. Error and attack tolerance in complex networks. Nature 406, 378 (2000)

    ADS  CAS  Article  Google Scholar 

  13. 13

    de Waal, F. B. M. & Luttrell, L. The formal hiearchy of rhesus monkeys: An investigation of the bared-teeth display. Am. J. Primatol. 9, 73–85 (1985)

    Article  Google Scholar 

  14. 14

    Flack, J. C. & de Waal, F. B. M. in Macaque Societies: A Model for the Study of Social Organization (eds Thierry, B., Singh, M. & Kaumanns, W.) 157–181 (Cambridge Univ. Press, Cambridge, UK, 2004)

    Google Scholar 

  15. 15

    Jeong, H., Mason, H. P., Barabasi, A. L. & Oltvai, Z. N. Lethality and centraility in protein networks. Nature 411, 41–42 (2001)

    ADS  CAS  Article  Google Scholar 

  16. 16

    Keppel, G. Design and Analysis: A Researcher's Handbook 329–415 (Prentice Hall, New Jersey, 1991)

    Google Scholar 

  17. 17

    Noe, R. & Hammerstein, P. Biological markets. Trends Ecol. Evol. 10, 336–339 (1995)

    CAS  Article  Google Scholar 

  18. 18

    Wasserman, S. & Faust, K. Social Network Analysis 107–108 (Cambridge Univ. Press, Cambridge, 1994)

    Google Scholar 

  19. 19

    de Waal, F. B. M. Attitudinal reciprocity in food sharing among brown capuchin monkeys. Anim. Behav. 60, 253–261 (2000)

    Article  Google Scholar 

  20. 20

    de Waal, F. B. M. & Luttrell, L. Mechanisms of social reciprocity in three primate species: symmetrical relationships characteristics or cognition? Ethol. Sociobiol. 9, 101–118 (1988)

    Article  Google Scholar 

  21. 21

    Newman, M. E. J. Mixing patterns in networks. Phys. Rev. E 67, 026126 (2003)

    ADS  MathSciNet  CAS  Article  Google Scholar 

  22. 22

    Trivers, R. The evolution of reciprocal altruism. Q. Rev. Biol. 46, 35–57 (1971)

    Article  Google Scholar 

  23. 23

    Watts, D. J. & Strogatz, S. H. Collective dynamics of small-world networks. Nature 393, 1302–1305 (1998)

    Article  Google Scholar 

  24. 24

    Caldecott, J. O. An Ecological and Behavioral Study of the Pigtailed Macaque (Contributions to Primatology, S. Karger, Basel, 1986).

  25. 25

    Thierry, B. in Natural Conflict Resolution (eds Aureli, F. & de Waal, F. B. M.) 106–128 (Univ. California, Berkeley, 2000)

    Google Scholar 

  26. 26

    de Waal, F. B. M. The organization of agonistic social relationships within two captive groups of Java-monkeys (Macaca fasicularis). Z. Tierpsychol. 44, 225–282 (1977)

    CAS  Article  Google Scholar 

  27. 27

    Lusseau, D. & Newman, M. Identifying the role that individual animals play in their social network. Proc. R. Soc. Lond B 271, S477–S481 (2004)

    Article  Google Scholar 

  28. 28

    Freeman, L. C. A set of measures of centrality based upon betweenness. Sociometry 40, 35–41 (1977)

    Article  Google Scholar 

  29. 29

    Altmann, S. Observational study of behaviour: sampling methods. Behaviour 49, 227–267 (1974)

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thank E. Jen, E. Goldberg, J. Miller, E. Smith, D. Erwin, L. Marino, H. Gouzoules, C. Boehm, N. Ay, Y. Sato, M. Morris and J. Padgett for discussions, M. Seres for assistance with the data collection, and the animal care staff at YNPRC. YNPRC is fully accredited by the American Association for Accreditation of Laboratory Animal Care. This work was supported by the Packard Foundation (D.C.K.), the McDonnell Foundation (D.C.K., J.C.F., M.G.), the Wenner-Gren Foundation (J.C.F.), the Proteus Foundation (D.C.K.), the NSF (F.B.M.d.W.) and the NIH (F.B.M.d.W., J.C.F., D.C.K.).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Jessica C. Flack.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

This file contains Supplementary Figure 1 (illustration of social niche, overlapping networks), Supplementary Methods (removal procedure), Supplementary Data (detailed statistical results; analyses of potential nonpolicing functions performed by males; control analyses for removal of low-ranking female), Supplementary Table 1 (reach descriptive results) and Supplementary Notes (random graph generation procedure). (PDF 300 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Flack, J., Girvan, M., de Waal, F. et al. Policing stabilizes construction of social niches in primates. Nature 439, 426–429 (2006). https://doi.org/10.1038/nature04326

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.