Unfavourable environment limits social conflict in Yuhina brunneiceps

Article metrics


Identifying the factors that modulate cooperative and competitive behaviours is the key to understanding social evolution. However, how ecological factors affect social conflict and their fitness consequences remain relatively unexplored. Here, using both a game-theoretical model and empirical data, we show that Taiwan yuhinas (Yuhina brunneiceps)—a joint-nesting species in which group members are unrelated—employ more cooperative strategies in unfavourable environmental conditions. Fighting duration was lower, fewer total eggs were laid and incubation was more likely to start after all females completed egg laying (which causes more synchronous egg hatching). Surprisingly, as a consequence, there were more surviving offspring in unfavourable conditions because the cooperative strategies resulted in fewer dead nestlings. To our knowledge, this study is the first theoretical analysis and empirical study demonstrating that an unfavourable environment reduces social conflict and results in better fitness consequences in social vertebrates.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1: A group of Taiwan yuhinas huddled together.
Figure 2: The effect of hatching order on offspring fitness components.
Figure 3: The effect of timing and rainfall on female tussling durations.
Figure 4: Consequences of rainfall level on yuhina breeding.


  1. 1

    West, S. A., Griffin, A. S. & Gardner, A. Evolutionary explanations for cooperation. Curr. Biol. 17, 661–672 (2007).

  2. 2

    Sachs, J. L., Mueller, U. G., Wilcox, T. P. & Bull, J. J. The evolution of cooperation. Q. Rev. Biol. 79, 135–160 (2004).

  3. 3

    Lehmann, L. & Keller, L. The evolution of cooperation and altruism–a general framework and a classification of models. J. Evol. Biol. 19, 1365–1376 (2006).

  4. 4

    Bourke, A. F. G. Principles of Social Evolution, Oxford University Press, USA, 2011.

  5. 5

    Krause, J. & Ruxton, G. D. Living in Groups, Oxford University Press, 2002.

  6. 6

    Alexander, R. D. The evolution of social behavior. Annu. Rev. Ecol. Syst. 5, 325–383 (1974).

  7. 7

    Emlen, S. T. The evolution of helping I: an ecological constraints model. Am. Nat. 119, 29–39 (1982).

  8. 8

    Jetz, W. & Rubenstein, D. R. Environmental uncertainty and the global biogeography of cooperative breeding in birds. Curr. Biol. 21, 72–78 (2010).

  9. 9

    Rubenstein, D. R. & Lovette, I. J. Temporal environmental variability drives the evolution of cooperative breeding in birds. Curr. Biol. 17, 1414–1419 (2007).

  10. 10

    Hamilton, W. D. Genetical evolution of social behaviour. I.. J. Theor. Biol. 7, 1–16 (1964).

  11. 11

    Maynard Smith, J. & Price, G. R. The logic of animal conflict. Nature 246, 15–18 (1973).

  12. 12

    Axelrod, R. & Hamilton, W. D. The evolution of cooperation. Science 211, 1390–1396 (1981).

  13. 13

    Clutton-Brock, T. H. & Parker, G. A. Punishment in animal societies. Nature 373, 209–216 (1995).

  14. 14

    Ratnieks, F. L. W. & Visscher, P. K. Worker policing in the honeybee. Nature 342, 796–797 (1989).

  15. 15

    Frank, S. A. Mutual policing and repression of competition in the evolution of cooperative groups. Nature 377, 520–522 (1995).

  16. 16

    Gardner, A. & Foster, K. R In Ecology of Social Evolution eds Korb, J., Heinze, J. 1–36 Springer, 2008.

  17. 17

    Korb, J. & Heinze, J. Ecology of Social Evolution, Springer, 2008.

  18. 18

    Reeve, H. K. & Nonacs, P. Social contracts in wasp societies. Nature 359, 823–825 (1992).

  19. 19

    Vehrencamp, S. L. Relative fecundity and parental effort in communally nesting anis, Crotophaga sulcirostris. Science 197, 403–405 (1977).

  20. 20

    Young, A. J. & Clutton-Brock, T. Infanticide by subordinates influences reproductive sharing in cooperatively breeding meerkats. Biol. Lett. 2, 385–387 (2006).

  21. 21

    Yuan, H.- W., Liu, M. & Shen, S.- F. Joint nesting in Taiwan Yuhinas: a rare passerine case. Condor 106, 862–872 (2004).

  22. 22

    Vehrencamp, S. L. & Quinn, J. S. In Ecology and Evolution of Cooperative Breeding in Birds eds Koenig W.D., Dickinson J.L. 177–196 Cambridge University Press, 2004.

  23. 23

    Cant, M. A. A model for the evolution of reproductive skew without reproductive suppression. Anim. Behav. 55, 163–169 (1998).

  24. 24

    Cant, M. A. & Johnstone, R. A. Costly young and reproductive skew in animal societies. Behav. Ecol. 10, 178–184 (1999).

  25. 25

    Shen, S.- F., Reeve, H. K. & Vehrencamp, S. L. Parental care, cost of reproduction and reproductive skew: a general costly young model. J. Theor. Biol. 284, 24–31, (2011).

  26. 26

    Trivers, R. L. In Sexual Selection and the Descent of Man, 1871–1971 ed Campbell B. 136–179 Aldine, 1972.

  27. 27

    Frank, S. A. Foundations of Social Evolution, Princeton University Press, 1998.

  28. 28

    Taylor, P. D. & Frank, S. A. How to make a kin selection model. J. Theor. Biol. 180, 27–37 (1996).

  29. 29

    Taylor, P. D., Wild, G. & Gardner, A. Direct fitness or inclusive fitness: how shall we model kin selection? J. Evol. Biol. 20, 301–309 (2007).

  30. 30

    Reeve, H. K., Emlen, S. T. & Keller, L. Reproductive sharing in animal societies: reproductive incentives or incomplete control by dominant breeders? Behav. Ecol. 9, 267–278 (1998).

  31. 31

    Foster, K. R. Diminishing returns in social evolution: the not-so-tragic commons. J. Evol. Biol. 17, 1058–1072 (2004).

  32. 32

    Godfray, H. C. J. Parasitoids: Behavioral and Evolutionary Ecology, Princeton University Press, 1994.

  33. 33

    Bouwman, K. M. & Komdeur, J. Weather conditions affect levels of extra pair paternity in the reed bunting Emberiza schoeniclus. J. Avian Biol. 37, 238–244 (2006).

  34. 34

    Neal, J. C., James, D. A., Montague, W. G. & Johnson, J. E. Effects of weather and helpers on survival of nestling red-cockaded woodpeckers. Wilson Bull. 105, 666–673 (1993).

  35. 35

    Wilson, G. R., Cooper, S. J. & Gessaman, J. A. The effects of temperature and artificial rain on the metabolism of American kestrels (Falco sparverius). Comp. Biochem. Physiol. A 139, 389–394 (2004).

  36. 36

    Poulsen, B. O. Relationships between frequency of mixed species flocks, weather and insect activity in a montane cloud forest in Ecuador. Ibis 138, 466–470 (1996).

  37. 37

    Hardin, G. The tragedy of the commons. Science 162, 1243–1248 (1968).

  38. 38

    Frank, S. A. Perspective: repression of competition and the evolution of cooperation. Evolution 57, 693–705 (2003).

  39. 39

    Brockhurst, M. A., Buckling, A. & Gardner, A. Cooperation peaks at intermediate disturbance. Curr. Biol. 17, 761–765 (2007).

  40. 40

    Sapolsky, R. M. Endocrine and behavioral correlates of drought in wild olive baboons (Papio anubis). Am. J. Primatol. 11, 217–227 (1986).

  41. 41

    Hsiang, S. M., Meng, K. C. & Cane, M. A. Civil conflicts are associated with the global climate. Nature 476, 438–441 (2011).

  42. 42

    Zhang, Z. et al. Periodic climate cooling enhanced natural disasters and wars in China during AD 10–1900. Proc. R. Soc. Biol. Sci. Ser. B 277, 3745–3753 (2010).

  43. 43

    Burke, M. B., Miguel, E., Satyanath, S., Dykema, J. A. & Lobell, D. B. Warming increases the risk of civil war in Africa. Proc. Natl Acad. Sci. USA 106, 20670–20674 (2009).

  44. 44

    Shen, S.- F. The Ecology of Cooperative Breeding Taiwan Yuhina (Yuhina brunneiceps) in Mayfeng Areas Master thesis thesis, National Taiwan University, (2002).

  45. 45

    Yuan, H.- W., Shen, S.- F., Lin, K.- Y. & Lee, P.- F. Group-slze effects and parental investment strategies during incubation in joint-nesting Taiwan Yuhinas (Yuhina brunneiceps). Wilson Bull. 117, 306–312 (2005).

  46. 46

    Fridolfsson, A. K. & Ellegren, H. A simple and universal method for molecular sexing of non-ratite birds. J. Avian Biol. 30, 116–121 (1999).

  47. 47

    Huang, Y.- J., Chen, C. & Li, S.- H. Polymorphic tetranucleotide microsatellite loci in the Hwamei (Garrulax canorus canorus) (Timaliidae). Mol. Ecol. Notes 4, 170–172 (2004).

  48. 48

    Yeung, C., Huang, Y.- J. & Li, S.- H. Development of polymorphic microsatellite markers for the Steere's Liocichla (Liocichla steerii). Mol. Ecol. Notes 4, 420–422 (2004).

  49. 49

    Wang, M.- T., Hsu, Y.- C., Yao, C.- T. & Li, S.- H. Isolation and characterization of 12 tetranucleotide repeat microsatellite loci from the green-backed tit (Parus monticolus). Mol. Ecol. Notes 5, 439–442 (2005).

Download references


We thank Dustin Rubenstein, Mark Liu and Douglas Mock for helpful comments on early versions of the manuscript. S.-F.S. greatly appreciates the support of Director Wen-Hsiung Li at Academia Sinica, and the advice and support of Stephen Emlen, Sandra Vehrencamp and Kern Reeve during his Ph.D. study at Cornell University. Finally, we thank P.-F. Lee, I.-H. Chang, Sylvester Karimi, Q.-D. Zhong, S.-W. Fu, F.-Y. Huang, C.-J. Chang, Y.-H. Chang, I.-F. Liao, K.-C. Cheng, H.-C. Chen, Z.-N. Yuan, and more than 30 volunteers from the NTU Nature Conservation Students' Club, Department of Life Science and School of Forestry and Resource Conservation and the staffs in Mei-Feng Highland Experimental Farm for their help in the field and lab. This research was funded by the National Science Council of Taiwan (NSC, to H.-W.Y. and S.-F.S.), Academia Sinica, Laboratory of Ornithology, Department of Neurobiology and Behavior and Hu Shih Memorial Award, East Asia Program at Cornell University (to S.-F.S.).

Author information

S.-F.S., S.L.V. and H.-W.Y. designed the study; S.-F.S., H.-C.C., W.-Y.L. and K.-Y.L. performed the field study; and S.-F.S. and S.-F.C. analyzed the data. S.-F.S. and R.A.J. built the models, and S.-F.S., S.L.V., R.A.J. and H.-W.Y. wrote the paper.

Correspondence to Sheng-Feng Shen or Hsiao-Wei Yuan.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Figures

Supplementary Figures S1-S3 (PDF 360 kb)

Supplementary Movie 1

The tussling behavior in yuhinas shown by two females pushing each other to prevent the other from laying eggs. (AVI 3139 kb)

Rights and permissions

Reprints and Permissions

About this article

Further reading


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.