Evolutionary Ecology

, Volume 26, Issue 1, pp 43–54 | Cite as

New phylogenetic information suggests both an increase and at least one loss of cooperative breeding during the evolutionary history of Aphelocoma jays

  • Elena C. Berg
  • Robert A. Aldredge
  • A. Townsend Peterson
  • John E. McCormack
Original Paper


Efforts to identify ecological and life history factors associated with cooperative breeding have been largely unsuccessful, and interest is growing in the role of phylogenetic history in determining the distribution of this social system among lineages. In birds, cooperative breeding is distributed non-randomly among lineages, suggesting that phylogenetic inertia may play an important role in determining its distribution. The bird genus Aphelocoma has been particularly well studied because, although it is a relatively small genus, it shows broad among-lineage variation in level of cooperation. Previous analyses described an unusual unidirectional pattern of evolutionary loss of cooperation in Aphelocoma. Here, historical reconstructions based on new phylogenetic data suggest that evolutionary changes in cooperation have been bidirectional, with at least one gain and at least one loss over relatively recent timescales. This result emphasizes that, although history plays an important role in determining the incidence of cooperative breeding, cooperative behavior can switch relatively quickly in evolutionary time and may be influenced by the ecological context within which particular populations are distributed.


Character state reconstruction Phylogenetic history Cooperative breeding Corvidae Maximum likelihood Behavioral evolution 



Elena C. Berg would like to thank Scott Edwards for hosting her in his lab and for many stimulating discussions about the evolution of cooperative breeding in New World jays. Robert A. Aldredge would like to thank Cliff Cunningham for his help with initial ancestral character state reconstructions.


  1. Arnold KE, Owens IPF (1998) Cooperative breeding in birds: a comparative test of the life history hypothesis. Proc R Soc B Biol Sci 265:739–745CrossRefGoogle Scholar
  2. Arnold KE, Owens IPF (1999) Cooperative breeding in birds: the role of ecology. Behav Ecol 10:465–471CrossRefGoogle Scholar
  3. Axelrod D (1979) Age and origin of Sonoran desert vegetation. Occas Pap California Acad Sci 132:1–74Google Scholar
  4. Baglione V, Canestrari D, Marcos Jose M, Griesser M, Ekman J (2002) History, environment and social behaviour: experimentally induced cooperative breeding in the carrion crow. Proc R Soc B Biol Sci 269:1247–1251CrossRefGoogle Scholar
  5. Baglione V, Marcos JM, Canestrari D, Griesser M, Andreotti G, Bardini C, Bogliani G (2005) Does year-round territoriality rather than habitat saturation explain delayed natal dispersal and cooperative breeding in the carrion crow? J Animal Ecol 74:842–851CrossRefGoogle Scholar
  6. Baglione V, Canestrari D, Marcos JM, Ekman J (2006) Experimentally increased food resources in the natal territory promote offspring philopatry and helping in cooperatively breeding carrion crows. Proc R Soc B Biol Sci 273:1529–1535CrossRefGoogle Scholar
  7. Bardwell E, Benkman CW, Gould WR (2001) Adaptive geographic variation in Western Scrub-Jays. Ecology 82:2617–2627CrossRefGoogle Scholar
  8. Beauchamp G (1999) The evolution of communal roosting in birds: origin and secondary losses. Behav Ecol 10:675–687CrossRefGoogle Scholar
  9. Bonaccorso E, Peterson AT (2007) A multilocus phylogeny of New World jay genera. Mol Phylogenet Evol 42:467–476PubMedCrossRefGoogle Scholar
  10. Bonaccorso E, Peterson AT, Navarro-Sigenza AG, Fleischer RC (2010) Molecular systematics and evolution of the Cyanocorax jays. Mol Phylogenet Evol 54:897–909Google Scholar
  11. Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, PrincetonGoogle Scholar
  12. Brown JL (1987) Helping and communal breeding in birds. Princeton University Press, PrincetonGoogle Scholar
  13. Brown JL, Li SH (1995) Phylogeny of social behavior in Aphelocoma jays: a role for hybridization? Auk 112:464–472Google Scholar
  14. Burt DB, Peterson AT (1993) Biology of cooperative-breeding Scrub Jays (Aphelocoma coerulescens) of Oaxaca, Mexico. Auk 110:207–214Google Scholar
  15. Carling MD, Brumfield RT (2008) Haldane’s rule in an avian system: using cline theory and divergence population genetics to test for differential introgression of mitochondrial, autosomal, and sex-linked loci across the Passerina bunting hybrid zone. Evolution 62:2600–2615PubMedCrossRefGoogle Scholar
  16. Clutton-Brock T (2002) Breeding together: Kin selection and mutualism in cooperative vertebrates. Science 296:69–72PubMedCrossRefGoogle Scholar
  17. Cockburn A (1996) Why do so many Australian birds cooperate: social evolution in the Corvida? In: Floyd RB, Sheppard AW, De Barro PJ (eds) Frontiers of population ecology. CSIRO Publishing, Melbourne, pp 451–472Google Scholar
  18. Cockburn A (1998) Evolution of helping behavior in cooperatively breeding birds. Annu Rev Ecol Syst 29:141–177CrossRefGoogle Scholar
  19. Cockburn A (2006) Prevalence of different modes of parental care in birds. Proc R Soc B Biol Sci 273:1375–1383CrossRefGoogle Scholar
  20. Covas R, Griesser M (2007) Life history and the evolution of family living in birds. Proc R Soc B Biol Sci 274:1349–1357CrossRefGoogle Scholar
  21. Cunningham CW, Omland KE, Oakley TH (1998) Reconstructing ancestral character states: a critical reappraisal. Trends Ecol Evol 13:361–366PubMedCrossRefGoogle Scholar
  22. Curry RL, Peterson AT, Langen TA (2002) Western Scrub-Jay (Aphelocoma californica). In: Poole A, Gill F (eds) The birds of North America, No. 712. The American Ornithologists’ Union, Washington, DCGoogle Scholar
  23. Curtis EL, Miller RC (1938) The sclerotic ring in North American birds. Auk 55:225–243Google Scholar
  24. Dow DD (1980) Communally breeding Australian birds with an analysis of distributional and environmental factors. Emu 80:121–140CrossRefGoogle Scholar
  25. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214PubMedCrossRefGoogle Scholar
  26. Du Plessis MA, Siegfried WR, Armstrong AJ (1995) Ecological and life-history correlates of cooperative breeding in South African birds. Oecologia 102:180–188CrossRefGoogle Scholar
  27. Edwards SV, Naeem S (1993) The phylogenetic component of cooperative breeding in perching birds. Am Nat 141:754–789PubMedCrossRefGoogle Scholar
  28. Ekman J, Ericson PGP (2006) Out of Gondwanaland: the evolutionary history of cooperative breeding and social behaviour among crows, magpies, jays and allies. Proc R Soc B Biol Sci 273:1117–1125CrossRefGoogle Scholar
  29. Emlen ST (1982) The evolution of helping. I. An ecological constraints model. Am Nat 119:29–39CrossRefGoogle Scholar
  30. Emlen ST (1991) Evolution of cooperative breeding in birds and mammals. In: Krebs JR, Davies NB (eds) Behavioural ecology: an evolutionary approach. Blackwell Science, Oxford, pp 301–337Google Scholar
  31. Ford HA, Bell H, Nias R, Noske R (1988) The relationship between ecology and the incidence of cooperative breeding in Australian birds. Behav Ecol Sociobiol 22:239–249CrossRefGoogle Scholar
  32. Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768PubMedCrossRefGoogle Scholar
  33. Haldane JBS (1922) Sex ratio and unisexual sterility in animal hybrids. J Genet 12:101–109CrossRefGoogle Scholar
  34. Hamilton WD (1964) The genetical evolution of social behaviour. J Theor Biol 7:1–52PubMedCrossRefGoogle Scholar
  35. Hatchwell BJ (2009) The evolution of cooperative breeding in birds: kinship, dispersal and life history. Philos Trans R Soc B Biol Sci 364:3217–3227CrossRefGoogle Scholar
  36. Huelsenbeck JP, Nielsen R, Bollback JP (2003) Stochastic mapping of morphological characters. Syst Biol 52:131–158PubMedCrossRefGoogle Scholar
  37. Koenig W, Dickinson J (2004) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  38. Komdeur J (1992) Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler. Nature 358:493–495CrossRefGoogle Scholar
  39. Ligon JD, Burt DB (2004) Evolutionary origins. In: Koenig WD, Dickinson J (eds) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge, pp 5–34CrossRefGoogle Scholar
  40. Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis. Version 2.6. Available from
  41. Madge S, Burn H (1994) Crows and jays. Princeton University Press, PrincetonGoogle Scholar
  42. McCormack JE, Brown JL (2008) Mexican jay (Aphelocoma ultramarina). In: Poole A, Gill F (eds) The birds of North America, No. 118. The American Ornithologists’ Union, Washington, DCGoogle Scholar
  43. McCormack JE, Smith TB (2008) Niche expansion leads to small-scale adaptive divergence along an elevation gradient in a medium-sized passerine bird. Proc R Soc B Biol Sci 275:2155–2164CrossRefGoogle Scholar
  44. McCormack JE, Peterson AT, Bonaccorso E, Smith TB (2008) Speciation in the highlands of Mexico: genetic and phenotypic differentiation in the Mexican jay (Aphelocoma ultramarina). Mol Ecol 17:2505–2521PubMedCrossRefGoogle Scholar
  45. McCormack JE, Zellmer AJ, Knowles LL (2010) Does niche divergence accompany allopatric divergence in Aphelocoma jays as predicted under ecological speciation?:insights from tests with niche models. Evolution 64:1231–1244PubMedGoogle Scholar
  46. McCormack JE, Heled J, Delaney K, Peterson AT, Knowles LL (2011) Calibrating divergence times on species trees versus gene trees: implications for speciation history of Aphelocoma jays. Evolution 65:184–202PubMedCrossRefGoogle Scholar
  47. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884PubMedCrossRefGoogle Scholar
  48. Peterson AT (1992a) Phylogeny and rates of molecular evolution In the Aphelocoma jays (Corvidae). Auk 109:133–147Google Scholar
  49. Peterson AT (1992b) Philopatry and genetic differentiation in the Aphelocoma jays (Corvidae). Biol J Linn Soc 47:249–260CrossRefGoogle Scholar
  50. Peterson AT (1993) Adaptive geographic variation of beak shape in Scrub Jays (Aphelocoma coerulescens). Am Nat 142:508–527CrossRefGoogle Scholar
  51. Peterson AT, Burt DB (1992) Phylogenetic history of social evolution and habitat use in the Aphelocoma jays. Anim Behav 44:859–866CrossRefGoogle Scholar
  52. Peterson AT, Vargas-Barajas N (1993) Ecological diversity in scrub jays, Aphelocoma coerulescens. In: Ramamoorthy TP, Bye R, Lot A, Fa J (eds) Biological diversity of Mexico: origins and distribution. Oxford University Press, New York, pp 309–317Google Scholar
  53. Peterson AT, Martinez-Meyer E, Gonzalez-Salazar C (2004) Reconstructing the Pleistocene geography of the Aphelocoma jays (Corvidae). Divers Distrib 10:237–246CrossRefGoogle Scholar
  54. Pitelka FA (1951) Speciation and ecologic distribution in American Jays of the genus Aphelocoma. Univ Calif Publ Zool 50:195–464Google Scholar
  55. Rice NH, Martinez-Meyer E, Peterson AT (2003) Ecological niche differentiation in the Aphelocoma jays: a phylogenetic perspective. Biol J Linn Soc 80:369–383CrossRefGoogle Scholar
  56. Rubenstein DR, Lovette IJ (2007) Temporal environmental variability drives the evolution of cooperative breeding in birds. Curr Biol 17:1414–1419PubMedCrossRefGoogle Scholar
  57. Schluter D, Price T, Mooers A, Ludwig D (1997) Likelihood of ancestor states in adaptive radiation. Evolution 51:1699–1711CrossRefGoogle Scholar
  58. Sherman PW (1988) The levels of analysis. Anim Behav 36:616–619CrossRefGoogle Scholar
  59. Strahl SD, Brown JL (1987) Geographic variation in social structure and behavior of Aphelocoma ultramarina. Condor 89:422–424CrossRefGoogle Scholar
  60. Taborsky M (1994) Sneakers, satellites, and helpers: parasitic and cooperative behavior in fish reproduction. Adv Stud Behav 23:1–100CrossRefGoogle Scholar
  61. Wcislo WT, Danforth BN (1997) Secondarily solitary: the evolutionary loss of social behavior. Trends Ecol Evol 12:468–474PubMedCrossRefGoogle Scholar
  62. Webber T, Brown JL (1994) Natural history of the Unicolored Jay in Chiapas, Mexico. Proc West Found Vertebr Zool 5:135–160Google Scholar
  63. Woolfenden GE, Fitzpatrick JW (1984) The Florida Scrub Jay: demography of cooperative-breeding bird. Princeton University Press, PrincetonGoogle Scholar
  64. Woolfenden GE, Fitzpatrick JW (1996) Florida Scrub-Jay (Aphelocoma coerulescens). In: Poole A, Gill F (eds) The birds of North America, No. 228. The American Ornithologists’ Union, Washington, DCGoogle Scholar
  65. Zusi RL (1987) A feeding adaptation of the jaw articulation in New World jays (Corvidae). Auk 104:665–680Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Elena C. Berg
    • 1
    • 5
  • Robert A. Aldredge
    • 2
  • A. Townsend Peterson
    • 3
  • John E. McCormack
    • 4
  1. 1.Department of Biology IILudwig Maximilian University of MunichPlanegg/MartinsriedGermany
  2. 2.Department of BiologyUNC-Chapel HillChapel HillUSA
  3. 3.Biodiversity InstituteUniversity of KansasLawrenceUSA
  4. 4.Moore Laboratory of ZoologyOccidental CollegeLos AngelesUSA
  5. 5.Animal Ecology, Evolutionary Biology CentreUppsala UniversityUppsalaSweden

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