Evolutionary Ecology

, Volume 32, Issue 2–3, pp 215–229 | Cite as

Environmental mismatch results in emergence of cooperative behavior in a passerine bird

  • Ahva L. PotticaryEmail author
  • Renée A. Duckworth
Original Paper


A major problem in the evolution of maternal effects is explaining the origin and persistence of maternally induced phenotypes that lower offspring fitness. Recent work focuses on the relative importance of maternal and offspring selective environments and the mismatch between them. However, an alternative approach is to directly study the origin and performance of offspring phenotypes resulting from mismatch. Here, we capitalize on a detailed understanding of the ecological contexts that provide both the cue and the functional context for expression of maternally induced offspring phenotypes to investigate the consequences of environmental mismatch. In western bluebirds, adaptive integration of offspring dispersal and aggression is induced by maternal competition over nest cavities. When nest cavities are locally abundant, mothers produce nonaggressive offspring that remain in their natal population, and when nest cavities are scarce, mothers produce aggressive dispersers. However, a few offspring neither disperse nor breed locally, instead helping at their parent’s nest, and as a result these offspring have unusually low fitness. Here, we investigate whether females produce helpers to increase their own fitness, or whether helpers result from a mismatch between the cues mothers experience during offspring production and the breeding environment that helpers later encounter. We found that producing helpers does not enhance maternal fitness. Instead, we show that helpers, which were the least aggressive of all returning sons in the population, were most common when population density increased from the time sons were produced to the time of their reproductive maturity, suggesting that the helper phenotype emerges when cues of resource competition during offspring development do not match the actual level of competition that offspring experience. Thus, environmental mismatch might explain the puzzling persistence of maternally induced phenotypes that decrease offspring fitness.


Predictive adaptive response Maternally induced phenotype Competition Aggression 



We thank Alex Badyaev, Erin Morrison, Dawn Higginson, Kelly Hallinger, Anne Storey, Kathryn Chenard, Georgy Semenov, and Chris Seliga for comments that greatly improved the manuscript. We thank Stepfanie Aguillon, Nerissa Hall, Megan Jacobson and numerous field and lab assistants for invaluable help with data collection and processing. Support for this project was provided by NSF DGE-1143953 to ALP and NSF DEB-918095 and DEB-1350107 to RAD).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was carried out in accordance with the recommendations and guidelines approved by University Institutional and Animal Care and Use Committees, as well as complied with all state and federal permitting guidelines for using bluebirds in this study.

Supplementary material

10682_2018_9933_MOESM1_ESM.tif (10 kb)
Supplementary material 1 (TIFF 9 kb)


  1. Aguillon SM, Duckworth RA (2015) Kin aggression and resource availability influence phenotype-dependent dispersal in a passerine bird. Behav Ecol Sociobiol 69(4):625–633. CrossRefGoogle Scholar
  2. Arcese P, Smith JNM (1988) Effects of population density and supplemental food on reproduction in song sparrows. J Anim Ecol 57(1):119–136. CrossRefGoogle Scholar
  3. Austad SN, Rabenold KN (1986) Demography and the evolution of cooperative breeding in the bicolored wren, Campylorhynchus griseus. Behaviour 97:308–324. CrossRefGoogle Scholar
  4. Badyaev AV (2005) Maternal inheritance and rapid evolution of sexual size dimorphism: passive effects or active strategies? Am Nat 166(4):S17–S30. CrossRefPubMedGoogle Scholar
  5. Burgess SC, Marshall DJ (2014) Adaptive parental effects: the importance of estimating environmental predictability and offspring fitness appropriately. Oikos 123(7):769–776. CrossRefGoogle Scholar
  6. Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) (2012) Dispersal ecology and evolution. Oxford University Press, OxfordGoogle Scholar
  7. Cockburn A (1998) Evolution of helping behavior in cooperatively breeding birds. Annu Rev Ecol Syst 29:141–177. CrossRefGoogle Scholar
  8. Crespi B, Semeniuk C (2004) Parent-offspring conflict in the evolution of vertebrate reproductive mode. Am Nat 163(5):635–653. CrossRefPubMedGoogle Scholar
  9. Dickinson JL (2004) A test of the importance of direct and indirect fitness benefits for helping decisions in western bluebirds. Behav Ecol 15(2):233–238. CrossRefGoogle Scholar
  10. Dickinson JL, Akre JJ (1998) Extrapair paternity, inclusive fitness, and within-group benefits of helping in western bluebirds. Mol Ecol 7(1):95–105. CrossRefGoogle Scholar
  11. Dickinson JL, Koenig WD, Pitelka FA (1996) Fitness consequences of helping behavior in the western bluebird. Behav Ecol 7(2):168–177. CrossRefGoogle Scholar
  12. Duckworth RA (2006a) Aggressive behaviour affects selection on morphology by influencing settlement patterns in a passerine bird. Proc R Soc B Biol Sci 273(1595):1789–1795. CrossRefGoogle Scholar
  13. Duckworth RA (2006b) Behavioral correlations across breeding contexts provide a mechanism for a cost of aggression. Behav Ecol 17(6):1011–1019. CrossRefGoogle Scholar
  14. Duckworth RA (2008) Adaptive dispersal strategies and the dynamics of a range expansion. Am Nat 172:S4–S17. CrossRefPubMedGoogle Scholar
  15. Duckworth RA (2009) Maternal effects and range expansion: a key factor in a dynamic process? Philos Trans R Soc B Biol Sci 364(1520):1075–1086. CrossRefGoogle Scholar
  16. Duckworth RA (2013) Human-induced changes in the dynamics of species coexistence: an example with two sister species. In: Gil D, Brumm H (eds) Avian urban ecology: physiological and behavioural adaptations to the urban habitat. Oxford University Press, Oxford, pp 181–191Google Scholar
  17. Duckworth RA, Aguillon SM (2015) Eco-evolutionary dynamics: investigating multiple causal pathways linking changes in behavior, population density and natural selection. J Ornithol 156:S115–S124. CrossRefGoogle Scholar
  18. Duckworth RA, Badyaev AV (2007) Coupling of dispersal and aggression facilitates the rapid range expansion of a passerine bird. Proc Natl Acad Sci USA 104(38):15017–15022. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Duckworth RA, Kruuk LEB (2009) Evolution of genetic integration between dispersal and colonization ability in a bird. Evolution 63(4):968–977. CrossRefPubMedGoogle Scholar
  20. Duckworth RA, Sockman KW (2012) Proximate mechanisms of behavioural inflexibility: implications for the evolution of personality traits. Funct Ecol 26(3):559–566. CrossRefGoogle Scholar
  21. Duckworth RA, Belloni V, Anderson SR (2015) Cycles of species replacement emerge from locally induced maternal effects on offspring behavior in a passerine bird. Science 347(6224):875–877. CrossRefPubMedGoogle Scholar
  22. Duckworth RA, Potticary AL, Badyaev AV (2018) On the origins of adaptive behavioral complexity: developmental channeling of structural trade-offs. Adv Study Behav.
  23. Emlen ST (1982) The evolution of helping. 1. An ecological constraints model. Am Nat 119(1):29–39. CrossRefGoogle Scholar
  24. Ferree ED, Dickinson JL, Kleiber D, Stern CA, Haydock J, Stanback MT et al (2008) Development and cross-species testing of western bluebird (Sialia mexicana) microsatellite primers. Mol Ecol Resour 8(6):1348–1350. CrossRefPubMedGoogle Scholar
  25. Gluckman PD, Hanson MA, Spencer HG, Bateson P (2005) Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies. Proc R Soc B Biol Sci 272(1564):671–677. CrossRefGoogle Scholar
  26. Godfrey KM, Lillycrop KA, Burdge GC, Gluckman PD, Hanson MA (2007) Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease. Pediatr Res 61(5):5R–10R. CrossRefPubMedGoogle Scholar
  27. Green DJ, Cockburn A, Hall ML, Osmond H, Dunn PO (1995) Increased opportunities for cuckoldry may be why dominant male fairy-wrens tolerate helpers. Proc R Soc B Biol Sci 262(1365):297–303. CrossRefGoogle Scholar
  28. Guinan JA, Gowaty PA, Eltzroth EK (2000) Western bluebird (Sialia mexicana). Birds N Am 510:1–31Google Scholar
  29. Hales CN, Barker DJP (1992) Type-2 (non-insuliln dependent) diabetes-mellitus: the thrifty phenotype hypothesis. Diabetologia 35(7):595–601. CrossRefPubMedGoogle Scholar
  30. Jamieson IG (1989) Behavioral heterochrony and the evolution of birds’ helping at the nest: an unselected consequence of communal breeding? Am Nat 133:394–406CrossRefGoogle Scholar
  31. Ketterson ED, Nolan V, Wolf L, Ziegenfus C (1992) Testosterone and avian life histories: effects of experimentally elevated testosterone on behavior and correlates of fitness in the dark-eyed junco (Junco hyemalis). Am Nat 140(6):980–999. CrossRefGoogle Scholar
  32. Keyser AJ, Keyser MT, Promislow DEL (2004) Life-history variation and demography in western bluebirds (Sialia mexicana) in oregon. Auk 121(1):118–133.[0118:lvadiw];2 CrossRefGoogle Scholar
  33. Koenig WD, Dickinson JL (2004) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  34. Komdeur J (1992) Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles warbler. Nature 358(6386):493–495. CrossRefGoogle Scholar
  35. Marshall DJ, Uller T (2007) When is a maternal effect adaptive? Oikos 116:1957–1963CrossRefGoogle Scholar
  36. McGlothlin JW, Jawor JM, Ketterson ED (2007) Natural variation in a testosterone-mediated trade-off between mating effort and parental effort. Am Nat 170(6):864–875. PubMedCrossRefGoogle Scholar
  37. Potticary AL, Dowling JL, Barron DG, Baldassarre DT, Webster MS (2016) Subtle benefits of cooperation to breeding males of the red-backed fairywren. Auk 133(2):286–297. CrossRefGoogle Scholar
  38. Pruett- Jones SG, Lewis MJ (1990) Sex-ratio and habitat limitation promote delayed dispersal in superb fairy-wrens. Nature 348(6301):541–542. CrossRefGoogle Scholar
  39. Ridder ED, Pinxten R, Eens M (2000) Experimental evidence of a testosterone-induced shift from paternal to mating behaviour in a facultatively polygynous songbird. Behav Ecol Sociobiol 49:24–30CrossRefGoogle Scholar
  40. Rossiter M (1998) The role of environmental variation in parental effects expression. In: Mousseau TA, Fox CW (eds) Maternal effects as adaptations. Oxford University Press, Oxford, pp 112–136Google Scholar
  41. Russell AF, Lummaa V (2009) Maternal effects in cooperative breeders: from hymenopterans to humans. Philos Trans R Soc B Biol Sci 364(1520):1143–1167. CrossRefGoogle Scholar
  42. Sheriff MJ, Love OP (2013) Determining the adaptive potential of maternal stress. Ecol Lett 16(2):271–280. CrossRefPubMedGoogle Scholar
  43. Simola DF, Graham RJ, Brady CM, Enzmann BL, Desplan C, Ray A et al (2016) Epigenetic (re)programming of caste-specific behavior in the ant Camponotus floridanus. Science 351(6268):42-U69. CrossRefGoogle Scholar
  44. Uller T (2008) Developmental plasticity and the evolution of parental effects. Trends Ecol Evol 23(8):432–438. CrossRefPubMedGoogle Scholar
  45. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New YorkGoogle Scholar
  46. Zeh DW, Zeh JA (2000) Reproductive mode and speciation: the viviparity-driven conflict hypothesis. BioEssays 22(10):938–946.<938:aid-bies9>;2-9CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA

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