Social parasitism as an alternative reproductive tactic in a cooperatively breeding cuckoo

Abstract

Cooperatively nesting birds are vulnerable to social parasites that lay their eggs in host nests but provide no parental care1,2,3,4. Most previous research has focused on the co-evolutionary arms race between host defences and the parasites that attempt to circumvent them5,6,7,8,9, but it remains unclear why females sometimes cooperate and sometimes parasitize, and how parasitic tactics arise in cooperative systems10,11,12. Here we show that cooperative and parasitic reproductive strategies result in approximately equal fitness pay-offs in the greater ani (Crotophaga major), a long-lived tropical cuckoo, using an 11-year dataset and comprehensive genetic data that enable comparisons of the life-histories of individual females. We found that most females in the population nested cooperatively at the beginning of the breeding season; however, of those birds that had their first nests destroyed, a minority subsequently acted as reproductive parasites. The tendency to parasitize was highly repeatable, which indicates individual specialization. Across years, the fitness pay-offs of the two strategies were approximately equal: females who never parasitized (a ‘pure cooperative’ strategy) laid larger clutches and fledged more young from their own nests than did birds that both nested and parasitized (a ‘mixed’ strategy). Our results suggest that the success of parasites is constrained by reproductive trade-offs as well as by host defences, and illustrate how cooperative and parasitic tactics can coexist stably in the same population.

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Fig. 1: Attributes of eggs laid by hosts and parasites.
Fig. 2: Mean annual reproductive output of females practicing pure cooperative versus mixed strategies.

Data availability

Source datasets for this manuscript are available in the Dryad Digital Repository https://doi.org/10.5061/dryad.1gf7803.

References

  1. 1.

    Emlen, S. T. & Wrege, P. H. Forced copulations and intraspecific parasitism: two costs of social living in the white-fronted bee-eater. Ethology 71, 2–29 (1986).

    Google Scholar 

  2. 2.

    Andersson, M. Relatedness and the evolution of conspecific brood parasitism. Am. Nat. 158, 599–614 (2001).

    CAS  PubMed  Google Scholar 

  3. 3.

    Riehl, C. A simple rule reduces costs of extragroup parasitism in a communally breeding bird. Curr. Biol. 20, 1830–1833 (2010).

    CAS  PubMed  Google Scholar 

  4. 4.

    Zink, A. G. & Lyon, B. E. Evolution of conspecific brood parasitism versus cooperative breeding as alternative reproductive tactics. Am. Nat. 187, 35–47 (2016).

    PubMed  Google Scholar 

  5. 5.

    Lyon, B. E. & Eadie, J. M. A. Conspecific brood parasitism in birds: a life-history perspective. Annu. Rev. Ecol. Syst. 39, 343–363 (2008).

    Google Scholar 

  6. 6.

    Shizuka, D. & Lyon, B. E. Coots use hatch order to learn to recognize and reject conspecific brood parasitic chicks. Nature 463, 223–226 (2010).

    ADS  CAS  PubMed  Google Scholar 

  7. 7.

    Lemons, P. R. & Sedinger, R. S. Egg size matching by an intraspecific brood parasite. Behav. Ecol. 22, 696–700 (2011).

    Google Scholar 

  8. 8.

    Wang, L. et al. Increase of clutch size triggers clutch destruction behavior in common moorhens (Gallinula chloropus) during the incubation period. Behaviour 150, 215–223 (2013).

    Google Scholar 

  9. 9.

    Baran, N. M. & Reeve, H. K. Coevolution of parental care, parasitic, and resistance efforts in facultative parasitism. Am. Nat. 186, 594–609 (2015).

    PubMed  Google Scholar 

  10. 10.

    Nee, S. & May, R. M. Population-level consequences of conspecific brood parasitism in birds and insects. J. Theor. Biol. 161, 95–109 (1993).

    Google Scholar 

  11. 11.

    Gross, M. R. Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol. Evol. 11, 92–98 (1996).

    CAS  PubMed  Google Scholar 

  12. 12.

    Lyon, B. E. & Eadie, J. M. in Avian Brood Parasitism: Behavior, Ecology, Evolution, and Coevolution (ed. Soler, M.) 105–124 (Springer, Cham, 2017).

  13. 13.

    Yom-Tov, Y. & Geffen, E. in Avian Brood Parasitism: Behavior, Ecology, Evolution, and Coevolution (ed. Soler, M.) 95–104 (Springer, Cham, 2017).

  14. 14.

    Field, J. Intraspecific parasitism as an alternative reproductive tactic in nest-building wasps and bees. Biol. Rev. Camb. Philos. Soc. 67, 79–126 (1992).

    Google Scholar 

  15. 15.

    Brown, C. R. Laying eggs in a neighbor’s nest: benefit and cost of colonial nesting in swallows. Science 224, 518–519 (1984).

    ADS  CAS  PubMed  Google Scholar 

  16. 16.

    Nielsen, C. R., Parker, P. G. & Gates, R. J. Intraspecific nest parasitism of cavity-nesting wood ducks: costs and benefits to hosts and parasites. Anim. Behav. 72, 917–926 (2006).

    Google Scholar 

  17. 17.

    Sorenson, M. D. Parasitic egg-laying in Canvasbacks – frequency, success, and individual behavior. Auk 110, 57–69 (1993).

    Google Scholar 

  18. 18.

    McRae, S. B. Relative reproductive success of female moorhens using conditional strategies of brood parasitism and parental care. Behav. Ecol. 9, 93–100 (1998).

    Google Scholar 

  19. 19.

    Åhlund, M. & Andersson, M. Female ducks can double their reproduction. Nature 414, 600–601 (2001).

    ADS  PubMed  Google Scholar 

  20. 20.

    Lyon, B. E. Egg recognition and counting reduce costs of avian conspecific brood parasitism. Nature 422, 495–499 (2003).

    ADS  CAS  Google Scholar 

  21. 21.

    Field, J., Accleton, C. & Foster, W. A. Crozier’s effect and the acceptance of intraspecific brood parasites. Curr. Biol. 28, 3267–3272.e3 (2018).

    CAS  PubMed  Google Scholar 

  22. 22.

    Davies, N. B. Cuckoos, Cowbirds, and Other Cheats (T. & A. D. Poyser, Glasgow, 2000).

    Google Scholar 

  23. 23.

    Zink, A. G. Intraspecific brood parasitism as a conditional reproductive tactic in the treehopper Publilia concava. Behav. Ecol. Sociobiol. 54, 406–415 (2003).

    Google Scholar 

  24. 24.

    Loeb, M. L. G. Evolution of egg dumping in a subsocial insect. Am. Nat. 161, 129–142 (2003).

    PubMed  Google Scholar 

  25. 25.

    Riehl, C. Living with strangers: direct benefits favour non-kin cooperation in a communally nesting bird. Proc. R. Soc. Lond. B 278, 1728–1735 (2011).

    Google Scholar 

  26. 26.

    Riehl, C. & Jara, L. Natural history and reproductive biology of the communally breeding Greater Ani (Crotophaga major) at Gatún Lake, Panama. Wilson J. Ornithol. 121, 679–687 (2009).

    Google Scholar 

  27. 27.

    Almany, G. R. et al. Permanent genetic resources added to molecular ecology resources database 1 May 2009–31 July 2009. Mol. Ecol. Resour. 9, 1460–1466 (2009).

    CAS  PubMed  Google Scholar 

  28. 28.

    Jaatinen, K., Lehtonen, J. & Kokko, H. Strategy selection under conspecific brood parasitism: an integrative modeling approach. Behav. Ecol. 22, 144–155 (2011).

    Google Scholar 

  29. 29.

    Møller, A. P. Intraspecific nest parasitism and antiparasite behavior in swallows, Hirundo rustica. Anim. Behav. 35, 247–254 (1987).

    Google Scholar 

  30. 30.

    Schielzeth, H. & Bolund, E. Patterns of conspecific brood parasitism in zebra finches. Anim. Behav. 79, 1329–1337 (2010).

    Google Scholar 

  31. 31.

    Andersson, M. Helping relatives survive and reproduce: inclusive fitness and reproductive value in brood parasitism. Am. Nat. 189, 138–152 (2017).

    PubMed  Google Scholar 

  32. 32.

    Riehl, C. & Strong, M. J. Social living without kin discrimination: experimental evidence from a communally breeding bird. Behav. Ecol. Sociobiol. 69, 1293–1299 (2015).

    Google Scholar 

  33. 33.

    Riehl, C. Evolutionary routes to non-kin cooperative breeding in birds. Proc. R. Soc. Lond. B 280, 20132245 (2013).

    Google Scholar 

  34. 34.

    Strong, M. J., Sherman, B. L. & Riehl, C. Home field advantage, not group size, predicts outcomes of inter-group conflicts in a social bird. Anim. Behav. 143, 205–213 (2017).

    Google Scholar 

  35. 35.

    Riehl, C. & Strong, M. J. Stable social relationships between unrelated females increase individual fitness in a cooperative bird. Proc. R. Soc. Lond. B 285, 20180130 (2018).

    Google Scholar 

  36. 36.

    Riehl, C. Infanticide and within-clutch competition select for reproductive synchrony in a cooperative bird. Evolution 70, 1760–1769 (2016).

    PubMed  Google Scholar 

  37. 37.

    Riehl, C. Parental care and reproductive skew in a communally breeding cuckoo: hard-working males do not sire more young. Anim. Behav. 84, 707–714 (2012).

    Google Scholar 

  38. 38.

    Schmaltz, G., Somers, C. M., Sharma, P. & Quinn, J. S. Non-destructive sampling of maternal DNA from the external shell of bird eggs. Conserv. Genet. 7, 543–549 (2006).

    CAS  Google Scholar 

  39. 39.

    Strausberger, B. M. & Ashley, M. V. Eggs yield nuclear DNA from egg-laying female cowbirds, their embryos and offspring. Conserv. Genet. 2, 385–390 (2001).

    CAS  Google Scholar 

  40. 40.

    Wang, J. COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol. Ecol. Resour. 11, 141–145 (2011).

    PubMed  Google Scholar 

  41. 41.

    Queller, D. C. & Goodnight, K. F. Estimating relatedness using genetic markers. Evolution 43, 258–275 (1989).

    PubMed  Google Scholar 

  42. 42.

    Ritland, K. Estimators for pairwise relatedness and individual inbreeding coefficients. Genet. Res. 67, 175–185 (1996).

    Google Scholar 

  43. 43.

    Wang, J. An estimator for pairwise relatedness using molecular markers. Genetics 160, 1203–1215 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: a Practical Information–Theoretic Approach (Springer Science & Business Media, New York, 2003).

    Google Scholar 

  45. 45.

    Arnold, T. W. Uninformative parameters and model selection using Akaike’s Information Criterion. J. Wildl. Mgmt. 74, 1175–1178 (2010).

    Google Scholar 

  46. 46.

    Nakagawa, S. & Schielzeth, H. A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142 (2013).

    Google Scholar 

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Acknowledgements

We thank C. Arvind, L. Carabbia, L. Jara, A. Savagian, Z. Smart, J. Touchton and W. Webber for assistance in the field, and E. Jiang and M. Smith for assistance in the laboratory. We are grateful to S. Bogdanowicz and the Cornell Laboratory of Ornithology for support in genotyping and in developing genetic markers, and to the Smithsonian Tropical Research Institute for their continued support of the Barro Colorado Island field station. Z. Volenec assisted with the preparation of Figs. 1, 2. D. T. Baldassarre, M. E. Hauber, D. I. Rubenstein and A. G. Savagian provided comments on earlier drafts and presentations of this work. Funding for this project was provided by the Smithsonian Tropical Research Institute, the Harvard Society of Fellows, the William F. Milton Fund at Harvard University, the Department of Ecology and Evolutionary Biology at Princeton University, the Program in Latin American Studies at Princeton University and the Princeton Environmental Institute at Princeton University.

Reviewer information

Nature thanks John M. Eadie, Dai Shizuka, Andrew G. Zink and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Contributions

C.R. conceived the project, conducted the statistical analyses and wrote the manuscript with input from M.J.S., who conducted spatial analyses and managed the database. Both C.R. and M.J.S. collected field data and performed genetic analyses.

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Correspondence to Christina Riehl.

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Extended data figures and tables

Extended Data Fig. 1 Genetic relatedness between hosts and parasites.

Distributions of relatedness values between host and parasite females (black bars, n = 111 dyads) and all possible dyads of females in the study population (white bars, n = 221,736 dyads).

Extended Data Fig. 2 Cumulative frequency distribution of relatedness values between hosts and parasites.

Difference of average relatedness values between host–parasite dyads (n = 111 dyads) and randomly selected dyads from all possible dyads of females in the study population (n = 221,736 dyads), obtained by bootstrapping (1,000 bootstraps). Because the observed difference in mean relatedness values between host–parasite dyads and randomly selected dyads (r = 0.00131, vertical black bar) lies between the 5th and 95th percentiles of the distribution obtained by bootstrapping, this difference was not significant at α = 0.05.

Extended Data Fig. 3 Distributions of distances between host and parasite nests.

Distributions of linear distances (in km) between parasite nests (that is, failed nests at which a female subsequently acted as a parasite) and host nests that were parasitized (black bars, n = 60 dyads); and between parasite nests and all other nests in the study area (white bars, n = 1,762 dyads).

Extended Data Fig. 4 Mean distances between host and parasite nests.

Box-and-whisker plots of linear distances (in km) between parasite nests (that is, failed nests at which a female subsequently acted as a parasite) and host nests that were parasitized (n = 60 dyads) and between parasite nests and all other nests in the study area (n = 1762 dyads). Boxes represent interquartile ranges, horizontal lines indicate the median and whiskers extend to lowest and highest values. Mixed-effects logistic regression predicting likelihood of being parasitized (controlling for year and group identity); two-tailed Wald test for linear distance as predictor, P = 0.0001.

Extended Data Table 1 Model selection for predictors of the likelihood of a female acting as a parasite
Extended Data Table 2 Model selection for predictors of the probability of a host nest being parasitized
Extended Data Table 3 Sample sizes of sources of genetic material used in the maternity assignment of eggs

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Riehl, C., Strong, M.J. Social parasitism as an alternative reproductive tactic in a cooperatively breeding cuckoo. Nature 567, 96–99 (2019). https://doi.org/10.1038/s41586-019-0981-1

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