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

Naturevolume 567pages9699 (2019) | Download Citation

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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Data availability

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

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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.

Author information

Affiliations

  1. Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA

    • Christina Riehl
    •  & Meghan J. Strong

Authors

  1. Search for Christina Riehl in:

  2. Search for Meghan J. Strong in:

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.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Christina Riehl.

Extended data figures and tables

  1. 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).

  2. 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.

  3. 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).

  4. 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.

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

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