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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Source datasets for this manuscript are available in the Dryad Digital Repository https://doi.org/10.5061/dryad.1gf7803.
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).
Andersson, M. Relatedness and the evolution of conspecific brood parasitism. Am. Nat. 158, 599–614 (2001).
Riehl, C. A simple rule reduces costs of extragroup parasitism in a communally breeding bird. Curr. Biol. 20, 1830–1833 (2010).
Zink, A. G. & Lyon, B. E. Evolution of conspecific brood parasitism versus cooperative breeding as alternative reproductive tactics. Am. Nat. 187, 35–47 (2016).
Lyon, B. E. & Eadie, J. M. A. Conspecific brood parasitism in birds: a life-history perspective. Annu. Rev. Ecol. Syst. 39, 343–363 (2008).
Shizuka, D. & Lyon, B. E. Coots use hatch order to learn to recognize and reject conspecific brood parasitic chicks. Nature 463, 223–226 (2010).
Lemons, P. R. & Sedinger, R. S. Egg size matching by an intraspecific brood parasite. Behav. Ecol. 22, 696–700 (2011).
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).
Baran, N. M. & Reeve, H. K. Coevolution of parental care, parasitic, and resistance efforts in facultative parasitism. Am. Nat. 186, 594–609 (2015).
Nee, S. & May, R. M. Population-level consequences of conspecific brood parasitism in birds and insects. J. Theor. Biol. 161, 95–109 (1993).
Gross, M. R. Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol. Evol. 11, 92–98 (1996).
Lyon, B. E. & Eadie, J. M. in Avian Brood Parasitism: Behavior, Ecology, Evolution, and Coevolution (ed. Soler, M.) 105–124 (Springer, Cham, 2017).
Yom-Tov, Y. & Geffen, E. in Avian Brood Parasitism: Behavior, Ecology, Evolution, and Coevolution (ed. Soler, M.) 95–104 (Springer, Cham, 2017).
Field, J. Intraspecific parasitism as an alternative reproductive tactic in nest-building wasps and bees. Biol. Rev. Camb. Philos. Soc. 67, 79–126 (1992).
Brown, C. R. Laying eggs in a neighbor’s nest: benefit and cost of colonial nesting in swallows. Science 224, 518–519 (1984).
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).
Sorenson, M. D. Parasitic egg-laying in Canvasbacks – frequency, success, and individual behavior. Auk 110, 57–69 (1993).
McRae, S. B. Relative reproductive success of female moorhens using conditional strategies of brood parasitism and parental care. Behav. Ecol. 9, 93–100 (1998).
Åhlund, M. & Andersson, M. Female ducks can double their reproduction. Nature 414, 600–601 (2001).
Lyon, B. E. Egg recognition and counting reduce costs of avian conspecific brood parasitism. Nature 422, 495–499 (2003).
Field, J., Accleton, C. & Foster, W. A. Crozier’s effect and the acceptance of intraspecific brood parasites. Curr. Biol. 28, 3267–3272.e3 (2018).
Davies, N. B. Cuckoos, Cowbirds, and Other Cheats (T. & A. D. Poyser, Glasgow, 2000).
Zink, A. G. Intraspecific brood parasitism as a conditional reproductive tactic in the treehopper Publilia concava. Behav. Ecol. Sociobiol. 54, 406–415 (2003).
Loeb, M. L. G. Evolution of egg dumping in a subsocial insect. Am. Nat. 161, 129–142 (2003).
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).
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).
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).
Jaatinen, K., Lehtonen, J. & Kokko, H. Strategy selection under conspecific brood parasitism: an integrative modeling approach. Behav. Ecol. 22, 144–155 (2011).
Møller, A. P. Intraspecific nest parasitism and antiparasite behavior in swallows, Hirundo rustica. Anim. Behav. 35, 247–254 (1987).
Schielzeth, H. & Bolund, E. Patterns of conspecific brood parasitism in zebra finches. Anim. Behav. 79, 1329–1337 (2010).
Andersson, M. Helping relatives survive and reproduce: inclusive fitness and reproductive value in brood parasitism. Am. Nat. 189, 138–152 (2017).
Riehl, C. & Strong, M. J. Social living without kin discrimination: experimental evidence from a communally breeding bird. Behav. Ecol. Sociobiol. 69, 1293–1299 (2015).
Riehl, C. Evolutionary routes to non-kin cooperative breeding in birds. Proc. R. Soc. Lond. B 280, 20132245 (2013).
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).
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).
Riehl, C. Infanticide and within-clutch competition select for reproductive synchrony in a cooperative bird. Evolution 70, 1760–1769 (2016).
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).
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).
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).
Wang, J. COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol. Ecol. Resour. 11, 141–145 (2011).
Queller, D. C. & Goodnight, K. F. Estimating relatedness using genetic markers. Evolution 43, 258–275 (1989).
Ritland, K. Estimators for pairwise relatedness and individual inbreeding coefficients. Genet. Res. 67, 175–185 (1996).
Wang, J. An estimator for pairwise relatedness using molecular markers. Genetics 160, 1203–1215 (2002).
Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: a Practical Information–Theoretic Approach (Springer Science & Business Media, New York, 2003).
Arnold, T. W. Uninformative parameters and model selection using Akaike’s Information Criterion. J. Wildl. Mgmt. 74, 1175–1178 (2010).
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).
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.
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.
The authors declare no competing interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Extended data figures and tables
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.
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).
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.
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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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