Abstract
The repayment hypothesis for offspring sex allocation predicts that breeders in cooperatively breeding groups should overproduce the helping sex, particularly when they lack helpers. In birds that produce sexually size-dimorphic nestlings, sex allocation is further predicted to vary across hatching order to maximize brood survival. This could occur by biasing late-hatched nestlings toward either the energetically inexpensive sex (the intra-brood sharing-out hypothesis) or the more competitive sex (the intra-brood competitive equilibrium hypothesis). Here, we test these hypotheses using data from 553 nestlings in 109 broods of greater anis (Crotophaga major), a cooperatively breeding bird that breeds in groups composed of multiple reproductive pairs and non-breeding helpers. Helpers are predominantly males and increase the reproductive output of breeders; late-hatched nestlings are more vulnerable to starvation. Therefore, the repayment hypothesis predicts that groups without helpers should produce male-biased broods, whereas the intra-brood sharing-out and competitive equilibrium hypotheses predict that either females (the energetically inexpensive sex) or males (the more competitive sex), respectively, should be overproduced at the end of the laying sequence. Contrary to these predictions, population-wide sex ratios did not differ significantly from 50:50, and we found no evidence for facultative sex ratio adjustment within broods by helper presence or by hatch order. These results support a growing consensus that facultative sex allocation is less widespread in birds than once thought, even in cooperatively breeding species with sex-biased helping behavior.
Significance statement
Evolutionary biologists have long been interested in offspring sex ratios. Despite a rich body of literature, few clear trends have emerged among the many hypotheses proposed to explain offspring sex biases in birds, and relatively few studies have examined multiple hypotheses or long-term datasets. This study leverages an 11-year dataset on the cooperatively breeding greater ani to address three adaptive hypotheses for offspring sex allocation. However, consistent with recent meta-analyses, we find no support for adaptive sex allocation in line with the predictions of any of the three hypotheses. Facultative adjustment of sex ratios in birds may be more constrained than once thought, even in species in which it is predicted to be adaptive.
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Data availability
The dataset analyzed during the current study is available in the figshare repository, 10.6084/m9.figshare.22816907.
Code availability
The R code used in this study is available in the figshare repository, 10.6084/m9.figshare.21761462.
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Acknowledgements
We are grateful to the Smithsonian Tropical Research Institute for hosting the long-term greater ani project on Barro Colorado Island and for providing logistical support and infrastructure. Meghan J. Strong managed the database and conducted molecular sexing analyses. Oliver Whang, Danielle K. Almstead, Chiti Arvind, Luke Carabbia, Christa Morris, Laura Jara Reyes, Meghan J. Strong, Amanda G. Savagian, Maria G. Smith, and Zachariah Smart assisted with data collection in the field. We also thank Amanda G. Savagian, Maria G. Smith, and Joshua B. LaPergola for comments on earlier drafts of this manuscript. Finally, we thank Bernhard Voelkl and an anonymous reviewer for providing insightful feedback on the manuscript.
Funding
The Smithsonian Tropical Research Institute, the Milton Fund of Harvard University, the Putnam Expedition Fund of the Museum of Comparative Zoology at Harvard University, the Program for Latin American Studies at Princeton University, the High Meadows Environmental Institute at Princeton University, and the National Science Foundation (IOS-1755279; IOS-184543) have supported the long-term monitoring of the greater ani study population via grants to CR. Funding to TCH was provided by Princeton University.
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CR conceived the study, collected field data, conducted genetic sexing, and managed the study system. TCH organized the dataset, conducted statistical analyses, and created figures. Both authors wrote the paper and contributed to the interpretation and presentation of data.
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The research in this study was approved by the Institutional Animal Care and Use Committee of the Smithsonian Tropical Research Institute. Genetic samples were collected and exported with approval from the Ministerio de Ambiente de Panamá and imported to the USA with approval from the US Department of Agriculture. All applicable international, national, and/or institutional guidelines for the use of animals were followed.
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Hendrix, T.C., Riehl, C. No evidence for adaptive sex ratio adjustment in a cooperatively breeding bird with helpful helpers. Behav Ecol Sociobiol 77, 80 (2023). https://doi.org/10.1007/s00265-023-03355-1
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DOI: https://doi.org/10.1007/s00265-023-03355-1