Brood parasitism is a breeding strategy adopted by many species of cuckoos across the world. This breeding strategy influences the evolution of life histories of brood parasite species.In this study, we tested whether the degree on diet specialization is related to the breeding strategy in cuckoo species, by comparing brood parasite and nonparasite species. We measured the gradient of diet specialization of cuckoos, by calculating the Gini coefficient, an index of inequality, on the multiple traits describing the diet of species. The Gini coefficient is a measure of statistical dispersion on a scale between 0 and 1, reflecting a gradient from low to high specialization, respectively. First, we tested the strength of the phylogenetic signal of diet specialization index among cuckoo species worldwide. Then, we ran phylogenetic generalized least square (PGLS) models to compare diet specialization, distribution range, and body mass of parasitic and nonparasitic cuckoo species, considering the phylogenetic signal of data.After adjusting for the phylogenetic signal of the data and considering both, species distribution range and species body mass, brood parasitic cuckoos were characterized by higher diet specialization than nonbrood parasitic species. Brood parasitic species were also characterized by a larger breeding distribution range than nonparasitic species.The findings of this study provide an additional understanding of the cuckoos' ecology, relating diet and breeding strategies, information that could be important in conservation ecology.

Ecologie Systématique Evolution Université Paris Sud CNRS Université Saclay Orsay Cedex France

Faculty of Biological Sciences University of Zielona Góra Zielona Góra Poland

Faculty of Environmental Sciences Department of Applied Geoinformatics and Spatial Planning Czech University of Life Sciences Prague Czech Republic

See more in PubMed

Barnagaud, J. Y. , Devictor, V. , Jiguet, F. , & Archaux, F. (2011). When species become generalists: On‐going large‐scale changes in bird habitat specialization. Global Ecology and Biogeography, 20, 630–640.

Barr, L. M. , Pressey, R. L. , Fuller, R. A. , Segan, D. B. , McDonald‐Madden, E. , & Possingham, H. P. (2011). A new way to measure the world's protected area coverage (M. Perc, Ed.). PLoS ONE, 6(9), e24707). PubMed PMC

Bell, G. P. (1990). Birds and mammals on an insect diet: A primer on diet composition analysis in relation to ecological energetics In Morrison M. L., Ralph C. J., Verner J., & Jehl J. R., Jr. (Eds.), Studies in avian biology, 13. Avian foraging: Theory, methodology, and applications (pp. 416–426). San Diego, CA: Cooper Ornithological Society.

Blomberg, S. P. , & Garland, T. (2003). Tempo and mode in evolution: Phylogenetic inertia, adaptation and comparative methods. Journal of Evolutionary Biology, 15, 899–910.

Blomberg, S. P. , Garland, T. J. , & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57, 717–745. PubMed

Bolnick, D. I. , Svanbäck, R. , Araújo, M. S. , & Persson, L. (2007). Comparative support for the niche variation hypothesis that more generalized populations also are more heterogeneous. Proceedings of the National Academy of Sciences of the United States of America, 104, 10075–10079. PubMed PMC

Bolnick, D. I. , Svanbäck, R. , Fordyce, J. A. , Yang, L. H. , Davis, J. M. , Hulsey, C. D. , & Forister, M. L. (2003). The ecology of individuals: Incidence and implications of individual specialization. American Naturalist, 161, 1–28. PubMed

Burnham, K. P. , & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information‐theoretic approach, 2nd ed Verlag, New York, NY: Springer.

Clavel, J. , Julliard, R. , & Devictor, V. (2011). Worldwide decline of specialist species: Toward a global functional homogenization? Frontiers in Ecology and the Environment, 9, 222–228.

Colles, A. , Liow, L. H. , & Prinzing, A. (2009). Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches. Ecology Letters, 12, 849–863. PubMed PMC

Colwell, F. A. (2011). Measuring inequality. Oxford, UK: Oxford University Press.

Cramp, S. , & Perrins, C. (1994). The birds of the western palearctic. Oxford, UK: Oxford University Press.

Davies, N. B. (2000). Cuckoos, cowbirds and other cheats, 1st ed. London, UK: Poyser.

R Development Core Team. , (2019). R: A language and environment for statistical computing.

Devictor, V. , Clavel, J. , Julliard, R. , Lavergne, S. , Mouillot, D. , Thuiller, W. , … Mouquet, N. (2010). Defining and measuring ecological specialization. Journal of Applied Ecology, 47, 15–25.

Ducatez, S. (2014). Brood parasitism: a good strategy in our changing world? Proceedings of the Royal Society B: Biological Sciences, 281, 20132404. PubMed PMC

Ducatez, S. , Clavel, J. , & Lefebvre, L. (2015). Ecological generalism and behavioural innovation in birds: Technical intelligence or the simple incorporation of new foods? Journal of Animal Ecology, 84, 79–89. PubMed

Ericson, P. G. P. , Anderson, C. L. , Britton, T. , Elzanowski, A. , Johansson, U. S. , Källersjö, M. , … Mayr, G. (2006). Diversification of Neoaves: Integration of molecular sequence data and fossils. Biology Letters, 2, 543–547. PubMed PMC

Erritzøe, J. , Mann, C. F. , Brammer, F. P. , & Fuller, R. A. (2012). Cuckoos of the World, 1st ed London, UK: Christopher Helm Publishers Ltd.

Fox, J. , & Weisberg, S. (2019). An R Companion to Applied Regression. Thirdn: SAGE Publications Inc, Thousand Oaks CA.

Futuyma, D. J. , & Agrawal, A. A. (2009). Evolutionary history and species interactions. Proceedings of the National Academy of Sciences of the United States of America, 106, 18043–18044. PubMed PMC

Garvey, J. E. , & Whiles, M. (2019). Trophic Ecology. Boca Raton, FL: CRC Press.

Gastwirh, J. (1972). The estimation of the lorenz curve and Gini index. The Review of Economics and Statistics, 54, 306–316.

Gini, C. (1921). Measurement of inequality and incomes. The Economic Journal, 31, 124–126.

Harvey, P. H. , & Purvis, A. (1991). Comparative methods for explaining adaptations. Nature, 351, 619–624. PubMed

Irschick, D. , Dyer, L. , & Sherry, T. W. (2005). Phylogenetic methodologies for studying specialization. Oikos, 110, 404–408.

IUCN & BirdLife International . (2017). IUCN 2017. The IUCN Red List of Threatened Species. Version 2016–3. www.iucnredlist.org

Jetz, W. , Carbone, C. , Fulford, J. , & Brown, J. H. (2004). The scaling of animal space use. Science, 306, 266–268. PubMed

Kamilar, J. M. , & Cooper, N. (2013). Phylogenetic singal in primate behaviour, ecology anf life history. Philosophical Transactions of the Royal Society B, 368, 20120341. PubMed PMC

Krüger, O. (2007). Cuckoos, cowbirds and hosts: Adaptations, trade‐offs and constraints. Philosophical Transactions of the Royal Society B, 362, 1873–1886. PubMed PMC

Krüger, O. , & Davies, N. B. (2002). The evolution of cuckoo parasitism: a comparative analysis. Proceedings of the Royal Society of London. Series B: Biological Sciences, 269(1489), 375–381. PubMed PMC

Krüger, O. , Sorenson, M. D. , & Davies, N. B. (2009). Does coevolution promote species richness in parasitic cuckoos? Proceedings of the Royal Society B: Biological Sciences, 276(1674), 3871–3879. PubMed PMC

Lanyon, S. M. (1992). Interspecific brood parasitism in Balckbirds (Icterinae): A phylogenetic perspective. Science, 255, 77–79. PubMed

Lerman, R. I. , & Yitzhaki, S. (1984). A note on the calculation and interpretation of the Gini index. Economic Letters, 15, 363–368.

Maklakov, A. A. , Simpson, S. J. , Zajitschek, F. , Hall, M. D. , Dessmann, J. , Clissold, F. , … Brooks, R. C. (2008). Sex‐specific fitness effects of nutrient intake on reproduction and lifespan. Current Biology, 18, 1062–1066. PubMed

Maldonado, K. , Bozinovic, F. , Newsome, S. D. , & Sabat, P. (2017). Testing the niche variation hypothesis in a community of passerine birds. Ecology, 98, 903–908. PubMed

McKinney, M. (1997). Extinction vulnerability and selectivity: Combining ecological and paleontological views. Annual Review of Ecology and Systematics, 28, 495–516.

Medina, I. , Langmore, N. E. , & Norris, R. (2016). The evolution of host specialisation in avian brood parasites. Ecology Letters, 19, 1110–1118. PubMed

Møller, A. P. (1997). Parasitism and the evolution of host life history In Clayton J. & Moore D. H. (Eds.), Host‐parasite evolution. General principles & avian models, (pp. 105–127.), Oxford, UK: University Press.

Morelli, F. , Benedetti, Y. , Møller, A. P. , & Fuller, R. A. (2019). Measuring avian specialization. Ecology and Evolution, 9, 8378–8386. PubMed PMC

Morelli, F. , Benedetti, Y. , Møller, A. P. , Liang, W. , & Carrascal, L. M. (2018). Cuckoos host range is associated positively with distribution range and negatively with evolutionary uniqueness. Journal of Animal Ecology, 87, 765–773. PubMed

Olsen, A. M. (2015). Exceptional avian herbivores: Multiple transitions toward herbivory in the bird order Anseriformes and its correlation with body mass. Ecology and Evolution, 5, 5016–5032. PubMed PMC

Paradis, E. , Claude, J. , & Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289–290. PubMed

Partridge, L. , & Harvey, P. H. (1985). Evolutionary biology: Costs of reproduction. Nature, 316, 20.

Payne, R. B. (2005). The cuckoos. New York: Oxford University Press.

Pineda‐Munoz, S. , Evans, A. R. , & Alroy, J. (2016). The relationship between diet and body mass in terrestrial mammals. Paleobiology, 42, 659–669.

Revell, L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223.

Revell, L. J. , & Chamberlain, S. A. (2014). Rphylip: an R interface for PHYLIP. Methods in Ecology and Evolution, 5(9), 976–981.

Rothstein, S. I. (1990). A model system for coevolution: Avian brood parasitism. Annual Review of Ecology and Systematics, 25, 481–508.

Rubolini, D. , Liker, A. , Garamszegi, L. Z. , Møller, A. P. , & Saino, N. (2015). Using the BirdTree.org website to obtain robust phylogenies for avian comparative studies: A primer. Current Zoology, 61, 959–965. PubMed PMC

Sam, K. , Koane, B. , Jeppy, S. , Sykorova, J. , & Novotny, V. (2017). Diet of land birds along an elevational gradient in Papua New Guinea. Scientific Reports, 7, 44018. PubMed PMC

Schliep, K. P. (2011). phangorn: Phylogenetic analysis in R. Bioinformatics, 27, 592–593. PubMed PMC

Signorell, A., (2019). DescTools: Tools for descriptive statistics. R package.

Soler, J. J. (1999). Brood parasites: The advantages of being a different species In Adams N. J., & Slotow R. H. (Eds.), Proc. 22 Int. Ornithol. Congr. (ed), (pp. 3098–3106). Johannesburg: BirdLife South Africa.

Terraube, J. , Guixé, D. , & Arroyo, B. (2014). Diet composition and foraging success in generalist predators: Are specialist individuals better foragers? Basic and Applied Ecology, 15, 616–624.

Thomas, F. , Guégan, J. F. , Michalakis, Y. , & Renaud, F. (2000). Parasites and host life‐history traits: Implications for community ecology and species co‐existence. International Journal for Parasitology, 30, 669–674. PubMed

Vázquez, D. P. , & Simberloff, D. (2002). Ecological specialization and susceptibility to disturbance: Conjectures and refutations. The American Naturalist, 159, 606–623. PubMed

Webb, G. J. W. (2008). The dilemma of accuracy in IUCN Red List categories, as exemplified by hawksbill turtles Eretmochelys imbricata. Endangered Species Research, 6, 161–172.

Williams, S. E. , Williams, Y. M. , VanDerWal, J. , Isaac, J. L. , Shoo, L. P. , & Johnson, C. N. (2009). Ecological specialization and population size in a biodiversity hotspot: How rare species avoid extinction. Proceedings of the National Academy of Sciences, 17, 19737–19741. PubMed PMC

Wilman, H. , Belmaker, J. , Simpson, J. , de la Rosa, C. , Rivadeneira, M. M. , & Jetz, W. (2014). EltonTraits 1.0: Species‐level foraging attributes of the world’s birds and mammals. Ecology, 95, 2027.

Woo, K. J. , Elliott, K. H. , Davidson, M. , Gaston, A. J. , & Davoren, G. K. (2008). Individual specialization in diet by a generalist marine predator reflects specialization in foraging behaviour. Journal of Animal Ecology, 77, 1082–1091. PubMed