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Climate change and coevolution in the cuckoo–reed warbler system

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Abstract

The evolution of traits in hosts may be influenced by their parasites and vice versa and a coevolutionary arms race often develops between the two. As part of such an arms race, the common cuckoo mimics the eggs of its hosts to avoid egg rejection. Traits related to this arms race may also be influenced by climatic conditions, such as temperature, affecting, for example, food availability and, thus, female condition and egg size (therefore may reflect Bergmann’s rule or the resource rule). The potential interaction between coevolution and climate has rarely been studied. We investigated whether egg and body size of cuckoos and reed warblers from Britain and Denmark had undergone change between 1868 and 1956, and whether such changes were correlated with climatic factors. Cuckoo egg size decreased during the studied period while warbler egg size remained stable. Hence, cuckoo and warbler eggs have become more similar in size over time. Cuckoo egg volume decreased with increasing annual precipitation, but annual precipitation decreased over time. Warbler egg volume increased with spring temperatures (which could not reflect Bergmann’s rule, but may support the resource rule). Hence, it seems that the measured climatic indices did not affect cuckoo egg size but may in part affect warbler egg size. Therefore, the decrease in cuckoo egg size may be the result of the coevolutionary arms race. Body and egg sizes in the cuckoos were negatively correlated whereas warbler body and egg sizes were uncorrelated, suggesting that selection probably acted on egg size directly and not via selection on body size. Taken together, these findings may indicate that climate change, the coevolutionary arms race, or both, affected egg sizes. It is suggested that drawing conclusions regarding the arms race without taking into account other selective pressures (e.g., climate) may confound conclusions regarding parasite-host systems.

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References

  • Anderson MG, Moskát C, Bán M et al (2009) Egg eviction imposes a recoverable cost of virulence in chicks of a brood parasite. PLoS ONE 4:e7725

    Article  PubMed Central  PubMed  Google Scholar 

  • Avilés JM, Stokke BG, Moksnes A et al (2006a) Environmental conditions influence egg color of reed warblers Acrocephalus scirpaceus and their parasite, the common cuckoo Cuculus canorus. Behav Ecol Sociobiol 61:475–485

    Article  Google Scholar 

  • Avilés JM, Stokke BG, Moksnes A et al (2006b) Rapid increase in cuckoo egg matching in a recently parasitized reed warbler population. J Evol Biol 19:1901–1910

    Article  PubMed  Google Scholar 

  • Avilés JM, Vikan JR, Fossøy F et al (2012) Egg phenotype matching by cuckoos in relation to discrimination by hosts and climatic conditions. Proc R Soc B 279:1967–1976

    Article  PubMed Central  PubMed  Google Scholar 

  • Bańbura M, Sulikowska-Drozd A, Kaliński A et al (2010) Egg size variation in blue tits Cyanistes caeruleus and great tits Parus major in relation to habitat differences in snail abundance. Acta Ornithol 45:121–129

    Article  Google Scholar 

  • Bell C (1996) The relationship between geographic variation in clutch size and migration pattern in the Yellow Wagtail. Bird Study 43:333–341

    Article  Google Scholar 

  • Blaise M (1965) Contribution à l’étude de la reproduction du Coucou gris Cuculus canorus dans le nord-est de la France. L’Oiseau et R F O 35:87–116

    Google Scholar 

  • Blueweiss L, Fox H, Kudzma V et al (1978) Relationships between body size and some life history parameters. Oecologia 37:257–272

    Article  Google Scholar 

  • Bolton M, Monaghan P, Houston DC (1993) Proximate determination of clutch size in Lesser black-backed gulls: the roles of food supply and body condition. Can J Zool 71:273–279

    Article  Google Scholar 

  • Brooke MDL, Davies NB (1987) Recent changes in host usage by cuckoos. J Anim Ecol 56:873–883

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference : a practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Canale CI, Henry PY (2010) Adaptive phenotypic plasticity and resilience of vertebrates to increasing climatic unpredictability. Clim Res 43:135–147

    Article  Google Scholar 

  • Cherry MI, Bennett ATD, Moskat C (2007) Do cuckoos choose nests of great reed warblers on the basis of host egg appearance? J Evol Biol 20:1218–1222

    Article  CAS  PubMed  Google Scholar 

  • Darwin C (1859) On the origin of species. John Murray, London

    Google Scholar 

  • Davies NB (2000) Cuckoos, cowbirds and other cheats. T. & A. D. Poyser, London

    Google Scholar 

  • Davies NB, Brooke MDL (1988) Cuckoos versus reed warblers : adaptations and counteradaptations. Anim Behav 36:262–284

    Article  Google Scholar 

  • Davies NB, Brooke MDL (1989) An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. J Anim Ecol 58:207–224

    Article  Google Scholar 

  • Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc B 205:489–511

    Article  CAS  Google Scholar 

  • del Hoyo J, Elliott A, Sargatal J (1997) Handbook of the birds of the world. Vol 4.Sandgrouse to Cuckoos. Lynx Edicions, Barcelona

    Google Scholar 

  • Erlinger G (1984) Untersuchung zum Kuckucks–Brutparasitismus in einer Teichrohrsängerpopulation. Öko-L 6:22–29

    Google Scholar 

  • Feeney WE, Welbergen JA, Langmore NE (2014) Advances in the study of coevolution between avian brood parasites and their hosts. Ann Rev Ecol Evol Syst 45:227–246

    Article  Google Scholar 

  • Grim T, Samas P, Moskat C et al (2011) Constraints on host choice: Why do parasitic birds rarely exploit some common potential hosts? J Anim Ecol 80:508–518

    Article  PubMed  Google Scholar 

  • Honza M, Šulc M, Jelínek V et al (2014) Brood parasites lay eggs matching the appearance of host clutches. Proc R Soc B 281:1471–2954

    Google Scholar 

  • Hoyt DF (1979) Practical methods of estimating volume and fresh weight of bird eggs. Auk 96:73–77

    Google Scholar 

  • Igic B, Cassey P, Grim T et al (2012) A shared chemical basis of avian host-parasite egg colour mimicry. Proc R Soc B 279:1068–1076

    Article  PubMed Central  PubMed  Google Scholar 

  • Jarvinen A (1994) Global warming and egg size of birds. Ecography 17:108–110

    Article  Google Scholar 

  • Jetz W, Sekercioglu CH, Böhning-Gaese K (2008) The worldwide variation in avian clutch size across species and space. PLoS Biol 12:2650–2657

    Google Scholar 

  • Johnson BJ, Omland KS (2004) Model selection in ecology and evolution. TREE 19:101–108

    PubMed  Google Scholar 

  • Joys AC, Crick HQP (2004) Breeding periods for selected bird species in England. British Trust for Ornithology, Thetford, Norfolk

    Google Scholar 

  • Kilner RM (2006) The evolution of egg colour and patterning in birds. Biol Rev Camb Philos Soc 81:383–406

    Article  CAS  PubMed  Google Scholar 

  • Krüger O, Davies NB (2004) The evolution of egg size in the brood parasitic cuckoos. Behav Ecol 15:210–218

    Article  Google Scholar 

  • Lack D (1946) The Significance of Clutch-size—part I and II. Ibis 89:302–352

    Article  Google Scholar 

  • Löhrl H (1979) Untersuchungen am Kuckuck, Cuculus canorus (Biologie, Ethologie und Morphologie). J Ornithol 120:139–173

    Article  Google Scholar 

  • Lotem A, Nakamura H, Zahavi A (1995) Constraints on egg discrimination and cuckoo-host co-evolution. Anim Behav 49:1185–1209

    Article  Google Scholar 

  • Marchetti K (2000) Egg rejection in a passerine bird: size does matter. Anim Behav 59:877–883

    Article  PubMed  Google Scholar 

  • McNab BK (2010) Geographic and temporal correlations of mammalian size reconsidered: a resource rule. Oecologia 164:13–23

    Article  PubMed  Google Scholar 

  • Meiri S, Dayan T (2003) On the validity of Bergmann’s rule. J Biogeogr 30:331–351

    Article  Google Scholar 

  • Meiri S, Dayan T, Simberloff D (2005) Biogeographic patterns in the Western Palearctic: the fasting-endurance hypothesis and the status of Murphy’s rule. J Biogeogr 32:369–375

    Article  Google Scholar 

  • Meiri S, Guy D, Dayan T et al (2009) Global change and carnivore body size: data are stasis. Glob Ecol Biogeogr 18:240–247

    Article  Google Scholar 

  • Millien V, Lyons SK, Olson L et al (2006) Ecotypic variation in the context of global climate change: revisiting the rules. Ecol Lett 9:853–869

    Article  PubMed  Google Scholar 

  • Moksnes A, Røskaft E (1995) Egg-morphs and host preference in the common cuckoo (Cuculus canorus): an analysis of cuckoo and host eggs from European museum collections. J Zool 236:625–648

    Article  Google Scholar 

  • Møller AP, Saino N, Adamík P et al (2011) Rapid change in host use of the common cuckoo Cuculus canorus linked to climate change. Proc R Soc B 278:733–738

    Article  PubMed Central  PubMed  Google Scholar 

  • Moskat C, Honza M (2000) Effect of nest and nest site characteristics on the risk of cuckoo Cuculus canorus parasitism in the great reed warbler Acrocephalus arundinaceus. Ecography 23:335–341

    Article  Google Scholar 

  • Moskat C, Honza M (2002) European Cuckoo Cuculus canorus parasitism and host’s rejection behaviour in a heavily parasitized Great Reed Warbler Acrocephalus arundinaceus population. Ibis 144:614–622

    Article  Google Scholar 

  • Nordskog AW, Tolman HS, Casey DW et al (1974) Selection in small populations of chickens. Poult Sci 53:1188–1219

    Article  CAS  PubMed  Google Scholar 

  • Øien JI, Moksnes A, Røskaft E (1995) Evolution of variation in egg color and marking pattern in European passerines: adaptations in a revolutionary arms race with the cuckoo, Cuculus canorus. Behav Ecol 6:166–174

    Article  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Payne RB (2005) The Cuckoos. Oxford University Press, Oxford, New York

    Google Scholar 

  • R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org

  • Rahn H, Paganellai CV, Ar A (1975) Relation of avian egg weight to body weight. Auk 92:750–765

    Article  Google Scholar 

  • Rothstein SI (1982) Mechanisms of avian egg recognition: Which egg parameters elicit responses by rejecter species? Behav Ecol Sociobiol 11:229–239

    Article  Google Scholar 

  • Rothstein SI (1990) A model system for coevolution: avian brood parasitism. Annu Rev Ecol Syst 21:481–508

    Article  Google Scholar 

  • Rychlik L, Jancewicz E (2001) Prey size, prey nutrition, and food handling by shrews of different body sizes. Behav Ecol 13:216–223

    Article  Google Scholar 

  • Salewski V, Hochachka WM, Fiedler W (2010) Global warming and Bergmann’s rule: do central European passerines adjust their body size to rising temperatures? Oecologia 162:247–260

    Article  PubMed Central  PubMed  Google Scholar 

  • Senar JC, Pascual J (1997) Keel and tarsus length may provide a good predictor of avian body size. Ardea 85:269–274

    Google Scholar 

  • Servedio MR, Lande R (2003) Coevolution of an avian host and its parasitic cuckoo. Evolution 57:1164–1175

    Article  PubMed  Google Scholar 

  • Sheridan JA, Bickford D (2011) Shrinking body size as an ecological response to climate change. Nat Clim Chang 1:401–406

    Article  Google Scholar 

  • Spottiswoode CN, Stevens M (2012) Host-parasite arms races and rapid changes in bird egg appearance. Am Nat 179:633–648

    Article  PubMed  Google Scholar 

  • Stevens M (2013) Bird brood parasitism. Curr Biol 23:R909–R913

    Article  CAS  PubMed  Google Scholar 

  • Stokke BG, Hafstad I, Rudolfsen G et al (2008) Predictors of resistance to brood parasitism within and among reed warbler populations. Behav Ecol 19:612–620

    Article  Google Scholar 

  • Stokke BG, Polacikova L, Dyrcz A et al (2010) Responses of reed warblers Acrocephalus scirpaceus to non-mimetic eggs of different sizes in a nest parasitism experiment. Acta Ornithol 45:98–104

    Article  Google Scholar 

  • Teplitsky C, Mills JA, Alho JS et al (2008) Bergmann’s rule and climate change revisited: disentangling environmental and genetic responses in a wild bird population. PNAS 105:13492–13496

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thorogood R, Davies NB (2013) Reed warbler hosts fine-tune their defenses to track three decades of cuckoo decline. Evolution 67:3545–3555

    Article  PubMed Central  PubMed  Google Scholar 

  • Tryjanowski P, Sparks TH, Kuczyński L et al (2004) Should avian egg size increase as a result of global warming? A case study using the red-backed shrike (Lanius collurio). J Ornithol 145:264–268

    Article  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New York

    Book  Google Scholar 

  • Walther G, Post E, Convey P et al (2002) Ecological responses to recent climate change. Nature 416:389–395

    Article  CAS  PubMed  Google Scholar 

  • Wetzel DP, Stewart IRK, Westneat DF (2012) Heterozygosity predicts clutch and egg size but not plasticity in a house sparrow population with no evidence of inbreeding. Mol Ecol 21:406–420

    Article  CAS  PubMed  Google Scholar 

  • Wyllie I (1981) The cuckoo. B. T. Batsford Ltd., London

    Google Scholar 

  • Yom-Tov Y, Geffen E (2011) Recent spatial and temporal changes in body size of terrestrial vertebrates: probable causes and pitfalls. Biol Rev Camb Philos Soc 86:531–541

    Article  PubMed  Google Scholar 

  • Yom-Tov Y, Yom-Tov S, Wright J et al (2006) Recent changes in body weight and wing length among some British passerine birds. Oikos 1:91–101

    Article  Google Scholar 

  • Zuur AF, Leno NE, Elphick SC (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecol Evol 1:3–14

    Article  Google Scholar 

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Acknowledgments

Comments made by four anonymous referees significantly improved the manuscript. This research received support from the SYNTHESYS Project: http://www.synthesys.info, which was financed by the European Community Research Infrastructure Action under the FP7 “Capacities” Program. BGS was funded by the Research Council of Norway (218144). The research was further funded by a seed money grant from Oranim College awarded to Shai Markman. We thank Arnon Lotem and Tamar Dayan for valuable comments on an earlier version of this manuscript. We also thank Rainee Kaczorowski, Oliver Tallowin and Naomi Paz for going over the final version of this manuscript. We are grateful to the collection managers and curators at the Natural History museums: in Tring, UK—to Robert Prys-Jones, Mark Adams, and especially to Douglas Russell, the curator of the egg collection; in Copenhagen—to Jon Fjeldså, and Jan Bolding Kristensen, and in Berlin—to Sylke Frahnert and Pascal Eckhoff. We thank Oliver Tallowin and Uri Obolski for statistical advice.

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Authors and Affiliations

  1. Department of Zoology, Tel Aviv University, Tel Aviv, Israel

    Daniel Berkowic & Shai Meiri

  2. Department of Biology, Norwegian University of Science and Technology (NTNU), Trondheim, Norway

    Bård G. Stokke

  3. Department of Biology and Environment, University of Haifa – Oranim, Tivon, 36006, Israel

    Shai Markman

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  1. Daniel Berkowic
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  2. Bård G. Stokke
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  4. Shai Markman
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Correspondence to Shai Markman.

Appendix

Appendix

See Tables 3, 4, 5, 6, 7 and 8.

Table 3 Number of reed warbler eggs and nests, first and last years of egg and nest collection
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Table 4 Variance Inflation Factor (VIF) for all multiple regression models related to the cuckoos and reed warblers that were measured during the studied period
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Table 5 Cuckoo egg volumes: the parameters included in the four best models (i.e., models with ΔAICc < 10) and their model-selection statistics
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Table 6 Reed warbler egg volumes: the parameters included in the five best models (i.e., models with ΔAICc < 10) and their model-selection statistics
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Table 7 Cuckoo tarsus lengths: the parameters included in the seven best models (i.e., models with ΔAICc < 10) and their model-selection statistics
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Table 8 Reed warbler tarsus lengths: the parameters included in the seven best models (i.e., models with ΔAICc < 10) and their model-selection statistics
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Berkowic, D., Stokke, B.G., Meiri, S. et al. Climate change and coevolution in the cuckoo–reed warbler system. Evol Ecol 29, 581–597 (2015). https://doi.org/10.1007/s10682-015-9763-x

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