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Melanin-based coloration and immunity in polymorphic population of pied flycatcher, Ficedula hypoleuca

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Abstract

A specific interest in the persistence of color polymorphism in some populations of birds and other vertebrates is often linked to ideas about the signaling honesty of bright coloration. The evolution of conspicuous ornamentation could be associated with physiological costs including limitations of the immune system. The study of this process is crucial for an understanding of the maintenance of polymorphic coloration. Here we summarized the results of a study of a pied flycatcher population from the Moscow region (Russia) in 2010–2013. We experimentally induced antibody production by injecting sheep red blood cells (SRBC) and inflammatory swelling by injecting phytohaemagglutinin (PHA) after which we estimated the immune response in breeding males. We used leucocytes-to-erythrocytes and heterophils-to-lymphocytes (H/L) ratios as indicators of infectious, inflammatory processes and stress. The results showed that the feeding rates of males treated with SRBC decreased and negatively related to the intensity of their immune responses. Non-molting males of different color types did not significantly differ in antibody production. Among molting breeders, the immune response to SRBC was significantly higher in pale males than in bright ones with rich melanin-based coloration. In contrast to non-molting males, molting pale males had an increased antibody titer after immunization. The lower humoral immune response was associated with the higher H/L stress index before immunization. The change in H/L after immunization positively correlated with the intensity of the humoral immune response. As opposed to humoral immunity, we did not find any significant predictors, including coloration, molt, or their two-way interaction, to explain the variation in cutaneous inflammatory response to PHA. The results suggest that the apparent advantage of a cryptic male phenotype over a conspicuous phenotype occurring in one of two types of immune response has an impact on the maintenance of color polymorphism in the pied flycatcher.

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Acknowledgements

Financial support for this study was provided by RFBR (Grants Nos. 09-04-01690a and 10-04-00278a) and Russian Ministry of Education and Science (R&D Project No. 6-09/10). The analysis of blood smears and maintenance of the hematological data was supported by the Russian Science Foundation (RSF Grant No. 14-50-00029). We thank I.S. Litvinov and A.P. Barannik from the Institute of Bioorganic Chemistry of the Russian Academy of Sciences (IBCh RAS) for consultations and practical help in hematological handling. We are very grateful to anonymous reviewers and to the executive editor for their constructive criticism and helpful suggestions. Dr. Jan A. Randall kindly corrected our English and gave us some excellent advice. Joanne Turnbull helped us with English at the final stage of working with the manuscript. In our study, we followed the requirements of “Guidelines for the treatment of animals in behavioral research and teaching” (ASAB/ABS 2012) and the Federal Law of the Russian Federation.

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Correspondence to Konstantin A. Rogovin.

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Kerimov, A.B., Ilyina, T.A., Ivankina, E.V. et al. Melanin-based coloration and immunity in polymorphic population of pied flycatcher, Ficedula hypoleuca . Evol Ecol 32, 89–111 (2018). https://doi.org/10.1007/s10682-017-9926-z

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Keywords

  • Ficedula hypoleuca
  • Melanin-based coloration
  • Polymorphic coloration
  • Antibody production
  • Immune response
  • PHA
  • SRBC