Independent sources of condition dependency and multiple pathways determine a composite trait: lessons from carotenoid-based plumage colouration

Authors

  • C. Romero-Diaz,

    Corresponding author
    • Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales (MNCN-CSIC), Madrid, Spain
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  • H. Richner,

    1. Institute of Ecology and Evolution, University of Bern, Bern, Switzerland
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  • F. Granado-Lorencio,

    1. Unidad de Vitaminas, Servicio de Bioquímica Clínica, Hospital Universitario Puerta de Hierro-Majadahonda, Madrid, Spain
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  • B. Tschirren,

    1. Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, Switzerland
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  • P. S. Fitze

    1. Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales (MNCN-CSIC), Madrid, Spain
    2. Fundación Araid, Zaragoza, Spain
    3. Instituto Pirenaico de Ecología (IPE-CSIC), Jaca, Spain
    4. Department of Ecology and Evolution (DEE), University of Lausanne, Lausanne, Switzerland
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Correspondence: Cristina Romero Díaz, Museo Nacional de Ciencias Naturales (MNCN-CSIC), c/ José Gutiérrez Abascal 2, 28006 Madrid, Spain. Tel.: +34 914111328; fax: +34 915645078; e-mail: cromero@mncn.csic.es

Abstract

Many colour ornaments are composite traits consisting of at least four components, which themselves may be more complex, determined by independent evolutionary pathways, and potentially being under different environmental control. To date, little evidence exists that several different components of colour elaboration are condition dependent and no direct evidence exists that different ornamental components are affected by different sources of variation. For example, in carotenoid-based plumage colouration, one of the best-known condition-dependent ornaments, colour elaboration stems from both condition-dependent pigment concentration and structural components. Some environmental flexibility of these components has been suggested, but specifically which and how they are affected remains unknown. Here, we tested whether multiple colour components may be condition dependent, by using a comprehensive 3 × 2 experimental design, in which we carotenoid supplemented and immune challenged great tit nestlings (Parus major) and quantified effects on different components of colouration. Plumage colouration was affected by an interaction between carotenoid availability and immune challenge. Path analyses showed that carotenoid supplementation increased plumage saturation via feather carotenoid concentration and via mechanisms unrelated to carotenoid deposition, while immune challenge affected feather length, but not carotenoid concentration. Thus, independent condition-dependent pathways, affected by different sources of variation, determine colour elaboration. This provides opportunities for the evolution of multiple signals within components of ornamental traits. This finding indicates that the selective forces shaping the evolution of different components of a composite trait and the trait's signal content may be more complex than believed so far, and that holistic approaches are required for drawing comprehensive evolutionary conclusions.

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