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Variability, heritability and condition-dependence of the multidimensional male colour phenotype in a passerine bird

Abstract

Elaborate ornamental traits are commonly assumed to be honest signals of individual quality, owing to the presumed costs involved in their production and/or maintenance. Such traits are often highly variable, possibly because of condition-dependence and/or high underlying genetic variation, and it has been suggested that their expression should be more sensitive to condition and/or more heritable than non-ornamental traits. Many bird species display colourful plumage with multiple distinct patches of different developmental origins, forming complex colour phenotypes. Despite this complexity, colourful ornaments are often studied in isolation, without comparison to suitable non-ornamental controls. Based on plumage reflectance data collected over 8 years, we assessed the signalling potential of the multidimensional male colour phenotype in a tropical bird: the purple-crowned fairy-wren Malurus coronatus. Specifically, we tested the predictions that the expression of putative ornamental colours (purple and black – the breeding colours – and blue) is (1) more variable, (2) more heritable and (3) more condition-dependent compared to year-round non-ornamental colours (buff-white and brown). Our results show that ornamental colours exhibit greater levels of variability, and some chromatic components of purple and blue colouration appear slightly heritable (h² = 0.19–0.30). However, contrary to predictions of heightened condition-dependence in ornaments, only brightness of the buff-white and brown colouration increased with male body condition, although brightness of the purple colouration was related to male age as expected. Despite partial support for predictions, the lack of consistent patterns illustrates the complexity of visual signals and highlights the need to study colour phenotypes in their entirety.

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Fig. 1: Breeding plumage in male purple-crowned fairy-wrens.
Fig. 2: Plumage reflectance spectra measured in male purple-crowned fairy-wrens and represented in their visual space.
Fig. 3: Effect size estimates of correlations between age class (1- vs. 2+-year-old), social status (subordinate vs. dominant), body condition and territory quality and the chromatic (PC1, PC2) and achromatic (L) components of the colour phenotype of male purple-crowned fairy-wrens.
Fig. 4: Heritability of chromatic (PC1, PC2) and achromatic (L) components of colour variation in five plumage patches of male purple-crowned fairy-wrens (posterior mean values obtained using MCMCglmm).
Fig. 5: Proportion of total phenotypic variance explained by random effects (stacked) for the chromatic (PC1, PC2) and achromatic (L) components of the colour phenotype (obtained using MCMCglmm).

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Acknowledgements

This research was approved by the Australian Bird and Bat Banding Scheme (license 2230); Western Australia Department of Parks and Wildlife; Australian Wildlife Conservancy; and the ethics committees of the School of Biological Sciences at Monash University and the Max Planck Institute for Ornithology. Our thanks to numerous volunteers during fieldwork and the support of staff at Australian Wildlife Conservancy’s Mornington Wildlife Sanctuary. We thank three anonymous reviewers for their constructive feedback. We are grateful for support by the Max Planck Society, the Australian Research Council (FT10100505 and DP150103595), the Holsworth Wildlife Research Endowment – Equity Trustees Charitable Foundation/Ecological Society of Australia, and the Australian Wildlife Conservancy and its supporters.

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Fan, M., Hall, M.L., Roast, M. et al. Variability, heritability and condition-dependence of the multidimensional male colour phenotype in a passerine bird. Heredity 127, 300–311 (2021). https://doi.org/10.1038/s41437-021-00453-6

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