Investigating the Role of the Melanocortin-1 Receptor Gene in an Extreme Case of Microgeographical Variation in the Pattern of Melanin-Based Plumage Pigmentation

Yann X C Bourgeois,Christophe Thébaud,Joris A M Bertrand,Borja Milá,Carles Lalueza-Fox

doi:10.1371/journal.pone.0050906

Abstract

The Réunion grey white-eye (Zosterops borbonicus) is a single-island endemic passerine bird that exhibits striking geographically structured melanic polymorphism at a very small spatial scale. We investigated the genetic basis of this color polymorphism by testing whether the melanocortin-1 receptor (MC1R), a gene often involved in natural melanic polymorphism in birds, was associated with the observed plumage variation. Although we found three non-synonymous mutations, we detected no association between MC1R variants and color morphs, and the main amino-acid variant found in the Réunion grey white-eye was also present at high frequency in the Mauritius grey white-eye (Zosterops mauritianus), its sister species which shows no melanic polymorphism. In addition, neutrality tests and analysis of population structure did not reveal any obvious pattern of positive or balancing selection acting on MC1R. Altogether these results indicate that MC1R does not play a role in explaining the melanic variation observed in the Réunion grey white-eye. We propose that other genes such as POMC, Agouti or any other genes involved in pigment synthesis will need to be investigated in future studies if we are to understand how selection shapes complex patterns of melanin-based plumage pigmentation.Trial RegistrationAll sequences submitted to Genbank. Accession number: JX914505 to JX914564.

Highlights

The genetic basis and origin of color polymorphism in natural populations is a classic theme in our understanding of ultimate and proximate causes of phenotypic variation and evolution [1]
In chicken Ala45 is replaced by a Thr45, having a neutral lateral chain, suggesting this site is less constrained. These substitutions do not seem to modify greatly the chemical properties of the protein and are unlikely to have a large impact on the receptors structure. This was supported by McDonald-Kreitman tests which failed to detect any sign of positive selection on amino acid-altering mutations at melanocortin-1 receptor (MC1R) (Table 4)
Despite its frequent involvement in pigmentation patterns in vertebrates, especially in birds (Table 1), MC1R does not seem to play a role in explaining variation in plumage pigmentation in Z. borbonicus

Summary

Introduction

The genetic basis and origin of color polymorphism in natural populations is a classic theme in our understanding of ultimate and proximate causes of phenotypic variation and evolution [1]. The study of melanic coloration has led to the characterization of important target genes that may underlie phenotypic variation and divergence in natural populations [2,3]. One recurrent result emerging from most studies is the involvement of the melanocortin-1 receptor (MC1R) coding region in explaining variation in melanism, sometimes showing shared mutations due to convergent evolution between distantly related species [4]. While most studies have focused on functional substitutions in MC1R coding region in species displaying discrete color dimorphism, few have tried to examine amino acid variation in species with diverse melanin-based patterns of plumage pigmentation (but see [12,14])

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