A novel locus on chromosome 1 underlies the evolution of a melanic plumage polymorphism in a wild songbird

Abstract

Understanding the mechanisms responsible for phenotypic diversification within and among species ultimately rests with linking naturally occurring mutations to functionally and ecologically significant traits. Colour polymorphisms are of great interest in this context because discrete colour patterns within a population are often controlled by just a few genes in a common environment. We investigated how and why phenotypic diversity arose and persists in the Zosterops borbonicus white-eye of Reunion (Mascarene archipelago), a colour polymorphic songbird in which all highland populations contain individuals belonging to either a brown or a grey plumage morph. Using extensive phenotypic and genomic data, we demonstrate that this melanin-based colour polymorphism is controlled by a single locus on chromosome 1 with two large-effect alleles, which was not previously described as affecting hair or feather colour. Differences between colour morphs appear to rely upon complex cis-regulatory variation that either prevents the synthesis of pheomelanin in grey feathers, or increases its production in brown ones. We used coalescent analyses to show that, from a ‘brown’ ancestral population, the dominant ‘grey’ allele spread quickly once it arose from a new mutation. Since colour morphs are always found in mixture, this implies that the selected allele does not go to fixation, but instead reaches an intermediate frequency, as would be expected under balancing selection.

Differential divergence in autosomes and sex chromosomes is associated with intra‐island diversification at a very small spatial scale in a songbird lineage

“…However, cases of long‐term balancing selection may be harder to detect because of the short haplotypes typically found in this case due to extensive recombination. Together with previous findings (Bourgeois, Bertrand, Thébaud, & Milá, 2012; Bourgeois et al, 2017), this suggests that a large part of plumage colour variation between the geographical forms of the Reunion grey white‐eye may be controlled by a set of a few loci of major effect. More detailed studies of hybrid zones between the different lowland forms may help to characterize the exact association of alleles that produce a given plumage colour phenotype.…”

“…The likelihood is high, however, that recent selective sweeps would have been detected if such genes had been targeted by selection. For example, the locus underlying colour polymorphism in the high‐elevation form shows clear signs of a selective sweep reducing diversity over 500 kb (see Figure 3 in Bourgeois et al, 2017), a region which is large enough to be covered by tens of RAD‐seq loci. However, cases of long‐term balancing selection may be harder to detect because of the short haplotypes typically found in this case due to extensive recombination.…”

“…A fourth form, restricted to the highlands (between 1,400 and 3,000 m), is relatively larger than the lowland forms and comprises two very distinct colour morphs, with birds showing predominantly grey (GRY) or brown (highland brown‐headed brown form, HBHB) plumage, respectively (Bertrand et al, 2016; Cornuault et al, 2015; Gill, 1973; Milá, Warren, Heeb, & Thébaud, 2010). Both of these latter morphs occur in sympatry and represent a clear case of plumage colour polymorphism (Bourgeois et al, 2017). This highland form is separated from all three lowland forms by relatively narrow contact zones located along the elevational gradient (Gill, 1973).…”

Colour plumage polymorphism in the Booted Eagle: inheritance pattern and temporal stability of the morph frequencies

“…Morph inheritance has been tested in wild populations of some raptor species such as Ferruginous hawk ( Buteo regalis ) (Schmutz & Schmutz, ), Common Buzzard ( Buteo buteo ) (Krüger et al ., ), Swainson's Hawk ( Buteo swainsoni ) (Briggs, Woodbridge & Collopy, ), Eleonora's Falcon ( Falco eleonorae ) (Gangoso et al ., ), Black Sparrowhawk ( Accipiter melanoleucos ) (Amar et al ., ) and also in the captive breed Gyr Falcons ( Falco rusticolus ) (Chang, Lejeune & Cheng, ). Among these raptor species, as occurs in other bird genera (Bourgeois et al ., ), colour polymorphism apparently follows a typical simple Mendelian inheritance pattern, with a single locus and two alleles, being the dark morph phenotype dominant, co‐dominant or recessive. In the case of Gyr Falcon, the phenotype is controlled by two locus or genes with two and three alleles respectively.…”

“…Using extensive phenotypic and genomic data, Bourgeois et al . () recently discovered a new locus on chromosome 1 with two large‐effect alleles, not previously described, as being responsible of melanin‐based colour polymorphism in the Reunion Grey White‐Eye ( Zosterops borbonicus ).…”