Hybridization helps to determine the genetic basis of head patterns in the White Wagtail

This plumage traits is associated with two small genomic regions.

Subspecies of the White Wagtail (Motacilla alba) show a large variety of head patterns: from the black cheeks of personata to the completely white face of dukhunensis. In a previous blog post, I described how some researchers suspect that these plumage patterns can be explained by a small toolkit of genes that is being shuffled around by hybridization. To test this idea, we first need to unravel the genetic basis of these plumage patches. And that is exactly what a recent study in the journal Nature Communications did. Georgy Semenov and his colleagues focused on the Siberian hybrid zone between the subspecies alba and personata. The hybrids from this region show a range of plumage combinations, making it easier to link particular genomic regions to these plumage traits. Recent studies on warblers and woodpeckers took a similar approach and successfully identified several “plumage genes”. What about the wagtails?

An overview of the plumage patterns in the subspecies alba, personata and their hybrids. From: Semenov et al. (2021) Nature Communications.

Interacting Genes

The researchers sequenced the genomes of 10 individuals from the alba range, 10 individuals from the personata range, and 62 birds from the hybrid zone. Patterns of genetic differentiation within the hybrid zone uncovered two small genomic regions, located on chromosomes 1A and 20. The region on chromosome 20 contained three genes, including the well-known agouti signaling protein (ASIP) which is involved in the regulation of melanogenesis (i.e. production of the pigment melanin). The other region overlapped with a non-coding sequence between two genes (NT5D3 and CCDC91).

To figure out how these two genomic regions determine the development of different head patterns, the researchers took a closer look at the inheritance patterns in the hybrids. The genetic variants at the ASIP-region were classified into an alba-variant (A) and a personata-variant (P). Individuals with two different ASIP-variants (i.e. heterozygotes, AP) showed alba-like plumage patterns, suggesting that the alba-variant is dominant. More detailed analyses indicated that the expression of the other genomic region (on chromosome 1A) depends on the ASIP-genotype. This genetic architecture of two interacting genomic regions is reminiscent of the situation in Carrion Crow (Corvus c. corone) and Hooded Crow (C. c. cornix), which I described in detail in another blog post. The exact mechanisms underlying this interaction in the wagtails remain to be determined.

Comparing the genomes of the subspecies outside (top figure) and within (bottom figure) the hybrid zone pointed to two differentiated genomic regions on chromosomes 1A and 20. From: Semenov et al. (2021) Nature Communications.

Asymmetric Introgression

The story does not end here though. Previous work found that the transition from alba-like to personata-like heads was located about 300 kilometers northwest from the genetic center of the hybrid zone. Additional analyses of the two genomic regions described above revealed that they introgressed from personata into alba. The explanation for this asymmetric introgression is not clear yet. The head plumage could represent the leading edge of a moving hybrid zone, or there might be selection for or against certain phenotypes outside the hybrid zone. Whatever the mechanism, hybridization seems to play a pivotal role in the evolution of head patterns in the White Wagtail (similar to patterns described in wood-warblers). Indeed, the authors conclude:

The reticulate nature of phenotypic variation in head and neck plumage suggests that variation in a small number of genes may underlie the rich phenotypic diversity in wagtails. Our study suggests that only two loci contribute to head plumage differences in alba and personata subspecies. Differentiation at the two loci is retained in allopatry despite hybridization and these loci, located on different chromosomes, introgress asymmetrically together from one population into another. These results suggest epistatic interactions contribute to the evolution of sexual signals and that the genetic architecture of a trait is an important determinant in introgression.

The location of the hybrid zone (left figure) and the displacement of the head plumage (yellow line) compared to the hybrid zone (green line). From: Semenov et al. (2021) Nature Communications.


Semenov, G. A., Linck, E., Enbody, E. D., Harris, R. B., Khaydarov, D. R., Alström, P., Andersson, L. & Taylor, S. A. (2021). Asymmetric introgression reveals the genetic architecture of a plumage trait. Nature Communications12(1), 1-9.

Featured image: White Wagtail (Motacilla alba) © J.M. Garg | Wikimedia Commons