Look into my eyes: Unraveling the genetic basis of iris color in domestic pigeons

A nonsense mutation in one gene underlies the “pearl” phenotype.

All roads lead to Rome. This saying was nicely illustrated by three research groups that independently discovered the genetic basis of the “pearl” eye color in the domestic pigeon (Columba livia). When you take a closer look at pigeons, you might notice three main eye colors: orange, pearl (white), and bull (dark brown). One of the three papers – by Emily Maclary and her colleagues – provided a nice summary of these three eye colors.

Orange iris color is the ancestral state, and “orange” eyes in actuality range in shades from yellow to red, depending on the density of blood vessels in the eye. The pearl iris color is white, with tinges of pink and red from blood vessels. Lastly, the bull iris color is named based on its similarity in color to dark bovine eyes, and ranges from dark brown to almost black.

In this blog post, I will focus on the genetic basis of the pearl eye color. Interested readers can check this Molecular Biology and Evolution study for more information on the genetics of the bull eye color.

One Candidate Gene

Using different approaches – from genome-wide association studies to laboratory crosses – the three research groups all zoomed in on the gene SLC2A11B (solute carrier family 2, facilitative glucose transporter, member 11b). Detailed analyses of this gene revealed a nonsense mutation that results in a premature stop codon. In their PLoS Genetics study, Si Si and co-workers noted that “the W49X mutation leads to the truncation of approximately 90% of the amino acids of SLC2A11B and is predicted to cause a total loss of function in the protein.”

Comparing the genomes of domestic pigeons with pearl-eye and wild-type colors revealed a clear candidate region that contained the gene SLC2A11B. From: Andrade et al. (2021).

Pteridine Pigments

In another PLoS Genetics study, Pedro Andrade and his colleagues quantified the expression of the candidate gene. They found that the gene SLC2A11B was down-regulated in pigeons with the pearl eye color. This expression pattern suggests that the nonsense mutation creates an aberrant RNA-molecule that is broken down by the cell. The product of SLC2A11B might thus be non-functional.

A functional SLC2A11B gene would be involved in the production of pteridine pigments which give the wild-type eye its orange color. No functional SLC2A11B gene means no pteridine pigments, resulting in a pearl iris color.

Expression data indicated that the SLC2A11B gene is down-regulated in pigeons with the pearl eye color. From: Andrade et al. (2021).

Artificial Selection

Finally, we can have a look at the evolutionary history of this mutation. Si Si and co-workers performed a phylogenetic analysis on 139 domestic pigeons (35 fancy pigeons, two feral pigeons, and 102 racing pigeons) and one Hill Pigeon (Columba rupestris, as an outgroup). The resulting evolutionary tree showed that the nonsense mutation arose approximately 5,400 years ago, coinciding with the possible start of pigeon domestication in the Fertile Crescent. The researchers also detected strong signals of positive selection pointing to artificial selection for this trait.

If you have read the Origin of Species, you know that Darwin used the case of artificial selection in pigeons as a starting point for his long argument in favor of evolution by natural selection. These studies would definitely have been an eye-opener for him.

Phylogenetic analyses revealed that the nonsense mutation (indicated in the orange branches) originated once about 5400 years ago. From: Si et al. (2021).

References

Andrade, P., Gazda, M. A., Araújo, P. M., Afonso, S., Rasmussen, J. A., Marques, C. I., … & Carneiro, M. (2021). Molecular parallelisms between pigmentation in the avian iris and the integument of ectothermic vertebrates. PLoS Genetics, 17(2), e1009404.

Maclary, E. T., Phillips, B., Wauer, R., Boer, E. F., Bruders, R., Gilvarry, T., … & Shapiro, M. D. (2021). Two genomic loci control three eye colors in the domestic pigeon (Columba livia). Molecular Biology and Evolution, 38(12), 5376-5390.

Si, S., Xu, X., Zhuang, Y., Gao, X., Zhang, H., Zou, Z., & Luo, S. J. (2021). The genetics and evolution of eye color in domestic pigeons (Columba livia). PLoS Genetics, 17(8), e1009770.

Featured image: Common Pigeon (Columba livia) © Satdeep Gill | Wikimedia Commons

Are there still “pure” populations of Rock Doves?

The impact of hybridization varies between populations.

“Great as the differences are between the breeds of pigeons, I am fully convinced that the common opinion of naturalists is correct, namely, that all have descended from the rock-pigeon (Columba livia).” In The Origin of Species, Charles Darwin provided ample evidence for the claim that domestic pigeon breeds are descendants from the wild Rock Dove (also known as the Rock Pigeon).

Nowadays, a new problem has emerged: hybridization between domestic pigeons and their wild progenitors. Domestic pigeons have become so common that it is uncertain whether there are any “pure” populations of Rock Doves left. This situation could lead to the genetic extinction of the wild Rock Dove. A recent study in the journal iScience used a combination of genomic data and morphometric analyses to assess the current status of wild Rock Dove populations across the British Isles.

Levels of Introgression

William Smith and his colleagues sequenced the genomes of 232 pigeons, representing three main groups: wild-caught birds from the British Isles, captive birds that are claimed to be ancestral-type Rock Doves, and domestic pigeons (breeds and feral birds). Genetic analyses confirmed these three groups, but also revealed introgression from the feral birds into the wild populations.

More detailed analyses showed that the level of introgression differs between populations. Birds from the Outer Hebrides were least introgressed, whereas populations in Scotland (particularly the Highlands and Orkney) contain more genetic material from feral pigeons. The Rock Dove populations in England and Isle of Man have been swamped by feral DNA.

Genetic analyses of wild and domestic pigeons revealed three main groups: feral pigeons (purple), captive pigeons (yellow) and wild Rock Doves (green). The genetic ancestry of individual birds shows that the Hebrides are least introgressed (mostly green in the figure). From: Smith et al. (2022).

Head Shape

The genetic patterns were mirrored in the morphometrics of the birds. The researchers could discriminate between the three groups based on the shape of the head. Wild Rock Doves tend to have smaller ceres and a smaller angle of the head rising from the base of the bill. Moreover, individuals with intermediate features were more common in regions with higher levels of introgression (e.g., Scotland).

In summary, Rock Doves populations on different islands have experienced varying levels of introgression ranging from the least admixed Outer Hebrides populations to locations where the ancestral-type pigeon may now be considered to be extinct. Conservation efforts to protect ancestral-type Rock Doves should thus focus on the least introgressed strongholds of this species.

Morphological analyses could discriminate between the three genetic groups. Wild Rock Doves could be identified based on head shape. From: Smith et al. (2022).

References

Smith, W. J., Sendell-Price, A. T., Fayet, A. L., Schweizer, T. M., Jezierski, M. T., van de Kerkhof, C., … & Clegg, S. M. (2022). Limited domestic introgression in a final refuge of the wild pigeon. iScience, 25(7).

Featured image: Common Pigeon (Columba livia) © Satdeep Gill | Wikimedia Commons