Two studies figured it out independently.
A rainbow painted on a bird. That seems a fitting description of the Gouldian Finch (Erythrura gouldiae). This small passerine is very popular among bird breeders and comes in a variety of colour morphs. In the wild, the two most common ones are the red and black head-colour morphs. A third orange morph occurs in very low frequency (less than 0.1%). What is the genetic basis of this diversity in head plumage?
The observation that colour morphs also show distinct behaviours suggests that an inversion might be involved. An inversion is a region in the DNA that has been flipped around, linking several genes together (you can check out this blog post for more avian inversions). Perhaps this happened in the Gouldian Finch, capturing genes involved in plumage colour and behaviour in one chunk of DNA.
This seems like a reasonable hypothesis, but two recent studies independently show it is not the case. The two studies, which appeared in Nature Communications and Proceedings of the Royal Society B, both honed in on a small non-coding region on the Z-chromosome.
This genomic region is about 72,000 base pairs long and lies within two genes: MOSC2 and FST. This intergenic location suggests that the region plays a regulatory role, controlling the expression levels of particular proteins. Matthew Toomey and his colleagues investigated the expression levels of the two neighbouring genes. But MOSC2 nor FST showed any differences between the colour morphs. The exact role of the candidate region remains to be determined.
Further analyses revealed that the genomes of the black and red colour morphs are very similar, except for the candidate region on the Z-chromosome. Kang-Wook Kim and his colleagues showed that this region is even more divergent between the colour morphs than it is between distinct species. This high level of divergence suggests that the colour morphs are being maintained by balancing selection.
Balancing selection refers “to a number of selective processes by which multiple alleles (different versions of a gene) are actively maintained in the gene pool of a population at frequencies larger than expected from genetic drift alone.” It is still unclear which processes are maintaining the different alleles. Here are some possible mechanisms.
Frequency-dependent selection. This mechanisms entails the situation in which selection depends on the frequency of a trait. Let’s say females prefer red-headed males (a reasonable assumption since Liverpool just made it to the Champions League final). When there are a lot of red-headed males, competition between them is fierce. This results in considerable stress and low reproductive output. Rare black-headed males benefit from this and increase in frequency. Until they are in the majority and the tables turn.
Sexual anatagonism. A genetic battle of the sexes can also explain the occurrence of different head morphs. Perhaps the genetic variant for a red head is beneficial in males but detrimental in females. This will prevent one colour morph from taking over the population, resulting in a balanced collection of head plumages.
A Final Note on the Orange Morph
You might be wondering what happened to the orange morph in these studies. At the candidate region, these birds are identical to the red-headed birds, but they use a different pigment in their head plumage. This differential expression is controlled by a genetic region on another chromosome. If your Italian is good enough (mine isn’t), you can check this study: Pigmenti e sistematica degli uccelli.
Kim, K.W., Jackson, B.C., Zhang, H., Toews, D.P.L., Taylor, S.A., Greig, E.I., Lovette, I.J., Liu, M.M., Davison, A., Griffith, S.C., Zeng, K. & Burke, T. (2019). Genetics and evidence for balancing selection of a sex-linked colour polymorphism in a songbird. Nature Communications, 10:1852.
Toomey, M.B., Marques, C.I., Andrade, P., Araújo, P.M., Sabatino, S., Gazda, M.A., Afonso, S., Lopes, R.J., Corbo, J.C. & Carneiro, M. (2018). A non-coding region near Follistatin controls head colour polymorphism in the Gouldian finch. Proceedings of the Royal Society B, 285(1888):20181788.