Pigeon patterning

24 August 2018

Interview with 

Mike Shapiro, University of Utah

PIGEONS.jpg

A specific genomic region gives pigeons their plumage patterns.

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How did pigeons come by their plumage patterns, and what genes control the process? Speaking with Chris Smith, Mike Shapiro explains how he has taken advantage of the diversity created by natural evolution to find out...

Mike - We were interested in trying to understand the DNA level changes that lead to animal pigment patterning. We've known for a long time the types of genes that control that type of pigments that are generated: blacks versus browns versus reds versus yellows. But an outstanding mystery in pigmentation genetics is how those pigments know where to go and how patterns are generated - spots and stripes and so forth

Chris - In terms of actually how the pigments are added to the skin, or in the case of birds, feathers, how is that achieved?

Mike - There are specialised cells that are called melanocytes that produce the pigment granules and those granules are exported onto the surface of the skin or a feather. There is a fair bit known about the recipe for the granules themselves but where are those granules go has remained a mystery for quite a while. And now, by taking advantage of things that are not laboratory mice were able to take advantage of evolutionary diversity to try to answer those questions.

Chris - So what have you done?

Mike - We've focused on pigeons as a model to try to understand how pigment patterns are generated and in particular in pigeons there are a few basic colour pattern types; and we've known for a long time - mostly through the work of pigeon hobbiests - that the genetic basis of this is relatively simple. That is, very few genes - possibly even one - have a major effect on how stripes are laid down versus a pattern called checkers because it resembles a checkerboard.

Chris - So you're saying that people who've bred pigeons over decades knew how to breed for certain traits, but they had no idea what the molecular genetics of this was?

Mike - That's correct; and I would extend that beyond decades to millennia, pigeons domesticated probably 5000 years ago and people have been raising them in captivity ever since. So we know from a long history of pigeon breeding a lot about the number of genes that go into making certain traits. But, as you pointed out, we know very little about the molecules involved.

Chris - So how did you track them down?

Mike - One way that geneticists track down genes that are responsible for particular traits or particular diseases is to identify groups with and without the trait that we're interested in. So in the case of pigeons the ancestral colour pattern is a pattern called "bar" - it's basically two stripes on the wing. And we compared the genomes of birds that have that bar pattern to pigeons that have what we call a checker pattern where there is more pigment on the wings in sort of a checkerboard-like pattern, and we try to identify what was different about their DNA sequences. And when we did that we identified just one place in the entire genome in over a billion base pairs of DNA that was different between those two groups.

Chris - And in what way is it different?

Mike - When we scanned through that region of the genome, looking for mutations that might affect places that are coding for protein, we didn't find anything that was consistently associated with having a bar or a checker pattern. However the mutations around those genes were indeed consistently associated. There is one gene in particular that piqued our interests. It's a gene called NDP, which stands for Norrie Disease Protein, and even though the gene itself wasn't different between the birds, the different patterns, the region very close to it was very different between the birds that had checkers and bars; and through some follow up experiments what we found is that that region was associated with differences in the way the gene was expressed. So rather than changing the gene itself, what appears to have happened in these pigeons is the way that gene is controlled - the way its expression is regulated - is different. In addition to that, this same region that differs between the bar and the checker birds was duplicated in some of the birds with darker colour patterns, so it appears not only that this region differentiated checker birds from the bar birds, but the more copies of DNA that the checker birds had in this region the darker they were.

Chris - So that's like a gene dosage effect?

Mike - We think it's something like that, and again it's not the gene itself, but when we assay how the gene is expressed the more copies of DNA the birds have in this region the higher the expression is in the feathers.

Chris - Now why do you think that there are these different animals in the first place. And do they actually have any impact on how the birds fare in the wild?

Mike - It appears that they do. Interestingly there is some evidence from ecological studies not done by us that the birds that have the checker pattern fare better in specific places and those specific places, oddly enough, are urban environments. The natural habitats for these birds are rock cliffs. You can think of like the Cliffs of Dover in the UK. They also live in deserts in the Middle East - that's one of their native habitats and part of their native range. But in urban habitats they're obviously more recent introductions, and the birds with the checker pattern fare better reproductively: their offspring fledge better from the nest; they survive to adulthood. Interestingly the converse is true in some rural environments: so in harsh rural environments such as the Faroe Islands, there is not much food available. The birds of the checker pattern don't fare as well. And one reason that may underlie this is that that checker birds are not as good at putting on fat over the winter as the bar birds. So this is a huge disadvantage in places that have really harsh winters but in cities, where there are French fries and other things available around, these checker birds do just fine and, again, in some cases they will breed year-round whereas the ones with the bar pattern will stop...

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