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How Birds Became Red

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Two teams of researchers have independently identified a gene-encoded enzyme in birds that converts yellow pigments obtained from the diet into red pigments, which birds then use to color their feathers, bills and bare skin

Birds seem to love the color red. Many songbirds, for example, use red as a visual signal to attract potential mates and to warn away potential challengers before a conflict escalates into a physical confrontation. In birds that use red coloration as a signal, redder is better, since the intensity of the color appears to be correlated with a bird's ability to attract mates and to scare rivals. Although red pigments are probably an honest signal of an individual bird's genetic quality (ref), we cannot know this for sure until we know what the molecular mechanisms might be for how birds actually create red pigments.

Two truly elegant studies were just published in one of my favorite journals, Current Biology, that finally push back the boundaries of what we know about how birds create red pigments. These studies -- each published independently by two different collaborations between several research teams studying different songbird species -- point to the same gene.

The first team compared the genomes of domesticated yellow and red factor canaries

The first study was conducted by an international collaboration between three different research teams headed by evolutionary biologist Ricardo Lopes, at the Universidade do Porto in Portugal; biochemist James Johnson, a PhD candidate in the Department of Biological Sciences at Auburn University; and integrative biologist Matthew Toomey, a postdoctoral fellow at the Washington University School of Medicine (ref). This study examined the source of red coloration in so-called "red factor" canaries (graphical abstract 1). These canaries are the product of hybrids created nearly 100 years ago between domesticated yellow canaries, Serinus canaria, and wild red siskins, Spinus cucullata.

In this study, the research teams compared whole-genome sequences from yellow and red canaries to red siskins to uncover the location and identity of the genes responsible for the canaries' red color. They identified two specific regions in red factor canary DNA, one on chromosome 8 and another on chromosome 25, that were identical to red siskin DNA. They followed up by using several methods to examine expression patterns in liver and skin tissues for all candidate genes found in those two chromosomal regions.

Their findings pointed directly at a particular cytochrome P450 enzyme on chromosome 8, known as CYP2J19. When the scientists examined this gene's expression pattern in skin and liver tissues from yellow and red factor canaries, they found it is up-regulated 1000-fold in both tissues from red factor canaries, suggesting this gene could be the source of red ketocarotenoid pigments.

"We discovered a gene that codes for an enzyme that enables this yellow-to-red conversion in birds," said co-author, Miguel Carneiro from the Universidade do Porto in Portugal.

"To produce red feathers, birds convert yellow dietary pigments known as carotenoids into red pigments and then deposit them in the feathers," said Dr Carneiro.

Could this be the mysterious "redness gene" that enables red factor canaries to make red plumage?

The second team studied the genes of domesticated wild-type and yellow-beaked zebra finches

The second study was the result of a collaboration between two other research teams, one group headed by evolutionary geneticist Nicholas Mundy, a Reader in the Zoology Department at the University of Cambridge, and the other group was led by evolutionary biologist Jessica Stapley, an independent research fellow in the Department of Animal and Plant Sciences at the University of Sheffield. These research teams collaborated to study the genes of domesticated zebra finches, Taeniopygia guttata (graphical abstract 2; ref).

Ironically, one of the co-authors of this zebra finch study, Timothy Birkhead, a professor of behavior and evolution at the University of Sheffield, was the author of a popular book that tells the fascinating story of how the red factor canary was developed in the 1920s by a couple of German canary hobbyist-breeders (2003).

Examining and comparing the genes between the wild-type finches with red beaks and the yellow-beaked finches pointed the researchers directly to the finch chromosome 8, where several genes in the cytochrome P450 gene cluster -- CYP2J19A, CYP2J19B, and CYP2J40 -- are located. Closer examination revealed that these genes were intact in the wild-type zebra finch genome, but were either damaged by multiple mutations or missing altogether in the yellow-beaked zebra finches.

The researcher's data showed that one of those genes, CYP2J40, has broad tissue expression that shows no differences between wild-type and yellow-beaked finches, so the scientists ruled this out as the source of red ketocarotenoid pigments. However, in wild-type finches, they found that the CYP2J19 genes are expressed in tissues containing red ketocarotenoid pigments but were barely detectable in the same tissues from yellow-beaked finches. Thus, the research teams concluded that CYP2J19 was the source of red pigmentation in zebra finch beaks and legs.

The "redness gene" is involved in avian color vision and later was co-opted as a visual signal

"On their own, these studies are beautiful examples of tracking down the genetic origins of color traits", said Mike Shapiro, an Associate Professor of Biology at the University of Utah, who was not part of either study.

"Together, they tell an even more powerful story", said Professor Shapiro in email.

"Canaries and finches appear to have converged on similar genetic solutions to converting yellow pigments to red ones in the skin and its derivatives (scales, beaks, feathers). This raises the possibility [that] a limited number of genetic mechanisms are available to control the red traits", said Professor Shapiro.

Since most birds have the CYP2J19 "redness gene", even those that lack red plumage, this indicates the "redness gene" has a more universal biological role than just creating red pigments.

"Diurnal birds appear to use this gene to produce red pigments in the retina to enhance color vision", said one of the co-authors of the canary study, Joseph Corbo, who researches retinal diseases at the Washington University School of Medicine.

The retina is a layer of tissue inside the eye that is comprised of light-sensitive neurons, also known as photoreceptor cells. One type of photoreceptor cell, the rods, provide vision under dim light, whilst the other types of photoreceptors, the cones, are responsible for color vision. But unlike mammalian cones, the cones in birds' eyes contain an assortment of brightly-colored oil droplets, including green, yellow, and red, that enable birds to see more colors than mammals can see.

"It was quite a surprise that the same genes are involved both in seeing red colors and making red coloration", said Dr Mundy.

But the "redness gene" is not expressed everywhere in every bird.

"[O]nly birds with red feathers additionally express the gene in their skin", said Professor Corbo.

Professor Corbo elaborated further: "These findings suggest that nearly all birds have the latent capacity to make red feathers, but in order to actually do so, they must evolve the means of expressing [this gene] in the skin in addition to the retina."

In addition to creating red pigments and enhancing color vision, the "redness gene" is a member of the enormous cytochrome P450 family of enzymes. These enzymes are important because some of them break down a variety of toxic compounds, mostly in the liver. A number of the cytochrome P450 enzymes are well-studied in humans because they are associated with the metabolism of drugs.

"In sexual selection, red color is thought to signal individual quality and one way it can do this is if the type or amount of pigmentation is related to other physiological processes, like detoxification", said another co-author of the canary study, Leif Andersson, at Uppsala University in Sweden.

Now that they know the identity of the "redness gene", researchers can better understand the evolutionary phenomenon known as an "honest signal", where a particular trait, such as bright red feathers, is genuinely associated with higher-quality genes.

"Given the repeated origins of red coloration among birds, and the frequent involvement of red coloration in sexually-selected traits, this contribution towards a mechanistic understanding of red coloration is a major accomplishment", said evolutionary geneticist Christopher Balakrishnan, an assistant professor at East Carolina University, who was not involved with either study.

"I think, however, that the most exciting aspect of all of this is the component both papers touch on at the end. These studies provide a mechanism by which the mechanisms of coloration can be linked to the overall health of the individual", said Professor Balakrishnan in email.

"In doing so, these studies provide a potentially critical insight for classic 'honest signaling' hypotheses in sexual selection", said Professor Balakrishnan.

That the "redness gene" plays a number of different roles is not a new motif in evolutionary biology.

"This is a theme that the evolutionary genetics community is seeing repeatedly in a variety of different organisms. Even in different species with different evolutionary histories, the same or similar genes are often major players in similar traits", said Professor Shapiro.

The future is rich with possibilities that I am eagerly awaiting. According to Professor Mundy, he and his colleagues are now working on the genetics of red coloration in African widowbirds and bishops, which show "spectacular differences among different species."

Professor Corbo and his colleagues plan to explore red feathers in many more bird species, to see whether they use the same or different mechanisms to create red pigments. They also plan to continue using the domestic canary as a model for uncovering the genetic basis of other interesting traits in birds.

Sources:

Ricardo J. Lopes, James D. Johnson, Matthew B. Toomey, Mafalda S. Ferreira, Pedro M. Araujo, José Melo-Ferreira, Leif Andersson, Geoffrey E. Hill, Joseph C. Corbo, and Miguel Carneiro (2016). Genetic Basis for Red Coloration in Birds, Current Biology, 26, published online ahead of print on 19 May 2016 | doi:10.1016/j.cub.2016.03.076

Nicholas I. Mundy, Jessica Stapley, Clair Bennison, Rachel Tucker, Hanlu Twyman, Kang-Wook Kim, Terry Burke, Tim R. Birkhead, Staffan Andersson, and Jon Slate (2016). Red Ketocarotenoid Pigmentation in the Zebra Finch Is Controlled by a Cytochrome P450 Gene Cluster, Current Biology, 26, published online ahead of print on 19 May 2016 | doi:10.1016/j.cub.2016.04.047

Also cited:

Sarah R. Pryke, Staffan Andersson, Michael J. Lawes and Steven E. Piper (2002). Carotenoid status signaling in captive and wild red-collared widowbirds: independent effects of badge size and color, Behavioral Ecology 13(5): 622-631 | doi:10.1093/beheco/13.5.622

Birkhead, T. (2003). A Brand-New Bird: How Two Amateur Scientists Created the First Genetically Engineered Animal (Basic Books, ISBN: 978-0465006656).

How Birds Became Red | @GrrlScientist

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