title: Red Carotenoid Coloration in the Zebra Finch Is Controlled by a Cytochrome P450 Gene Cluster.
abstract: Bright-red colors in vertebrates are commonly involved in sexual, social, and interspecific signaling [1-8] and are largely produced by ketocarotenoid pigments. In land birds, ketocarotenoids such as astaxanthin are usually metabolically derived via ketolation of dietary yellow carotenoids [9, 10]. However, the molecular basis of this gene-environment mechanism has remained obscure. Here we use the yellowbeak mutation in the zebra finch (Taeniopygia guttata) to investigate the genetic basis of red coloration. Wild-type ketocarotenoids were absent in the beak and tarsus of yellowbeak birds. The yellowbeak mutation mapped to chromosome 8, close to a cluster of cytochrome P450 loci (CYP2J2-like) that are candidates for carotenoid ketolases. The wild-type zebra finch genome was found to have three intact genes in this cluster: CYP2J19A, CYP2J19B, and CYP2J40. In yellowbeak, there are multiple mutations: loss of a complete CYP2J19 gene, a modified remaining CYP2J19 gene (CYP2J19(yb)), and a non-synonymous SNP in CYP2J40. In wild-type birds, CYP2J19 loci are expressed in ketocarotenoid-containing tissues: CYP2J19A only in the retina and CYP2J19B in the beak and tarsus and to a variable extent in the retina. In contrast, expression of CYP2J19(yb) is barely detectable in the beak of yellowbeak birds. CYP2J40 has broad tissue expression and shows no differences between wild-type and yellowbeak. Our results indicate that CYP2J19 genes are strong candidates for the carotenoid ketolase and imply that ketolation occurs in the integument in zebra finches. Since cytochrome P450 enzymes include key detoxification enzymes, our results raise the intriguing possibility that red coloration may be an honest signal of detoxification ability.
authors.affiliation: Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK. Electronic address: nim21@cam.ac.uk.
authors.forename: Nicholas I
authors.initials: NI
authors.lastname: Mundy
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
authors.forename: Jessica
authors.initials: J
authors.lastname: Stapley
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
authors.forename: Clair
authors.initials: C
authors.lastname: Bennison
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
authors.forename: Rachel
authors.initials: R
authors.lastname: Tucker
authors.affiliation: Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK.
authors.forename: Hanlu
authors.initials: H
authors.lastname: Twyman
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
authors.forename: Kang-Wook
authors.initials: KW
authors.lastname: Kim
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
authors.forename: Terry
authors.initials: T
authors.lastname: Burke
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
authors.forename: Tim R
authors.initials: TR
authors.lastname: Birkhead
authors.affiliation: Department of Biological and Environmental Sciences, University of Gothenburg, Göteborg 40530, Sweden. Electronic address: staffan.andersson@bioenv.gu.se.
authors.forename: Staffan
authors.initials: S
authors.lastname: Andersson
authors.affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
authors.forename: Jon
authors.initials: J
authors.lastname: Slate
mesh_terms: D000818:Animals; D030161:Avian Proteins / Q000235:genetics* / Q000378:metabolism; D001502:Beak / Q000502:physiology; D003577:Cytochrome P-450 Enzyme System / Q000235:genetics* / Q000378:metabolism; D005260:Female; D046369:Finches / Q000235:genetics / Q000502:physiology*; D008297:Male; D010858:Pigmentation; D010860:Pigments, Biological / Q000235:genetics* / Q000378:metabolism; D012160:Retina / Q000502:physiology; D013643:Tarsus, Animal / Q000502:physiology
chemical_list: D030161:Avian Proteins; D010860:Pigments, Biological; D003577:Cytochrome P-450 Enzyme System