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 thiscluster: CYP2J19A, CYP2J19B, and CYP2J40. In yellowbeak, there are multiple mutations: loss of acomplete 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.
Highlights
Ketocarotenoids occur in avian retinas, where astaxanthin is the pigment in the red oil droplets [18] that are present in longwave-sensitive (LWS) cones and act as cut-off filters to improve color discrimination [19]
Bright-red coloration of skin or plumage is a major component of avian color diversity and depends, with few exceptions, on the ability to enzymatically convert yellow dietary carotenoids to red C4 ketocarotenoid pigments such as astaxanthin or canthaxanthin
Using a combination of long-range PCR and Illumina MiSeq sequencing, we found direct evidence for three adjacent CYP2J2-like loci on chromosome 8, incorporating some sequence from the previously unanchored region (Figure 3D; Supplemental Experimental Procedures; Figure S1B)
Summary
Ketocarotenoids occur in avian retinas, where astaxanthin is the pigment in the red oil droplets [18] that are present in longwave-sensitive (LWS) cones and act as cut-off filters to improve color discrimination [19]. The two flanking markers had weaker support (LOD = 5.42 in both cases), and the interval spanning the flanking markers covers 24.269– 25.029 Mb. This interval contains five genes on the zebra finch genome assembly, two CYP2J2-like loci, NF1A, HOOK, and FGGY (Figure 3C). Long-range PCR results indicated the presence of an $13 kb deletion of a full copy of CYP2J19 in yellowbeak birds (Figure S1D).
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