Independent pseudogenization ofCYP2J19in penguins, owls and kiwis implicates gene in red carotenoid synthesis

Abstract

Carotenoids have important roles in bird behavior, including pigmentation for sexual signaling and improving color vision via retinal oil droplets. Yellow carotenoids are dietderived, but red carotenoids (ketocarotenoids) are typically synthesized from yellow precursors via a carotenoid ketolase. Recent research on passerines has provided evidence that a cytochrome p450 enzyme, CYP2J19, is responsible for this reaction, though it is unclear if this function is phylogenetically restricted. Here I provide evidence that CYP2J19 is the carotenoid ketolase common to Aves using the genomes of 65 birds and the retinal transcriptomes of 15 avian taxa. CYP2J19 is functionally intact and robustly transcribed in all taxa except for several species adapted to foraging in dim light conditions. Two penguins, an owl and a kiwi show evidence of genetic lesions and relaxed selection in their genomic copy of CYP2J19, and six owls show evidence of marked reduction in CYP2J19 retinal transcription compared to nine diurnal avian taxa. Notably, none of these taxa are known to use red carotenoids for sexual signaling and several species of owls and penguins represent the only birds known to completely lack red retinal oil droplets. The remaining avian taxa belong to groups known to possess red oil droplets, known or expected to deposit red carotenoids in skin and/or plumage, and/or frequently forage in bright light.The loss and reduced expression of CYP2J19 is likely an adaptation to maximize retinal sensitivity, given that oil droplets reduce the amount of light available to the retina.

Northern Spotted Owl (Strix occidentalis caurina) Genome: Divergence with the Barred Owl (Strix varia) and Characterization of Light-Associated Genes

“…S. o. caurina has a 1 nt insertion and 2 nt deletion in exon 9. As Emerling (2017c ) described, the T. alba assembly contains a premature stop codon in each of exons 1, 5, and 6 as well as a 5 nt deletion in exon 3. Both the S. o. caurina (ω = 0.33–0.34; P < 0.05) and T. alba (ω = 0.68–0.72; P < 0.0001) branches have elevated dN/dS ratios compared with the background (0.15–0.16), which is consistent with the hypothesis that these mutations have led to a loss of function of CYP2J19 .…”

“…2016 ; Mundy etal. 2016 ; Emerling 2017c ). Carotenoids, in addition to being involved in pigmentation of avian skin and feathers, are located in oil droplets anterior to the photosensitive outer segments of cone photoreceptors.…”

“…In S. aluco , the red oil droplets are limited to <1% of the cone photoreceptor population ( Bowmaker and Martin 1978 ), which is an extremely low proportion compared with other avian species ( Bowmaker 1980 ; Partridge 1989 ). Additionally, there is recent evidence that CYP2J19 is inactivated in T. alba , is transcribed as a pseudogene in the retinal transcriptome of Asio otus (long-eared owl), and is transcribed at low levels in five other owl species as compared with the level observed in diurnal outgroup avian taxa ( Emerling 2017c ). Among non-owl Aves, the absence of red cone oil droplets has only been reported in two penguin species, S. humboldti ( Bowmaker and Martin 1985 ) and Aptenodytes patagonicus ( Gondo and Ando 1995 ).…”

“…Among non-owl Aves, the absence of red cone oil droplets has only been reported in two penguin species, S. humboldti ( Bowmaker and Martin 1985 ) and Aptenodytes patagonicus ( Gondo and Ando 1995 ). Among nonowls, CYP2J19 is inactivated in the penguins P. adeliae and A. forsteri as wells as in the kiwi A. mantelli ( Emerling 2017c ), which all forage under dim-light conditions. The CYP2J19 pseudogene reported here for S. occidentalis caurina provides further evidence that owls have repeatedly been losing red carotenoid oil droplets in parallel, potentially to maximize retinal sensitivity in their predominantly nocturnal niche.…”

Expression of a carotenoid‐modifying gene and evolution of red coloration in weaverbirds (Ploceidae)

“…It therefore appears that the estrildid CYP2J19 duplication occurred after the split between ploceids and estrildids. More broadly, a single copy of CYP2J19 was reported also in the red factor canary (Lopes et al., ), as well as in chicken and ostrich (Twyman et al., ) and GenBank searches reveal only a single copy in the vast majority of available avian genomes (Emerling, , Twyman, Andersson, & Mundy, ), which means that a single CYP2J19 copy probably is the “normal” situation for birds.…”