Independent pseudogenization of CYP2J19 in penguins, owls and kiwis implicates gene in red carotenoid synthesis

Christopher A Emerling

doi:10.1016/j.ympev.2017.09.016

Abstract

Carotenoids have important roles in bird behavior, including pigmentation for sexual signaling and improving color vision via retinal oil droplets. Yellow carotenoids are diet-derived, 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. Furthermore, one of the owls appears to transcribe a CYP2J19 pseudogene. 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, are 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.

Highlights

IntroductionCarotenoids perform numerous functions in animals (Olson and Owens, 1998), with much of the research on avian fauna focusing on its roles in sexual signaling (Gray, 1996; McGraw et al, 2002; Blount et al, 2003; Blas et al, 2006) and fine-tuning of color vision (Vorobyev et al, 1998; Vorobyev, 2003; Stavenga and Wilts, 2014; Toomey et al, 2015)
Though both yellow and red carotenoids are deposited on external anatomy and in retinal oil droplets of birds, these colors are typically produced via different pathways
Strigiformes came out as paraphyletic with the strigiform Otus bakkamoena recovered with Cuculus canorus (Cuculiformes)

Summary

Introduction

Carotenoids perform numerous functions in animals (Olson and Owens, 1998), with much of the research on avian fauna focusing on its roles in sexual signaling (Gray, 1996; McGraw et al, 2002; Blount et al, 2003; Blas et al, 2006) and fine-tuning of color vision (Vorobyev et al, 1998; Vorobyev, 2003; Stavenga and Wilts, 2014; Toomey et al, 2015). Carotenoids are deposited in oil droplets located in retinal cone photoreceptors (Toomey et al, 2015), the cells that facilitate color vision They are believed to function as microlenses (Stavenga and Wilts, 2014) and act as long pass wavelength filters that minimize spectral sensitivity overlap between different cone classes (Vorobyev et al, 1998; Vorobyev, 2003), thereby enhancing color vision. Though both yellow and red carotenoids are deposited on external anatomy and in retinal oil droplets of birds, these colors are typically produced via different pathways. CYP2J19 was further found to be expressed in the beak and tarsus of wild-type zebra finches and the retinas of both wild-type and yellowbeak finches, but is barely detectable in the beaks of yellowbeak individuals

Methods

Results

Discussion

Conclusion