Seeing red to being red: conserved genetic mechanism for red cone oil droplets and co-option for red coloration in birds and turtles

Abstract

Avian ketocarotenoid pigments occur in both the red retinal oil droplets that contribute to colour vision and bright red coloration used in signalling. Turtles are the only other tetrapods with red retinal oil droplets, and some also display red carotenoid-based coloration. Recently, the CYP2J19 gene was strongly implicated in ketocarotenoid synthesis in birds. Here, we investigate CYP2J19 evolution in relation to colour vision and red coloration in reptiles using genomic and expression data. We show that turtles, but not crocodiles or lepidosaurs, possess a CYP2J19 orthologue, which arose via gene duplication before turtles and archosaurs split, and which is strongly and specifically expressed in the ketocarotenoid-containing retina and red integument. We infer that CYP2J19 initially functioned in colour vision in archelosaurs and conclude that red ketocarotenoid-based coloration evolved independently in birds and turtles via gene regulatory changes of CYP2J19 Our results suggest that red oil droplets contributed to colour vision in dinosaurs and pterosaurs.

Keywords: CYP2J; birds; carotenoid coloration; colour vision; retinal oil droplets; turtles.

Figure 1.

JTT model-based protein phylogeny based on all CYP2J, CYP2R1 and CYP2D6 sequences obtained. Bootstrap values are based on 1000 pseudoreplicates. CYP2J19-like sequences and CYP2J40-like sequences are outlined in red and blue, respectively. CYP2R1 and CYP2D6 clades have been collapsed. For fully expanded phylogeny, see the electronic supplementary material, figure S1.

Figure 2.

Results of qRT-PCR experiments quantifying male and female tissue-specific expression for CYP2J19 normalized against TBP, GAPDH and HPRT1. Error bars represent s.e.m. from three individual males and females.

Figure 3.

Reconstructed scenario for evolution of CYP2J19 function in red retinal oil droplets and red ketocarotenoid integumentary coloration in reptiles. Red lines denote the presence of red retinal oil droplets. The inferred presence of ketocarotenoid-containing retinal oil droplets coincides with the inferred duplication of CYP2J2 prior to the turtle–archosaur split, followed by subsequent loss of oil droplets and CYP2J19 in the crocodilian lineage. Red highlighted branches show the independent gain of red ketocarotenoid-based coloration in certain turtle and bird lineages associated with co-option of CYP2J19 expression for coloration.