Evolution of CYP2J19, a gene involved in colour vision and red coloration in birds: positive selection in the face of conservation and pleiotropy

Abstract

BackgroundExaggerated signals, such as brilliant colours, are usually assumed to evolve through antagonistic coevolution between senders and receivers, but the underlying genetic mechanisms are rarely known. Here we explore a recently identified “redness gene”, CYP2J19, that is highly interesting in this context since it encodes a carotenoid-modifying enzyme (a C4 ketolase involved in both colour signalling and colour discrimination in the red (long wavelength) spectral region.)ResultsA single full-length CYP2J19 was retrieved from 43 species out of 70 avian genomes examined, representing all major avian clades. In addition, CYP2J19 sequences from 13 species of weaverbirds (Ploceidae), seven of which have red C4-ketocarotenoid coloration were analysed. Despite the conserved retinal function and pleiotropy of CYP2J19, analyses indicate that the gene has been positively selected throughout the radiation of birds, including sites within functional domains described in related CYP (cytochrome P450) loci. Analyses of eight further CYP loci across 25 species show that positive selection is common in this gene family in birds. There was no evidence for a change in selection pressure on CYP2J19 following co-option for red coloration in the weaverbirds.ConclusionsThe results presented here are consistent with an ancestral conserved function of CYP2J19 in the pigmentation of red retinal oil droplets used for colour vision, and its subsequent co-option for red integumentary coloration. The cause of positive selection on CYP2J19 is unclear, but may be partly related to compensatory mutations related to selection at the adjacent gene CYP2J40.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1136-y) contains supplementary material, which is available to authorized users.

Testosterone regulates CYP2J19 -linked carotenoid signal expression in male red-backed fairywrens ( Malurus melanocephalus )

“…Our results corroborate a growing number of studies suggesting the importance of CYP2J19 for red coloration in birds [23,24,82,83] and other animals [84,85]. The genetic basis of carotenoid-based coloration is not yet well resolved [3,32], but a handful of genes with large effects have been identified in recent years that are associated with carotenoid coloration (e.g.…”

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.…”

Red and White Chinook Salmon (Oncorhynchus tshawytscha): Differences in the Transcriptome Profile of Muscle, Liver, and Pylorus

“…Recently, two molecular studies in coloration of two mutant bird systems: the yellowbeak in zebra finch mutant (Mundy et al 2016) and the red factor in canary (Lopes et al 2016) have identified a gene, Cyp2j19, as a ketolase responsible for the conversion of yellow dietary carotenoids into red ketocarotenoids. A single copy of Cyp2j19 appears to be widespread across avian lineages (Twyman et al 2018).…”