Genomic organization of duplicated short wave-sensitive and long wave-sensitive opsin genes in the green swordtail, Xiphophorus helleri

Abstract

BackgroundLong wave-sensitive (LWS) opsin genes have undergone multiple lineage-specific duplication events throughout the evolution of teleost fishes. LWS repertoire expansions in live-bearing fishes (family Poeciliidae) have equipped multiple species in this family with up to four LWS genes. Given that color vision, especially attraction to orange male coloration, is important to mate choice within poeciliids, LWS opsins have been proposed as candidate genes driving sexual selection in this family. To date the genomic organization of these genes has not been described in the family Poeciliidae, and little is known about the mechanisms regulating the expression of LWS opsins in any teleost.ResultsTwo BAC clones containing the complete genomic repertoire of LWS opsin genes in the green swordtail fish, Xiphophorus helleri, were identified and sequenced. Three of the four LWS loci identified here were linked in a tandem array downstream of two tightly linked short wave-sensitive 2 (SWS2) opsin genes. The fourth LWS opsin gene, containing only a single intron, was not linked to the other three and is the product of a retrotransposition event. Genomic and phylogenetic results demonstrate that the LWS genes described here share a common evolutionary origin with those previously characterized in other poeciliids. Using qualitative RT-PCR and MSP we showed that each of the LWS and SWS2 opsins, as well as three other cone opsin genes and a single rod opsin gene, were expressed in the eyes of adult female and male X. helleri, contributing to six separate classes of adult retinal cone and rod cells with average λmax values of 365 nm, 405 nm, 459 nm, 499 nm, 534 nm and 568 nm. Comparative genomic analysis identified two candidate teleost opsin regulatory regions containing putative CRX binding sites and hormone response elements in upstream sequences of LWS gene regions of seven teleost species, including X. helleri.ConclusionsWe report the first complete genomic description of LWS and SWS2 genes in poeciliids. These data will serve as a reference for future work seeking to understand the relationship between LWS opsin genomic organization, gene expression, gene family evolution, sexual selection and speciation in this fish family.

The Genome of the Trinidadian Guppy, Poecilia reticulata, and Variation in the Guanapo Population

“…Using published opsin cDNA and genomic sequences from guppies [67, 68, 70] and from closely related poeciliid species [69], we confirmed the presence of rhodopsin and nine cone opsin genes (S3 Table). Seven are in two clusters on LG5, one including the green-sensitive RH2-1 and RH2-2, and the other including the blue sensitive SWS2A and SWS2B and three red/orange-sensitive LWS genes.…”

Divergent selection for opsin gene variation in guppy (Poecilia reticulata) populations of Trinidad and Tobago

“…In our study, the A-type was the major allele in southern Trinidad and in Tobago, whereas the S-type was the major allele in northern Trinidad (that is, the Northern Drainage and the Caroni Drainage). In the green swordtail (Xiphophorus helleri), a closely related species to the guppy, LWS-1 was reported to be the S-type (Watson et al, 2010). In a study of the four-eyed fish (Anableps anableps) (Owens et al, 2009), a close outgroup of the guppy and the swordtail, multiple M/LWStype opsin genes were also reported and residue 180 was Ser in all these genes.…”

“…However, it is also possible that it was derived secondarily from LWS-3 by gene conversion. Gene conversion has also been implicated in the generation of M/LWS gene variation in the guppy, the s wordtail and the four-eyed fish (Owens et al, 2009;Watson et al, 2010Watson et al, , 2011. The present study included samples from two populations (UA and LA) in the Aripo river that Archer and Lythgoe (1990) had also sampled and they detected sensory polymorphisms.…”

“…Downstream of two SWS2 genes (SWS2-A and SWS2-B), the LWS-1, LWS-2 and LWS-3 genes are physically linked in this numerical order, with LWS-3 in the opposite orientation (Watson et al, 2011). LWS-4 is located in a different linkage group and lacks introns (Ward et al, 2008), except intron 1 (Watson et al, 2010(Watson et al, , 2011. Based on the amino acid that corresponds to residue 180 of the human M/LWS opsins that is known to affect l max , the LWS-1, LWS-2, LWS-3 and LWS-4 genes were originally designated as A180, P180, S180 and S180r, respectively.…”

Exploring visual plasticity: dietary carotenoids can change color vision in guppies (Poecilia reticulata)

“…The wavelengths by which a cone cell is stimulated is largely determined by which opsin protein is bound to either an A1 or A2 chromophore (which chromophore is used can also change wavelength sensitivity) (Hofmann and Carleton 2009). Guppies possess nine opsin genes which are classified according to the wavelength of light they maximally detect; short wavelength sensitive 1 opsin (SWS1-detect ultraviolet), short wavelength sensitive 2 opsin (SWS2A and SWS2B-detect blues and purples), rhodopsin-like 2 opsin (RH2-1 and RH2-2-detect greens), and long wavelength sensitive opsins (LWS-1, LWS-2, LWS-3 and LWS-Rdetect reds/oranges) (Ward et al 2008;Watson et al 2010Watson et al , 2011Sandkam et al 2012;Tezuka et al 2014). Proportional measures of total retina opsin gene expression have been shown to provide a good proxy for cone cell abundance across a range of taxa including humans (Hagstrom et al 2000), killifish (Fuller et al 2005), black bream (Shand et al 2008), and cichlids (Carleton et al 2008).…”