Gene Duplication and Divergence of Long Wavelength-Sensitive Opsin Genes in the Guppy, Poecilia reticulata

Abstract

Female preference for male orange coloration in the genus Poecilia suggests a role for duplicated long wavelength-sensitive (LWS) opsin genes in facilitating behaviors related to mate choice in these species. Previous work has shown that LWS gene duplication in this genus has resulted in expansion of long wavelength visual capacity as determined by microspectrophotometry (MSP). However, the relationship between LWS genomic repertoires and expression of LWS retinal cone classes within a given species is unclear. Our previous study in the related species, Xiphophorus helleri, was the first characterization of the complete LWS opsin genomic repertoire in conjunction with MSP expression data in the family Poeciliidae, and revealed the presence of four LWS loci and two distinct LWS cone classes. In this study we characterized the genomic organization of LWS opsin genes by BAC clone sequencing, and described the full range of cone cell types in the retina of the colorful Cumaná guppy, Poecilia reticulata. In contrast to X. helleri, MSP data from the Cumaná guppy revealed three LWS cone classes. Comparisons of LWS genomic organization described here for Cumaná to that of X. helleri indicate that gene divergence and not duplication was responsible for the evolution of a novel LWS haplotype in the Cumaná guppy. This lineage-specific divergence is likely responsible for a third additional retinal cone class not present in X. helleri, and may have facilitated the strong sexual selection driven by female preference for orange color patterns associated with the genus Poecilia.

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

“…The amino acid compositions of the spectrally effective sites, that is, 180, 197, 277, 285 and 308 of the four M/LWS-type opsin genes, were as follows: Ala, His, Tyr, Thr and Ala (designated Ala/His/Tyr/Thr/Ser), respectively, in LWS-1; Pro/His/Phe/Ala/Ser in LWS-2; and Ser/His/Tyr/ Thr/Ser in LWS-3 and LWS-4, as reported previously (Watson et al, 2011). The composition was invariant within and between populations except residue 180 of LWS-1 where an Ala/Ser polymorphism was found.…”

“…We designed PCR primers (Supplementary Table S1) based on the untranslated regions of six opsin genes (SWS2-B, LWS-1, LWS-2, LWS-3, LWS-4 and SWS1), according to published sequences of Cumana guppy opsin genes (Watson et al, 2011) (GenBank accession numbers HM540108 and HM540107) and our unpublished data. The complete coding sequences of these opsin genes were amplified using these primers.…”

“…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.…”

“…Subsequently, the paralogous composition of the guppy M/ LWS opsins was found to comprise four genes (Ward et al, 2008), that is, LWS-1, LWS-2, LWS-3 and LWS-4, where the nomenclature of the first three genes follows that in the study by Sandkam et al (2013) and that of the last was renamed in this study, for simplicity. 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.…”

Developmental plasticity in vision and behavior may help guppies overcome increased turbidity

“…Guppies have nine opsin types, named for the range of wavelengths detected: one short wave-sensitive-1 (SWS1: detecting ultraviolet), two short wave-sensitive-2 (SWS2: detecting blue/purple), two midwave-sensitive (RH2: detecting green), and four long wavesensitive (LWS: detecting red/orange) opsins (Hoffmann et al 2007;Ward et al 2008;Watson et al 2011). While all opsins are thought to play a role in color vision (Archer et al 1987;Archer and Lythgoe 1990;Watson et al 2011;Sandkam et al 2015), motion detection has been shown to rely most heavily on long-wavelength sensitivity, mediated by the L-class of cone cells, which contain LWS opsins (Anstis et al 1998;Schaerer and Neumeyer 1996;Krauss and Neumeyer 2003). Thus, a rebalancing of the trade-off between color vision (involving all opsins) and motion detection (involving primarily LWS opsins) can be measured by assessing differences in the proportion of opsins in the retina that are LWS opsins for fish reared in turbid water vs. clear water.…”