Intra-retinal variation of opsin gene expression in the guppy (<i>Poecilia reticulata</i>)

Rennison, Diana J.; Owens, Gregory L.; Allison, W. Ted; Taylor, John S.

doi:10.1242/jeb.057836

Cited by 20 publications

(29 citation statements)

References 40 publications

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“…Thus, there may be further variation in l max among the four M/LWS loci, and there is a further possibility of allelic differentiation in the four loci related to l max because of amino acid variations other than the five sites as well as different expression patterns. The sensory variation could also be related to interindividual variation in the relative expression levels among opsin loci, as found in the Venezuelan guppies (Rennison et al, 2011). Direct measurements of l max for the reconstituted photopigments and quantification of the expression of the alleles are necessary to resolve these questions.…”

Section: Discussionmentioning

confidence: 99%

“…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. More recently, studies have demonstrated intraretinal variations and age/sex differences in opsin gene expression in guppies (Laver and Taylor, 2011;Rennison et al, 2011). Despite these advances, the genetic basis of interindividual sensory variation and the selection forces that maintain this variation remain unexplored.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2014

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The guppy is known to exhibit remarkable interindividual variations in spectral sensitivity of middle to long wavelength-sensitive (M/LWS) cone photoreceptor cells. The guppy has four M/LWS-type opsin genes (LWS-1, LWS-2, LWS-3 and LWS-4) that are considered to be responsible for this sensory variation. However, the allelic variation of the opsin genes, particularly in terms of their absorption spectrum, has not been explored in wild populations. Thus, we examined nucleotide variations in the four M/LWS opsin genes as well as blue-sensitive SWS2-B and ultraviolet-sensitive SWS1 opsin genes for comparison and seven non-opsin nuclear loci as reference genes in 10 guppy populations from various light environments in Trinidad and Tobago. For the first time, we discovered a potential spectral variation (180 Ser/Ala) in LWS-1 that differed at an amino acid site known to affect the absorption spectra of opsins. Based on a coalescent simulation of the nucleotide variation of the reference genes, we showed that the interpopulation genetic differentiation of two opsin genes was significantly larger than the neutral expectation. Furthermore, this genetic differentiation was significantly related to differences in dissolved oxygen (DO) level, and it was not explained by the spatial distance between populations. The DO levels are correlated with eutrophication that possibly affects the color of aquatic environments. These results suggest that the population diversity of opsin genes is significantly driven by natural selection and that the guppy could adapt to various light environments through color vision changes.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2014

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“…The MSP data further suggests that some individuals may be expressing at least one different LWS as a double cone with peak absorption at 526/533 nm or as a twin cone with λ max of 553/553 nm but never both. At this point, we have no conclusive evidence suggesting that the LWS photopigments are either polymorphic or sex-linked (as in guppies [22], [52], [54], [72], [73], [74]), despite the extreme male color polymorphism. Our sample size is low and more in depth sampling across populations may perhaps reveal a sex-linked pattern of polymorphism.…”

Section: Discussionmentioning

confidence: 74%

“…Possible hexachromatic eyes would be composed of the following photoreceptors combinations (i) 355–407–456–526–533–543; and, (ii) 355–407–456–526–533–553. The choice of these two modeling approaches is based on our current knowledge of the differential expression of the SWS1, SWS2B, SWS2A, RH2 and LWS opsin subfamilies (often expressed in double cones) in Cyprinodontiformes, which suggests either a penta- or hexachromatic vision for these fishes (e.g., [50], [51], [52]). …”

Section: Methodsmentioning

confidence: 99%

Variation in the Visual Habitat May Mediate the Maintenance of Color Polymorphism in a Poeciliid Fish

Hurtado-Gonzales

Loew

2014

PLoS ONE

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The conspicuousness of animal signals is influenced by their contrast against the background. As such, signal conspicuousness will tend to vary in nature because habitats are composed of a mosaic of backgrounds. Variation in attractiveness could result in variation in conspecific mate choice and risk of predation, which, in turn, may create opportunities for balancing selection to maintain distinct polymorphisms. We quantified male coloration, the absorbance spectrum of visual pigments and the photic environment of Poecilia parae, a fish species with five distinct male color morphs: a drab (i.e., grey), a striped, and three colorful (i.e., blue, red and yellow) morphs. Then, using physiological models, we assessed how male color patterns can be perceived in their natural visual habitats by conspecific females and a common cichlid predator, Aequidens tetramerus. Our estimates of chromatic and luminance contrasts suggest that the three most colorful morphs were consistently the most conspicuous across all habitats. However, variation in the visual background resulted in variation in which morph was the most conspicuous to females at each locality. Likewise, the most colorful morphs were the most conspicuous morphs to cichlid predators. If females are able to discriminate between conspicuous prospective mates and those preferred males are also more vulnerable to predation, variable visual habitats could influence the direction and strength of natural and sexual selection, thereby allowing for the persistence of color polymorphisms in natural environments.

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“…Of note, LWS‐4 expression has only been reported in the peripheral‐dorsal retina of some individuals (Rennison et al. ), its role in guppy vision is currently unknown and it is the only Rh2 or LWS opsin that is found on a separate chromosome (e.g., Künstner et al. ; Watson et al.…”

Section: Resultsmentioning

confidence: 99%

Light environment change induces differential expression of guppy opsins in a multi‐generational evolution experiment

et al. 2018

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Light environments critically impact species that rely on vision to survive and reproduce. Animal visual systems must accommodate changes in light that occur from minutes to years, yet the mechanistic basis of their response to spectral (color) changes is largely unknown. Here, we used a laboratory experiment where replicate guppy populations were kept under three different light environments for up to 8-12 generations to explore possible differences in the expression levels of nine guppy opsin genes. Previous evidence for opsin expression-light environment "tuning" has been either correlative or focused exclusively on the relationship between the light environment and opsin expression over one or two generations. In our multigeneration experiment, the relative expression levels of nine different guppy opsin genes responded differently to light environment changes: some did not respond, while others differed due to phenotypic plasticity. Moreover, for the LWS-1 opsin we found that, while we observed a wide range of plastic responses under different light conditions, common plastic responses (where the population replicates all followed the same trajectory) occurred only after multigenerational exposure to different light environments. Taken together this suggests that opsin expression plasticity plays an important role in light environment "tuning" in different light environments on different time scales, and, in turn, has important implications for both visual system function and evolution.

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Intra-retinal variation of opsin gene expression in the guppy (Poecilia reticulata)

Cited by 20 publications

References 40 publications

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

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

Variation in the Visual Habitat May Mediate the Maintenance of Color Polymorphism in a Poeciliid Fish

Light environment change induces differential expression of guppy opsins in a multi‐generational evolution experiment

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