Effects of light environment during growth on the expression of cone opsin genes and behavioral spectral sensitivities in guppies (Poecilia reticulata)

Abstract

BackgroundThe visual system is important for animals for mate choice, food acquisition, and predator avoidance. Animals possessing a visual system can sense particular wavelengths of light emanating from objects and their surroundings and perceive their environments by processing information contained in these visual perceptions of light. Visual perception in individuals varies with the absorption spectra of visual pigments and the expression levels of opsin genes, which may be altered according to the light environments. However, which light environments and the mechanism by which they change opsin expression profiles and whether these changes in opsin gene expression can affect light sensitivities are largely unknown. This study determined whether the light environment during growth induced plastic changes in opsin gene expression and behavioral sensitivity to particular wavelengths of light in guppies (Poecilia reticulata).ResultsIndividuals grown under orange light exhibited a higher expression of long wavelength-sensitive (LWS) opsin genes and a higher sensitivity to 600-nm light than those grown under green light. In addition, we confirmed that variations in the expression levels of LWS opsin genes were related to the behavioral sensitivities to long wavelengths of light.ConclusionsThe light environment during the growth stage alters the expression levels of LWS opsin genes and behavioral sensitivities to long wavelengths of light in guppies. The plastically enhanced sensitivity to background light due to changes in opsin gene expression can enhance the detection and visibility of predators and foods, thereby affecting survival. Moreover, changes in sensitivities to orange light may lead to changes in the discrimination of orange/red colors of male guppies and might alter female preferences for male color patterns.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0679-z) contains supplementary material, which is available to authorized users.

Heterochronic opsin expression due to early light deprivation results in drastically shifted visual sensitivity in a cichlid fish: Possible role of thyroid hormone signaling

“…Opsin expression patterns are known to be susceptible to variation in light conditions, especially during development (Dalton, Lu, Leips, Cronin, & Carleton, ; Fuller, Carleton, Fadool, Spady, & Travis, ; Härer, Torres‐Dowdall, & Meyer, ; Hofmann, O'Quin, Smith, & Carleton, ; Novales Flamarique, ; Sakai, Ohtsuki, Kasagi, Kawamura, & Kawata, ; Wagner and Kröger, ). For instance, teleost fish reared in murky environments where short wavelength light is rapidly scattered by suspended particles, or in red light enriched environments, have opsin expression patterns resulting in visual sensitivities shifted toward longer wavelengths (Fuller et al., ; Härer et al., ).…”

Light exposure during embryonic and yolk‐sac alevin development of Chinook salmon Oncorhynchus tshawytscha does not alter the spectral phenotype of photoreceptors

“…With the exception of electroretinogram (ERG) and behavioural optomotor responses supporting enhanced sensitivity to the longer wavelength rearing spectrum in M. atlanticus (Schweikert & Grace, ), P. reticulata (Sakai et al, ) and cichlids (Smith et al, ), respectively, there is no evidence that reported plastic changes in opsin gene expression have any relevance for the visual capabilities of other fishes. Even the study on M. atlanticus (Schweikert & Grace, ) is hard to interpret as there was no control group examined, preventing any assessment of natural variation in opsin expression and ERG responses during the study period.…”

“…Besides genetically programmed opsin switches that occur during retinal development, studies on black bream Acanthopagrus butcheri (Munro 1949) (Shand et al, ), cichlids (Dalton et al, ; Härer et al, ; Nandamuri et al, ), bluefin killifish Lucania goodei Jordan 1880 (Fuller & Claricoates, ), guppies Poecilia reticulata Peters 1859 (Sakai et al, ) and Atlantic tarpon Megalops atlanticus Valenciennes 1847 (Schweikert & Grace, ) have shown plasticity in opsin gene expression in response to changes in the light environment. In guppies (Sakai et al, ) and the M. atlanticus (Schweikert & Grace, ), which seem to upregulate opsin gene products to match the dominant wavelengths of new spectral backgrounds, behavioural and electroretinogram observations suggest enhanced sensitivity to the prevalent spectrum. In contrast, both adult (Novales Flamarique et al, ) and developing (Rennison et al, ) threespine sticklebacks Gasterosteus aculeatus L. 1758 show minute, if any, plasticity in opsin expression and the same appears to be the case for other species including Atlantic molly Poecilia mexicana Steindachner 1863 (Tobler et al, ) and Atlantic cod Gadus morhua L. 1758 (Valen et al, ).…”

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

“…By increasing the relative signal received by cones expressing LWS opsins compared to those expressing RH2 opsins (the next shortest class), the red/orange colors may be perceived as brighter. Indeed, Sakai et al (2016) recently showed that guppies with higher LWS expression have a greater sensitivity to orange light. Furthermore, expression of LWS opsins has been shown to co-vary with mate preferences for orange male coloration across natural populations in Trinidad (Sandkam et al 2015a).…”

“…Traditionally, color vision was thought to only vary across species, but recent work in several taxa has found that color vision can also vary across populations [e.g., bluefin killifish (Fuller et al 2004), cichlids , stickleback (Flamarique et al 2013), guppies and close relatives (Sandkam et al 2015a, b)] which can be due to both genetic variation and plasticity (Fuller et al 2005;O'Quin et al 2012;Ehlman et al 2015; reviewed in Carleton et al 2016). Several studies have recently shown that visual systems are plastic with respect to developmental stage, time of day, and lighting environment (Fuller and Claricoates 2011;Johnson et al 2013;Flamarique et al 2013;Dalton et al 2015;Ehlman et al 2015;Sakai et al 2016).…”