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

Abstract

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.

Beauty in the eyes of the beholders: colour vision is tuned to mate preference in the Trinidadian guppy (Poecilia reticulata)

“…Dissolved oxygen has been used as a proxy for differences in lighting environment elsewhere (Tezuka et al . ), yet for this environmental variable, we still found no differences between high‐ and low‐predation populations in either the Aripo ( t = −0.0354, P = 0.9736) or the Marianne ( t = −1.7165, P = 0.1954) watersheds. We also found no significant differences between high‐ and low‐predation populations within watershed for temperature (Aripo— t = −1.2522, P = 0.2817; Marianne— t = 0.3288, P = 0.7629), conductivity (Aripo— t = 4.0328, P = 0.0529; Marianne— t = 1.4242, P = 0.2332), pH (Aripo— t = −0.5048, P = 0.6593; Marianne— t = 1.8954, P = 0.1311) or total dissolved solids (Aripo— t = −0.3474, P = 0.7602; Marianne— t = 1.4661, P = 0.2218).…”

Differential Survival between Visual Environments Supports a Role of Divergent Sensory Drive in Cichlid Fish Speciation

“…This content downloaded from 130.092.009.056 on February 07, 2017 07:14:13 AM variation in visual environments and variation in fish visual properties (e.g., Carleton et al 2005;Fuller et al 2005;Davies et al 2009;Hofmann et al 2009) and signatures of selection on visual pigment genes (e.g., Terai et al 2006;Hofmann et al 2009Hofmann et al , 2012Larmuseau et al 2010;Weadick et al 2012;Tezuka et al 2014;Gaither et al 2015;TorresDowdall et al 2015). Some of the strongest evidence comes from populations of the Lake Victoria cichlids Pundamilia pundamilia and Pundamilia nyererei, in which the extent of depth segregation between these two species, causing exposure to different visual environments, correlates with the extent of divergence in visual properties, visual communication traits, and reproductive isolation .…”

Differentiation of visual spectra and nuptial colorations of two Paratanakia himantegus subspecies (Cyprinoidea: Acheilognathidae) in response to the distinct photic conditions of their habitats

“…The light environment is a factor known to drive both the reception and production of visual signals of fishes (Hornsby et al 2013;Hurtado-Gonzales et al 2014;Shin and Choi 2014;Terai et al 2006;Tezuka et al 2014). Indeed, the present study showed that the spectral sensitivities of P. h. himantegus and P. h. chii are distinct: P. h. himantegus is more sensitive than P. h. chii to longer wavelength light, while it is less sensitive than P. h. chii at shorter wavelengths.…”

“…For example, the spectral sensitivity of milkfish (Chanos chanos), humpback salmon (Oncorhynchus gorbuscha), and yellowfin tuna (Thunnus albacares) ontogenetically change to fit the photic environment during each developmental stage (Chang et al 2009a;Cheng and Flamarique 2004;Loew et al 2002). Moreover, it has been reported that spectral sensitivity has evolved to adapt to environmental light parameters in cichlids, seabreams, and moray eels (Seehausen et al 2008;Wang et al 2011;Wang et al 2009), especially, the adaptations of RH1 and LWS opsins to light environments which are documented in cichlid fishes (Sugawara et al 2005;Terai et al 2006), as well as in different populations of three-spined stickleback (Gasterosteus aculeatus) and guppy (Poecilia reticulata) (McDonald and Hawryshyn 1995;Tezuka et al 2014). The retinal photoreceptor cells of fishes utilize visual pigments, which contain a chromophore (11-cis-retinal, A1 retinal, or 11-cis-3,4-dehydroretinal, A2 retinal) and opsin, to capture photons.…”