Success of the receptor noise model in predicting colour discrimination in guppies depends upon the colours tested.

Accurate knowledge of species colour discrimination is fundamental to explain colour based behaviours and the evolution of colour patterns. We tested how the receptor noise limited model, widely used in behavioural ecology, matched actual colour discrimination thresholds obtained using behavioural tests. Guppies (Poecilia reticulata) were first trained to push a target coloured disk placed among eight grey disks of various luminances on a grey plate. Guppies were then tested to find target disks, which varied in colour contrast from the plate. The target disks followed a gradient going from high contrast to inconspicuous against the grey background. We plotted the percentage of correct choices of each colour in the gradient against the model prediction and determined the discrimination thresholds using the inflection point of the fitted sigmoid curve. We performed the experiment on six colour gradients: red, orange, yellow, green, blue and purple. Four colour gradients: red, orange, green and blue, showed a discrimination threshold that matched the model predictions. However, deviations of the model for the yellow and purple gradients suggest that ecological relevance of some colours could affect decision-making in behavioural tests and that we can no longer assume that the rules for colour discrimination are independent of colours.

How viewing objects with the dorsal or ventral retina affects colour-related behaviour in guppies (Poecilia reticulata).

Visual pigments can vary across the retina in many vertebrates, but the behavioural consequences of this retinal heterogeneity are unknown. Guppies (Poecilia reticulata) vary dorsoventrally in visual pigments and forage both on the ground and at the water surface, exposing different retinal regions to two very different visual environments. We tested guppy behaviour towards a moving stimulus presented below or above the guppy. We used 12 different narrow-band wavelength stimuli matching each of the opsin peak sensitivities presented either at the top or the bottom of our experimental apparatus. We analysed behaviours of 50 male and 50 female guppies over 4800 trials where a moving stimulus pattern was presented to each guppy. We found that wavelength, position and speed of the stimuli influenced male and female behaviour and seems to be mediated by the long wavelength sensitive photoreceptors. Males also had stronger behavioural responses than females whereas females performed more foraging-related pecking behaviour. Our results suggest that the spatial requirement of visual tasks and their ecological context are important and appear to be partly correlated with photoreceptor arrangement in the retina.

Colour pattern component phenotypic divergence can be predicted by the light environment.

The sensory drive hypothesis predicts that across different light environments sexually selected colour patterns will change to increase an animal's visual communication efficiency within different habitats. This is because individuals with more efficient signal components are likely to have more successful matings and hence produce more offspring. However, how colour pattern signals change over multiple generations under different light environmental conditions has not been tested experimentally. Here, we manipulated colour pattern signal efficiency by providing different ambient light environments over multiple generations to examine whether male colour pattern components change within large replicated populations of guppies (Poecilia reticulata). We report that colour patches change within populations over time and are phenotypically different among our three different light environments. Visual modelling suggests that the majority of these changes can be understood by considering the chroma, hue and luminance of each colour patch as seen by female guppies under each light environment. Taken together, our results support the hypothesis that different environmental conditions during signal reception can directly or indirectly drive the phenotypic diversification of visual signals within species.

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

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.

Change in male coloration associated with artificial selection on foraging colour preference.

Sensory drive proposes that natural selection on nonmating behaviours (e.g. foraging preferences) alters sensory system properties and results in a correlated effect on mating preferences and subsequently sexual traits. In colour-based systems, we can test this by selecting on nonmating colour preferences and testing for responses in colour-based female preferences and male sexual coloration. In guppies (Poecilia reticulata), individual functional links of sensory drive have been demonstrated providing an opportunity to test the process over more than one link. We measured male coloration and female preferences in populations previously artificially selected for colour-based foraging behaviour towards two colours, red and blue. We found associated changes in male coloration in the expected direction as well as weak changes in female preferences. Our results can be explained by a correlated response in female preferences due to artificial selection on foraging preferences that are mediated by a shared sensory system or by other mechanisms such as colour avoidance, pleiotropy or social experiences. This is the first experimental evidence that selection on a nonmating behaviour can affect male coloration and, more weakly, female preferences.

Male courtship decisions are influenced by light environment and female receptivity.

The appearance of animal colour signals depends jointly upon the ambient light spectrum and the signal's reflectance spectra. Light environment heterogeneity might, therefore, allow individuals to enhance their signal by signalling in an environment that increases signal efficacy. We tested this hypothesis by providing male guppies (Poecilia reticulata), a choice of three light environments in which to display their colour signal to females: green, lilac, and clear. We paired males with both receptive and non-receptive females to test whether female response might affect male behavioural decisions. Males preferred the clear environment in all trials and this environment also resulted in males having the highest average visual contrast. Sexual behaviour was influenced by complex interactions between female receptivity, light environment, and male colour pattern contrast. Males spent significantly more time in the environment in which their colour signal had the highest contrast, but only when paired with receptive females. Significant interactions between light environment and individual male colour components were also seen only in receptive trials. Our results suggest that males use light environment to enhance their colour pattern, but only in the presence of receptive females.

Variable environmental effects on a multicomponent sexually selected trait.

Multicomponent signals are made up of interacting elements that generate a functional signaling unit. The interactions between signal components and their effects on individual fitness are not well understood, and the effect of environment is even less so. It is usually assumed that color patterns appear the same in all light environments and that the effects of each color are additive. Using guppies, Poecilia reticulata, we investigated the effect of water color on the interactions between components of sexually selected male coloration. Through behavioral mate choice trials in four different water colors, we estimated the attractiveness of male color patterns, using multivariate fitness estimates and overall signal contrast. Our results show that females exhibit preferences that favor groups of colors rather than individual colors independently and that each environment favors different color combinations. We found that these effects are consistent with female guppies selecting entire color patterns on the basis of overall visual contrast. This suggests that both individuals and populations inhabiting different light environments will be subject to divergent, multivariate selection. Although the appearance of color patterns changes with light environment, achromatic components change little, suggesting that these could function in species recognition or other aspects of communication that must work across environments. Consequently, we predict different phylogenetic patterns between chromatic and achromatic signals within the same clades.

Artificial selection for food colour preferences.

Colour is an important factor in food detection and acquisition by animals using visually based foraging. Colour can be used to identify the suitability of a food source or improve the efficiency of food detection, and can even be linked to mate choice. Food colour preferences are known to exist, but whether these preferences are heritable and how these preferences evolve is unknown. Using the freshwater fish Poecilia reticulata, we artificially selected for chase behaviour towards two different-coloured moving stimuli: red and blue spots. A response to selection was only seen for chase behaviours towards the red, with realized heritabilities ranging from 0.25 to 0.30. Despite intense selection, no significant chase response was recorded for the blue-selected lines. This lack of response may be due to the motion-detection mechanism in the guppy visual system and may have novel implications for the evolvability of responses to colour-related signals. The behavioural response to several colours after five generations of selection suggests that the colour opponency system of the fish may regulate the response to selection.