Inter-species variation in colour perception

Inter-species variation in colour perception poses a serious problem for the view that colours are mind-independent properties. Given that colour perception varies so drastically across species, which species perceives colours as they really are? In this paper, I argue that all do. Specifically, I argue that members of different species perceive properties that are determinates of different, mutually compatible, determinables. This is an instance of a general selectionist strategy for dealing with cases of perceptual variation. According to selectionist views, objects simultaneously instantiate a plurality of colours, all of them genuinely mind-independent, and subjects select from amongst this plurality which colours they perceive. I contrast selectionist views with relationalist views that deny the mind-independence of colour, and consider some general objections to this strategy

Colour Vision in Birds : Comparing behavioural thresholds and model predictions

Birds use colour vision for many biologically relevant behaviours such as foraging and mate choice. Bird colour vision is mediated by four types of single cones, giving them an extra dimension of colour information compared to trichromatic humans. The cone photoreceptors of birds have coloured oil droplets that are assumed to increase the discriminability of colours in bright light at the cost of dim light sensitivity. In this thesis I present four studies where we have trained chickens to perform colour discrimination and tested the limits of their behavioural performance. In paper I we tested how small colour differences chickens can discriminate. This allowed us to test the predictions of the most well established model for bird colour vision, the receptor noise limited model. There was a reasonably good fit between model and behaviour. Furthermore, we tested in how dim light chickens could discriminate colours and found that the intensity threshold was affected by the colour difference between the stimuli and their intensity. In Paper II we continued testing colour discrimination in dim light and tested the hypothesis that chickens sum the signals from many photoreceptors to increase contrast sensitivity at the cost of spatial resolution in dim light, so called spatial pooling. We used food containers covered with larger, smaller, more or fewer colour patches. Supporting the hypothesis, the containers covered by more colour could be discriminated in dimmer light. In Paper III we tested colour constancy, the ability to maintain colour perception in different spectral illuminations that would otherwise confuse colour perception. Our aim was to find the largest illumination change that chicken colour constancy could tolerate. We found that chicken colour constancy could tolerate larger illumination changes when discriminating stimuli that were more different from each other. In paper IV we continued the work on colour constancy but allowed the chickens to use relative colour learning, which was specifically excluded in paper III. In Paper IV we found that their colour constancy could tolerate larger illumination changes. In nature relative colour cues are available and may be an important aspect of colour learning and perception. These results suggest that such cues can make colour constancy more robust to larger illumination changes. In both experiments chicken colour constancy was improved if they were adapted for 5 minutes in the tested illumination before performing the discrimination task. We compared the illuminations for which chickens retained colour constancy, to the difference between natural illuminations and we can conclude that chickens are well equipped to maintain accurate colour perception when changing between habitats in the wild. Objects are detected both by their chromatic and achromatic contrasts. The receptor noise limited model can be used to predict discriminability through both chromatic and achromatic vision. To use the model reliably its assumptions and predictions must be compared to behavioural results. This has been done for the chromatic version of the model but not the achromatic. In Paper V we compiled all known chromatic and achromatic contrast detection thresholds, and used them to derive the limiting noise level to be used when predicting visual discrimination in a range of animals. We discuss the limitations of using modelling in the wild such as the need to consider the spatial pattern of the stimuli and the light intensities in which the modelling occurs

Outcomes of Brood Parasite–Host Interactions Mediated by Egg Matching: Common Cuckoos Cuculus canorus versus Fringilla Finches

Antagonistic species often interact via matching of phenotypes, and interactions between brood parasitic common cuckoos (Cuculus canorus) and their hosts constitute classic examples. The outcome of a parasitic event is often determined by the match between host and cuckoo eggs, giving rise to potentially strong associations between fitness and egg phenotype. Yet, empirical efforts aiming to document and understand the resulting evolutionary outcomes are in short supply.We used avian color space models to analyze patterns of egg color variation within and between the cuckoo and two closely related hosts, the nomadic brambling (Fringilla montifringilla) and the site fidelic chaffinch (F. coelebs). We found that there is pronounced opportunity for disruptive selection on brambling egg coloration. The corresponding cuckoo host race has evolved egg colors that maximize fitness in both sympatric and allopatric brambling populations. By contrast, the chaffinch has a more bimodal egg color distribution consistent with the evolutionary direction predicted for the brambling. Whereas the brambling and its cuckoo host race show little geographical variation in their egg color distributions, the chaffinch's distribution becomes increasingly dissimilar to the brambling's distribution towards the core area of the brambling cuckoo host race.High rates of brambling gene flow is likely to cool down coevolutionary hot spots by cancelling out the selection imposed by a patchily distributed cuckoo host race, thereby promoting a matching equilibrium. By contrast, the site fidelic chaffinch is more likely to respond to selection from adapting cuckoos, resulting in a markedly more bimodal egg color distribution. The geographic variation in the chaffinch's egg color distribution could reflect a historical gradient in parasitism pressure. Finally, marked cuckoo egg polymorphisms are unlikely to evolve in these systems unless the hosts evolve even more exquisite egg recognition capabilities than currently possessed

Color vision models : some simulations, a general n-dimensional model, and the colourvision R package

The development of color vision models has allowed the appraisal of color vision independent of the human experience. These models are now widely used in ecology and evolution studies. However, in common scenarios of color measurement, color vision models may generate spurious results. Here I present a guide to color vision modeling (Chittka (1992, Journal of Comparative Physiology A, 170, 545) color hexagon, Endler & Mielke (2005, Journal Of The Linnean Society, 86, 405) model, and the linear and log-linear receptor noise limited models (Vorobyev & Osorio 1998, Proceedings of the Royal Society B, 265, 351; Vorobyev et al. 1998, Journal of Comparative Physiology A, 183, 621)) using a series of simulations, present a unified framework that extends and generalize current models, and provide an R package to facilitate the use of color vision models. When the specific requirements of each model are met, between-model results are qualitatively and quantitatively similar. However, under many common scenarios of color measurements, models may generate spurious values. For instance, models that log-transform data and use relative photoreceptor outputs are prone to generate spurious outputs when the stimulus photon catch is smaller than the background photon catch; and models may generate unrealistic predictions when the background is chromatic (e.g. leaf reflectance) and the stimulus is an achromatic low reflectance spectrum. Nonetheless, despite differences, all three models are founded on a similar set of assumptions. Based on that, I provide a new formulation that accommodates and extends models to any number of photoreceptor types, offers flexibility to build user-defined models, and allows users to easily adjust chromaticity diagram sizes to account for changes when using different number of photoreceptors

Chromatic processing in the zebrafish (Danio rerio) inner retina: bipolar cell physiology and open hardware designs for spectrally accurate stimulation under two-photon

Colour vision describes the ability of animals to differentiate objects based on their spectral reflectance properties independent of light intensity. It is an essential evolutionary trait that allows species to efficiently forage for food, avoid predation, break camouflage, communicate with conspecifics, or to find mates. Zebrafish is a powerful model for studying colour vision as it possesses four cone-photoreceptor types which can be categorised as Red-, Green-, Blue- and UV-sensitive. From first principles, its retina therefore holds the potential to process diverse chromatic computations. In the presented work, the focus was on retinal bipolar cells (BC). These are the retina’s first projection neurons. They receive inputs from the photoreceptors in the outer retina, and send their axon terminals to the inner retina, the inner plexiform layer (IPL). Diverse types within this class of interneuron shape light responses collected by the photoreceptor array into parallel channels with diverse spectral properties. BCs also make connections with all other neuron types within the retina, including horizontal cells in the outer retina, and amacrine as well as retinal ganglion cells in the inner retina. This makes them a central hub for spectral processing within the retina. By combining genetically encoded calcium indicator and two-photon microscopy, light-driven activity from larval zebrafish BC synaptic terminals was systematically recorded in vivo. Synaptic responses to tetrachromatic light stimulation unveiled an unprecedented degree of visual specialisation, including retinal regions dedicated to distinct light-guided behaviours. These regional characteristics were further correlated to functional BC types which were strongly associated with specific retinal positions and axonal stratification depths. Overall, BC projections to the inner plexiform layer displayed a sophisticated level of organisation, structured into chromatic and achromatic functional layers which systematically adjusted their response profiles across the eye to match natural spectral input statistics. Together, these findings bolster our understanding of “colour-processing” in this animal’s inner retina and suggest that unlike in mammals, teleost fish BCs already encode complex chromatic responses in the inner plexiform layer before driving retinal ganglion cells. Additionally, the study of colour vision from an organism requires precise control over the light stimuli’s temporal, spatial and spectral features. Therefore, chromatic stimulators, designed to be combined with two-photon microscopy, were developed throughout this work. These devices allowed circumventing experimental limitations, such as spectral crosstalk between the microscope and the stimulus light. Furthermore, they were conceived as open source projects to be easily replicated and adapted to any organism’s retina with different spectral sensitivities through the free control over the number and spectra of stimulation light sources. These open source projects originated from the desire to set up a stimulation standard for the field of visual neuroscience

FROM GENES TO BEHAVIOR: VARIATION IN THE VISUAL SYSTEMS OF LAKE MALAWI CICHLID FISHES

Visual systems are ideal models for the study of sensory evolution. The cichlids of Lake Malawi possess an elaborated complex of genes (opsins) that encode chromatic visual pigments, which allows us to study the evolution and diversification of chromatic vision in great detail. In this dissertation, we investigated the molecular and behavioral properties of cichlid visual systems in order to more thoroughly understand the diversification of visual systems and the behavioral consequences of these changes. The work is organized into three research projects, with the following results: (1) Opsin gene sequence variation, with corresponding functional sensitivity changes, were found for the SWS1 (ultraviolet-sensitive), SWS2B (violet-sensitive), RH2Aβ (green-sensitive), and LWS (red-sensitive) opsin genes. Of the two genera profiled, each had two variable genes, suggesting that diversifying selection acts on different opsins in each genus. Furthermore, our data suggest that the variation in the SWS1 gene has arisen recently in Lake Malawi and is under rapid selection. (2) Intraspecific cone opsin gene expression variation was found in wild populations of multiple species. Expression variation was found primarily for the LWS and SWS1 genes, while the other genes were relatively consistent within species. This finding suggests that expression can be modulated by adding genes to what may otherwise be considered a species-specific expression pattern. Quantitative models suggested that this expression variation was not the result of environmental constraint. (3) Fish raised in different ambient developmental light environments had different cone opsin gene expression, primarily in the LWS opsin gene. These expression differences caused an increase in behavioral sensitivity in the optomotor response. Furthermore, analyses indicated that the OMR response is determined solely by the LWS cone pigment, rather than a complement of different cone types. Taken together, these findings shed new light on how visual systems diversify over short evolutionary time-scales, and the possible linkage of early determinants of visual sensitivities (opsin genes) and processes that directly influence speciation (behavior)

Fragmentary Blue: Resolving the Rarity Paradox in Flower Colors

Blue is a favored color of many humans. While blue skies and oceans are a common visual experience, this color is less frequently observed in flowers. We first review how blue has been important in human culture, and thus how our perception of blue has likely influenced the way of scientifically evaluating signals produced in nature, including approaches as disparate as Goethe’s Farbenlehre, Linneaus’ plant taxonomy, and current studies of plant-pollinator networks. We discuss the fact that most animals, however, have different vision to humans; for example, bee pollinators have trichromatic vision based on UV-, Blue-, and Green-sensitive photoreceptors with innate preferences for predominantly short-wavelength reflecting colors, including what we perceive as blue. The subsequent evolution of blue flowers may be driven by increased competition for pollinators, both because of a harsher environment (as at high altitude) or from high diversity and density of flowering plants (as in nutrient-rich meadows). The adaptive value of blue flowers should also be reinforced by nutrient richness or other factors, abiotic and biotic, that may reduce extra costs of blue-pigments synthesis. We thus provide new perspectives emphasizing that, while humans view blue as a less frequently evolved color in nature, to understand signaling, it is essential to employ models of biologically relevant observers. By doing so, we conclude that short wavelength reflecting blue flowers are indeed frequent in nature when considering the color vision and preferences of bees.publishedVersio

Image calibration and analysis toolbox: a free software suite for objectively measuring reflectance, colour and pattern

Article"This is the pre-peer reviewed version of the following article: Image Calibration and Analysis Toolbox – a free software suite for objectively measuring reflectance, colour and pattern, which has been published in final form at http://onlinelibrary.wiley.com/doi/10.1111/2041-210X.12439/abstract. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving."1.Quantitative measurements of colour, pattern, and morphology are vital to a growing range of disciplines. Digital cameras are readily available and already widely used for making these measurements, having numerous advantages over other techniques, such as spectrometry. However, off-the-shelf consumer cameras are designed to produce images for human viewing, meaning that their uncalibrated photographs cannot be used for making reliable, quantitative measurements. Many studies still fail to appreciate this, and of those scientists who are aware of such issues, many are hindered by a lack usable tools for making objective measurements from photographs. 2.We have developed an image processing toolbox that generates images that are linear with respect to radiance from the RAW files of numerous camera brands, and can combine image channels from multispectral cameras, including additional ultraviolet photographs. Images are then normalised using one or more grey standards to control for lighting conditions. This enables objective measures of reflectance and colour using a wide range of consumer cameras. Furthermore, if the camera's spectral sensitivities are known, the software can convert images to correspond to the visual system (cone-catch values) of a wide range of animals, enabling human and non-human visual systems to be modelled. The toolbox also provides image analysis tools that can extract luminance (lightness), colour, and pattern information. Furthermore, all processing is performed on 32-bit floating point images rather than commonly used 8-bit images. This increases precision and reduces the likelihood of data loss through rounding error or saturation of pixels, while also facilitating the measurement of objects with shiny or fluorescent properties. 3.All cameras tested using this software were found to demonstrate a linear response within each image and across a range of exposure times. Cone-catch mapping functions were highly robust, converting images to several animal visual systems and yielding data that agreed closely with spectrometer-based estimates. 4.Our imaging toolbox is freely available as an addition to the open source ImageJ software. We believe that it will considerably enhance the appropriate use of digital cameras across multiple areas of biology, in particular researchers aiming to quantify animal and plant visual signals

Quantitative definition of phenotypic variation in land snail shells

The study of both animal colouration and patterning across the natural world has been imperative for understanding some of the key principles of biology throughout the past century, particularly with respect to evolution and genetics. Generally, colour and pattern have each been described qualitatively, often being binned into discrete groups relying on human perception of colour or pattern, rather than being considered in a biologically relevant context. ‘Binning’ traits into discrete groups has the consequence that variation within discrete morphs is often overlooked. Terrestrial gastropods, such as the selected study genera Cepaea and Auriculella, provide an ideal system for the study of polymorphisms and colour variation due to the extreme variety of morphs present across the taxa, as well as the nature of shell growth providing a complete ontogeny of an individual. The aims of this thesis are threefold; firstly, I aimed to understand finescale variation within and between established banding pattern morphs in Cepaea, to allow inferences to be made regarding the genetic mechanisms responsible for this variation. The implementation of two quantitative methods for measuring variation in band position and width in individual shells found that individual band absence has a minor but significant effect on the position of the remaining bands, implying that the locus controlling band presence/absence acts mainly after the position of bands is determined. I establish a method which is useful for comparative studies of quantitative banding variation in snail shells, and for extraction of growth parameters and morphometrics, highlighting the importance and usefulness of gastropod shells in the understanding of how variation is established and maintained in a population. Secondly, I aimed to understand the shell colour variation present in both Cepaea nemoralis and Cepaea hortensis by using spectrophotometry and psychophysical modelling in tandem. It was revealed that colour variation in Cepaea hortensis is continuous, with no detectable effects of geographic location with the exception of an association of the paleness of yellow shells with latitude. Differences between the colour of Cepaea hortensis and Cepaea nemoralis, both in terms of exact shade and overall colour were revealed; Cepaea hortensis are generally paler, and less pink-toned, but slightly more brown-toned. Precise shade variation of yellow individuals from genetically diverse lineages of Cepaea nemoralis were also detected. The results presented have significance in furthering the understanding of the precise nature of the colour polymorphism displayed in Cepaea spp., and the nature of the selection which acts upon it, as well as highlighting the importance of considering colour as a continuous trait, rather than binning it into discrete groups. Thirdly, I aimed to investigate colour variation across a number of scales in the Hawaiian land snail genus Auriculella, to allow inferences about the genetic architecture responsible for the variation, and to highlight the usefulness of museum collections of gastropod shells in understanding variation in extinct or endangered species. I demonstrated that there are differences in colour within single shells of Auriculella, similar to variation displayed by other Pacific Island snails. I described significant variation between isolated populations of the same species, and determined that there is no difference in colour variation between shells on the islands of Maui and Oahu. Finally, I demonstrated that there is no difference in colour between shell chiralities, suggesting that interchiral mating is not uncommon, and that the loci responsible for colour variation and chirality are not closely linked. By describing the variation present in Auriculella in a biologically relevant context, inference regarding genetic mechanisms of variation becomes possible in a taxa of conservation concern. By achieving these aims, and synthesising conclusions drawn from their achievement, I have highlighted the importance of accurately defining phenotypes for the purposes of evolutionary ecology and genetics. Defining phenotypes and investigating variation present within morphs has allowed inferences to be made regarding the underpinning genetic mechanisms which control variation in two gastropod genera, although the principles are applicable to other taxonomic groups. Finally, and more broadly, I have demonstrated the usefulness of gastropods as study systems, particularly where large collections of shells are available