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Visual Modelling Suggests a Weak Relationship Between the Evolution of Ultraviolet Vision and Plumage Colouration in Birds

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Visual Modelling Suggests a Weak Relationship Between the Evolution of Ultraviolet Vision and Plumage Colouration in Birds 1 Almost as it appears in the final version published in Journal of Evolutionary Biology (doi: 10.1111/jeb.12595) Visual modelling suggests a weak relationship between the evolution of ultraviolet vision and plumage colouration in birds Olle Lind1,2 and Kaspar Delhey3 1Department of Philosophy, Lund University 2Department of optometry and Vision Science, The University of Auckland 3School of Biological Sciences, Monash University Corresponding author: olle.lind[at]lucs.lu.se tel. +64 (0)21 08174657 Short title: Visual sensitivity and bird colours 2 Abstract Birds have sophisticated colour vision mediated by four cones types that cover a wide visual spectrum including ultraviolet (UV) wavelengths. Many birds have modest UV- sensitivity provided by violet-sensitive (VS) cones with sensitivity maxima between 400- 425 nm. However, some birds have evolved higher UV-sensitivity and a larger visual spectrum given by UV-sensitive (UVS) cones maximally sensitive at 360-370 nm. The reasons for VS-UVS transitions and their relationship to visual ecology remain unclear. It has been hypothesized that the evolution of UVS-cone vision is linked to plumage colours so that visual sensitivity and feather colouration are “matched”. This leads to the specific prediction that UVS-cone vision enhance the discrimination of plumage colours of UVS-birds while such an advantage is absent or less pronounced for VS-bird colouration. We test this hypothesis using knowledge of the complex distribution of UVS-cones among birds combined with mathematical modelling of colour discrimination during different viewing conditions. We find no support for the hypothesis, which, combined with previous studies suggests only a weak relationship between UVS-cone vision and plumage colour evolution. Instead we suggest that UVS- cone vision generally favours colour discrimination, which creates a non-specific selection pressure for the evolution of UVS-cones. 3 Introduction Many birds have conspicuous plumage colours that strongly contrast with their surroundings. It is widely accepted that the function of many such colours is to attract mating partners or deter rivals (e.g. Andersson & Amundsen, 1997; Bennett et al., 1997; Hunt et al., 1997; Andersson et al., 1998; reviews in Bennett & Cuthill, 1994; Bennett & Théry, 2007). Matching the colourful feathers, birds have well developed colour vision mediated by four types of single cones with different visual pigments; the UVS/VS (ultraviolet or violet sensitive), SWS (short-wavelength-sensitive), MWS (medium- wavelength-sensitive), and LWS-cones (long-wavelength-sensitive; Hart, 2001; fig. 1). Visual pigment sensitivity is highly conserved across bird species except for the UVS/VS pigments that exist in two variants; UVS-pigments that have sensitivity maxima between 360-370 nm, and VS-pigments that have sensitivity maxima between 400-425 nm (Bowmaker, 2008). According to this characteristic, birds fall into two major groups; birds with UVS-cones and higher UV-sensitivity, and birds with VS-cones and lower UV-sensitivity (fig. 1). Hereafter, we will refer to species within these classes simply as UVS-birds and VS-birds, and their corresponding visual systems as UVS-cone and VS- cone vision. The ancestral UVS/VS-cone in birds was of the VS-type while several independent VS-UVS transitions have led to a complex distribution of increased UV-sensitivity among species within the orders of Charadriiformes, Coraciiformes, Passeriformes, Psittaciformes, Pteroclidiformes, Trogoniformes, and possibly Struthioniformes (Ödeen & Håstad, 2013). It has been suggested that the evolution of UVS-cone vision is linked to UV-reflecting plumage feathers so that feather colouration and a higher UV-sensitivity in UVS-birds are “matched”. UV-reflecting feathers are potentially important for colour signalling in sexual communication, and studies have demonstrated that UV-reflectance in amounts relevant for vision, is ubiquitous in bird feathers (Eaton & Lanyon, 2003; Hausmann et al., 2003) while other studies indicate stronger UV-reflectance or UV- reflectance peaks at shorter wavelengths in UVS-birds (Mullen and Pohland, 2008; Ödeen et al, 2012; Bleiweiss, 2014). However, these studies rely on analyses of correlation between feather reflectance properties and visual pigment sensitivity, which represents a simplification of visual processes that has little relevance to perception and the evolution of colours signals. Instead, visual modelling provides an adequate estimate of visual perception and a powerful tool for addressing the complexity of visual ecology (Endler & Théry, 1996) and exploring the evolution of colour vision signals (e.g. Kelber et al., 2003; Delhey et al., 2013). Here, we use visual modelling to test the hypothesis of a general match between bird plumage colouration and high UV-sensitivity using extensive data on 1657 own and published reflectance spectra from 72 UVS species and 85 VS species. Material and methods Spectral data Feather reflectance data were kindly provided by M.C. Stoddard (Stoddard & Prum, 2011; 76 species, 665 spectra), obtained from our own measurements (56 species, 887 spectra), and from the literature (25 species, 105 spectra). A list of species and a more detailed description of measured plumage regions is available in Supplementary methods and table S1. We obtained reflectance spectra from live birds and museum specimen using a back-scattering probe (FCR-7UV400-2-ME, Avantes, Eerbeek, The Netherlands) connected to a spectroradiometer (Avaspec 2048, Avantes) and a pulsed Xenon light source (XE Avalight) through a bifurcated light guide (diameter 400 µm). The probe was fitted with a plastic cylinder to standardize measuring distance and angle (perpendicular to feather surface), and to exclude ambient light. Reflectance was expressed relative to a 4 UVSVS SWS MWS LWS 1 Figure 1. The spectral sensitivity of single cones in budgerigars (Melopsittacus 0.8 undulatus, black) and chicken (Gallus gallus, 0.6 grey). Cone sensitivity (normalized to 1) is the result of the transmittance of ocular 0.4 media, transmittance of oil droplets, and Sensitivity (a.u.) Sensitivity 0.2 the absorbance of the visual pigments. The UVS/VS-cone comes in two variants UVS 0 350 400 450 500 550 600 650 700 and VS, each associated with two less Wavelength (nm) differentiated variants of the SWS cones. By contrast, there is little variation in MWS and LWS cone sensitivity across species (Hart, 2001; Hart & Vorobyev, 2005). WS-2 white standard with the program Avaspec (Avantes). Reflectance data from the literature were collected by scanning plots with plot Digitizer (Huwaldt, 2010) and fit the spectral function with an 11-point running average. We used data for species with known UVS/VS-cone type that included measurements from at least two plumage patches and spectral range of at least 320 to 700 nm. For most species, the UVS/VS-cone type has been inferred based on DNA sequencing of the SWS1 opsin gene. This approach agrees well with other more direct methods such as microspectrometry (Ödeen et al. 2009), with the possible exception of the ostrich (Ödeen & Håstad 2013). All data are from male individuals and for measurements of feather reflectance at multiple angles in the literature, we included the data with the most pronounced reflectance peaks. Visual modelling The quantum catch of cone photoreceptors depends on their sensitivity given by a combination of the absorption of the visual pigment (r), the transmittance of pigmented oil droplet (p), and the transmittance of the ocular media (o) (Hart, 2001): �! � = �! � �! � � � , (1) where R is the sensitivity of cone i (i = UVS/VS, SWS, MWS, LWS). Visual pigment absorption was estimated using the Govardovskii template (Govardovskii et al., 2000), and oil droplets were assumed to function as cut-off filters as described by Hart and Vorobyev (2005). We ignored self-screening of the visual pigment that is negligible in the short photoreceptors of birds (Lind et al., 2013). The quantum catch of a cone, Q, for a visual stimulus, S, is given by: !"" � = � � � � � � � ��, ! ! !"# ! (2) where k is a scaling coefficient for cone sensitivity given by receptor adaptation and I is the illuminating spectrum given by the ambient light condition. We assumed bright light conditions and von Kries adaptation (Wyszecki & Stiles, 2000) so that the adaptation coefficient is determined as: ! �! = !"" , (3) !"# !! ! !! ! ! ! !" 5 where Sb is the spectrum of the adaptive background. We assume that chromatic discrimination is independent of intensity differences and thus given by relative quantum catch; !! �! = , (4) !!"#/!"!!!"!!!!"#!!!"# Receptor contrast, c, between the cone responses for two visual stimuli, j and k, is given by the Euclidean distance between the projection of relative cone quantum catch in receptor space; ! ! �!" = !!! �!,! − �!,! , (5) Finally, we determined contrast gain as: !!,!,!"# �!" = 100 − 1 , (6) !!,!,!" where contrast gain is the percentage increase or decrease in receptor contrast resulting from using UVS instead of VS-cone based vision (including all corresponding changes in other visual pigments, oil droplet absorbance and ocular media transmittance, Hart, 2001; Lind et al., 2914) . To estimate the performance of “average” UVS and VS-cone visual systems, we used average receptor contrasts for three UVS birds (Blackbird, Zebra finch, and Budgerigar), and three VS birds (Chicken, Pigeon, and Peafowl; model parameters are tabulated in Table S2). Calculations were carried out
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