Daniel Osorio

Tetrachromacy, oil droplets and bird plumage colours

Abstract There is a growing body of data on avian eyes, including measurements of visual pigment and oil droplet spectral absorption, and of receptor densities and their distributions across the retina. These data are sufficient to predict psychophysical colour discrimination thresholds for light-adapted eyes, and hence provide a basis for relating eye design to visual needs. We examine the advantages of coloured oil droplets, UV vision and tetrachromacy for discriminating a diverse set of avian plumage spectra under natural illumination. Discriminability is enhanced both by tetrachromacy and coloured oil droplets. Oil droplets may also improve colour constancy. Comparison of the performance of a pigeons eye, where the shortest wavelength receptor peak is at 410 nm, with that of the passerine Leiothrix, where the ultraviolet-sensitive peak is at 365 nm, generally shows a small advantage to the latter, but this advantage depends critically on the noise level in the sensitivity mechanism and on the set of spectra being viewed.

Animal colour vision – behavioural tests and physiological concepts

Over a century ago workers such as J. Lubbock and K. von Frisch developed behavioural criteria for establishing that non‐human animals see colour. Many animals in most phyla have since then been shown to have colour vision. Colour is used for specific behaviours, such as phototaxis and object recognition, while other behaviours such as motion detection are colour blind. Having established the existence of colour vision, research focussed on the question of how many spectral types of photoreceptors are involved. Recently, data on photoreceptor spectral sensitivities have been combined with behavioural experiments and physiological models to study systematically the next logical question: ‘what neural interactions underlie colour vision ?‘This review gives an overview of the methods used to study animal colour vision, and discusses how quantitative modelling can suggest how photoreceptor signals are combined and compared to allow for the discrimination of biologically relevant stimuli.

Colour Vision as an Adaptation to Frugivory in Primates

Most mammals possess two classes of cone, sensitive to short and to long wavelengths of light, but Old World primates (Catarrhini) have distinct medium and long wavelength sensitive classes. The sensitivities of these cones photopigments are alike in all catarrhines with peaks at about 440 nm (‘blue’), 533 nm (‘green’) and 565 nm (‘red’). One possible reason for the evolution and conservatism of catarrhine trichromacy is that colour vision is a specialization for finding food. A model of retinal coding of natural spectra, based on discrimination thresholds, is used to examine the usefulness of dichromatic and trichromatic vision for finding fruit, and for identifying fruit and leaves by colour. For identification tasks the dichromat’s eye is almost as good as a trichromat’s, but the trichromat has an advantage for detecting fruit against a background of leaves.

Photoreceptor spectral sensitivities in terrestrial animals: Adaptations for luminance and colour vision

This review outlines how eyes of terrestrial vertebrates and insects meet the competing requirements of coding both spatial and spectral information. There is no unique solution to this problem. Thus, mammals and honeybees use their long-wavelength receptors for both achromatic (luminance) and colour vision, whereas flies and birds probably use separate sets of photoreceptors for the two purposes. In particular, we look at spectral tuning and diversification among ‘long-wavelength’ receptors (sensitivity maxima at greater than 500 nm), which play a primary role in luminance vision. Data on spectral sensitivities and phylogeny of visual photopigments can be incorporated into theoretical models to suggest how eyes are adapted to coding natural stimuli. Models indicate, for example, that animal colour vision—involving five or fewer broadly tuned receptors—is well matched to most natural spectra. We can also predict that the particular objects of interest and signal-to-noise ratios will affect the optimal eye design. Nonetheless, it remains difficult to account for the adaptive significance of features such as co-expression of photopigments in single receptors, variation in spectral sensitivities of mammalian L-cone pigments and the diversification of long-wavelength receptors that has occurred in several terrestrial lineages.

Evolution and selection of trichromatic vision in primates

Trichromatic colour vision is of considerable importance to primates but is absent in other eutherian mammals. Primate colour vision is traditionally believed to have evolved for finding food in the forest. Recent work has tested the ecological importance of trichromacy to primates, both by measuring the spectral and chemical properties of food eaten in the wild, and by testing the relative foraging abilities of dichromatic and trichromatic primates. Molecular studies have revealed the genetic mechanisms of the evolution of trichromacy, and are providing new insight into visual pigment gene expression and colour vision defects. By drawing together work from these different fields, we can gain a better understanding of how natural selection has shaped the evolution of trichromatic colour vision in primates and also about mechanisms of gene duplication, heterozygote advantage and balancing selection.

A review of the evolution of animal colour vision and visual communication signals.

The visual displays of animals and plants are often colourful, and colour vision allows animals to respond to these signals as they forage for food, choose mates and so-forth. This article discusses the evolutionary relationship between photoreceptor spectral sensitivities of four groups of land animals--birds, butterflies, primates and hymenopteran insects (bees and wasps)--, the colour signals that are relevant to them, and how understanding is informed by models of spectral coding and colour vision. Although the spectral sensitivities of photoreceptors are known to vary adaptively under natural selection there is little evidence that those of hymenopterans, birds and primates are specifically adapted to the reflectance spectra of food plants or animal visual signals. On the other hand, the colours of fruit, flowers and feathers may have evolved to be more discriminable for the colour vision of their natural receivers than for other groups of animals. Butterflies are unusual in that they have enjoyed a major radiation in receptor numbers and spectral sensitivities. The reasons for the radiation and diversity of butterfly colour vision remain unknown, but may include their need to find food plants and to select mates.

Detection of fruit and the selection of primate visual pigments for color vision

Primates have X chromosome genes for cone photopigments with sensitivity maxima from 535 to 562 nm. Old World monkeys and apes (catarrhines) and the New World (platyrrhine) genus Alouatta have separate genes for 535‐nm (medium wavelength; M) and 562‐nm (long wavelength; L) pigments. These pigments, together with a 425‐nm (short wavelength) pigment, permit trichromatic color vision. Other platyrrhines and prosimians have a single X chromosome gene but often with alleles for two or three M/L photopigments. Consequently, heterozygote females are trichromats, but males and homozygote females are dichromats. The criteria that affect the evolution of M/L alleles and maintain genetic polymorphism remain a puzzle, but selection for finding food may be important. We compare different types of color vision for detecting more than 100 plant species consumed by tamarins (Saguinus spp.) in Peru. There is evidence that both frequency‐dependent selection on homozygotes and heterozygote advantage favor M/L polymorphism and that trichromatic color vision is most advantageous in dim light. Also, whereas the 562‐nm allele is present in all species, the occurrence of 535‐ to 556‐nm alleles varies between species. This variation probably arises because trichromatic color vision favors widely separated pigments and equal frequencies of 535/543‐ and 562‐nm alleles, whereas in dichromats, long‐wavelength pigment alleles are fitter.

The effect of colour vision status on the detection and selection of fruits by tamarins (Saguinus spp.)

SUMMARY The evolution of trichromatic colour vision by the majority of anthropoid primates has been linked to the efficient detection and selection of food, particularly ripe fruits among leaves in dappled light. Modelling of visual signals has shown that trichromats should be more efficient than dichromats at distinguishing both fruits from leaves and ripe from unripe fruits. This prediction is tested in a controlled captive setting using stimuli recreated from those actually encountered by wild tamarins (Saguinus spp.). Dietary data and reflectance spectra of Abuta fluminum fruits eaten by wild saddleback (Saguinus fuscicollis) and moustached (Saguinus mystax) tamarins and their associated leaves were collected in Peru. A. fluminum leaves, and fruits in three stages of ripeness, were reproduced and presented to captive saddleback and red-bellied tamarins (Saguinus labiatus). Trichromats were quicker to learn the task and were more efficient at selecting ripe fruits than were dichromats. This is the first time that a trichromatic foraging advantage has been demonstrated for monkeys using naturalistic stimuli with the same chromatic properties as those encountered by wild animals.

Evolution and function of routine trichromatic vision in primates.

Abstract Evolution of the red-green visual subsystem in trichromatic primates has been linked to foraging advantages, namely the detection of either ripe fruits or young leaves amid mature foliage. We tested competing hypotheses globally for eight primate taxa: five with routine trichromatic vision, three without. Routinely trichromatic species ingested leaves that were “red shifted” compared to background foliage more frequently than species lacking this trait. Observed choices were not the reddest possible, suggesting a preference for optimal nutritive gain. There were no similar differences for fruits although red-greenness may sometimes be important in close-range fruit selection. These results suggest that routine trichromacy evolved in a context in which leaf consumption was critical.

Color signals in natural scenes: characteristics of reflectance spectra and effects of natural illuminants

Multispectral images of natural scenes were collected from both forests and coral reefs to represent typical, complex scenes that might be viewed by modern animals. Both reflectance spectra and modeled visual color signals in these scenes were decorrelated spectrally by principal-component analysis. Nearly 98% of the variance of reflectance spectra and color signals can be described by the first three principal components for both forest and coral reef scenes, which implies that three well-designed visual channels can recover almost all of the spectral information of natural scenes. A variety of natural illuminants affects color signals of forest scenes only slightly, but the variation in ambient irradiance spectra that is due to the absorption of light by water has dramatic influences on the spectral characteristics of coral reef scenes.