**1. Introduction**

28 Zoology

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Primate colour vision has intrigued scientists for many decades and will likely continue to do so for the foreseeable future. Primates are the most visually adapted order of mammals and a considerable proportion of their large brain size is devoted to processing visual information (e.g. Barton, 2006). Most eutherian mammals have dichromatic (two-colour) vision, and chromatic distinctions are based on discriminating relatively shorter from relatively longer wavelengths within the visual spectrum (~400-700nm). These distinctions are made by neural comparison of cone cells possessing short (S) wavelength-sensitive photopigments, which are maximally sensitive to bluish light, and long (L) wavelengthsensitive pigments, which are maximally sensitive to greenish light. These photopigments are encoded by an autosomal S opsin gene and an X-chromosomal L opsin gene respectively. Primates have an additional colour channel enabling trichromatic vision via a duplication and divergence of the L opsin gene, resulting in long and middle (L-M) wavelength-sensitive photopigments (reviewed in Hunt et al., 2009; Regan et al., 2001). This arrangement permits enhanced discrimination of light and perception of different shades of green, yellow, orange and red.

Old World monkeys, apes and humans are routinely trichromatic, having two loci for L-M opsin genes on each X-chromosome due to a gene duplication event (Jacobs, 2008), in addition to the autosomal S opsin locus. Alternatively, New World monkeys and some lemurs exhibit polymorphic trichromacy (Jacobs, 2007; Tan & Li, 1999; Tan et al., 2005; Veilleux & Bolnick, 2009). This alternate path to trichromacy results from a genetic polymorphism at a single locus of the X-chromosomal L-M opsin gene. Females with two different L-M opsin genes, combined with the common autosomal S opsin gene, possess trichromacy (Mollon et al., 1984). However, males, being hemizygotes, can inherit only one L-M opsin gene and are always dichromatic; homozygous females are also dichromatic. Variation in primate trichromacy and the selective pressures that led to trichromacy are under considerable debate (Caine et al., 2010).

Protein Limitation Explains Variation in Primate

2011).

*geoffreyi*, Kuhl, 1820).

regarding the evolution of trichromacy.

(Araújo et al., 2008; Jacobs et al., 1996).

**3. The young leaf hypothesis** 

**2.1 Problems with the frugivory hypothesis** 

Colour Vision Phenotypes: A Unified Model for the Evolution of Primate Trichromatic Vision 31

(*Cebus capucinus*, Linnaeus, 1758) population, monkeys possessing the phenotype with the most spectrally separated L-M opsin alleles showed the highest acceptance index for red fruits (Melin et al., 2009). For this same population of capuchin monkeys, colourful fruits comprise 60% of the diet and are preferred to cryptically coloured fruits (Melin,

Trichromatic vision may also afford a selective advantage by allowing trichromats to forage on fruit under a greater range of light conditions than dichromats (Yamashita et al., 2005). In two species of *Saguinus* (Hoffmannsegg, 1807), captive trichromatic individuals were more efficient than dichromats at selecting ripe fruits, both in isolation and against a background of leaves (Smith et al., 2003). In a study linking nutritional value to fruit colouration, Riba-Hernandez et al. (2005) have provided additional support for this hypothesis. Arguing that the principle reward of ripe fruits is sugar, these authors demonstrated a positive correlation between fruit glucose content and the red-green colour channel of spider monkeys (*Ateles* 

In summary, the evidence for a ripe fruit foraging advantage for trichromats is compelling. Behavioural evidence for ripe fruit foraging advantages in wild and captive trichromats, the trichromat-accessible colour space of tropical fruits, the dietary importance of colourful fruits, and a positive correlation between nutritional value and fruit colouration all indicate that a ripe fruit foraging advantage may indeed result in the evolution and persistence of trichromacy. However, the frugivory hypothesis is problematic on several accounts. In the sections below, we review problems with the frugivory hypothesis and alternate hypotheses

There is compelling empirical evidence that trichromacy is not necessary for detection of ripe fruits. Dominy and Lucas (2001) found that four routinely trichromatic catarrhine species in Uganda did not choose fruit on the basis of chromaticity, and that consumed fruits did not differ in chromaticity from unconsumed fruits. Comparing routinely trichromatic *Alouatta palliata* (Gray, 1849) fruit choices with polymorphically trichromatic *Ateles geoffroyi* in Costa Rica, Stoner et al. (2005) found that, contrary to expectations of a fruit foraging advantage for trichromats, the polymorphic *Ateles* consumed reddish fruits more often while routinely trichromatic *Alouatta* concentrated primarily on green fruits. Further studies of wild primates have also demonstrated that trichromats do not feed on brightly coloured fruits at faster rates than dichromats (Hiramatsu et al., 2008; Vogel et al., 2007). Additionally many fruits that are consumed and dispersed by primates are dull, and green or brown (Janson, 1983; Link & Stevenson, 2004), colours that can be detected through the blue-yellow colour channel of the dichromat (Dominy & Lucas, 2001). Intriguingly, the only genus of routinely trichromatic platyrrhine, *Alouatta*, is not a frugivore, but a folivore

Many frugivorous primates, and specifically catarrhines, rely on leaves as fallback foods during periods of habitat-wide fruit scarcity (Lucas et al., 2003). Building on this observation, Dominy and Lucas (2001) argued that it is the ability to distinguish young

In order to evaluate routine and polymorphic trichromacy in primates within an evolutionary framework, it is necessary to review the behavioural, experimental, genetic, biogeographical and ecological evidence pertaining to primate trichromacy. We focus this review on the evidence for and against foraging hypotheses because the vast majority of research to date evaluates and supports the utility of trichromacy for finding and selecting food. We begin with an overview of the fruit foraging and the young leaf hypotheses. We additionally introduce a new hypothesis - that both routine and polymorphic trichromacy confer a selective advantage to primates in the detection and selection of proteinaceous foods (either leaves or fruit), and present evidence for *Ficus* (Moraceae) as a protein source for neotropical primates. To explain the foundation for this new hypothesis, we review primate foraging patterns on *Ficus*, and discuss the abundance and density of *Ficus* in African and neotropical forests.
