Palm fruit colours are linked to the broad-scale distribution and diversification of primate colour vision systems

Abstract

A long-standing hypothesis in ecology and evolution is that trichromatic colour vision (the ability to distinguish red from green) in frugivorous primates has evolved as an adaptation to detect conspicuous (reddish) fruits. This could provide a competitive advantage over dichromatic frugivores which cannot distinguish reddish colours from a background of green foliage. Here, we test whether the origin, distribution and diversity of trichromatic primates is positively associated with the availability of conspicuous palm fruits, i.e. keystone fruit resources for tropical frugivores. We combine global data of colour vision, distribution and phylogenetic data for more than 400 primate species with fruit colour data for more than 1700 palm species, and reveal that species richness of trichromatic primates increases with the proportion of palm species that have conspicuous fruits, especially in subtropical African forests. By contrast, species richness of trichromats in Asia and the Americas is not positively associated with conspicuous palm fruit colours. Macroevolutionary analyses further indicate rapid and synchronous radiations of trichromats and conspicuous palms on the African mainland starting 10 Ma. These results suggest that the distribution and diversification of African trichromatic primates is strongly linked to the relative availability of conspicuous (versus non-conspicuous) palm fruits, and that interactions between primates and palms are related to the coevolutionary dynamics of primate colour vision systems and palm fruit colours.

Keywords: animal-mediated seed dispersal; coevolution; fruit coloration; plant–frugivore interaction; primatology; sensory adaptation.

Figure 1.

Global variation in trichromatic colour vision of primates and conspicuous fruit colours of palms. Maps depict the global distribution and variation of: (a) polymorphic primates, (b) routine trichromatic primates, and (c) the proportion of palms with conspicuous (i.e. yellow, red or orange) fruit colours (from a total including all palm species with primate fruits, i.e. brown, green, orange, yellow, red and purple fruits). Values are quantified at the spatial resolution of botanical countries. Grey colours indicate countries where no primate and palm species occur. (Online version in colour.)

Figure 2.

Structural equation models (SEMs) showing the effects of predictor variables on day-active, frugivorous polymorphic and trichromatic primate species richness. SEMs illustrate how the proportion of conspicuous palm fruits (red arrows) determines (a) polymorphic and (b,c) trichromatic primate richness at (a,b) the global scale (botanical country resolution) and (c) across mainland Africa (where no polymorphic primates occur) (resolution of 110 × 110 km grid cells) once direct and indirect effects of forest height, climate and area are accounted for. Effect sizes represent standardized coefficients and arrows indicate the direction of the effect, with arrow thickness being proportional to effect strength. Only statistically significant effects (at p < 0.05) are illustrated. Results are qualitatively similar to those obtained focusing on all (not only day-active, frugivorous) primates (electronic supplementary material, figures S2 and S7). prec. = annual precipitation, temp. = annual mean temperature, tseas. = temperature seasonality, pseas. = precipitation seasonality, conspicuous fruits = proportion of conspicuous palm fruits, polymorphs = day-active, frugivorous, polymorphic primate species richness, trichromats = day-active, frugivorous, routine trichromatic primate species richness. (Online version in colour.)

Figure 3.

The importance of the proportion of conspicuous palm fruits on day-active, frugivorous, trichromatic primate species richness along a gradient from arid to humid tropical climates in mainland Africa. Standardized coefficients (±s.d.) representing the effect of the proportion of conspicuous palm fruits on day-active, frugivorous, trichromatic primate species richness were obtained from structural equation models (SEMs) (n = 16). These SEMs were fitted by progressively delimiting the number of included grid cells based on the minimum number of palm food plant species richness present (see the electronic supplementary material, figure S10 for spatial delimitation). Effect strength peaks in arid-subtropical transition zones with low-to-intermediate levels of palm food plant species richness. (Online version in colour.)

Figure 4.

Diversity changes of trichromatic and polymorphic primates and conspicuous palm fruits through geological time. The pie charts reflect ancestral nodes in the phylogenies and their probability to have the focal trait, obtained from ancestral state reconstructions: trichromatic (red) or polymorphic (yellow) vision in primates (a,c,e,g) and conspicuous fruit colours (red) in palms (b,d,f,h). Globally, trichromatic primates (a) and palms (b) show rapid diversity increases at ca 10 Ma, after the innovation of polymorphic and routine trichromatic vision ca 20–30 Ma. In the Americas, (c) polymorphic primates (yellow colour in pie charts) and (d) non-conspicuous palm fruits (grey colour in pie charts) show rapid diversity increases from 10 Ma onwards. In Africa (excluding Madagascar), parallel radiations of trichromatic primates (e) and conspicuous palms (f) are initiated ca 20 Ma, with rapid diversity increases from ca 10 Ma onwards, compared to more gradual diversification of non-trichromatic African primates, and lineages with non-conspicuous palm fruits. Asia also shows rapid increases of trichromatic primates (g) from 10 Ma onwards and both palm lineages with conspicuous or non-conspicuous fruits (h) diversify rapidly during this time. (Online version in colour.)