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

Citation

Onstein, Renske et al. (2020), Palm fruit colours are linked to the broad-scale distribution and diversification of primate colour vision systems, Dryad, Dataset, https://doi.org/10.5061/dryad.6hdr7sqwn

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.

Methods

Primate data

We collected, inferred or interpolated data on functional traits (colour vision, diet and activity level), species distributions and phylogenetic relationships for 411 primate species (100% of total species assessed for the International Union for Conservation of Nature's Red List 2017). For the colour vision data, we classified species as routine trichromatic, polymorphic or non-trichromatic (i.e. monochromatic or dichromatic) based on 15 studies from the primary scientific literature (see Appendix S1). Polymorphic primates have males with dichromatic vision and females with dichromatic or trichromatic vision. Six primate species were excluded because their vision data was missing, and therefore 405 primate species remained. For 90 primate species, vision data was available at the family level, for 295 species at the genus level, and for 17 species at the species level. Moreover, three primate species (Cacajao ayresi, C. hosomi and C. melanocephalus) were interpolated with vision data from a species in their genus.

For diet, we classified frugivores as those primates that include fruits as part of their diet (using the 1–3 ranking in the MammalDIET dataset, the ranking indicates the relative importance of fruits in the diet as compared to other food types) (Kissling et al., 2014, for 95% matching the recent update by Gainsbury et al., 2018). For activity status, we collected data on whether a species is day-active or not (i.e. night-active or crepuscular) from the EltonTraits 1.0 database (317 primate species, Wilman et al., 2014), supplemented with data from the Handbook of the Mammals of the World: Primates (61 species, Mittermeier et al., 2013). For 27 primate species the activity data were interpolated from the genus. These species belong to eight genera, and in all of these genera the activity level is conserved (see Appendix S1). This resulted in n = 158 routine trichromatic primates (n = 126 species of day-active, frugivores trichromatic primates, i.e. 31% of total primates) and n = 126 polymorphic primates (all polymorphic primates are day-active frugivores). All trait data and references are available from Appendix S1 and Dryad 10.5061/dryad.6hdr7sqwn.

Palm data

From a total of 2557 palm species (following the World Checklist of palms, Govaerts and Dransfield, 2005), ripe fruit colour data were assembled for 1749 species (c. 70% of total) from species descriptions in primary literature, monographs, the e-monocot database and from herbaria (Royal Botanic Gardens Kew Herbarium [K], Aarhus University Herbarium [AAU]) (Kissling et al., 2019). Fruit colours can be classified as ‘non-conspicuous’ when light reflectance spectra of fruits are similar to leaves, whereas fruits can be classified as ‘conspicuous’ when spectra differ between fruits and leaves (Regan et al., 2001). Since availability of spectral measurements is limited, we measured fruit reflectance spectra from 54 fresh palm fruits belonging to 18 species and compared them to qualitative colour descriptions from the literature (for details see below). This confirmed that colour descriptions of conspicuous fruits based on human vision match up with measured fruit reflectance data (see Table S3 and Fig. S16). This is also supported by fruit reflectance data from a wider variety of plant species (Sinnott-Armstrong et al., 2018). Following (Dominy et al., 2003), we then classified orange, red, yellow and pink fruits as conspicuous, and brown, black, green, blue, cream, grey, ivory, straw-coloured, white and purple fruits as non-conspicuous. Although purple fruits could be seen as conspicuous, both dichromats and trichromats can distinguish or detect the ‘dark’ colour against the background, and here they were thus included in the ‘non-conspicuous’ classification. If a fruit was described as a combination of non-conspicuous and conspicuous colours (e.g. ‘green/yellow’, ‘yellow-brown’, ‘brown orange’) then the non-conspicuous colour was the dominant hue and the fruit colour was classified as non-conspicuous. Colours that were described with a suffix -ish or -ey were considered to have only a touch of that colour. Primates mostly feed on brown, green, orange, yellow, red and purple fruits (Fleming and Kress, 2013). Therefore, we excluded palm fruits that did not have these colours in their description from the analyses, and only included the species with brown, green, orange, yellow, red or purple fruit colours (n = 1444 palm species remained).

Fig data

Fruit colour data were assembled for all 86 African fig species (100% of figs on African mainland, thus excluding Madagascar) from the FigWeb of the Iziko Museums of Cape Town (http://www.figweb.org/Ficus/Species_index/afrotropical_species.htm). Species distribution maps of all 86 African figs were based on expert-based range maps provided by the Iziko Museums of Cape Town (for details see Kissling et al., 2007). For the phylogenetic data, we pruned the fossil-calibrated Moraceae MCC phylogenetic tree from Zhang et al. (2018) to include only African figs (n = 34 species, i.e. 52 African fig species with trait data were missing from the phylogeny).

Funding

Netherlands Organization for Scientific Research, Award: 824.15.007

Deutsche Forschungsgemeinschaft (DFG, German Research Foundation), Award: FZT 118

SYNTHESYS, Award: GB-TAF-6695