DOI: 10.5061/dryad.6hdr7sqwn
title: Palm fruit colours are linked to the broad-scale distribution and diversification of primate colour vision systems

description: 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.
description: <b>Primate data
 </b> 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 <i>(Cacajao ayresi,
 C. hosomi </i>and <i>C. melanocephalus) </i>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 <i>n</i> = 158
 routine trichromatic primates (<i>n</i> = 126 species of
 day-active, frugivores trichromatic primates, i.e. 31% of total primates)
 and <i>n</i> = 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.
 <b>Palm data</b>
 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 <i>-ish</i> or
 <i>-ey </i>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 (<i>n</i> = 1444 palm species
 remained). <strong>Fig
 data</strong> 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 (<i>n</i> = 34 species,
 i.e. 52 African fig species with trait data were missing from the
 phylogeny).