Introduction
Seed dispersal, a mutualistic interaction resulting from fruit consumption, shapes evolutionary patterns (Burin et al. 2021), and is a major engine for trait diversification in both plants and frugivores (Guimarães et al 2011, Lengyel et al 2010, Gomez & Verdu 2012, Rojas et al. 2012, but see Scott 2019). Mutual gains set the odds of interactions, and are reciprocally crucial: fruits are key resources for many vertebrates, whereas most tropical forest trees rely on fruit-eating vertebrates as dispersal vectors (Howe 2014). Frugivory has evolved independently numerous times along the evolutionary history of vertebrates. This is also true for Neotropical primates (Hawes and Peres 2014), a major order of fruit-eating vertebrates (Fleming & Kress 2011). Fruit intake is clearly related to dispersal potential, and all Platyrrhini primates routinely eat fruits (Hawes and Peres 2014). The amount of fruit in diet has significant consequences for primate seed dispersal effectiveness (Fuzessy et al 2016, 2017). Yet, the extent to which variation in the degree of frugivory explains the evolutionary history of primates shared with Angiosperms remains largely unexplored (but see Gomez and Verdú 2012).
A key knowledge gap preventing a better assessment of the role of frugivory in shaping the evolution of primates and plants lies in the difficulties in understanding the consequences of seed dispersal to the concurrent diversification of both interacting clades (DeCasien et al 2017, Scott 2019). Seed dispersal is characterized by low degrees of specialization (Stiles & Rosselli 1993, Donatti et al 2011), and most primates have generalist feeding habits (Hawes and Peres 2014). Thus, the potential of the mutual gains to promote plant-primate codiversification (correlation in speciation events) and/or coevolution (reciprocal evolutionary changes in traits) remains challenging to assess.
Considerable effort has been dedicated to uncover how Primates have diversified and to what extent behavioral, ecological and morphological traits have contributed to both speciation and extinction rates (Gittleman & Purvis, 1998; Gómez & Verdú, 2012; Harcourt, Coppeto & Parks, 2002; Isaac et al. 2005; Matthews et al. 2011; Nunn et al., 2004). Primates are socially and ecologically complex (Lefebvre et al. 2004, Dunbar and MacDonald 2013, Tran 2014), but unequivocal evidence supporting the role of frugivory and seed dispersal in primate diversification is lacking. The capacity to efficiently detect and consume fruits and disperse seeds is linked to larger range size, and higher diversification rates (Gómez & Verdú 2012, Valenta et al. 2018) and cognitive complexity (DeCasien et al. 2017). However, activity pattern, but not frugivory, is the only parameter correlated with primate diversification, with higher rates observed in diurnal primates compared to nocturnal species (Scott 2019). Considering that a diurnal habit is tightly related to primate color vision, the emerging pattern may also underscore a relationship between foraging behavior and the capacity to visually detect fruits (Kawamura 2016). For example, 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 (Smith et al. 2003).
The evolutionary consequences of seed dispersal also remain unclear from the plant perspective. The intimate relation with certain groups of vertebrates is hypothesized to promote the evolution of dispersal syndromes, i.e., the nonrandom association of plant traits with specific disperser groups (Gautier-Hion et al 1985). For instance, many studies attempted to distinguish bird-dispersed from primate-dispersed fruits (Janson 1983; Gautier-Hion et al 1985; Voigt et al 2004; Lomáscolo et al 2008), although the specificity of such syndromes remains a contentious issue (Valenta et al. 2018).
Theoretical studies on mutualistic networks suggest that the establishment of a link between two partners occurs when an interaction evolves successfully, and more species can be attached by evolutionary trait convergence (Guimarães et al 2011). Although we are still unable to draw strong evidence of the potential of seed dispersal in promoting reciprocal selective responses between closely linked primates and plants (but see Guimarães et al. 2017), recent eco-phylogenetic tools allow to assess both the shared evolutionary histories and the contribution of a particular clade to the coevolutionary dynamics (Hutchinson et al. 2017). In particular, eco-phylogenetic analysis allows the detection of a non-random shared pattern or signal in the evolutionary trajectories of unrelated species groups that interact in some way (e.g., frugivores and plants, hosts and parasites, etc.).
By estimating the cophylogenetic signals (‘CS’) in plant-primate interactions we can quantify the degree at which the topology and chronology of the phylogenies of interacting clades are congruent, and whether interaction between evolutionarily coupled taxa still occurs. Thus, CS allows more precise inferences on how ecological interactions shape diversification patterns (Balbuena et al. 2013, Aizen et al. 2016, Hutchinson et al. 2017).
Here we tested for a phylogenetic congruence in primates and plants both at continental and regional scales in the Neotropics, the most biodiverse region of the planet (Raven et al. 2020). Under a strong CS, we expect a low overlap in fruit consumption among primates and other fruit-eating vertebrates, since strong associations involve strong shared selection pressures. We further assessed whether the magnitude of CS can be explained by primate feeding guild and frugivory degree, and fruit traits known to shape seed dispersal abilities (fruit length and seed diameter). We hypothesize that CS will particularly arise in the most frugivore lineages, whereas clades with the lowest frugivory degree will contribute less to define the past history shared among Neotropical primates and Angiosperms. As for fruit traits, we expect larger fruits and seeds sizes to contribute more to CS than smaller fruits and seeds, since the former are associated to plants exclusively or primarily dispersed by primates (Jordano 1995, Valenta et al. 2018).