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).