Discussion
Understanding the eco-evolutionary dynamics of species interactions
remains challenging due to intrinsic complexities involved in
mutualisms, especially in species-rich communities (Hall et al. 2020).
Complexities arise from the multi-specific, mega-diversified nature of
most mutualisms among free-living species, but also from difficulties to
infer process from the simple co-phylogenetic patterns (Poisot 2015).
Seed dispersal has been hypothesized to drive coevolution between plants
and frugivores, shaping the present-day patterns of interactions and the
evolution of fruit traits (Guimarães et al 2011, 2017, Lengyel et al
2010, Rojas et al. 2012, Eriksson 2016), but empirical evidence remains
elusive both for pattern and process. We show a significant
cophylogenetic signal (CS) which is strong evidence that phylogenies of
interacting Platyrrhini primates and fleshy-fruiting Angiosperms are
congruent across the Neotropics, supporting long-standing claims that
interactions between Angiosperms and primates are shaped by coevolution
(Sussman 1991, 1995; Eriksson 2016). CS emerged independently in three
tropical rainforests (Mesoamerica, Amazonia and Atlantic Forest),
asymmetrically driven by generalist primates dispersing specialist
angiosperms. Interestingly, the consistency between the continental and
local scales evidence spatial replication of the process, and support
the idea of similar eco-evolutionary dynamics operating irrespective of
species composition in regional/biome meta-communities.
Recent estimates suggest primate origins from 55.8 to 50.3 Mya, in the
early Eocene (O’Leary et al. 2013), consistent with the rise and
dominance of modern tropical rainforests (Sussman 2017). During primate
diversification, adaptive locomotion, reproductive biology, skull
morphology, dentition and feeding niches have possibly arisen as a
coevolutionary response to fruiting plants (Sussman et al. 2013). In the
specific case of the New World primates, the divergence times in the
modern Platyrrhini is estimated to be 20.1 Mya, during the
Oligocene-Miocene boundary (Schrago 2007). This was nearly the time of
diversification of many extant lineages of fleshy-fruited Angiosperms.
Even though many families seem to have conserved fruit traits ever since
the Eocene (Eriksson et al. 2000), drupes and berries, the most consumed
fleshy-fruits by primates, have evolved much more recently. For
instance, Bolmgren & Eriksson (2005) found that almost half of
fleshy-fruited clades are younger than 40 Mya, and Eriksson (2016)
provides many examples in Arecaceae, Rubiaceae and Solanaceae with a
drastic increase in diversification between 40 to 18 Mya. This
time-scale overlap in diversification of both Neotropical primates and
fleshy-fruiting plants is consistent with our idea that seed dispersal
somehow coupled their evolutionary history.
The congruence in phylogenies was clearly driven by seed dispersal, as
evidenced from strong effects of the primate frugivory-related
variables. Chronological evidence supports the origin of primate
frugivory at the end of the first stage of Angiosperm diversification
(Eriksson 2016). As expected, the cophylogenetic relation among plants
and primates was shaped mainly by the most frugivorous taxa, although
specific plant traits were not pivotal in driving such a signal. At the
continental scale, mainly frugivores and frugivores-folivores, the major
seed dispersers (Fuzessy et al. 2016), were the feeding guilds
contributing most to the signal, whereas, not surprisingly, seed
predators had the least contribution. Seed predators (Pitheciidae) are
absent in Mesoamerican forests (Estrada et al. 2005), where
frugivore-insectivores were found to contribute the least, while
omnivores were followed by the frugivores and frugivore-folivores as
those with the highest contribution. This variation may be a consequence
of the relative importance in terms of number of species in each guild
inhabiting different regions, added to their conservation status, and
therefor the number of interactions performed. For instance, in the
Atlantic Forest, the only mainly frugivores are the Brachyteles ,
with only two species threatened by extinction. On the other hand, in
the Amazon, Ateles and the Lagothrix play the most
important role as frugivores, and are much better represented.
Recent studies on the visual adaptations of primates support intrinsic
relationships between primate diversification and the capacity to detect
plant resources (Valenta et al. 2018, Onstein et al. 2020, but see
Heymann & Fuzessy 2021). The evolution of modern primates, therefore,
may be directly related to improved means of efficiently exploiting
fleshy-fruit food resources (Sussman 2017), although in some cases
evidence is limited to particular clades and recent times (e.g., Onstein
et al. 2020). Our analysis reveals a CS at the whole phylogenetic tree,
although some clades (e.g., Atelidae) had larger contributions to the
signal. These findings, together with the evidence of an early
frugivorous habit over primate diversification (Sussman et al. 2013),
supports the prominent phylogenetic congruence in Neotropical
primate-fruit interactions driven by primate frugivore-related,
functional traits. It also provides clues that diversification is an
ongoing process, given the large contribution from recent Plathyrrini
clades.
Reconstructing the evolutionary history of plants based on fruit traits
as a response to selective pressures generated by interacting primates
is still challenging. In this case, the phenotypic responses may be more
strongly subjected to phylogenetic constraints, i.e., reflect inherited
ancestral characteristics rather than traits adapted to an ecological
niche (Jordano 1995, Valenta and Nevo 2020). Our results show that
diaspore size, key morphological constraint to the establishment of
mutualistic interactions (Dehling et al. 2014), was not an important
driver of the CS. Most studies evaluating plant adaptive responses to
mutualisms with primates based on current empirical data have found weak
evidences of phylogenetic signals (Valenta et al. 2016, Valenta et al.
2018 - fruit color; Nevo et al. 2018, Nevo et al. 2020 - fruit scent;
Valenta et al. 2016 - size, mass and hardness), a likely consequence of
the low specificity found in extant interactions.
Frugivorous birds and mammals are the major seed dispersers in the
tropics (Fleming and Kress 2011). Considering the primate-centered basis
of our dataset, and despite the low overlap in fruit consumption among
primates and other fruit-eating vertebrates, our results reflect the
trend of plants to share multiple dispersers. This is not only true for
recent times, so it is important to consider that, throughout
evolutionary history, primates were not the only interacting taxa with
the radiating fruiting plants.
At the time of Angiosperm radiation, the diversification of the earliest
modern-looking primates in parallel with that of other mammals and
fruit-eating birds, propelled the beginning of a shared evolutionary
relationship (Sussman 2017). It helps us to explain how such low
specificity prevents a detection of strong phylogenetic patterns.
However, the CS appears even in a supergeneralist system where other
frugivorous groups may be also shaping plant diversification. We also
observed an asymmetry in terms of the number of interactions performed
by each plant genera and primate species, which explained the influence
on the CS in an opposite direction: primates dispersing the greater
diversity of plants (i.e., generalists), and plants dispersed by fewer
primates (i.e., specialists), contributed the most to CS strength.
Interestingly, asymmetry is an inherent property of coevolutionary
networks that allows the long-term coexistence of the interacting
species (Bascompte et al 2006).
Besides fruits, Platyrrhini primates also include leaves, flowers,
seeds, nuts, nectar, and animal preys as feeding resource (Hawes and
Peres 2014). Distinct amounts of each item vary across taxa (Hawes and
Peres 2014), thus less frugivorous primates and other coexisting
frugivorous clades, may be acting together favoring a process known as
diffuse coevolution (Erikson 2016). It is unlikely that frugivores and
plants share a very tight coevolutionary history (Valenta and Nevo
2020), such as those observed in host-parasite interactions (Brooks
1988, Gandon 2002), or plant-pollinator interactions (Herrera 2019).
Instead, spatio-temporal asymmetries, disruptions in relationships
between patterns, and shifts between periods of coevolution among
coexisting clades should lead to reciprocal adaptive changes, ultimately
resulting in a weak process (Erikson 2016), as shown here. Primate
evolution seem to have somehow “tracked” plant radiations, resulting
in a coevolutionary history with asymmetric influences.
The multi-specific character of the process delineating the CS does not
mean that primates and plants have not coevolved or that coevolution has
necessarily been the primary force fueling diversification (see e.g.,
Althoff et al. 2014, Poisot 2015). Instead, it seems to occur in a much
more complex framework, including both direct and indirect effects
underlined by three non-exclusive main processes (Guimarães et al 2011,
2017). First, selection regimes imposed by generalized multiple-partner
interactions, such as seed dispersal, are the outcome of a complex
interplay among selection pressures operating through multiple pathways,
leading to slow, but continuous, coevolution. Coevolution repeatedly
reshapes selection regimes and species traits by speeding up the overall
diversification rate in interacting clades. Second, coevolution results
in higher trait complementarity among interacting partners (reduced
mismatch and increased trait convergence), and the level of integration
may provide a mechanism for the emergence of community-level trait
patterns. Finally, convergence tends to be higher in the presence of
super-generalists, here represented by the most frugivorous primates,
responsible to interact with a wide-range of plant species and thus
establishing the magnitude of the observed CS. Our results evidence and
indicate a strong non-random pattern in the diversification of primarily
primate-dispersed neotropical genera and their primate disperser
partners, reinforced by the replicated consistency found in three major
neotropical biomes. While the processes involved in such high-level
macroevolutionary patterns remain obscure, our approach highlights
replicated consistence over large biogeographic extents and evidences
the strong potential of highly-diversified mutualisms among free-living
species in macroevolution.