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.