Abstract
New World Monkeys (NWM) (platyrrhines) are one of the most diverse groups of primates, occupying today a wide range of ecosystems in the American tropics and exhibiting large variations in ecology, morphology, and behavior. Although the relationships among the almost 200 living species are relatively well understood, we lack robust estimates of the timing of origin, ancestral morphology, and geographic range evolution of the clade. Herein, we integrate paleontological and molecular evidence to assess the evolutionary dynamics of extinct and extant platyrrhines. We develop novel analytical frameworks to infer the evolution of body mass, changes in latitudinal ranges through time, and species diversification rates using a phylogenetic tree of living and fossil taxa. Our results show that platyrrhines originated 5–10 million years earlier than previously assumed, dating back to the Middle Eocene. The estimated ancestral platyrrhine was small—weighing 0.4 kg—and matched the size of their presumed African ancestors. As the three platyrrhine families diverged, we recover a rapid change in body mass range. During the Miocene Climatic Optimum, fossil diversity peaked and platyrrhines reached their widest latitudinal range, expanding as far South as Patagonia, favored by warm and humid climate and the lower elevation of the Andes. Finally, global cooling and aridification after the middle Miocene triggered a geographic contraction of NWM and increased their extinction rates. These results unveil the full evolutionary trajectory of an iconic and ecologically important radiation of monkeys and showcase the necessity of integrating fossil and molecular data for reliably estimating evolutionary rates and trends.
Highlights
The fossil record of New World Monkeys (NWM) is relatively diverse as compared with many other Neotropical animals (33 extinct genera; Tejedor and Novo 2017) but scarce in proportion to other mammals occurring in the same localities
We develop novel analytical frameworks to infer the evolution of body mass, changes in latitudinal ranges through time, and species diversification rates using a phylogenetic tree of living and fossil taxa
The mean absolute percentage error (MAPE, see Methods section) ranged from 0.11 to 0.22 for the rate parameter and the mean absolute error (MAE) between 0.11 and 0.23 for the trend parameter, in data sets with 20 fossils included, that is, fewer than those included in empirical analyses of platyrrhines (Fig. 2 and Supplementary Fig. S1 available on Dryad)
Summary
The fossil record of NWM is relatively diverse as compared with many other Neotropical animals (33 extinct genera; Tejedor and Novo 2017) but scarce in proportion to other mammals occurring in the same localities. These records conform to what is recognized as a first stage in platyrrhine evolution, with primitive and, in some cases, odd SYSTEMATIC BIOLOGY morphologies and often unclear phylogenetic positions (Rosenberger et al 2009) It was not until the Middle Miocene of Colombia, in the renowned fossiliferous area of La Venta, that the crown platyrrhines started to evolve into anatomically more modern forms, with morphologies in some cases indistinguishable from some living genera (Hartwig and Meldrum 2002, Tejedor and Novo 2017). Directional evolution is thought to be rare (Hunt 2007), it is well documented in the fossil record of several mammalian clades, including a trend towards larger body size in equids (Shoemaker and Clauset 2014) and a strong increase in brain volume in the hominin lineage (Seymour et al 2016) These issues should be important in modeling the evolution of NWMs, where the spectrum of body sizes and the geographic ranges are larger in extinct taxa than among living species. We expand the implementation of FBD process to infer speciation and extinction rates and their temporal variation while accounting for extinct and extant taxa
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