Evolutionary history of New World monkeys revealed by molecular and fossil data

Abstract

New World monkeys (parvorder Platyrrhini) 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, the ancestral morphology, and the evolution of the distribution of the clade. Here we integrate paleontological and molecular evidence to investigate the evolutionary dynamics of extinct and extant platyrrhines. We develop an analytical framework to infer ancestral states, the evolution of body mass, and changes in latitudinal ranges through time. Our results show that extant platyrrhines originated some 5-10 million years earlier than previously assumed, likely dating back to the Middle Eocene ([~] 43 million years ago, Ma). The estimated ancestral platyrrhine was strikingly small - weighing [~] 0.4 kg, as compared to the largest modern species over 10 kg - matching the size of their presumed Eocene North African ancestors. Small-sized callitrichines (marmosets and tamarins) retained a small body mass throughout their evolutionary history, thus challenging the hypothesis of phyletic dwarfism as an explanation to their adaptive traits. In contrast, a rapid change in body mass range took place as the three families diverged between the Late Oligocene and the Early Miocene. That period also marks a peak in diversity of fossil platyrrhines and is associated with their widest latitudinal range, expanding as far to the South as Patagonia. This geographic expansion is temporally coincident with a significant increase in platyrrhine population size inferred from genomic data, and with warm and humid climatic conditions linked to the Miocene Climatic Optimum and the lower elevation of the Andes. These results unveil the early evolution of an iconic group of monkeys and showcase the advantages of integrating fossil and molecular data for estimating evolutionary rates and trends.