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

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.

[1]  J. Goldbogen,et al.  Independent evolution of baleen whale gigantism linked to Plio-Pleistocene ocean dynamics , 2017, Proceedings of the Royal Society B: Biological Sciences.

[2]  M. Strecker,et al.  Miocene orographic uplift forces rapid hydrological change in the southern central Andes , 2016, Scientific Reports.

[3]  N. Zimmermann,et al.  Fossils matter: improved estimates of divergence times in Pinus reveal older diversification , 2016, bioRxiv.

[4]  Anusha Ramdarshan,et al.  Neotropics provide insights into the emergence of New World monkeys: New dental evidence from the late Oligocene of Peruvian Amazonia. , 2016, Journal of human evolution.

[5]  D. Silvestro,et al.  Bridging Inter- and Intraspecific Trait Evolution with a Hierarchical Bayesian Approach. , 2016, Systematic biology.

[6]  Aaron R. Wood,et al.  First North American fossil monkey and early Miocene tropical biotic interchange , 2016, Nature.

[7]  Daniel Neuhoff,et al.  Reversible Jump Markov Chain Monte Carlo , 2016 .

[8]  D. Silvestro,et al.  Decoupled evolution of floral traits and climatic preferences in a clade of Neotropical Gesneriaceae , 2015, BMC Evolutionary Biology.

[9]  D. Duchêne,et al.  Phylogenetic patterns in the geographic distributions of birds support the tropical conservatism hypothesis , 2015 .

[10]  P. Chakrabarty,et al.  Reply to Lessios and Marko et al.: Early and progressive migration across the Isthmus of Panama is robust to missing data and biases , 2015, Proceedings of the National Academy of Sciences.

[11]  P. Chakrabarty,et al.  Biological evidence supports an early and complex emergence of the Isthmus of Panama , 2015, Proceedings of the National Academy of Sciences.

[12]  M. Bond,et al.  Eocene primates of South America and the African origins of New World monkeys , 2015, Nature.

[13]  G. Slater.  Iterative adaptive radiations of fossil canids show no evidence for diversity-dependent trait evolution , 2015, Proceedings of the National Academy of Sciences.

[14]  D. Silvestro,et al.  Measurement errors should always be incorporated in phylogenetic comparative analysis , 2015 .

[15]  R. F. Kay.  Biogeography in deep time - What do phylogenetics, geology, and paleoclimate tell us about early platyrrhine evolution? , 2015, Molecular phylogenetics and evolution.

[16]  C. Bonvicino,et al.  Multispecies Coalescent Analysis of the Early Diversification of Neotropical Primates: Phylogenetic Inference under Strong Gene Trees/Species Tree Conflict , 2014, Genome biology and evolution.

[17]  Luke J. Harmon,et al.  Geiger V2.0: an Expanded Suite of Methods for Fitting Macroevolutionary Models to Phylogenetic Trees , 2014, Bioinform..

[18]  Tanja Stadler,et al.  Bayesian Inference of Sampled Ancestor Trees for Epidemiology and Fossil Calibration , 2014, PLoS Comput. Biol..

[19]  Dong Xie,et al.  BEAST 2: A Software Platform for Bayesian Evolutionary Analysis , 2014, PLoS Comput. Biol..

[20]  M. C. Tellería,et al.  Fossil pollen records indicate that Patagonian desertification was not solely a consequence of Andean uplift , 2014, Nature Communications.

[21]  Daniele Silvestro,et al.  Bayesian estimation of speciation and extinction from incomplete fossil occurrence data. , 2014, Systematic biology.

[22]  J. Huelsenbeck,et al.  The fossilized birth–death process for coherent calibration of divergence-time estimates , 2013, Proceedings of the National Academy of Sciences.

[23]  Susanne A. Fritz,et al.  Diversity in time and space: wanted dead and alive. , 2013, Trends in ecology & evolution.

[24]  L. Harmon,et al.  Unifying fossils and phylogenies for comparative analyses of diversification and trait evolution , 2013 .

[25]  Leandro Aristide,et al.  Divergence Times and the Evolutionary Radiation of New World Monkeys (Platyrrhini, Primates): An Analysis of Fossil and Molecular Data , 2013, PloS one.

[26]  C. Jaramillo,et al.  Global Warming and Neotropical Rainforests: A Historical Perspective , 2013 .

[27]  L. Harmon,et al.  INTEGRATING FOSSILS WITH MOLECULAR PHYLOGENIES IMPROVES INFERENCE OF TRAIT EVOLUTION , 2012, Evolution; international journal of organic evolution.

[28]  W. Murphy,et al.  Macroevolutionary Dynamics and Historical Biogeography of Primate Diversification Inferred from a Species Supermatrix , 2012, PloS one.

[29]  B. O’Meara.  Evolutionary Inferences from Phylogenies: A Review of Methods , 2012 .

[30]  E. Seiffert.  Early primate evolution in Afro‐Arabia , 2012, Evolutionary anthropology.

[31]  Seraina Klopfstein,et al.  A Total-Evidence Approach to Dating with Fossils, Applied to the Early Radiation of the Hymenoptera , 2012, Systematic biology.

[32]  Liam J. Revell,et al.  phytools: an R package for phylogenetic comparative biology (and other things) , 2012 .

[33]  William A. Walters,et al.  Evolutionary Inferences from Phylogenies: A Review of Methods , 2012 .

[34]  C. Strömberg.  Evolution of Grasses and Grassland Ecosystems , 2011 .

[35]  Tanja Stadler,et al.  Mammalian phylogeny reveals recent diversification rate shifts , 2011, Proceedings of the National Academy of Sciences.

[36]  L. Sloan,et al.  Modelling the Response of Amazonian Climate to the Uplift of the Andean Mountain Range , 2010 .

[37]  L. Clerici.  Sistemática de la familia Polydolopidae (Mammalia, Marsupialia, Polydolopimorphia) de América del Sur y la Antártida , 2010 .

[38]  Kate E. Jones,et al.  PanTHERIA: a species‐level database of life history, ecology, and geography of extant and recently extinct mammals , 2009 .

[39]  P. Garber.  South American primates : comparative perspectives in the study of behavior, ecology, and conservation , 2009 .

[40]  E. Molina,et al.  Paleogeography of the South Atlantic: a Route for Primates and Rodents into the New World? , 2009 .

[41]  S. Pekar,et al.  Platyrrhine Ecophylogenetics in Space and Time , 2009 .

[42]  R. Mittermeier,et al.  The Diversity of the New World Primates (Platyrrhini): An Annotated Taxonomy , 2009 .

[43]  A. Lemmon,et al.  A likelihood framework for estimating phylogeographic history on a continuous landscape. , 2008, Systematic biology.

[44]  L. Revell.  On the Analysis of Evolutionary Change along Single Branches in a Phylogeny , 2008, The American Naturalist.

[45]  Gerald R. Dickens,et al.  An early Cenozoic perspective on greenhouse warming and carbon-cycle dynamics , 2008, Nature.

[46]  S. Cachel.  Primate adaptation and evolution , 1989, International Journal of Primatology.

[47]  G. Conroy.  Problems of body-weight estimation in fossil primates , 1987, International Journal of Primatology.

[48]  E. Ortiz-Jaureguizar,et al.  Paleoenvironmental evolution of southern South America during the Cenozoic , 2006 .

[49]  M. E. Palacios,et al.  New primate genus from the Miocene of Argentina. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[50]  J. J. Flynn,et al.  Ancestral state reconstruction of body size in the Caniformia (Carnivora, Mammalia): the effects of incorporating data from the fossil record. , 2006, Systematic biology.

[51]  M. Tejedor.  Primate canines from the early Miocene Pinturas Formation, Southern Argentina. , 2002, Journal of human evolution.

[52]  T. Setoguchi,et al.  New fossil materials of the earliest new world monkey, Branisella boliviana, and the problem of platyrrhine origins. , 2000, American journal of physical anthropology.

[53]  M. Stephens.  Bayesian analysis of mixture models with an unknown number of components- an alternative to reversible jump methods , 2000 .

[54]  P. Green.  Reversible jump Markov chain Monte Carlo computation and Bayesian model determination , 1995 .

[55]  A. Rosenberger,et al.  Szalatavus attricuspis, an early platyrrhine primate. , 1991, Folia primatologica; international journal of primatology.

[56]  R. Pascual,et al.  Evolving climates and mammal faunas in Cenozoic South America , 1990 .

[57]  J. Felsenstein.  Phylogenies and quantitative characters , 1988 .

[58]  J. Felsenstein.  Phylogenies and the Comparative Method , 1985, The American Naturalist.

[59]  P. Gingerich,et al.  Allometric scaling in the dentition of primates and prediction of body weight from tooth size in fossils. , 1982, American journal of physical anthropology.

[60]  D. Tarling.  The Geologic Evolution of South America with Special Reference to the Last 200 Million Years , 1980 .

[61]  M. Novacek,et al.  Evolutionary Biology of the New World Monkeys and Continental Drift , 1980, Advances in Primatology.

[62]  W. K. Hastings,et al.  Monte Carlo Sampling Methods Using Markov Chains and Their Applications , 1970 .

[63]  N. Metropolis,et al.  Equation of State Calculations by Fast Computing Machines , 1953, Resonance.