Divergence Times and the Evolutionary Radiation of New World Monkeys (Platyrrhini, Primates): An Analysis of Fossil and Molecular Data

Primates): An Analysis of Fossil and Molecular Data. PLoS ONE 8(6): e68029. doi:10.1371/journal.pone.0068029 Divergence Times and the Evolutionary Radiation of New World Monkeys (Platyrrhini, Primates): An Analysis of Fossil and Molecular Data S. Ivan Perez 0 Marcelo F. Tejedor 0 Nelson M. Novo 0 Leandro Aristide 0 Donald James Colgan, Australian Museum, Australia 0 1 Divisio n Antropolog a at Museo de La Plata, CONICET, La Plata , Buenos Aires Province, Argentina, 2 Centro Nacional Patago nico, CONICET, Puerto Madryn, Chubut Province , Argentina The estimation of phylogenetic relationships and divergence times among a group of organisms is a fundamental first step toward understanding its biological diversification. The time of the most recent or last common ancestor (LCA) of extant platyrrhines is one of the most controversial among scholars of primate evolution. Here we use two molecular based approaches to date the initial divergence of the platyrrhine clade, Bayesian estimations under a relaxed-clock model and substitution rate plus generation time and body size, employing the fossil record and genome datasets. We also explore the robustness of our estimations with respect to changes in topology, fossil constraints and substitution rate, and discuss the implications of our findings for understanding the platyrrhine radiation. Our results suggest that fossil constraints, topology and substitution rate have an important influence on our divergence time estimates. Bayesian estimates using conservative but realistic fossil constraints suggest that the LCA of extant platyrrhines existed at ca. 29 Ma, with the 95% confidence limit for the node ranging from 27-31 Ma. The LCA of extant platyrrhine monkeys based on substitution rate corrected by generation time and body size was established between 21-29 Ma. The estimates based on the two approaches used in this study recalibrate the ages of the major platyrrhine clades and corroborate the hypothesis that they constitute very old lineages. These results can help reconcile several controversial points concerning the affinities of key early Miocene fossils that have arisen among paleontologists and molecular systematists. However, they cannot resolve the controversy of whether these fossil species truly belong to the extant lineages or to a stem platyrrhine clade. That question can only be resolved by morphology. Finally, we show that the use of different approaches and well supported fossil information gives a more robust divergence time estimate of a clade. - Funding: Supported by grants from the FONCyT (PICT-2011-0307 to SIP and PICT-2011-2520 to MFT). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. The estimation of phylogenetic relationships and divergence times among a group of organisms is a fundamental first step toward understanding its biological diversification [1,2]. Because of the importance of macroevolutionary and macroecological studies for explaining current diversity and the recent development of statistics for evolutionary inference based on time calibrated phylogenies [2,3], interest in estimating robust phylogenies and divergence times of different clades has grown significantly. Consequently, divergence times have been widely investigated among several key clades. The Order Primates is one of the most widely studied groups [46]. Among primates, the temporal divergence of the platyrrhine clade is one of the most controversial among scholars. Platyrrhines are a monophyletic group that migrated into South America and evolved in isolation from the Old World primates. Their current biodiversity stands at 100 to 125 extant species and at least 16 genera [79]. Within South America and the Caribbean, they experienced a broad radiation occupying a large range of ecological niches, resulting in a great variation in morphology and body size [7,10]. Although the most recent estimations of platyrrhine phylogeny generated topologies that are generally similar even considering differences in interpreting the position of Aotus [11] the divergence times are a cause of considerable debate [1217]. Moreover, these divergence time estimations have been used to support or contradict different higher order hypotheses which attempt to explain the shape of platyrrhine evolution. For example, Hodgson et al. [15] used mtDNA data and fossil calibrations to support the idea that platyrrhine diversification is characterized by two successive, sister-group radiations [16], the most recent of which is crown Platyrrhini, and to contradict the so called long lineages hypothesis of Rosenberger and co-workers [1720], which interprets possibly all platyrrhines, living and extinct, as belonging to a single holophyletic group, and stresses the role of morphological stasis as a deep evolutionary phenomenon. The latter hypothesis considers the oldest records of platyrrhines (certainly those from the early to middle Miocene of Patagonia and Chile and possibly those from the late Oligocene of Bolivia) as part of the crown Platyrrhini, thus phylogenetically related to the lineages of anatomically modern forms. These also include the most diverse collection of platyrrhine fossils from La Venta, Colombia, deposits of middle Miocene age. The recent studies of divergence times have used two sources of evidence to discuss estimations, the fossil record and molecular sequences [6,21,22]. The fossil record is the only direct source of evidence about the existence of an extant lineage during a time period in the past [4,5] and it relies on establishing the phylogenetic relationships among fossil and extant forms based on morphological similarities. Particularly, the age of the geological formation containing the fossil provides an unobjectionable minimum boundary for the divergence time of the lineage it represents [5]. Molecular distances between DNA or protein sequences obtained from extant species provide indirect estimations of divergence times, based on the substitutions accumulated along the phylogenetic branches during the divergence process. However, the molecular based method also use external sources of information to calibrate the substitution rates within lineages and derive estimates of divergence times of clades in years, generally fossil record and estimates of the substitution rate per generation [5,6,21,22]. Both approaches have intrinsic sources of uncertainty for divergence time estimations. For the approach that uses the fossil record directly to calibrate the molecular divergence, the uncertainty is related to problems of misclassification or dating error of the fossils [23]. In the approach that uses substitution rate per generation there is uncertainty in the estimations of generation time and substitution rates [22]. These two complementary approaches have (...truncated)