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BMC Evolutionary Biology Biomed Central BMC Evolutionary Biology BioMed Central Research article Open Access Estimating the phylogeny and divergence times of primates using a supermatrix approach Helen J Chatterjee*†1, Simon YW Ho†2,3, Ian Barnes†4 and Colin Groves†5 Address: 1Research Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, UK, 2Department of Zoology, University of Oxford, Oxford OX1 3PS, UK, 3Centre for Macroevolution and Macroecology, Research School of Biology, Australian National University, Canberra, ACT 0200, Australia, 4School of Biological Sciences, Royal Holloway University of London, Egham, Surrey, TW20 0EX, UK and 5School of Archaeology and Anthropology, Australian National University, Canberra, ACT 0200, Australia Email: Helen J Chatterjee* - [email protected]; Simon YW Ho - [email protected]; Ian Barnes - [email protected]; Colin Groves - [email protected] * Corresponding author †Equal contributors Published: 27 October 2009 Received: 8 April 2009 Accepted: 27 October 2009 BMC Evolutionary Biology 2009, 9:259 doi:10.1186/1471-2148-9-259 This article is available from: http://www.biomedcentral.com/1471-2148/9/259 © 2009 Chatterjee et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: The primates are among the most broadly studied mammalian orders, with the published literature containing extensive analyses of their behavior, physiology, genetics and ecology. The importance of this group in medical and biological research is well appreciated, and explains the numerous molecular phylogenies that have been proposed for most primate families and genera. Composite estimates for the entire order have been infrequently attempted, with the last phylogenetic reconstruction spanning the full range of primate evolutionary relationships having been conducted over a decade ago. Results: To estimate the structure and tempo of primate evolutionary history, we employed Bayesian phylogenetic methods to analyze data supermatrices comprising 7 mitochondrial genes (6,138 nucleotides) from 219 species across 67 genera and 3 nuclear genes (2,157 nucleotides) from 26 genera. Many taxa were only partially represented, with an average of 3.95 and 5.43 mitochondrial genes per species and per genus, respectively, and 2.23 nuclear genes per genus. Our analyses of mitochondrial DNA place Tarsiiformes as the sister group of Strepsirrhini. Within Haplorrhini, we find support for the primary divergence of Pitheciidae in Platyrrhini, and our results suggest a sister grouping of African and non-African colobines within Colobinae and of Cercopithecini and Papionini within Cercopthecinae. Date estimates for nodes within each family and genus are presented, with estimates for key splits including: Strepsirrhini-Haplorrhini 64 million years ago (MYA), Lemuriformes-Lorisiformes 52 MYA, Platyrrhini-Catarrhini 43 MYA and Cercopithecoidea-Hominoidea 29 MYA. Conclusion: We present an up-to-date, comprehensive estimate of the structure and tempo of primate evolutionary history. Although considerable gaps remain in our knowledge of the primate phylogeny, increased data sampling, particularly from nuclear loci, will be able to provide further resolution. Page 1 of 19 (page number not for citation purposes) BMC Evolutionary Biology 2009, 9:259 http://www.biomedcentral.com/1471-2148/9/259 Background The timescale of primate evolution has also been the sub- The evolutionary relationships of our own order, Pri- ject of numerous molecular analyses over the past few dec- mates, have been of central interest since the birth of phy- ades [4,11,18,20,21,23-32]. Typically, divergence time logenetic analysis. There has been consistent attention estimates made using molecular phylogenetic approaches towards the relationships of primates to other mammals, have supported a much more protracted timeframe for with molecular and (more recently) morphological evi- primate evolution than that suggested by the fossil record dence providing strong support for the placement of Pri- [27,33]. Inferring the age of the most recent common mates in the superorder Euarchontoglires [1-3]. Within ancestor of all primates using molecular data has been of Primates, the relationships within and between various particular interest, owing to the poor understanding of families and genera continue to cause debate, despite the early primate fossils and the contested affinity of Plesiad- numerous molecular estimates of the phylogeny that have apiformes. The oldest unambiguous primate fossil is been presented over the past 10 to 15 years [4]. With dated at 55 million years [34,35], whereas molecular esti- increasing concerns over the extinction risks facing many mates often place the common primate ancestor in excess primates, along with the recent publication of complete of 80 million years ago (MYA) [4,18]. Estimates have var- nuclear genomes from the chimpanzee [5] and rhesus ied with the reconstruction method employed and genetic macaque [6], there has been a resurgence of interest in loci used. In some instances this has resulted in consider- resolving the evolutionary relationships amongst these ably different date estimates; for example, Raaum et al. diverse taxa [4,7]. [29] recently dated the Cercopithecoidea-Hominoidea split at 23 MYA, whilst Yoder and Yang [27] and Steiper In modern classifications, the order Primates comprises and Young [26] favored an older date of 30-40 MYA. This two suborders: Strepsirrhini (wet-nosed primates) and is further exemplified by Kumar et al. [36], who showed Haplorrhini (dry-nosed primates). This has not always that both sampling method and calibration dates affect been the case. One of the foremost debates in primate sys- the confidence limits of the estimated timing of the tematics has long concerned the position of tarsiers. Tra- human-chimpanzee divergence (calculated at 4.86 - 7.02 ditionally viewed as being more closely associated with MYA, depending on the preferred date of the split between lemurs and lorises, tarsiers were placed within a suborder apes and Old World monkeys). Furthermore, previous Prosimii, under the gradistic view of primate taxonomy estimates have been limited by the number and range of [8]. Modern taxonomic schemes generally recognize their primate species, genera and families included in phyloge- closer affiliation with monkeys and apes, grouping them netic analyses, leaving certain groups (such as Tarsiidae with Haplorrhini [9]. The majority of molecular evidence and Daubentoniidae) in need of further study. supports the latter grouping [4,10-13], although a large number of molecular studies still provide support for the The task of estimating primate divergence times has been Prosimii concept [14-18]. The question is succinctly complicated by the presence of pronounced substitution reviewed by Yoder [19] and is further examined by Eizirik rate heterogeneity among lineages, a phenomenon that et al. [18]. There is now general agreement on the higher- has been of long-standing interest. For example, Good- level relationships within the two suborders [20], with man's 'hominoid slowdown' hypothesis was proposed in Strepsirrhini comprising Lorisiformes (galagos and the early 1960s [37,38], and has recently been strongly lorises) and the sister-pairing of the monophyletic supported by genomic studies [39,40]. Detailed analyses Lemuriformes (lemurs) and Chiromyiformes (the aye- of primate sequences have revealed extensive departures aye), and with Haplorrhini consisting of Platyrrhini (New from rate constancy in several other parts of the tree World monkeys) and Catarrhini (apes and Old World [4,18,27], calling for the employment of relaxed-clock monkeys). Within these groups, however, there are methods that can explicitly accommodate rate heteroge- numerous disagreements over interfamilial relationships. neity among lineages [41,42]. Molecular evidence has sometimes favored Cheirogalei- dae as sister group to Lemuridae, although current evi- While there may be consensus regarding relationships dence suggests that the four lemuriform families across the main primate clades, there is continued disa- (Lemuridae, Cheirogaleidae, Lepilemuridae and Indrii- greement at the species, genus and even family levels. One dae) represent a four-way split, which may be real or may of the primary challenges in primate molecular phyloge- simply reflect a lack of resolution [4,21,22]. Within Hapl- netics remains the issue that different markers support orrhini, controversial taxonomic issues remain. The para- conflicting trees. Introgression between congeneric spe- phyly of an all-encompassing Cebidae with respect to the cies, occasionally even between species in different (if tamarins and marmosets is widely recognized now closely related) genera, is an ever-present possibility, as is [9,23,24], but the branching order of the major lineages is the origin of whole species by hybridization. The still questionable. Among the Old World monkeys, partic- macaque example, as analyzed by Tosi et al. [43,44], ularly within Colobinae, intergeneric relationships are serves as a warning. still unclear. Page 2 of 19 (page number not for citation purposes) BMC Evolutionary Biology 2009, 9:259 http://www.biomedcentral.com/1471-2148/9/259 Previous attempts
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