Molecular Phylogenetics and Evolution 82 (2015) 348357Contents lists available at ScienceDirect

Molecular Phylogenetics and Evolution

journal homepage: www.elsevier .com/locate /ympevReviewThe systematics and evolution of New World primates A review1055-7903/$ - see front matter 2013 Elsevier Inc. All rights reserved.http://dx.doi.org/10.1016/j.ympev.2013.10.017

Corresponding author. Fax: +55 9134251745.E-mail addresses: horacio@ufpa.br (H. Schneider), ira@ufpa.br (I. Sampaio).Horacio Schneider , Iracilda SampaioInstituto de Estudos Costeiros, Universidade Federal do Par, Campus de Bragana, Alameda Leandro Ribeiro s/n, Bragana, Par, CEP 68600-000, Brazil

a r t i c l e i n f o a b s t r a c tArticle history:Available online 4 November 2013

Keywords:New World primatesMolecular phylogeneticsPhylogenomicsAlu insertionsPlatyrrhinesAmazonian ForestThis paper provides an overview of the taxonomy of New World primates from proposals of the 1980sbased on morphology to the great number of studies based on molecular data aiming for the elucidationof the phylogeny of New World monkeys. The innovations of the first molecular phylogeny presented bySchneider et al. (1993) positioned Callimico as a sister group of Callithrix and Cebuella; Callicebus as amember of the pitheciids; Brachyteles as sister to Lagothrix; and the night monkeys (Aotus), capuchins(Cebus) and squirrel monkeys (Saimiri) in the same clade with the small callitrichines. These results weresubsequently confirmed by dozens of subsequent studies using data from DNA sequences. Some issuesdifficult to resolve with the phylogenetic analyses of DNA sequences, such as the diversification of theoldest lineages (pitheciids, atelids and cebids), and the confirmation of Aotus as a member of the Cebinaeclade (together with Cebus/Saimiri), were clarified with new molecular approaches based on the presenceor absence of Alu insertions as well as through the use of phylogenomics. At this time, all relationships atthe intergeneric level had been deciphered, with the exception of the definition of the sister group of cal-litrichines (whether Aotus or Cebus/Saimiri are sister to callitrichines, or if Aotus, Saimiri and Cebus form aclade together). Future studies should prioritize the alpha taxonomy of most Neotropical primate groups,and the use of phylogenetic and geographic data, combined with reliable estimates of divergence times,to clarify the taxonomic status at species and genus level, as well as to help understand the evolutionaryhistory of this remarkable and highly diversified group.

2013 Elsevier Inc. All rights reserved.Contents1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3492. The Molecular era . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3492.1. The pioneers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3492.2. The first doubts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3502.2.1. Capuchins (Cebus) vs. squirrel monkeys (Saimiri). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3502.2.2. Goeldis monkey (Callimico goeldii) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3502.2.3. Amazonian vs. Atlantic forest marmosets. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3502.2.4. Brachyteles, Ateles, and Lagothrix . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3502.3. Persistent doubts. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3502.4. The Alu markers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3512.5. The phylogenomics approach . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3513. A more definitive classification of the platyrrhines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3534. Recent controversies about the number of platyrrhine genera . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3534.1. Mico vs. Callithrix . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3544.2. Callibella . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3544.3. Oreonax . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3544.4. Cebus vs. Sapajus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3545. Biogeography and evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 354Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356

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Fig. 1. Phylogenetic tree obtained by Bayesian analysis in Schneider et al. (2003,2006). Numbers at nodes symbolize maximum credibility values. Branches in colorsignify arrangements with low statistical support. (For interpretation of thereferences to color in this figure legend, the reader is referred to the web versionof this article.)

H. Schneider, I. Sampaio /Molecular Phylogenetics and Evolution 82 (2015) 348357 3491. Introduction

The systematics of New World monkeys has been the cause ofmuch research and debate, especially since the 1970s. The tradi-tional classification of the infraorder Platyrrhini divided these pri-mates into Cebidae and the Callitrichidae, with Callimico beingallocated to either the former (Simons, 1972; Simpson, 1945) orthe latter family (Napier and Napier, 1967; Pocock, 1925, Szalay,1979). Hill (1957) and Hershkovitz (1972, 1977) proposed a thirdfamily Callimiconidae to accommodate Callimico, because itshares characteristics that define both cebids (births of single off-spring and the presence of a third molar) and callitrichids (smallsize and the presence of claws on all the digits except the hallux).According to Hershkovitz (1977), then, all New World primatesshould be included in one of three families the Callitrichidae Tho-mas, 1903, which comprised the marmosets (Callithrix and Cebuel-la) tamarins (Saguinus) and lion tamarins (Leontopithecus), themonotypic Callimiconidae Dollman, 1933 (Callimico) and the Cebi-dae Bonaparte, 1831, (Cebus, Saimiri, Aotus, Alouatta, Ateles, Lago-thrix, Brachyteles, Callicebus, Pithecia, Chiropotes, and Cacajao).

At the time, this classification was largely undisputed. The asso-ciation of the marmosets and tamarins in the Callitrichidae is asound arrangement, and Hershkovitz did not attempt to decipherthe relationships of the four problematic genera Aotus, Cebus,Saimiri, and Callicebus but rather, he assigned each one to itsown subfamily (Aotinae, Cebinae, Saimiriinae, and Callicebinae,respectively). His interpretation of the position of Callimico wasbased on traits that he presumed to be important for the differen-tiation of this genus from other platyrrhines.

During the subsequent decade, the main protagonists SusanFord, Richard Kay, and Alfred Rosenberger brought new ideasto the interpretation of platyrrhine systematics (Ford, 1986; Kay,1990; Rosenberger, 1984). The principal advance was the unani-mous identification of three monophyletic clades, one made upof the small, clawed monkeys (Callitrichinae), a second clade com-prising the large frugivorousfolivorous monkeys with prehensiletails (Atelinae: Alouatta, Ateles, Lagothrix, and Brachyteles), andthe third by the specialized seed predators, (Pitheciinae: Pithecia,Chiropotes, and Cacajao). There was also consensus on the basal po-sition of Callimico in the callitrichine lineage, rather than in its ownfamily. The authors nevertheless differed with regard to the inter-nal arrangement of each of the three principal groups, as well asthe position of Saimiri, Cebus, Aotus, and Callicebus.

Rosenberger (1981) considered Cebus and Saimiri to be sistergroups of the callitrichines, whereas Ford (1986) concluded thatCebus and Aotus, and Saimiri and Callicebus were the earliest off-shoots of the platyrrhine radiation. Subsequently, Kay (1990) di-verged from both viewpoints by classifying Callicebus and Cebusas the basal platyrrhines, Saimiri as a sister group of the callitri-chines, and Aotus as an early offshoot of the ateline radiation.The position of Callicebus remained unclear. Kay (1990) consideredthis genus to be the most basal platyrrhine taxon, while Ford(1986) grouped it with Cebus and Saimiri in the most basal platyr-rhine clade. By contrast, Rosenberger (1981, 2011; Rosenbergeret al., 1990) has argued cogently that Callicebus and Aotus are sisterlineages linked to the pitheciine clade.

In the case of the ateline clade, while Rosenberger (1981) con-sidered Ateles and Brachyteles to be sister groups, Ford (1981) re-corded a non-resolved trichotomy for Brachyteles, Lagothrix, andAteles, whereas Kay (1990) identified two clades AtelesLagothrixand AlouattaBrachyteles. Similarly, while all three authors consid-ered the gummivorous marmosets (Cebuella and Callithrix) to bethe most derived lineage, they disagreed on the relative positionof Saguinus and Leontopithecus. Whereas Rosenberger (1981) andFord (1986) placed Leontopithecus as the sister group of the Calli-thrixCebuella clade, Kay (1990) identified Saguinus as the sistergroup.2. The Molecular era

2.1. The pioneers

The work of Baba et al. (1979) on the immunodiffusion system-atics of primates can be seen as the precursor of the molecularstudies of this order. These authors estimated antigenic distancesusing antisera produced in rabbits and applied this approach to alarge number of primate species including those of nine NewWorld genera Alouatta, Aotus, Ateles, Callicebus, Cebus, Chiropotes,Lagothrix, Saimiri, and Saguinus. The phenogram derived from thisanalysis emphasized the monophyletic status of the Ceboidea, withfour principal clusters Alouatta, Ateles, Lagothrix; Chiropotes, andCacajao; Aotus, Saguinus, Callimico and Callicebus; and Saimiri andCebus, as a single complex lineage.

Molecular data suitable for the cladistic analysis of New Worldmonkeys were first obtained thanks to a fortuitous association be-tween two research groups: one from Wayne State University(USA) led by Dr. Morris Goodman and other from the Federal Uni-versity of Par (Brazil) headed by Dr. Horacio Schneider. This scien-tific collaboration lasted more than a decade. These authors(Schneider et al. 1993) sequenced the complete epsilon-globingene in addition to the up- and downstream regions in sixteenplatyrrhine genera and seven catarrhines, with the tarsier as theoutgroup. Subsequently, Schneider et al. (1996) sequenced 1.8 kbof the interphotoreceptor binding protein (IRBP) intron 1 in thesame 16 platyrrhine genera. The phylogenetic tree based on thesetwo unlinked genes provided strong statistical support for the exis-tence of three well-supported clades (Fig. 1): the first clade in-cluded Saguinus as the basal genus, followed by Leontopithecus,and then Callimico as the sister group of CallithrixCebuella (Calli-trichinae). Curiously, Aotus and the CebusSaimiri group joinedthe callitrichines to form a very well supported clade. The secondclade contained Callicebus, which was strongly connected to theclassical pitheciines (Pithecia, Cacajao and Chiropotes). The thirdand final clade was composed of Alouatta as the basal genus,

350 H. Schneider, I. Sampaio /Molecular Phylogenetics and Evolution 82 (2015) 348357followed by Ateles, and LagothrixBrachyteles as sister groups, anarrangement that was strongly supported.

Despite the persistence of some unanswered questions, thesefirst cladistic analyses based on the DNA sequences of epsilon-glo-bin and IRBP provided an excellent resolution for the interpretationof platyrrhine phylogeny. The position of Callicebus as a sistergroup of the pitheciines was unequivocal, and resolved one ofthe principal points of disagreement between Rosenberger, Ford,and Kay. Furthermore, the molecular phylogeny reinforced themonophyly of the cebids, which include Aotus, Cebus, Saimiri, andthe callitrichines, marked by a close relationship between Cebusand Saimiri. The major finding was the identification of Callimicoas the sister group of Callithrix/Cebuella, a completely novelarrangement. The reallocation of Cebuella to the genus Callithrixwas also supported, representing one of the first attempts to applya molecular phylogeny to the taxonomic classification of organ-isms. The study also revealed a consistent pattern of bifurcationin the ateline clade, with Alouatta as the oldest lineage, followedby Ateles, and BrachytelesLagothrix as sister groups, a completelynew arrangement for these primates.

However, as with all such major phylogenies, some relation-ships could not be determined reliably based on the two genesanalyzed. A number of the branch nodes had low statistical support(Fig. 1; branches marked in color), and demanded special attentionin the subsequent studies.

2.2. The first doubts

2.2.1. Capuchins (Cebus) vs. squirrel monkeys (Saimiri)The close relationship of Cebus and Saimiri was reinforced by

our original analysis (Schneider et al., 1993), although it lacked sig-nificant statistical support. Harada et al.s (1995) subsequent re-analysis of the same markers (epsilon-globin and IRBP) was basedon a larger sample an additional three Saimiri taxa (S. sciureussciureus, S. boliviensis, and S. sciureus macrodon) and three Cebusspecies (Cebus kaapori, Cebus albifrons, and C. nigrivittatus) andgenerated even more support for the sister grouping of Cebus andSaimiri. This arrangement was recovered subsequently by Canavezet al. (1999), Schneider et al. (2001), and Opazo et al. (2006).

2.2.2. Goeldis monkey (Callimico goeldii)The first molecular data (Schneider et al., 1993) indicated

clearly that Goeldis monkey was not basal to the callitrichine radi-ation, as previously thought, but rather, that Callimico was closelyrelated to Callithrix and Cebuella. This arrangement had been sug-gested previously by Cronin and Sarich (1978) using albumin andtransferrin immunological data. In their paper they aligned Callim-ico with Callithrix with a prior divergence of Leontideus and Sagui-nus. Similarly, Seunez et al. (1989) obtained a consensus treetopology with LINE-1 elements which is identical to that obtainedby Cronin and Sarich (1978), suggesting that Callimico is closer tothe Callithrix/Cebuella lineages than Saguinus and Leontopithecus.

The sequence data was subsequently confirmed by Pastoriniet al. (1998) based on the DNA sequence of the mitochondrialND4 coding region and the tRNAHis, tRNASer, and tRNALeu genes.Both nuclear and mitochondrial data convincingly placed Callimicoas nested within the callitrichines, as the sister group to the mar-mosets (Callithrix and Cebuella).

Porter et al. (1997) used a 2 kb dataset of the 50 flanking regionof the epsilon-globin gene and Barroso et al. (1997) analyzed a1.8 kb sequence of the long intron 1 of the IRBP gene in an attemptto clarify the relationships among the callitrichines. For the firsttime, these studies revealed a close affinity between the pygmymarmoset (Cebuella pygmaea) and the marmosets of the Callithrixargentata group, and indicated that the genus Callithrix would beparaphyletic unless it included Cebuella. Barroso et al. (1997) alsoproposed a classification with three families: Atelidae, Pitheciidae,and Cebidae (with three subfamilies Cebinae, Aotinae, and Calli-trichinae). This study provided evidence that Cebuella and the C.argentata and C. jacchus species groups had separated from one an-other around 5 million years ago (5 Ma) and, furthermore, that abasal callitrichine stock had branched into two clades Saguinusand the ancestral population of Leontopithecus and CallimicoCalli-thrix (or LeontopithecusCallimico and Callithrix) sometime in themid Miocene (1011 Ma). The evolutionary history and the taxo-nomic position of Callimico were evaluated in further detail byChaves et al. (1999), who added a 0.9-kb sequence of intron 11of the nuclear von Willebrand Factor gene (vWF) obtained from arange of different platyrrhine taxa, including numerous marmosetspecies from both the Amazonian and Atlantic forest groups. Theresults of this study provided further support for the status of Cal-litrichinae as a monophyletic subfamily within the Cebidae, whichalso includes Cebus, Saimiri, and Aotus. This robust arrangementindicated that the callitrichines were even more closely-relatedthan previously thought, and that they should be allocated to thetribe Callitrichini. Once again, Callimico stood out as the sistergroup of Callithrix. The data also reconfirmed Saguinus as the basalbranch of the group, followed by Leontopithecus, and finally the sis-ter taxa Callimico and Callithrix. By adding different Callithrix spe-cies to the dataset, this analysis also confirmed that Callithrixargentatawas more closely related to C. pygmaea than to the C. jac-chus species group, reinforcing the evidence for inclusion of thepygmy marmoset in the genus Callithrix in order to uphold themonophyly of the genus.

2.2.3. Amazonian vs. Atlantic forest marmosetsThe study of Tagliaro et al. (2000), based on the DNA sequences

of both nuclear (Transferrin gene, exon 4 to exon 6; 1472 basepairs.) and mitochondrial genes (ND1; 951 bp), was the first toindicate the existence of two distinct clades of marmosets theAtlantic clade composed of C. jacchus, C. penicillata, C. kuhlii andC. geoffroyi, and the Amazonian clade, composed of C. argentataand the pygmy marmoset, which corroborated the proposal of Por-ter et al. (1997), Barroso et al. (1997) and Chaves et al. (1999) thatthe pygmy marmoset should be included in the genus Callithrix.However, Rylands et al. (2000) recommended the maintenance ofCebuella as a distinct genus, while supporting the separation ofthe Atlantic and Amazonian clades into Callithrix Erxleben, 1777,andMico Lesson, 1840, respectively. This arrangement is consistentwith the monophyletic status of the three groups.

2.2.4. Brachyteles, Ateles, and LagothrixBased on their analysis of molecular data, Schneider et al. (1993,

1996) proposed that Lagothrix is the sister group of Brachyteles,rather than Ateles, as had been proposed by Rosenberger et al.(1981). We addressed this issue once more (Lima et al., 2007) byincorporating all the available data (G6PD, epsilon-globin, B2 M,gamma-globin, IRBP, ALDA, mtDNA-12S, mtDNA-16S, andmtDNA-COII) and including new sequences from two non-codingregions (introns) of two nuclear genes: Transferrin (TF) and vonWillebrand Factor (vWF). This provided a dataset of almost18 kb, and the results were emphatic and unequivocal in linkingLagothrix from the Amazon region to Brachyteles from the AtlanticForest.

2.3. Persistent doubts

At this point, the resolution of at least two aspects of the phy-logeny of the New World primates remained unsatisfactory. Onewas the exact relationship between the CebusSaimiri and Aotusgroup and the callitrichines. The other was the nature of the rela-tionship among the three major lineages pitheciines, atelines,

Fig. 2. Phylogenetic relationships among NewWorld monkey genera obtained fromSINE insertion analyses (adapted from Osterholz et al. 2009). Black (5), orange (10),yellow (17) and white (7) rays represent the number of SINE inserted into theancestor lineages of atelidscebids, cebids, tamarins and marmosets and CallimicoCallithrix, respectively. Blue (11), light blue (3) and green (7) represent the numberof Alus inserted into the most recent common ancestor (MRCA) of atelids; woollymonkeys, muriqui and spider monkeys, and Pitheciidae, respectively.

H. Schneider, I. Sampaio /Molecular Phylogenetics and Evolution 82 (2015) 348357 351and cebines. A number of papers were published in subsequentyears, using distinct genetic markers, in an attempt to provide amore reliable and definitive interpretation of these questions.

Horovitz and Meyer (1995) used 16S mtDNA sequences to eval-uate the phylogenetic information content of various secondarystructures of a fragment of the large ribosomal mitochondrial gene(16S) from 13 species of platyrrhine, three species of catarrhines,and Tarsius. Unfortunately, 16S turned out to be a poor markerfor the resolution of the relationships among the platyrrhines. Sub-sequently, Horovitz et al. (1998) combined the mtDNA 16S datawith a morphological analysis and concluded that this provided acladogram consistent with the nuclear data published previously.

Canavez et al. (1999) presented a phylogenetic arrangement forall the Neotropical primate genera based on sequences of thebeta2-microglobulin gene. This cladistic analysis also favored theinclusion of Cebuella in Callithrix as the sister group of the C. argen-tata species group, thus reducing the number of platyrrhine generafrom 16 to 15. This study also provided further evidence for the sis-ter grouping of Callimicowith Callithrix and the association of Leon-topithecus with the CallithrixCallimico clade.

Using a 1.3 kb sequence from two introns of the glucose-6-phosphate dehydrogenase (G6PD) gene in 24 platyrrhine species,von Dornum and Ruvolo (1999) produced a phylogeny roughlysimilar to the previous analyses. Steiper and Ruvolo (2003) subse-quently added two G6PD introns, with a total sequence of 2.1 kb,and reconfirmed the results.

Opazo et al. (2006) obtained orthologous sequences of six nu-clear (B2M, epsilon-globin, G6PD4, G6PD5, IRBP, vWF and TOM)and one mitochondrial gene (16S) for the fifteen recognized generaof New World monkeys (9137 bp). The results reinforced the exis-tence of three clades (families Pitheciidae, Cebidae and Atelidae),and reinforced the proximity of the triad AotusSaimiriCebus tothe callitrichines within the family Cebidae. The data also con-firmed the basal position of Callimico in relation to the marmosetsand that of Callicebus within the pitheciids, as well as the sistergrouping of Lagothrix and Brachyteles. However, the position of Ao-tus relative to Cebus/Saimiri or the callitrichines and the relation-ships among the three major clades (families) remained unclear.Maximum parsimony analysis grouped Atelidae with Cebidae assister families, whereas the maximum likelihood approach andBayesian inference grouped Atelidae with Pitheciidae. Despite themajor advances in our understanding of platyrrhine phylogenyprovided by the molecular data offered by all these studies, thetwo fundamental questions stated above remained unanswered.

2.4. The Alu markers

New insights into the phylogeny of the platyrrhines were pro-vided by the discovery of homoplasy-free molecular markers, theso-called transposons, which are capable of producing copies ofthemselves that are inserted into different sites on the chromo-somes. These copies, or Short INterspersed Elements (SINEs), areconsidered to be perfect homologies because, once inserted, theypersist through the lineage of all descendants. So, if two taxa sharean insertion, they must have inherited it from their most recentcommon ancestor. Primates have a specific family of transposons,known as Alu (Salem et al., 2003). Singer et al. (2003) used pri-mate-specific Alu elements as molecular cladistic markers in aphylogenetic analysis of platyrrhine species, and identified sixpolymorphic loci in the PCR amplification pattern, indicating ashared derived character state due to the presence of orthologousAlu elements. They concluded that (i) Callithrix and Cebuella weremore closely related to each other than either was to any other cal-litrichine; (ii) callitrichines form a monophyletic clade which in-cludes Callimico, and (iii) Cebus, Saimiri, and Aotus are moreclosely related to the callitrichines than to other platyrrhines.Ray et al. (2005) based on 183 markers that were specific to nineplatyrrhines (Aotus trivirgatus, Saguinus labiatus, Ateles geoffroyi,Lagothrix lagotricha, Cebuella pygmaea, Alouatta sara, Saimiri sciure-us, Pithecia pithecia, Callicebus donacophilus) found very exciting re-sults. The cladogram produced from these data supported thesister relationship between the atelids (spider, woolly, and howlermonkeys) and cebids (marmosets, tamarins, capuchins, squirreland owl monkeys), with the pitheciids (titis and sakis) as the firstbranch on the phylogenetic tree, in contrast with the arrangementexpected based on morphological parameters. However, this studywas unable to elucidate the relationship between Aotus and/or Sai-miri (Cebus) as the sister group to the callitrichines.

Using a similar approach, Osterholz et al. (2009) analyzed thepresence/absence pattern of 128 SINEs in 15 platyrrhine genera.Forty Alu insertions were informative for the elucidation of thephylogenetic relationships among the genera. The most importantresults were the confirmation of the monophyly of the three fam-ilies (Cebidae, Atelidae, and Pitheciidae) as well as the evidence fora sister grouping of the Cebidae with the Atelidae (supported byfive Alu insertions), with the Pitheciidae positioned externally, asobserved by Ray et al. (2005). In the study of Osterholz et al.(2009), the monophyly of the Pitheciidae was supported by sevenAlu insertions (shown in green in Fig. 2), the Atelidae by 11 (shownin blue in Fig. 2), and the Cebidae by 10 (shown in orange in Fig. 2).In addition, the cladistic markers linked the owl monkeys (Aotus)unequivocally to Cebus, Saimiri, and the callitrichines; these taxashared 10 exclusive Alu insertions (shown in red in Fig. 2) notshared by any other platyrrhine. It is also important to emphasizethe seven exclusive Alu shared by Callimico and marmosets (shownin white in Fig. 2). This not only solved the puzzle of the principallineages, but also confirmed the inclusion of Aotus in the Cebidae,sensu Schneider (2000). However, as no Alu insertions were sharedexclusively between Aotus and either CebusSaimiri or the callitri-chines, the identity of the sister group of the callitrichines re-mained unclear.2.5. The phylogenomics approach

Wildman et al. (2009) adopted a different approach based oneleven nuclear DNA markers derived from a random genomic shot-gun library generated from Aotus lemurinus. These markers were

352 H. Schneider, I. Sampaio /Molecular Phylogenetics and Evolution 82 (2015) 348357sequenced in at least one representative of each platyrrhine genus.The concatenated alignment of the 22 taxa (7.7 kb) analyzed aloneor together with about 10 kb of seven nuclear genes derived fromprevious studies reported in Opazo et al. (2006) were congruentand converged to a single topology for the Platyrrhini. In particular,the results confirmed that Pitheciidae is the sister taxon of theother two families (Cebidae, Atelidae). This relationship was sup-ported by high values of branch support as well as the results ofthe topology tests. However, while Aotus grouped with CebusSai-miri to form a sister clade to the callitrichines, bootstrap supportwas not significant (Maximum Parsimony [MP] = 62%; MaximumLikelihood [ML] = 84%).

The recent studies of Wildman et al. (2009) and Perelman et al.(2011) represent the beginning of a new phase in primate phylog-eny the phylogenomic approach. In a joint study (Perelman et al.2011) involving some members of our research team, 42 autosom-ic, four Y-linked, and eight X-linked genes, with a total of approx-imately 35,000 base pairs, were sequenced in representatives of191 primate taxa. This was the most exhaustive and robust molec-ular primate phylogeny produced to date. The findings of this studyfor the platyrrhines are represented in Fig. 3. All the nodes in thetopology obtained by Perelman et al. (2011) had significant statis-tical support, with the exception of that which defines the sistertaxon of the callitrichines. The robust and gracile capuchins (Sapa-jus and Cebus, respectively see below) were also clearly sepa-rated, with significant statistical support. As expected, Lagothrixand Brachyteles were strongly linked. Once again, the Pitheciidaewas the most basal family, and the sister relationship betweenAtelidae and Cebidae was well supported. The results indicatedthat Aotus was closely linked to the callitrichines, with CebusSai-miri as a sister group, but with reduced bootstrap support(MP = 80% and ML = 91%). However, this particular arrangementwas challenged by Perez et al. (2012), who reanalyzed most ofthe available molecular data, including those of Perelman et al.(2011), Wildman et al. (2009), Opazo et al. (2006), Canavez et al.(1998), and Schneider et al. (1996), exploiting these databases toinfer species and gene trees using the Bayesian Markov ChainMonte Carlo method for multispecies coalescence. For this proce-dure, Perez et al. (2012) split the data into coding and non-codingFig. 3. Multispecies tree obtained in Beast v.17.4 (Heled and Drummond, 2010) baevolutionary models described by the authors were used in this re-analysis. Tree was rendindicate millions of years of divergence time.sequences, and conducted a variety of analyses with combined orisolated data. The BEAST multispecies results for the differentanalyses were not totally consistent on the position of Aotus. Thecombined data set (68 loci and 47,233 bp or 36 loci and27,360 bp) resulted in an unresolved trichotomy between Aotus,CebusSaimiri, and the callitrichines. For example, the BEAST anal-ysis of the 21 sequences reported by Wildman et al. (2009) pro-duced contrasting topologies for the different genes sixdatabases grouped Aotus within the Cebidae, two with CebusSaimiri and two with the callitrichines. These apparent incongrui-ties in the position of Aotus are not totally unexpected, given theshort time scale separating the lineages, as shown consistently inall the studies of these lineages (see below).

Interestingly, Perez et al. (2012) argued that the inclusion ofAotus within the Cebidae in previous molecular studies may bedue to long branch attraction and taxon sampling, which hadnot been investigated previously using a Bayesian approach. Thisargument is quite interesting. In fact, the correct assignment of avery divergent taxon faces multiple challenges such as longbranch attraction, taxon density, short intervals between clado-genetic events or even a combination of all these phenomena.In this particular case, however, there is no doubt that Aotus be-longs to the Cebidae. Unfortunately, Perez et al. (2012) com-pletely ignored Osterholz et al.s (2009) comprehensive studyof Alu elements, which unequivocally place this genus in the ce-bid lineage. Aotus shares 10 exclusive Alu elements with SaimiriCebus and the callitrichines. From a cladistic point of view, these10 insertions are shared homologies, that is, unequivocal synapo-morphies. In addition, Aotus does not share any exclusive Aluelements with any other platyrrhine genus, and thus cannot bea member of the ateline or pitheciine clades, that is, a sistergroup of Callicebus, as proposed by Rosenberger et al. (1981),or conversely, closely related to the atelines, as suggested byKay (1990). Nor can Aotus be an early offshoot of the platyrrhineradiation, as indicated by Ford (1986).

Following this monumental sequencing effort (Wildman et al.,2009; Perelman et al., 2011), it is now possible to affirm that onlythe position of Aotus in the cebid clade (sensu Schneider, 2000) re-mains unclear. It seems likely that the most promising approachsed on 25 autosome introns (16,656 bp) from Perelman et al. (2011). The sameered in FigTree v1.4.0 (http://tree.bio.ed.ac.uk/software/figtree/). Numbers at nodes

http://www.tree.bio.ed.ac.uk/software/figtree/

H. Schneider, I. Sampaio /Molecular Phylogenetics and Evolution 82 (2015) 348357 353for the resolution of this final enigma of platyrrhine phylogeny liesin the analysis of the virtually homoplasy-free SINE insertions.

3. A more definitive classification of the platyrrhines

After almost twenty years of intense investigation, many as-pects of platyrrhine phylogeny have been resolved. But, based onwhat we know now, which classification of the main lineages isthe most reliable interpretation of the phylogenetic relationshipsamong the platyrrhines?

Divergence time estimates have indicated consistently thatthe radiation of the ancestors of the Cebus/Saimiri, Aotus, andthe modern callitrichine lineages took place within a short timeperiod. Goodman et al. (1998), for example, estimated that thefirst branching occurred at 22 Ma, and the second at 20 Ma,while Schneider (2000) proposed dates of 23.2 and 22.4 Ma,and Opazo et al. (2006) estimated 22.05 and 19.50 Ma. Schragoet al. (2007) further reinforced this conclusion, timing the Ce-busSaimiri/callitrichine split at 16.8 Ma and the separation ofAotus and the callitrichines at 16.5 Ma. Perelman et al. (2011)estimated that the split originating the ancestor of the CebusSaimiri and Aotus occurred at 19.95 Ma, with the second diver-gence, which originated the genus Aotus and the callitrichines,taking place at 19.25 Ma.

Despite some discrepancies in the estimates generated by theslightly different topologies, distinct calibrations, and markers, allthe studies agree on the fact that the process leading to the sepa-ration of the modern CebusSaimiri, Aotus, and callitrichine lin-eages occurred over a relatively brief timeframe. As mentionedabove, Perez et al. (2012) argued that the exact position of Aotusin the tree changes according to the set of genes analyzed. Thereare three possible arrangements for the night monkey (a) Aotusis the sister group of callitrichines; (b) Aotus is the sister group ofCebusSaimiri; (c) Cebus and Saimiri are the sister group of theTable 1Three recent proposals for the classification of the New World primates.

Schneider, 2000 Groves, 2001

1 Family Cebidae 1 Family Cebida1.1 Subfamily Callitrichinae 1.1 Subfamily Call

Callithrix, Cebuella, Mico, Saguinus, Leontopithecus,Callimico

Callithrix Erxle

Callimico MiraLeontopithecus

Saguinus Hoffm

1.2 Subfamily Cebinae 1.2 Subfamily CebCebus, Saimiri Cebus Erxleben

1.3 Subfamily SaimSaimiri Voigt, 1

1.3 Subfamily Aotinae 2 Family AotidaeAotus Aotus Illiger, 1

2 Family Pitheciidae 3 Family Pitheci2.1 Subfamily Pitheciinae 3.1 Subfamily Pith

Pithecia, Chiropotes, Cacajao Pithecia DesmaChiropotes LessCacajao Lesson

2.2 Subfamily Callicebinae 3.2 Subfamily CallCallicebus Callicebus Thom

3 Family Atelidae 4 Family Atelida3.1 Subfamily Alouattinae 4.1 Subfamily Alou

1897Alouatta Alouatta Lacep

3.2 Subfamily Atelinae 4.2 Subfamily AteAteles, Brachyteles, Lagothrix Ateles . Geoffr

Brachyteles SpiLagothrix . GeOreonax Thomcallitrichines. Whatever the exact arrangement is, there is no doubtthat Aotus belongs to a monophyletic clade including CebusSaimiriand the callitrichines, given that they share 10 exclusive synapo-morphies (Alu insertions) not found in any other platyrrhine. Anyclassification scheme should include Atelidae, Pitheciidae and athird family (Cebidae) containing a monophyletic group supportedby 10 Alu insertions. As the internal arrangement of this third claderemains unclear, although, one possibility is to place each of theselineages Aotus, CebusSaimiri and the callitrichines in a separatefamily. Secondly, callitrichines and CebusSaimiri would be placedin one family (Cebidae) and Aotus in another (Aotidae), as proposedby Groves (2001). However, Grovess proposal is not phylogeneti-cally sound because it would create a paraphyletic taxon, i.e., Cebi-dae (with callitrichines) without Aotus. In our opinion, given theuncertain arrangement of the cebid clade and the short timeframeof the divergence between the three main groups (Aotus, CebusSaimiri, and callitrichines), the most parsimonious arrangementfor the Platyrrhini would appear to be the three families Atelidae,Pitheciidae and Cebidae as recommended by Schneider (2000;see Table 1) and three subfamilies within Cebidae (Callitrichinae,Aotinae, and Cebinae).

4. Recent controversies about the number of platyrrhine genera

Rylands et al. (2012) provide a comprehensive overview of themore recent changes in the systematic arrangement of platyrrhinefamilies (Table 2). Initially, three families were recognized, Cebi-dae, Callitrichidae, and Atelidae, or Cebidae, Pitheciidae, and Ateli-dae. Subsequently, four families have been considered valid(Atelidae, Pitheciidae, Cebidae and Aotidae), and some authorshave added a fifth family, Callitrichidae. In addition to the ongoingcontroversies at family and species levels, a number of new generahave also been discovered or proposed in recent years, most nota-bly Mico, Callibella, Oreonax, and Sapajus (Table 2).Rylands and Mittermeier, 2009

e 1 Family Callitrichidaeitrichinae Gray, 1821 Callithrix, Saguinus, Callimico, Leontopithecusben, 1777

nda-Ribeiro, 1911 Cebuella Gray, 1866Lesson, 1840 Callibella, Van Roosmalen & Van Roosmalen,

2003annsegg, 1807 Mico Lesson, 1840

2 Family Cebidaeinae Bonaparte, 1821 2.1 Subfamily Cebinae, 1777 Cebusiriinae Miller, 1812 2.2 Subfamily Saimiriinae831 SaimiriElliot, 1913 3 Family Aotidae

811 Aotusidae Mivart, 1965 4 Family Pitheciidaeeciinae Mivart, 1965 4.1 Subfamily Pitheciinaerest, 1804 Pithecia, Chiropotes, Cacajaoon, 1840, 1840icebinae Pocock, 1925 4.2 Subfamily Callicebinaeas, 1903 Callicebus

e Gray, 1825 5 Family Atelidaeattinae Trouessart, 5.1 Subfamily Alouattinae

ede, 1799 Alouattalinae Gray, 1825 5.2 Subfamily Atelinaeoy, 1806 Ateles, Brachyteles, Lagothrix, Oreonaxx, 1823offroy, 1806as, 1927

Table 2Families, species and subspecies of New World primatesa.

Familiesb Genera Species Subspecies

Cebidae Cebuella 1 2Mico 15 15Callithrix 6 6Callimico 1 1Saguinus 15 33Leontopithecus 4 4Saimiri 5 10Cebus 4 17Sapajus 8 9Aotus 10 12

Pitheciidae Callicebus 28 28Pithecia 5 9Chiropotes 5 5Cacajao 3 6

Atelidae Alouatta 14 19Ateles 7 15Brachyteles 2 2Lagothrix 5 6

138 199

a Adapted from Rylands et al., 2012.b Sensu Schneider, 2000. Callibella humilis and Oreonax flavicauda were reinte-

grated into the Mico and Lagothrix genera, respectively.

354 H. Schneider, I. Sampaio /Molecular Phylogenetics and Evolution 82 (2015) 3483574.1. Mico vs. Callithrix

The molecular data have shown consistently that the marmo-sets from the Amazon basin are closer, in phylogenetic terms, tothe pygmy marmoset (Cebuella) than the Atlantic Forest marmo-sets (Barroso et al., 1997; Chaves et al., 1999; Porter et al., 1997;Tagliaro et al., 1997; Tagliaro et al., 2000). As mentioned before,these findings stimulated a number of questions with regard tothe taxonomic status of Cebuella. Rylands et al. (2000) decided thatthe evidence reciprocal monophyly, allopatry, and a relativelyancient divergence supported the division of the marmosets intotwo genera, the Amazonian Mico and Callithrix, from the AtlanticForest. This alternative interpretation of Rylands et al. (2000) keepsCebuella with genus status. Perelman et al. (2011) and Schneideret al. (2012) estimated that Atlantic Callithrix and Amazonia Micoand Cebuella split around 5 Ma, during the transition from the Mio-cene to the Pliocene.4.2. Callibella

Van Roosmalen and van Roosmalen (2003) proposed raising thespecies originally described as Callithrix humilis to the genus level(Callibella) based both on morphology and a molecular phylogenyderived from the nucleotide sequences of the fast-evolving mito-chondrial Control Region. The proposal of a new genus was basedon the hypothesis that the C. humilis form was placed in a basal po-sition in relation to the CebuellaMicoCallithrix clade. More re-cently, however, Schneider et al. (2012) combined Control Regionsequences with those of four nuclear regions containing Alu ele-ments for the analysis of the relationships within the marmosetgroup. Based on a large number of callitrichine species, includingCebuella, the results indicated clearly that Cebuella, Mico, and Calli-thrix are independent lineages and are consistent with genus-leveldifferentiation. In addition, Cebuella, rather than the humilis form,was the basal taxon, contradicting the findings of van Roosmalenand van Roosmalen (2003). Despite its diminutive size, in fact, C.humilis was more closely related to Mico than Cebuella. The sumof the evidence presented by Schneider et al. (2012) emphaticallysupports the classification of C. humilis as a member of the genusMico.4.3. Oreonax

In 1963, Fooden published an excellent review of the genusLagothrix based on the preserved specimens available in a numberof different American institutions, and concluded that Lagothrix in-cludes two allopatric species L. lagotricha, found throughout theupper Amazon Basin and neighboring regions, and the yellow-tailed woolly monkey, L. flavicauda, which is restricted to a smallarea of the eastern slope of the central Andes in northern Peru.So restricted, in fact, that at that time, the scientific communityassumed the species was extinct, given that the last recorded sight-ing was in 1926. However, Mittermeier et al. (1975) subsequentlyrediscovered the species living in its natural habitat in Peru. In acomparative study of ateline skull morphology, Groves (2001) pro-posed the reinstatement of the monotypic genus Oreonax Thomas,1927, separating flavicauda from the other woolly monkeys. How-ever, Matthews and Rosenberger (2008) re-examined the cranialevidence and claimed that the cladistic rationale for resurrectingthe Oreonax generic distinction for the yellow-tailed woolly mon-key (Lagothrix flavicauda) was based on an artifact of samplingwithin the study group below the genus level (p. 245). As nomolecular analysis has included samples of the flavicauda form,any such conclusions on its classification remain speculative, butgiven the critically endangered status of the yellow-tailed woollymonkey, DNA sequences are urgently needed.4.4. Cebus vs. Sapajus

Silva (2001) investigated the capuchins comprehensively, andconcluded that the morphology of the tufted and untufted forms,sensu Hershkovitz (1949, 1955), is so distinct that they should beconsidered separate genera. It was only more recently, however,that an extensive review of the morphological, genetic, behavioral,ecological, and biogeographic evidence (Boubli et al., 2012; LynchAlfaro et al., 2012a,b) permitted the establishment of a formal divi-sion between the robust (tufted) capuchins, Sapajus Kerr, 1792, andthe gracile (untufted) capuchins, Cebus Erxleben, 1777. The molec-ular study (Lynch Alfaro et al., 2012a,b) of mitochondrial DNA esti-mated that the split between the two capuchin genera would haveoccurred in the late Miocene, more than 6 Ma. These estimates arein accordance with the conclusions of Perelman et al. (2011) basedon data from the nuclear genome.5. Biogeography and evolution

According to Perelman et al. (2011), the Platyrrhini and Catar-rhini diverged from their common ancestor in the middle Eocene(43 Ma), but it was only in the late Oligocene (25 Ma) and earlyMiocene (23.8 Ma) that the cladogenesis producing the crownfamilies Pitheciidae, Atelidae and Cebidae occurred (Fig. 2). In thepitheciids, the Callicebus clade emerged at approximately 20 Maand began to diversify some 10 Ma later. Pithecia separated fromthe ancestor of Chiropotes and Cacajao clades at 14 Ma, but thediversification of extant species within these three genera beganmuch more recently (24 Ma).

In the Atelidae, the initial divergence of the Alouatta lineage oc-curred at about 16 Ma, followed by the splitting of Ateles (11.5 Ma)from the sister genera Brachyteles and Lagothrix, which diverged at9.5 Ma. While the ancestral woolly monkeys (Lagothrix) remainedin the Amazon Forest, the predecessors of the muriqui (Brachyteles)lineage migrated south and east to the exuberant Atlantic Forest. Inthe meantime, the modern diversification of the two other atelidlineages (Alouatta and Ateles) began sometime between 5 and6 Ma (Fig. 2).

H. Schneider, I. Sampaio /Molecular Phylogenetics and Evolution 82 (2015) 348357 355Perelman et al. (2011) phylogenetic arrangements suggestedthat the cebids passed through two cladogenetic events during avery short period (19 Ma), leading to the lineages of Aotus, Ce-busSaimiri, and the callitrichines. The SamiriCebus split has beenestimated at 15.5 Ma, while the callitrichine radiation began atabout 15 Ma (see Perelman et al., 2011; Schneider et al., 2012).

Based on our previous studies, summarized in Schneider et al.(2012), we postulate that the callitrichine radiation arose from abasal population in the central Amazon Basin. The first branchingevent (A) would have given origin to the ancestor of the Saguinusclade and a proto lion tamarin/Callimico/marmoset clade. Not longafterwards (13 Ma), a second event (B) would have led to a protoCallimico-marmoset group and the ancestor of the lion tamarins,which migrated south and eastwards, colonizing the present-dayBrazilian Atlantic Forest. Meanwhile (10 Ma), in the central Ama-zon Basin, the stock of proto-Callimico-marmosets (C) gave rise toCallimico and the ancestor of the marmosets (CebuellaMicoCalli-thrix). The subsequent split (D: 5 Ma) separated the AmazonianCebuella and Mico from the proto Callithrix lineage, which had mi-grated eastwards to colonize the Atlantic Forest the second calli-trichine invasion of this forest biome. Shortly afterwards, the lastsplit (E) occurred, separating the Amazonian marmosets, Cebuellaand Mico (See Fig 4).

At least two different callitrichine lineages appear to have in-vaded the Atlantic Forest during distinct periods (9 Ma: lion tam-arins and 5 Ma: Callithrix ancestors). Interestingly, the timing ofthe split between the Amazonian and Atlantic Forest groups of titis(Callicebus moloch and C. personatus groups: Perelman et al., 2011),howler monkeys (Alouatta seniculus and A. fusca groups: Corts-Ortiz et al., 2003), and capuchins (Cebus and Sapajus: Lynch Alfaroet al., 2012a,b) also coincided with the late Miocene to early Plio-cene, that is, 46 Ma. This suggests a period of greater connectivitybetween these major forest biomes in Brazil.

In a recent review of the geomorphological, climatic, and bio-geographic processes that shaped the biodiversity of the AmazonBasin, Hoorn et al. (2010) provided new insights into the role of dif-ferent factors in the formation of the present-day landscape.According to these authors, during the Paleogene (6534 Ma), thewestern Amazonian lowlands were characterized by interchangingfluvial conditions and marine embayments, with plate abductionFig. 4. Proposal of an evolutionary pathway for the callitrichines. Ages at the nodeswere based on Perelman et al. (2011) estimates. Colored branches indicate Atlantic(blue) and Amazon (green) biomes.along the Pacific margin causing an uplifting of the central Andes.Subsequent plate breaking in the Pacific and the collision of thenew plates with the South American and Caribbean plates resultedin increased mountain building in the northern Andes. Later, paral-lel to further uplift in the Andes, a mega-wetland of shallow lakesand swamps developed in the western Amazon basin (12 Ma).This scenario depicted by Hoorn et al. (2010) also includes the for-mation of deep canyons into the central and northern Andes,increasing sedimentation in the Andean forebasin, a cooling cli-mate and a decline in global sea levels.

One of the most intriguing questions for understanding of therecent history of the New World monkeys is the establishment ofthe modern Amazonian Basin as we can see today. According toHoorn et al. (2010), Andean sediments began to reach the Atlanticcoast through the Amazon drainage system, and the Amazon Riveritself became fully established at 7 Ma. As a consequence, themegawetland of the western Amazon Basin changed from a lacus-trine to a pluvial system similar to the present-day Pantanal, andsubsequently shifted to a floodplain environment. The floodplainswere initially dominated by grasslands, but ultimately substitutedby forests. The final episode in this process was characterized byfurther Andean uplift, the closure of the Isthmus of Panama(3.5 Ma) and the ice ages (2.50.01 Ma). There is no doubt thatthe New World monkeys played out within this complex scenario.

The Mio-Pliocene may have been an especially crucial period,with the shift from grassland to forest and the formation of theintricate river systemwith its diversity of habitats, niches, and zoo-geographic barriers. It seems that the present-day diversity of theplatyrrhines occurred in the context of the formation of the luxuri-ous Amazon rainforest at the end of the Miocene and throughoutmost of the Pliocene.

Over the past decade, a number of studies of the intra-genericphylogeny and phylogeography of the platyrrhines have providednew insights into the evolutionary history of these primates inthe context of this recent geological history. For example, the phy-logenetics of Saguinus based on mitochondrial and nuclear markers(Tagliaro et al., 2000, Araripe et al., 2008 and Da Cunha et al., 2011)confirm that the diversification of this genus occurred primarily inthe western Amazon basin, with the more recent migration of themost derived forms (bicolor-midas-niger group) to the easternAmazon, including the colonization of the southeastern Amazonbasin by S. niger.

Corts-Ortiz et al. (2003) generated a robust molecular phylog-eny of Alouatta based on the DNA sequences of three mitochondrialand two nuclear genes. These authors estimated that the initialdiversification event in Alouatta occurred at 6.8 Ma. The split ofthe groups A. seniculus/A. sara/A. macconnelli/A. caraya, and A. belz-ebul/A. guariba took place at 5.1 Ma. The subsequent split betweenA. caraya and A. seniculus/A. sara/A. macconnelli as well as the splitbetween the Amazonian/Atlantic A. belzebul and the strict AtlanticForest A. guariba were estimated at 4 Ma. The separation betweenAlouatta palliata/A. coibensis and A. pigra split occurred around3.0 Ma.

The molecular phylogeny of Aotus is relatively well explored.Menezes et al. (2010) analyzed the phylogeny of this genus usingfive mitochondrial regions and the nuclear SRY (Y-linked) gene aswell as karyological data, and identified a major diversificationevent at around 4.62 Ma (interval: 3.076.43 Ma) related to thepresence of at least three refuges the Andean refuge (Aotus aza-rae, A. infulatus, and A. nigriceps), the Guyanan refuge (A. trivirga-tus), and the Brazilian refuge (A. griseimembra, A. lemurinus, A.zonalis, A. brumbacki, A. vociferans, A. miconax, and A. nancymae).

Regarding the evolution of capuchin monkeys, Lynch Alfaroet al. (2012a,b) estimated that the first diversification event beganat around 6 Ma, isolating the gracile Amazonian form (Cebus) fromthe robust form of the Atlantic Forest (Sapajus). Additionally, they

356 H. Schneider, I. Sampaio /Molecular Phylogenetics and Evolution 82 (2015) 348357undoubtedly demonstrated that Sapajus reinvaded the Amazon ba-sin very recently (400,000 years ago).

The same research team investigated the diversification of Sai-miri in South America, and its expansion into Central Americausing complete mitochondrial DNA sequences (Chiou et al.,2011). The results indicate that this genus went through a muchmore recent radiation in comparison with similar genera, such asCebus, Aotus, and Callicebus. The initial radiation in squirrel mon-keys was estimated to have occurred in the Pleistocene (1.5 Ma),with subsequent events occurring between 1.1 and 0.9 Ma.

Diverse platyrrhine taxa with an ample distribution in both theAmazon and Atlantic forests, such as Callicebus, demand more sys-tematic phylogeographic studies. Perelman et al. (2011) analyzedeight species in this genus Callicebus donacophilus from Bolivia,C. caligatus C. cupreus, C. brunneus, and C. moloch from the BrazilianAmazon basin, as well as C. coimbrai, C. personatus, and C. nigrifronsfrom the Atlantic Forest. Two major diversification events wereidentified in this study, the first occurring in the western Amazonbasin at around 9 Ma, the split the ancestors of C. donacophilus/C.caligatus from the other species. The second event separated theAmazon and Atlantic Forest taxa at 5.2 Ma.

Despite all these advances, a number of questions on the evolu-tion of New World monkeys remain unanswered, especially withregard to the history of the Amazon basin and the outstandingdiversity of the platyrrhines. The phylogeography of some groupslike titi, night, howler and spider monkeys have been neglectedand will require special attention in the near future. On the otherhand, the understanding of the mechanisms responsible for thisdiversity remains a major challenge, and will depend on interdisci-plinary efforts combining fields such as systematics, molecularphylogeny, paleontology, biogeography, and geology.

Acknowledgments

Funding for this research was provided by CNPq (Grants306233/2009-6 to IS, 473341/2010-7 and 305645/2009-9 to HS)and FAPESPA (PRONEX 2007 to HS).

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The systematics and evolution of New World primates A review1 Introduction2 The Molecular era2.1 The pioneers2.2 The first doubts2.2.1 Capuchins (Cebus) vs. squirrel monkeys (Saimiri)2.2.2 Goeldis monkey (Callimico goeldii)2.2.3 Amazonian vs. Atlantic forest marmosets2.2.4 Brachyteles, Ateles, and Lagothrix

2.3 Persistent doubts2.4 The Alu markers2.5 The phylogenomics approach

3 A more definitive classification of the platyrrhines4 Recent controversies about the number of platyrrhine genera4.1 Mico vs. Callithrix4.2 Callibella4.3 Oreonax4.4 Cebus vs. Sapajus

5 Biogeography and evolutionAcknowledgmentsReferences