Comparative Genomics and Molecular Evolution

Cytogenet Genome Res 108:38–46 (2005)DOI: 10.1159/000080800

The primates of the Neotropics: genomes andchromosomesH.N. Seuanez,a,b C.R. Bonvicinoa,c and M.A.M. Moreiraa

a Genetics Division, Instituto Nacional de Câncer, Rio de Janeiro; b Department of Genetics, Universidade Federal doRio de Janeiro; c Department of Tropical Medicine, Instituto Oswaldo Cruz, Rio de Janeiro (Brazil)

Supported by Instituto Nacional de Câncer, Fundaçao Ary Frauzino and PRONEX(Brazil).

Received 15 September 2003; revision accepted 3 November 2003.

Request reprints from: Héctor N. Seuanez, Division of GeneticsInstituto Nacional de Câncer, Rua André Cavalcanti, 4th floor20231-050 Rio de Janeiro, RJ (Brazil)telephone: +55-21-3233-1458; fax: +55-21-3233-1423e-mail: genetics@inca.gov.br

ABC Fax + 41 61 306 12 34E-mail karger@karger.chwww.karger.com

© 2005 S. Karger AG, Basel0301–0171/05/1083–0038$22.00/0

Accessible online at:www.karger.com/cgr

Abstract. The classification of neotropical primates hasbeen controversial. Different arrangements have been pro-posed, depending on taxonomic criteria and on the traits select-ed for phylogenetic reconstructions. These include gross mor-phologic characters, karyotypic attributes and DNA sequencedata of nuclear and mitochondrial genes and of repetitive

genomic components. These approaches have substantiallyclarified the main intergeneric relationships although severalintrageneric arrangements still remain to be elucidated. In thisreview, we compare karyologic and molecular data of this spe-ciose group.

Copyright © 2005 S. Karger AG, Basel

Neotropical primates (Platyrrhini) are presently distributedin a vast region of the New World, extending from Mexico toNorthern Argentina. Some 40 MYBP, a common ancestor ofthe extant platyrrhine species split from the common stock withthe Old World primates, a group which includes our own spe-cies, Homo sapiens. Since then, the phyletic radiation of neo-tropical primates accounts for a wide spectrum of morphologi-cally and karyotypically distinct taxa.

Morphological arrangements

Neotropical primates have been traditionally grouped intotwo or three families based on body size, dentition and pres-ence or absence of twin births (Simpson, 1945; Napier andNapier, 1967). Most authors divided them into two differentfamilies: one comprising the larger platyrrhines and another

grouping the squirrell-like clawed monkeys. Hershkovitz(1977), however, proposed a third, monotypic family (Callimi-conidae) where Callimico goeldii was included as an interme-diate morphotype between the large-sized and the small-sizedplatyrrhines. Conflicting propositions were put forward toexplain size differences because small body size was considereda primitive trait (Hershkovitz, 1977) or, alternatively, a veryderived attribute (Ford, 1986). Regardless of these consider-ations, morphologic studies coincided in recognizing 16 Pla-tyrrhini genera although cladistic analyses of morphologic andmorphometric attributes grouped them in different phylogenet-ic arrangements (Rosenberger, 1981; Ford, 1986; Kay, 1990).Furthermore, the number of recognized species within generahas also been subject to continuous revisions in biogeographicand morphologic analyses. A good example of these yet unsett-led taxonomic criteria is the case of the genus Callicebus inwhich the number of recognized species has recently increasedto 28 (van Roosmalen et al., 2002) from a previous report of 13species (Hershkovitz, 1990).

Molecular arrangements of platyrrhine genera

Molecular analyses have been more congruent in estab-lishing the phylogenetic relationship of platyrrhine genera(Schneider et al., 1993, 1996; Canavez et al., 1999a; von Dor-num and Ruvolo, 1999). Conjoint analyses of four nucleargenes [interphotoreceptor retinoid-binding protein (IRBP),

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Â-globin, glucose-6-phosphate dehydrogenase (G6PD) and ß-2-microglobulin (ß2m); Schneider et al., 2001] showed threemonophyletic clades (Fig. 1): one, corresponding to the cebidssensu Schneider et al., 2001 grouping the small, squirrel-likemarmosets and tamarins (Cebuella, Callithrix, Callimico,Leontopithecus and Saguinus) with Saimiri, Cebus and Aotus; asecond clade comprising the four genera previously grouped inthe atelids by morphological criteria (Alouatta, Ateles, Lago-thrix and Brachyteles); and a third clade (pithecids) groupingthe three pitheciine genera (Chiropotes, Cacajao and Pithecia)with a fourth genus (Callicebus).

Although the phylogenetic relationships of platyrrhine gen-era are presently well resolved by molecular analyses, a fewpoints still require clarification. One is the proposition of 15genera by abolishing the genus Cebuella (Barroso et al., 1997;Porter et al., 1997). A second point is the exact branching pat-tern of the cebids (Aotus, Cebus, Saimiri and callitrichines),and a third one accounts for the relationship between the threemain clades (cebids, pithecids, atelids) to precisely determinewhich two are more closely related to one another. On the otherhand, at the subgeneric level, all platyrrhines deserve to be thor-oughly investigated. Thus, a better understanding of the evolu-tionary process of New World primates requires a holisticapproach, encompassing traditional morphology, biogeographyand cytogenetics in association with molecular studies.

Cladistic analyses of molecular data from nuclear genes pro-vide useful inferences of phyletic divergences that took place along time ago (Schneider et al., 1993, 1996; Barroso et al., 1997;Porter et al., 1997). Conversely, analyses of mitochondrialDNA may provide more reliable phylogenetic reconstructionsof recently derived taxa in view of the higher rate of nucleotidesubstitutions occurring in the mitochondrial genome (Jacobs etal., 1995; Moreira, 1996; Tagliaro et al., 1997; Horovitz et al.,1998).

Callitrichine radiation: molecular and cytogenetic data

The Callitrichinae sensu Rosenberger (1981), formerly Cal-litrichidae sensu Napier and Napier (1967) comprise the smal-lest-sized species of neotropical primates. The extant five gen-era of Callitrichinae, Callimico, Callithrix, Cebuella, Leontopi-thecus and Saguinus are exclusively distributed in South Amer-ica, except for Saguinus, whose distribution extends to CentralAmerica (Hershkovitz, 1977).

Analyses of ß2m sequence data resulted in a consensus topo-logy shown in Fig. 2. Saguinus appeared as the most basal calli-trichine offshoot followed by Leontopithecus while Callimicoappeared as a sister branch of the clade formed by Callithrixand Cebuella (Canavez et al., 1999b). Similar topologies indi-cating that Callimico was a derived lineage were found withLINE-1 patterns (Seuanez et al., 1989), tandemly combined Â-globin and IRBP gene sequences (Schneider et al., 1996), mito-chondrial DNA topologies based on ND4 (Pastorini et al.,1998), 12S+16S genes (Horovitz et al., 1998) and cytochrome bDNA (Moreira and Seuanez, 1999), analyses of G-banded chro-mosomes (Canavez et al., 1996) and phylogenetic reconstruc-tions of painted chromosomes (Neusser et al., 2001). These

Fig. 1. Topology obtained by Schneider et al. (2001), by conjoint analysisof interphotoreceptor retinoid-binding protein (IRBP), Â-globin, glucose-6-phosphate dehydrogenase (G6PD) and ß-2-microglobulin (ß2 m ). The sametopology was obtained by maximum parsimony, neighbor joining and maxi-mum likelihood analyses. Numbers above nodes indicate bootstrap valuesfor neighbor joining topology.

findings contradicted previous cladistic analyses of morpholog-ical characters indicating that Callimico was the most basal cal-litrichine lineage (Rosenberger, 1984; Ford, 1986; Kay, 1990;Horovitz et al., 1998) and the postulation that Saguinus was themost derived taxon (Hershkovitz, 1977). The finding of Ce-buella as a derived callitrichine was also contradictory to theproposition that it represented a relict morphotype similar tothe common callitrichine ancestor. In fact, tamarins (Saguinusand Leontopithecus) were clearly more basal than marmosets(Callithrix, Cebuella and Callimico) and reduction of body sizeappeared to be a derived trait, in agreement with the hypothesisof phyletic dwarfism (Ford, 1986).

Distance estimates between Callithrix and Cebuella weresimilar to those between congeneric species rather than be-tween genera. Callithrix appeared as a paraphyletic genusbecause the Amazonian, argentata group was associated withCebuella pygmaea rather than with Callithrix species of thecoastal jacchus group. Similar arrangements were shown bymolecular analyses of Â-globin and 5)-flanking regions (Porter etal., 1997), mitochondrial DNA (Moreira, 1996; Tagliaro et al.,1997), karyological comparisons (Canavez et al., 1996) andmorphometric data (Natori, 1994) suggesting the inclusion ofCebuella pygmaea in the genus Callithrix, as Callithrix pyg-maea (Barroso et al., 1997; Porter et al., 1997).

Inside the argentata group, C. humeralifera appeared as asister branch of the C. argentata/C. emiliae clade in agreementwith morphological studies that considered C. emiliae as a sub-species of C. argentata (Hershkovitz, 1977). C. argentata,

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Fig. 2. Maximum parsimony topology ob-tained with ß-2-microglobulin DNA sequences.Numbers above nodes indicate bootstrap values(Canavez et al., 1999b).

C. emiliae and C. humeralifera were shown to be karyotypicallyidentical, with a diploid number of 44 chromosomes (Canavezet al., 1996), with large heterochromatic, telomeric blocks asso-ciated to a satellite DNA sequence (CarB) composed of 1,528-bp monomers (Alves et al., 1995). Presumably, this repetitivesequence was amplified in the common ancestor of C. argenta-ta, C. emiliae and C. humeralifera after the branching off ofCallithrix (Cebuella) pygmaea.

Cytogenetic analyses of five species of the jacchus groupshowed that they comprised a karyotypically identical cladewith a diploid number of 46 chromosomes (Nagamachi et al.,1997) and therefore uninformative for inferring phylogeneticrelationships within this group.

Molecular topologies and karyotypic analyses (Canavez etal., 1996) indicated that Leontopithecus was the second mostbasal callitrichine lineage. Comparisons of three Leontopithe-cus species, L. rosalia, L. chrysopygus and L. chrysomelas,showed that they shared a diploid number of 46 chromosomesand identical G-band karyotypes (Seuanez et al., 1988), aninvariance that might be indicative of a short time of diver-gence. Sequence analyses of ß2m in several individuals of threeLeontopithecus species failed to show interspecific or intraspe-cific differences, precluding resolution of their phylogeneticrelationship (Canavez et al., 1998). Mundy and Kelly (2001),however, using sequence data from intron 1 of the IRBP gene,proposed a clear sister-taxon relationship between golden liontamarins (L. rosalia) and black lion tamarins (L. chrysopygus).

Endonuclease restriction mapping (Hillis et al., 1996), as-sessing the presence or absence of particular cleavage sites inthe intergenic spacer (IGS) regions of rDNA, provided partialinsight to phylogenetic relationships between lion tamarins(Seuanez et al., 2002). This analysis, using five restriction

enzymes and based on 89 mapped sites, showed four differentfixed sites between L. rosalia and L. chrysomelas and betweenL. rosalia and L. chrysopygus, and two different fixed sitesbetween L. chrysomelas and L. chrysopygus. Phylogenetic anal-ysis under Dollo parsimony (assuming that informative charac-ters – in this case restriction sites – are more frequently lostthan gained because nucleotide substitutions alter base pairsequences at recognition sites) showed a closer relationshipbetween L. chrysomelas and L. chrysopygus, sustained by ashared gain of one HindIII and one EcoRI site. This arrange-ment was in agreement with the distance-based allozyme dataof Forman et al. (1986), but contradictory to both the distance-based reconstruction derived from cytochrome b sequence data(Moreira et al., 1996; Moreira and Seuanez, 1999) and nuclearIRBP sequences (Mundy and Kelly, 2001).

The internal arrangements of Saguinus obtained by Cana-vez et al. (1999b) in the most parsimonious consensus tree fol-lowing analyses of ß2m sequence data showed S. fuscicollis asthe most basal Saguinus lineage in contradiction to previousmorphometric topologies so far reported (Hanihara and Natori,1987; Natori, 1988; Natori and Hanihara, 1988, 1992; Mooreand Cheverud, 1992). Associations among Saguinus speciesgroups also differed from morphological arrangements, al-though S. midas/S. bicolor and S. mystax/S. imperator wereclosely grouped as previously reported (Natori, 1988).

Following the emergence of S. fuscicollis, the clade wasdivided in three trichotomic branches: one leading to S. bico-lor/S. midas, another to S. imperator/S. mystax, and a thirdone to S. oedipus. In the first branch, one S. midas subspecies(S. m. midas) strongly grouped with both S. bicolor subspecies(S. bicolor bicolor and S. bicolor martinsi) rather than withS. midas niger. This grouping was coincident with biogeo-

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graphic data because S. b. bicolor and S. b. martinsi are con-tained within the distribution of S. m. midas on the left bank ofthe Amazonas river. Conversely, S. m. niger is distributed atthe right bank of the Amazonas river, being allopatric in respectto S. m. midas and the two S. bicolor subspecies. A comparisonof molecular and biogeographic data therefore suggested thatgeographic isolation of S. m. niger from S. m. midas/S. b. bico-lor/S. b. martinsi must have taken place before these threegroups diverged from one another. Our topology indicated,moreover, a paraphyletic arrangement for S. midas, requiring ataxonomic revision of this taxon.

Chromosome studies in Saguinus have not yet provided aclear consensus karyotype of this speciose genus. Regardless ofthis fact, all species so far described showed a diploid numberof 46 chromosomes as was the case of S. midas midas and S.midas niger (Nagamachi et al., 1999), S. fuscicollis fuscicollisand S. mystax (Pieczarka et al., 2001), and S. oedipus (Müller etal., 2001). S. oedipus and human chromosomes have been usedas probes in experiments of reciprocal chromosome painting(Neusser at al., 2001) and this analysis was congruent withmolecular data in placing Saguinus as the most basal callitri-chine lineage (Neusser et al., 2001).

Mitochondrial DNA sequence analyses were not coincidentwith these arrangements. Although analyses of the D-loopregion coincided in dividing the genus Callithrix (includingCallithrix pygmaea) into two groups (coastal and Amazonian),paraphyletic arrangements were observed (Tagliaro et al.,1997). In the Amazonian group, C. mauesi was paraphyletic,with specimens grouping with C. humeralifera while, in thecoastal group, C. jacchus, C. kuhlii and C. penicillata were alsoparaphyletic and more derived in respect to C. geoffroyi and tothe most basal C. aurita. In both groups, paraphyly indicatedpresence of trans-specific mitochondrial polymorphisms thatwere present in the common ancestor of each group and ante-ceded species divergence.

Interestingly, cytochrome b pseudogenes, resulting frommultiple insertions of different cytochrome b segments in thenuclear genome, were found in all callitrichine genera (Mundyet al., 2000). They originated at different times and lineagesduring callitrichine evolution and some sequences were dupli-cated following nuclear insertion. As the rate of nucleotide sub-stitution in the nuclear genome is lower than in mitochondria,these paralogous sequences are useful indicators for phyloge-netic reconstructions due to retention of ancestral states(Zischler et al., 1995). This was helpful for demonstrating thestrong association of Cebuella with the argentata species group(Moreira and Seuanez, 1999).

Contrary to the maternal transmission of mitochondrialDNA, the sex determining region Y gene (SRY) is paternallytransmitted. The parsimony SRY topology of callitrichines(Moreira, 2002) was in agreement with other molecular ar-rangements despite showing a lower resolution, with somenodes collapsing in polytomies (Fig. 3). Callimico was associat-ed to a trichotomic clade comprising Callithrix (Cebuella) pyg-maea, Callithrix aurita and a third branch leading to a polyto-my with the remaining Callithrix species of the jacchus group(C. jacchus, C. geoffroyi, C. kuhlii and C. penicillata). Interest-ingly, the species of the jacchus group were not associated in a

monophyletic clade consequently to absence of SRY synapo-morphies between C. aurita and the remaining species. Thistopology was not, however, in disagreement with mitochon-drial arrangements showing C. aurita as a basal offshoot of thejacchus-group (Tagliaro et al., 1997). In fact, differences be-tween autosomal, mitochondrial and male-specific topologies(like SRY) as well as evidences of ancestral polymorphismsamong Callithrix species are indicative of recent speciationevents and reflect the limits of phylogenetic resolution of close-ly related groups.

Cebus, Saimiri and Aotus

The genus Cebus has been traditionally divided into twospecies groups based on pelage and presence of head tufts(Hershkovitz, 1949) but the number of recognized species andsubspecies is controversial. Although Cebus taxonomy isbeyond the scope of this work, most arrangements include fourspecies, one belonging to the “tufted group” (C. apella; 2n = 54)and three others to the “untufted group”: C. albifrons (2n = 54),C. capucinus (2n = 54) and C. nigrivittatus = C. olivaceus (2n =52).

Cebus species have been extensively studied since theirbanded karyotypes were first reported by Torres de Caballero etal. (1976). C. apella populations or subspecies from differentgeographic regions showed chromosome polymorphisms due tovariations in constitutive heterochromatin (Matayoshi et al.,1987; Martinez et al., 2002) while C. apella xanthosternos (2n =54) showed a distinctive chromosome pair in respect to otherC. apella (Seuanez et al., 1986). The conspicuous amount ofconstitutive heterochromatin of Cebus apella contained twodifferent types of highly repetitive sequences, named CapA andCapB (Fanning et al., 1993). The former satellite DNA, consist-ing of 1,500-bp monomers, hybridized in situ at regions con-taining interstitial and terminal heterochromatic blocks. Con-versely, CapB consisted of monomeric units of ca. 340 bp thatshowed sequence similarity to alphoid sequences that hybrid-ized at centromeric regions of the acrocentric chromosomes ofC. apella (Fig. 4).

Comparisons of the four Cebus species with G/C bandingand painting with human chromosome probes allowed infer-ences to be made on the presumed ancestral karyotype of thegenus (Garcia et al., 2002). It seems that the Cebus ancestor hada diploid number of 54 chromosomes, with a karyotype similarto the ancestral platyrrhine karyotype and that chromosomeinversions were the most common rearrangement among theCebus karyotypes. Moreover, the 2n = 52 of C. nigrivittatusappears to be a derived trait resulting from a fusion event oftwo acrocentric chromosomes. These findings are not entirelycongruent with those from molecular data, although moleculardata are still too fragmentary to solve the phylogenetic relation-ships of Cebus species. Moreira (2002), analyzing SRY se-quence data, obtained a phylogeny supporting the morphologicproposition of two groups (tufted and untufted). The formergroup included C. apella in one branch and C. apella xantho-sternos in another while, in the untufted group, C. nigrivittatusappeared as a more basal offshoot in respect to a more derived

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Fig. 3. Maximum parsimony topology obtained with SRY DNA sequences. Numbers above nodesindicate bootstrap values (Moreira, 2002).

Fig. 4. In situ hybridization of CapB satelliteDNA to Cebus apella acrocentric chromosomes(Fanning et al., 1993).

trichotomic clade comprising one C. capucinus and two C. albi-frons specimens.

The genus Saimiri is widely spread in several regions ofSouth America and the species holotype, Saimiri sciureus, has adiploid number of 44 chromosomes. Comparisons with othercongeneric species (S. boliviensis boliviensis and S. boliviensisperuviensis) showed pericentric inversions and significant dif-ferences in distribution of constitutive heterochromatin(Moore et al., 1990), in agreement with previous findings inspecimens from Peru, Colombia, Bolivia and Guyana (Ariga etal., 1978). Chromosome painting analyses (Stanyon et al.,2000) and phylogenetic reconstructions of painted chromo-somes (Neusser et al., 2001) coincide in placing Saimiri as asister branch of the lineage leading to the callitrichine clade and

diverging from it by five fusions and one fission. This studyindicated, however, that Saimiri was more closely related thanCebus to the callitrichines, a finding that is not evident inmolecular arrangements.

The genus Aotus is very complex due to difficulties in differ-entiating species by morphological attributes. Classical taxono-my divided Aotus in two groups, one comprising four speciesdistributed north of the Amazonas river and another, with fivespecies, south of this river (Hershkovitz, 1983). Altogether thisgenus occupies a vast region of the neotropics, from Panama tonorthern Argentina. Recent molecular analyses (Schneider etal., 2001) placed Aotus as the most basal offshoot of the cebidclade although the precise position of Aotus within this claderequires additional confirmation. Karyologic studies of this

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genus have been extensively carried out by Ma and her co-workers and a survey of captive animals showed eleven differ-ent karyotypes (Ma et al., 1976a, b; Ma, 1984). These studiesand more recent reports of Colombian specimens (Torres et al.,1998) indicated that the diploid chromosome number in Aotusranges from 2n = 46 to 2n = 59. Comparative gene assignmentand karyotypic comparisons of banded chromosomes indicatedthat Aotus is a highly rearranged group in which genomic shuf-fling has been prominent. Although several studies showedsyntenic homologies with humans and confirmed that chromo-some evolution within this genus occurred mainly by fusionand fission events (Ma, 1984; Ma and Gerhard, 1992), a phylo-genetic reconstruction of the Aotus ancestral karyotype isrequired for a reliable comparison with other platyrrhine gen-era.

Pithecid radiation: molecular and cytogenetic data

Phylogenetic reconstructions based on molecular datashowed a well-supported pithecid clade comprising four gen-era, with Callicebus as the most basal lineage (Schneider et al.,2001; Fig. 1). This genus is complex and diversified, with a geo-graphic distribution throughout most of the tropical forests ofthe Amazonas and Orinoco basins, parts of the Atlantic andParana river forests of south-eastern Brazil, and in Bolivia andParaguay (Hershkovitz, 1990). Van Roosmalen et al. (2002)recognized 28 species arranged in five species groups (donaco-philus, moloch, cupreus, torquatus and personatus) while karyo-logic studies showed a wide spectrum of variation in diploidchromosome number, ranging from 2n = 50 in C. hoffmannsi to2n = 16 in C. lugens, the species with the lowest diploid numberin the primate order (Fig. 5; Bonvicino et al., 2003b). Whilemolecular studies associated Callicebus with Pithecia, Cacajaoand Chiropotes, it has been so far impossible to clearly link Cal-licebus to any other platyrrhine genus by phylogenetic recon-structions based on comparative karyology. Three Callicebuskaryotypes, belonging to C. moloch with 2n = 50 (Stanyon et al.,2000), C. donacophilus pallescens with 2n = 50 (Barros et al.,2003) and C. lugens with 2n = 16 (Stanyon et al., 2003), paintedwith human chromosome probes showed a high number of dis-ruptions and associations of human syntenic clusters, especiallyin C. lugens whose diploid number has been drastically re-duced. These results demonstrated that these species have gonethrough considerable genomic shuffling with respect to thehuman and to the putative platyrrhine ancestral karyotype butfailed to establish a clear representation of the ancestral Callice-bus karyotype. Here again, as in Aotus, intrageneric karyotypiccomparisons are needed before reliable intergeneric compari-sons can be carried out.

The clade (Pithecia (Cacajao, Chiropotes)) is well estab-lished in arrangements based on morphology (Rosenberger,1981; Ford, 1986; Kay, 1990) and molecular data of nucleargenes (Schneider et al., 2001) and alphoid satellite DNAs(Alves et al., 1998). Phylogenetic reconstructions based oncytochrome b DNA data (Bonvicino et al., 2003a) confirmedthat the three pitheciine genera were strongly associated, thatPithecia was the most basal offshoot and this basal genus split

Fig. 5. Karyotype of Callicebus lugens (2n =16). The X chromosome in female animals wasidentified by ZOO-FISH by Bonvicino et al.,2003b).

into two branches: one leading to P. irrorata and a sister branchto P. albicans and P. monachus. The other pitheciine clade splitinto two branches: one leading to Cacajao calvus/Cacajaomelanocephalus and the other leading to Chiropotes. In this lat-ter clade, C. albinasus appeared as the most basal lineage withrespect to C. utahicki and Chiropotes israelita from Rio Negro(Brazil). Comparisons of G-banded chromosomes (Moura-Pen-sin et al., 2001) indicated that Pithecia (2n = 48) showed themost primitive karyotype followed by Chiropotes (2n = 54) and,finally by the most rearranged karyotype of Cacajao (2n = 45 inmales and 46 in females due to Y-autosome translocation).

Atelid radiation: molecular and cytogenetic data

Phylogenetic reconstructions based on molecular datashowed a well-supported atelid clade comprising four genera,with Alouatta as the most basal lineage (Schneider et al., 2001;Fig. 1). Alouatta is the most widespread neotropical primategenus whose distribution extends from southern Mexico tonorthern Argentina. It can be divided into a trans-Andeangroup, with species from Mexico, Central America and thenorthwestern coast of South America (Colombia and Ecuador)and a cis-Andean group that includes most of South Americanspecies. Morphologic, karyologic and molecular studies of thiscomplex genus show disparate intrageneric arrangements(Hershkovitz, 1949; Gregorin, 1996; Bonvicino et al., 2001; deOliveira et al., 2002; Cortés-Ortiz et al., 2003).

Phylogenic reconstructions based on mitochondrial DNAshowed a dichotomic separation between trans-Andean andcis-Andean species, which was proposed to occur some 6.8MYA (Cortés-Ortiz et al., 2003). While the trans-Andean cladeshowed two separate branches, one leading to A. palliata mexi-cana/A. coibensis trabeata and another to A. pigra, the cis-Andean group split into two branches: one leading to A. belze-bul/A. guariba and the other leading to the clade (A. caraya(A. macconnelli (A. seniculus, A. sara))). However, a previousreport (Bonvicino et al., 2001) on seven Brazilian Alouatta spe-cies showed that A. caraya was the most basal lineage of theclade (A. caraya ((A. seniculus (A. nigerrima (A. stramineus,A. macconnelli))) (A. guariba, A. belzebul))). This arrange-ment, based on cytochrome b DNA data confirmed the ar-

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rangement (A. caraya (A. seniculus (A. guariba, A. belzebul)))proposed by Meireles et al. (1995, 1999) based on Á1 -globinpseudogene sequences. (Note: A. guariba is the synonymoussenior of A. fusca. Species names in the text follow citations inthe literature).

Karyotypic studies of Alouatta showed that diploid chromo-some number varies from 2n = 43 to 54. In some species, likeA. seniculus the diploid number may vary due to presence ofdifferent numbers of microchromosomes. Several sex chromo-some systems have also been described in different species likeXX/XY, X1X1X2X2/X1X2Y,X1X1X2X2/X1X2Y1Y2 andX1X1X2X2X3X3/X1X2X3Y1Y2 (see Yunis et al., 1976; Ar-mada et al., 1987; Lima and Seuanez, 1991; de Oliveira et al.,2002). A correlation of molecular and karyotypic data providessome clues on how Alouatta species evolved. Three species dif-fering by low genetic distance estimates like A. macconnelli, A.stramineus and A. nigerrima are, however, karyotypically dif-ferent from one another (Armada et al., 1987; Lima and Seua-nez, 1991) because A. macconnelli and A. stramineus share thesame diploid number (2n = 47, 48 or 49) and an X1X1X2X2/X1X2Y1Y2 sex chromosome system. A. macconnelli and A.stramineus are karyotypically very similar, differing from oneanother in only two chromosome pairs that can be derived fromone another by a translocation. On the other hand, A. nigerrimahas a diploid chromosome number of 50 in the female and itskaryotype showed, moreover, nine pairs of biarmed autosomepairs against 11 pairs in A. macconnelli and A. stramineus.Karyotypic comparisons thus indicated that A. macconnelliand A. stramineus are more similar to one another than any ofthem is to A. nigerrima (see Armada et al., 1987; Lima andSeuanez, 1991), thus confirming the branching pattern hereinobtained with cytochrome b data. The three above-mentionedspecies are karyotypically different from A. seniculus (2n = 43to 45) in which an XX/XY sex chromosome system wasreported (Yunis et al., 1976). Conversely, A. belzebul showed adiploid number of 50,X1X1X2X2 in the female and 49,X1X2Yin the male (Armada et al., 1987). A. fusca (= A. guariba)showed different karyomorphic groups: 2n = 52, with anXX/XY sex chromosome system in Espırito Santo state, Brazil;2n = 48 and 2n = 50 with an XX/XY sex chromosome systemin Sao Paulo State; 2n = 49,X1X2Y/50,X1X1X2X2 in Rio deJaneiro and Sao Paulo states, Brazil; and 2n = 45,X1X2Y/46,X1X1X2X2 in Santa Catarina, Parana and south of SaoPaulo states in Brazil (de Oliveira, 1996; de Oliveira et al.,1998). A more recent report (de Oliveira et al., 2002) con-sidered the 2n = 45/46 specimens as belonging to A. fusca cla-mitans and the 2n = 49/50 as A. fusca fusca (the former karyo-type was derived from the latter by two Robertsonian fusionsand, in both subspecies, the sex chromosome system wasX1X1X2X2X3X3/X1X2X3Y1Y2). In A. caraya specimenswith 2n = 52 the sex chromosome system, initially described asXX/XY (Mudry et al., 1990; de Oliveira, 1996) was later con-sidered to be X1X1X2X2/X1X2Y1Y2 (Mudry et al., 2001; deOliveira et al., 2002). The X1X1X2X2/X1X2Y1Y2 sex chro-mosome system was also reported in A. sara and A. arctoidea(Stanyon et al., 1995; Consigliere et al., 1996). Chromosomepainting of A. caraya, A. macconnelli, A. fusca clamitans,A. fusca fusca, A. sara and A. arctoidea with human chromo-

some probes showed that X2p and X2q corresponded to ahuman 15/3 association and that the Y2 chromosome waspainted by the same human probe 3. This indicated that therearrangements originating these chromosomes were the sameand must have occurred only once and that an additional rear-rangement took place in A. fusca clamitans and A. fuscafusca to account for the emergence of an X1X1X2X2X3X3/X1X2X3Y1Y2 system.

De Oliveira et al. (2002), when comparing painting karyo-types proposed a chromosome phylogeny based on an ancestralAtelid karyotype of 2n = 62 and an ancestral Alouatine karyo-type with the same diploid number for explaining karyotypicevolution in A. arctoidea, A. sara, A. macconnelli, A. caraya, A.fusca, A. belzebul and A. caraya. This proposition relies, how-ever, on the assumption that the rearrangements that originat-ed the X1 and X2 chromosomes, or the X1X1X2X2/X1X2Y1Y2 sex chromosome system, were synapomorphictraits for all alouatines. This assumption overlooked two im-portant findings: the XX/XY system in A. seniculus (Yunis etal., 1976) and the X1X1X2X2/X1X2Y system in A. belzebul.The former system is the most frequent in mammals and there-fore more likely to be ancestral than any other derived by sexchromosome rearrangements with autosomes while the latter,derived from a Y-autosome translocation, is simpler than theX1X1X2X2/X1X2Y1Y2 sex chromosome system and ispresent in other neotropical primates like Aotus, Callimico andCacajao (Ma et al., 1976a; Seuanez et al., 1989; Moura-Pensinet al., 2001).

Ateline radiation: molecular and cytogenetic data

Molecular analyses (Schneider et al., 2001) showed a well-supported ateline clade (Ateles (Lagothrix, Brachyteles)) inagreement with karyotypic data showing a diploid chromosomenumber of 32 or 34 in Ateles (Seuanez et al., 2001) and 62 inLagothrix and Brachyteles (Viegas-Pequignot et al., 1985).Comparative charts of 80 assigned loci in Ateles paniscus cha-mek (Seuanez et al., 2001) and chromosome painting in Atelesgeoffroyi (Morescalchi et al., 1997) provided clear evidence thatboth species were karyotypically very similar and highly de-rived with respect to the presumed ancestral karyotype of theplatyrrhines. This accounted for several associations of sepa-rate human syntenic clusters as well as for disruptions associat-ed with reduction in diploid number to 2n = 34 in these twospecies.

Human and Lagothrix chromosome probes, when used inexperiments of reciprocal painting showed more refined datafor inferring karyotypic evolution in platyrrhines (Stanyon etal., 2001). While the 23 human probes produced 39 signals inLagothrix, reciprocal painting of human chromosomes withLagothrix probes produced 45 signals. These experiments iden-tified a derived association, similar to a human 4/15 transloca-tion, as a synapomorphic trait for all atelids in conjunction withfragmentations of human chromosome clusters 1, 4 and 15.These data have been useful for phylogenetic reconstructionson Alouatta species (de Oliveira et al., 2002) and Callicebuslugens (Stanyon et al., 2003). Finally, the karyotype of Brachy-

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teles was considered to be ancestral with respect to Lagothrixby analyses of banded chromosomes (Viegas-Pequignot et al.,1985) but this proposition, however, did not consider represen-tative species of closely related genera.

Conclusion and perspectives

Neotropical primates are taxonomically complex althoughphylogenetic relationships, at the generic level, are now wellestablished. Intrageneric arrangements are, however, more

problematic and need to be resolved by conjoint analyses ofmorphological, molecular and karyotypic data. In addition,biogeographic data are needed for proper identification of thearea of capture and for relevant information on the distributionof congeneric species. Moreover, population studies are mostuseful to see how a species has evolved under the selective pres-sures imposed by different habitats. Additional sequence datamight be required to sort out controversial nodes in conflictingtopologies. Reciprocal chromosome painting and comparativegene charts will eventually identify many of the complex karyo-typic rearrangements.

References

Alves G, Canavez FC, Seuanez HN, Fanning TG:Recently amplified satellite DNA in Callithrix ar-gentata (Primates, Platyrrhini). Chromosome Res3:207–213 (1995).

Alves G, Seuanez HN, Fanning T: A clade of NewWorld primates with distinctive alphoid satelliteDNAs. Mol Phylogenet Evol 9:220–224 (1998).

Ariga S, Dukelow WR, Emley GS, Hutchinson RR:Possible errors in identification of squirrel mon-keys (Saimiri sciureus) from different South Amer-ican points of export. J Med Primatol 7:129–135(1978).

Armada JLA, Barroso CML, Lima MMC, MunizJAPC, Seuanez HN: Chromosome studies inAlouatta belzebul. Am J Primatol 13:283–296(1987).

Barros RMS, Nagamachi CY, Pieczarka JC, RodriguesLRR, Neusser M, de Oliveira EH, Wienberg J,Muniz JAPC, Rissino JD, Muller S: Chromosomalstudies in Callicebus donacophilus pallescens, withclassic and molecular cytogenetic approaches: Mul-ticolour FISH using human and Saguinus oedipuspainting probes. Chromosome Res 11:327–334(2003).

Barroso CML, Schneider H, Schneider MPC, SampaioMIC, Harada ML, Czelusniak J, Goodman M:Update on phylogenetic systematics of New Worldmonkeys: further DNA evidence for placing thepygmy marmoset (Cebuella) within the marmosetgenus Callithrix. Int J Primatol 18:651–673(1997).

Bonvicino CR, Lemos B, Seuanez HN: Molecular phy-logenetics of howler monkeys (Alouatta, Platyr-rhini). A comparison with karyotypic data. Chro-mosoma 110:241–246 (2001).

Bonvicino CR, Boubli JP, Otazu IB, Almeida FA, Nas-cimento FF, Coura JC, Seuanez HN: Morphologic,karyotypic and molecular evidence of a new formof Chiropotes (Primates, Pitheciinae). Am J Prima-tol 61:123–133 (2003a).

Bonvicino CR, Penna-Firme V, Nascimento FF, Le-mos B, Stanyon R, Seuanez HN: The lowest dip-loid number (2n=16) yet found in any primates,Callicebus lugens (Humboldt, 1811). Folia Prima-tol 74:141–149 (2003b).

Canavez FC, Alves G, Fanning TG, Seuanez HN: Com-parative karyology and evolution of the Amazon-ian Callithrix (Platyrrhini, Primates). Chromoso-ma 104:348–357 (1996).

Canavez F, Ladasky JJ, Muniz JA, Seuanez HN, Par-ham P: ß2 -Microglobulin in neotropical primates(Platyrrhini). Immunogenetics 48:133–140 (1998).

Canavez FC, Moreira MAM, Ladasky JJ, Pissinatti A,Parham P, Seuanez HN: Molecular phylogeny ofNew World primates (Platyrrhini) based on ß2 -microglobulin DNA sequences. Mol PhylogenetEvol 12:74–82 (1999a).

Canavez FC, Moreira MAM, Simon F, Parham P,Seuanez HN: Phylogenetic relationships of the Cal-litrichinae (Platyrrhini, Primates) based on ß-2 mi-croglobulin sequences. Am J Primatol 48:225–236(1999b).

Consigliere S, Stanyon R, Koehler U, Agoramoorhty G,Wienberg J: Chromosome painting defines ge-nomic rearrangements between red howler monkeysubspecies. Chromosome Res 4:264–270 (1996).

Cortés-Ortiz L, Bermingham E, Rico C, Rodrıguez-Luna E, Sampaio I, Ruiz-Garcıa M: Molecular sys-tematics and biogeography of the Neotropicalmonkey genus, Alouatta. Mol Phylogenet Evol26:64–81 (2003).

de Oliveira EHC: Estudos citogenéticos e evolutivosnas espécies brasileiras e argentinas do gêneroAlouatta Lacépède 1799 (Primates, Atelidae).MSc. dissertation, Universidade Federal do Para-na, Curitiba (1996).

de Oliveira EHC, Lima MMC, Sbalqueiro IJ, PissinattiA: The karyotype of Alouatta fusca clamitans fromRio de Janeiro state, Brazil: evidence for a Y-auto-some translocation. Genet Mol Biol 31:361–364(1998).

de Oliveira EH, Neusser M, Figueiredo WB, Nagama-chi C, Pieczarka JC, Sbalqueiro IJ, Wienberg J,Muller S: The phylogeny of howler monkeys(Alouatta, Platyrrhini): reconstruction by multico-lor cross-species chromosome painting. Chromo-some Res 10:699–683 (2002).

Fanning TG, Seuanez HN, Forman L: Satellite DNAsequences in the new world primate Cebus apella(Platyrrhini, Primates). Chromosoma 102:306–311 (1993).

Ford SM: Systematics of New World monkeys; inSwindler DR, Erwin J (eds): Comparative PrimateBiology, pp 73–135 (Alan R. Liss Inc., New York1986).

Forman L, Kleiman DG, Bush RM, Dietz JM, BallouJD, Phillips LG, Coimbra-Filho AF, O’Brien SJ:Genetic variation within and among lion tamarins.Am J Phys Anthropol 71:1–11 (1986).

Garcıa F, Ruiz-Herrera A, Egozcue J, Ponsa M, GarciaM: Chromosomal homologies between Cebus andAteles (Primates) based on ZOO-FISH and G-banding comparisons. Am J Primatol 57:177–188(2002).

Gregorin R: Variaçao geografica e taxonômica dasespécies brasileiras do Alouatta Lacépède, 1799(Primates, Atelidae). MSc dissertation, Universi-dade de Sao Paulo, Sao Paulo (1996).

Hanihara T, Natori M: Preliminary analysis of numer-ical taxonomy of the genus Saguinus based on den-tal measurements. Primates 28:517–523 (1987).

Hershkovitz P: Mammals of northern Colombia. Pre-liminary report No. 4. Monkeys (Primates), withtaxonomic revisions of some forms. Proc US NatMus 98:323–427 (1949).

Hershkovitz P: Living New World monkeys (Platyr-rhini). (The University of Chicago Press, Chicago1977).

Hershkovitz P: Two new species of the night monkeys,genus Aotus (Cebidae, Platyrrhini): a preliminaryreport on Aotus taxonomy. Am J Primatol 4:209–243 (1983).

Hershkovitz P: Titis, new world monkeys of the genusCallicebus (Cebidae, Platyrrhini): a preliminarytaxonomic review. Field Zool, N.s. 55:1–109(1990).

Hillis DM, Moritz C, Mable BK: Molecular Systemat-ics, 2nd ed (Sunderland, Sinauer Associates 1996).

Horovitz I, Zardoya R, Meyer A: Platyrrhine Systemat-ics: A simultaneous analysis of molecular and mor-phometrical data. Am J Phys Anthropol 106:261–281 (1998).

Jacobs SC, Larson A, Cheverud JM: Phylogenetic rela-tionships and orthogenetic evolution of coat coloramong tamarins (genus Saguinus). Syst Biol 44:515–532 (1995).

Kay RF: The phyletic relationships of extant and fossilPitheciinae (Platyrrhini, Anthropoidea). J HumEvol 19:175–208 (1990).

Lima MMC, Seuanez HN: Chromosome studies in thered howler monkey, Alouatta seniculus strami-neus (Platyrrhini, Primates): description of aX1X2Y1Y2/X1X1X1X2X2 sex chromosome sys-tem and karyological comparisons with other sub-species. Cytogenet Cell Genet 57:151–156 (1991).

Ma NSF: Linkage and syntenic relationship in chromo-somes of owl monkeys (with karyotypes I, III, V,VI, VII) homologous to man, in O’Brien SJ (ed):Genetic Maps, Volume 3, pp 410–413 (ColdSpring Harbor Press, New York 1984).

Ma NSF, Gerhard DS: Mapping of five human chro-mosome 19 DNA markers to owl monkey chromo-somes. Cytogenet Cell Genet 59:57–62 (1992).

Ma NSF, Elliot NW, Morgan L, Miller A, Jones TC:Translocation of Y chromosome to an autosome inthe Bolivian owl monkey, (Aotus). Am J PhysAnthropol 45:191–202 (1976a).

Ma NSF, Jones TC, Miller AC, Morgan LM, AdamsEA: Chromosome polymorphism and banding pat-tern in the owl monkey (Aotus). Lab Anim Sci26:1022–1036 (1976b).

Martinez RA, Giudice A, Szapkievich VB, Ascunce M,Nieves M, Zunino G, Mudry MD: Parametersmodeling speciogenic processes in Cebus apella(Primates: Platyrrhini) from Argentina. MastozoolNeotr 9:171–186 (2002).

Matayoshi T, Seuanez HN, Nasazzi N, Nagle C, Ar-mada JLA, Freitas L, Alves G, Barroso CML,Howlin E: Heterochromatic variation in Cebusapella (Cebidae, Platyrrhini) of different geograph-ic regions. Cytogenet Cell Genet 44:158–162(1987).

Dow

nloa

ded

by:

Uni

v. o

f Mic

higa

n, T

aubm

an M

ed.L

ib.

141.

213.

236.

110

- 9/

6/20

13 2

:06:

54 A

M

46 Cytogenet Genome Res 108:38–46 (2005)

Meireles CMM, Schneider MPC, Sampaio MIC,Schneider H, Slightom JL, Chiu C-H, NeiswangerK, Gumucio DL, Stanhope M, Czelusniak J, Good-man M: Fate of a redundant Á-gene in the atelidclade of New World monkeys: Implications con-cerning fetal globin gene expression. Proc NatlAcad Sci USA 92:2607–2611 (1995).

Meireles CM, Czelusniak J, Ferrari SF, SchneiderMPC, Goodman M: Phylogenetic relationshipsamong Brazilian howler monkeys, genus Alouatta(Platyrrhini, Atelidae), based on Á-globin pseudo-gene sequences. Genet Mol Biol 22:337–344(1999).

Moore AJ, Cheverud JM: Systematics of the Saguinusoedipus group of the bare-face tamarins: evidencefrom facial morphology. Am J Phys Anthropol89:73–84 (1992).

Moore CM, Harris CP, Abee CR: Distribution of chro-mosomal polymorphisms in three subspecies ofsquirrel monkeys (genus Saimiri). Cytogenet CellGenet 53:118–122 (1990).

Moreira MAM: Relaçoes filogenéticas dos calitriquı-neos (Primates, Platyrrhini) a partir de seqüênciasde citocromo b e pseudogenes mitocondriaispresentes no nucleo, e de espécies do grupo jacchusdo gênero Callithrix a partir de seqüências de alçaD. PhD. dissertation, Universidade Federal do Riode Janeiro (1996).

Moreira MAM: SRY evolution in Cebidae (Platyrrhini,Primates). J Mol Evol 55:92–103 (2002).

Moreira MAM, Seuanez HN: Mitochondrial pseudo-genes and phylogenetic relationships of Cebuellaand Callithrix (Platyrrhini, Primates). Primates40:353–364 (1999).

Moreira MAM, Almeida CAS, Canavez FC, Olicio R,Seuanez HN: Heteroduplex mobility assays(HMAs) and analogous sequence analyses of acytochrome b region indicate phylogenetic rela-tionships of selected callitrichids. J Hered 87:456–460 (1996).

Morescalchi MA, Schempp W, Consigliere S, Bigoni F,Wienberg J, Stanyon R: Mapping chromosomalhomology between humans and the black handedspider monkey by fluorescence in situ hybridiza-tion. Chromosome Res 5:527–536 (1997).

Moura-Pensin C, Pieczarka JC, Nagamachi CY, MunizJAPC, Brigido MCO, Pissinatti A, Marinho A,Barros RMS: Cytogenetic relations among the gen-era of the subfamily Pitheciinae (Cebidae, Pri-mates). Caryologia 54:385–391 (2001).

Mudry MD, Slavutsky I, Vinuesa ML: Chromosomecomparison among five species of Platyrrhini(Alouatta caraya, Aotus azarae, Callithrix jacchus,Cebus apella and Saimiri sciureus). Primates31:415–420 (1990).

Mudry MD, Rahn IM, Solari AJ: Meiosis and chromo-some painting of sex chromosome systems in Ce-boidea. Am J Primatol 54:65–78 (2001).

Müller S, Neusser M, O’Brien PC, Wienberg J: Molecu-lar cytogenetic characterization of the EBV-pro-ducing cell line B95-8 (Saguinus oedipus, Platyrr-hini) by chromosome sorting and painting. Chro-mosome Res 9:689–693 (2001).

Mundy N, Kelly J: Phylogeny of lion tamarins (Leonto-pithecus spp) based on interphotoreceptor retinolbinding protein sequences. Am J Primatol 54:33–40 (2001).

Mundy NI, Pissinatti A, Woodruff DS: Multiple nu-clear insertions of mitochondrial cytochrome b se-quences in Callitrichine Primates. Mol Biol Evol17:1075–1080 (2000).

Nagamachi CY, Pieczarka JC, Schwarz M, Barros RM,Mattevi MS: Comparative chromosomal study offive taxa of genus Callithrix, group jacchus (Pla-tyrrhini, Primates). Am J Primatol 41:53–60(1997).

Nagamachi CY, Pieczarka JC, Muniz JA, Barros RM,Mattevi MS: Proposed chromosomal phylogenyfor the South American primates of the Callitrichi-dae family (Platyrrhini). Am J Primatol 49:133–152 (1999).

Napier JS, Napier PH: A Handbook of Living Primates(Academic Press, New York 1967).

Natori M: A cladistic analysis of interspecific relation-ships of Saguinus. Primates 29:263–276 (1988).

Natori M: Craniometral variation among Eastern Bra-zilian marmosets and their systematic relation-ships. Primates 35:167–176 (1994).

Natori M, Hanihara T: An analysis of interspecific rela-tionships of Saguinus based on cranial measure-ments. Primates 29:255–262 (1988).

Natori M, Hanihara T: Variations in dental measure-ments between Saguinus species and their system-atic relationships. Folia Primatol 58:84–92 (1992).

Neusser M, Stanyon R, Bigoni F, Wienberg J, Müller S:Molecular cytotaxonomy of New World monkeys(Platyrrhini) – comparative analysis of five speciesby multi-color chromosome painting gives evi-dence for a classification of Callimico goeldii with-in the family of Callitrichidae. Cytogenet Cell Ge-net 94:206–215 (2001).

Pastorini J, Forstner MRJ, Martin RD, Melnick DJ: Areexamination of the phylogenetic position of Cal-limico (Primates) incorporating new mitochon-drial DNA sequence data. J Mol Evol 47:32–41(1998).

Pieczarka JC, Nagamachi CY, Muniz JA, Barros RM,Mattevi MS: Restriction enzyme and fluoro-chrome banding analysis of the constitutive hete-rochromatin of Saguinus species (Callitrichidae,Primates). Cytobios 105:13–26 (2001).

Porter CA, Czelusniak J, Schneider H, Schneider MP,Sampaio I, Goodman M: Sequences of the primateepsilon-globin gene: implications for systematics ofthe marmosets and other New World primates.Gene 205:59–71 (1997).

Rosenberger AL: Systematics: the higher taxa, in Coim-bra-Filho AF, Mittermeier RA (eds): Ecology andBehavior of Neotropical primates, Volume 1, pp9–27 (Academia Brasileira de Ciências, Rio deJaneiro 1981).

Rosenberger AL: Fossil New World monkeys disputethe molecular clock. J Hum Evol 13:737–742(1984).

Schneider H, Schneider MPC, Sampaio MIC, HaradaML, Stanhope M, Czelusniak J, Goodman M: Mo-lecular phylogeny of the New World monkeys (Pla-tyrrhini, Primates). Mol Phylogenet Evol 2:225–242 (1993).

Schneider H, Sampaio MIC, Harada ML, BarrosoCML, Schneider MPC, Czelusniak J, Goodman M:Molecular Phylogeny of the New World monkeys(Platyrrhini, Primates) based on two unlinked nu-clear genes: IRBP intron 1 and Â-globin sequences.Am J Phys Anthropol 100:153–179 (1996).

Schneider H, Canavez FC, Sampaio I, Moreira MA,Tagliaro CH, Seuanez HN: Can molecular dataplace each neotropical monkey in its own branch?Chromosoma 109:515–523 (2001).

Seuanez HN, Armada JLA, Freitas L, Rocha e Silva R,Pissinatti A, Coimbra-Filho AF: Intraspecific chro-mosome variation in Cebus apella (Cebidae, Pla-tyrrhini). The chromosomes of the yellow breastedcapuchin Cebus apella xanthosternos Wied, 1920.Am J Primatol 10:237–247 (1986).

Seuanez HN, Forman L, Alves G: Comparative chro-mosome morphology in three Callitrichid genera:Cebuella, Callithrix and Leontopithecus. J Hered79:418–424 (1988).

Seuanez HN, Forman L, Matayoshi T, Fanning TG:The Callimico goeldii (Primates, Platyrrhini) ge-nome: karyology and middle repetitive (LINE-1)DNA sequences. Chromosoma 98:389–395(1989).

Seuanez HN, Lima CR, Lemos B, Bonvicino CR,Moreira MAM, Canavez FC: Gene assignment inAteles paniscus chamek (Platyrrhini, Primates). Al-location of 18 markers of human syntenic groups1,2,7,14,15,17 and 22. Chromosome Res 9:631–639 (2001).

Seuanez HN, DiFiore A, Moreira MAM, AlmeidaCAS, Canavez FC: Genetic studies in Leontopithe-cus, in Kleiman DG, Rylands AB (eds): Lion Tam-arins: Biology and Conservation, pp 117–132(Smithsonian Institution Press, Washington DC2002).

Simpson GG: The principles of classification of mam-mals. Bull Amer Mus Nat Hist 85:1–350 (1945).

Stanyon R, Tofanelli S, Morescalchi MA, Agoramoor-thy G, Ryder OA, Wienberg J: Cytogenetic analysisshows extensive genomic rearrangements betweenred howler (Alouatta seniculus, Linnaeus) subspe-cies. Am J Primatol 35:171–183 (1995).

Stanyon R, Consigliere S, Müller S, Morescalchi A,Neusser M, Wienberg J: Fluorescence in situ hy-bridization (FISH) maps chromosomal homologiesbetween dusky titi and squirrel monkey. Am J Pri-matol 50:95–107 (2000).

Stanyon R, Consigliere S, Bigoni F, Ferguson-Smith M,O’Brien PC, Wienberg J: Reciprocal chromosomepainting between a new world primate, the woollymonkey, and humans. Chromosome Res 9:95–106(2001).

Stanyon R, Bonvicino CR, Svartman M, Seuanez HN:Chromosome painting in Callicebus lugens, thespecies with the lowest diploid number (2n = 16)known in primates. Chromosoma 112:201–206(2003).

Tagliaro CH, Schneider MPC, Schneider H, SampaioIC, Stanhope MJ: Marmoset phylogenetics, conser-vation perspectives, and evolution of the mtDNAcontrol region. Mol Biol Evol 14:674–684 (1997).

Torres de Caballero O, Ramirez C, Yunis E: GenusCebus: Q- and G- band karyotypes and naturalhybrids. Folia Primatol 26:310–321 (1976).

Torres OM, Enciso S, Ruiz F, Silva E, Yunis I: Chro-mosome diversity of the genus Aotus from Colom-bia. Am J Primatol 44:255–275 (1998).

van Roosmalen MGM, van Roosmalen T, MittermeierRA: Taxonomic review of the titi monkeys, genusCallicebus, Thomas, 1903, with the description oftwo new species, Callicebus bernhardi and Callice-bus stephennashi, from Brazilian Amazonia. Neo-tropical Primates 10:1–52 (2002).

Viegas-Pequignot E, Koiffmann CP, Dutrillaux B:Chromosomal phylogeny of Lagothrix, Brachytelesand Cacajao. Cytogenet Cell Genet 39:99–104(1985).

von Dornum M, Ruvolo M: Phylogenetic relationshipsof the new world monkeys (Primates, Platyrrhini)based on nuclear G6PD DNA sequences. Mol Phy-logenet Evol 11:459–476 (1999).

Yunis EJ, Torres de Caballero OM, Ramirez C, Rami-rez ZE: Chromosomal variation in the primateAlouatta seniculus seniculus. Folia Primatol 25:215–224 (1976).

Zischler H, Geisert H, von Haeseler A, Paabo S: Anuclear “fossil” of the mitochondrial D-loop andthe origin of modern humans. Nature 378:489–492(1995).

Dow

nloa

ded

by:

Uni

v. o

f Mic

higa

n, T

aubm

an M

ed.L

ib.

141.

213.

236.

110

- 9/

6/20

13 2

:06:

54 A

M