Systematics and Evolution of the Jacchus Group ofMarmosets (Platyrrhini)Gabriel Marroig,1* Susan Cropp,2 and James M. Cheverud2

1Departamento de Biologia Celular e Genetica, Instituto de Biologia, Universidade do Estado do Rio de Janeiro,Rio de Janeiro, Brazil 20550-0132Department of Anatomy and Neurobiology, Washington University School of Medicine, Saint Louis, Missouri 63110

KEY WORDS Callitrichidae; geographic variation; taxonomy; morphological evolution;speciation

ABSTRACT Interspecific differentiation and geo-graphic variation patterns in 39 skull traits of easternBrazilian marmosets are analyzed. Eastern Callithrixtaxa are distinct morphologically, and no evidence of in-tergradation among taxa is observed. Instead, there aresharp, stepped morphological boundaries among taxa,consistent with species-level distinction. The morphologi-cal similarity cluster diagram obtained from Mahalanobisdistances is different from available molecular trees, andthe general picture emerging is that the eastern Callithrixtaxa should be considered as good species arising recentlyin South American history. In particular, C. kuhlii ismorphologically distinct from other marmoset taxa, in-cluding C. geoffroyi and C. penicillata, which were previ-ously hypothesized to be the parental populations that

formed C. kuhlii by hybridization. Furthermore, C. kuhliipopulations from southeastern Bahia do not overlap mor-phologically with any C. penicillata population, includingthe upper Sao Francisco River populations that displayskin colors and pelage patterns to some extent similar totrue Kuhli’s marmosets. There is a negative, though in-significant, correlation between the morphological dis-tance matrix and a Mahalanobis distance matrix esti-mated from nine climatic variables, a pattern opposite tothat expected under a parapatric speciation model. Thisresult, together with the lack of clinal variation in skulltraits, suggests that an allopatric model of speciationmight best explain eastern marmoset diversification. AmJ Phys Anthropol 123:11–22, 2004. © 2004 Wiley-Liss, Inc.

Marmosets belong to the neotropical primate genusCallithrix. As with many other New World monkeytaxa, marmoset species are usually distinguished bytheir highly diverse color and pelage patterns (Hersh-kovitz, 1977). In fact, in his volume on callitrichidtaxonomy, Hershkovitz (1977) grouped the marmosetsinto two main species groups, based largely on bioge-ography and coat-color differences: the Argentatagroup and the Jacchus group. The two groups areseparated geographically, with the Argentata groupoccupying the area south of the Amazonas River toParaguay between the Madeira and Tocantins Rivers,and members of the Jacchus group occuring in east,northeast, and central Brazil (Fig. 1) (Hershkovitz,1977; de Vivo, 1991). Recently, Rylands et al. (2000)suggested that in order to be consistent with the sister-group relationship between Cebuella and the Argen-tata group of Callithrix, the Callithrix species groupsshould be considered as separate genera, with the Ar-gentata group marmosets belonging to the genus Micoand the Jacchus group to the genus Callithrix (strictosensu). While this designation seems sensible givencurrent information, it remains important to explicitlytest whether or not Cebuella is the sister group to allAmazonian marmosets, or else Mico will continue to bea paraphyletic genus. Here, we use the generic name

Callithrix to refer to all marmosets and not only to theJacchus group, as suggested by Rylands et al. (2000).

Marmoset species are allo-parapatrically distrib-uted, and hybrids have been reported at some contactzones (Hershkovitz, 1977; Alonso et al., 1987; Rylandset al., 1988; Mendes, 1993, 1997; Ferrari and Mendes,1991; Oliver and Santos, 1991; de Vivo, 1991; Coim-bra-Filho et al., 1993; Passamani et al., 1997). Hybridzones have been observed only in the Jacchus group(Coimbra-Filho et al., 1993) whenever a contact zone

Grant sponsor: Conselho Nacional de Pesquisas; Grant sponsor:Fundacao de Amparo a Pesquisas do Estado do Rio de Janeiro; Grantsponsor: Fundacao de Amparo a Pesquisa do Estado de Sao Paulo—Biota Sao Paulo; Grant sponsor: Fundacao Jose Bonifacio; Grantsponsor: Projeto de Conservacao e Utilizacao Sustentavel da DiversidadeBiologica; Grant sponsor: American Museum of Natural History Collec-tions Study Grant; Grant sponsor: NSF, Grant number: SBR-9632163.

*Correspondence to: Gabriel Marroig, now at the Departmento deBiologia, Instituto de Biociencias, Universidade de Sao Paulo, CaixaPostal 11.461, 05422-970 Sao Paulo, SP, Brazil.E-mail: Gmarroig@ib.usp.br

Received 7 January 2002; accepted 30 May 2002.

DOI 10.1002/ajpa.10146

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 123:11–22 (2004)

© 2004 WILEY-LISS, INC.

occurs between two pairs of parapatric species. Theexception is that no hybrid zones are reported betweenC. penicillata X C. aurita, C. geoffroyi X C. aurita, andC. geoffroyi X C. kuhlii. The existence of hybrids innature has been used to justify subspecific status in along-standing taxonomic controversy about Callithrix

lineages (Hershkovitz, 1977; de Vivo, 1991; Rylands etal., 1993; Marroig, 1995; Mendes, 1997).

The taxonomic status and group membership ofmarmoset taxa have been the subject of much de-bate. Hershkovitz (1977) subdivided the Argentatagroup into two species, each with three subspecies,

Fig. 1. Eastern Brazil, showing distribution of skull samples of six marmoset populations analyzed in this study. SF populationis of uncertain taxonomic status.

12 G. MARROIG ET AL.

and the Jacchus group into a single species with fivesubspecies. Other recent taxonomies, based on mor-phology and geographic distribution, disagree as tothe species status of most of the marmoset taxa,particularly those of the Jacchus group. Some au-thors (Coimbra-Filho and Mittermeier, 1973; Mit-termeier and Coimbra-Filho, 1981; Mittermeier etal., 1988; Natori, 1986; de Vivo, 1991; Marroig, 1995)argued that all marmoset taxa in the Jacchus groupshould be considered good species, and not subspe-cies of C. jacchus (see also Rylands et al., 2000). Inaddition, many of these studies (Mittermeier et al.,1988; Natori, 1990; Rylands et al., 2000) also recog-nized C. kuhlii as a species within the Jacchusgroup, although others regard this taxon as a hybridbetween C. geoffroyi and C. penicillata (Hershkovitz,1977) or as a junior synonym of C. penicillata (deVivo, 1991). Recent molecular studies (Tagliaro etal., 1997) indicate that an ancestral polymorphismmight be still segregating among eastern Brazilianmarmosets, or that extensive hybridization occursamong C. jacchus, C. penicillata, and C. kuhlii, be-cause multiple individual sequences from thosethree taxa mix together in the phylogenetic tree.Since field evidence does not support the hybridiza-tion hypothesis (Alonso et al., 1987; Rylands et al.,1988; Marroig and Cerqueira, unpublished find-ings), an ancestral polymorphism might suggest arecent origin for these taxa.

In this study, we make a quantitative analysis ofdifferentiation patterns in skull morphology amongthe members of the Jacchus group of marmosets. Wethen examine these morphological patterns within ageographical context in order to compare the geo-graphical differentiation patterns to expectationsderived from the South American diversificationmodels. Several hypotheses have been postulated toexplain species diversity in the neotropics, includingcenter of origin and dispersion (Hershkovitz, 1977),ecological gradients (Endler, 1977), riverine barriersto dispersal (Patton et al., 1994), river dynamics(Salo et al., 1986), geotectonic vicariance (Platnickand Nelson, 1978), refugia (ecological vicariance)(Haffer, 1993), and the Amazon lagoon (Marroig andCerqueira, 1997). These hypotheses all make ex-plicit predictions concerning the topology of phylo-genetic trees (sensu Kirkpatrick and Slatkin, 1993),geographical relationships of sister species and hy-brid zones, mode of speciation, evolutionary mecha-nisms causing diversification, and patterns of inter-and intraspecific geographic variation (reviewed inMarroig and Cerqueira, 1997). In particular, thisstudy examines the latter of these predictions. Ifmarmoset taxa are to be considered as subspecies,then smooth clines are expected to occur amongpopulations at contact zones, a geographic variationpattern that could be the result of either parapatricor allopatric speciation (Endler, 1977; Marroig andCerqueira, 1997). Alternatively, for marmosets to beconsidered as species, geographic distributions ofseparate species would be expected to show sharp

morphological boundaries between taxa (Marroigand Cerqueira, 1997).

Before considering the taxonomic consequences ofquantitative differentiation patterns in marmosets,it is necessary to define what we mean by “species”throughout this paper. We refer the reader to deQueiroz (1998) for a particularly instructive discus-sion about the general agreement among currentconcepts and criteria used to recognize species (seealso O’Hara, 1993). Historically, taxonomic debateover Callithrix species classification has been cen-tered on the orthodox “biological species concept” (ormore appropriately called “isolation species con-cept”; Templeton, 1989; de Queiroz, 1998) popular-ized by Mayr (1963). In order to remain consistentwith previous debates, our discussion will be framedusing the isolation concept. The rationale here isthat if we find morphological breaks among popula-tions and those differences are not notably associ-ated with their geographic proximity, then thesebreaks could be interpreted as evidence of the rarityof hybridization among eastern Brazil marmosets,and therefore that these taxa are good species.

MATERIALS AND METHODS

Samples and measurements

Specimens of Jacchus group marmosets were exam-ined and measurements were obtained from 391 cra-nia deposited at the following institutions: the Ameri-can Museum of Natural History (AMNH), FieldMuseum of Natural History (FMNH), Museu Nacionaldo Rio de Janeiro (MNRJ), Museu Paranaense EmılioGoeldi (MPEG), and National Museum of Natural His-tory (USNM). A complete list of measured specimenssorted by species and museum can be obtained fromthe authors on request. Only adult crania were used inthe subsequent analyses. Specimens were consideredadult when they had totally erupted and functionaldentition, as well as closed or fused spheno-occipitaland/or spheno-ethmoidal sutures. Five of the 6 recog-nized Jacchus group taxa (C. aurita, C. geoffroyi, C.kuhlii, C. jacchus, and C. penicillata) were analyzed.Only C. flaviceps was not included, because its smallsample size (N � 1) precludes statistical comparisons.

Geographical coordinates were obtained for allknown collection localities of the measured skulls.The following nine climatic variables were obtainedfor each locality, using the program LABVERTCLI(see also Cerqueira et al., 1998) to be releasedsoon (see http://www.biologia.ufrj.br/labs/labvert):annual maximum (MAXT), minimum (MINT), andmean temperatures (MEAT); absolute maximum(ABMAX) and minimum (ABMIN) temperatures;annual total precipitation (PRE); annual nebulosity(NEB); annual relative humidity (RH); and annualaverage of rainy days (RAID). The program is adigitized version of the climatic Atlas of Brazil (Bra-sil, 1969), and the general methods of climatic data-gathering are described in Cerqueira et al. (1998).

SYSTEMATICS AND EVOLUTION OF MARMOSETS 13

Three-dimensional coordinates were recorded for36 landmarks (Table 1, Fig. 2), using a Polhemus3Draw digitizer. The general procedure for measur-ing specimens followed that of Cheverud (1995). Aset of 70 linear measurements describing cranialmorphology was calculated from the coordinate val-ues. This set was reduced to 39 measurements byaveraging the measurements present on both sidesof the skull (Table 2). Whenever one of the skullsides was damaged, preventing us from taking anyparticular measurement, the undamaged side wasused as the average. All results are presented inmillimeters. These 39 measurements are classifiedin functional/developmental groups following Chev-erud (1995; see Table 2).

A total of 339 skulls with all 39 measurements(without missing values) was used in the multivar-iate analyses below. Generally, little or no sexualdimorphism in cranial traits of marmosets wasfound in previous studies (Hershkovitz, 1977; deVivo, 1991). In this study, we tested for differencesbetween taxa, sexes, and an interaction betweensexes and taxa using multivariate analysis of vari-ance (MANOVA).

Analyses: interspecific differentiation

Differences among marmoset skulls were exam-ined through linear discriminant function analysis(DFA). Mahalanobis D2 morphological distances be-tween group centroids were also computed from thediscriminant function analysis in order to estimate

the degree of differentiation among taxa. A pheno-gram based on a cluster analysis of the morpholog-ical distances between taxa was generated using theaverage linkage method (UPGMA), as recommendedby Sneath and Sokal (1973). The cophenetic correla-tion between the distance tree and the D2 valuesused to produce it was calculated in order to mea-sure how well the tree represents the data. Therelative magnitude of morphological distance amongtaxa was considered a measure of their morpholog-ical distinctiveness (Klecka, 1980), and therefore thephenogram displays the pattern of morphologicalsimilarity among marmoset skulls. This cluster di-agram should not be considered to reflect phyloge-netic history, but instead to serve as a graphicalrepresentation of similarities in skull morphology.

One-way analysis of variance (ANOVA) was usedto explore differences between marmosets. Tukey’spost hoc tests were used to compare the 39 traitsamong species, and significance tests were adjustedfor multiple comparisons using the Bonferroni cor-rection (Rice, 1989).

De Vivo (1991) suggests that skin-color variants inthe marmoset populations of the upper Sao Fran-cisco River drainage in the center of Minas GeraisState (see Fig. 1) are more similar to southeasternBahia State populations, usually considered as C.kuhlii, than they are to populations from the rest ofthe C. penicillata distribution. A second discrimi-nant function analysis was performed using only theC. penicillata (N � 68) and C. kuhlii (N � 148)specimens collected from known localities, alongwith the upper Sao Francisco River drainage popu-

TABLE 1. Landmarks recorded in neotropical primate skulls,using three-dimensional digitizer1

Landmark Description Position(s)

IS Intradentale superior, A MidlinePM Premaxillary suture at

alveolus, ARight, left

NSL Nasale, A MidlineNA Nasion, A MidlineBR Bregma, AP MidlinePT Pterion, AP Right, leftFM Fronto-malare, A Right, leftZS Zygomaxillare superior, A Right, leftZI Zygomaxillare inferior, A Right, leftMT Maxillary tuberosity, A Right, leftPNS Posterior nasal spine, A MidlineAPET Anterior petrous temporal, A Right, leftBA Basion, AP MidlineOPI Opisthion, AP MidlineEAM Anterior external auditory

meatus, ARight, left

PEAM Posterior external auditorymeatus, A

Right, left

ZYGO Inferior zygo-temporalsuture, A

Right, left

TSP Temporo-spheno-parietaljunction, A

Right, left

TS Temporo-sphenoidal junctionat the petrous, AP

Right, left

JP Jugular process, AP Right, leftLD Lambda, P MidlineAS Asterion, P Right, left

1 Designation A (anterior) or P (posterior) after landmark nameindicates in which position(s) landmark was recorded. Land-marks are also identified in Figure 2.

Fig. 2. The 36 craniofacial landmarks recorded from marmo-set skulls, using a three-dimensional digitizer. Refer to Table 1for a description of landmarks.

14 G. MARROIG ET AL.

lations as a separate group provisionally referred toas SF (N � 15). This analysis tests whether speci-mens from the upper Sao Francisco River localities(SF) should be grouped with C. kuhlii or C. penicil-lata. Geographical variation among C. penicillataand C. kuhlii populations was examined by plottingDFA scores against the latitude and longitude ofcollecting localities.

A discriminant function analysis with species asgrouping variable was performed on climatic data toestimate a Mahalanobis (D2) climatic distance ma-trix. This climatic distance matrix was correlatedwith the morphological distance matrix in order totest one prediction of the parapatric model of spe-ciation. Under a parapatric model of speciation, weexpect larger morphological and genetic differentia-tion among habitats than within habitats (Endler,1977). While the climatic variables used here do notcompletely define the species habitats, they are tosome extent a continuous function related to habitatdifferentiation. Therefore, we expect a positive and

significant correlation of climatic and morphologicaldistances under a parapatric model of speciation.

RESULTS

A MANOVA was performed on the 39 measure-ments using sex, taxon, and sex by taxon interactionas independent variables in order to determinewhether sexual dimorphism needs to be accountedfor in the analyses. Two hundred fifty-three individ-uals were analyzed, since 138 specimens were eitherof unknown sex or had missing values. No signifi-cant multivariate (Wilk’s � � 0.840, df � 39, 205,P � 0.472) or univariate (all P � 0.05) differencesbetween sexes were found. In addition, there was nosignificant multivariate sex by taxon interaction(Wilk’s � � 0.479, df � 156, 819, P � 0.294). Twosignificant univariate sex by taxon interactions werefound for PT-TSP (P � 0.022) and FM-ZS (P �0.015); all other univariate tests were nonsignificant(all P � 0.12). These two significant results mostlikely represent a type I error, given the lack ofmultivariate significance and their failure to reachBonferroni levels of significance (P � 0.05/39). Incontrast to the results for sex, there were highlysignificant multivariate differences among taxa(Wilk’s � � 0.012, df � 156, 819, P � 1.0 � 10�6).Statistically significant univariate differencesamong taxa were observed in 33 of the 39 measure-ments, using the conservative sequential Bonferronilevels of significance (Rice, 1989). Given that nosignificant multivariate sex differences or sex bytaxon interactions were found, all future analyseswere performed without regard to sex.

Table 3 presents the basic statistics with the sexespooled for the five marmoset taxa. Overall, discrimi-nant function analysis performed on the 339 com-plete skulls using the five taxa described above asgroups was highly significant (Wilk’s � � 0.016, df �156, 1178, P � 0.0001). All four individual discrimi-nant functions (DF1–4) were also highly significant(P � 0.0001), indicating that all possible contrastsamong taxa are statistically significant. Correla-tions between DF scores and skull measurementsare presented in Table 4. Based on the correlationsbetween variables and functions, DF1 is a size factorbecause all significant correlations are positive, ex-cept for NA-BRs. DF1 has large contributions fromboth neurocranial and facial traits. DF2 also hascontributions from neurocranial and facial traits,but the significant neurocranial traits are restrictedto those involving pterion (PT) and bregma (BR).Nearly all significant correlations with DF2 are neg-ative, except for OPI-LD and PT-FM. DF3 contraststwo facial traits (IS-NSL and EAM-ZYGO) againstthree neurocranial (PT-TSP, LD-AS, and OPI-LD)and one facial trait (ZI-ZYGO). DF4 contrastsOPI-LD against ZI-TSP, APET-BA, and ZYGO-TSP.

Post hoc classification of cases with groups fromthe DFA is presented in Table 5. Ninety-six percentof the total cases were classified correctly with re-gard to membership in the five taxa according to the

TABLE 2. Thirty-nine linear skull measurements(distances between landmarks) and membership in the six

functional/developmental groups and two major cranial regions1

MeasurementFunctional/

developmental group(s) Region

IS-PM Oral FaceIS-NSL Nasal FaceIS-PNS Oral, asal FacePM-ZS Oral FacePM-ZI Oral FacePM-MT Oral FaceNSL-NA Nasal FaceNSL-ZS Nasal FaceNSL-ZI Oral, nasal FaceNA-BR Cranial vault NeurocraniumNA-FM Orbit NeurocraniumNA-PNS Nasal FaceBR-PT Cranial vault NeurocraniumBR-APET Cranial vault NeurocraniumPT-FM Orbit NeurocraniumPT-APET Cranial vault NeurocraniumPT-BA Cranial vault NeurocraniumPT-EAM Cranial vault NeurocraniumPT-ZYGO Zygomatic FacePT-TSP Cranial vault,

zygomaticNeurocranium,

faceFM-ZS Orbit NeurocraniumFM-MT Zygomatic FaceZS-ZI Oral FaceZI-MT Oral FaceZI-ZYGO Zygomatic FaceZI-TSP Zygomatic FaceMT-PNS Oral FacePNS-APET Cranial base NeurocraniumAPET-BA Cranial base NeurocraniumAPET-TS Cranial base NeurocraniumBA-EAM Cranial base NeurocraniumEAM-ZYGO Zygomatic FaceZYGO-TSP Zygomatic FaceLD-AS Cranial vault NeurocraniumBR-LD Cranial vault NeurocraniumOPI-LD Cranial vault NeurocraniumPT-AS Cranial vault NeurocraniumJP-AS Cranial base NeurocraniumBA-OPI Cranial base Neurocranium

1 Table 1 defines each landmark, and Figure 2 shows their loca-tions in a generalized Platyrrhine skull.

SYSTEMATICS AND EVOLUTION OF MARMOSETS 15

discriminant functions, while the same figure was92% for the jackknifed classification matrix (Table5). Original and jackknifed classification matricesdisplay the same pattern, except that larger propor-tions of individuals are misclassified in the latter.Therefore, only the jackknifed results are reported.

The morphological distance matrix is given in Ta-ble 6, and the cluster diagram based on the averagelinkage method is presented in Figure 3. The cophe-netic correlation between the tree distance and theD2 values used to produce it is 0.70, a statisticallysignificant result indicating that about 50% of theinformation in the distances is represented in thephenogram (P � 0.016). Morphological distancesamong marmosets are large, ranging from D2 �16.53 between C. penicillata and C. geoffroyi to D2 �52.00 between C. aurita and C. jacchus. Interest-ingly, C. penicillata and C. geoffroyi are morpholog-ically more similar to each other than either taxon isto C. kuhlii. Overall, marmoset taxa are morpholog-ically distinct at a level usually found among taxaaccepted as good taxonomic species. For example, C.argentata and C. humeralifera show a Mahalanobisdistance of 23.00 among them using the same 39trait data set used here. (See also, Moore and Chev-erud, 1992; Ackermann and Cheverud, 2000, 2002.)

Table 7 presents the results of analyses of vari-ance (ANOVAs) and Tukey multiple comparison

tests for the 37 traits that present at least one sig-nificant contrast. Overall, these results confirm thediscriminant function analysis and show that thereare significant contrasts between all pairs of species.

Latitude and longitude are significantly corre-lated with the discriminant functions scores (Table8). One interesting pattern is the positive correla-tion between latitude and DF1 (size), which mightsuggest that larger animals live at southern, colderlatitudes, while smaller marmosets occur in north-ern, hotter areas. However, there is no positive sig-nificant correlation between latitude and DF1 scoreswithin each species (data not shown), and the corre-lation is negative for C. geoffroyi and C. kuhlii.

The separate discriminant function analysis of theC. kuhlii, C. penicillata, and SF populations washighly significant (Wilk’s � � 0.124, df � 78, 382,P � 0.0001), with both discriminant functions beingsignificant. A post hoc classification of cases withgroups using the DFA scores results in 96% of thecases being correctly classified, while the same fig-ure was 90% for the jackknifed classification matrix.However, only 53% of the SF cases were correctlyclassified in the jackknifed matrix. Forty percent ofthe SF cases were misclassified as C. penicillata,and only 7% misclassified with C. kuhlii. This resultindicates that the upper Sao Francisco River popu-lations are not morphometrically distinct from the

TABLE 3. Basic statistics for each species1

Traits

C. aurita C. geoffroyi C. jacchus C. kuhlii C. penicillata

N Mean Std. C.V. N Mean Std. C.V. N Mean Std. C.V. N Mean Std. C.V. N Mean Std. C.V.

ISPM 17 4.66 0.097 0.09 56 4.72 0.045 0.07 44 4.69 0.047 0.07 171 4.88 0.033 0.09 101 4.85 0.070 0.15ISNSL 17 8.26 0.155 0.08 54 8.76 0.092 0.08 42 7.68 0.121 0.10 148 8.95 0.061 0.08 96 8.51 0.085 0.10ISPNS 17 16.49 0.212 0.05 55 16.80 0.095 0.04 44 15.43 0.124 0.05 171 16.22 0.069 0.06 99 16.00 0.120 0.07PMZS 16 9.07 0.164 0.07 56 9.10 0.069 0.06 44 8.04 0.074 0.06 172 8.64 0.041 0.06 101 8.75 0.072 0.08PMZI 16 13.22 0.169 0.05 56 13.82 0.090 0.05 44 12.48 0.090 0.05 172 13.67 0.045 0.04 100 13.11 0.087 0.07PMMT 17 12.39 0.136 0.05 56 12.84 0.068 0.04 44 12.01 0.102 0.06 172 12.85 0.041 0.04 101 12.03 0.066 0.06NSLNA 17 6.96 0.168 0.10 54 6.91 0.083 0.09 42 6.15 0.067 0.07 149 6.54 0.060 0.11 97 6.23 0.071 0.11NSLZS 16 11.39 0.132 0.05 54 11.27 0.085 0.06 42 10.35 0.080 0.05 149 11.00 0.056 0.06 97 11.04 0.088 0.08NSLZI 16 18.49 0.144 0.03 54 18.84 0.101 0.04 42 17.26 0.106 0.04 149 18.80 0.057 0.04 96 18.18 0.115 0.06NABR 17 24.46 0.198 0.03 56 25.06 0.140 0.04 44 25.37 0.335 0.09 172 24.45 0.106 0.06 101 24.90 0.171 0.07NAFM 16 13.20 0.123 0.04 56 12.98 0.075 0.04 44 12.38 0.077 0.04 172 13.01 0.048 0.05 102 12.77 0.082 0.07NAPNS 17 16.00 0.201 0.05 55 15.64 0.099 0.05 44 14.20 0.109 0.05 172 15.64 0.053 0.04 100 15.10 0.100 0.07BRPT 17 18.31 0.177 0.04 56 18.84 0.115 0.05 44 17.88 0.221 0.08 172 17.63 0.076 0.06 101 18.10 0.131 0.07BRAPET 17 20.99 0.188 0.04 56 20.70 0.087 0.03 44 19.42 0.109 0.04 172 20.23 0.062 0.04 101 19.74 0.117 0.06PTFM 16 7.19 0.125 0.07 56 7.36 0.087 0.09 44 7.74 0.086 0.07 172 7.84 0.057 0.09 101 7.60 0.088 0.12PTAPET 17 14.80 0.218 0.06 56 14.57 0.087 0.04 44 13.46 0.093 0.05 172 14.40 0.050 0.05 101 14.19 0.082 0.06PTBA 16 23.94 0.193 0.03 55 24.03 0.134 0.04 44 22.27 0.098 0.03 172 23.21 0.061 0.03 98 22.90 0.093 0.04PTEAM 17 15.23 0.185 0.05 56 15.41 0.125 0.06 44 14.14 0.087 0.04 172 14.94 0.058 0.05 101 14.71 0.079 0.05PTZYGO 15 12.60 0.220 0.07 55 12.37 0.134 0.08 44 11.71 0.106 0.06 172 12.35 0.062 0.07 92 11.57 0.101 0.08PTTSP 17 7.42 0.202 0.11 56 6.75 0.101 0.11 44 6.31 0.083 0.09 172 6.90 0.060 0.11 101 6.22 0.079 0.13FMZS 16 7.74 0.173 0.09 56 8.06 0.065 0.06 44 8.02 0.071 0.06 172 8.45 0.045 0.07 101 7.61 0.068 0.09FMMT 16 14.71 0.147 0.04 56 14.95 0.078 0.04 44 14.45 0.076 0.03 172 15.18 0.046 0.04 101 14.59 0.089 0.06ZSZI 16 8.40 0.149 0.07 56 8.80 0.075 0.06 44 8.05 0.109 0.09 172 8.83 0.039 0.06 100 8.33 0.078 0.09ZIMT 16 6.32 0.090 0.06 56 6.30 0.077 0.09 44 6.16 0.050 0.05 172 6.36 0.038 0.08 100 6.40 0.069 0.11ZIZYGO 15 8.75 0.160 0.07 55 9.07 0.131 0.11 44 9.40 0.115 0.08 172 9.06 0.068 0.10 93 8.58 0.105 0.12ZITSP 16 8.90 0.187 0.08 56 9.39 0.076 0.06 44 9.07 0.069 0.05 172 9.42 0.050 0.07 100 9.03 0.082 0.09MTPNS 17 6.64 0.129 0.08 55 6.54 0.050 0.06 44 5.65 0.047 0.06 172 6.02 0.025 0.05 100 6.09 0.048 0.08PNSAPET 17 6.96 0.161 0.10 55 7.40 0.066 0.07 44 7.15 0.095 0.09 172 7.95 0.049 0.08 100 7.22 0.062 0.09APETBA 16 11.30 0.182 0.06 55 11.59 0.087 0.06 44 11.28 0.071 0.04 172 11.05 0.043 0.05 99 11.06 0.076 0.07APETTS 17 7.11 0.122 0.07 56 6.80 0.049 0.05 44 6.91 0.072 0.07 172 6.66 0.037 0.07 102 6.86 0.078 0.12BAEAM 16 13.43 0.159 0.05 55 13.59 0.065 0.04 44 12.72 0.072 0.04 172 13.39 0.035 0.03 99 12.91 0.076 0.06EAMZYGO 15 8.03 0.156 0.08 55 7.66 0.143 0.14 44 7.05 0.137 0.13 172 7.72 0.063 0.11 93 7.95 0.092 0.11ZYGOTSP 15 6.87 0.142 0.08 55 7.22 0.084 0.09 44 7.05 0.072 0.07 172 6.81 0.039 0.08 93 6.91 0.064 0.09LDAS 16 12.52 0.199 0.06 56 11.40 0.095 0.06 44 11.27 0.132 0.08 172 10.98 0.067 0.08 102 11.06 0.125 0.11BRLD 17 23.08 0.305 0.05 56 22.15 0.152 0.05 44 17.92 0.422 0.16 172 21.72 0.117 0.07 101 20.25 0.151 0.08OPILD 15 13.06 0.497 0.15 56 10.99 0.108 0.07 44 12.85 0.238 0.12 172 11.85 0.076 0.08 98 11.33 0.113 0.10PTAS 16 23.81 0.151 0.03 56 24.40 0.145 0.04 44 22.14 0.102 0.03 172 23.59 0.067 0.04 101 22.79 0.101 0.04JPAS 16 11.69 0.179 0.06 56 11.89 0.064 0.04 44 11.05 0.081 0.05 172 12.40 0.047 0.05 102 11.70 0.081 0.07BAOPI 15 6.63 0.110 0.06 55 6.54 0.074 0.08 44 6.03 0.076 0.08 172 6.30 0.031 0.06 97 6.25 0.052 0.08

1 N, sample size; Std., standard error; C.V., coefficient of variation. All measurements are in millimeters.

16 G. MARROIG ET AL.

remaining populations of C. penicillata. This resultis confirmed by the inspection of latitude/longitudeplots of DF scores (Fig. 4) where C. kuhlii separatesclearly from the C. penicillata and SF populations,while these latter two groups are indistinct.

Table 6 also presents the D2 distance matrix ob-tained from the discriminant analysis upon the nineclimatic variables. Climactic variation among taxawas highly significant (Wilk’s � � 0.005, df � 36,1,347, P � 1.0 � 10�6), with each discriminant func-tion being highly significant (at least P � 0.0001).There is a negative (r � �0.147), statistically insig-nificant (P � 0.47) correlation between climatic andmorphological distances, indicating that there is notrend of morphological differentiation being higheramong habitats that within habitats.

DISCUSSION

Our results suggest that taxa within the C. jac-chus group should be classified as separate speciesrather than subspecies. DFA correctly classified

specimens into taxa, indicating that on the basis ofskull morphology, these are distinct species. Simp-son (1962) pointed that an empirical finding by tax-onomists is that different subspecies usually presentno more that a 75% nonoverlap in a continuous traitdistribution. We are able to discriminate much morepowerfully than 75% in all comparisons, exceptwhen comparing SF with C. penicillata (see below),indicating that these comparisons are among goodspecies. Significant contrasts between any possiblepairwise combinations of species are observed in theANOVA results, also supporting specific status.Morphological distances among marmosets are sim-ilar to or higher than distances found among otherrelated taxa usually accepted as good species, likethe tamarins (Moore and Cheverud, 1992; Acker-mann and Cheverud, 2000, 2002) or Amazonianmarmosets. The geographical variation analysisbased on the plot of latitude and longitude againstDFA scores reinforces this conclusion. There is noevidence for intergradation along contact zones, asmight be expected among subspecies that still sharethe ability to exchange genes at a significant level (seeMarroig and Cerqueira, unpublished results). Instead,there is a sharp, steep morphological boundary be-tween taxa, with no trend of species being more mor-phologically similar at contact zones than at otherparts of their ranges, consistent with species level dis-tinction. A species level distinction is also consistentwith the qualitative intra- and interespecific analysesby de Vivo (1991) of skull and skin traits, interspecificquantitative analyses of skull morphology (Natori,1986, 1994), and dentition (Natori and Shigehara,1992). Therefore, we suggest that marmoset taxawithin the Jacchus group should be regard as goodtaxonomic species.

C. jacchus and C. penicillata both share an overallsmaller cranial vault in comparison with the re-maining species, and conversely C. aurita have anoverall larger vault, even when compared to C. geof-froyi. C. aurita is more similar to C. geoffroyi than toany of the remaining taxa (Table 7), with a fewdifferences in the neurocranial region and on theoral functional group. While C. aurita have a largevault, conversely C. geoffroyi present a larger buccalapparatus, a feature shared with but less pro-nounced in C. kuhlii. C. kuhlii show an enlargedorbit, with the landmark FM being repositioned to ahigher position in the outer rim of the orbit. Also, C.kuhlii show an enlarged cranial base when com-pared to the other species, resulting from a posteriorrepositioning of the landmark APET, a repositioningshared with C. jacchus and C. penicillata. C. jacchusis the smallest of the marmoset species in the Jac-chus group, showing 15 unique contrasts that differ-entiate it from all other species. Seven of these con-trasts are in the neurocranium (5 in the vault) and 8in the face. The cranial vault, oral, and nasal devel-opmental/functional groups are the most affected bythe reduction in C. jacchus size, with 45.5% of allvault traits, 55.6% of the total number of oral traits,

TABLE 4. Correlations (r) of 39 skull traits with fourdiscriminant functions (df1–df4)1

Trait DF1 DF2 DF3 DF4

ISPM 0.16 0.09 0.08 0.03ISNSL 0.48*** �0.13 0.30*** 0.07ISPNS 0.26*** �0.34*** 0.02 0.15PMZS 0.15 �0.48*** 0.18 0.02PMZI 0.55*** �0.29*** 0.12 0.17PMMT 0.60*** �0.13 �0.18 0.24**NSLNA 0.23** �0.31*** �0.19 0.11NSLZS 0.18 �0.37*** 0.11 �0.08NSLZI 0.55*** �0.31*** 0.13 0.05NABR �0.25*** 0.00 �0.04 0.14NAFM 0.33*** �0.20* 0.01 �0.11NAPNS 0.54*** �0.34*** 0.08 �0.12BRPT �0.17 �0.32*** �0.06 0.21*BRAPET 0.27*** �0.41*** �0.12 �0.06PTFM 0.13 0.28*** 0.09 �0.03PTAPET 0.36*** �0.36*** 0.08 �0.10PTBA 0.28*** �0.51*** �0.04 0.12PTEAM 0.26*** �0.41*** 0.04 0.05PTZYGO 0.35*** �0.16 �0.23** 0.05PTTSP 0.34*** �0.13 �0.26*** �0.19FMZS 0.51*** 0.19* �0.22** 0.21*FMMT 0.51*** �0.01 �0.04 0.08ZSZI 0.46*** �0.14 0.05 0.15ZIMT 0.12 �0.02 0.08 �0.07ZIZYGO 0.06 0.12 �0.28*** 0.25***ZITSP 0.30*** 0.00 �0.04 0.27***MTPNS 0.14 �0.66*** 0.01 0.02PNSAPET 0.57*** 0.16 0.00 0.08APETBA �0.14 �0.26*** �0.14 0.27***APETTS �0.15 �0.05 �0.17 0.00BAEAM 0.47*** �0.29*** �0.18 0.18EAMZYGO 0.11 �0.17 0.25*** �0.23**ZYGOTSP �0.13 �0.16 �0.09 0.30***LDAS �0.09 �0.24** �0.39*** �0.15BRLD 0.59*** �0.46*** 0.04 �0.13OPILD �0.09 0.28*** �0.48*** �0.33***PTAS 0.46*** �0.49*** �0.07 0.20*JPAS 0.63*** �0.04 0.22** �0.02BAOPI 0.16 �0.32*** �0.06 �0.03

1 Bonferroni-corrected probabilities (P) are indicated.* P � 0.05.** P � 0.01.*** P � 0.001.

SYSTEMATICS AND EVOLUTION OF MARMOSETS 17

and 66.5% of the nasal traits being significantlysmaller than in any of the other species. Besides asmaller cranial height (BR-APET), C. jacchus and C.penicillata also share an overall reduction in severaloral and zygomatic traits (ZS-ZI, FM-MT, PT-ZYGO,PT-TSP, and PM-MT) that might reflect their higherdependence on gum relative to other marmosets.

The topology of the morphological similarity dia-gram (Fig. 3) contrasts with the phylogenetic treesof marmosets based on mtDNA sequences, d-loop(Tagliaro et al., 1997), cytochrome b (Mundy et al.,2000), and ND1 (Tagliaro et al., 2000). There is ageneral agreement among these three data sets,with ND1 lacking resolution to disentangle specieswithin the geoffroyi-kuhlii-penicillata-jacchus clade.Given the general agreement among data sets, Ta-gliaro et al. (1997) will be used here as a referencebecause they include a larger number of taxa andmore individuals per taxon. The DNA tree indicatesthat C. aurita was the earliest offshoot of the Jac-chus group (with high support from the bootstrap

test), which agrees with the outlier position of C.aurita in the dendrogram reflecting its great mor-phological distinctiveness. C. geoffroyi is the nextbranch in the DNA tree, and appears as clearlymonophyletic (bootstrap value of 99 in the neighbor-joining tree), followed by a closely related group oftaxa (C. kuhlii, C. jacchus, and C. penicillata) in anunresolved polytomy (low bootstrap values), with C.kuhlii and C. penicillata being paraphyletic (see Fig.3 in Tagliaro et al., 1997). The comparison of this DNAderived phylogenetic pattern with our morphologicalsimilarity diagram indicates that morphological diver-sification among Jacchus group marmosets might beto some extent uncoupled from cladogenesis.

Hershkovitz (1977) hypothesized that the south-eastern Bahia populations named C. kuhlii are hy-brids among C. penicillata and C. geoffroyi at theircontact zone. Our morphological analysis contra-dicts this hypothesis and supports C. kuhlii as avalid species. Furthermore, the molecular tree (Ta-gliaro et al., 1997) indicates that C. kuhlii is phylo-genetically closer to the C. jacchus-C. penicillataclade than to C. geoffroyi, which also contradicts thehybrid origin hypothesis of Hershkovitz (1977) for C.kuhlii. Interestingly, C. geoffroyi is more similar inskull morphology to C. penicillata than either is toC. kuhlii. Under a strictly additive inheritancemodel, we would expect that if C. kuhlii had a hybridorigin, it should present morphology somewhat in-termediate between C. penicillata and C. geoffroyi.While the fact that C. kuhlii is not intermediatebetween purported parental species is not diagnostic ofit not being a hybrid, their distinct morphology fromall other eastern Brazil marmosets is meaningful.

Contrary to the hybrid origin hypothesis of Hersh-kovitz (1977) for C. kuhlii, de Vivo (1991) suggeststhat the southeastern Bahia populations (C. kuhlii)are within the range of variation observed for C.penicillata populations. In particular, he arguesthat coat color and pelage variants observed in theC. kuhlii populations are similar to the variants

TABLE 5. Post hoc jackknifed classification matrix of cases according to discriminant functions1

C. aurita C. geoffroyi C. jacchus C. kuhlii C. penicillata % correct

C. aurita 12 1 0 0 1 86C. geoffroyi 1 47 0 3 0 92C. jacchus 0 0 39 0 3 93C. kuhlii 0 1 2 142 3 96C. penicillata 0 6 4 3 71 85Total 13 55 45 148 78 92

1 Percentages of cases correctly assigned to species according to DFs are shown in last column.

TABLE 6. Mahalanobis (D2) morpholgical distances among species are presented below diagonal,and D2 climatic distances above diagonal

C. aurita C. geoffroyi C. jacchus C. kuhlii C. penicillata

C. aurita 0.0 25.44 33.73 57.65 9.11C. geoffroyi 22.08 0.0 14.38 50.22 24.05C. jacchus 52.00 38.15 0.0 63.44 22.08C. kuhlii 40.05 19.35 31.11 0.0 81.98C. penicillata 34.80 16.53 18.24 18.03 0.0

Fig. 3. Morphological relationships among marmoset speciesderived from a UPGMA analysis of Mahalanobis D2 values.

18 G. MARROIG ET AL.

observed in the upper Sao Francisco River C. peni-cillata populations, and therefore that C. kuhliishould be considered synonymous with C. penicil-lata. The analysis of C. kuhlii and C. penicillatapopulations clearly show that true C. kuhlii popula-tions from southeastern Bahia are quite distinctfrom C. penicillata populations. Furthermore, upperSao Francisco River populations of uncertain taxo-nomic status are also distinct from southeasternBahia populations and, conversely, are indistinctfrom other C. penicillata populations. This resultsuggests that the name C. kuhlii should be used todesignate only the marmoset populations of south-

eastern Bahia, and that upper Sao Francisco Riverpopulations should be designated as C. penicillata.

The lack of clinal geographic variation among taxasupports the view that marmosets are good speciesrather than subspecies, and indicates that a para-patric speciation model does not fit the diversifica-tion of the Jacchus group Callithrix species. Thelack of association between climatic and morpholog-ical distances reinforces this conclusion, indicatingthat one major prediction of the parapatric specia-tion model (Endler, 1977) does not hold for easternmarmosets. While there is a general trend acrossspecies of increased size at more southerly latitudes,with C. geoffroyi, C. aurita, and C. kuhlii beinglarger than C. penicillata and C. jacchus (see Table3 and Fig. 5), this trend is not found within species.The data at hand do not allow us to distinguishbetween geological and ecological vicariance models(Marroig and Cerqueira, 1997). While Tagliaro et al.(1997) do not discuss the time framework of marmo-set diversification, the observed paraphyly in sev-eral purported species, coupled with short branchesamong taxa, suggests that marmoset taxa are recentneotropical species, and that ancestral polymor-phisms may still be segregating in extant species.

TABLE 7. Tukey test results for 37 significant ANOVAs1

C. aurita C. geoffroyi C. jacchus C. kuhlii C. penicillata

IS-NSL AB AC B C AIS-PNS AC A B C CPM-ZS AC A B C CPM-ZI AD B C AB DPM-MT A B A B ANSL-NA AC A B C BNSL-ZS A A B A ANSL-ZI AC A B A CNA-BR AB AB A B ABNA-FM AC AC B C ANA-PNS A A B A CBR-PT ABC B AC A CBR-APET A A B C BPT-FM A A AB B ABPT-APET A A B AC CPT-BA A A B C DPT-EAM AC A B C CPT-ZYGO A A B A BPT-TSP A B C AB CFM-ZS AC A A B CFM-MT ABC AC B C BZS-ZI ABC AC B C BZI-ZYGO A A A A BZI-TSP AC AB AC B CMT-PNS A A B C CPNS-APET A A A B AAPET-BA AB B AB A AAPET-TS A AB AB B ABBA-EAM A A B A BEAM-ZYGO A A B A AZYGO-TSP AB A AB B BLD-AS A B BC C BCBR-LD A AD B D COPI-LD A B A C BPT-AS AC A B C DJP-AS A A B C ABA-OPI AC A B CD BD

1 Same letters denote nonsignificant contrasts, and conversely, different letters denote significant differences among groups. Forexample, for IS-NSL, C. aurita (AB) is not significantly different from any taxon listing either an A or a B. It is only significantlydifferent from C. kuhlii (C).

TABLE 8. Correlation of latitude and longitude withdiscriminant functions1

Latitude Longitude

DF1 0.283*** �0.460***DF2 �0.739*** �0.277***DF3 0.333*** 0.449***DF4 �0.004 �0.186*

1 Bonferroni-corrected probabilities (P) are indicated.* P � 0.05.** P � 0.01.*** P � 0.001.

SYSTEMATICS AND EVOLUTION OF MARMOSETS 19

However, genetic distances (Tagliaro et al., 1997)among species within the Jacchus group indicatethat their diversification may have occurred duringthe last 1.0 or 1.5 million years. Barroso et al. (1997)estimated the divergence date between C. jacchusand C. geoffroyi at 0.5 Myr, indicating a very recentcommon ancestry. Eastern Brazil has a quite stablerecent geological history, with no major uplifting ortilting occurring at least since the Pliocene. Con-versely, South America has a quite dynamic climatichistory, especially during the Pliocene-Pleistocene,but also extending far back to Tertiary times (Haf-fer, 1993; Marroig and Cerqueira, 1997). This sug-gests that an ecologically driven allopatric specia-tion model seems more probable than a geologicalone for diversification during the time frame consid-ered. Climatic cycles triggered by Milankovitch cy-cles, with cold, dry, low-sea-level periods alternatingwith hot, humid, high-sea-level periods (Marroigand Cerqueira, 1997), could be responsible for therecent diversification of the Jacchus group marmo-sets. Below, some expectations that should hold ifthis latter hypothesis is true are presented. Theseexpectations can be tested with further data, andare presented here as a perspective on the subjectthat hopefully might stimulate future work.

Marroig and Cerqueira (1997) advanced a newhypothesis, which could help to explain diversifica-tion in the neotropics. This hypothesis states thatsea-level rise and fall associated with Milankovitchcycles, at least during the last 2.5 million years,produce recurrent events of appearance and disap-pearance of a large body of water (the AmazonasLagoon) covering the Amazon basin. Also, and morerelevant to the evolution of the Jacchus group, isthat those sea-level risings inundate the SouthAmerican Atlantic coast (Marroig and Cerqueira,1997). The Amazonas Lagoon intrusions would haveseveral consequences for speciation and extinctionprocesses in South America, yielding specific predic-tions about evolutionary patterns. Some predictionsof the Amazonas Lagoon are: 1) divergence timesamong South America congeneric species wouldhave values ranging from 2.5 my BP to the present;2) differentiation between Amazonian lowlands andAtlantic forest would have occurred from 2.5 Myr to750,000 years ago; 3) South American taxa couldshow phylogenetic tree shapes topologically moresymmetric than asymmetric, with independentnodes in the tree appearing around the same timeand having nearly identical derived branch lengths,both features being a consequence of synchronous

Fig. 4. Plot of latitude and longitude against first discriminant function scores for C. penicillata and C. kuhlii specimens.

20 G. MARROIG ET AL.

speciation; 4) speciation is predominantly allopatric;5) species distributed in Amazonas would presentphylogeographic patterns suggesting a centripetalinvasion of lowlands from the neighboring high-lands; 6) rivers may act as range delimiters, butsister species would not necessarily occupy contigu-ous ranges; and 7) a corollary of prediction 6 is thatwe might expect that when partial breakdown ofisolating mechanisms occurs among taxa on oppo-site river margins, the resulting hybridization canoccur either between sister taxa (species or subspe-cies) or among more basal taxa (see Marroig andCerqueira (1997) for a revision of South Americadiversification models and how to test for these al-ternative models). Therefore, future tests of our hy-pothesis that speciation in eastern marmosets oc-curred through an ecologically driven vicariancemodel should examine the patterns described above.

ACKNOWLEDGMENTS

We thank those people and institutions who pro-vided generous help and access to marmoset skeletalmaterial: R. Voss and R. MacPhee (American Mu-seum of Natural History); the staff at the BritishMuseum of Natural History; B. Paterson, B. Stan-ley, and L. Heaney (Field Museum of Natural His-tory); L. Salles, J. Oliveira, F. Barbosa, and S.

Franco (Museu Nacional do Rio de Janeiro); S. Costaand J. de Queiroz (Museu Paraense Emılio Goeldi);and R. Thorington and R. Chapman (National Mu-seum of Natural History, Washington, DC).

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