Inés Horovitz* andRoss D. E.MacPhee†*Department of VertebratePaleontology, AmericanMuseum of Natural History,New York, NY 10024-5192,U.S.A. E-mail:horovitz@amnh.org and†Department of Mammalogy,American Museum of NaturalHistory, New York, NY10024-5192, U.S.A.

Received 23 February 1998revision received 20 June1998and accepted 6 July 1998

Keywords: New Worldmonkeys, platyrrhines,Antilles, Quaternary,Antillothrix, Xenothrix,Paralouatta, Caribbean.

The quaternary Cuban platyrrhineParalouatta varonai and the origin ofAntillean monkeys

We describe recently recovered dental and mandibular remains of theCuban platyrrhine Paralouatta varonai, previously known from theholotype only (a nearly complete skull with very worn teeth). We alsoexpand on the original description of the type specimen.

Paralouatta is one of three extinct taxa of Greater AntilleanQuaternary monkeys known from craniodental remains. The othertwo, Xenothrix mcgregori and Antillothrix bernensis, occurred in Jamaicaand Hispaniola, respectively. It has been common practice to assumethat Antillean monkeys were more closely related to individualmainland taxa than to each other. Thus, P. varonai was thought to berelated to Alouatta; Antillothrix bernensis to Saimiri or Cebus; and X.mcgregori to Callicebus, or to callitrichines, or even to be of unknownaffinity. With the discovery of well-preserved dental remains ofParalouatta, it can now be ascertained that this species was in fact verydifferent from Alouatta. Cladistic analysis reveals a sister-grouprelationship between Antillothrix and Paralouatta, followed on thecladogram by Xenothrix and Callicebus (last taxon being the closestmainlaind relative of the Antillean clade). This conclusion has animportant biogeographic implication: recognition of an Antilleanclade, as advocated here, assumes only one primate colonization fromthe South American mainland, not several as previously believed.

? 1999 Academic Press

Journal of Human Evolution (1999) 36, 33–68Article No. jhev.1998.0259Available online at http://www.idealibrary.com on

Introduction

Platyrrhine primates have been a notable partof the mammalian fauna of South Americasince at least the late Oligocene/earlyMiocene (Hoffstetter, 1969; MacFadden,1990). The living species are found fromsouthern Mexico to northern Argentina, butthe fossil record establishes the New Worldmonkeys once ranged more widely, fromPatagonia to the Greater Antilles (i.e., theisland group consisting of Cuba, Hispaniola,Puerto Rico, and Jamaica). The past diver-sity of platyrrhines at the southern end oftheir distribution is becoming increasinglywell known, thanks to more than a centuryof dedicated work in this region (Ameghino,1906; Rusconi, 1934, 1935; Kraglievich,1951; Hershkovitz, 1970, 1974, 1981,

0047–2484/99/010033+36$30.00/0

1984; Fleagle & Bown, 1983; Fleagle et al.,1987; Fleagle, 1990). By comparison, thediversity of the endemic platyrrhines of theGreater Antilles (hereafter, the Antilleanmonkeys) is known only in barest outline.The objective of this paper is to reviewrecent progress in unravelling and interpret-ing the phylogeny of these monkeys, withparticular emphasis on the late Quaternaryspecies from Cuba, Paralouatta varonai.

Our understanding of the fossil history ofAntillean monkeys may be getting broaderin a geographical sense, but it is not verydeep temporally. Cuba, Jamaica, andHispaniola each supported one or moreendemic platyrrhines during the late Quater-nary, but Cuba is the only island with aTertiary primate record—currently consist-ing of a single fossil, a talus of early Miocene

? 1999 Academic Press

34 . . . .

age from the important locality of Domo deZaza (MacPhee & Iturralde-Vinent, 1995;Iturralde-Vinent & MacPhee, in press).

Fossils of extinct Antillean monkeys werefound (although not properly recognized assuch) as early as the 1920s in Hispaniola andJamaica (MacPhee, 1996), but Williams &Koopman (1952) were responsible for shed-ding the first real light on the subject. Sincethen, a number of new discoveries have beenmade (Rímoli, 1977; Rosenberger, 1977;MacPhee & Woods, 1982; Ford & Morgan,1988; Ford, 1990; Rivero & Arredondo,1991; MacPhee et al., 1995; MacPhee,1996), but the Antillean record is stillclouded by a variety of uncertainties. Froma systematic standpoint, the most seriousof these concerns how many species areactually represented in existing fossil assem-blages, and how they are related to oneanother. There are three named taxa:Paralouatta varonai Rivero & Arredondo,1991, from Cuba; Xenothrix mcgregoriWilliams & Koopman, 1952, from Jamaica;and Antillothrix bernensis MacPhee et al.,1995 (formerly Saimiri bernensis Rímoli,1977), from Hispaniola. There are, inaddition, a number of primate-like post-cranial remains from these islands that, forone reason or another, have not yet beenallocated; some may represent unknowntaxa (MacPhee & Fleagle, 1991; MacPhee,1996). It is a safe bet that we are farfrom having a complete roster of Antilleanmonkeys, even for the Quaternary (Ford,1990).

The relationships of Antillean monkeysare obscure. Indeed, until very recently, theonly conclusion one could draw from thescanty literature on this subject was thatthese monkeys had little to do with oneanother. Thus, it might be concluded thatCuban Paralouatta, supposedly a close rela-tive of Alouatta (Rivero & Arredondo,1991), could not also be a near affine ofHispaniolan Antillothrix bernensis becausethe latter was viewed as either a giant squir-

rel monkey (Rímoli, 1977) or some kind ofcebine related to both Saimiri and Cebus(MacPhee & Woods, 1982). Similarly, itseemed unlikely that Jamaican Xenothrix,variously considerd to be a callicebin,cebine, or a taxon of unknown affinities(Rosenberger, 1977; MacPhee & Fleagle,1991), could be closely related to the mon-keys from Cuba and Hispaniola. Adding tothis already complex picture, Ford (1986a)and Ford & Morgan (1988) argued thatseveral of the previously mentioned isolatedpostcranials from Hispaniola and Jamaicaare specifically marmoset like, which impliedthat yet another major platyrrhine clade wasonce represented in the Greater Antilles.

It is self-evident that, if the primate com-plements of Cuba, Jamaica, and Hispaniolahad multiple origins, there had to have beenmultiple colonization events. However,thanks to a number of new discoveries,especially ones made in the present decade,this picture of multiple separate coloniza-tions by unrelated propagules is no longerso easily maintained. The multiple originsviewpoint was explicitly challenged byMacPhee et al. (1995), who demonstratedon the basis of a preliminary cladistic studythat Paralouatta and Antillothrix are relatedas sister groups, and that Callicebus may bethe closest living relative of this dyad. Theposition of Xenothrix was not investigated.However, it is of interest that Rosenberger(1977) independently posited that Xenothrixmight be related to Callicebus on the basisof evidence then available. New fossils ofXenothrix (description of which is in prep-aration) provide an opportunity to determinewhether all Antillean monkeys (or at leastthose represented by adequate material) mayderive from a single colonizing ancestor.

One objective of this paper is to put onrecord a description and evaluation of allcraniodental specimens of P. varonai so farrecovered. Another is to present a com-prehensive cladistic analysis of Antilleanmonkeys. We address the latter goal within

35 PARALOUATTA VARONAI

the larger issue of platyrrhine systematics.To avoid ambiguity, in this paper we explic-itly define pitheciins as including Pithecia,Chiropotes, and Cacajao, atelines as Ateles,Brachyteles, Lagothrix, and Alouatta, and cal-litrichines as Callimico, Callithrix, Cebuella,Leontopithecus, and Saguinus.

Abbreviations

AMNH, American Museum of NaturalHistory, New York

CMC, Claremont-McKenna College,California

GPBSEC, Grupo Espeleológico ‘‘PedroBorrás’’ of the SociedadEspeleológica de Cuba

MNHNH V, Museo Nacional de HistoriaNatural, La Habana,Vertebrate Collection

M-D, mesiodistalB-L, buccolingual

Craniodental morphology andrelationships of Paralouatta varonai

Fossils allocated to P. varonai have beenrecovered at only two localities in Cuba,Cueva del Mono Fósil and nearby CuevaAlta (Rivero & Arredondo, 1991; JáimezSalgado et al., 1992). These sites are situ-

ated on the same south-facing slope of theSierra de Galeras, one of several blocks ofuplifted Jurassic limestones that make up theCordillera de Guaniguanico (Figure 1).

The first primate fossils from Cueva delMono Fósil were found in 1988 andincluded the type skull (Figure 2) and adistal humerus. Remains belonging to othervertebrates indicated that the temporal con-text of the site was Quaternary. The firstdetailed account of this material, by Rivero& Arredondo (1991), included a formaldescription of P. varonai and emphasizedthe similarity of the type skull to that of theliving howler monkey, Alouatta.

Since the late 1980s, accessible portionsof Cueva Alta and Cueva Mono Fósil havebeen carefully combed for new fossils byexpeditions of the GPBSEC, MNHNH, andAMNH. A number of additional platyrrhineremains have been recovered as a result,including a mandible, numerous isolatedteeth, and several postcranial pieces.Although exploration continues in thenumerous caves that riddle the rest of thesouth face of Sierra de Galeras, to date nonew primate-bearing fossil sites have beenidentified. This is, therefore, an opportunetime to review, describe, and interpret whathas been collected thus far.

Figure 1. Map of Cuba showing principal localities: CA, Cueva Alta and Cueva del Mono Fósil(Quaternary); DZ, Domo de Zara (early Miocene).

36 . . . .

Cueva del Mono Fósil and Cueva Alta arelocated on a mogote (a steep-walled lime-stone hill with a flat or gently rounded top).

It is now evident that most of the remainsfound in each cave did not occur thereoriginally, but were brought down from

Figure 2.

37 PARALOUATTA VARONAI

passages higher on the mogote through asystem of fissures. Evidence for this suppo-sition is the discovery of small bones (notprimate) in the upper part of the majorvertical fissure which transects Cueva delMono Fósil, and the fact that all discoveriesof consequence made at Cueva Alta camefrom a single locus—a small, sediment-choked chimney (Jáimez Salgado et al.,1992). Efforts to date bone from these caveschronometrically have not been successfulbecause the bones retain too little collagento permit 14C (radiocarbon) dating.Whether this means that they are actuallybeyond the range of radiocarbon dating hasnot been established, but it is certainly apossibility. If the Galeras faunule is com-paratively old, it would help to explain(although not fully clarify) why monkeybones have not been recovered elsewherein Cuba.

Craniodental morphology ofParalouatta

Rivero & Arredondo’s (1991) description ofthe holotype skull of P. varonai focused onsystematically important features and wasnot intended to be comprehensive. In thissection we provide a fuller account of this

important fossil, both to round out know-ledge of the cranial anatomy of Paralouattaand to provide a descriptive basis for someof the character analyses conducted in thenext section. It should be noted that thetemporary museum number cited by Rivero& Arrendondo (1991) for the holotypespecimen (MNHNH 90-25) has now beenreplaced by a permanent accession string(MNHNH V194).

Because the teeth of MNHNH V194 areexceptionally worn, Rivero & Arrendondo(1991) were unable to provide an adequatedescription of the dentition of P. varonai.Later collecting has resulted in the discoveryof a lower jaw (MNHNH V195) and some80 isolated teeth, many in excellent condi-tion. These new fossils yield a wealth ofdetail unknown previously. Our descriptionis conducted by element and we providemeasurements of dental elements in Table 1[for additional measurements, see originaldescription of type skull by Rivero &Arrendondo (1991)].

Rivero & Arrendondo (1991) interpretedoverall skull shape in Paralouatta as essen-tially indicative of alouattine affinity. Forexample, both display a substantial angle(airorhynchy) between the facial and neuralregions of the skull. However, Alouatta is a

Figure 2. Holotype specimen of Paralouatta varonai(MNHNH V194): (a) dorsal, (b) ventral (from a cast),(c) lateral, and (d) frontal views [(a) and (c) fromRivero & Arredondo, 1991].

38 . . . .

clear outlier among platyrrhines for thisfeature, while the condition in Paralouatta isbest described as incipient. Thus, while itcan be said that the skulls are broadly similarin this aspect, the two differ in many othercharacters—as our data matrix brings out.This point applies particularly strongly tothe dentition, which was previously poorlyknown. With the new dental remains ofParalouatta now available, it can be shownthat the Cuban monkey differs markedlyfrom both Alouatta and Stirtonia.

SkullIn most respects the neurocranium and basi-cranium of MNHNH V194 are exception-ally well preserved; by contrast, the facialregion is damaged extensively (Figure 2).

Frontal. Except for the glabella/nasionregion and the orbital processes, the frontalbone is quite complete. Shaped like an isos-celes triangle, with its largest dimensionoriented anteroposteriorly, the frontal isdelimited rostrally by a low supraorbitalridge surmounting the orbits [Figure 2(a)].Dorsally, each supraorbital ridge is throwninto relief by a slight depression in thefrontal, immediately behind the line of theridge. In lateral view, the typical platyrrhinecontact pattern is displayed, with the zygo-matic and the parietal interposed betweenthe frontal and alisphenoid. Within theorbit, the frontal runs from dorsolateralto medioventral, intersecting the lateral

Table 1 Dental measurements (in mm) of newremains of P. varonai1

Specimen B-L M-D

I1 V150 3·9 5·9V152 3·9 5·7V153 4·2 5·4V154 3·9 5·6V156 3·9 6·1V158 4·4 5·8

I2 V105 3·8 4·3V149 4·1 4·7V151 3·4 4·2V155 3·7 4·1

P2 V115 5·7 5·5V160 5·4 5·3V164 4·9 5·3V165 6·0 5·4

P3 V163 7·2 5·1V169 8·0 4·9V176 8·2 4·6V178 7·0 4·5V578 8·6 5·3

dP4 V166 6·7 5·6P4 V106 9·1 5·4

V116 9·1 5·5V170 10·0 5·2V171 9·2 5·2

M1,2 V120 9·1 6·6V179 9·0 6·9V180 9·7 7·0V181 9·3 6·5V183 8·8 6·6

M3 V122 7·0 6·3V191 7·2 5·5V192 7·1 5·3

I1 V126 3·6 2·8I2 V195 3·8 3·2C1 V127 3·2 5·1

V195 4·1 4·7P2 V117 5·3 5·4

V128 5·2 5·2V195 4·5 4·8

P3 V118 5·9 4·9V129 5·8 4·9V130 5·7 5·4V131 5·5 4·7V132 5·5 4·9V195 5·9 5·9

P4 V119 6·7 5·8V146 6·6 5·6V147 5·8 5·5V195 5·9 6·4

M1 V195 5·6 7·4M1,2 V123 5·3 7·1

V138 5·9 7·0V144 6·0 7·1V145 5·5 6·6

Table 1 Continued

Specimen B-L M-D

M2 V195 5·6 7·4M3 V124 5·1 7·8

V134 4·5 6·6V135 5·0 7·0V579 5·5 7·8V195 5·0 7·2

1Measurements for best preserved teeth only.

39 PARALOUATTA VARONAI

orbital fissure. Medial to its contact with thezygomatic, the frontal contacts successivelythe alisphenoid, the orbitosphenoid (abovethe orbital foramen) and, slightly moreanteriorly on the medial wall of the orbit, theethmoid (little of which is preserved).

Breakage in the glabellar region provides awindow into the midsagittal portion of thefrontal sinuses, which appear to have beenextensive (see below). Dorsally, the coronalsuture is drawn into a long, posteriorlydirected ‘‘V’’, corresponding to the tworemaining sides of the isosceles triangle.Bregma is located far to the rear, at thetransverse level of the posterior carotidformen (with skull in Frankfurt plane).

Ethmoid. Because of fusions and breakage,sutural boundaries in the ethmoid regioncannot be followed for any distance.However, it is clear that the ethmoid waspneumatized extensively and that, in con-sequence, the interorbital septum wascomparatively substantial. The septum’sthickness suggests that it was not fenes-trated. The anterior portion of the orbitalwall and upper face, including the lacrimalsand the nasals, are not preserved.

Maxilla. The maxillae are well preservedexcept for their medial portions. The bonyorbits jut from the face to a marked degree(especially evident in norma verticalis), whichsuggests that the eyes were very large,although not as large as in Aotus (for obser-vations on orbital size in Paralouatta, seeRivero & Arredondo, 1991). The maxillaextends backward to form much of theorbital floor and the medial side of theinferior orbital fissure (sphenomaxillary fis-sure) up to the point of contact with thepalatine. The facial portions of the maxillaebear multiple infraorbital foramina. Thearea normally formed by the premaxilla hasbeen lost through breakage, and there areno identifiable remnants of the maxillo–premaxillary suture.

The zygomatic process of the maxilla issituated low on the face. The preserved partof its ventral edge lies just above the planeof the alveolar border (

40 . . . .

cavity, at the level of the highest infraorbitalforamen, and is directed medioventrally.

A point of minor paleopathological inter-est concerns the large abscess chamber per-forating the wall of the maxilla above themesial root of the left M2.

Palatine. The palatine bones are partly pre-served [Figure 2(b)]. Each maxillo–palatinesuture parallels the dental series up to thelevel of M2, then runs medially to meet itsfellow (midsagittal contact lost throughbreakage). The greater palatine foramen, atthe level of M3, lies on or just medial to thetrack of this suture.

The posteromedial palatine spine islocated posterior to the transverse level ofM3. Its apparent degree of projection isincreased by deep scalloping of the choanalmargin of the palatines. The arc of thescallops does not reach the transverse levelof M3. The palatine enters into the con-struction of the orbit along the medial wallof the inferior orbital fissure. Posteriorly itcontacts the alisphenoid and anteriorly themaxilla.

Vomer. The bladelike vomer is visible onthe base of the skull beneath the pre-sphenoid, part of which it covers. Irregularlysutured into the palatines, the vomerextends to the rear edge of the palate andthereby helps to define the choanal aper-tures. The choanae are relatively enormous(right aperture, 14·1#9·1 mm), theirentrances being approximately four times aslarge in area as those of AMNHM 230805, aspecimen of Alouatta seniculus of similarskull length (right aperture, 8·6#3·7 mm).

Temporal. The temporal squamae are verylow, as in platyrrhines generally, and thepostglenoid process is notably elongated.The large postglenoid foramen [Figure 2(b)]is situated on the medial side of the latterprocess, rather than behind it or within it.There is a pronounced gap between the

anterior crus of the ectotympanic and thepostglenoid process; this is unlike mostplatyrrhines, in which these two structuresform a continuous surface or are situatedvery close together. The squamosal contactsthe alisphenoid medially, with which itforms a suture that runs parallel to themidsagittal plane to approximately the levelof the lateral pterygoid process. At this pointthe suture turns laterally and runs along theventral edge of the parietal.

The ectotympanic is completely fused tothe tympanic bulla (here assumed to bepetrosal in origin); no sign of a sutureremains. The aperture of the meatus is anoval ring, the long axis of which runsanteroventrally/posterocaudally. The meatalmargin is raised and highly rugose except onits dorso-caudal face, which is smooth andflattened.

The elongated tympanic bullae are mod-erately inflated. The anteromedial portionsof both are broken, thus exposing parts ofthe middle ear cavity. As seen from theoutside, the alisphenoid forms the rostraland lateral edges of the foramen ovale, whilethe bulla makes up this aperture’s medialand caudal edges. The canal for the auditorytube opens immediately beneath the caudalborder of the foramen ovale. The posteriorcarotid foramen is located on the medialcurvature of the bulla in the typical platyr-rhine position, just in advance of a lineconnecting the jugular foramina. It isrecessed into a small basin whose border isdefined by a sharp line or crest on the bulla’sventral surface. The stylomastoid foramen,which is only slightly smaller than thecarotid foramen, is located posteriorly on ornear the apparent margin of the ectotym-panic. The hypoglossal canal is buried in adeep pit above the anterior margin of theoccipital condyles.

The petrosal promontorium, seen bylooking through the external auditorymeatus, displays two bulges or prominences.The first is the margin of the aperture of

41 PARALOUATTA VARONAI

the fenestra cochleae; the second bulge,situated more anterodorsally, appears to beeither a bony eminence or (more likely) thenext turn of the cochlea itself, seen in reliefas it swells the lateral aspect of the pro-montorium. Similar bulges are present inCallicebus, Pithecia, callitrichines, Cebus,Saimiri, and Aotus. In all other genera exam-ined by us the promontorium is eitherwithout relief in this region or only the firstbulge is present.

Paralouatta has a typically anthropoidanterior accessory (paratympanic) cavitywhose posterior wall is partly defined by thetrack of the bony carotid canal (seeMacPhee & Cartmill, 1986). The dorsallyplaced epitympanic recess is large and filledwith short, irregular septa. Similar relief isalso present in the posterior part of thehypotympanic region.

The posterior end of the temporal is com-pleted by the mastoid region. In Paralouattathe mastoids are considerably swollen, andthey project laterally and especially posteri-orly much more than in Alouatta. Smallfenestrations created by breakage exposebony cellules within the mastoids, indicatingsignificant pneumatization.

Sphenoid complex. The ventral aspect of thesphenoid complex is unremarkable. Thepresphenoid–basisphenoid synchondrosis iscompletely fused, although a faint linemarks its original position. Cellules of largesize (possibly evidence of pneumatization)have been exposed by abrasion at the site ofthe basisphenoid–basioccipital synchrondo-sis. The body of the basisphenoid bears lowridges paralleling the tympanic bullae, prob-ably for the origin of prevertebral muscles(see description of occipital).

The dorsal wing of the alisphenoid con-tacts the zygomatic, parietal, and squam-osal. The dorsal wing forms the lateral edgeof the inferior orbital fissure. The ventral(pterygoid) wing forms a small fraction ofthe medial edge of the inferior orbital fissure

and most of the pterygoid process (theanterior third of each process is contributedby the palatine). Neither the lateral nor themedial pterygoid plates are completely pre-served, but it is clear that the lateral plateswere much larger than the medial, as inplatyrrhines generally. It is not possible todetermine whether the medial plates pro-jected substantially. However it is possibleto see that the pterygoid fossa between themedial and lateral pterygoid processes wasvery shallow and did not excavate the base ofthe skull. In this regard Paralouatta is similarto Callicebus, pitheciins and atelines, butcontrasts markedly with Cebus, Saimiri, andAotus, in which the fossa indents the skullbase.

Parietal. In Paralouatta the parietals meetthe zygomatics along an irregular, dorso-ventrally oriented line. A projecting portionof the parietal’s ventralmost edge intervenesbetween the zygomatic and the alisphenoid,and thereby manages to border on the lateralorbital fissure. Parietal contribution to thedelimitation of the lateral orbital fissure is acharacter present (although frequently poly-morphic) in most platyrrhines. However, inAlouatta, Brachyteles, and Cebus, the lateralorbital fissure is normally defined by thezygomatic exclusively, or by this bone and(for a small distance) the alisphenoid. Theparieto–alisphenoid suture, about one-quarter of the length of the parieto–squamosal contact, terminates close to theposterior (squamosal) root of the zygomaticarch.

As seen from above, the temporal linesare remarkably sinusoidal, flaring onceanteriorly (at the level of the supraorbitalridge), again centrally (at bregma), and onceagain posteriorly (just in advance of thelambdoidal suture).

Zygomatic. This bone is not preserved com-pletely on either side: the orbital marginsare missing bilaterally, and the zygomatic

42 . . . .

roots of the zygomatic arches are only par-tially preserved. The fronto– and parieto–zygomatic sutures and the formation of thelateral orbital fissure have already beendescribed. The maxillo–zygomatic sutureslants posteroventrally, with the result thatthe maxilla and the zygomatic form respect-ively the ventral and dorsal halves of the rootof the zygomatic arch.

Multiple zygomaticofacial foramina arelocated on the face, near the ventrolateralmargin of each orbit (although this is notobvious in the figures because of breakage).At least three foramina are preserved on theright side, the central one being the largest[see Rivero & Arredondo (1991)]. In mostplatyrrhines, there is a single zygomatico-facial foramen on each zygomatic (Figure 3);however Alouatta, some pitheciins, and Ao-tus occasionally display multiple foramina.

Occipital. The basioccipital widens caudally.Its ventral surface is marked by the con-tinuation of the low ridges for muscleattachment seen on the basisphenoid.

Ridging is extensive, more so than in anyliving platyrrhine, including Alouatta. Thewidth of the skull in norma occipitalisis considerably increased by the lateralprojection of the mastoids.

The skull qualifies as airoryhnchicbecause the basioccipital is angled (ventrallyflexed) with respect to the dental series,somewhat more than most platyrrhinesexcept Alouatta, in which the angle ismarkedly larger.

The foramen magnum is positioned sothat if faces downward as much as back-ward when the skull is placed in theFrankfurt plane, as in platyrrhines otherthan Alouatta. By contrast, in Alouatta theforamen magnum is more posteriorly posi-tioned and is oriented at a sharp angle to thebasioccipital.

The supraoccipitals form an angle ofapproximately 45) with the Frankfurt plane.The surface of the occipital planum is excep-tionally rugose, suggesting that there was aconsiderable investment in postural musclemass.

Figure 3. Skull of adult Alouatta (lateral view) showing several characters (see Appendix 1).

43 PARALOUATTA VARONAI

MandibleThe mandible (MNHNH V195) of Para-louatta was found in 1991 in Cueva delMono Fósil, but at a considerable removefrom the position of discovery of the typeskull. The mandible (Figure 4) is that of an

adult animal, although it is far too small toarticulate with the type skull. The specimenpreserves the left ascending and horizontalrami, with P2–M3 in situ and alveoli for otheranterior teeth, the symphyseal portion, bear-ing I2 and C1 and a small part of the inferior

Figure 4. Paralouatta varonai mandible (MNHNH V195), in (a) occlusal and (b) lateral views.

44 . . . .

border of the right horizontal ramus. Onthe preserved left ascending ramus, thecoronoid process is broken at its root andthe medial aspect of the mandibular condyleis abraded. Otherwise, the specimen is inextremely good condition. However, as theteeth of both the type skull and the mandibleare exceedingly worn, descriptions of indi-vidual loci are based largely on isolatedspecimens found during screening opera-tions at Cueva Alta.

DentitionAlthough Rivero & Arrendondo (1991) con-cluded that P. varonai was a definite alouat-tin, they noted that the teeth of the Cubanspecies appeared to differ in several waysfrom those of howler monkeys. Thus theynoted that molar pericones were present andlarge, and that, curiously, the maxillarycanine (as indicated by a preserved root)would have been tiny. Additional markeddifferences between Paralouatta andAlouatta were briefly documented byMacPhee et al. (1995).

To a greater degree than in any otherknown platyrrhine, the entire dental series ofParalouatta evidently wore down in such a

way that asperities (cusps and cristae) wererapidly removed, effectively converting theocclusal surfaces of the cheek teeth intolarge, flat milling surfaces (see Figure 4).Paralouatta is unusual in displaying, in com-bination, the following features usuallyassociated with hominine dentitions:extreme bunodonty, premolar hypertrophy,widened maxillary incisor crowns, and, mostinterestingly, marked canine reduction(crowns incisiform, projecting little or not atall beyond occlusal plane of cheek teeth, andcanine root small).

The dental formula of Paralouatta is 2133/2133, as in all known platyrrhines exceptcallitrichines (other than Callimico) andXenothrix.

Maxillary teethCentral incisors. MNHNH V150, 152–154,156–158. Large size (compared to lateralincisors), substantial breadth, and lowcrown height are noteworthy features of themaxillary central incisors [Figure 5(a)]. InAlouatta, Brachyteles, Ateles, and, to a lesserdegree, Lagothrix, incisors are higher-crowned but narrower. As is frequently thecase in platyrrhines, the mesial margin of

Figure 5. P. varonai, stereoscopic views of isolated front teeth: (a) I1 (MNHNH V154), (b) I2 (MNHNHV155), (c) I1 (MNHNH V126), and (d) C1 (MNHNH V127).

45 PARALOUATTA VARONAI

the crown is higher than the distal, and thebiting edge is distinctly curved. On little-worn specimens, a bean-shaped fovea isvisible on the lingual surface.

Incisor tooth use in Paralouatta seems tohave involved considerable amounts of bite-pulling, because worn teeth display numer-ous small grooves arrayed normal to theedge of the occlusal surface. Wear featuressuggest that maxillary incisors were drawnorthally across lowers during biting, or thatfood items were shredded by pulling themmanually between clenched incisor teeth. Asa result, wear on the lingual or foveal surfaceof I1 is often substantial (for example, allenamel lost from foveal surface MNHNHV158). Step-fracturing and pitting of theenamel is visible in, and restricted to, theareas immediately adjacent to the bite sur-face. This localization suggests that thesedefects were acquired during life, probablyas the result of small fragments of enamelspalling off during powerful biting.

Lateral incisors. MNHNH V105, 149, 151,155. Maxillary lateral incisors have shorterroots, considerably smaller crowns, andnarrower cervical regions than do centralincisors [Figure 5(b)].

Characteristic of I2s of Paralouatta is thepresence of interproximal facets on boththe mesial and distal margins of the crown.The existence of the distal interproximalfacet implies that I2 and C1 were in perma-nent contact, that is, they were not separatedby a diastema. (This point was not obviouswhen only the type skull was available, sinceit lacks incisors and preserves only the stumpof one canine root.) In this feature Paral-ouatta is unlike any living large-bodied NewWorld monkey, in all of which the caninesare enlarged and diastemata are present. Inthese latter platyrrhines, the distal aspects ofI2 crowns sometimes display an oval facet forthe mesial aspect of the tip of C1. However,because the C1 meets the I

2 at an obliqueangle, the resulting facet is never vertically

aligned. In Paralouatta, the I2 distal facet isvertical, circular rather than oval in form, andseparated from facetting on the bite edge bya significant gap. Therefore it cannot be a C1facet, but must instead be for the C1. Takentogether, these features strongly imply thatin the Cuban monkey, maxillary incisorsand canines were in intimate contact andprone to develop interproximal facetting.

Canine. MNHNH V194. The type skullretains only the deepest part of the root ofthe right C1, which at that level, is smallerthan the alveolus for P2. The tiny size ofthis root was confirmed by X-ray of theholotype.

Premolars. MNHNH V115, 160–162, 164,165 (P2); 163, 169, 174–178, 578 (P3);MNHNH V106, 116, 167, 168, 170–173(P4); MNHNH V166 (dP4).

P2 (MNHNH V115, 165) is double-rooted in the type specimen (MNHNHV194), as reported by Rivero & Arredondo(1991). However, the three isolated speci-mens in which the roots are complete ornearly complete (V160, 162, 164, 165) arein fact single-rooted, as is normally but notuniversally the case in other platyrrhines(Hershkovitz, 1977). For example, in mostspecimens of Callicebus the P2 root is singleand undivided, but a split root is occasion-ally seen. P2 bears a single cusp on its buccalside, and its trigon widens distally [Figure6(a)]. P3 and P4 [Figure 6(b), (j)] are mor-phologically similar, although P3 is some-what smaller. Both of the distal premolarloci bear two cusps, with the protoconebeing situated in the mesiobuccal quarter ofthe trigon. The lingual cingulum is promi-nent and mesially projecting relative to thetrigon (cingular buccolingual width at leasthalf that of trigon). In the type specimen,both P3 and P4 exhibit two buccal roots inaddition to a lingual root. Among isolatedspecimens, MNHNH V163 and V178 (bothP3s) are single-rooted, whereas MNHNH

46 . . . .

V106 (a P4) has two roots (one buccal, onelingual). Platyrrhines display some varia-bility in root number in P3 and P4. In Cebus,

Saimiri, Aotus, Cacajao, Alouatta, Callicebus,and Xenothrix, P3 normally possesses tworoots (three occasionally in Alouatta). On

Figure 6.

47 PARALOUATTA VARONAI

the other hand, in Ateles the roots of P3 tendto be fused and only the tips of the rootsare separate. P4 normally has two roots inCebus, Saimiri, Cacajao, Alouatta, Callicebus,and Ateles (as in P3, tips barely separate); inAotus the normal condition is three roots.

Only one deciduous premolar, a dP4

(MNHNH V166), has been recognized withcertainty (Figure 7). Very low crowned withthree broadly splayed roots (two buccal, onelingual), it resembles upper molars in gen-eral outline, but the proportions of the majorcusps are somewhat different. The lingual

cingulum is less developed (crown moretriangular), and overall the tooth is muchsmaller than true molars.

Molars. MNHNH V104, 120, 121, 179–184, 186–190 (M1,2); MNHNH V122, 185,191–193 (M3). We have found no reliableway to separate first and second upper mo-lars, and therefore will discuss them together.

Upper molars of Paralouatta display sev-eral diagnostically interesting features. Onesuch feature is the size and differentiationof cingular structures [Figure 6(f), (m)].

Figure 6. P. varonai, stereoscopic views of permanent premolars and molars with explanatory keys: (a) P2

(MNHNH V115), (b) P4 (V116), (c) P2 (MNHNH V117), (d) P3 (MNHNH V118), (e) P4 (MNHNHV119), (f ) M1,2 (MNHNH V120), (g) M3 (MNHNH V122), (h) M1,2 (MNHNH V123), (i) M3(MNHNH V124), (j) P2 (MNHNH V115), (k) P3 (MNHNH V118), (l) P4 (MNHNH V119), (m) M

1,2

(MNHNH V120), and (n) M1,2 (MNHNH V123).

Figure 7. Stereoscopic view of P. varonai deciduous P4 (MNHNH V166).

48 . . . .

Except on the mesial side of molar trigons,a continuous ledge borders upper molarcrowns; the ledge is best developed buccallyand lingually. In the least worn examplesof M1,2 (e.g., MNHNH V120, 180), thebuccal cingulum is continuous from thepreparacrista to the postmetacrista, althoughit is scored by a tiny groove in the ectoflexus.The buccal cingulum is adorned with arelatively discrete distostyle distobucally, avery faint parastyle, and two low bumps(=mesostyles) on either side of the groove inthe ectoflexus.

The lingual cingulum is massively devel-oped and forms a continuous band from themesiolingual aspect of the protocone to thedistostyle of the buccal cingulum. There isa well-developed hypocone and a smallerbut nevertheless well-developed entostyle(=pericone), doubled in some specimens(e.g., MNHNH V120, 180). The hypoconeis connected to the metaloph via a well-developed prehypocrista (hypocone crest).The hypocone is large in howler monkeys,and there is a deep incisure between thehypocone and protocone that is lackingin Paralouatta.

One of the outstanding features of molarconstruction in Paralouatta is the position ofthe protocone, which appears to be situatedvirtually in the centre of the occlusal surface.This appearance is in large measure due tothe great width of the lingual cingulum,which isolates the protocone from the crownmargin. In Alouatta, the protocone is notlingually bordered by a cingulum at all, whilein Stirtonia (see Material and methods) thelatter is very narrow and discontinuous.

The major trigon cusps are markedlybunodont and enclose a large but shallowtrigon basin. In unworn teeth (MNHNHV120, 180), the deepest part of the basin iscorrugated by a number of tiny cuspules andgrooves. However, the type of crenulationis not readily comparable to that seen onpitheciin molars; in the latter they are muchfiner, and have the shape of elongated

ridges. As in other platyrrhines, M1,2 displaythree roots, two buccal and one lingual.

M3, smaller than M1,2, displays fourcusps, of which the paracone is best devel-oped. The hypocone appears on the lingualcingulum bordering the distal side of thetooth and is barely cuspiform. The floor ofthe trigon is irregularly rugose, as in M1,2.This tooth may exhibit two discrete roots(as in MNHNH V185, 193) or only asingle, fused one (MNHNH V122, 191,192) [Figure 6(g)].

Mandibular teethCentral and lateral incisors. MNHNH V126(I1); MNHNH V195 (I2). The narrow-crowned I1 and I2 are tiny compared to theupper incisors [Figure 4, 5(c)]. There is onlyone identifiable I1 in the existing sample(MNHNH V126); its flat occlusal edgepresents a large dentine lake exposedthrough wear. Central incisors are missing inthe jaw (MNHNH V195), but I2 is pre-served on the right ramus. Compared to I1,the I1 has a narrower crown and a smallerroot (as suggested by empty alveoli in thejaw). In both teeth, many sub-parallelstriations can be seen running normal to thebite surface (cf. maxillary incisors).

Canine. MNHNH V195, 127 [Figure 4,5(d)]. The C1 is present in situ in the MonoFósil lower jaw (MNHNH V127); thisspecimen demonstrates beyond any doubtthat extreme canine reduction was the nor-mal condition in Paralouatta. It is also clearfrom this specimen that C1 was no moreprojecting than P2, from which it may bedistinguished only by its greater degree ofbuccolingual compression and single, blade-like, mesiodistally oriented principal cusp. Asubtle lingual cingulum is present in V127.

Premolars. MNHNH V195 (mandible withP2–4); MNHNH V117, 128 (P2); MNHNHV118, 129–132 (P3); MNHNH V119,146–148 (P4). Dimensions of mandibular

49 PARALOUATTA VARONAI

premolars increase distally, making P2 thesmallest member of the premolar row(Figure 4). This premolar locus–size rela-tionship is seen in other platyrrhines havingdiminutive canines (e.g., Callicebus). In con-trast, in all atelines except Brachyteles, P2 isthe largest premolar. In Paralouatta, P2 andP3 are single-rooted; none of the isolated P4shas a completely preserved root.

The P2 has one buccal cusp from whichradiate three crests: one runs mesially,another curves slightly as it passes disto-lingually, while the third and shortest crestoriginates slightly distal to the cusp, runslingually, and ends in a small swelling[Figure 6(c)]. About twice as much of thetooth is located mesial to the last crest as liesdistal to it. The cingulum is not continuousaround the lingual and distal surfaces of theP2 crown (as it is in atelines) because it isinterrupted by the lingual crest.

The P3 has two distinct cusps of subequalheight, a metaconid and a larger (in diam-eter) protoconid. A crest running mesiallyfrom the metaconid describes a sharp angleand then curves distolingually onto theprotoconid. The talonid bears no cusps,is longer mesiodistally on the lingual side,and is completely enclosed by a crest. Thetrigonid is notably larger than the talonid[Figure 6(d), (k)].

The P4, the largest of the three premolars[Figure 6(e), (l)], has a square outline and awell developed protoconid and metaconid.Both cusps are subequal in height, but theprotoconid has a much larger volume thanthe metaconid. As in the molars, the buccal(protoconid) side of the tooth is swollen andprojecting. Trigonid and talonid basins areoriginally distinct, but quickly become worndown to shallow grooves. It displays hypo-conid and entoconid.

Molars. MNHNH V195 (mandible withM1–3); MNHNH V123, 136, 138–142, 144,145, 579 (M1,2); MNHN V124, 134, 135(M3).

As in the case of M1 and M2 we cannotidentify any consistent morphological or sizedifferences between M1 and M2. All man-dibular molars display two roots, one mesialand the other distal.

Compared to Alouatta, lower molar cuspsare stouter, crests are much less markedeven in unworn teeth, and in worn teeththere is almost no difference in cusp heightprofile between talonid and trigonid cusps[Figure 6(h), (n)].

Alouatta and Stirtonia distinctively differfrom Lagothrix, Ateles, and Brachyteles in thatthe talonid is transversely wider than thetrigonid. Inspection shows that breadth dif-ference is mainly due to the fact that, inAlouatta, the apex of the entoconid bulgeslingually to a noticeable degree, giving thetalonid an almost pear-shaped outline. Par-alouatta critically differs in that protoconidand hypoconid apices are not displaced.Instead, the entire buccal aspect of the lowermolars is swollen, making the protoconidand hypoconid seem proportionately largerthan the metaconid and entoconid and giv-ing the tooth a lop-sided look, similar toXenothrix molars (see figure in Williams &Koopman, 1952).

The distal wall of lower molar trigonids is acontinuous, raised crest joining metaconidand protoconid. It is on a sharp oblique, asin Alouatta and Stirtonia. In all molars thecristid obliqua (=premetacristid) is stronglybuilt and intersects the distal wall of the tri-gonid at a position intermediate between theprotoconid and metaconid. As a result theectoflexid is very deep in all lower molars, itsapex being situated within the middle one-third of the tooth’s breadth. In little-wornspecimens (e.g., V579) the ectoflexid isfrequently adorned with one or two smallcuspules (ectostylids), usually positioned onthe distobuccal wall of the protoconid.

On M3 there is a hypoconulid, of moderatesize, situated directly distal to the entoconidand separated from it by a sulcus leadinginto a small distolingual basin [Figure 6(i)].

50 . . . .

The hypoconulid is occasionally present onthe M3 of many platyrrhine species.

Cladistic analysis

Materials and methodsA total of 80 characters are listed anddefined in Appendix 1. These are scored inAppendix 2 for the taxa making up thecomparative set, which include Cebupithecia,Stirtonia, Paralouatta, Antillothrix, Xenothrix,the 16 extant genera of New World mon-keys, and several outgroups. Cebupitheciasarmientoi (Stirton & Savage, 1951), Stirto-nia tatacoensis (Stirton, 1951; Herschkovitz,1970) and S. victoriae (Kay et al., 1987)are fossil species from the Middle Mioceneof Colombia. C. sarmientoi has been pre-viously placed among pitheciines (Stirton &Savage, 1951; Stirton, 1951; Orlosky, 1973;Rosenberger, 1979; Kay 1990). Stirtonia iscurrently considered the sister group ofAlouatta (Rosenberger, 1979; Setoguchiet al., 1981; Kay et al., 1987, 1989). Asmentioned in the Introduction, P. varonai,A. bernensis, and X. mcgregori are Quaternaryspecies from Cuba, Hispaniola and Jamaicarespectively. Character analysis of X.mcgregori is based on the type mandibleplus several new fossils recently collectedby RDEM, Donald A. McFarlane (CMC),and co-workers in southern Jamaica (twopartial mandibles, a maxillary fragment, anda partial skull preserving the palate and mostof the nasal fossae and maxillary sinuses;Horovitz et al., 1997). Outgroup taxa con-sisted of Tarsius, a wide array of living catar-rhines (including both cercopithecoids andhominoids), and the Oligocene Fayumanthropoid Aegytopithecus. Unlike mostfossil taxa that might have been used asoutgroups in this investigation, Aegypto-pithecus is represented by relatively completeskeletal remains and could therefore bescored for many characters.

Most of the characters utilized in thisstudy are based on craniodental mor-

phology, although a few pertain to the post-cranium and soft tissue anatomy. Characterstaken from the literature were verified be-fore utilization. With respect to continuouscharacters, we used only those that showedstates separated by gaps in distributionamong groups of terminal taxa. These char-acters were considered additive. Missingcharacters were scored as question marks(see Appendix 2). Phylogenetic analysis wasperformed using the program PAUP (Phylo-genetic Analysis Using Parsimony), version3.1.1 (Swofford, 1993) applying a heuristicsearch with stepwise random additionsequence of taxa and TBR, done over 100replications. All characters were weightedequally and variable ones were consideredpolymorphic. Trees were rooted by desig-nating Tarsius as the outgroup.

We obtained Bremer support values foreach branch (Bremer, 1988; Källersjö et al.,1992), inspecting the strict consensus oftrees up to four steps longer than the mostparsimonious ones. For example, branchesthat collapse in a strict consensus of treesa step longer than the minimum, have aBremer support of ‘‘1’’.

Results

The heuristic search yielded three most par-simonious trees (CI=0.51, RI=0.66, treelength=269 steps) the strict consensus ofwhich is shown in Figure 8. In this con-sensus, Aegyptopithecus is positioned as thesister group of all other anthropoids, andplatyrrhines appear as monophyletic. Thethree trees differ in how relationships amongatelines are portrayed. Brachyteles appearseither as the sister group of the Alouatta–Stirtonia dyad (with Lagothrix–Ateles as thenext branch), or as basal within atelines. Inthe latter case, Ateles appears either as thenext offshoot within atelines, or as the sistergroup of Lagothrix. Characters supportingall clades in the trees represented by theconsensus depicted in Figure 8 are listedin Table 2.

51 PARALOUATTA VARONAI

The Bremer support values (Figure 8)indicate that most branches of the depic-ted topology are unstable, including therelationships of Paralouatta to the otherAntillean monkeys and Callicebus. Thetopology suggested by the original descrip-tion of Paralouatta (Rivero & Arredondo,1991), in which Paralouatta is regarded asthe sister group of Alouatta, is 11 steps

longer than the most parsimonious tree. Aslightly different formulation, ten stepslonger than the most parsimonious tree, hasParalouatta as sister group of the Alouatta–Stirtonia pair. Though our new hypothesismay be falsified with new data, it contra-dicts rather strongly the contention thatParalouatta may be closely related toAlouatta.

Figure 8. Strict consensus of the three most parsimonious trees obtained with 80 morphological characters(see Appendices 1 and 2); ‘‘†’’ indicates fossil taxon. Antillean clade enclosed in rectangle. Unambiguouscharacter support for each node (labelled with circles) shown in Table 2. Numbers above branchesindicate level of Bremer support.

52 . . . .

Table 2 Unambiguous characters supporting tree nodes depicted in Figure 81

Branch Character Change

node_47]node_46 47. P4 metaconid/protoconid height 0]148. P4 hypoconid presence/absence 0]149. P4 entoconid presence/absence 0]155. M1,2 buccal cingulum presence/absence 1]073. M1 postmetacrista slope 0]1

node_46]node_43 13. Tentorium cerebelli ossification 0]117. Canal subarcuate fossa/sigmoid sinus 0]124. Pterion region contact 1]078. M3/P4 length 3]2

node_43]node_32 15. Paired prominences in middle ear 0]146. P3 meta/protoconid height 1]254. M1 entoconid position 1]058. M3/P4 length 3]260. I1 lingual heel presence/absence 1]078. M3/P4 length 2]1

node_32]node_31 58. M3/P4 length 2]1node_31]node_30 38. C1 lingual cingulum spike-like vertix 0]1

40. dP2 angle mesiodistal axis/postprotocristid 1]079. M’s parastyles presence/absence 0]1

node_30]node_29 6. Presence of claws 0]121. Eyeball physically enclosed 0]122. Cranial capacity 1]048. P4 hypoconid presence/absence 1]049. P4 entoconid presence/absence 1]0

node_29]node_28 1. Number of offspring at a time 0]116. Pterygoid fossa depth 0]144. P3/P4 protoconid size 0]158. M3/P4 length 1]072. M1 hypocone/prehypocrista presence/absence 1]276. M2 hypocone presence 1]078. M3/P4 length 1]0

node_28]node_27 14. Pneumatization in middle ear 0]1node_27]node_26 28. dI2 shape 1]0

29. I1/I2 height 2]130. I1/I2 alignment 0]131. I1,2 shape 0]132. Meso- and distostyles of I1,2 0]134. C1 root shape 0]135. C1 lingual cingulum 1]038. C1 lingual cingulum spike-like vertix 1]045. P3/P2 talonid 0]147. P4 meta/protoconid height 1]063. dP2 trigon 1]0

node_43]node_42 16. Pterygoid fossa depth 0]141. dP2 cross section shape 1]0

node_42]node_39 56. M2 trigonid/talonid height 0]172. M1 hypocone/prehypocrista presence/absence 1]0

node_39]node_35 33. Diastema between C1 and I2 0]136. C1 lingual crest sharpness 0]137. C1 lingual cingulum mesial elevation 1]058. M3/P4 length 3]261. I2 orientation 0]165. P3 preparacrista 0]1

node_35]node_34 59. Molar enamel surface 0]167. P4 lingual cingulum 1]0

53 PARALOUATTA VARONAI

Three unique, unambiguously positionedcharacters support Platyrrhini: presence ofan ossified tentorium cerebelli (Character13), presence of a canal which traverses theposterior wall of the subarcuate fossa toconnect with the channel for the sigmoidsinus (Character 17), and zygomatico–parietal contact (Character 24). Thesecharacters constitute a morphology-basedargument for platyrrhine monophyly anddeserve additional comment.

Character 13. Hershkovitz (1977) notedthat the tentorium is extensively ossified inatelines and, to a lesser degree, in otherplatyrrhines; tentorial ossification alsooccurs in lemuroids. However, we find that,as a group, platyrrhines may be distin-

guished from other primates by the fact thattentorial ossification extends behind thesubarcuate fossa as well as above and infront of it (Figure 9). Neverthless, NewWorld monkeys differ in the degree to whichthe tentorium is ossified. In atelines ossifica-tion is always extensive, whereas in somecallitrichines and some specimens of Saimirionly the portion of the tentorium attachingto the petrosal apex displays any sign ofbone formation. Indeed, in some specimensof Saimiri there is no indication of tentorialossification at all, and for this reason wescore this character as polymorphic insquirrel monkeys (see Appendix 1).

Our survey of other primates showedthat lemuroids characteristically present arestricted, T-shaped tentorial ossification in

Table 2 Continued

Branch Character Change

node_34]node_33 70. P4/M1 buccolingual breadth 0]172. M1 hypocone/prehypocrista presence/absence 0]1

node_39]node_38 15. Paired prominences in middle ear 0]123. Zygomatic arch ventral extent 1]034. C1 root shape 0]162. C1/P4 alveolus size 0]1

node_38]node_37 25. Nasal fossa width 0]139. C1/P4 buccolingual alveolus size 0]153. M1 buccal bulging of protoconid 0]1

node_37]node_36 52. M1 oblique cristid and protolophid intersection 0]168. P4 lingual cingulum mesial projection 0]170. P4/M1 buccolingual breadth 0]175. M1 pericone/lingual cingulum presence/absence 1]273. M1 postmetacrista slope 1]074. M1 protocone/hypocone alignment 0]1

node_42]node_41 2. Number of lumbar vertebrae 0]15. Ventral glabrous surface on tail presence/absence 0]1

20. Temporal emissary foramen presence/absence 1]066. P4 protocone position 1]067. P4 lingual cingulum 1]0

node_41]node_40 52. M1 oblique cristid and protolophid intersection 0]1node_46]node_45 7. Carpo-metacarpal joint of thumb 0]1

19. Ectotympanic shape 1]067. P4 lingual cingulum 1]0

node_45]node_44 4. External tail, presence/absence 1]08. Rib cage shape 0]19. Ulnar participation in wrist 0]1

10. Sternebral proportions 0]1

1Based on morphological data set shown in Appendices 1 and 2.

54 . . . .

front of the petrosal apex, quite unlike theplatyrrhine condition. Like catarrhines andTarsius, lemurs lack a posterior extension oftentorial ossification behind the subarcuatefossa. The presence and nature of tentorialossification could not be determined in oursample of fossil Old World anthropoids.

Character 17. The innominate canal con-necting the subarcuate fossa and sigmoidsinus was first identified by Cartmill et al.(1981). This canal is located behind andbelow the aperture of the vestibularaqueduct, and is presumably for venousdrainage. Although Cartmill et al. (1981)reported this canal to be absent in atelines,we determined on the basis of our moreextensive sampling that this feature is regu-larly present in all New World monkeys,including atelines (feature not yet confirmedfor poorly-sampled Brachyteles). The vesseltraversing the canal does not appear to bethe homolog of the sigmoido–antral veinand canal described by Saban (1963) inlemurines in approximately the same loca-tion. In lemurines this vein issues from themastoid antrum and drains to the sigmoidsinus, but in platyrrhines there is no evi-dence of a mastoid connection.

Two anthropoid petrosals from theFayum Oligocene were described byCartmill et al. (1981). One of them has beenassigned tentatively to the fossil anthropoidApidium; the other may belong to any ofthe larger anthropoids (i.e., Aegyptopithecus,Parapithecus, Propliopithecus). The canal inthe subarcuate fossa is absent in sampledextant catarrhines, Tarsius, and the isolatedpetrosals of ?Apidium and ?Aegyptopithecusdiscussed by Cartmill et al. (1981).

Character 24. Another unambiguouscharacter on the most parsimonious treesthat supports platyrrhine monophyly iszygomatic–parietal contact on the sidewallof the skull as seen in side view (Figure 3).In Tarsius, living catarrhines, Aegypto-pithecus, and possibly Apidium (Simons,1959; Fleagle & Rosenberger, 1983), thesetwo bones do not make contact on thesidewall of the skull because the alisphenoidand frontal are interposed between them.However, in Apidium the surface of thetemporal process of the frontal has a rugosesurface suggestive of broken bone (Simons,1959; Fleagle & Kay, 1987) which couldhave contained the parietal zygomaticsuture, as in platyrrhines (Fleagle & Kay,

Figure 9. Medial view of sagittal section of Callicebus moloch skull (after Hershkovitz, 1977), illustratingpartial ossification of tentorium cerebelli (Character 13) and presence of canal connecting subarcuatefossa and sigmoid sinus (Character 17).

55 PARALOUATTA VARONAI

1987). This possibility needs to be evaluatedon more complete cranial remains.

Relationships of Greater Antillean monkeysIn the most parsimonious trees, the cladeconsisting of Callicebus and the GreaterAntillean monkeys is supported by fourunambiguously placed characters. Theyshare the derived condition of Character 15,possession of two prominences on the lateralwall of the promontorium. The primitivecondition for this character is the presenceof a flat surface or a single prominence. Theother three unambiguously placed charac-ters are: ventral border of zygomatic archextending below plane of alveolar border(Character 23, derived from a conditionin which zygomatic arch is situated higheron face); mandibular canine root highlycompressed (Character 34, derived froma more rounded condition); and alveolusof maxillary canine smaller than that ofP4 (Character 62, derived from reversecondition).

The Antillean clade itself is supported bythree unambiguous characters: nasal fossawider than palate at level of M1 (Character25, derived from narrower conditiondepicted in Figure 10); alveolus of mandibu-lar canine buccolingually smaller than thatof P4 (Character 39, derived from reversecondition), and mandibular M1 protoconidhaving bulging buccal surface (Character53, derived from condition in which featureis absent).

The dyad consisting of Paralouatta andAntillothrix is supported by six unambiguouscharacters: M1 oblique cristid intersects pro-tolophid lingual to protoconid (Character52, derived from a position directly distal toprotoconid); P4 lingual cingulum projectsmesially (Character 68, derived from condi-tion in which cingulum projects directlylingually); P4 subequal to M1 in bucco-lingual dimension (Character 70, derivedfrom condition in which P4 is smaller); M1

possesses distinct pericone (Character 75,

derived from absence of pericone); M1 post-metacrista slopes distobuccally (Character73, derived from slope directed distallyor distolingually); and M1 hypocone islocated lingually with respect to proto-cone (Character 74, derived from condi-tion in which this pair of cusps is alignedmesiodistally).

Figure 10. Width of nasal fossa (Character 25) illus-trated in (a) Cebus nigrivittatus at the level of M1, infrontal section (from Hershkovitz, 1977); (b) P. varonaiat similar level, in imaginary frontal section. In Cebus,nasal fossa is narrower than palate between lingualedges of left and right M1; in Paralouatta, it is wider(condition shared only with X. mcgregori). Featuresnf and ms are nasal fossa and maxillary sinus,respectively.

56 . . . .

Discussion

At present there is no broadly acceptedcladogram of platyrrhine intergeneric rela-tionships. Although there are many reasonsfor this, it is nevertheless the case that in-formative morphological characters appearto be relatively hard to find in this group:individual taxa are highly autapomorphic,and published trees contain large amountsof homoplasy.

Rosenberger (1981, 1984), Ford (1986b),Kay (1990), and MacPhee et al. (1995) havepresented trees that have some features incommon. Thus all of these workers recog-nize 16 living genera, and apportion themajority of them in the same way amongthree major phylogenetic groupings: Atelinae,including Ateles, Brachyteles, Lagothrix, andAlouatta; Pitheciini, including Pithecia,Cacajao, and Chiropotes; and Callitrichinae,including Callimico, Callithrix, Cebuella,Saguinus, and Leontopithecus. It has provenmuch more problematic to come to a con-sensus regarding how the specified groupsare related to each other and to the severalgenera—Cebus, Saimiri, Callicebus, andAotus—that are especially difficult to fit intoexisting schemes.

Molecular data amenable to cladisticanalysis have only been collected since1993. In the first data set to be published(Schneider et al., 1993), sequences ofnucleus-encoded å-globin genes producedhighly consistent trees and a highly resolvedconsensus diagram. However, in that paperthe relationships among Saimiri, Cebus,Aotus, and callitrichines remained unsettled,although there were strong indicationsthat these taxa form a clade. Additionof sequences of another gene, the inter-stitial retinol-binding protein gene (IRBP)intron 1 orthologues (Harada et al., 1995;Schneider et al., 1996) did not resolve thisuncertainty. Addition of mitochondrial data(part of the 16 S ribosomal gene and thecomplete 12 S ribosomal gene) to the

nuclear data set by Horovitz et al. (1998)resulted in Aotus being positioned as thebasal member of a clade otherwise formedby the set ((callitrichines) (Cebus, Saimiri)),although the support for this topology isweak. The other major clade consisted ofatelines and pitheciines, with the latterincluding Callicebus and the pitheciins.

Most branches of the molecular andmorphological trees mentioned above areshort, except for those supporting the threemajor groups, atelines (Ateles, Lagothrix,Alouatta, and Brachyteles), callitrichines(Callithrix, Cebuella, Saguinus, and Leonto-pithecus) and pitheciins (Pithecia, Cacajao,and Chiropotes). This suggests that a rapidbasal radiation of this group of primatesoccurred, and provides a plausible reasonwhy the topology of their phylogenetic tree ishighly unstable. The trees we obtained forNew World monkeys in the present studysuggest a similar conclusion.

In the present study, retrieved relation-ships are almost identical to those obtainedby Horovitz & Meyer (1997) and Horovitzet al. (1998) for morphological characters,despite the addition of three fossil taxa fromthe Caribbean. Compared to results of otherworkers, our findings correspond closely toRosenberger’s original analyses, as well asto those obtained with nuclear sequences(Schneider et al., 1993, 1996; Harada et al.,1995) and combined data sets [nuclear andmitochondrial sequences plus morphologi-cal data (Horovitz & Meyer, 1997; Horovitzet al., 1998)].

Our results also confirm our preliminaryideas (MacPhee et al., 1995) regarding thecladogeny of Greater Antillean monkeys.Thus, in this study, as in the preceding one,Callicebus emerges as the sister group ofGreater Antillean monkeys. But whereaspreviously we considered only the relation-ships of Paralouatta and Antillothrix (whichremain sister taxa, as before), we nowfind that parsimony favours the inclusionof Xenothrix within this group. We

57 PARALOUATTA VARONAI

conclude from this that the monophyly ofthe Antillean radiation can be considered tobe further confirmed, with Xenothrix as thebasal taxon and Callicebus as the mainlandsister group.

The chief biogeographical implication ofthe discovery that Greater Antillean mon-keys form a monophyletic group is obvious:it is now parsimonious to assume that onlyone primate colonization took place fromthe South American mainland, as opposedto several unrelated events invoked orimplied by previous studies. The minimumdate for this colonization event is earlyMiocene, since this is the age of the earliestprimate fossil recovered from the GreaterAntilles, the Zaza talus. However, the colo-nization could have taken place well beforethis, since Paleogene land-mammal fossilshave been recovered from Puerto Rico(MacPhee & Iturralde-Vinent, 1995) andJamaica (Domning et al., 1997).

Acknowledgements

The specimens of Paralouatta varonai dis-cussed in this paper were collected between1988 and 1996 (see Jáimez Salgado et al.,1992; MacPhee et al., 1995), and have beenincorporated into the permanent collectionsof the MNHNH. For various forms ofassistance over the years, we are happy torecord our grateful thanks to GrupoEspeleológico Pedro Borrás of the SociedadEspeleológica de Cuba, especially EfrénJáimez Salgado, Divaldo Gutiérrez Cal-vache, Rolando Crespo Díaz, and OsvaldoJiménez Vásquez, and the staff of theMNHNH, especially Manuel Iturralde-Vinent, Stephen Díaz Franco, and ReinaldoRojas Consuegra. Our thanks also go toDonald A. McFarlane for permitting us toinclude in our investigation the specimens ofXenothrix mcgregori collected by him and thejunior author. Clare Flemming also partici-pated in the fieldwork in Cuba and Jamaica.We are additionally grateful to Lorraine

Meeker (photography and Figures 1, 6, and10) and Clare Flemming (editorial assist-ance and Figure 3). Finally, we thank JohnFleagle and three anonymous reviewers forhelpful and perceptive comments on thispaper.

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Appendix 1

Character listNOTE: Characters that are multistate andnon additive are noted. All others areadditive.

60 . . . .

( 1) Offspring per birth, number (Wislocki,1939; Hill, 1926): 0=one, 1=two.Callithrix, Cebuella, Saguinus, andLeontopithecus always have dizygotictwins. Singletons occur rarely and arebelieved to be survivors of dizygoticpregnancies (Hershkovitz, 1977).

( 2) Lumbar vertebrae, number (Erikson,1963): 0=more than five, 1=five orfewer.

( 3) External thumb (Pocock, 1925):0=absent or reduced, 1=present.Thumb is nearly or completely absentas an external feature in Ateles andBrachyteles. In the latter, it is reducedto a very small metacarpal and a singlephalanx.

( 4) External tail: 0=absent (not project-ing), 1=present. External tail universalin New World monkeys; not project-ing (as coccyx) in hominoids.

( 5) Tail, ventral glabrous surface (Pocock,1925): 0=absent, 1=present. Severalgenera of New World monkeys displaydifferent degrees of prehensility intheir tails, which they use either as anadditional point of support, to suspendthemselves, and/or as a fifth memberin locomotion. However, only fourgenera (Ateles, Lagothrix, Brachyteles,and Alouatta) display a patch of nakedskin on the distal end of the ventralside of the tail. This feature is readilyrecognizable on specimens and is pre-sumably related to use in suspension.

( 6) Claws on all manual and pedal digitsexcept hallux (Buffon, 1767): 0=absent, 1=present. Of taxa consideredin this study, only five genera possessthis feature as defined. Claws andnails are both horny coverings of theterminal phalanges; they differ in thatclaws are long, sharp, laterally com-pressed, transversely convex and pro-truding, whereas nails are broad,blunt, and protrude little or not at all(Hershkovitz, 1977).

( 7) Carpo-metacarpal joint of thumb(Napier, 1961; Fick, 1911): 0=non-saddle, 1=saddle. Catarrhines possessa saddle-shaped joint; all other haplo-rhines possess conformations that arenot saddle-shaped. Napier (1961)described saddle-type articulating sur-faces as reciprocally concavo–convexin section and incongruent in at leastone plane in joint’s mid-position.

( 8) Rib cage, shape (Schultz, 1961):0=larger dorso-ventrally, 1=largerlaterally. Platyrrhines and Old Worldmonkeys differ from hominoids in thetransverse shape of their rib-cages: inmonkeys, cages are taller than theyare wide, in hominoids the reverseobtains.

( 9) Ulnar participation in wrist articu-lations (Lewis, 1974): 0=present,1=absent. In most primates excepthominoids, ulna articulates with tri-quetral and pisiform. In hominoids,ulna does not articulate with any wristbones.

(10) Sternebral proportions (Schultz,1930): 0=manubrium shorter than36% of corpus length, 1=manubriumlonger than 46% of corpus length.

(11) Orbit size (Character 4, MacPheeet al., 1995): 0=smaller than 1.9, 1=larger than 2.1. Size measured as orbitheight divided by foramen magnumwidth; definition of states takes advan-tage of gap in distribution of ratios.

(12) Postglenoid foramen (Horovitz, 1997):0=absent, 1=reduced, 2=large. Cod-ing of this character distinguishesbetween large foramina, throughwhich interior of braincase is easilyvisible, and conditions in whichforamina are reduced or absent (in-terior of braincase not visible).

(13) Tentorium cerebelli, ossification(Hershkovitz, 1977; Horovitz, 1995):0=absent, 1=present. Tentorium cer-ebelli presents some degree of ossifica-

61 PARALOUATTA VARONAI

tion in all New World monkey genera(coded as present); it is unossified inall outgroups in which this regioncould be explored (all extant outgrouptaxa used in this study, coded asabsent). Degree of ossification is vari-able, with atelines showing greatestdegree and callitrichines and Saimirithe least. Saimiri is polymorphic (someindividuals show slight ossification,others none) (see Figure 9).

(14) Middle ear, pneumatization of antero-ventral region (Horovitz, 1997):0=absent, 1=present. Anterior floor ofmiddle ear in Callithrix, Cebuella, andLeontopithecus displays typical macro-scopic consequences of pneumaticactivity (Cartmill et al., 1981). Theseinclude formation of septa, smallvacuities or cellules, and repositioningof entire sheets of bone such that shapeof internal carotid canal is revealed onfloor.

(15) Middle ear, paired prominences oncochlear housing (Horovitz, 1997):0=absent, 1=present. Lateral wall ofcochlear housing, exposed in medialwall of middle ear cavity, shows vari-able relief in New World monkeys. Insome taxa it is flat or displays a singleprominence. In others (callitrichines,Cebus, Aotus, Saimiri, Callicebus,Pithecia) there is an additional promi-nence, situated higher and more medi-ally than the first. Also presumablypresent in Apidium.

(16) Pterygoid fossa, depth (Horovitz,1997): 0=deep, 1=shallow. Pterygoidfossa is defined by medial and lateralpterygoid processs. In Paralouatta,atelines, living pitheciins, Callicebus,and callitrichines, medial pterygoidprocess is greatly reduced. Instead oforiginating from base of skull, it isrestricted to medial side of lateralpterygoid process. As a consequence,pterygoid fossa defined by these

processes is shallow, and does notexcavate base of skull.

(17) Canal connecting sigmoid sinusand subarcuate fossa (Character6, MacPhee et al., 1995) (Cartmill,1981; Horovitz, 1995): 0=absent,1=present. Present in all examinedplatyrrhines: Brachyteles scored asunknown because status could not bedetermined in material available (seeFigure 9).

(18) Vomer, exposure in orbit (Cartmill,1978; Rosenberger, 1979): 0=absent,1=present. Exposed only in Cebus andSaimiri.

(19) Ectotympanic, shape (nonadditive):0=tube I, 1=ring, 2=tube II. Catar-rhines and Tarsius display a tube-shaped ectotympanic. However, theydiffer in detail, suggesting nonhomol-ogy (scored as ‘‘I’’ and ‘‘II’’). Fordiscussion, see MacPhee & Cartmill(1986).

(20) Temporal emissary foramen(Character 7, MacPhee et al., 1995):0=present and large, 1=small orabsent (see Figure 3).

(21) Eyeball physically enclosed (Martin,1992): 0=absent, 1=present. Diam-eter of external orbital aperture issmaller than greatest internal diameterof eyeball in Callithrix, Cebuella,Leontopithecus, and Saguinus. This isso because the eyeball is physicallyenclosed by the external orbital margin(Martin, 1992).

(22) Cranial capacity (Horovitz, 1997):0=less than 15 cm3, 1=more than15 cm3. Cranial capacities of NewWorld monkey genera overlap overa wide range of values; however, agap (reflected in character definition)separates Callithrix, Cebuella, Callimico,Leontopithecus, and Saguinus (as agroup) from other genera.We use this character instead of themore traditionally used body size

62 . . . .

because the former displays an actualgap in its distribution, whereas there isa slight overlap in body size betweenSaimiri and the callitrichines.

(23) Zygomatic arch, ventral extent(Horovitz, 1997): 0=below plane ofalveolar border, 1=above plane ofborder. In most terminal taxa, entirezygomatic arch is located above toothrow. Some degree of ventral projectionmay be present, but rarely exceedslevel of plane of alveolar border (Cal-licebus, Aotus, and Xenothrix only).

(24) Pterion region, contacts (Ashley-Montagu, 1933): 0=zygomatic-parietal, 1=frontal-alisphenoid. Inplatyrrhines, zygomatic and parietalbones are almost always in contacton external surface of skull in normalateralis. In all outgroups in whichcondition is known, frontal contactsalisphenoid (see Figure 3).

(25) Nasal fossa width (Horovitz, 1997):0=narrower than palate at level of M1,1=wider. In anthropoids, nasal fossa isgenerally narrower than width of palatemeasured between lingual edges ofalveoli of M1s. By contrast, Paralouattaand Xenothrix possess unusually widenasal fossae that (at their maximumwidth) are broader than palate (seeFigure 10).

(26) Infraorbital foramen, vertical posi-tion relative to maxillary cheekteethin Frankfurt plane (Character 5,MacPhee et al., 1995): 0=above inter-val between (or caudal to) M1 and P4,1=above interval between P4 and P3,2=above (or rostral to) anteriormostpremolar (see Figure 3).

(27) Zygomaticofacial foramen, size relativeto maxillary M1 breadth (Character 1,MacPhee et al., 1995): 0=small,1=large (see Figure 3).

(28) Deciduous I2, shape (nonadditive)(Horovitz, 1997): 0=bladelike, lingualheel absent, 1=bladelike, lingual heel

present, 2=styliform, lingual heelabsent. Deciduous I2s of Callithrix andCebuella are unique among examinedhaplorhines: they are bladelike, verti-cally implanted in mandible, with flatlingual and buccal sides (no lingualheel). Deciduous incisors of Pithecia,Cacajao, and Chiropotes also lack alingual heel, but they are styliform andclosely resemble permanent ones. Allother taxa have spatulate deciduousand permanent mandibular incisorswith lingual heels.

(29) Relative height of I1–I2 (Rosenberger,1979): 0=I1 absent, 1=I1 lower thanI2, 2=I1–I2 subequal. Tarsius is onlytaxon in this analysis having a singleincisor on each side. In Callithrix,Cebuella, and Alouatta, central incisorsare lower than lateral ones; subequal inall other taxa. AMNHM Brachytelesspecimens not evaluated because teethtoo worn to interpret.

(30) Alignment of I1–I2 (Hershkovitz,1970, 1977; Rosenberger, 1979):0=transversely arcuate, 1=staggered.Hershkovitz (1970, 1977) noted that,uniquely in Callithrix and Cebuella,mandibular incisors are staggered insuch a way ‘‘that their mesiodistal axesare not linearly aligned but parallel[to] one another in a ranked, en echelonspacing’’ (Rosenberger, 1979: 107).Incisors arrayed in transverse orarcuate arrangement in all other taxa.

(31) Permanent I1–I2, shape (Rosenberger,1979): 0=spatulate, 1=styliform. Per-manent mandibular incisors of Tarsius,Callithrix, Cebuella, Pithecia, Cacajaoand Chiropotes are mesiodistally com-pressed and display no lingual heel; inall other taxa they are spatulate, with alingual heel.

(32) Mesostyles and distostyles of I1–I2(Hershkovitz, 1977): 0=absent, 1=present. Mandibular incisors inCallithrix and Cebuella display small

63 PARALOUATTA VARONAI

mesial and distal cusps flanking majorcone.

(33) Diastema between C1 and I2(Rosenberger, 1979): 0=absent, 1=present. Pithecia, Cacajao, Chiropotes,and Cebupithecia all display man-dibular diastemata large enough toaccommodate maxillary canines whentooth rows are in complete occlusion.

(34) Root of C1 shape (Character 11,MacPhee et al., 1995): 0=rounded/suboval, 1=highly compressed.

(35) Lingual cingulum on C1, complete-ness (Kinzey, 1973): 0=complete,1=incomplete or absent.

(36) Lingual crest on C1, sharpness (Kay,1990): 0=rounded, 1=sharp.

(37) Lingual cingulum on C1, mesial elev-ation of (Horovitz, 1997): 0=notelevated, 1=elevated. In most taxa,lingual cingulum of mandibularcanines is mesially elevated (i.e., cin-gular band is tilted relative to the longaxis of the tooth such that it intersectstooth’s mesial edge at higher level thanits distal edge, usually the lowest pointthe cingulum reaches).

(38) Lingual cingulum on C1, forming spikeon mesial edge of tooth (Horovitz,1997): 0=absent, 1=present. Lingualcingulum of mandibular canine termi-nates in a spikelike feature on mesialedge of tooth. In other taxa, this regionis flat, not spikelike.

(39) Buccolingual breadth of alveolus of C1compared to P4 (Horovitz, 1997): 0=C1larger than P4, 1=C1 smaller than P4.

(40) Deciduous P2, angle sub