Proc. Natl. Acad. Sci. USAVol. 88, pp. 9082-9086, October 1991Evolution

Phylogenetic and functional affinities of Babakotia (Primates), afossil lemur from northern Madagascar

(Palaeopropithecidae/primate evolution/postcranium)

WILLIAM L. JUNGERSt, LAURIE R. GODFREYt, ELWYN L. SIMONS§, PRITHUJIT S. CHATRATH§,AND BERTHE RAKOTOSAMIMANANA$tDepartment of Anatomical Sciences, State University of New York, Stony Brook, NY 117948081; tDepartment of Anthropology, University ofMassachusetts, Amherst, MA 01003; §Department of Biological Anatomy and Anthropology and Primate Center, Duke University,Durham, NC 27705; and IService de Paldontologie, Universit6 d'Antananarivo, Antananarivo, Madagascar

Contributed by Elwyn L. Simons, July 2, 1991

ABSTRACT Recent paleontological expeditions to the An-karana range of northern Madagascar have recovered thepartial remains offour individuals ofa newly recognized extinctlemur, Babakoda radofia. Craniodental and postcranial ma-terial serve to identify Babakota as a member of the palae-opropithecids (also including the extinct genera Palaeopropith-ecus, Archaeoindris, and Mesopropithecus). Living indridsform the sister group to this fossil lade. The postcranialanatomy indicates thatBabakotia was a medium-sized (=15 kg)indroid whose inferred positional behaviors were primarilyslow climbing and hanging. Although it is probable that aleaping component typified the ancestral positional repertoireof all Malagasy lemurs, the mosaic nature of the locomotorskeleton of Babakota further suggests that vertical dcimbingand hang-feeding rather than ricochetal leaping were primitivefor indrids and palaeopropithecids and that the dramaticsaltatory adaptations of the living indrids postdate the diver-gence of these two lineages.

Babakotia radofilai is the first new genus of extinct "sub-fossil" lemur to be discovered in Madagascar since 1909 (1,2). All of the fossil remains of this genus recovered to datewere found in Antsiroandoha cave in the Ankarana Range ofnorthern Madagascar (3). Field seasons from 1988 to 1990have yielded parts of four individuals, including the typespecimen at Antananarivo University (UA/LPV-8713; upperjaw plus postcranial fragments), another maxillary fragment[Duke University Primate Center (DUPC) 9144], numerousparts of a subadult (DUPC 9116), including craniodentalfragments and many postcrania, and additional fragmentarypostcrania (DUPC 9921). The dental formula 2*1*2*3 andmaxillary dental morphology clearly ally Babakotia with theindroid superfamily of Malagasy primates and more specifi-cally with indrids (Avahi, Propithecus, and Indri) and palae-opropithecids (Palaeopropithecus, Archaeoindris, and Me-sopropithecus) as opposed to archaeolemurids (Archaeole-mur and Hadropithecus) (2). However, analysis of cranialand dental characters alone has proven to be inconclusiveregarding the more precise affinities of Babakotia within theindrid-palaeopropithecid group. We believe that the postcra-nial evidence presented here serves to clarify the issue ofphylogenetic affinities and offers an opportunity to assess thelocomotor adaptation of this new genus. Taken together, theavailable information gleaned from the fossil remains ofBabakotia leads us to offer a new phylogeny for indroidprimates and an alternative hypothesis for the evolution oflocomotion and skeletal design.

Craniodental Anatomy and Tooth Shape

With an estimated body mass ofjust over 15 kg, Babakotiais a medium-sized indroid somewhat larger than the largestliving indrid (Indri) but similar in size to several of thesmallest extinct lemurs, Mesopropithecus and Pachylemur(4). A detailed description of the maxillary dentition ofBabakotia exists (2), but several important features meritmention here (Fig. 1 compares the type maxilla ofBabakotiato that of Mesopropithecus). Babakotia maxillae can bedistinguished readily from other indroids by their possessionof more laterally compressed and mesiodistally elongatedpostcanine teeth (with especially elongated upper premolarsand third molar), a prominent mesial projection of the crownof the upper anterior premolar beyond the cervix, andincipient bilophodonty of the second molar. The palate alsoappears elongate, narrow, and squared off mesially. In thislast respect, Babakotia exhibits a condition more fully de-veloped in Palaeopropithecus and Archaeoindris. As in mostindroids, the root of the zygoma begins between the first andsecond maxillary molars. The type specimen possesses avery prominent malar tubercle that is anteriorly situated(opposite the distal moiety of the first molar); in this lastrespect Babakotia is more similar to Palaeopropithecus thanto either extant indrids or Mesopropithecus.A few additional characteristics ally Babakotia generally

with the palaeopropithecids and indrids but not specificallywith any one species. The central upper incisors are largerthan the lateral and separated by a small gap; the cheek teethare laterally compressed, the premolars more so than themolars; the premolar series is about two-thirds as long as themolar series; M2 is squarer than Ml and possesses moretransversely aligned mesial and distal pairs of cusps; M3 issmaller than M1 and M2.

Similarity in overall tooth shape in Babakotia and all otherindroids [except for the newly recognized Propithecus tat-tersalli (5)] was assessed by distance measures and clusteringmethods. We first created buccolingual/mesiodistal ratios foreach tooth from the canine to last molar in all living andextinct indroids; the P2 of the three-premolared archaeole-murids was omitted to facilitate interspecific comparisons.Following standardization to Z scores to weight each ratioequally, mean shape variables for each species were used tocompute average taxonomic distances among taxa, and this13 x 13 matrix was summarized using six different clusteringalgorithms (6, 7): UPGMA, WPGMA, single linkage, com-plete linkage, and (3-flexible with B equal to 0.25 and 0.50.Most clustering methods did an excellentjob of capturing thedistance structure as reflected in cophenetic correlations

Abbreviations: DUPC, Duke University Primate Centers; UA/LPV,Universit6 d'Antananarivo/Laboratoire de Paltontologie des Ver-tebres.

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FIG. 1. Comparison (not to scale) of the maxillary dentition of the type specimen ofB. radofilai (UA/LPV-8713; Upper) to Mesopropithecusglobiceps (Laboratoire d'Anatomie Comparee, Paris; Lower). The postcanine tooth row ofBabakotia is 45 mm long; that ofthe Mesopropithecusspecimen is 31 mm long. Note the relatively long and narrow premolars of Babakotia.

around 0.9. Fig. 2 presents the strict consensus phenogram(Fig. 2A) of all six methods along with the UPGMA (Fig. 2B)and p(0.5)-flexible (Fig. 2C) solutions. The strict consensusphenogram underscores the distinctiveness of the archaeole-murids, which have relatively short and broad teeth. Thesecond major cluster unites all other indroids, which haverelatively longer and narrower postcanine teeth. Within thislatter group, the extant indrids share enough similarity intooth shape to form their own cluster regardless of methodused (as do Avahi and Indri within this cluster). The twospecies of Mesopropithecus also always cluster together asdo the large-bodied species of the Palaeopropithecus-Archaeoindris group. The findings most relevant to the issuesat hand are that Babakotia either joins the nonarchaeolemu-rid cluster as its last member (e.g., UPGMA algorithm; Fig.2B) or links to Mesopropithecus (e.g., the P-flexible algo-rithm; Fig. 2C). The former phenogram emphasizes theunique narrowing and elongation of the premolars and thirdmolar in Babakotia (and it also allies Mesopropithecus withPalaeopropithecus-Archaeoindris), whereas the latter re-flects the position of Mesopropithecus as the minimum linkto Babakotia. In sum, although Babakotia is most similar inoverall tooth shape to Mesopropithecus, the peculiarly buc-colingually compressed and mesiodistally elongated premo-lars and last molar of Babakotia serve to distinguish thisgenus from all other indroids.

Postcranial Remains and Their Affinities

The only postcrania associated with the type specimen ofBabakotia are portions ofthe shafts ofa right femur and a lefthumerus (2). The subadult skeleton (DUPC 9116) recoveredin the 1989 and 1990 field seasons includes craniodentalremains (e.g., parts of the left and right petrous portions ofthe temporal bones, the right occipital condyle, an edentulousmandibular fragment, a left M1, and some unidentified frag-ments), but its primary significance resides in the wide varietyof postcranial elements preserved. These include elements of

the axial skeleton (two partial lumbar vertebrae, one cervicalvertebra, and one caudal vertebra), parts of the upper ex-tremity (medial portion of the right clavicle, most of the leftulna, distal third of the left radius, most of the left carpus, acomplete right fourth metacarpal, a fragmentary left fourthmetatarsal, a left pollical proximal phalanx, and distal partsof two proximal phalanges) and parts of the lower extremity(the distal end of the right femur, part of the left femoraldiaphysis, a portion ofthe right greater trochanter, left fibularhead and shaft fragments, a virtually complete right calca-neus, and the distal half of one metatarsal). The 1990 fieldseason added other fragmentary shafts and right proximalfemur (DUPC 9921) to the inventory of postcranial remains.Detailed descriptions of these remains will be presentedelsewhere, but their implications for function and phylogenyserve as our focus here. Fig. 3 illustrates part of this post-cranial sample.Four regions of the locomotor skeleton are sufficiently

complete to permit a multivariate assessment of the morpho-logical affinities of Babakotia: proximal ulna, proximal fe-mur, distal femur, and lumbar vertebra. To broaden thetaxonomic and adaptive base of our comparisons, we con-trast Babakotia with two relatively large-bodied living Mal-agasy species (Indri indri and Varecia variegata) and severalextinct Malagasy lemurs, including three indroids (Palae-opropithecus maximus, Mesopropithecus, and Archaeole-mur majori) as well as Pachylemurjullyi, and Megaladapisedwardsi. For each region a suite of measurements wastaken, and shape measurements were created by dividingeach variable by the geometric mean of the entire suite (8).This resulted in 25 region-specific shape variables: 5 for theproximal ulna (olecranon lever arm, span of the sigmoidnotch, mid-sigmoid breadth, height of the proximal radioul-nar facet, and breadth of the olecranon process); 5 for theproximal femur (average femoral head diameter, breadth ofthe greater trochanter, neck height, neck breadth, and bio-mechanical neck length), 7 for the distal femur (width ofpatellar groove, biepicondylar breadth, intercondylar width,

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0.80 0.64 0.48 0.32 0.16

2.40 1.80 1.20 0.60 0.00

UPGMA , 1. indrircoph=0.9 1 Adiger

P. venTeauxM. pihecoidesM. globcepsP. ingensA fontoynontiP. maximusB. radofilalA majoriA. eduards!H. stenognathus

10.00 7.50 5.00 2.50 0.00

, -FLEXIBLErcop=0.89

C

indri

A. laniger

P. verreauxi

P. diadema

M. pihecoidesM. globicps

B. radofilalP. ingensA. fontoynontP. maxlmus

A. majoriL A. eduardsi

H. stenognathus

FIG. 2. Clustering of indroid taxa based on average taxonomicdistances derived from maxillary tooth shape. (A) Phenogram is thestrict consensus clustering from six different algorithms. (B) Pheno-gram is the UPGMA solution, which emphasizes the overall nar-rowness of the Babakotia dentition and places this species on theperiphery of the cluster formed by indrids and the remaining palae-opropithecids. (C) Phenogram is the p(O.5)-flexible solution; thismethod reduces the impact of outliers on the resulting clusters andplaces Babakotia next to Mesopropithecus (which has the minimumspanning tree link to Babakotia). The cophenetic correlation betweenthe original distance matrix and that implied by the phenograms isindicated by rph.

medial condyle breadth, lateral condyle breadth, anteropos-terior projection of the medial condyle, and anteroposteriorprojection of the lateral condyle), and 8 for the lumbarvertebra (anterior height of the body, inferior width of thebody, inferior anteroposterior diameter of the body, pedicleheight, pedicle breadth, lamina height, lamina width, andspine length; the first three vertebral body measurementsrequired some reconstruction in Babakotia).

FIG. 3. Several of the most informative elements of the partialpostcranial skeleton of Babakotia, including the ulna (a), distal halfof radius (b), most of the carpus (c), the fourth metacarpal (d), twopartial lumbar vertebrae (e), three femoral fragments (f-h), and acomplete calcaneus (i).

Following standardization, the 25 shape variables wereused to calculate an 8 x 8 average taxonomic distance matrix.Because clustering did a poorjob of summarizing this matrix,we present the results of a three-dimensional principal coor-dinates ordination in Fig. 4. The correlation between thedistances implied by this three-dimensional representationand those of the original dissimilarity matrix is 0.97, indicat-ing that most of the information is adequately summarized inthis ordination space. These three axes account for 80%o ofthe total variance (45.3%, 19.7%, and 14.5% for axes 1, 2, and3, respectively).Axis 1 separates Indri at one extreme from Palaeoprop-

ithecus at the other; in other words, leapers are maximallycontrasted with and distinguished from nonleaping, suspen-sory forms along this most important axis. Correlationsbetween shape variables and the scores on axis 1 indicate thatanimals with short lumbar spinous processes, short lumbarbodies, anteroposteriorly flattened and mediolaterally ex-panded distal femora, short biomechanical femoral necks,and short olecranon lever arms (i.e., Palaeopropithecus) arebeing differentiated from animals with the opposite charac-teristics (i.e., Indri). Babakotia occupies an intermediateposition along this axis. Axes 2 and 3 do not lend themselvesto easy functional interpretation but do highlight certainidiosyncratic features of several taxa. For example, Archae-olemur is separated maximally from Varecia along axis 2primarily on the basis of neural arch shape (pedicle andlamina heights) versus relative breadth of the medial femoral

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Babakotia

-0.77

0.73

AXIS 3 (14.5%o

is

Indri

0.58AXIS 1 (45.3%)

1.30

FIG. 4. The three-dimensional principal coordinates ordination of the average taxonomic distance matrix created from 25 region-specificshape variables. The percentage ofvariance explained by each axis is indicated. Axis 1 is the most important axis of shape variation and separatesleapers (e.g., Indri) from suspensory species (e.g., Palaeopropithecus); Babakotia occupies an intermediate position along this axis and is mostsimilar overall to Mesopropithecus.

condyle. Radioulnar facet height contributes significantly toaxis 3 and is especially large in Babakotia. In overall pheneticterms, as judged' again by minimum distance, Babakotia ismost similar to Mesopropithecus; as such, this finding recallsthe results of the dental shape analysis.A closer focus on specific traits of clearcut functional

significance (including some that do not appear in the phe-netic evaluation because they are difficult to quantify) pro-vides a clearer and complementary perspective on the adap-tive and phylogenetic affinities of the postcranium'of Baba-kotia. It also underscores the mosaic nature of indroidsimilarities and differences.The forelimb of Babakotia is in many ways a more robust

version of that seen in extant indrids-i.e., while widths andcircumferences are consistently greater, absolute lengths ofmost of the forelimb elements of Babakotia fall well withinthe range of Indri. In other important aspects of its morphol-ogy, it is quite similar specifically to palaeopropithecids.Overall robusticity is most like that seen in Mesopropithecus;this generalization is clearly true for the humerus, ulna,radius, carpus, and metacarpus. The anteroposteriorly com-pressed radial shaft flares distally; its ventral surface is quiteflat. In these features it resembles Mesopropithecus morethan Palaeopropithecus, although some degree of flatteningcharacterizes all indroids. The reconstructed maximumlength of the nearly complete ulna of Babakotia is 189 mm,within the range of Indri in spite of its greater robusticity; itis slightly longer and more robust than an undescribedspecimen of Mesopropithecus (-174 mm) from the samecave. 'The shaft of the Babakotia ulna also'shares a markedventral keel with Mesopropithecus. The carpus ofBabakotia,represented by a scaphoid, lunate, triquetrum, hamate, andcapitate, is slightly longer and much more robust than thesame region in Indri, but the overall morphology is quitesimilar (e.g., exhibiting fusion of the os centrale and sca-phoid, a relatively large hamate, and a strongly developedfacet on the triquetrum for articulation with the ulnar head).The right fourth metacarpal and pollical proximal phalanx aremore robust versions of the same bones in Indri, although,with a ratio ofphalangeal length to metacarpal length of 0.48,the pollex of Babakotia may be slightly reduced in relativelength (two Indri and two Propithecus specimens range from0.50 to 0.57).

In other aspects of upper limb anatomy Babakotia is moresimilar specifically to Palaeopropithecus than to Mesopro-

pithecus or extant indrids. As in Palaeopropithecus themetacarpal heads possess a long curvilinear surface withmaximum metacarpophalangeal curvature occurring in ex-treme flexion. This joint in Babakotia, however, lacks thehighly derived wedge-like configuration typical ofPalaeopro-pithecus. As in Palaeopropithecus and Mesopropithecus (9),the proximal phalanges (excluding the pollical one) arecurved and bear marked flexor ridges.The morphology of the hindlimb and lumbar vertebrae in

Babakotia is even more similar to Palaeopropithecus andMesopropithecus and diverges strongly from -that seen inextant indrids. For example, the femoral head is relativelylarge and more cranially oriented; as a consequence, thegreater trochanter appears reduced in height (and is relativelynarrower). The femoral diaphysis is relatively flat anteropos-teriorly; the distal epiphysis is also very expanded mediolat-erally and flattened anteroposteriorly (exceeded only byPalaeopropithecus in this respect). The patellar articularsurface of the distal femur is very broad and flat withoutelevated medial and lateral margins. The calcaneus is rela-tively short and possesses a prominent, plantar directed heelprocess like'that ofPalaeopropithecus (10). In virtually all ofthese respects, Babakotia is intermediate between Mesopro-pithecus and Palaeopropithecus.We interpret this constellation of characteristics as strong

evidence for a significant component of suspensory behavior(especially hindlimb suspension) in the positional repertoireof Babakotia. We also believe they constitute a suite ofshared derived characters that places Babakotia firmly withinthe family Palaeopropithecidae.

Conclusions

Within the palaeopropithecid clade, which we believe in-cludes Mesopropithecus, Palaeopropithecus, Archaeoindris(11), and now Babakotia, we propose that Babakotia is thesister species of the Palaeopropithecus-Archaeoindris groupand that Mesopropithecus joins this clade rather than that ofthe extant indrids (12). Despite radical differences in theirhindlimb and lumbar morphology, the indrids and the newlyconstituted palaeopropithecids can be regarded as sister taxadistinct from the archaeolemurids. This phylogenetic hypoth-esis of relationships is depicted in the cladogram of Fig. 5.The total morphological pattern of postcranial features

seen in Babakotia points to a significant commitment to

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Archaeolemur

Hadropithecus

Mesopropithecus

Babakotia

Archaeoindris

Palaeopropithecus

Propithecus

Indri

Avahi

FIG. 5. This cladogram summarizes our current hypothesis as tophylogenetic relationships among the indroid primates of Madags-car. Note that Babakotia is depicted as the sister taxon of thePalaeopropithecus-Archaeoindris clade and that Mesopropithecusis considered a member of the palaeopropithecid rather than theindrid clade.

suspensory behaviors, especially those arboreal activitiesthat involve hindlimb suspension but no leaping. Althoughnot as specialized a suspensory form as the sloth-like Palae-opropithecus (13-15), Babakotia was clearly well along thisadaptive path; as such, it provides a plausible structuralmodel for the ancestral condition of the clade that includesBabakotia, Palaeopropithecus, and Archaeoindris. Unlikeextant indrids, which climb upon, cling to, and leap betweenvertical supports and which also assume hang-feeding pos-tures (10, 16), Babakotia had clearly sacrificed its leapingcapability and instead emphasized climbing and hanging.Although we acknowledge the probability of a leaping com-ponent in the ancestral positional- repertoire of Malagasyprimates (17, 18), we propose that vertical climbing-clingingand hang-feeding rather than ricochetal leaping and bipedal

hopping were primitive for indrids and palaeopropithecids.After the separation of the two lineages, thigh-poweredvertical saltation developed as the dominant element in thelocomotor repertoire of the Indridae (19), whereas adapta-tions for slow, quadrupedal suspensory progression evolvedin the Palaeopropithecidae.

We thank the government of Madagascar and University ofTananarive for its sponsorship under which the DUPC's protocol ofcollaboration operates. We thank Martine Vuillaume-Randria-manantena for sharing unpublished data on the lumbar vertebrae ofMesopropithecus. This work would not have been possible withoutthe help of our cave guides, Salimo Golo, Christian Housseny,Raymond Antilahy, and Alphonse Tafara, and our collectors,Bodoarinivo Andrianarisoa, David Brewer, Mario Gagnon, ClaireHemingway, David Meyers, Robert Paine, Joseph Clement Rabariv-ola, Dieu Donn6 Ratsimbazafy, Jeannette Ravaoarisoa, and VerneF. H. Simons. Fig. 1 was prepared by S. Amsel; Luci Betti-Nashdrafted Figs. 2 and 4; and JeffWalker produced the cladogram in Fig.5. The research reported here was supported in 1989 and 1990 byNational Science Foundation Grant BNS-8911315 and in 1988 by theDUPC and donations from the Boise Fund, Margot W. Marsh,Gordon P. Getty, and Verna C. Simons. This is DUPC publicationno. 473.

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