The secrets of lemur teeth

ARTICLES

The Secrets of Lemur TeethLAURIE R. GODFREY,1 GARY T. SCHWARTZ,2 KAREN E. SAMONDS,3,4 WILLIAM L. JUNGERS,4 ANDKIERSTIN K. CATLETT2

Beginning three-quarters of a cen-tury ago with the pioneering work ofAdolf Schultz, primatologists have

shown a sustained interest in the skel-etal developmental correlates of pri-mate life-history variation and theirimplications for understanding theevolution of life history. More re-cently, the fossil record has been thedirect focus of such comparativework.1–6 Most fossil studies to date,constrained by the fragmentary na-ture of the fossil record and the diffi-culty in obtaining an adequate growthseries even for extant species, arebased on limited cross-sectional sam-ples. However, because teeth preservea permanent record of their develop-ment, dental microstructural analysisallows researchers to retrieve longitu-dinal developmental data from singleadult specimens. Such work hasproven useful for exploring life histo-ries of extinct species. It also promisesto revolutionize our understanding ofsome aspects of the life histories ofextant species.7–11

We have begun to apply these toolsof analysis to extinct lemurs.12–16

Dental microstructural data are nowavailable for members of threefamilies: the Palaeopropithecidae(Palaeopropithecus ingens), Archae-olemuridae (especially Archaeolemurmajori), and Megaladapidae (Megal-adapis edwardsi). We have also ex-amined other attributes of theirenamel crowns, including relativeenamel thickness and the degree ofenamel prism decussation, both pos-sible indicators of crack resistance

and correlates of diet. By combininganalysis of single individuals withanalysis of growth and dental wearacross ontogenetic series, we havebeen able to address questions neverbefore asked of extinct lemurs or,indeed, most extinct primates: Howrapidly did their molar crownsform? How dentally precocious werethey at birth? At what age did theirfirst permanent molars erupt? Atwhat age did weaning likely occur?How long was gestation? We havealso begun to chronicle the relation-ships among crown formation time(CFT), adult brain size, and adultbody size in extinct lemurs and otherprimates, and to test current hypoth-eses regarding the evolution of lifehistory in one of the world’s mostunusual adaptive radiations.14

LIFE-HISTORY RECONSTRUCTIONIN EXTINCT SPECIES: TOOLS OF

ANALYSIS

To build a chronology of dental de-velopmental “events” from which life-history profiles can be inferred, onemust document the position and tim-ing of accentuated lines in the enameland dentine for each analyzed tooth.These lines usually correspond to“stressful events.” They are simulta-neously recorded in all developingteeth and therefore can be used to reg-ister the relative degree of crown androot formation in each tooth at themoment the stressful event occurred.This technique yields a dental chro-nology for each specimen, and can beused to assess age at death of dentallyimmature individuals.12,14,17–19 Deathis taken to have occurred at the timedevelopment was terminated, as indi-cated by the last-formed portion oftooth crown or root. Age-at-death es-

1Department of Anthropology, 240 HicksWay, University of Massachusetts, Am-herst, MA 010032Institute for Human Origins, School of Hu-man Evolution and Social Change, ArizonaState University, Tempe, AZ 85287-24023Redpath Museum, McGill University,859 Sherbrooke St. West, Montreal, Que-bec, H3A 2K6 Canada4Department of Anatomical Sciences,School of Medicine, Stony Brook Univer-sity, Stony Brook, NY 11974Laurie Godfrey and William Jungers havestudied Madagascar’s extinct lemurs forover three decades and have conductedpaleontological fieldwork with Elwyn Si-mons and David Burney. Gary Schwartzstudies the incremental nature of dental tis-sue formation in extant and extinct Pri-mates. Karen Samonds studies the originand evolutionary history of Madagascar’smodern fauna, especially bats. KierstinCatlett is a doctoral student at ArizonaState University interested in comparativeprimate root development.Email addresses: [email protected] (Laurie R. Godfrey), [email protected](Gary T. Schwartz), [email protected]. (Karen E. Samonds), [email protected] (William L. Jungers),and [email protected] (Kierstin K.Catlett).

Key words: dental microstructure, subfossil le-murs, life history

© 2006 Wiley-Liss, Inc.DOI 10.1002/evan.20102Published online in Wiley InterScience(www.interscience.wiley.com).

New tools are available for teasing out aspects of life-history variation amongextinct species. Here we summarize research on the life histories of the extinctlemurs of Madagascar. There is a wide range of variation in dental developmentaltiming among these species, from among the most accelerated (Palaeopropithe-cus) to among the most prolonged (Hadropithecus) within the Order Primates.Rather than reflecting variation in body size, this diversity appears to relate to nichecharacteristics and encephalization.

Evolutionary Anthropology 15:142–154 (2006)

timates generated in this manner pro-vide a measure of “age for stage”; thatis, the pattern, sequence, and amountof tooth crown and root formationachieved at a particular age.

Dental developmental chronologiescan be used to compare the degrees ofmolar crown formation of differenttaxa at different life-history eventssuch as birth or weaning. For exam-ple, the position of the neonatal line,the prominent incremental featurethat coincides with birth,19–21 can beused to calculate the proportionalamounts of tooth crown formed pre-natally and postnatally, and to assessdental precocity at birth. The time ofemergence of the first molar (M1) is ofspecial interest, given its purportedcorrelation with other life-historyvariables.22 The best way to obtain ageat M1 emergence in extinct lemurs isto target immature individuals withM1 erupting or just erupted and rela-tively unworn. Lacking that, and as-suming we can identify a neonatal lineon M1, we can use postnatal CFT plusinformation on root extension ratesand the amount of root present atemergence to estimate age at M1 gin-gival eruption. Postnatal ages atcrown completion, coupled with esti-mates for root extension, can be usedto estimate emergence ages for secondand third molars as well.

Minimum gestation length can alsobe determined from the dental chro-nologies of fossil taxa if they have ahigh percentage of M1 crown forma-tion occurring prenatally. If it is as-sumed that calcification of the perma-nent M1 cannot begin before the endof the first trimester, the normal tran-sition from embryological to fetalgrowth phase, then the duration ofprenatal M1 CFT as determined by theposition of the neonatal line providesa minimum value for gestation length.More compelling estimates of gesta-tion length in a fossil taxon can bemade using gestation lengths for thattaxon’s closest living relatives, cou-pled with knowledge of exactly when,within those gestation periods, M1crown mineralization begins. In an-thropoid primates, mineralization ofthe permanent M1 crown normallybegins late in the third trimester; inliving lemurs, it can begin much ear-lier.

The teeth provide clues to dietaryproclivity, which in turn may corre-late with life-history variation. Twosuch indicators are relative enamelthickness (RET) and the degree ofenamel prism decussation. RET is adimensionless index commonly usedto compare enamel thickness acrosstaxa that differ in tooth size. It is cal-culated using the formula ([c/e]/�b) � 100, where “c” is the enamel capcross-sectional area (or area ofenamel exposed in the section), “e” isthe length of the enamel-dentine junc-tion (EDJ) in the exposed section, and“b” is the exposed dentine area. Rela-tively thicker enamel increases thefunctional longevity of teeth. Speciessubjecting their teeth to high occlusalloads resulting from hard food tritu-ration should possess thicker enamelthan species with softer diets.

Enamel prism decussation, the 3-di-mensional undulation of enamelprisms in and out of the plane of sec-tion as they make their way from theEDJ toward the future enamel sur-face,23–26 is difficult to quantify. It canvary qualitatively in terms of the pres-ence and morphology of Hunter-Schreger bands, the optical manifes-tations of enamel prisms undulatingand crossing over one another; it canalso vary regionally across both cus-pal and imbricational enamel. Heavydecussation is thought to enhancestructural resistance to crack propa-gation.27 Animals subsisting onharder, coarser diets exhibit a greaterdegree of decussation, particularly inthe cuspal portions of their crowns.27

As yet, no means of quantifying theprecise degree of decussation exists,but broad levels of decussation(heavy, moderate, and slight) are eas-ily recognizable and are used here tocharacterize a sample of primate mo-lars. Heavy decussation is a high de-gree of enamel prism undulationthroughout the full thickness ofenamel. Decussation is only moderateif prism undulation is not severe andoccurs only throughout one-half ofthe thickness of enamel. Slight de-cussation occurs when the enamel pri-marily comprises radial prisms run-ning fairly straight from the EDJ tothe outer enamel surface or de-cussates marginally close to the EDJ.

THE CASE OF THE SUBFOSSILLEMURS

The results reported here dependlargely on chronologies developed forthree individuals: Palaeopropithecusingens (UA AM-PPH1) from Anka-zoabo Grotte in Southwest Mada-gascar; Megaladapis edwardsi (UA4620/AM 6567) from Beloha Anavohain Southwest Madagascar; and Ar-chaeolemur majori (uncataloguedhemi-mandible) from Taolambiby,Southwest Madagascar.

The Palaeopropithecus specimen isa cranium of a juvenile individual,originally figured by Lamberton in1938.28 All but two of the permanentteeth were fully erupted at the time ofdeath; the exceptions are the canine,which is in its crypt, and the M3,which is nearly fully erupted. The de-ciduous canines are missing, butsmall alveoli located just mesial to thebuccal edge of P3 bear testimony totheir former presence. Lingual to eachis the gubernacular canal accommo-dating the tip of the permanent ca-nine. The apices of the roots of P4, M1,and M2 are closed, and M3 has sub-stantial root development. All threemaxillary molars of this immature in-dividual were sectioned. Aspects ofthe chronology derived from thosesections have been published.12,13 Ad-ditional details are provided here.

The Megaladapis specimen com-prises a partial mandible with dp4 andM1 fully erupted and M2 unerupted.The first and second molars of thisindividual have been sectioned andtheir chronology has been reported.14

The Archaeolemur specimen is a man-dible with full adult dentition; it wasfigured by its discoverer29 and aspectsof its molar microstructure have beendescribed.15 All three molars havenow been sectioned. The full chronol-ogy is reported here for the first time.

Limited microstructural data werealso collected for the extinct lemur,Hadropithecus stenognathus, on thebasis of an isolated second molar re-covered in 2003 at AndrahomanaCave in Southeast Madagascar byDavid Burney and his co-workers.15

Comparative microstructural data onextant lemurs were collected for mo-lars (M1–3) of Propithecus verreauxi(BMOC #88), Lemur catta (DPC6530F), and Varecia variegata (DPC

ARTICLES The Secrets of Lemur Teeth 143

5870F). Comparative microstructuraldata for anthropoids were taken fromthe literature or personal observations(GTS), as indicated. It goes withoutsaying that data on CFT are sparse,not merely for extinct primate speciesbut also for most extant ones, and thatintraspecific variance in CFT is poorlyunderstood. It is only with this caveatmade explicit that we take our mea-sured values of CFT in single individ-uals as “representative” for the taxa inquestion.

Molar Crown Formation Timein Subfossil Lemurs

Table 1 shows molar CFTs for threespecies of extinct lemur and severalselected anthropoids (roughly compa-rable in body mass to our extinct le-mur taxa).30 Table 2 compares theirmolar dimensions. At ca. 40–50 kg,Palaeopropithecus ingens was slightlyheavier than the largest female Pongopygmaeus, but had considerablylarger first and second molars. At ca.80–90 kg, Megaladapis edwardsi ap-proximated the mass of adult femaleGorilla gorilla; its first molars were

somewhat larger than those of femalegorillas and its second and third mo-lars were substantially so. At ca. 15–20kg, Archaeolemur majori roughlymatched the body mass of some adultmale baboons, but had slightlysmaller first and second molars andconsiderably smaller third molars.Figure 1 displays our data on the mo-lar crown developmental chronolo-gies for extinct lemurs and for Papio,the anthropoid in our comparative da-tabase with the least protracted dentaldevelopmental chronology.

Crown formation time tends to varyintraspecifically but not interspecifi-cally with molar size. Thus, CFT isroughly equal for the like-sized M1and M2 in both Palaeopropithecus andArchaeolemur, and far longer in themuch larger M2 than M1 of Megalada-pis. But M1 CFT is much shorter inPalaeopropithecus (221 days) andMegaladapis (380 days) than in themuch smaller-toothed Archaeolemur(522 days). Our only datum for the30–35 kg archaeolemurid, Hadro-pithecus stenognathus, reveals an ex-tremely long M2 CFT (2.59 years or945 days).15 This is close to recorded

M2 CFTs in Pan troglodytes and Pongopygmaeus. M1 CFT is roughly similarin Archaeolemur and Papio. For allother giant lemur molars examinedthus far, CFTs are much shorter thanin like-sized anthropoids, regardlessof molar size.

Age at Death of ImmatureIndividuals, with Implicationsfor the Pace of DentalDevelopment

Box 1 illustrates how, by construct-ing a complete chronology, includingroot formation, for M1 and M2, wedetermined the age at death, to theday, of our immature Megaladapis ed-wardsi. M2 was crown complete 442days after birth. The individual died66 days later (at 508 days, or 17months, after presumptive birth),with its M2 root partially developedbut its M2 crown unerupted. The M1

CFT is 380 days and the first molarwas crown-complete at 248 days afterbirth. In contrast, M1 of a recentlyanalyzed female gorilla was crown-complete at 1,212 days (3.3 years) af-

TABLE 1. CROWN FORMATION TIME, IN DAYS, IN EXTINCT LEMURS AND OTHER PRIMATES

Taxon M1 CFT M2 CFT M3 CFT Sources (reference numbers)

Palaeopropithecus ingens 221 246 133 12, 13Megaladapis edwardsi 380 517 (No data) 14, 16Archaeolemur majori 522 460 408 15Pongo pygmaeus 993 1267 (No data) 17Pan troglodytes 1004 1333 (No data) 16, 19Gorilla gorilla 1237 �1200 (No data) Schwartz, Dean, & Reid, unpublishedPapio hamadryas 529 559 715 31Papio cynocephalus 642 555 708 10

TABLE 2. MAXILLARY AND MANDIBULAR MOLAR MESIODISTAL AND BUCCOLINGUAL DIMENSIONS (MM) IN EXTINCTLEMURS AND LIKE-SIZED ANTHROPOID PRIMATES; MEAN IN MM (STANDARD DEVIATION)a

Taxon Jaw M1 md/bl M2 md/bl M3 md/bl

Palaeopropithecus ingens Upper 17.9 (0.7)/13.7 (1.1) 17.7 (0.9)/13.5 (1.3) 9.1 (0.5)/8.8 (0.5)Palaeopropithecus ingens Lower 18.0 (1.0)/10.3 (1.1) 17.0 (0.9)/9.5 (.7) 14.0 (0.8)/8.7 (0.7)Pongo pygmaeus, female Upper 11.9 (0.8)/12.2 (0.9) 12.1 (0.8)/12.9 (1.1) 11.5 (0.5)/12.6 (0.4)Pongo pygmaeus, female Lower 11.4 (2.7)/11.3 (0.6) 13.3 (0.6)/12.1 (0.7) 12.9 (.8)/11.8 (0.6)

Megaladapis edwardsi Upper 18.2 (1.0)/16.1 (0.6) 23.0 (1.1)/20.6 (0.8) 25.9 (1.4)/21.7 (1.0)Megaladapis edwardsi Lower 17.2 (0.6)/12.0 (0.6) 22.0 (0.9)/14.7 (0.8) 34.8 (1.5)/15.8 (0.8)Gorilla gorilla, female Upper 14.8 (0.9)/15.0 (1.1) 16.0 (0.9)/15.8 (0.8) 14.6 (0.7)/14.5 (1.2)Gorilla gorilla, female Lower 15.4 (0.8)/13.2 (0.6) 17.0 (0.9)/15.1 (0.8) 15.6 (0.6)/14.4 (0.6)

Archaeolemur majori Upper 7.8 (0.5)/9.6 (0.6) 6.8 (0.5)/8.6 (0.6) 5.8 (0.4)/7.0 (0.5)Archaeolemur majori Lower 8.0 (0.5)/8.1 (0.6) 7.6 (0.5)/8.0 (0.5) 6.6 (0.4)/7.1 (0.5)Papio cynocephalus, female Upper 10.3 (0.3)/9.3 (0.4) 11.7 (0.4)/10.9 (0.6) 11.8 (0.6)/11.2 (1.0)Papio cynocephalus, female Lower 10.1 (0.4)/8.1 (0.4) 11.6 (0.5)/9.5 (0.5) 14.3 (0.8)/10.2 (0.5)

a Molar dimensions for extinct lemurs were collected by Godfrey; molar dimensions for anthropoids (means for samples of females)are taken from Swindler.32

144 Godfrey et al. ARTICLES

ter birth, and her total M1 CFT was1,237 days. The contrast in dental de-velopmental between Megaladapis andGorilla is striking.16

Whereas we cannot directly mea-sure age at death for the other subfos-sils in our database, we can assess theages at which their third molarsreached crown completion (Table 1).For Palaeopropithecus ingens, this wasan astounding 135 days (4.2 months)after birth. For Archaeolemur majori,it was 576 days (1.6 years) after birth.For Palaeopropithecus, the third mo-lar is one of the last teeth to erupt,with only the upper canine and per-haps the anterior-most upper premo-lar erupting later. In Archaeolemur,several replacement teeth erupt afterthe third molar, including some pre-

molars and incisors, as well as the up-per canine, depending on the species.It is clear that there was tremendousvariation within the giant lemurs inage at dental maturity.

Dental Developmental Stageat Birth

Table 3 shows prenatal crown for-mation and the state of molar devel-opment at birth for our three extinctspecies, with comparative data forboth extant lemurs and selected an-thropoids. Both the timing of crowninitiation and overall CFT contributeto making crown completion rela-tively early in Palaeopropithecus andrelatively late in Archaeolemur. InPalaeopropithecus, M1 CFT is short (7

months total) and M1 initiates the ear-liest (6 months before birth), so thatM1 is crown-complete at a very youngage. In Megaladapis, M1 has a longerCFT (12.5 months) and initiates 4.5months before birth. In Archaeolemur,M1 CFT is longer yet (17 months), andit initiates less than 3 months prior tobirth. Of these three taxa, Archaeole-mur is the last to complete M1 crownformation. Also, there is an apparentphylogenetic signal, with Palaeopro-pithecus exhibiting a pattern commonin indriids, wherein all three molarsinitiate crown formation before birth,and contrasting with that of the moredistantly related Archaeolemuridae.

Age at Molar CrownCompletion and M1 GingivalEruption

Table 4 provides age at M1 crowncompletion and estimates for the ageat M1 gingival emergence for each ofthe three extinct lemurs. Gingivalemergence, the initial appearance ofthe occlusal surface as it passesthrough the gumline,35 occurs aftercrown completion but before theroots are fully formed. Roots continueto form during eruption and, indeed,after the teeth have attained full oc-clusion, as the jaws continue to growin height or depth.

Data on ages at M1 crown comple-tion and gingival emergence in an-thropoids reveal a lag of between fivemonths and a year.35 Preliminary datafor lemurs suggest a shorter lag, asso-ciated with extremely rapid root ex-tension rates (Box 2). In extant le-murs, gingival emergence oftenoccurs within a month of crown com-pletion. Cusps initiate and finish atdifferent times, as do their corre-sponding roots; therefore, roots asso-ciated with cusps that complete firstwill begin to form before the very lastportion of crown is formed. The over-lap can be great. In Propithecus ver-reauxi, for example, M1 root forma-tion begins only a few weeks afterbirth. M1 root formation initiates sev-eral weeks later, but the first molarcrowns are not fully formed until ca. 3months.14 M1 begins erupting shortlythereafter, certainly by 4 months,when the mandibular corpus height isonly slightly greater than half its total

Figure 1. Molar crown chronologies for Palaeopropithecus, Megaladapis, Archaeolemur,and Papio. The M1 CFT of Archaeolemur resembles that of Papio; both Palaeopropithecusand Megaladapis have shorter M1 CFTs.


Box 1. Mapping Out GrowthG.T. Schwartz

Box 1 Figure.

Life-history reconstruction for extinctspecies depends on our ability to deci-pher when teeth initiate their formation,how long they take to complete theircrowns and roots, and when theyemerge into the oral cavity. Buildingdental developmental chronologies al-lows us to answer questions such as:Did permanent teeth begin their forma-

tion in utero? At what age do particularteeth, such as the M1, erupt? And howmuch root is present at the time oferuption?

Using incremental growth lines, bothshort- and long-period, in enamel anddentine, we can readily pinpoint whencrowns initiate and complete forma-tion. To chart the chronology of molar

development, for example, one mustknow when each molar initiated andcompleted its crown formation relativeto the timing for each other molar; thatis, it is necessary to register all devel-oping crowns to one another. Doingso requires the use of a special classof incremental features, accentuatedlines.


adult value, and the longest roots haveattained a corresponding proportionof their full adult length. Eruption it-self proceeds rapidly, and individualswith fully erupted first molars (at fivemonths in Propithecus verreauxi) canexhibit an advanced stage of first mo-lar root formation (more than threequarters complete). At 8 months inPropithecus, all of the postcaninecheek teeth have erupted, althoughroot formation is not complete.38,39

The only giant lemur for which wehave directly measured root forma-tion time is Megaladapis edwardsi. Theroots of the M1 in this individual arelong, but their apices are not fullyclosed; we infer that the root was in itsterminal phase of growth when thisindividual died. This occurred 260days (or eight-and-a-half months) af-ter M1 crown completion at 248 dayspostnatal. Assuming a constant rootextension rate and no overlap betweencrown and root formation, this im-

plies an upper limit of just over 4months for the first 50% of root for-mation, and thus the time betweencrown completion and gingival emer-gence, assuming a similar amount ofroot formation at emergence as inPropithecus. Bracketing this further toaccount for the likelihood of variableroot extension rates, overlapping rootand crown formation, and variabledegrees of root formation at gingivaleruption, we estimate M1 gingivaleruption at not less than one and notmore than five months after crowncompletion (thus, between the ages of9 and 13 months in Megaladapis ed-wardsi; Table 4). Here, the timing ofroot extension was empirically deter-mined as part of the process of deter-mining the age at death of this imma-ture individual.14 The M2 root formedat a slower rate than did M1. After 66days of root formation, little root waspresent and the second molar wasunerupted.

Given its accelerated dental devel-opment, it is not unreasonable to as-sume that the M1 root extension ratefor Palaeopropithecus ingens was atleast as rapid as that of Megaladapisedwardsi. Using the same estimate fortime from crown completion to gingi-val emergence, and given M1 age atcrown completion of 1.1 months afterbirth, we estimate M1 gingival emer-gence at between the ages of 2–6months, and probably closer to theearly end of this range (Table 4). Thisis on a par with M1 emergence in themuch smaller-bodied Propithecus andconsiderably earlier than in like-sizedanthropoids. For example, in Pan trog-lodytes, the M1 crown is complete at985 days (2.7 years) on average,19 anddoes not erupt until ca. 3.5–4.0 years.

First-molar root extension mayhave been slower in Archaeolemur ma-jori than in Megaladapis. However, itwas probably faster than in like-sizedbaboons. M1 crown completion oc-

Box 1. Mapping Out Growth (continued)

The etiology of the striae of Retzius islargely unknown. Superimposed on thesestriae are lines that appear more markedunder transmitted polarized light. Thesecan be coincident with striae, but oftenoccur between successive Retzius lines.The etiology of accentuated lines is evenless clear; however, we do know thatthese lines chart the temporal position ofstressful episodes.33 Any single “stressful”event, which may be nutritional, physio-logical, or even psychological,34 will af-fect the cells of all developing teeth andwill therefore mark the same moment intime. To build a precise chronology re-quires cross-matching accentuated striaethat correspond to the same “stressful”event across all of the developing teeth.One special kind of accentuated line, the

neonatal line, allows us to root that chro-nology to day 0 in the life of that individ-ual; that is, to the day of birth. In thefigure, we provide an example of thistechnique using the developing dentitionof the giant subfossil lemur Megaladapisedwardsi.

Incremental lines in enamel (daily crossstriations and striae of Retzius) were usedto determine the time of initiation andcompletion for the M1 and M2 of a juve-nile specimen of M. edwardsi,14 indicatedby the two horizontal gray bars in the fig-ure. At the termination of crown forma-tion, root development begins (open hor-izontal box). The absolute timeline on thebottom reveals total crown formationtimes of 380 days and 517 days for M1 andM2, respectively. But at what point during

M1 development did M2 initiate? To an-swer that, we found a set of three accen-tuated lines, one of which is the neonatalline. We determined that these samethree lines, labeled Neonatal Line, Line A,and Line B, appear in both molars bycounting the number of daily lines be-tween each. The first line, the NeonatalLine, occurred 22 days before the secondline, Line A, which occurred 17 days be-fore the third line, Line B, in both molars.The position of these lines relative to thefirst- and last-formed enamel for eachmolar enabled us to determine the totalamounts of prenatal and postnatal molardevelopment, and thus to derive a chro-nology, rooted in real time, from 132 daysbefore birth until this individual died 640days later, at 508 days old.

TABLE 3. PRENATAL CROWN FORMATION (DAYS) IN EXTINCT AND EXTANT LEMURS AND OTHER PRIMATESa

Taxon Prenatal M1 CFT Prenatal M2 CFT Prenatal M3 CFT

Palaeopropithecus ingens 187 days (6 months) 111 days 24 daysMegaladapis edwardsi 132 days (4.5 months) 75 days —Archaeolemur majori 85 days (3 months) None NonePropithecus verreauxi 94 days 56 days 16 daysLemur catta 67 days None NoneVarecia variegata 55 days None NonePongo pygmaeus 24 days (�1 month) None NoneGorilla gorilla 25 days (�1 month) None NonePapio hamadyras 36 days (1 month) None None

a Sources for data are given in Table 1.


curs in the Archaeolemur majori indi-vidual at 437 days (14.6 months) afterbirth. It occurs in like-sized baboonsabout two months later; for example,493 days, 511 days. In baboons, thefirst molar erupts at around 20months.35 We project a slightly earliereruption in Archaeolemur (Table 4).Whereas age at M1 emergence is sim-ilar in the two, the whole dental erup-tion chronology was certainly lessprotracted in Archaeolemur than inPapio, given that M3 is crown-com-plete in the former at 19 months, butnot until 5.71 years in Papio.31 Never-theless, the contrast is not as stronghere as it is between other giant lemurspecies and like-sized anthropoids. Atleast for M1 emergence, the differencebetween Archaeolemur and baboonsappears to have been minimal.

Given the rapidity of root formationin extant lemurs for which we havedata, it is reasonable to assume thatgingival emergence occurs within afew months of crown completion, andthat age at gingival emergence is cor-related with age at crown completion.It follows that, in comparison to like-sized anthropoids, giant lemurs ex-hibited relatively early gingival emer-gence, and that this was particularlythe case for Palaeopropithecus andMegaladapis, the largest-bodied of ex-tinct lemurs in our sample.

Age at Weaning, JuvenileForaging, and Acquisition ofAdult Diet

There is no simple way to infer ageat weaning in extinct species. Smith22

noted a correlation among Primatesbetween age at weaning and age at M1eruption. This relationship holdspoorly, however, for lemurs.38,39

There may be a trace element or iso-topic signal of weaning,40–44 but re-search along these lines for subfossillemurs is very preliminary.

Another strategy is to examinetooth wear across ontogenetic series.Flanagan15,45 examined microwearunder low magnification for ontoge-netic series of Macaca fascicularis andArchaeolemur spp. For Macaca fas-cicularis, she could map life-historylandmarks such as weaning and sex-ual maturation on the microwear on-togeny, as the schedule for dentaleruption is well known for this spe-cies. Flanagan observed an increase inpit and scratch counts per unit areafrom early to later infancy, leveling offafter M1 comes into occlusion. This isfollowed by a prolonged period duringwhich feature counts remain rela-tively stable. This is apparently a post-weaning juvenile foraging phase. Mi-crowear feature counts do notincrease until around sexual matura-tion, at which time adult values fortheir range and frequencies are man-ifested. Interestingly, Archaeolemurshows the same pattern, including aprolonged phase before dental adult-hood during which scratch counts,particularly hypercoarse scratchcounts, remain relatively low.15 Mi-crowear feature counts and variabili-ties are higher for individuals withfull adult dentitions than for dentallyimmature individuals. Nevertheless,whereas Archaeolemur youngsterswith only M1 erupted do not exhibit afull adult signal for scratches and pits,they do show moderately high fre-quencies of both. It may be reasonableto assume that weaning occurred inArchaeolemur, as in macaques, ataround the age of M1 eruption at ca.15–19 months, and that youngstersexperienced a prolonged period there-after during which they slowly ac-quired full adult foraging skills.

In contrast, in Megaladapis, by thetime M1 comes into full occlusion andbegins to wear, which certainly is be-fore 17 months and likely before 13months of age, the microwear signal

cannot be distinguished from that offull adults. This suggests an earlierage for acquisition of adult foragingskills.16 We project an even earlier agefor acquisition of adult foraging skillsin Palaeopropithecus on the basis of itsextremely rapid dental development.As in Propithecus, it is likely thatPalaeopropithecus was dentally preco-cious at weaning and, shortly thereaf-ter, was handling tough, fibrous foods.Half-year old Propithecus have full per-manent teeth and are weaned; weaninggenerally begins at between 4 and 5months. New weanlings may subsistlargely on young leaves and other foodsthat are available during the season ofplenty, but the full adult repertoire isacquired within a few months, duringthe season of scarce resources.

In summary, relatively early wean-ing can be inferred for larger-bodiedspecies, even if we assume that wean-ing did not occur until after young-sters had erupted many of their per-manent teeth. There is evidence ofprolonged acquisition of adult forag-ing skills in Archaeolemur and of rapidacquisition of adult foraging skills inMegaladapis and especially Palaeopro-pithecus.

Brain Growth in Giant Lemurs

With some reconstruction of theposterior portion of the neurocra-nium, we were able to estimate thecranial capacity of our immaturePalaeopropithecus ingens at 65–70 cc.Full adult Palaeopropithecus ingensaverage a capacity of 101 cc. There islittle question that individuals at thestage of dental development repre-sented by the Palaeopropithecus indi-vidual described here, which has fulladult dentition except the upper ca-nine, would have been weaned. Cra-nial capacity at weaning was perhapswell under 65% of the adult value.

We also measured the cranial ca-pacity of an immature Megaladapis ed-wardsi (AM-MGH2/UA 5491) at a den-tal developmental stage slightly moreadvanced than that of the 17-monthold individual from which we derivedour dental developmental chronology(Fig. 2). At death, AM-MGH2 had anerupting M2; in all other features(fully erupted M1, unreplaced decidu-ous teeth) the dental development ofthe two was comparable. The mea-

TABLE 4. ESTIMATED AGE AT M1 ERUPTION FOR EXTINCT LEMURS

TaxonAge at M1 CrownCompletion Age at M1 Eruptiona

Palaeopropithecus ingens 34 days (1.1 months) �2–6 monthsMegaladapis edwardsi 248 days (8.3 months) �9–13 monthsArchaeolemur majori 437 days (14.6 months) �15–19 months

a Estimated as age at M1 crown completion plus 1–5 months.


Box 2. Getting to the Root of the MatterK.K. Catlett and K.E. Samonds

Box 2 Figure. Image of Hadropithecus stenognathus RM2 illustrating variables used toobtain RERs (see text). Angle I (dotted line) is formed between the developing rootsurface and a dentine tubule (DT) where they intersect an accentuated growth line(AGL). Angle D (solid line) formed by the intersection of AGL with the root surface.

Whereas recent histological re-search on molar crown formationtimes has greatly aided reconstruc-tions of extinct lemur life histories,these studies have largely ignored theincremental data preserved withindeveloping roots. Long and short in-cremental lines preserved in dentineenable researchers to reconstruct thetiming and sequence of root develop-ment, just as similar lines preserved inenamel allow the reconstruction ofcrown development. Because root ex-tension continues well after crowncompletion, the daily incremental linespreserved in roots allow the interpola-tion of aspects of growth that occurduring eruption and even much later inan individual’s life. Roots also provideresearchers with increased opportuni-ties to correlate “events” histologicallyrecorded in different teeth, which iscrucial for constructing comprehensivedental chronologies. We have begun touse such histological techniques, alongwith dissection and radiographic anal-ysis, to expand our knowledge of lemurdevelopment.

Shellis36 developed a geometricformula, c � d[(sin I/tan D) � cos I)],using the cell secretion rate (d) andprism direction to calculate the exten-sion rate, c, of imbricational enamel.The similar nature of enamel and den-tine secretion makes Shellis’ equationalso appropriate for estimating rootextension rates (RERs) for any lengthof root.18 To determine d, the dailydentine secretion rates (DSRs), onemust take several measurementsacross long-period dentine lines anddivide by the periodicity.

Using these techniques, we calcu-lated the average RER for the M1 in aPropithecus verreauxi (BMOC #88) tobe approximately 29.8 �m/day with anaverage DSR of 3.0 �m/day. Theserates suggest that approximately 175days were required to grow 4.8 mm ofmeasurable root. The calculated M1RERs for both extant and extinct an-thropoid species (other than humans)range from 5.20 �m/day in Hylobateslar37 to 19.40 �m/day in Proconsul.18

Regardless of body size, it is clear thatPropithecus has not only acceleratedenamel development,14 but also ex-tremely rapid root development.

We also devised a scoring technique

to compare measurements from radio-graphs and from extracted teeth of thesame individuals to attain stages ofroot formation for an ontogenetic seriesof known-aged specimens. The stagescorrespond to percentages of develop-ing root lengths calculated againstadult root lengths, determined by directmeasurement of extracted teeth. Usingthis technique, we scored mandibularmolars for a series of Varecia variegataand Propithecus verreauxi ranging fromnewborn individuals to dental adults.Results indicate that in Propithecus, M1

roots reach 29% of adult root length atonly 2.5 months of age, while Vareciarequires an additional 100 days toreach a comparable stage of M1 rootdevelopment. In Propithecus, M1 gingi-val emergence, estimated to occur at�3–4 months, closely follows the initi-ation of M1 root formation. The amountof root formation at M1 alveolar emer-

gence is relatively consistent betweenspecies, with mesial roots at �35% ofadult length and distal roots at �45%of adult length by the time M1 hasstarted to cross the alveolar plane.

These results suggest that chartingroot extension rates and formationtimes will enhance our ability to gleandental developmental information froman individual’s entire dentition. Histo-logical research on root dentine pro-vides longitudinal data that can assistin refining our understanding of theamount of daily root growth, informa-tion not captured in radiographs from across-sectional sample. Such analyseswill enable us to compare the pace oflemur and similarly sized anthropoidtooth root development to determinehow much root is present at the time oferuption and how much time is re-quired for lemur tooth roots to achieveapical closure.


sured cranial capacity, 90 cc, was ca.65% of the adult value of 137 cc forMegaladapis edwardsi. If we are cor-rect in inferring that individuals atthis stage of dental development hadbeen weaned, this implies a small cra-nial capacity for Megaladapis edwardsiat weaning as well.

Both Palaeopropithecus and Megal-adapis bear testimony to a phenome-non that is not manifested in anthro-poids: relatively slow acquisition ofadult cranial capacity with respect todental development and weaning.Typically among anthropoids, cranialcapacity is at 90%–95% of the adultvalue at weaning.46–51 Clearly, thiswas not the case for Palaeopropithecusor Megaladapis.

To better understand this phenome-non, we collected cranial capacitygrowth trajectories for living strepsir-rhines. Between 4 and 6 months, thecranial capacities of Propithecus in-crease from 65% to 75% of their adultvalue. This is far less than the 90%–95%of adult cranial capacity typical of an-thropoid weanlings. This phenomenonin sifakas is part of the “fast teeth-slowgrowth” pattern described by Godfreyand colleagues,39 and was evidentlyshared, to varying degrees, by Palaeo-propithecus and Megaladapis.

In contrast, Varecia variegata at-tains 65% of adult cranial capacity atless than 3 months. At 6 months, afterweaning but before any permanentteeth, including M1, have erupted, its

brain measures �95% of the adultvalue. Varecia weanlings may not have90% of their adult cranial capacityquite yet, but their brain growth tra-jectory is well ahead of their dentaldevelopmental trajectory. In otherwords, Varecia exhibits, in stark con-trast to Propithecus, slow teeth-fastgrowth.

Preliminary data for Archaeolemursuggest a pattern more similar to thatof Varecia than Propithecus. Thismatches expectations derived fromstudies of other aspects of craniofacialgrowth.5,6 Archaeolemur exhibits a rel-atively rapid pace of craniofacialgrowth when benchmarked againstdental development. Thus, it appearsthat Megaladapis and especially Paleo-propithecus, giant lemurs with rela-tively rapid dental development, expe-rienced relatively slow brain growth,while the opposite applied to specieswith relatively slow dental develop-ment such as Archaeolemur. It also isinteresting to note that the archaeole-murids are the only larger-bodiedlemurs that even approach anthro-poid-like brain-body relationships.14

Palaeopropithecus and Megaladapishave very small brains for their adultbody size.

Gestation Length

Schwartz and colleagues12 used theposition of the neonatal line, and thusthe inferred time in utero that M1 be-gan forming, to estimate gestationlength for Palaeopropithecus ingens.Their estimate of over 9 months mustbe regarded as a theoretical mini-mum; it is based on the assumptionthat no part of M1 crown formationcan occur during the embryonicphase of gestation—essentially thefirst third. Table 5 shows estimates ofgestation length for Megaladapis, Ar-chaeolemur, and Palaeopropithecus,using this theoretical minimummethod as well as models based onextant-lemur analogs. For example, amodel based on Propithecus verreauxi

Figure 2. Specimens of Megaladapis edwardsi used in analysis of dental microstructure andendocranial growth. A. Buccal view of the left hemi-mandible of a juvenile specimen (UA4620/AM 6567) illustrating the erupted dp4 and M1, and the M2 in crypt. B. Buccal view of theunerupted M2 after removal from the crypt. The arrow points to the few millimeters of initialroot formation. C. Lingual view of hemi-mandible showing dp4 and M1. D. Cranium ofMegaladapis edwardsi (AM-MGH2). Scale bar � 10 cm.

TABLE 5. RECONSTRUCTING GESTATION LENGTH, IN DAYS, IN EXTINCT LEMURS

TaxonPrenatal M1CFT

MinimumModel

PropithecusModel

VareciaModel Lemur Model

Palaeopropithecus ingens 187 279 317 346 381Megaladapis edwardsi 132 197 224 244 269Archaeolemur majori 85 127 144 157 173


begins with the observation that ges-tation averages 158 days in this spe-cies38,52 and that molar crown forma-tion begins �94 days prior to birth(our data for BMOC #088, Propithecusverreauxi from Beza Mahafaly). A Pro-pithecus model assumes that M1crown formation occupies the sameproportion of overall gestation in theextinct taxon as it does in Propithecus.This proportion is calculated as theobserved prenatal crown formationtime divided by the observed gestationlength (in Propithecus, 94/158 � 0.59).To calculate the estimated gestationtime in the extinct species, the ob-served prenatal CFT is divided by thisratio; for example, for Palaeopropithe-cus ingens, 187 days/0.59 � 317 daysor, 10.5 months. Gestation lengths inextant lemurids are much shorterthan in Propithecus, ca. 102–136 daysfor the largest-bodied lemurids.53–55

Also, the proportion of the gestationperiod during which M1s are develop-ing is smaller. A Varecia model (gesta-tion length of 102 days and prenatalcrown formation time of 55 days)yields a ratio of 0.54; a Lemur cattamodel (gestation length of 136 daysand a prenatal crown formation timeof 67 days) yields a ratio of 0.49.

M1 crown formation time in Palaeo-propithecus ingens is 221 days, with187 prenatal days of crown forming.

Even if M1 crown mineralization in P.ingens began at the end of the firsttrimester, our theoretical minimum,gestation length would have had to belonger than 9 months. Using a Pro-pithecus model, gestation in Palaeo-propithecus is estimated at 10.5months. Using extant lemurids as amodel for P. ingens would result in farlonger and probably unrealistic esti-mates of gestation length (12.5months), underscoring the impor-tance of using the appropriate mod-ern analog in our analyses. We take amodel based on the theoretical mini-mum or the Propithecus model as themost appropriate for Palaeopropithe-cus and therefore estimate gestationlength as 9–11 months (Table 5).

The theoretical minimum is muchshorter for Megaladapis edwardsi (6.5months) and Archaeolemur majori (4.2months) (Table 5). Applying a lemuridmodel to these species, we derive ges-tation estimates of 8–9 months forMegaladapis and 5–6 months for Ar-chaeolemur. Gestation would havebeen longer in Archaeolemur only if itsdental developmental trajectory wasmore similar to those of anthropoids,which initiate M1 crown formationcloser to birth.14

In summary, gestation was notshort in giant lemurs, a phenomenonthat may reflect their early initiation

of molar crown formation. Indeed,there is credible evidence that the ges-tation period was longer in Palaeopro-pithecus ingens than in humans,which is all the more remarkablegiven that this is a species with one ofthe most rapid dental developmentaltrajectories of all primates.

Dental Structural Indicators ofTrophic Adaptations

Enamel prism morphology and therelative thickness of the enamel varywidely across extant and extinct le-murs (Table 6). They provide strongevidence of a coarse diet with hard-object processing in Archaeolemur,but not in Megaladapis or Palaeopro-pithecus.15,58 For these two indicatorsof diet, nearly all extant lemurs aresimilar to Megaladapis and Palaeopro-pithecus, with only Daubentoniamadagascariensis exhibiting relativelythick enamel (RET � 21.7).59 In Ar-chaeolemur, molar enamel prism de-cussation and relative enamel thick-ness are no less than remarkable (Fig.3; Table 6). Only a few extant pri-mates, including the omnivoroushard-object processor Cebus apella,have molars that combine thickenamel and well-defined Hunter-Schreger bands, suggesting enhancedresistance to high occlusal loads and

TABLE 6. MACRO- AND MICROSTRUCTURAL INDICATORS OF TROPHIC ADAPTATIONS IN EXTINCT LEMURSAND OTHER PRIMATES

TaxonCuspalDecussationa

ImbricationalDecussationa

R.E.T. (Means and Range, WhenAvailable)b

Varecia variegata 1 1 5.7Lemur catta 1 1 7.3 (6.7–8.1)Gorilla gorilla 1 1 10.0 (6.8–13.4)Pan troglodytes 1 1 10.1 (7.0–13.3)Propithecus verreauxi 1 1 10.7Palaeopropithecus ingens 1 1 11.3Megaladapis edwardsi 1 1 13.7 (10.6–16.0)Papio cynocephalus 1 1 15.4 (12.4–18.6)Pongo pygmaeus 1–2 1 15.9 (11.3–20.5)Hadropithecus stenognathus 2 1 14.4 (13.9–15.2)Cebus apella 2 2 19.2Archaeolemur majori 3 3 28.3 (24.9–35.2)Archaeolemur sp. cf. edwardsi 3 3 30.6 (25.7–35.2)Paranthropus boisei 3 3 34.9 (31.0–38.6)

a Decussation 1 � slight or none, 2 � moderate, 3 � heavyb Relative enamel thickness: ([c/e]/� b) � 100. See text for explanation. RET data for Palaeopropithecus, Archaeolemur, andHadropithecus are taken from Godfrey and coworkers.15 Data for Megaladapis are new, and are combined for M1 and M2. Allother data are taken from references Schwartz, Liu, and Zheng56 and Smith, Martin, and Leakey57 and are means based on RETvalues for M1–M3. Recent work68 documents metameric variation in enamel thickness in hominoids. However, these differencesare trivial in comparison to the variation in subfossil and extant strepsirrhines.


crack propogation. Pitheciins (Caca-jao, Chiropotes, and Pithecia) havewell-defined Hunter-Schreger bandsbut relatively thinner enamel and are,in this manner, more like Hadropithe-cus.60 Certain extinct anthropoidshave striking microstructural similar-ities to Archaeolemur, including Grae-copithecus freybergi and Paranthropusspp.61

LESSONS FROM THE LEMURS

The data described here underscorea remarkable diversity of developmen-tal patterns in the lemurs of Madagas-car.6,38,62–64 In many ways, dental de-velopment in Palaeopropithecus isvery like that of indriids: Palaeopro-pithecus is on a par with or even“ahead” of Propithecus in its scheduleof molar crown formation and dentalprecocity at birth. As in Propithecus,“fast” teeth are apparently accompa-nied by slow craniofacial growth.Many of the craniofacial correlates ofdental precocity in indriids, includingdiminutive milk teeth, crowding ofunerupted and newly erupted teeth,and dissociation of the rates of cranio-facial and dental development, aremanifested in Palaeopropithecus.6 Weadd to this list the observation that

brain growth was slow in Palaeopro-pithecus, as it is in Propithecus.

Only a single deciduous tooth (adp4) is known for any individual be-longing to a palaeopropithecid spe-cies, including Palaeopropithecus andits closest relatives Archaeoindris, Me-sopropithecus, and Babakotia. Thisalone suggests rapid passage throughthe milk-tooth stage of dental develop-ment. The known deciduous tooth,belonging to a very young Palaeopro-pithecus ingens (DPC 17307), wasfound in association with additionalloose teeth, including an M1 and M2,P4, M1, and P4. The state of develop-ment of the M1, a crown with no rootformation, suggests that this individ-ual was not more than one month oldat death. M1 is crown-complete andhas some root formation. The dp4 hasroots and exhibits some macrowear.The M2 has no roots but is at an ad-vanced stage of crown development,as is P4. A second, somewhat older,infant Palaeopropithecus ingens (DPC18750) is represented by a left maxillaand associated partial mandible. Themaxilla has an erupted M1, eruptingP4, and full crowns of P3 and C1, with-out roots, in their crypts. The roots ofM1 are not fully formed. The secondand third molars are missing. The

mandibular molars are missing buttheir sockets suggest that they had orwere erupting and had partial roots.

These specimens establish that thepremolars erupt from back to front, asin indriids, that month-old infantswere processing solid food, and thatthe crown of the upper canine, the lasttooth to erupt, had fully formed be-fore the precocious first molar hadcompleted its root formation. Theeruption sequence manifested inthese individuals matches that exhib-ited by some Propithecus. It is possiblethat the entire chronology of dentaldevelopment in Palaeopropithecuswas very like those of extant indriids,and that, as in extant indriids, Palaeo-propithecus was born with all decidu-ous teeth erupting or erupted.

Megaladapis also shows rapid den-tal development, but was not as pre-cocious at birth as was Palaeopro-pithecus or extant indriids. In fact, weknow that Megaladapis, like lemurids,was born without its deciduous teethfully erupted. The youngest knownMegaladapis (DPC 17150) has an une-rupted dp4 lacking roots but a fullyerupted dp3 with roots. The crypt forM1 is present but broken and the M1

crown is missing. Because the distalportion of the corpus is also missing,it is impossible to tell the state of de-velopment of the second or third mo-lars.

Specimens of Archaeolemur spp.and Hadropithecus stenognathus sug-gest very different scheduling of devel-opmental events. Numerous knownarchaeolemurid specimens bear milkdentitions, which appear to have en-dured for a prolonged period beforethey were replaced. There is no dimi-nution of the milk teeth; indeed, thedp4s in both maxilla and mandible arealmost as large in the occlusal area asare the M1s.6 In effect, they serve asfunctional substitutes for M1 beforefull eruption of the latter, which wenow know did not occur until 15months or later.15 Microstructuraldata confirm a prolonged infancy inArchaeolemur prior to the onset of theeruption of the permanent dentition.Microwear data suggest a prolongedperiod of juvenile foraging followingweaning. The pattern of slow growthand fast teeth, manifested so strik-ingly in Palaeopropithecus, does not

Figure 3. Heavy enamel prism decussation in Archaeolemur.


characterize Archaeolemur. Instead,Archaeolemur exhibits a growth pat-tern more like that of lemurids, withrelatively rapid somatic growth andslow dental development, but moreextreme.5,39

We can now draw preliminary in-ferences regarding the overall patternof growth and development in large-bodied lemurs. We know that Palaeo-propithecus and Megaladapis, the gi-ant lemur species with the largestmolars, do not have the longest CFTs.There is no tendency, as there isamong anthropoids, for large-bodiedspecies to exhibit slow growth and de-velopment while small-bodied speciesexhibit rapid growth and develop-ment. Instead, there is evidence of anecological divide, with the hard-objectprocessors, the archaeolemurids,exhibiting relatively slow dental devel-opment, while other species (Palaeo-propithecus especially and Megalada-pis somewhat) have relatively rapiddental development. The former is as-sociated with relatively rapid acquisi-tion of adult skull and brain size. Theformer is also associated with rela-tively high adult encephalization,while the latter is associated with lowadult encephalization.15 The patternmanifested in Palaeopropithecus andMegaladapis appears to have been as-sociated with early acquisition offood-processing independence. Thepattern manifested in Archaeolemurappears to have been associated withprolonged acquisition of complexfood-processing skills. The parallelhere with Daubentonia madagascar-iensis is striking.65,66 This is the onlyliving lemur with relatively high en-cephalization, and with a microwearand enamel thickness signature simi-lar to Archaeolemur.56,64,67

The econiche characteristics of theprimate communities of Madagascarhave changed dramatically with thedisappearance of nearly one-third oftheir species, including all speciesgreater than 9 kg in body mass. Bydrawing appropriate comparisons be-tween the extinct lemurs and theirmuch smaller-bodied extant relatives,we will be able to develop a compre-hensive understanding of the influ-ence of body size and phylogeny onvariation in development and life-his-tory strategies in these species. We

can better understand how diet pre-dicts life-history strategy. By com-paring the giant lemurs to like-sizedanthropoids, we gain a better under-standing of the phylogenetic baggagethese species carry. Why did the large-bodied species disappear? To separatefact from fiction, we must do a betterjob than has been done in the past ofreconstructing the niche characteris-tics of these extinct species and, towhatever extent possible, their life-history strategies.

ACKNOWLEDGMENTS

This work was supported by NSFGrants BCS-0237338 to LRG, BCS-0503988 to GTS, and BCS-0129185 toDavid Burney, LRG, and WLJ. Wegratefully acknowledge the help ofJohn Fleagle and three reviewers, andof the many people who contributedto this work, including Frank Cuozzo,Erin Flanagan, Gina Semprebon,Patrick Mahoney and, particularly,our Malagasy hosts (Gisele Randria,the late Berthe Rakotosamimanana)and colleagues in the field.

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The secrets of lemur teeth