The Secrets of Lemur Teeth

Evolutionary Anthropology 15:142–154 (2006)

ARTICLES

LAURIE R. GODFREY,1 GARY T. SCHWARTZ,2 KAREN E. SAMONDS,3,4 WILLIAM L. JUNGERS,4 AND KIERSTIN K. CATLETT2

New tools are available for teasing out aspects of life-history variation among and correlates of diet. By combining extinct species. Here we summarize research on the life histories of the extinct analysis of single individuals with lemurs of Madagascar. There is a wide range of variation in dental developmental analysis of growth and dental wear timing among these species, from among the most accelerated (Palaeopropithe- across ontogenetic series, we have cus) to among the most prolonged (Hadropithecus) within the Order Primates. been able to address questions never Rather than reflecting variation in body size, this diversity appears to relate to niche before asked of extinct lemurs or, characteristics and encephalization. indeed, most extinct primates: How rapidly did their molar crowns form? How dentally precocious were Beginning three-quarters of a cen- shown a sustained interest in the skel- they at birth? At what age did their tury ago with the pioneering work of etal developmental correlates of pri- first permanent molars erupt? At Adolf Schultz, primatologists have mate life-history variation and their what age did weaning likely occur? implications for understanding the How long was gestation? We have evolution of life history. More re- also begun to chronicle the relation- cently, the fossil record has been the ships among crown formation time (CFT), adult brain size, and adult 1Department of Anthropology, 240 Hicks direct focus of such comparative Way, University of Massachusetts, Am- work.1–6 Most fossil studies to date, body size in extinct lemurs and other herst, MA 01003 primates, and to test current hypoth- 2 constrained by the fragmentary na- Institute for Human Origins, School of Hu- eses regarding the evolution of life man Evolution and Social Change, Arizona ture of the fossil record and the diffi- State University, Tempe, AZ 85287-2402 culty in obtaining an adequate growth history in one of the world’s most 3Redpath Museum, McGill University, unusual adaptive radiations.14 859 Sherbrooke St. West, Montreal, Que- series even for extant species, are bec, H3A 2K6 Canada based on limited cross-sectional sam- 4 Department of Anatomical Sciences, ples. However, because teeth preserve School of Medicine, Stony Brook Univer- LIFE-HISTORY RECONSTRUCTION sity, Stony Brook, NY 11974 a permanent record of their develop- IN EXTINCT SPECIES: TOOLS OF Laurie Godfrey and William Jungers have ment, dental microstructural analysis studied Madagascar’s extinct lemurs for ANALYSIS over three decades and have conducted allows researchers to retrieve longitu- paleontological fieldwork with Elwyn Si- dinal developmental data from single To build a chronology of dental de- mons and David Burney. Gary Schwartz adult specimens. Such work has studies the incremental nature of dental tis- velopmental “events” from which life- sue formation in extant and extinct Pri- proven useful for exploring life histo- history profiles can be inferred, one mates. Karen Samonds studies the origin ries of extinct species. It also promises must document the position and tim- and evolutionary history of Madagascar’s modern fauna, especially bats. Kierstin to revolutionize our understanding of ing of accentuated lines in the enamel Catlett is a doctoral student at Arizona some aspects of the life histories of and dentine for each analyzed tooth. State University interested in comparative extant species.7–11 These lines usually correspond to primate root development. Email addresses: [email protected]. We have begun to apply these tools “stressful events.” They are simulta- edu (Laurie R. Godfrey), [email protected] of analysis to extinct lemurs.12–16 neously recorded in all developing (Gary T. Schwartz), Karen.Samonds@mail. Dental microstructural data are now mcgill.ca. (Karen E. Samonds), william. teeth and therefore can be used to reg- [email protected] (William L. Jungers), available for members of three ister the relative degree of crown and and [email protected] (Kierstin K. families: the Palaeopropithecidae root formation in each tooth at the Catlett). (Palaeopropithecus ingens), Archae- moment the stressful event occurred. olemuridae (especially Archaeolemur This technique yields a dental chro- majori), and Megaladapidae (Megal- nology for each specimen, and can be Key words: dental microstructure, subfossil lemurs, life history adapis edwardsi). We have also ex- used to assess age at death of dentally amined other attributes of their immature individuals.12,14,17–19 Death enamel crowns, including relative is taken to have occurred at the time © 2006 Wiley-Liss, Inc. enamel thickness and the degree of development was terminated, as indi- DOI 10.1002/evan.20102 Published online in Wiley InterScience enamel prism decussation, both pos- cated by the last-formed portion of (www.interscience.wiley.com). sible indicators of crack resistance tooth crown or root. Age-at-death es- ARTICLES The Secrets of Lemur Teeth 143 timates generated in this manner pro- The teeth provide clues to dietary THE CASE OF THE SUBFOSSIL vide a measure of “age for stage”; that proclivity, which in turn may corre- LEMURS is, the pattern, sequence, and amount late with life-history variation. Two of tooth crown and root formation such indicators are relative enamel The results reported here depend achieved at a particular age. thickness (RET) and the degree of largely on chronologies developed for three individuals: Palaeopropithecus Dental developmental chronologies enamel prism decussation. RET is a ingens (UA AM-PPH1) from Anka- can be used to compare the degrees of dimensionless index commonly used zoabo Grotte in Southwest Mada- molar crown formation of different to compare enamel thickness across gascar; Megaladapis edwardsi (UA taxa at different life-history events taxa that differ in tooth size. It is cal- 4620/AM 6567) from Beloha Anavoha such as birth or weaning. For exam- culated using the formula ([c/e]/͌ in Southwest Madagascar; and Ar- where “c” is the enamel cap ,100 ء (ple, the position of the neonatal line, b chaeolemur majori (uncatalogued the prominent incremental feature cross-sectional area (or area of hemi-mandible) from Taolambiby, that coincides with birth,19–21 can be enamel exposed in the section), “e” is Southwest Madagascar. used to calculate the proportional the length of the enamel-dentine junc- The Palaeopropithecus specimen is amounts of tooth crown formed pre- tion (EDJ) in the exposed section, and a cranium of a juvenile individual, natally and postnatally, and to assess “b” is the exposed dentine area. Rela- originally figured by Lamberton in dental precocity at birth. The time of tively thicker enamel increases the 1938.28 All but two of the permanent emergence of the first molar (M1) is of functional longevity of teeth. Species teeth were fully erupted at the time of special interest, given its purported subjecting their teeth to high occlusal death; the exceptions are the canine, correlation with other life-history loads resulting from hard food tritu- which is in its crypt, and the M3, variables.22 The best way to obtain age ration should possess thicker enamel which is nearly fully erupted. The de- at M1 emergence in extinct lemurs is than species with softer diets. ciduous canines are missing, but to target immature individuals with Enamel prism decussation, the 3-di- small alveoli located just mesial to the M1 erupting or just erupted and rela- mensional undulation of enamel buccal edge of P3 bear testimony to tively unworn. Lacking that, and as- prisms in and out of the plane of sec- their former presence. Lingual to each suming we can identify a neonatal line tion as they make their way from the is the gubernacular canal accommo- on M1, we can use postnatal CFT plus EDJ toward the future enamel sur- dating the tip of the permanent ca- information on root extension rates 4 1 face,23–26 is difficult to quantify. It can nine. The apices of the roots of P ,M , and the amount of root present at 2 3 vary qualitatively in terms of the pres- and M are closed, and M has sub- emergence to estimate age at M1 gin- ence and morphology of Hunter- stantial root development. All three gival eruption. Postnatal ages at Schreger bands, the optical manifes- maxillary molars of this immature in- crown completion, coupled with esti- tations of enamel prisms undulating dividual were sectioned. Aspects of mates for root extension, can be used and crossing over one another; it can the chronology derived from those to estimate emergence ages for second also vary regionally across both cus- sections have been published.12,13 Ad- and third molars as well. pal and imbricational enamel. Heavy ditional details are provided here. Minimum gestation length can also The Megaladapis specimen com- be determined from the dental chro- decussation is thought to enhance prises a partial mandible with dp4 and nologies of fossil taxa if they have a structural resistance to crack propa- gation.27 Animals subsisting on M1 fully erupted and M2 unerupted. high percentage of M1 crown forma- The first and second molars of this harder, coarser diets exhibit a greater tion occurring prenatally. If it is as- individual have been sectioned and degree of decussation, particularly in sumed that calcification of the perma- their chronology has been reported.14 the cuspal portions of their crowns.27 nent M1 cannot begin before the end The Archaeolemur specimen is a man- As yet, no means of quantifying the of the first trimester, the normal tran- dible with full adult dentition; it was precise degree of decussation exists, sition from embryological to fetal figured by its discoverer29 and aspects but broad levels of decussation growth phase, then the duration of of its molar microstructure have been (heavy, moderate, and slight) are eas- prenatal M1 CFT as determined by the described.15 All three molars have position of the neonatal line provides ily recognizable and are used here to now been sectioned. The full chronol- a minimum value for gestation length. characterize a sample of primate mo- ogy is reported here for the first time. More compelling estimates of gesta- lars. Heavy decussation is a high de- Limited microstructural data were tion length in a fossil taxon can be gree of enamel prism undulation also collected for the extinct lemur, made using gestation lengths for that throughout the full thickness of Hadropithecus stenognathus, on the taxon’s closest living relatives, cou- enamel. Decussation is only moderate basis of an isolated second molar re- pled with knowledge of exactly when, if prism undulation is not severe and covered in 2003 at Andrahomana within those gestation periods, M1 occurs only throughout one-half of Cave in Southeast Madagascar by crown mineralization begins. In an- the thickness of enamel. Slight de- David Burney and his co-workers.15 thropoid primates, mineralization of cussation occurs when the enamel pri- Comparative microstructural data on the permanent M1 crown normally marily comprises radial prisms run- extant lemurs were collected for mo- begins late in the third trimester; in ning fairly straight from the EDJ to lars (M1–3) of Propithecus verreauxi living lemurs, it can begin much ear- the outer enamel surface or de- (BMOC #88), Lemur catta (DPC lier. cussates marginally close to the EDJ. 6530F), and Varecia variegata (DPC 144 Godfrey et al. ARTICLES

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, 13 Megaladapis edwardsi 380 517 (No data) 14, 16 Archaeolemur majori 522 460 408 15 Pongo pygmaeus 993 1267 (No data) 17 Pan troglodytes 1004 1333 (No data) 16, 19 Gorilla gorilla 1237 Ͼ1200 (No data) Schwartz, Dean, & Reid, unpublished Papio hamadryas 529 559 715 31 Papio cynocephalus 642 555 708 10

5870F). Comparative microstructural somewhat larger than those of female M2 CFTs in Pan troglodytes and Pongo data for anthropoids were taken from gorillas and its second and third mo- pygmaeus. M1 CFT is roughly similar the literature or personal observations lars were substantially so. At ca. 15–20 in Archaeolemur and Papio. For all (GTS), as indicated. It goes without kg, Archaeolemur majori roughly other giant lemur molars examined saying that data on CFT are sparse, matched the body mass of some adult thus far, CFTs are much shorter than not merely for extinct primate species male baboons, but had slightly in like-sized anthropoids, regardless but also for most extant ones, and that smaller first and second molars and of molar size. intraspecific variance in CFT is poorly considerably smaller third molars. understood. It is only with this caveat Figure 1 displays our data on the mo- made explicit that we take our mea- lar crown developmental chronolo- Age at Death of Immature sured values of CFT in single individ- gies for extinct lemurs and for Papio, Individuals, with Implications uals as “representative” for the taxa in the anthropoid in our comparative da- for the Pace of Dental question. tabase with the least protracted dental developmental chronology. Development Molar Crown Formation Time Crown formation time tends to vary Box 1 illustrates how, by construct- intraspecifically but not interspecifi- ing a complete chronology, including in Subfossil Lemurs cally with molar size. Thus, CFT is root formation, for M1 and M2,we Table 1 shows molar CFTs for three roughly equal for the like-sized M1 determined the age at death, to the species of extinct lemur and several and M2 in both Palaeopropithecus and day, of our immature Megaladapis ed- selected anthropoids (roughly compa- Archaeolemur, and far longer in the wardsi. M2 was crown complete 442 rable in body mass to our extinct le- much larger M2 than M1 of Megalada- days after birth. The individual died mur taxa).30 Table 2 compares their pis. But M1 CFT is much shorter in 66 days later (at 508 days, or 17 molar dimensions. At ca. 40–50 kg, Palaeopropithecus (221 days) and months, after presumptive birth),

Palaeopropithecus ingens was slightly Megaladapis (380 days) than in the with its M2 root partially developed heavier than the largest female Pongo much smaller-toothed Archaeolemur but its M2 crown unerupted. The M1 pygmaeus, but had considerably (522 days). Our only datum for the CFT is 380 days and the ﬁrst molar larger ﬁrst and second molars. At ca. 30–35 kg archaeolemurid, Hadro- was crown-complete at 248 days after

80–90 kg, Megaladapis edwardsi ap- pithecus stenognathus, reveals an ex- birth. In contrast, M1 of a recently proximated the mass of adult female tremely long M2 CFT (2.59 years or analyzed female gorilla was crown- Gorilla gorilla; its ﬁrst molars were 945 days).15 This is close to recorded complete at 1,212 days (3.3 years) af-

TABLE 2. MAXILLARY AND MANDIBULAR MOLAR MESIODISTAL AND BUCCOLINGUAL DIMENSIONS (MM) IN EXTINCT LEMURS 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 ARTICLES The Secrets of Lemur Teeth 145

months total) and M1 initiates the ear- liest (6 months before birth), so that M1 is crown-complete at a very young

age. In Megaladapis, M1 has a longer CFT (12.5 months) and initiates 4.5 months before birth. In Archaeolemur, M1 CFT is longer yet (17 months), and it initiates less than 3 months prior to birth. Of these three taxa, Archaeole- mur is the last to complete M1 crown formation. Also, there is an apparent phylogenetic signal, with Palaeopro- pithecus exhibiting a pattern common in indriids, wherein all three molars initiate crown formation before birth, and contrasting with that of the more distantly related Archaeolemuridae.

Age at Molar Crown Completion and M1 Gingival Eruption Table 4 provides age at M1 crown completion and estimates for the age at M1 gingival emergence for each of the three extinct lemurs. Gingival emergence, the initial appearance of the occlusal surface as it passes through the gumline,35 occurs after crown completion but before the roots are fully formed. Roots continue to form during eruption and, indeed, after the teeth have attained full occlusion, as the jaws continue to grow Figure 1. Molar crown chronologies for Palaeopropithecus, Megaladapis, Archaeolemur, in height or depth. and Papio. The M1 CFT of Archaeolemur resembles that of Papio; both Palaeopropithecus Data on ages at M1 crown comple- and Megaladapis have shorter M1 CFTs. tion and gingival emergence in anthropoids reveal a lag of between five months and a year.35 Preliminary data for lemurs suggest a shorter lag, asso- ter birth, and her total M1 CFT was molars and incisors, as well as the up- 1,237 days. The contrast in dental de- per canine, depending on the species. ciated with extremely rapid root ex- velopmental between Megaladapis and It is clear that there was tremendous tension rates (Box 2). In extant le- Gorilla is striking.16 variation within the giant lemurs in murs, gingival emergence often occurs within a month of crown com- Whereas we cannot directly mea- age at dental maturity. pletion. Cusps initiate and finish at sure age at death for the other subfos- different times, as do their corre- sils in our database, we can assess the sponding roots; therefore, roots asso- ages at which their third molars Dental Developmental Stage ciated with cusps that complete first reached crown completion (Table 1). at Birth will begin to form before the very last For Palaeopropithecus ingens, this was Table 3 shows prenatal crown for- portion of crown is formed. The over- an astounding 135 days (4.2 months) mation and the state of molar devel- lap can be great. In Propithecus ver- after birth. For Archaeolemur majori, opment at birth for our three extinct reauxi, for example, M1 root forma- it was 576 days (1.6 years) after birth. species, with comparative data for tion begins only a few weeks after For Palaeopropithecus, the third mo- both extant lemurs and selected an- birth. M1 root formation initiates sev- lar is one of the last teeth to erupt, thropoids. Both the timing of crown eral weeks later, but the first molar with only the upper canine and per- initiation and overall CFT contribute crowns are not fully formed until ca. 3 14 haps the anterior-most upper premo- to making crown completion rela- months. M1 begins erupting shortly lar erupting later. In Archaeolemur, tively early in Palaeopropithecus and thereafter, certainly by 4 months, several replacement teeth erupt after relatively late in Archaeolemur. In when the mandibular corpus height is the third molar, including some pre- Palaeopropithecus, M1 CFT is short (7 only slightly greater than half its total 146 Godfrey et al. ARTICLES

Box 1. Mapping Out Growth G.T. Schwartz

Box 1 Figure.

Life-history reconstruction for extinct tion in utero? At what age do particular development, for example, one must species depends on our ability to deci- teeth, such as the M1, erupt? And how know when each molar initiated and pher when teeth initiate their formation, much root is present at the time of completed its crown formation relative how long they take to complete their eruption? to the timing for each other molar; that crowns and roots, and when they Using incremental growth lines, both is, it is necessary to register all devel- emerge into the oral cavity. Building short- and long-period, in enamel and oping crowns to one another. Doing dental developmental chronologies al- dentine, we can readily pinpoint when so requires the use of a special class lows us to answer questions such as: crowns initiate and complete forma- of incremental features, accentuated Did permanent teeth begin their formation. To chart the chronology of molar lines. ARTICLES The Secrets of Lemur Teeth 147

Box 1. Mapping Out Growth (continued)

The etiology of the striae of Retzius is neonatal line, allows us to root that chro- M1 development did M2 initiate? To an- largely unknown. Superimposed on these nology to day 0 in the life of that individ- swer that, we found a set of three accen- striae are lines that appear more marked ual; that is, to the day of birth. In the tuated lines, one of which is the neonatal under transmitted polarized light. These ﬁgure, we provide an example of this line. We determined that these same can be coincident with striae, but often technique using the developing dentition three lines, labeled Neonatal Line, Line A, occur between successive Retzius lines. of the giant subfossil lemur Megaladapis and Line B, appear in both molars by The etiology of accentuated lines is even edwardsi. counting the number of daily lines be- less clear; however, we do know that Incremental lines in enamel (daily cross tween each. The ﬁrst line, the Neonatal these lines chart the temporal position of striations and striae of Retzius) were used Line, occurred 22 days before the second stressful episodes.33 Any single “stressful” to determine the time of initiation and line, Line A, which occurred 17 days be-

event, which may be nutritional, physio- completion for the M1 and M2 of a juve- fore the third line, Line B, in both molars. logical, or even psychological,34 will af- nile specimen of M. edwardsi,14 indicated The position of these lines relative to the fect the cells of all developing teeth and by the two horizontal gray bars in the ﬁg- ﬁrst- and last-formed enamel for each will therefore mark the same moment in ure. At the termination of crown forma- molar enabled us to determine the total time. To build a precise chronology re- tion, root development begins (open hor- amounts of prenatal and postnatal molar quires cross-matching accentuated striae izontal box). The absolute timeline on the development, and thus to derive a chro- that correspond to the same “stressful” bottom reveals total crown formation nology, rooted in real time, from 132 days

event across all of the developing teeth. times of 380 days and 517 days for M1 and before birth until this individual died 640

One special kind of accentuated line, the M2, respectively. But at what point during days later, at 508 days old.

adult value, and the longest roots have plies an upper limit of just over 4 Given its accelerated dental devel- attained a corresponding proportion months for the first 50% of root for- opment, it is not unreasonable to as- of their full adult length. Eruption it- mation, and thus the time between sume that the M1 root extension rate self proceeds rapidly, and individuals crown completion and gingival emer- for Palaeopropithecus ingens was at with fully erupted first molars (at five gence, assuming a similar amount of least as rapid as that of Megaladapis months in Propithecus verreauxi) can root formation at emergence as in edwardsi. Using the same estimate for exhibit an advanced stage of first mo- Propithecus. Bracketing this further to time from crown completion to gingi- lar root formation (more than three account for the likelihood of variable val emergence, and given M1 age at quarters complete). At 8 months in root extension rates, overlapping root crown completion of 1.1 months after Propithecus, all of the postcanine and crown formation, and variable birth, we estimate M1 gingival emer- cheek teeth have erupted, although degrees of root formation at gingival gence at between the ages of 2–6 38,39 root formation is not complete. eruption, we estimate M1 gingival months, and probably closer to the The only giant lemur for which we eruption at not less than one and not early end of this range (Table 4). This have directly measured root forma- more than five months after crown is on a par with M1 emergence in the tion time is Megaladapis edwardsi. The completion (thus, between the ages of much smaller-bodied Propithecus and roots of the M1 in this individual are 9 and 13 months in Megaladapis ed- considerably earlier than in like-sized long, but their apices are not fully wardsi; Table 4). Here, the timing of anthropoids. For example, in Pan trog- closed; we infer that the root was in its root extension was empirically deter- lodytes, the M1 crown is complete at terminal phase of growth when this mined as part of the process of deter- 985 days (2.7 years) on average,19 and individual died. This occurred 260 mining the age at death of this imma- does not erupt until ca. 3.5–4.0 years. 14 days (or eight-and-a-half months) af- ture individual. The M2 root formed First-molar root extension may ter M1 crown completion at 248 days at a slower rate than did M1. After 66 have been slower in Archaeolemur ma- postnatal. Assuming a constant root days of root formation, little root was jori than in Megaladapis. However, it extension rate and no overlap between present and the second molar was was probably faster than in like-sized crown and root formation, this im- unerupted. baboons. M1 crown completion oc- 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 days Megaladapis edwardsi 132 days (4.5 months) 75 days — Archaeolemur majori 85 days (3 months) None None Propithecus verreauxi 94 days 56 days 16 days Lemur catta 67 days None None Varecia variegata 55 days None None Pongo pygmaeus 24 days (Ͻ1 month) None None Gorilla gorilla 25 days (Ͻ1 month) None None Papio hamadyras 36 days (1 month) None None a Sources for data are given in Table 1. 148 Godfrey et al. ARTICLES

TABLE 4. ESTIMATED AGE AT M1 ERUPTION FOR EXTINCT LEMURS cannot be distinguished from that of Age at M1 Crown full adults. This suggests an earlier Taxon Completion Age at M1 Eruptiona age for acquisition of adult foraging skills.16 We project an even earlier age Palaeopropithecus ingens 34 days (1.1 months) ϳ2–6 months for acquisition of adult foraging skills Megaladapis edwardsi 248 days (8.3 months) ϳ9–13 months Archaeolemur majori 437 days (14.6 months) ϳ15–19 months in Palaeopropithecus on the basis of its extremely rapid dental development. a Estimated as age at M1 crown completion plus 1–5 months. As in Propithecus, it is likely that Palaeopropithecus was dentally precocious at weaning and, shortly thereaf- curs in the Archaeolemur majori indi- Another strategy is to examine ter, was handling tough, fibrous foods. vidual at 437 days (14.6 months) after tooth wear across ontogenetic series. Half-year old Propithecus have full per- birth. It occurs in like-sized baboons Flanagan15,45 examined microwear manent teeth and are weaned; weaning about two months later; for example, under low magnification for ontoge- generally begins at between 4 and 5 493 days, 511 days. In baboons, the netic series of Macaca fascicularis and months. New weanlings may subsist first molar erupts at around 20 Archaeolemur spp. For Macaca fas- largely on young leaves and other foods months.35 We project a slightly earlier cicularis, she could map life-history that are available during the season of eruption in Archaeolemur (Table 4). landmarks such as weaning and sex- plenty, but the full adult repertoire is Whereas age at M1 emergence is sim- ual maturation on the microwear on- acquired within a few months, during ilar in the two, the whole dental erup- togeny, as the schedule for dental the season of scarce resources. tion chronology was certainly less eruption is well known for this spe- In summary, relatively early wean- protracted in Archaeolemur than in cies. Flanagan observed an increase in ing can be inferred for larger-bodied Papio, given that M3 is crown-com- pit and scratch counts per unit area species, even if we assume that wean- plete in the former at 19 months, but from early to later infancy, leveling off ing did not occur until after young- not until 5.71 years in Papio.31 Never- after M1 comes into occlusion. This is sters had erupted many of their per- theless, the contrast is not as strong followed by a prolonged period during manent teeth. There is evidence of here as it is between other giant lemur which feature counts remain rela- prolonged acquisition of adult forag- species and like-sized anthropoids. At tively stable. This is apparently a post- ing skills in Archaeolemur and of rapid least for M1 emergence, the difference weaning juvenile foraging phase. Mi- acquisition of adult foraging skills in between Archaeolemur and baboons crowear feature counts do not Megaladapis and especially Palaeopro- appears to have been minimal. increase until around sexual matura- pithecus. Given the rapidity of root formation tion, at which time adult values for in extant lemurs for which we have their range and frequencies are man- Brain Growth in Giant Lemurs data, it is reasonable to assume that ifested. Interestingly, Archaeolemur With some reconstruction of the gingival emergence occurs within a shows the same pattern, including a few months of crown completion, and posterior portion of the neurocra- prolonged phase before dental adult- that age at gingival emergence is cor- nium, we were able to estimate the hood during which scratch counts, related with age at crown completion. cranial capacity of our immature particularly hypercoarse scratch It follows that, in comparison to like- Palaeopropithecus ingens at 65–70 cc. counts, remain relatively low.15 Mi- sized anthropoids, giant lemurs ex- Full adult Palaeopropithecus ingens crowear feature counts and variabili- hibited relatively early gingival emer- average a capacity of 101 cc. There is ties are higher for individuals with gence, and that this was particularly little question that individuals at the full adult dentitions than for dentally the case for Palaeopropithecus and stage of dental development repre- immature individuals. Nevertheless, Megaladapis, the largest-bodied of ex- sented by the Palaeopropithecus indi- whereas Archaeolemur youngsters tinct lemurs in our sample. vidual described here, which has full with only M1 erupted do not exhibit a adult dentition except the upper ca- full adult signal for scratches and pits, nine, would have been weaned. Cra- Age at Weaning, Juvenile they do show moderately high fre- nial capacity at weaning was perhaps quencies of both. It may be reasonable Foraging, and Acquisition of well under 65% of the adult value. to assume that weaning occurred in We also measured the cranial ca- Adult Diet Archaeolemur, as in macaques, at pacity of an immature Megaladapis ed- There is no simple way to infer age around the age of M1 eruption at ca. wardsi (AM-MGH2/UA 5491) at a den- at weaning in extinct species. Smith22 15–19 months, and that youngsters tal developmental stage slightly more noted a correlation among Primates experienced a prolonged period there- advanced than that of the 17-month between age at weaning and age at M1 after during which they slowly ac- old individual from which we derived eruption. This relationship holds quired full adult foraging skills. our dental developmental chronology poorly, however, for lemurs.38,39 In contrast, in Megaladapis, by the (Fig. 2). At death, AM-MGH2 had an There may be a trace element or iso- time M1 comes into full occlusion and erupting M2; in all other features topic signal of weaning,40–44 but re- begins to wear, which certainly is be- (fully erupted M1, unreplaced decidu- search along these lines for subfossil fore 17 months and likely before 13 ous teeth) the dental development of lemurs is very preliminary. months of age, the microwear signal the two was comparable. The mea- ARTICLES The Secrets of Lemur Teeth 149

Box 2. Getting to the Root of the Matter K.K. Catlett and K.E. Samonds Whereas recent histological research on molar crown formation times has greatly aided reconstruc- tions of extinct lemur life histories, these studies have largely ignored the incremental data preserved within developing roots. Long and short incremental lines preserved in dentine enable researchers to reconstruct the timing and sequence of root development, just as similar lines preserved in enamel allow the reconstruction of crown development. Because root extension continues well after crown completion, the daily incremental lines preserved in roots allow the interpola- tion of aspects of growth that occur during eruption and even much later in an individual’s life. Roots also provide researchers with increased opportuni- ties to correlate “events” histologically recorded in different teeth, which is crucial for constructing comprehensive dental chronologies. We have begun to use such histological techniques, along with dissection and radiographic analysis, to expand our knowledge of lemur development. Shellis36 developed a geometric formula, c ϭ d[(sin I/tan D) Ϫ cos I)], using the cell secretion rate (d) and prism direction to calculate the extension rate, c, of imbricational enamel. Box 2 Figure. Image of Hadropithecus stenognathus RM2 illustrating variables used to The similar nature of enamel and den- obtain RERs (see text). Angle I (dotted line) is formed between the developing root tine secretion makes Shellis’ equation surface 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. also appropriate for estimating root extension rates (RERs) for any length to compare measurements from radio- gence is relatively consistent between of root.18 To determine d, the daily graphs and from extracted teeth of the species, with mesial roots at ϳ35% of dentine secretion rates (DSRs), one same individuals to attain stages of adult length and distal roots at ϳ45%

must take several measurements root formation for an ontogenetic series of adult length by the time M1 has across long-period dentine lines and of known-aged specimens. The stages started to cross the alveolar plane. divide by the periodicity. correspond to percentages of develop- These results suggest that charting Using these techniques, we calcu- ing root lengths calculated against root extension rates and formation

lated the average RER for the M1 in a adult root lengths, determined by direct times will enhance our ability to glean Propithecus verreauxi (BMOC #88) to measurement of extracted teeth. Using dental developmental information from be approximately 29.8 ␮m/day with an this technique, we scored mandibular an individual’s entire dentition. Histo- average DSR of 3.0 ␮m/day. These molars for a series of Varecia variegata logical research on root dentine pro- rates suggest that approximately 175 and Propithecus verreauxi ranging from vides longitudinal data that can assist days were required to grow 4.8 mm of newborn individuals to dental adults. in reﬁning our understanding of the

measurable root. The calculated M1 Results indicate that in Propithecus, M1 amount of daily root growth, informa- RERs for both extant and extinct an- roots reach 29% of adult root length at tion not captured in radiographs from a thropoid species (other than humans) only 2.5 months of age, while Varecia cross-sectional sample. Such analyses range from 5.20 ␮m/day in Hylobates requires an additional 100 days to will enable us to compare the pace of 37 ␮ 18 lar to 19.40 m/day in Proconsul. reach a comparable stage of M1 root lemur and similarly sized anthropoid

Regardless of body size, it is clear that development. In Propithecus, M1 gingi- tooth root development to determine Propithecus has not only accelerated val emergence, estimated to occur at how much root is present at the time of enamel development,14 but also ex- ϳ3–4 months, closely follows the initi- eruption and how much time is re-

tremely rapid root development. ation of M1 root formation. The amount quired for lemur tooth roots to achieve

We also devised a scoring technique of root formation at M1 alveolar emer- apical closure. 150 Godfrey et al. ARTICLES

brain measures ϳ95% of the adult value. Varecia weanlings may not have 90% of their adult cranial capacity quite yet, but their brain growth trajectory is well ahead of their dental developmental trajectory. In other words, Varecia exhibits, in stark contrast to Propithecus, slow teeth-fast growth. Preliminary data for Archaeolemur suggest a pattern more similar to that of Varecia than Propithecus. This matches expectations derived from studies of other aspects of craniofacial growth.5,6 Archaeolemur exhibits a relatively rapid pace of craniofacial growth when benchmarked against dental development. Thus, it appears that Megaladapis and especially Paleo- propithecus, giant lemurs with relatively rapid dental development, experienced relatively slow brain growth, while the opposite applied to species with relatively slow dental development such as Archaeolemur. It also is Figure 2. Specimens of Megaladapis edwardsi used in analysis of dental microstructure and interesting to note that the archaeole- endocranial growth. A. Buccal view of the left hemi-mandible of a juvenile specimen (UA murids are the only larger-bodied

4620/AM 6567) illustrating the erupted dp4 and M1, and the M2 in crypt. B. Buccal view of the lemurs that even approach anthro- 14 unerupted M2 after removal from the crypt. The arrow points to the few millimeters of initial poid-like brain-body relationships. root formation. C. Lingual view of hemi-mandible showing dp4 and M1. D. Cranium of Palaeopropithecus and Megaladapis ϭ Megaladapis edwardsi (AM-MGH2). Scale bar 10 cm. have very small brains for their adult body size. sured cranial capacity, 90 cc, was ca. To better understand this phenome- Gestation Length 65% of the adult value of 137 cc for non, we collected cranial capacity Schwartz and colleagues12 used the Megaladapis edwardsi. If we are cor- growth trajectories for living strepsir- position of the neonatal line, and thus rect in inferring that individuals at rhines. Between 4 and 6 months, the the inferred time in utero that M1 be- this stage of dental development had cranial capacities of Propithecus in- gan forming, to estimate gestation been weaned, this implies a small cra- crease from 65% to 75% of their adult length for Palaeopropithecus ingens. nial capacity for Megaladapis edwardsi value. This is far less than the 90%–95% Their estimate of over 9 months must at weaning as well. of adult cranial capacity typical of an- be regarded as a theoretical mini- Both Palaeopropithecus and Megal- thropoid weanlings. This phenomenon mum; it is based on the assumption adapis bear testimony to a phenome- in sifakas is part of the “fast teeth-slow that no part of M1 crown formation non that is not manifested in anthro- growth” pattern described by Godfrey can occur during the embryonic poids: relatively slow acquisition of and colleagues,39 and was evidently phase of gestation—essentially the adult cranial capacity with respect to shared, to varying degrees, by Palaeo- ﬁrst third. Table 5 shows estimates of dental development and weaning. propithecus and Megaladapis. gestation length for Megaladapis, Ar- Typically among anthropoids, cranial In contrast, Varecia variegata at- chaeolemur, and Palaeopropithecus, capacity is at 90%–95% of the adult tains 65% of adult cranial capacity at using this theoretical minimum value at weaning.46–51 Clearly, this less than 3 months. At 6 months, after method as well as models based on was not the case for Palaeopropithecus weaning but before any permanent extant-lemur analogs. For example, a or Megaladapis. teeth, including M1, have erupted, its model based on Propithecus verreauxi

TABLE 5. RECONSTRUCTING GESTATION LENGTH, IN DAYS, IN EXTINCT LEMURS Prenatal M1 Minimum Propithecus Varecia Taxon CFT Model Model Model Lemur Model Palaeopropithecus ingens 187 279 317 346 381 Megaladapis edwardsi 132 197 224 244 269 Archaeolemur majori 85 127 144 157 173 ARTICLES The Secrets of Lemur Teeth 151

TABLE 6. MACRO- AND MICROSTRUCTURAL INDICATORS OF TROPHIC ADAPTATIONS IN EXTINCT LEMURS AND OTHER PRIMATES Cuspal Imbricational R.E.T. (Means and Range, When Taxon Decussationa Decussationa Available)b Varecia variegata 1 1 5.7 Lemur 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 10.7 Palaeopropithecus ingens 1 1 11.3 Megaladapis 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 19.2 Archaeolemur 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 ϭ slight or none, 2 ϭ moderate, 3 ϭ heavy See text for explanation. RET data for Palaeopropithecus, Archaeolemur, and .100 ء (b Relative enamel thickness: ([c/e]/͌ b Hadropithecus are taken from Godfrey and coworkers.15 Data for Megaladapis are new, and are combined for M1 and M2. All other data are taken from references Schwartz, Liu, and Zheng56 and Smith, Martin, and Leakey57 and are means based on RET values for M1–M3. Recent work68 documents metameric variation in enamel thickness in hominoids. However, these differences are trivial in comparison to the variation in subfossil and extant strepsirrhines.

begins with the observation that ges- Even if M1 crown mineralization in P. of molar crown formation. Indeed, tation averages 158 days in this spe- ingens began at the end of the first there is credible evidence that the ges- cies38,52 and that molar crown forma- trimester, our theoretical minimum, tation period was longer in Palaeopro- tion begins ϳ94 days prior to birth gestation length would have had to be pithecus ingens than in humans, (our data for BMOC #088, Propithecus longer than 9 months. Using a Pro- which is all the more remarkable verreauxi from Beza Mahafaly). A Pro- pithecus model, gestation in Palaeo- given that this is a species with one of pithecus model assumes that M1 propithecus is estimated at 10.5 the most rapid dental developmental crown formation occupies the same months. Using extant lemurids as a trajectories of all primates. proportion of overall gestation in the model for P. ingens would result in far extinct taxon as it does in Propithecus. longer and probably unrealistic esti- Dental Structural Indicators of This proportion is calculated as the mates of gestation length (12.5 observed prenatal crown formation months), underscoring the impor- Trophic Adaptations time divided by the observed gestation tance of using the appropriate mod- Enamel prism morphology and the length (in Propithecus, 94/158 ϭ 0.59). ern analog in our analyses. We take a relative thickness of the enamel vary To calculate the estimated gestation model based on the theoretical mini- widely across extant and extinct le- time in the extinct species, the ob- mum or the Propithecus model as the murs (Table 6). They provide strong served prenatal CFT is divided by this most appropriate for Palaeopropithe- evidence of a coarse diet with hard- ratio; for example, for Palaeopropithe- cus and therefore estimate gestation object processing in Archaeolemur, cus ingens, 187 days/0.59 ϭ 317 days length as 9–11 months (Table 5). but not in Megaladapis or Palaeopro- or, 10.5 months. Gestation lengths in The theoretical minimum is much pithecus.15,58 For these two indicators extant lemurids are much shorter shorter for Megaladapis edwardsi (6.5 of diet, nearly all extant lemurs are than in Propithecus, ca. 102–136 days months) and Archaeolemur majori (4.2 similar to Megaladapis and Palaeopro- for the largest-bodied lemurids.53–55 months) (Table 5). Applying a lemurid pithecus, with only Daubentonia Also, the proportion of the gestation model to these species, we derive ges- madagascariensis exhibiting relatively period during which M1s are develop- tation estimates of 8–9 months for thick enamel (RET ϭ 21.7).59 In Ar- ing is smaller. A Varecia model (gesta- Megaladapis and 5–6 months for Ar- chaeolemur, molar enamel prism de- tion length of 102 days and prenatal chaeolemur. Gestation would have cussation and relative enamel thick- crown formation time of 55 days) been longer in Archaeolemur only if its ness are no less than remarkable (Fig. yields a ratio of 0.54; a Lemur catta dental developmental trajectory was 3; Table 6). Only a few extant pri- model (gestation length of 136 days more similar to those of anthropoids, mates, including the omnivorous and a prenatal crown formation time which initiate M1 crown formation hard-object processor Cebus apella, of 67 days) yields a ratio of 0.49. closer to birth.14 have molars that combine thick M1 crown formation time in Palaeo- In summary, gestation was not enamel and well-defined Hunter- propithecus ingens is 221 days, with short in giant lemurs, a phenomenon Schreger bands, suggesting enhanced 187 prenatal days of crown forming. that may reflect their early initiation resistance to high occlusal loads and 152 Godfrey et al. ARTICLES

mandibular molars are missing but their sockets suggest that they had or were erupting and had partial roots. These specimens establish that the premolars erupt from back to front, as in indriids, that month-old infants were processing solid food, and that the crown of the upper canine, the last tooth to erupt, had fully formed before the precocious first molar had completed its root formation. The eruption sequence manifested in these individuals matches that exhib- ited by some Propithecus. It is possible that the entire chronology of dental development in Palaeopropithecus was very like those of extant indriids, and that, as in extant indriids, Palaeo- propithecus was born with all deciduous teeth erupting or erupted. Megaladapis also shows rapid dental development, but was not as precocious at birth as was Palaeopro- Figure 3. Heavy enamel prism decussation in Archaeolemur. pithecus or extant indriids. In fact, we know that Megaladapis, like lemurids, was born without its deciduous teeth fully erupted. The youngest known crack propogation. Pitheciins (Caca- brain growth was slow in Palaeopro- Megaladapis (DPC 17150) has an une- jao, Chiropotes, and Pithecia) have pithecus, as it is in Propithecus. rupted dp lacking roots but a fully well-defined Hunter-Schreger bands 4 Only a single deciduous tooth (a erupted dp with roots. The crypt for but relatively thinner enamel and are, 3 dp4) is known for any individual be- M is present but broken and the M in this manner, more like Hadropithe- 1 1 longing to a palaeopropithecid spe- crown is missing. Because the distal cus.60 Certain extinct anthropoids cies, including Palaeopropithecus and portion of the corpus is also missing, have striking microstructural similar- its closest relatives Archaeoindris, Me- it is impossible to tell the state of de- ities to Archaeolemur, including Grae- sopropithecus, and Babakotia. This velopment of the second or third mo- copithecus freybergi and Paranthropus alone suggests rapid passage through lars. spp.61 the milk-tooth stage of dental develop- Specimens of Archaeolemur spp. ment. The known deciduous tooth, and Hadropithecus stenognathus sug- belonging to a very young Palaeopro- gest very different scheduling of devel- LESSONS FROM THE LEMURS pithecus ingens (DPC 17307), was opmental events. Numerous known found in association with additional The data described here underscore archaeolemurid specimens bear milk loose teeth, including an M and M , a remarkable diversity of developmen- 1 2 dentitions, which appear to have en- P ,M1, and P4. The state of develop- tal patterns in the lemurs of Madagas- 4 dured for a prolonged period before ment of the M1, a crown with no root car.6,38,62–64 In many ways, dental de- they were replaced. There is no dimi- velopment in Palaeopropithecus is formation, suggests that this individ- nution of the milk teeth; indeed, the very like that of indriids: Palaeopro- ual was not more than one month old dp4s in both maxilla and mandible are pithecus is on a par with or even at death. M1 is crown-complete and almost as large in the occlusal area as “ahead” of Propithecus in its schedule has some root formation. The dp4 has are the M1s.6 In effect, they serve as of molar crown formation and dental roots and exhibits some macrowear. functional substitutes for M1 before precocity at birth. As in Propithecus, The M2 has no roots but is at an ad- full eruption of the latter, which we “fast” teeth are apparently accompa- vanced stage of crown development, now know did not occur until 15 4 nied by slow craniofacial growth. as is P . A second, somewhat older, months or later.15 Microstructural Many of the craniofacial correlates of infant Palaeopropithecus ingens (DPC data confirm a prolonged infancy in dental precocity in indriids, including 18750) is represented by a left maxilla Archaeolemur prior to the onset of the diminutive milk teeth, crowding of and associated partial mandible. The eruption of the permanent dentition. unerupted and newly erupted teeth, maxilla has an erupted M1, erupting Microwear data suggest a prolonged and dissociation of the rates of cranio- P4, and full crowns of P3 and C1, with- period of juvenile foraging following facial and dental development, are out roots, in their crypts. The roots of weaning. The pattern of slow growth manifested in Palaeopropithecus.6 We M1 are not fully formed. The second and fast teeth, manifested so strik- add to this list the observation that and third molars are missing. The ingly in Palaeopropithecus, does not ARTICLES The Secrets of Lemur Teeth 153 characterize Archaeolemur. Instead, can better understand how diet pre- inoid evolution and adaptations. New York: Ple- Archaeolemur exhibits a growth pat- dicts life-history strategy. By com- num Press. p 173–208. 10 Macho GA. 2001. Primate molar crown for- tern more like that of lemurids, with paring the giant lemurs to like-sized mation times and life history evolution revisited. relatively rapid somatic growth and anthropoids, we gain a better under- Am J Primatol 55:189–201. slow dental development, but more standing of the phylogenetic baggage 11 Dean C, Leakey MG, Reid D, Schrenk F, extreme.5,39 these species carry. Why did the large- Schwartz GT, Stringer C, Walker A. 2001. Growth processes in teeth distinguish modern We can now draw preliminary in- bodied species disappear? To separate humans from Homo erectus and earlier homin- ferences regarding the overall pattern fact from fiction, we must do a better ids. Nature 414:628–631. of growth and development in large- job than has been done in the past of 12 Schwartz GT, Samonds KE, Godfrey LR, Jungers WL, Simons EL. 2002. Dental micro- bodied lemurs. We know that Palaeo- reconstructing the niche characteris- structure and life history in subfossil Malagasy propithecus and Megaladapis, the gi- tics of these extinct species and, to lemurs. Proc Natl Acad Sci 99:6124–6129. ant lemur species with the largest whatever extent possible, their life- 13 Schwartz GT, Godfrey LR. 2003. Box 3. Big molars, do not have the longest CFTs. history strategies. bodies, fast teeth. Evol Anthropol 12:259. 14 Schwartz GT, Mahoney P, Godfrey LR, There is no tendency, as there is Cuozzo FP, Jungers WL, Randria GFN. 2005. among anthropoids, for large-bodied ACKNOWLEDGMENTS Dental development in Megaladapis edwardsi species to exhibit slow growth and de- (Primates, Lemuriformes): implications for understanding life history variation in subfossil le- velopment while small-bodied species This work was supported by NSF murs. J Hum Evol 49:702–721. exhibit rapid growth and develop- Grants BCS-0237338 to LRG, BCS- 15 Godfrey LR, Semprebon GM, Schwartz GT, ment. Instead, there is evidence of an 0503988 to GTS, and BCS-0129185 to Burney DA, Jungers WL, Flanagan EK, Cuozzo David Burney, LRG, and WLJ. We FP, King SJ. 2005. New insights into old lemurs: ecological divide, with the hard-object the trophic adaptations of the Archaeolemuridae. processors, the archaeolemurids, gratefully acknowledge the help of Int J Primatol 26:825–854. exhibiting relatively slow dental devel- John Fleagle and three reviewers, and 16 Schwartz GT, Godfrey LR, Mahoney P. n.d. opment, while other species (Palaeo- of the many people who contributed Inferring primate growth, development, and life to this work, including Frank Cuozzo, history from dental microstructure: the case of propithecus especially and Megalada- the extinct giant Malagasy lemur, Megaladapis. pis somewhat) have relatively rapid Erin Flanagan, Gina Semprebon, In: Bailey S, Hublin J-J, editors. Dental perspec- dental development. The former is as- Patrick Mahoney and, particularly, tives on human evolution: state of the art re- our Malagasy hosts (Gise`le Randria, search in dental anthropology. 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