Evolutionary Anthropology 15:142–154 (2006) ARTICLES The Secrets of Lemur Teeth 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 le- murs, 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.