Tooth eruption and life history in living chimpanzees

T.M. Smith & Z.P. Machanda

Leakey Final Report

This goal of this study was to understand the pattern of dental emergence in a

population of East African chimpanzees (Pan troglodytes schweinfurthii) living in Kibale National Park (KNP), Uganda. We tested the long-­‐held belief that certain dental developmental benchmarks are highly correlated with life history variables such as age at weaning, interbirth intervals and age at first reproduction. Subadults (0-­‐18 years old) of known birthdates from the Kanyawara community of chimpanzees were routinely photographed over the course of 3 years and their tooth emergence stages as well as the duration of eruption (tooth movement from the gumline to the occlusal plane) were assessed. These data were then compared to long-­‐term behavioral and life history datasets from the same population.

Understanding dental development in chimpanzees, our closest living relatives, is of fundamental importance for reconstructing the evolution of human development. Most early hominin species are believed to show rapid ape-­‐like patterns of development, implying that a prolonged modern human childhood evolved quite recently. However, most data on developmental patterns in chimpanzees has been derived from captive individuals. Given the differential access to energy resources in captivity, it is doubtful that the developmental trajectories of captive chimpanzees are shared by their wild counterparts. Furthermore, previous studies of development in wild chimpanzees may not represent normative developmental patterns because they used skeletal collections of deceased individuals and data was often derived from only single individuals for a few tooth positions. Before our study, developmental standards were uncertain because they had never been based on living wild

individuals. The novelty of our study was the use of photography to obtain dental emergence ages of living individuals. This method also allowed us to assess dental development in several individuals at once and also allowed us to ascertain the timing of multiple markers in the same individual to better understand individual variation. Furthermore, we were able to correlate these markers with simultaneously recorded behavioral data.

Although our original proposal planned to also examine individuals of the Ngogo community also in KNP, scheduling issues made it difficult to obtain enough photographs of individuals in this group. Therefore, we were not able to provide comparisons between these two wild populations of chimpanzees and instead used previously published data from the Taї and Gombe communities. We were also able to make rigorous comparisons with the large sample of previously published data on captive individuals. The funds provided by the Leakey Foundation were used to purchase a digital SLR camera and to pay for the field costs of a photographer for one year. The camera was subsequently used in 2013 and 2014 by other photographers to continue photographic data collection of tooth development. This study has resulted in two published manuscripts.

Our first manuscript by Smith et al. (2013) was published in the Proceedings of the National Academy of Science. Here we examined the timing of first molar (M1) eruption and compared these patterns to behavioral data on nursing and feeding. Although it is well established that first molar tooth emergence (movement into the mouth) is correlated with the scheduling of growth and reproduction across primates broadly, its precise relation to solid food consumption, nursing behavior, or maternal life history was unknown, especially among apes. Our results using data from five healthy infants showed that wild chimpanzees emerged

their lower first molars by or before 3.3 y of age (Figure 1). This is nearly identical to captive chimpanzee mean ages (∼3.2 y, n = 53). First molar emergence in these chimpanzees did not directly or consistently predict the cessation of nursing or maternal interbirth intervals or the resumption of maternal estrous cycling. Instead, Kanyawara chimpanzees showed adult patterns of solid food consumption by the time M1 reached functional occlusion (~3.4-­‐4.0 years of age) (Figure 2). They also spent a greater amount of time on the nipple while M1 was erupting than in the preceding year, and continued to suckle during the following year (Figure 2). Interestingly, estimates of M1 emergence age in australopiths are remarkably similar to the Kanyawara chimpanzees. These results suggest that reconstructions of hominin life history that use M1 emergence age as a proxy for weaning should be cautious and would benefit from additional information on covariation in dental development, ecology and life history within and among populations, subspecies and species of living great apes. The ontogeny of feeding behavior and nutritional independence are potentially important developmental milestones that may covary with morphological development.

Figure 1: Azania showing eruption of both mandibular first molars (M1s). The left M1 (Right) was observed to be unerupted at 2.8 y of age, but a small dark spot was apparent by 3.0 y. It is unknown when the right M1 may have emerged, but it may have been earlier as it appears to be more advanced than the left M1. This photograph was taken at 3.1 y of age.

Figure 2: Average observed time spent feeding on (A) solid foods and (B) on the nipple by subadult Eastern chimpanzees. Community-­‐ level data are indicated with blue diamonds, and the five individuals known to have erupted their first molars during this study are indicated with red squares. The number of focal days for each age category are indicated next to the corresponding point, with the number of individuals in each category given in parentheses. The range of monthly averages of adult feeding time is indicated by the blue horizontal bar in A.

Our second manuscript, Machanda et al. (2015) has been published in the Journal of Human Evolution. In this publication we used the photographic data to generate a comprehensive three-­‐year record of dental eruption (including tooth emergence ages and the duration of eruption for both deciduous and permanent teeth) (Figure 3). We also compared our results with those from captivity and from living individuals at Gombe and deceased individuals at Taї. We found that emergence ages in the Kanyawara chimpanzees are very similar to living Gombe chimpanzees, and are broadly comparable to deceased Taï Forest chimpanzees. Early-­‐emerging teeth such as the deciduous dentition and first molar (M1) appear during a time of maternal dependence, and are almost indistinguishable from captive

chimpanzee emergence ages, while later forming teeth in the Kanyawara population emerge in the latter half of captive age ranges or beyond. We were also able to continue tracking the five individuals who were the focus of our previous paper (and added a sixth subject) to see when they completed nursing and if and when their mothers reproduced again. These six juveniles whose lower M1s emerged by or before 3.3 years of age continued to nurse for a year or more beyond M1 emergence, and their mothers showed considerable variation in reproductive rates. Furthermore, the third molars of two adolescent females emerged several months to several years prior to the birth of their first offspring.

Given that broad primate-­‐wide relationships between molar emergence and life history do not necessarily hold within this population of chimpanzees, particularly for variables that are reported to be coincident with molar emergence, we suggest that further study is required in order to predict life history variables in hominins or hominoids.

Figure 3: tooth emergence in two-­‐month old Buke showing initial emergence of her deciduous lower central incisors and deciduous third premolars (small white spots in the pink U-­‐ shaped dental arcade). Her deciduous lower lateral incisors appeared shortly before 93 days of age, the deciduous lower fourth premolars were first seen fully erupted at 315 days of age, and the deciduous lower canine appeared to cut the gum at 437 days of age.

In summary, this project has resulted in novel data on dental eruption in living wild

chimpanzees, including critical information on the relationship between first molar eruption and dietary ontogeny, which will inform studies of the evolution of human life history.

Smith, T.M., Machanda, Z., Bernard, A.B., Donovan, R.M., Papakyrikos, A.M., Muller, M.N., Wrangham, R. (2013) First molar eruption, weaning, and life history in living wild chimpanzees. Proc. Natl. Acad. Sci. USA 110:2787-­‐2791.

Machanda, Z., Brazeau, N.F., Bernard, A.B., Donovan, R.M., Papakyrikos, A.M., Wrangham, R., Smith, T.M. (in press) Dental eruption in East African wild chimpanzees. J. Hum. Evol.