B. Holly Smith

Evolution of the Human Life Cycle

Social mammals have three basic stages of postnatal development: infant, juvenile, and adult. Some species also have a brief female post‐reproductive stage. The human life cycle, however, is best described by five stages: infant, child, juvenile, adolescent, and adult. Women in both traditional and industrial societies may also have a long post‐reproductive stage. Analyses of bones and teeth of early hominids who died as subadults suggest that the evolution of the new life stages of childhood and adolescence are not of ancient origin. The current human pattern evolved after the appearance of Homo erectus. It is possible that evidence for the existence of the post‐reproductive stage for women will also be recoverable from the fossil record because the hormonal changes associated with menopause have profound effects on bone density and histology of tubular bones. It is hypothesized that the new life stages of the human life cycle represent feeding and reproductive specializations of the genus Homo.

Hind Limbs of Eocene Basilosaurus: Evidence of Feet in Whales

New specimens of middle Eocene Basilosaurus isis from Egypt include the first functional pelvic limb and foot bones known in Cetacea. These are important in corroborating the intermediate evolutionary position of archaeocetes between generalized Paleocene land mammals that used hind limbs in locomotion and Oligocene-to- Recent whales that lack functional pelvic limbs. The foot is paraxonic, consistent with derivation from mesonychid Condylarthra. Hind limbs of Basilosaurus are interpreted as copulatory guides.

Complete Primate Skeleton from the Middle Eocene of Messel in Germany: Morphology and Paleobiology

Background The best European locality for complete Eocene mammal skeletons is Grube Messel, near Darmstadt, Germany. Although the site was surrounded by a para-tropical rain forest in the Eocene, primates are remarkably rare there, and only eight fragmentary specimens were known until now. Messel has now yielded a full primate skeleton. The specimen has an unusual history: it was privately collected and sold in two parts, with only the lesser part previously known. The second part, which has just come to light, shows the skeleton to be the most complete primate known in the fossil record. Methodology/Principal Findings We describe the morphology and investigate the paleobiology of the skeleton. The specimen is described as Darwinius masillae n.gen. n.sp. belonging to the Cercamoniinae. Because the skeleton is lightly crushed and bones cannot be handled individually, imaging studies are of particular importance. Skull radiography shows a host of teeth developing within the juvenile face. Investigation of growth and proportion suggest that the individual was a weaned and independent-feeding female that died in her first year of life, and might have attained a body weight of 650–900 g had she lived to adulthood. She was an agile, nail-bearing, generalized arboreal quadruped living above the floor of the Messel rain forest. Conclusions/Significance Darwinius masillae represents the most complete fossil primate ever found, including both skeleton, soft body outline and contents of the digestive tract. Study of all these features allows a fairly complete reconstruction of life history, locomotion, and diet. Any future study of Eocene-Oligocene primates should benefit from information preserved in the Darwinius holotype. Of particular importance to phylogenetic studies, the absence of a toilet claw and a toothcomb demonstrates that Darwinius masillae is not simply a fossil lemur, but part of a larger group of primates, Adapoidea, representative of the early haplorhine diversification.

New Protocetid Whale from the Middle Eocene of Pakistan: Birth on Land, Precocial Development, and Sexual Dimorphism

Background Protocetidae are middle Eocene (49–37 Ma) archaeocete predators ancestral to later whales. They are found in marine sedimentary rocks, but retain four legs and were not yet fully aquatic. Protocetids have been interpreted as amphibious, feeding in the sea but returning to land to rest. Methodology/Principal Findings Two adult skeletons of a new 2.6 meter long protocetid, Maiacetus inuus, are described from the early middle Eocene Habib Rahi Formation of Pakistan. M. inuus differs from contemporary archaic whales in having a fused mandibular symphysis, distinctive astragalus bones in the ankle, and a less hind-limb dominated postcranial skeleton. One adult skeleton is female and bears the skull and partial skeleton of a single large near-term fetus. The fetal skeleton is positioned for head-first delivery, which typifies land mammals but not extant whales, evidence that birth took place on land. The fetal skeleton has permanent first molars well mineralized, which indicates precocial development at birth. Precocial development, with attendant size and mobility, were as critical for survival of a neonate at the land-sea interface in the Eocene as they are today. The second adult skeleton is the most complete known for a protocetid. The vertebral column, preserved in articulation, has 7 cervicals, 13 thoracics, 6 lumbars, 4 sacrals, and 21 caudals. All four limbs are preserved with hands and feet. This adult is 12% larger in linear dimensions than the female skeleton, on average, has canine teeth that are 20% larger, and is interpreted as male. Moderate sexual dimorphism indicates limited male-male competition during breeding, which in turn suggests little aggregation of food or shelter in the environment inhabited by protocetids. Conclusions/Significance Discovery of a near-term fetus positioned for head-first delivery provides important evidence that early protocetid whales gave birth on land. This is consistent with skeletal morphology enabling Maiacetus to support its weight on land and corroborates previous ideas that protocetids were amphibious. Specimens this complete are virtual ‘Rosetta stones’ providing insight into functional capabilities and life history of extinct animals that cannot be gained any other way.

Bias and Accuracy of Age Estimation Using Developing Teeth in 946 Children

Developing teeth are used to assess maturity and estimate age in several disciplines. The aim of the study was to determine which of the most well known dental age estimation methods was best at estimating age. The target sample of dental radiographs (N = 946, ages 3–16) was described by Maber et al. (Forensic Sci Int 159 (2006) S68–S73). Seven mandibular permanent teeth (I1–M2) were assessed, and dental age was calculated using four dental maturity scales and fifteen methods that use data for individual teeth. The mean difference between dental age and real age was calculated (bias) as well as several other measures of accuracy (mean/median absolute difference, percentage aged to within six months and to within 10% of real age). Most methods estimated age with significant bias and standard deviation of bias ranged from 0.86 to 1.03 years. Analysis by age group showed most methods over-aged younger children, and considerably under-aged older children. The method that performed best was the dental maturity scale of Willems et al. (J Forensic Sci 46 (2001) 893–895) with bias of −0.14 ± 0.86 years (N = 827), mean absolute difference of 0.66 years, 71% aged to 10% or less of age, and 49% aged to within six months. Two individual teeth, P2 and M2, estimated age with bias not significantly different to zero for most formation stages using methods based on a large reference sample (L9a Demirjian stages) and a uniform age distribution (N25a Moorrees stages). Standard deviation of bias was least for early crown stages and most for late root stages. Methods that average ages for individual teeth improve if schedules for ‘mean age entering a stage’ are adjusted for prediction. Methods that directly calculate ‘mean age within stage’ can be improved by drawing from a uniform age distribution.

Sequence of emergence of the permanent teeth in Macaca , Pan , Homo , and Australopithecus : Its evolutionary significance

There are two main questions about the sequence of emergence of the permanent teeth in humans: 1) Why is there so much variation in sequence within human populations? (2) What is the adaptive or evolutionary significance of emergence sequence? Here, the human condition is considered by comparing us to other living primates and to our evolutionary past and considered in the light of Schultzs hypothesis that sequence of tooth emergence is adapted to rate of postnatal growth (Schultz AH. In JM Tanner (ed.) Human Growth, pp 1–20, 1960). Frequencies of individual pairwise sequences (e.g., M1I1 vs. I1M1) in the emergence of the permanent dentition are described for N = 110 Macaca nemestrina, and compared to N = 157 Pan troglodytes and ≥6,000 Homo sapiens. In addition, sequences of gingival emergence are reconstructed for Australopithecus and early Homo. Trends observed across these catarrhine primates suggest that sequence and variability in sequence can be understood by a simple model of adaptation of tooth emergence to growth rate. As rate of postnatal growth slows, molars drift to later positions in sequence, either by always emerging late in sequence, or by varying in the direction of late emergence. “Augmented sequences” (sequences written with notations about variability) are important in recognizing evolutionary trends; further, they often alter perception of similarities and differences among taxa. Although samples are small, Australopithecus africanus resembles the rapidly developing genera Macaca and Pan more than it resembles Homo sapiens.

Supernumerary teeth in a subadult rhino mandible (Stephanorhinus hundsheimensis) from the middle Pleistocene of Mosbach in Wiesbaden (Germany)

A well preserved subadult rhino mandible from Mosbach 2 can be attributed toStephanorhinus hundsheimensis based on a metrical and morphological analysis. A comparison to tooth eruption of livingDiceros bicornis suggests an individual age for the animal of about 7 years at death. The described mandible shows a significant tooth anomaly: two teeth occupy the p3 position on each side of the mandible. Comparisons with three younger juvenileStephanorhinus hundsheimensis from Mosbach 2 show the sequence of tooth eruption for the species and allow us to determine that the anomalous teeth are not persistent milk teeth but are supernumerary teeth, which are morphologically intermediate between normal p2 and p3. The animal’s occlusion was compromised to some degree by the anomaly, and the functional disadvantage may have been critical during a harsh period.ZusammenfassungDer gut erhaltene Unterkiefers eines jungadulten Nashorns aus Mosbach 2 kann aufgrund der morphologischen Merkmale und der AbmessungenStephanorhiuns hundsheimensis zugeordnet werden. Nach der Abfolge, in der die Zähne beim Zahnwechsel in der Kauleiste erscheinen, war das Tier — verglichen mitDiceros bicornis — etwa 7 Jahre alt. Der Unterkiefer zeigt eine auffallende Anomalie in der Zahnreihe: In der Position des unteren p3 sind auf beiden Seiten jeweils zwei Zähne vorhanden. Aus dem Vergleich mit drei weiteren Kiefern vonStephanorhinus hundsheimensis aus Moosbach 2 kann der Zahnwechsel rekonstruiert und gezeigt werden, dass es sich bei den überzähligen Zähnen nicht um persistierende Milchzähne sondern um eine Verdoppelung der Zahnanlagen handelt. Morphologisch vermitteln diese Zähne zwischen p2 und p3. Die Funktion des Gebisses war zwar nicht schwerwiegend gestört, aber dennoch kann sich eine solche Anomalie während einer besonders schwierigen Nahrungssituation als Nachteil erwiesen haben.

Developmental Communalities in Tooth Emergence Timing

Intercorrelations and communalities are now well known for tooth formation (Garn et al., J Dent Res 39:1049, 1960), crown size of the permanent teeth (Moorees and Reed, Arch Oral Biol 9:685, 1964; Garn et al., J Dent Res 44:350, 1965), the deciduous teeth (Garn et al., JDentRes 56:1214, 1977), and crown size of deciduous teeth during odontogenesis (Garn et al., J Dent Res 58:554, 1979). However, comparable analytic information has not been presented for postnatal tooth emergence timing of 11 through M2. To explore these emergence relationships and their relative magnitudes, tooth emergence (timing) correlations were calculated using coded emergence data derived from serial casts of 204 participants in the Longitudinal Study of the University of Michigan (Moyers et aL, Standards of Human Occlusal Development, Ann Arbor: The Center for Human Growth and Development, 1976). Individual ages of tooth emergence were Z-scored for males and females separately for each of 28 permanent teeth, and the entire matrix of 121 pooled-sex tooth-pair intercorrelations was then computer correlated. Correlation coefficients for intra-quadrant pairs, antimeres, isomeres, and teeth separated by numbers of intervening teeth were separately averaged using the z transform of r As snown in the Table, where correlations are

Patterned Asymmetry in Tooth Emergence Timing

Although attention has been directed to asymmetries in mesiodistal and buccolingual crown dimensions, beginning with Ballard (Angle Ortho 68:67, 1944), there are also left-right differences in tooth emergence timing that are of investigative interest and possible clinical concern. Since isomeres may emerge several years apart in some cases, there is a need to ascertain the extent to which emergence asymmetry is patterned, the degree of correspondence in asymmetry between the jaws, and the possible relationship between permanent tooth emergence order and the degree of emergence timing asymmetry. To accomplish this we have made use of serial longitudinal tooth emergence data on Michigan boys and girls (Garn and Smith, J Dent Res, in press, 1980), calculating emergence asymmetry both as left-right correlations (r) using sex-specific Z-scores for emergence age and as R.M.S. asymmetry (ad) using absolute age difference in the emergence of antimeres. The first of these two measures corrects the differences in emergence timing variability, and the second does not. For means of comparison we ranked the coefficient of alienation (1-r2) and R.M.S. asymmetry (ad) from lowest to highest, for seven teeth within each jaw. Finally, we ranked permanent tooth emergence order using the male order of means as shown in the table. Where values of r, 1-r2 and (ad) asymmetry are given to two decimal places, the rankings of left-right asymmetry are somewhat different for the two measures within a jaw. They are, however, very similar between the jaws, as indicated by a rank order correlation (rho) for upper and lower

Eruption Sequence Similarities in the Maxilla and Mandible

Maxillary and mandibular dentitions exhibit correspondences to a truly remarkable degree. Correlations of upper and lower opponents (isomeres) in both the deciduous and permanent dentitions are exceeded only slightly by right-left (antimere) correspondences, both in crown size (Garn and Burdi, J Dent Res 50:1407, 1971) and in tooth emergence timing (Garn and Smith, J Dent Res, in press, 1980). Under these circumstances one might also expect inter-jaw correspondences in the order of tooth emergence, such that an M2P2 or P2M2 emergence order in one jaw would be associated with the same sequence in the opposing dentition. To explore this possibility we have made use of two data sources, restricting data analysis to those boys and girls for whom sequences were completely clear for both upper and lower dentitions. The first data base, which we have extensively explored, is that of the Ten-State Nutritional Survey of 1968-1970 (Garn et al., J Dent Res 51:1506, 1972). The second data base includes the participants of the University of Michigan Longitudinal Study (Moyers et al., Standards ofHuman Occlusal Development, Ann Arbor, Center for Human Growth and Development, 1976). The first data base provides 220 black individuals and 284 white individuals, analyzed separately because of population differences in emergence sequence and timing. The second data base yields a total of 60 boys and