Schultz's unruly rule: dental developmental sequences and schedules in small-bodied, folivorous lemurs

Schultz's rule (as reconstructed by Smith) states that there is a relationship between the pattern (or relative order) of eruption of molar versus secondary (replacement) teeth and the overall pace (or absolute timing) of growth and maturation. Species with 'fast' life histories (rapid dental development, rapid growth, early sexual maturation, short life spans) are said to exhibit relatively early eruption of the molars and late eruption of the secondary replacement teeth (premolars, canines, incisors), whereas species with 'slow' life histories are said to exhibit relatively late eruption of the molars and early eruption of the secondary dentition. In a recent review, B.H. Smith noted that primates with tooth combs might violate this rule because tooth combs tend to erupt early, regardless of the pace of life history. We show that exceptions to Schultz's rule among lemurs are not limited to the relative timing of eruption of the tooth comb. Rather, among lemurs, some species with extremely accelerated dental development exhibit a pattern of eruption of molars and of secondary teeth in direct opposition to the expectations of Schultz's rule. We focus particularly on the pattern (order) and pace (absolute timing) of dental development and eruption in Avahi and Lepilemur - two relatively small, nocturnal folivores with rapid dental development. These taxa differ markedly in their eruption sequences (the premolars erupt after M2 and M3 in Lepilemur but not Avahi ). We offer an explanation for the failure of Schultz's rule to predict these differences. Schultz's rule presumes that eruption timing is dependent on the size of the jaw and that, therefore, molar crown formation and eruption will be delayed in species with slow-growing jaws. We show that a variety of processes (including developmental imbrication) allows the crowns of permanent teeth to form and to erupt into jaws that might appear to be too small to accommodate them.     

First Fossil Evidence for the Advance of Replacement Teeth Coupled with Life History Evolution along an Anagenetic Mammalian Lineage

In mammals that grow up more slowly and live longer, replacement teeth tend to appear earlier in sequence than in fast growing mammals. This trend, known as ‘Schultz''s Rule’, is a useful tool for inferring life histories of fossil taxa. Deviations from this rule, however, suggest that in addition to the pace of life history, ecological factors may also drive dental ontogeny. Myotragus balearicus is an extinct insular caprine that has been proved to be an excellent test case to correlate morphological traits with life history. Here we show that Myotragus balearicus exhibits a slow signature of dental eruption sequence that is in agreement with the exceptionally slow life history of this species, thus conforming to ‘Schultz''s Rule’. However, our results also show an acceleration of the absolute pace of development of the permanent incisors in relation to that of the posterior teeth. The rodent-like incisors of Myotragus balearicus erupted early not only in relative but also in absolute terms (chronological age), suggesting that feeding characteristics also plays an important role in dental ontogeny. This is in agreement with ecological hypotheses based on primates. Our study documents a decoupling of the pace of development of teeth in mammals that is triggered by different selection pressures on dental ontogeny. Moreover, we show that Myotragus kopperi from the early Pleistocene (a direct ancestor of the late Pleistocene-Holocene M. balearicus) follows the pattern of first incisor replacement known in living bovids. Hence, the advance in the eruption sequence of the first incisors occurs along the Myotragus evolutionary lineage over a period of about 2.5 Myr. To our knowledge, this is the first fossil evidence of an advance of the emergence of the permanent first incisor along an anagenetic mammalian lineage.     

Platyrrhine dental eruption sequences

To determine dental eruption sequences of extant platyrrhines, 367 mandibles and maxillae of informative juvenile specimens from all 16 genera were scored for presence of permanent teeth including three intermediate eruption stages following Harvati (Am J Phys Anthropol 112 (2000) 69-85). The timing of molar eruption relative to that of the anterior dentition is variable in platyrrhines. Aotus is precocious, with all molars erupting in succession before replacement of any deciduous teeth, while Cebus is delayed in M2-3 eruption relative to I1-2. Callitrichines have a distinct tendency toward delayed canine and premolar development. Platyrrhine eruption sequences presented here show some evidence of conformity to Schultz's Rule, with relatively early replacement of deciduous dentition in "slower"-growing animals. The relationship of dental eruption sequences to degree of folivory, body mass, brain mass, and dietary quality is also examined. The early eruption of molars relative to anterior teeth in Pithecia, Chiropotes, and Cacajao, in comparison to genera such as Ateles, Lagothrix, and Alouatta, showing relatively later eruption of the molars, appears to be consistent with current phylogenetic hypotheses. Schultz (Am J Phys Anthropol 19 (1935) 489-581) postulated early relative molar eruption as the primitive dental eruption schedule for primates. The extremely early molar eruption of Aotus versus Callicebus (where both incisors erupt before M2 and M3, with M3 usually last) may lend support to the status of Aotus as a basal taxon. The early relative molar eruption of the fossil platyrrhine species Branisella boliviana is also consistent with this hypothesis (Takai et al.: Am J Phys Anthropol 111 (2000) 263-281).     

Dental Eruption Sequences in Fossil Colobines and the Evolution of Primate Life Histories

Unlike other catarrhines, colobines show early molar eruption relative to that of the anterior dentition. The pattern is variable, with Asian genera (Presbytina) showing a greater variability than the African genera (Colobina). The polarity of early relative molar eruption, as well as the degree to which it is related to phylogeny, are unclear. Schultz (1935) suggested that the trend reflects phylogeny and is primitive for catarrhines. More recently, however, researchers have proposed that life history and dietary hypotheses account for early relative molar eruption. If the colobine eruption pattern is primitive for catarrhines, it implies that cercopithecines and hominoids converged on delayed relative molar eruption. Alternatively, if the colobine condition is derived, factors such as diet and mortality patterns probably shaped colobine eruption patterns. Here we update our knowledge on eruption sequences of living colobines, and explore the evolutionary history of the colobine dental eruption pattern by examining fossil colobine taxa from Eurasia (Mesopithecus) and Africa (Kuseracolobus aramisi and Colobus sp.) and the basal cercopithecoid Victoriapithecus macinnesi. We scored specimens per Harvati (2000). The Late Miocene-Early Pliocene Mesopithecus erupts the second molar early relative to the incisors, while the Early Pliocene Kuseracolobus aramisi does not. These results demonstrate that the common colobine tendency for early molar eruption relative to the anterior dentition had appeared by the Late Miocene, and that some of the diversity observed among living colobines was already established in the Late Miocene/Early Pliocene. We discuss the implications of these results for phylogenetic, life history, and dietary hypotheses of dental development.     

Dental Eruption Series and Replacement Pattern in Miocene <Emphasis Type="Italic">Prosantorhinus</Emphasis> (Rhinocerotidae) as Revealed by Macroscopy and X-ray: Implications for Ontogeny and Mortality Profile

Fossil evidence of complete sequences of dental ontogeny in extinct mammals is rare but contains valuable information on the animal’s physiology, life history, and individual age. Here, we analyzed an exceptionally high number of juvenile dentaries at different developmental stages including highly fragile tooth germs of the extinct rhinoceros Prosantorhinus germanicus from the Miocene fossil lagerstätte Sandelzhausen in Germany. We used dental wear stages, eruption stages, and tooth germ development in order to reconstruct the tooth replacement pattern for P. germanicus. The results allow for the distinction of 11 dental eruption stages and document a tooth eruption sequence of (d2, d3), (d1, d4), m1, m2, p2, p3, p4, m3; a pattern identical to that reported for the extant African rhinoceros, Diceros bicornis. Moreover, our findings indicate that P. germanicus falls into the life history category of slow-growing, long-living mammals. The dental eruption stages of the fossil rhinoceros were correlated with data of living rhinoceroses in order to gain insight into the age-at-death distribution of P. germanicus at Sandelzhausen. The juvenile mortality profile of P. germanicus shows a trend of selective mortality at an inferred age range of about 3 months to 3 years. As this age range represents a life phase of increased natural risk of mortality, our findings indicate a gradual accumulation of corpses (attritional fossil assemblage). This result supports the interpretation of a taphocenosis found at the Sandelzhausen fossil site.     

Ecological factors affecting eruption timing of mandibular teeth in roe deer

Increasing evidence suggests that conditions in early life have important consequences for body size and fitness in mammals. As regards herbivores, teeth play a central role in the long-term performance of individuals. So far, however, patterns of teeth eruption have been scarcely investigated in relation to environmental and climatic factors experienced by herbivores. We described the eruption timing of mandibular teeth in a population of roe deer (Capreolus capreolus) located in the Apennines (Central Italy), through the analysis of 2161 jaws of fawns (1176 females and 985 males) shot in their first winter of life over three hunting seasons (2013–2015). Results showed that the percentage of juveniles exhibiting permanent teeth depends on the cohort. Among the factors that may affect both incisiviform and molariform teeth replacement timing, our findings include body mass and population density. Additional factors determining the relative speed of teeth replacement are (1) food availability for the mother during the last part of gestation, the birth period and the lactation, (2) winter temperature experienced by the mother, and (3) temperature experienced by fawns during their first summer and autumn. Besides, for the first time in literature, elevation was reported to delay front teeth replacement. A greater number of climatic factors were found to shape the eruption timing of the third molar (M₃) in comparison to that of incisiviform teeth. Also, a different pattern was found in males and females. The eruption of M₃ is, indeed, a costly and long-lasting process requesting optimal nutritional conditions and the meeting of a threshold jaw size. Our results indicate a strong correlation between environmental conditions and eruption process, i.e., between resource availability during the gestation and rearing periods and eruption timing.     

Gingival eruption sequences of permanent teeth in early hominids.

Gingival eruption of the permanent teeth of Australopithecus, Paranthropus, and early Homo, diagnosed from enamel scratches and facets, is similar save for two sequences: eruption of the canines relative to the premolars which may be sexually dimorphic; and agenesis of M3 with delayed eruption of M2, first seen in Homo at two million years. Gingival eruption sequences are similar also for early and modern Homo, except that in some individuals today M3, M2, M1 and I2 take longer to form and emerge through the gingiva as functioning teeth. Probably, from two million years to the present in the evolutionary history of Homo dental development slowed-down. More and more of ontogeny has been taken over for eruption.     

Teeth, brains, and primate life histories

This paper explores the correlates of variation in dental development across the order Primates. We are particularly interested in how 1) dental precocity (percentage of total postcanine primary and secondary teeth that have erupted at selected absolute ages and life cycle stages) and 2) dental endowment at weaning (percentage of adult postcanine occlusal area that is present at weaning) are related to variation in body or brain size and diet in primates. We ask whether folivores have more accelerated dental schedules than do like-sized frugivores, and if so, to what extent this is part and parcel of a general pattern of acceleration of life histories in more folivorous taxa. What is the adaptive significance of variation in dental eruption schedules across the order Primates? We show that folivorous primate species tend to exhibit more rapid dental development (on an absolute scale) than comparably sized frugivores, and their dental development tends to be more advanced at weaning. Our data affirm an important role for brain (rather than body) size as a predictor of both absolute and relative dental development. Tests of alternative dietary hypotheses offer the strongest support for the foraging independence and food processing hypotheses.     

Dental eruption sequence among colobine primates

Dental development is one aspect of growth that is linked to diet and to life history but has not been investigated among colobines since the work of Schultz [1935]. This study establishes the dental eruption sequence for several colobine species and compares it to that of other catarrhines. The mandibles and maxillae of two hundred and four juvenile colobine specimens were scored for presence or absence of permanent teeth and for stages of partial eruption. Eruption was defined as ranging between tooth emergence (any part of a tooth crown above the alveolar margin) and full occlusion, with three intermediate levels manifest between these boundaries. In African colobines, represented by C. guereza, C. angolensis and P. badius, M2 erupts before I2, and in C. angolensis it also erupts before I1. The canine is delayed, erupting after the premolars in females and after M3 in males. Asian colobines show greater diversity in eruption sequences. Nasalis shows no early eruption of the molars and is very similar to Macaca. In Trachypithecus and Pygathrix M(2) erupts before I(2). The canine in Trachypithecus is delayed, erupting after the premolars and, in some males, after M3. In Presbytis M2 erupts before both incisors; M3 erupts before C in both sexes, and often before both premolars. Although the actual timing of eruption is unknown, all colobine species examined except N. larvatus showed some degree of relatively early eruption of M2 and M3. The lack of this tendency in Nasalis sets this genus apart from all other colobines represented in this study. Dental eruption sequence is thought to reflect life history patterns. Early molar eruption in colobines was thought by Schultz (1935) to be a primitive character reflecting shorter life history. Faster growth rates found in folivorous primates have been interpreted as being related to an adaptation to folivory (Leigh 1994), and early eruption of molars may be part of this dietary specialization. The relationships between dental development and both diet and life history are investigated.     

A discussion of dental homology with reference to primates

The inconsistencies which exist when the traditional tooth-to-bony-landmark/tooth-to-occlusal-relationship criteria of identification of teeth are maintained are discussed. It is pointed out how these (e.g., "the canine is the tooth behind the premaxillary-maxillary suture") can be falsified. It is also suggested that some mammals, including Tarsius and Homo sapiens, develop homologies of three sets of "teeth," and that the "adult" antemolar dentition of a mammal may be composed of retained deciduous teeth as well as permanent teeth. Following a revision of dental homologies in most primates, an approach to reevaluating dental homologies is proposed, and a model of tooth "loss" presented.     

Tooth replacement in the upper jaw of the rainbow trout (Salmo gairdneri).

The present paper describes the pattern of tooth replacement in the upper jaw of two size ranges of rainbow trout (standard lengths 12-15 cm and 20-23 cm) as determined from wax impressions of the dentitions taken twice weekly on anaesthetised fish. There was considerable variation in the nature of replacement waves (lines constructed on dental charts linking eruption times of alternate teeth) between fish for both the premaxillary/maxillary and vomerine/palatine rows. The wave patterns obtained showed the same consistency of form for any one animal which is to be expected when consecutive generations show constant or proportionately changing life spans. Data relating to the life span of the teeth is given. The results are compared with those derived for the lower jaw and the significance of wave form discussed.     

Front dentition of the omomyiformes (Primates)

Within the primates the front dentition plays a major role in the classification of the different taxa. The extant strepsirhines are clearly characterized by the possession of a tooth comb. Tarsius differs in this complex by a construction which remembers the beak of an owl (vertically implanted medial incisors, upper pair bigger than mandibular pair). The front teeth of the extinct Microchoeridae are described. The dental formula of the group is discussed and compared with the Omomyidae. The wear pattern presents evidence of a dental comb as early as the Late Eocene.     

Does Hibernation Slow the “Pace of Life” in Dwarf Lemurs (Cheirogaleus spp.)?

The classic mammalian life history continuum polarizes small-bodied species that live fast and die young from larger-bodied species with longer life spans and reduced adult mortality rates. Hibernating mammals, however, deviate from this pattern and tend to have short gestations, accelerated early infant growth in preparation for hibernation, retardation of growth and development in association with hibernation, and delayed achievement of full adult size and first reproduction. This pattern has never been systematically tested in hibernating primates. We examine body mass, growth trajectories, dental development, and reproductive status of dwarf lemurs (genus Cheirogaleus), the only obligate hibernators among primates, to determine whether life histories in these small-bodied strepsirrhines vary in accord with expectations based on the use of energy-saving strategies. We show that this pattern does indeed hold for primates. Unlike similarly sized nonhibernating strepsirrhines such as bush babies (genus Galago), wild dwarf lemurs display short gestation and lactation periods, rapid early (pre-hibernation) growth and development followed by retardation of growth and dental development during hibernation, delayed attainment of adult size, and delayed first reproduction. We conclude that hibernation constrains the degree to which dwarf lemurs can experience life in the fast lane. Cheirogaleus have life history profiles that are neither fast nor slow but a combination of both.     

Critical revision of the alleged delayed dental eruption in South American “ungulates”

The endemic South American “ungulates” (SANU) were traditionally assumed to be a monophyletic offshoot of the Granorder Ungulata, but the current reorganization of the extant ungulates in Laurasiatheria and Afrotheria (based on molecular data) leaved them in an undetermined systematic position. The delayed dental eruption versus cranial growth was proposed as a hard-tissue synapomorphy of Afrotheria. In a recent paper, at least some endemic SANU (Notoungulata, Astrapotheria, and possibly Pyrotheria) were interpreted as allied to Afrotheres by having a late replacement of deciduous cheek teeth. This statement was based on: (1) the usual occurrence within these groups of individuals with deciduous and permanent teeth; (2) the individual size (estimated comparing the length/width ratio of cheek teeth) of specimens with permanent premolars erupted is indistinguishable from that of specimens with deciduous premolars (putative juveniles), and (3) the retention of at least dP1–dP3 in adult specimens of Parastrapotherium (Astrapotheria). Herein we critically examine the presumed existence of delayed dental eruption in astrapotheres, pyrotheres and xenungulates and the assumptions on which it was based. The alleged evidences supporting the occurrence of delayed dental eruption in SANU arise from misinterpreted information from the literature and conceptual mistakes (i.e. delayed dental eruption versus cranial growth was confused with delayed replacement of premolars versus molar eruption). Based on examination of at-hand specimens, we found that there is no evidence for a delayed premolar replacement relative to the eruption of the molars in astrapotheres, pyrotheres, and xenungulates. A delayed dental eruption in relation to jaw growth does not occur at least in Astrapotherium magnum. Although a very recent study proposed close relationships among afrotheres and at least notoungulates and xenungulates, a more complete analysis is still needed to elucidate the evolutionary relationships of astrapotheres and pyrotheres.     

A Faithful Record of Stressful Life Events Recorded in the Dental Developmental Record of a Juvenile Gorilla

The pattern and rate of dental development are critical components of the life history of primates. Much recent research has focused on dental development in chimpanzees and other hominoids, but comparatively little is known about dental development in Gorilla. To date, dental chronologies for Gorilla are based on a sample of 1 and information about variations in the time and timing of crown initiation and completion is lacking. We provide data on dental development in 1 captive, juvenile, female, western lowland Gorilla gorilla gorilla of known age, sex, life events, and date of death (carefully documented as part of zoo records) that experienced various physical insults during her first year of life. The perfect natural experiment allowed us to test the association of the timing of accentuated stress lines in teeth with significant physiological and psychological events during ontogeny of this juvenile gorilla. We analyzed histological sections from 14 permanent teeth (maxillary and mandibular I1-M2) and assessed crown initiation (CI) and crown formation times (CFT) using short- and long-period incremental lines in both enamel and dentine; they are advanced for all teeth compared to previously published chronology. The data suggest a relatively accelerated pace of dental development in gorillas compared to chimpanzees and fit an emerging pattern of an accelerated life history schedule in gorillas. Data on the timing of major accentuated lines in the developing dentition are tightly associated with exact dates of surgical procedures and follow-up hospital visits as recorded on zoo medical records. Our data highlight the importance of captive individuals with well-documented medical records for studying life history.

Dental homologies in lamniform sharks (Chondrichthyes: Elasmobranchii).

The dentitions of lamniform sharks are said to exhibit a unique heterodonty called the "lamnoid tooth pattern." The presence of an inflated hollow "dental bulla" on each jaw cartilage allows the recognition of homologous teeth across most modern macrophagous lamniforms based on topographic correspondence through the "similarity test." In most macrophagous lamniforms, three tooth rows are supported by the upper dental bulla: two rows of large anterior teeth followed by a row of small intermediate teeth. The lower tooth row occluding between the two rows of upper anterior teeth is the first lower anterior tooth row. Like the first and second lower anterior tooth rows, the third lower tooth row is supported by the dental bulla and may be called the first lower intermediate tooth row. The lower intermediate tooth row occludes between the first and second upper lateral tooth rows situated distal to the upper dental bulla, and the rest of the upper and lower tooth rows, all called lateral tooth rows, occlude alternately. Tooth symmetry cannot be used to identify their dental homology. The presence of dental bullae can be regarded as a synapomorphy of Lamniformes and this character is more definable than the "lamnoid tooth pattern." The formation of the tooth pattern appears to be related to the evolution of dental bullae. This study constitutes the first demonstration of supraspecific tooth-to-tooth dental homologies in nonmammalian vertebrates.     

Deciduous dentition and eruption pattern in late Miocene Pachyrukhinae (Hegetotheriidae,Notoungulata) from La Pampa Province,Argentina

The study of juvenile remains of Paedotherium Burmeister from Cerro Azul Formation (La Pampa Province, Argentina; late Miocene) is presented. Upper and lower deciduous dentition (or permanent molars supposed to be associated with non-preserved deciduous teeth) are recognised. Several ontogenetic stages are distinguished among juveniles, according to the degree of wear and the replaced deciduous teeth. Besides, some morphological and metrical differences are observed along the crown height. Deciduous cheek teeth are high-crowned and placed covering the apex of the corresponding permanent tooth. The height of the crown and the degree of wear allow establishing the pattern of dental replacement of deciduous and permanent premolars in a posterior–anterior direction (DP/dp4–2 and P/p4–2), as well as the eruption of M/m3 before DP/dp4 is replaced. Some of the studied remains are recognised as young individuals of Tremacyllus Ameghino, but with complete permanent dentition, which leads to propose a different timing in the dental replacement with respect to Paedotherium; they also allow the establishment of an opposite premolar eruption pattern, from P/p2 to P/p4. This knowledge of the deciduous dentition of Paedotherium suggests the need of revising the morphological and metrical characters previously used for defining species within this taxon.     

Growth, function and homology: aspects of dental replacement in toothcombed strepsirhines.

In maturing juvenile lemurs and lorises, it was found that the anteriormost lower deciduous premolar migrates forward and may become associated with the teeth of the toothcomb; this is similar to previous observations on the dentition of indriines. The mesial shift of dp2 appears to be associated with the eruption of P2 but, more importantly, also with replacement of the deciduous by the permanent teeth of the toothcomb--which is a period of functional disruption at the front of the jaw. It is suggested that this growth-related phenomenon should not be confused with other aspects of dental development and eruption which might be indicative of homology.     

The Evolution of Dental Eruption Sequence in Artiodactyls

The sequence of eruption of the second generation of teeth varies across taxa, is highly functional, and is strongly influenced by genetic effects. We assessed postcanine dental eruption sequence across artiodactyls in order to test two hypotheses: 1) dental eruption sequence is a good phylogenetic character for artiodactyls; and, 2) eruption sequence is adaptive and associated with life history variables like postnatal growth and longevity in artiodactyls (Schultz’s Rule). We examined postcanine eruption sequence in 81 genera (100 species) spanning ten families of Artiodactyla. Our ancestral state reconstruction supports the interpretation that the third molar erupted last in the ancestor of Artiodactyla, and that the fourth premolar erupted after the third molar in the ancestor of Ruminantia. Our results indicate that eruption of the third molar last evolved secondarily in the caprines, likely sometime in the Miocene. Overall, our results support the hypothesis that dental eruption sequence is phylogenetically conserved in artiodactyls. Caprines occupy high elevation habitats, and we hypothesize that evolution of their unique dental eruption sequence may be associated with limited resource availability in high elevation mountain systems and the necessity to process a wide range of vegetation types.