Dietary reconstruction of the Amphipithecidae (Primates, Anthropoidea) from the Paleogene of South Asia and paleoecological implications

The primate family, Amphipithecidae, lived during the early Cenozoic in South Asia. In this study, the diet of late middle Eocene amphipithecids from the Pondaung Formation (Central Myanmar) is characterized using three different approaches: body mass estimation, shearing quotient quantification and dental microwear analysis. Our results are compared with other Paleogene amphipithecids from Thailand and Pakistan, and to the other members of the primate community from the Pondaung Formation. Our results indicate a majority of frugivores within this primate community. Pondaungia and “Amphipithecus” included hard objects, such as seeds and nuts, in their diet. Folivory is secondary for these taxa. Myanmarpithecus probably had a mixed diet based on fruit and leaves. Contrasting results and a unique dental morphology distinguish Ganlea from other amphipithecids. These render interpretation difficult but nevertheless indicate a diet tending towards leaves and fruit. However, the anterior dentition of Ganlea suggests that this taxon engaged in seed predation, using its protruding canine as a tool to husk hard fruits and obtain the soft seeds inside. Bahinia and Paukkaungia, two other Pondaung primates, are small (<500 g) and therefore would have depended on insects as their source of protein. As such, they occupied a very different ecological niche from Pondaung amphipithecids. This primate community is then compared with the Eocene-Oligocene primate communities of the Fayum from North Africa. Similarities between the late middle Eocene Pondaung primate community and extant equatorial and tropical South American primate communities are noted.     

The BC200 RNA Gene and Its Neural Expression Are Conserved in Anthropoidea (Primates)

The gene encoding BC200 RNA arose from a monomeric Alu element. Subsequently, the RNA had been recruited or exapted into a function of the nervous system. Here we confirm the presence of the BC200 gene in several primate species among the Anthropoidea. The period following the divergence of New World monkeys and Old World monkeys from their common ancestor is characterized by a significantly higher substitution rate in the examined 5′ flanking region than in the BC200 RNA coding region itself. Furthermore, the conservation of CpG dimers in the RNA coding region (200 bp) is drastically increased compared to the 5′ flanking region (∼400 bp) over all 12 species examined. Finally, the brain-specific expression pattern of BC200 RNA and its presence as a ribonucleoprotein particle (RNP) are conserved in Old World and New World monkeys. Our studies indicate that the gene encoding BC200 RNA was created at least 35–55 million years ago and its presence, mode of expression, and association with protein(s) as an RNP are under selective pressure. Received: 1 December 1997 / Accepted: 3 June 1998     

Dental development in Megaladapis edwardsi (Primates, Lemuriformes): implications for understanding life history variation in subfossil lemurs

Teeth grow incrementally and preserve within them a record of that incremental growth in the form of microscopic growth lines. Studying dental development in extinct and extant primates, and its relationship to adult brain and body size as well as other life history and ecological parameters (e.g., diet, somatic growth rates, gestation length, age at weaning), holds the potential to yield unparalleled insights into the life history profiles of fossil primates. Here, we address the absolute pace of dental development in Megaladapis edwardsi, a giant extinct lemur of Madagascar. By examining the microstructure of the first and developing second molars in a juvenile individual, we establish a chronology of molar crown development for this specimen (M1 CFT = 1.04 years; M2 CFT = 1.42 years) and determine its age at death (1.39 years). Microstructural data on prenatal M1 crown formation time allow us to calculate a minimum gestation length of 0.54 years for this species. Postnatal crown and root formation data allow us to estimate its age at M1 emergence (approximately 0.9 years) and to establish a minimum age for M2 emergence (>1.39 years). Finally, using reconstructions or estimates (drawn elsewhere) of adult body mass, brain size, and diet in Megaladapis, as well as the eruption sequence of its permanent teeth, we explore the efficacy of these variables in predicting the absolute pace of dental development in this fossil species. We test competing explanations of variation in crown formation timing across the order Primates. Brain size is the best single predictor of crown formation time in primates, but other variables help to explain the variation.     

Epiphyseal union and dental eruption in Macaca mulatta

Age of dental eruption and epiphyseal fusion is estimated for the permanent dentition and long bone epiphyses of rhesus macaques (Macaca mulatta), with 299 skeletons of individuals with known age of death, from the Cayo Santiago skeletal collection. Epiphyses at a given joint tend to fuse at the same time. While males and females tend to have the same pattern of epiphyseal fusion, females' epiphyses fuse earlier than those of males, espeically at the elbow and knee joints. The order of epiphyseal fusion in rhesus macaques follows the general primate pattern. Times of dental eruption for males and females are generally the same, except for the relatively late eruption of the canine in the males. The order of eruption follows a common primate pattern (dm2?M1?I1?I2?M2?(P3,P4)?C?M3). Multiple regressions were calculated in order to allow determination of developmental state, or predictions of chronological age, from epiphyseal fusion and/or dental eruption scores in juvenile rhesus macaques. Standard deviations of residuals from these regressions indicate considerable variation in developmental state among aminals of the same chronological age. The lack of correlation between residuals from the separate skeletal and dental regressions, indicates that skeletal and dental development are largely independent.     

Dental function and diet in the Carpolestidae (Primates, Plesiadapiformes)

Microwear analysis has long been used to infer dental function in primates; however, this is the first study to combine microwear and morphometric analyses to infer the dental function of the highly derived dentition of an early Tertiary primate. The Carpolestidae, a family of plesiadapiform primates, are characterized in part by a bladelike lower dentition (P4 and trigonid of M1). This study reveals a dual function of this dental complex. During the preparatory cycle, the tall, vertical enamel surfaces and broad basal lobes on P4 and trigonid of M1 probably functioned to wedge foods apart. This cycle is designated slicing-crushing and is uncommon among mammals, having been documented only for two extinct taxa: the multituberculates and the carpolestids. In addition to this special function, P4 and trigonid of M1 were used extensively with the molars in Phase I shearing. Facet analysis has revealed two new Phase I facets located on P3,4, whose formation is a result of normal Phase I movements and the derived morphology of these teeth. Slicing-crushing, used with Phase I shearing, would probably be most useful in processing food items of combined textures, particularly a soft interior covered by either a brittle or ductile coat, which are characteristic of an omnivorous diet composed of invertebrates, nuts, and seeds.     

The ontogeny of premolar dental wear in Cercocebus albigena (cercopithecidae)

The orientation of striated wear facets on primate teeth serves as a useful guide for reconstructing jaw movements during mastication. Most wear facets on the molars are formed during one of the two well-documented movements, Phase I or Phase II, of the power stroke. Another jaw movement direction, “orthal retraction” (OR) has been proposed to account for a third set of facets occasionally present on the pointed tips of premolars and molars. Evidence advanced here indicates that OR facets on pointed anterior premolars (P₃) of cercopithecoids are actually Phase I facets that have become reoriented as a result of a rotation of this tooth during its eruption. “Orthal retraction” probably does not exist as a discrete masticatory phase.     

Uniquely derived upper molar morphology of Eocene Amphipithecidae (Primates: Anthropoidea): Homology and phylogeny

The extinct Southeast Asian primate family Amphipithecidae is regularly cited in discussions of anthropoid origins, but its phylogenetic position remains controversial. In part, the lack of consensus regarding amphipithecid relationships can be attributed to uncertainty regarding the homology of upper molar structures in this group. Here, we describe a virtually pristine upper molar of Pondaungia cotteri from the late middle Eocene Pondaung Formation of Myanmar, which is the first example of a relatively unworn and well-preserved amphipithecid upper molar ever recovered. The distolingual upper molar cusp in this new specimen of Pondaungia appears to be a lingually displaced and enlarged metaconule, rather than a hypocone or pseudohypocone as previous workers have thought. Reassessment of the upper molar morphology of other amphipithecids and putative amphipithecids reveals a very similar pattern in Siamopithecus, Myanmarpithecus and Ganlea, all of which are interpreted as having upper molars showing many of the same derived features apparent in Pondaungia. In contrast, the upper molar morphology of Bugtipithecus diverges radically from that of undoubted amphipithecids, and the latter taxon is excluded from Amphipithecidae on this basis. Phylogenetic analyses of several character–taxon matrices culled from the recent literature and updated to reflect the new information on amphipithecid upper molar morphology yield similar results. Consensus tree topologies derived from these analyses support amphipithecid monophyly and stable relationships within Amphipithecidae. Amphipithecids appear to be stem members of the anthropoid clade.     

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).     

Aspects of dental development in the orangutan prior to eruption of the permanent dentition

In spite of a resurgence of interest in the interpretation of the sequences of dental development and eruption in various Plio-Pleistocene hominoids as being either “modern human” or “ape-like,” the body of comparative material on the extant hominoids remains deficient in critical areas. In concert with recent attempts to rectify this situation, we present the results of our studies on dental morphogenesis in the orangutan. We have focused on the growth and eruption of the deciduous dentition as well as early stages of permanent tooth formation and have found that 1) many permanent teeth develop earlier than was thought, 2) differences exist between development in the upper and in the lower jaw, and 3) states of tooth formation can vary significantly among individuals of similar chronological age or tooth eruption status.     

Pattern and pace of dental eruption in Tarsius

This article uses data on the dental eruption pattern and life history of Tarsius to test the utility of Schultz's rule. Schultz's rule claims a relationship between the relative pattern of eruption and the absolute pace of dental development and life history and may be useful in reconstructing life histories in extinct primates. Here, we document an unusual eruption pattern in Tarsius combining early eruption (relative to molars) of anterior replacement teeth (P2 and incisors) and relatively late eruption of the posterior replacement teeth (C, P3, and P4). This eruption pattern does not accurately predict the "slow" pace of life documented for Tarsius [Roberts: Int J Primatol 15 (1994) 1-28], nor aspects of life history directly associated with dental development as would be expected using Schultz's rule. In Tarsius, the anterior teeth and M1 erupt at an early age and therefore are not only fast in a relative sense but also fast in an absolute sense. This seems to be related to a developmental anomaly in the deciduous precursor teeth, which are essentially skipped. This decoupling among dental eruption pattern, dental eruption pace, and life history pace in Tarsius undermines the assumptions that life histories can accurately be described as "fast" or "slow" and that dental eruption pattern alone can be used to infer overall life history pace. The relatively and absolutely early eruption of the anterior dentition may be due to the utility of these front teeth in early food acquisition rather than with the pace of life history.     

Continuous dental eruption identifies Sts 5 as the developmentally oldest fossil hominin and informs the taxonomy of Australopithecus africanus

The relatively small Australopithecus africanus specimen Sts 5 has figured prominently in taxonomic debates, and the determination of this specimen as a young male or an elderly female has the potential to offer a great deal of resolution on this question. Sts 5 has been argued to be either a small, immature male or a mature female based on a variety of characters.     

Dental eruption sequence and eruption times in Erythrocebus patas

Erythrocebus patas has a short inter-birth interval, juveniles become independent from their mother early, females are young at first birth, and adult females have a high mortality rate. According to Schultz’s rule, the molars of fast-growing and shorter-lived primate species erupt early relative to the replacement teeth. Based on the life history of E. patas, we hypothesized that the molars would erupt before the replacement teeth and/or that the eruption time of its molars would be early. The purpose of the present study was to determine the dental eruption sequence and eruption times for E. patas and to test our hypothesis. The eruption sequence for the permanent teeth of E. patas is \frac\textM1  \textI1  \textI2  \textM2  \textP3  \textP4  [\textC  \textM3]\textM1  \textI1  \textI2  \textM2  \textP4  [\textP3  \textC]\textM3 \frac{{{\text{M1}}\;{\text{I1}}\;{\text{I2}}\;{\text{M2}}\;{\text{P3}}\;{\text{P4}}\;[{\text{C}}\;{\text{M3}}]}}{{{\text{M1}}\;{\text{I1}}\;{\text{I2}}\;{\text{M2}}\;{\text{P4}}\;[{\text{P3}}\;{\text{C}}]{\text{M3}}}} in males and \frac\textM1  \textI1  \textI2  [\textM2  \textP4  \textP3  \textC]\textM3\textM1  \textI1  \textI2  [\textM2  \textP4  \textP3  \textC]\textM3 \frac{{{\text{M1}}\;{\text{I1}}\;{\text{I2}}\;[{\text{M2}}\;{\text{P4}}\;{\text{P3}}\;{\text{C}}]{\text{M3}}}}{{{\text{M1}}\;{\text{I1}}\;{\text{I2}}\;[{\text{M2}}\;{\text{P4}}\;{\text{P3}}\;{\text{C}}]{\text{M3}}}} in females. Because these sequences constitute the general pattern seen in cercopithecines, Schultz’s rule could not be applied to E. patas. The emergence time of upper and lower first molar (M1) is earlier in E. patas than in macaques, baboons, and mandrills and is similar to that in Chlorocebus aethiops. The emergence time of deciduous upper and lower fourth premolar (dp4) is similar to that in the above-mentioned cercopithecines but is later than that in Ch. aethiops. The emergence times of upper and lower second molar (M2) and upper and lower third molar (M3) in E. patas are earlier than those in the above-mentioned cercopithecines but later than those in Ch. aethiops. However, the intervals of the emergence time between each permanent molar in E. patas are similar to those of the above-mentioned cercopithecines. The early appearance of M2 and M3 in E. patas is related to the short interval of emergence time between dp4 and M1.     

Patterns of dental emergence in early anthropoid primates from the Fayum Depression,Egypt

Abstract

Paleontological field work in the Fayum Depression of Egypt has produced a remarkable diversity of fossil anthropoids, and this, combined with advances in genetic analyses of living anthropoids, has led to establishment of a temporal and phylogenetic framework for anthropoids that is achieving some degree of consensus. Less well understood are the evolutionary mechanisms and selective factors behind the origin and early diversification of anthropoids. One area that has remained under explored is investigation into the life history patterns of early anthropoids, a major omission given that understanding patterns of growth and development is essential for interpreting the paleobiology of fossil species. Here we detail dental emergence sequences for five species in four families of early anthropoid primates from the Fayum, and use these data to test Schultz’s Rule concerning the timing of emergence of molars versus premolars in mammals. Two important results are generated: (1) only one species had a dental eruption sequence identical to that observed among crown catarrhine primates; and (2) in all cases, the permanent canine was the last post-incisor dental element to fully erupt, a finding that may be significant for interpreting early anthropoid behavioral strategies.     

Dental remains from the Grotte du Renne at Arcy-sur-Cure (Yonne)

Human remains associated with the earliest Upper Paleolithic industries are sparse. What is preserved is often fragmentary, making it difficult to accurately assign them to a particular species. For some time it has been generally accepted that Neandertals were responsible for the Chatelperronian and anatomically modern humans for the early Aurignacian industries. However, the recent re-dating of several of the more-complete modern human fossils associated with the early Aurignacian (e.g., Vogelherd) has led some to question the identity of the makers and the context of these early Upper Paleolithic industries. The Grotte du Renne at Arcy-sur-Cure, France has yielded many hominin remains, from Mousterian, Chatelperronian, Aurignacian, and Gravettian layers. Previously, a child's temporal bone from the Chatelperronian Layer Xb was recognized as belonging to a Neandertal; however, most of the teeth from Chatelperronian layers VIII-X remain unpublished. We describe the dental remains from the Chatelperronian layers, place them in a comparative (Mousterian Neandertal and Upper Paleolithic modern human) context, and evaluate their taxonomic status. The teeth (n = 29) represent a minimum of six individuals aged from birth to adult. The permanent dental sample (n = 15) from the Chatelperronian layers of Arcy-sur-Cure exhibits traits (e.g., lower molar mid-trigonid crest) that occur more frequently in Neandertals than in Upper Paleolithic modern humans. Furthermore, several teeth show trait combinations, including Cusp 6/mid-trigonid crest/anterior fovea in the lower second molar, that are rare or absent in Upper Paleolithic modern humans. The deciduous teeth (n = 14) significantly increase the sample of known deciduous hominin teeth and are more similar to Mousterian Neandertals from Europe and Asia than to Upper Paleolithic modern humans. Thus, the preponderance of dental evidence from the Grotte du Renne strongly supports that Neandertals were responsible for the Chatelperronian industry at Arcy-sur-Cure.     

Tooth development and histology patterns in lamniform sharks (Elasmobranchii,Lamniformes) revisited

The dentition of lamniforme sharks exhibits several characters that have been used extensively to resolve the phylogenetic relationships of extant taxa, yet some uncertainties remain. Also, the development of different teeth of a tooth file within the jaws of most extant lamniforms has not been documented to date. High‐resolution micro‐computed tomography is used here to re‐evaluate the importance of two dental characters within the order Lamniformes, which were considered not to be phylogenetically informative, the histotype and the number of teeth per tooth file. Additionally, the development and mineralization patterns of the teeth of the two osteodont lamniforms Lamna nasus and Alopias superciliosus were compared. We discuss the importance of these dental characters for phylogenetic interpretations to assess the quality of these characters in resolving lamniform relationships. The dental characters suggest that (1) Lamniformes are the only modern‐level sharks exhibiting the osteodont histotype, (2) the osteodont histotype in lamniform sharks is a derived state in modern‐level sharks (Elasmobranchii), (3) the osteodont type, conversely is convergently achieved when the clade Chondrichthyes is considered and thus might comprise a functional rather than a phylogenetic signal, and (4) there is an increase in the number of teeth per file throughout lamniform phylogeny. Structural development of the teeth of L. nasus and A. superciliosus is congruent with a previous investigation of the lamniform shark Carcharodon carcharias. J. Morphol. 277:1584–1598, 2016. © 2016 Wiley Periodicals, Inc.     

Early and Middle Pleistocene hominins from Atapuerca (Spain) show differences in dental developmental patterns

The Bayesian statistical approach considers teeth as forming a developmental module, as opposed to a tooth-by-tooth analysis. This approach has been employed to analyze Upper Pleistocene hominins, including Neandertals and some anatomically modern humans, but never earlier populations. Here, we show its application on five hominins from the TD6.2 level of the Gran Dolina site (Homo antecessor, Early Pleistocene) and the Sima de los Huesos site (Middle Pleistocene) of the Sierra de Atapuerca (Burgos, northern Spain). Our results show an advanced development of the third molars in both populations with respect to modern Homo sapiens. In addition, the Sima de los Huesos hominins differ from H. sapiens and H. antecessor in the relatively advanced development of their second molar. The relative mineralization of I1/M1 in H. antecessor appears to be similar to that of modern humans, as opposed to that of Neandertals, which appear to be unique. These observations, combined with reduced enamel formation times and the advanced development of the third molars, appear to indicate a shorter ontogenetic period in the hominins from Gran Dolina and Sima de los Huesos in comparison to modern human average.     

Sequences and timing of dental eruption in semi-free-ranging mandrills (Mandrillus sphinx)

The chronology of tooth emergence is often used to examine the growth and development of individuals and to compare life histories across species. Emergence patterns are also used to age animals and to infer life history influences for extinct species. However, comparative studies of primates are hindered by a lack of dental development data for many species. Here we describe the sequences and timing of tooth emergence for a large sample of semi-free-ranging mandrills (Mandrillus sphinx) and compare this with other life history variables for this species. Deciduous dentition emerged in the sequence i1 i2 c p3 p4. The augmented sequence (including information about variability in emergence sequence) was i1 i2 [c p3] p4 for the female maxilla and the male mandible, and i1 i2 c p3 p4 for the female mandible and the male maxilla. Deciduous dentition was complete by 5.0 months in females and 6.4 months in males. The permanent dentition began to emerge at 26 months, and complete adult dentition had emerged by 68 months for males and 85 months for females. Sex differences occurred in the augmented eruption sequences: females M1 I1 I2 [M2 C] P3 P4 M3, males M1 I1 [I2 M2] [P4 = P3 = C] M3. The order of tooth eruption and the occurrence of sequence polymorphisms were very similar to those observed for baboons and macaques. Comparison with life history variables showed that mandrills have complete deciduous dentition at weaning, females possess both adult incisors and M1 when they first reproduce, but still have deciduous canines and premolars, and that both sexes have full adult dentition before they attain their full adult stature and mass.