Vincent Lazzari

Dental evidence for ontogenetic differences between modern humans and Neanderthals

Humans have an unusual life history, with an early weaning age, long childhood, late first reproduction, short interbirth intervals, and long lifespan. In contrast, great apes wean later, reproduce earlier, and have longer intervals between births. Despite 80 y of speculation, the origins of these developmental patterns in Homo sapiens remain unknown. Because they record daily growth during formation, teeth provide important insights, revealing that australopithecines and early Homo had more rapid ontogenies than recent humans. Dental development in later Homo species has been intensely debated, most notably the issue of whether Neanderthals and H. sapiens differ. Here we apply synchrotron virtual histology to a geographically and temporally diverse sample of Middle Paleolithic juveniles, including Neanderthals, to assess tooth formation and calculate age at death from dental microstructure. We find that most Neanderthal tooth crowns grew more rapidly than modern human teeth, resulting in significantly faster dental maturation. In contrast, Middle Paleolithic H. sapiens juveniles show greater similarity to recent humans. These findings are consistent with recent cranial and molecular evidence for subtle developmental differences between Neanderthals and H. sapiens. When compared with earlier hominin taxa, both Neanderthals and H. sapiens have extended the duration of dental development. This period of dental immaturity is particularly prolonged in modern humans.

Late Middle Eocene primate from Myanmar and the initial anthropoid colonization of Africa

Reconstructing the origin and early evolutionary history of anthropoid primates (monkeys, apes, and humans) is a current focus of paleoprimatology. Although earlier hypotheses frequently supported an African origin for anthropoids, recent discoveries of older and phylogenetically more basal fossils in China and Myanmar indicate that the group originated in Asia. Given the Oligocene-Recent history of African anthropoids, the colonization of Africa by early anthropoids hailing from Asia was a decisive event in primate evolution. However, the fossil record has so far failed to constrain the nature and timing of this pivotal event. Here we describe a fossil primate from the late middle Eocene Pondaung Formation of Myanmar, Afrasia djijidae gen. et sp. nov., that is remarkably similar to, yet dentally more primitive than, the roughly contemporaneous North African anthropoid Afrotarsius. Phylogenetic analysis suggests that Afrasia and Afrotarsius are sister taxa within a basal anthropoid clade designated as the infraorder Eosimiiformes. Current knowledge of eosimiiform relationships and their distribution through space and time suggests that members of this clade dispersed from Asia to Africa sometime during the middle Eocene, shortly before their first appearance in the African fossil record. Crown anthropoids and their nearest fossil relatives do not appear to be specially related to Afrotarsius, suggesting one or more additional episodes of dispersal from Asia to Africa. Hystricognathous rodents, anthracotheres, and possibly other Asian mammal groups seem to have colonized Africa at roughly the same time or shortly after anthropoids gained their first toehold there.

Anthropoid versus strepsirhine status of the African Eocene primates Algeripithecus and Azibius: craniodental evidence.

Recent fossil discoveries have demonstrated that Africa and Asia were epicentres for the origin and/or early diversification of the major living primate lineages, including both anthropoids (monkeys, apes and humans) and crown strepsirhine primates (lemurs, lorises and galagos). Competing hypotheses favouring either an African or Asian origin for anthropoids rank among the most hotly contested issues in paleoprimatology. The Afrocentric model for anthropoid origins rests heavily on the >45 Myr old fossil Algeripithecus minutus from Algeria, which is widely acknowledged to be one of the oldest known anthropoids. However, the phylogenetic position of Algeripithecus with respect to other primates has been tenuous because of the highly fragmentary fossils that have documented this primate until now. Recently recovered and more nearly complete fossils of Algeripithecus and contemporaneous relatives reveal that they are not anthropoids. New data support the idea that Algeripithecus and its sister genus Azibius are the earliest offshoots of an Afro–Arabian strepsirhine clade that embraces extant toothcombed primates and their fossil relatives. Azibius exhibits anatomical evidence for nocturnality. Algeripithecus has a long, thin and forwardly inclined lower canine alveolus, a feature that is entirely compatible with the long and procumbent lower canine included in the toothcomb of crown strepsirhines. These results strengthen an ancient African origin for crown strepsirhines and, in turn, strongly challenge the role of Africa as the ancestral homeland for anthropoids.

Modulation of Fgf3 dosage in mouse and men mirrors evolution of mammalian dentition

A central challenge in evolutionary biology is understanding how genetic mutations underlie morphological changes. Because highly calcified enamel enables preservation of detailed dental features, studying tooth morphology enables this question to be addressed in both extinct and extant species. Previous studies have found that mutant mice can have severe abnormalities in tooth morphology, and several authors have explored the evolutionary implications of tooth number modifications in mutants. However, although they can potentially shed much light on evolutionary mechanisms, anomalies in tooth shape remain poorly studied. Here, we report that alterations in dosage of the Fgf3 gene cause morphological changes in both genetically engineered mutant mice and in human patients. By comparing the dental morphologies in mice and humans carrying Fgf3 mutations with primitive rodent and primate fossils, we determined that decreases in dosage of Fgf3 lead to phenotypes that resemble the progressive reappearance of ancestral morphologies. We propose that modifications in the FGF signaling pathway have played an important role in evolution of mammalian dentition by giving rise to new cusps and interconnecting cusps by new crests. We anticipate that our multidisciplinary study will advance the detailed correlation of subtle dental modifications with genetic mutations in a variety of mammalian lineages.

Gaudeamus lavocati sp. nov. (Rodentia, Hystricognathi) from the early Oligocene of Zallah, Libya: first African caviomorph?

A new African species of hystricognathous rodent, Gaudeamus lavocati sp. nov., is described herein from the early Oligocene deposits of Zallah locality (Sirt basin, Central Libya). The dental morphology of this species is very close to that of some earliest South American caviomorphs. It allows a reinterpretation of molar crest homologies among earliest caviomorphs, pentalophodonty being confirmed as the plesiomorphic molar condition in Caviomorpha. This morphological resemblance argues for close affinities between Gaudeamus and earliest South American hystricognaths. Cladistic analysis supports Gaudeamus lavocati sp. nov. as the first known African representative of Caviomorpha, implying that its ancestors were part of the African phiomyid group that crossed the South Atlantic by a direct immigration route. Alternatively, the series of derived dental features of Gaudeamus could also be interpreted as evolutionary synchronous convergences of an African hystricognath lineage towards the specialized pattern of some caviomorphs. However, the high level of similarities concerning teeth morphology and enamel microstructure and the similar age of fossiliferous strata on both continents make this interpretation less probable. The phylogenetic position of this taxon is of considerable importance because it represents an enigmatic component of the phiomorph–caviomorph radiation in Africa and appears as a new clue toward the understanding of caviomorph origins.

Prospective in (Primate) Dental Analysis through Tooth 3D Topographical Quantification

The occlusal morphology of the teeth is mostly determined by the enamel-dentine junction morphology; the enamel-dentine junction plays the role of a primer and conditions the formation of the occlusal enamel reliefs. However, the accretion of the enamel cap yields thickness variations that alter the morphology and the topography of the enamel–dentine junction (i.e., the differential deposition of enamel by the ameloblasts create an external surface that does not necessarily perfectly parallel the enamel–dentine junction). This self-reliant influence of the enamel on tooth morphology is poorly understood and still under-investigated. Studies considering the relationship between enamel and dentine morphologies are rare, and none of them tackled this relationship in a quantitative way. Major limitations arose from: (1) the difficulties to characterize the tooth morphology in its comprehensive tridimensional aspect and (2) practical issues in relating enamel and enamel–dentine junction quantitative traits. We present new aspects of form representation based exclusively on 3D analytical tools and procedures. Our method is applied to a set of 21 unworn upper second molars belonging to eight extant anthropoid genera. Using geometrical analysis of polygonal meshes representatives of the tooth form, we propose a 3D dataset that constitutes a detailed characterization of the enamel and of the enamel–dentine junction morphologies. Also, for the first time, to our knowledge, we intend to establish a quantitative method for comparing enamel and enamel–dentine junction surfaces descriptors (elevation, inclination, orientation, etc.). New indices that allow characterizing the occlusal morphology are proposed and discussed. In this note, we present technical aspects of our method with the example of anthropoid molars. First results show notable individual variations and taxonomic heterogeneities for the selected topographic parameters and for the pattern and strength of association between enamel–dentine junction and enamel, the enamel cap altering in different ways the “transcription” of the enamel–dentine junction morphology.

To what extent is primate second molar enamel occlusal morphology shaped by the enamel-dentine junction?

The form of two hard tissues of the mammalian tooth, dentine and enamel, is the result of a combination of the phylogenetic inheritance of dental traits and the adaptive selection of these traits during evolution. Recent decades have been significant in unveiling developmental processes controlling tooth morphogenesis, dental variation and the origination of dental novelties. The enamel-dentine junction constitutes a precursor for the morphology of the outer enamel surface through growth of the enamel cap which may go along with the addition of original features. The relative contribution of these two tooth components to morphological variation and their respective response to natural selection is a major issue in paleoanthropology. This study will determine how much enamel morphology relies on the form of the enamel-dentine junction. The outer occlusal enamel surface and the enamel-dentine junction surface of 76 primate second upper molars are represented by polygonal meshes and investigated using tridimensional topometrical analysis. Quantitative criteria (elevation, inclination, orientation, curvature and occlusal patch count) are introduced to show that the enamel-dentine junction significantly constrains the topographical properties of the outer enamel surface. Our results show a significant correlation for elevation, orientation, inclination, curvature and occlusal complexity between the outer enamel surface and the enamel dentine junction for all studied primate taxa with the exception of four modern humans for curvature (p<0.05). Moreover, we show that, for all selected topometrical parameters apart from occlusal patch count, the recorded correlations significantly decrease along with enamel thickening in our sample. While preserving tooth integrity by providing resistance to wear and fractures, the variation of enamel thickness may modify the curvature present at the occlusal enamel surface in relation to enamel-dentine junction, potentially modifying dental functionalities such as blunt versus sharp dental tools. In terms of natural selection, there is a balance between increasing tooth resistance and maintaining efficient dental tools. In this sense the enamel cap acts as a functional buffer for the molar occlusal pattern. In primates, results suggest a primary emergence of dental novelties on the enamel-dentine junction and a secondary transposition of these novelties with no or minor modifications of dental functionalities by the enamel cap. Whereas enamel crenations have been reported by previous studies, our analysis do not support the presence of enamel tubercles without dentine relief nuclei. As is, the enamel cap is, at most, a secondary source of morphological novelty.

Occlusal Pattern in Paulchoffatiid Multituberculates and the Evolution of Cusp Morphology in Mammaliamorphs with Rodent-like Dentitions

Multituberculates developed a very complex masticatory apparatus during their long evolutionary history from the Jurassic to the Paleogene. Besides their rodent-like elongated incisors and diastemata, Cenozoic cimolodont Multituberculata display masticatory movements involving two distinct cycles in the mastication. An orthal slicing-crushing cycle associated with an enlarged lower fourth premolar precedes a palinal grinding cycle linked to upper molars with three longitudinal rows of cusps. With their plesiomorphic lower premolars and upper molars, the Late Jurassic/Early Cretaceous multituberculate family Paulchoffatiidae can provide the key for the understanding of the origin of the complex mastication of the Cimolodonta. Using for the first time propagation phase contrast Synchrotron X-Ray microtomography to perform both microwear and topographic analyses in order to characterize the mastication of Paulchoffatiidae, we digitized dental material from the Late Jurassic of the Guimarota Coal Mine (Leiria, Portugal) at the European Synchrotron Facility (Grenoble, France). Mastication in Paulchoffatiidae is characterized by a palinal grinding cycle. In contrast to Cimolodonta, no evidence of an orthal slicing-crushing cycle has been observed: the lower premolars mainly have a grinding function like the molars as they do exhibit buccal attrition facets bearing longitudinal striations. Nevertheless, the slightly oblique striations observed on the mesial part of the paulchoffatiid lower premolars possibly presage the orthal phase of the Cimolodonta. Our topographic analysis indicates that a strong relationship between individual cusp shape and direction of chewing is emphasized in rodents and rodent-like Mammaliamorpha such as Cimolodonta and Tritylodonta. Surprisingly, this relationship is not evident in Paulchoffatiidae. This unexpected result can be explained by the non-involvement in the attrition of many premolar cusps in Paulchoffatiidae, as indicated by our microwear analysis. The stronger the attrition, the more the direction of the masticatory movements influences the cusp morphology in Mammaliamorpha.

Molecular phylogeny of South-East Asian arboreal murine rodents

Recent phylogenetic studies and taxonomic reviews have led to nearly complete resolution of the phylogenetic divisions within the old world rats and mice (Muridae, Murinae). The Micromys division and Pithecheir division are two notable exceptions where groupings of species into these divisions based on morphology and arboreal lifestyle have not been supported by phylogenetic evidence. Several enigmatic species from these divisions have been missing from molecular studies, preventing a rigorous revision of phylogenetic relationships. In this study, we sequenced for the first time one mitochondrial and three nuclear genes from South‐East Asian keystone species of these two arboreal divisions: Hapalomys delacouri (Micromys division), Lenothrix canus and Pithecheir parvus (Pithecheir division). We also complemented the molecular data already available for the two divisions with new data from Sundaic Chiropodomys, Indian Vandeleuria oleracea and the recently described Sulawesian Margaretamys christinae. Using this new phylogenetic framework and molecular dating methodologies, our study allows some more detailed classification of the former Micromys and Pithecheir divisions, while confirming their polyphyletic status. Specifically, the former Micromys division should now be split into four monotypic divisions: Chiropodomys, Hapalomys, Micromys and Vandeleuria divisions. The former Pithecheir division is likely to be refined and restricted to Pithecheir and probably Pithecheirops, whereas Lenothrix and Margaretamys should now be recognized as representatives of the Dacnomys division. Our findings have profound implications with regard to the systematics of Murinae, as well as to the early evolution of murine morphology and dental characters.

Diversity and evolution of the molar radicular complex in murine rodents (Murinae, Rodentia).

OBJECTIVEnThis study was designed to characterize the radicular pattern diversity and evolution of murine molars. It aimed at identifying new morphological characters in order to improve our understanding of rodent diversity and systematics.nnnMETHODSnA non-invasive technique was applied to extant and extinct murine species. For each molar, a virtual slice was computed from X-ray microtomographic data to visualize root number and arrangement. A geometric morphometric study was then conducted on first upper molars on a sample of 40 specimens, representing 10 species of the tribe Arvicanthini.nnnRESULTSnThe radicular pattern enabled to retrieve phylogenetic murine groups settled by molecular data. Apodemus species, Malacomys longipes, Mus musculus, and species of the Praomys group all displayed a primitive pattern which consisted in two roots in each of their lower molars. Phloeomys cumingi and Batomys granti displayed singular root arrangements derived from this primitive pattern. Arvicanthini were distinguishable from all other African murines by their high root number. In addition, Procrustes analysis on first upper molars clustered specimens according to their genera.nnnCONCLUSIONSnAn evolutionary trend toward increasing the molar root number is shown in many murine groups. The increased complexity of root pattern occurs by a progressive splitting of the primitive pattern. The fossil record shows that the increase in the root number within Arvicanthini was initiated at least 7 Myr ago. Root number and root positioning are demonstrated to be characteristics equivalent to those of the crown in murine rodent evolutionary studies.