Paul Tafforeau

Earliest evidence of modern human life history in North African early Homo sapiens

Recent developmental studies demonstrate that early fossil hominins possessed shorter growth periods than living humans, implying disparate life histories. Analyses of incremental features in teeth provide an accurate means of assessing the age at death of developing dentitions, facilitating direct comparisons with fossil and modern humans. It is currently unknown when and where the prolonged modern human developmental condition originated. Here, an application of x-ray synchrotron microtomography reveals that an early Homo sapiens juvenile from Morocco dated at 160,000 years before present displays an equivalent degree of tooth development to modern European children at the same age. Crown formation times in the juveniles macrodont dentition are higher than modern human mean values, whereas root development is accelerated relative to modern humans but is less than living apes and some fossil hominins. The juvenile from Jebel Irhoud is currently the oldest-known member of Homo with a developmental pattern (degree of eruption, developmental stage, and crown formation time) that is more similar to modern H. sapiens than to earlier members of Homo. This study also underscores the continuing importance of North Africa for understanding the origins of human anatomical and behavioral modernity. Corresponding biological and cultural changes may have appeared relatively late in the course of human evolution.

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.

The Endocast of MH1, Australopithecus sediba

The brain endocast of Australopithecus sediba shows that despite retaining a small brain size, some reorganization of the frontal lobe had commenced, hinting at the later neural development seen in Homo. The virtual endocast of MH1 (Australopithecus sediba), obtained from high-quality synchrotron scanning, reveals generally australopith-like convolutional patterns on the frontal lobes but also some foreshadowing of features of the human frontal lobes, such as posterior repositioning of the olfactory bulbs. Principal component analysis of orbitofrontal dimensions on australopith endocasts (MH1, Sts 5, and Sts 60) indicates that among these, MH1 orbitofrontal shape and organization align most closely with human endocasts. These results are consistent with gradual neural reorganization of the orbitofrontal region in the transition from Australopithecus to Homo, but given the small volume of the MH1 endocast, they are not consistent with gradual brain enlargement before the transition.

The PyHST2 hybrid distributed code for high speed tomographic reconstruction with iterative reconstruction and a priori knowledge capabilities

We present the PyHST2 code which is in service at ESRF for phase-contrast and absorption tomography. This code has been engineered to sustain the high data flow typical of the 3rd generation synchrotron facilities (10 terabytes per experiment) by adopting a distributed and pipelined architecture. The code implements, beside a default filtered backprojection reconstruction, iterative reconstruction techniques with a priori knowledge. These latter are used to improve the reconstruction quality or in order to reduce the required data volume or the deposited dose to the sample and reach a given quality goal. The implemented a priori knowledge techniques are based on the total variation penalization and a new recently found convex functional which is based on overlapping patches. We give details of the different methods and discuss how they are implemented in the PyHST2 code, which is distributed under free license. We provide methods for estimating, in the absence of ground-truth data, the optimal parameters values for a priori techniques.

A Middle Miocene hominoid from Thailand and orangutan origins

The origin of orangutans has long been debated. Sivapithecus is considered to be the closest ancestor of orangutans because of its facial–palatal similarities, but its dental characteristics and postcranial skeleton do not confirm this phylogenetic position. Here we report a new Middle Miocene hominoid, cf. Lufengpithecus chiangmuanensis n. sp. from northern Thailand. Its dental morphology relates it to the Pongo clade, which includes Lufengpithecus, Sivapithecus, Gigantopithecus, Ankarapithecus and possibly Griphopithecus. Our new species displays striking dental resemblances with living orangutans and appears as a more likely candidate to represent an ancestor of this ape. In addition, it originates from the geographic area of Pleistocene orangutans. But surprisingly, the associated flora shows strong African affinities, demonstrating the existence of a temporary floral and faunal dispersal corridor between southeast Asia and Africa during the Middle Miocene, which may have played a critical role in hominoid dispersion.

The oldest known primate skeleton and early haplorhine evolution

Reconstructing the earliest phases of primate evolution has been impeded by gaps in the fossil record, so that disagreements persist regarding the palaeobiology and phylogenetic relationships of the earliest primates. Here we report the discovery of a nearly complete and partly articulated skeleton of a primitive haplorhine primate from the early Eocene of China, about 55 million years ago, the oldest fossil primate of this quality ever recovered. Coupled with detailed morphological examination using propagation phase contrast X-ray synchrotron microtomography, our phylogenetic analysis based on total available evidence indicates that this fossil is the most basal known member of the tarsiiform clade. In addition to providing further support for an early dichotomy between the strepsirrhine and haplorhine clades, this new primate further constrains the age of divergence between tarsiiforms and anthropoids. It also strengthens the hypothesis that the earliest primates were probably diurnal, arboreal and primarily insectivorous mammals the size of modern pygmy mouse lemurs.

The role of ammonites in the Mesozoic marine food web revealed by jaw preservation.

Analysis of x-ray microtomographic reconstructions of ammonite fossils reveal their feeding habits. Ammonites are prominent in macroevolutionary studies because of their abundance and diversity in the fossil record, but their paleobiology and position in the marine food web are not well understood due to the lack of preserved soft tissue. We present three-dimensional reconstructions of the buccal apparatus in the Mesozoic ammonite Baculites with the use of synchrotron x-ray microtomography. Buccal mass morphology, combined with the coexistence of food remains found in the buccal mass, suggests that these ammonites fed on plankton. This diet may have extended to all aptychophoran ammonites, which share the same buccal mass morphology. Understanding the role of these ammonites in the Mesozoic food web provides insights into their radiation in the Early Jurassic, as well as their extinction at the end of the Cretaceous/early Paleogene.

Three-dimensional synchrotron virtual paleohistology: A new insight into the world of fossil bone microstructures

The recent developments of phase-contrast synchrotron imaging techniques have been of great interest for paleontologists, providing three-dimensional (3D) tomographic images of anatomical structures, thereby leading to new paleobiological insights and the discovery of new species. However, until now, it has not been used on features smaller than 5-7 μm voxel size in fossil bones. Because much information is contained within the 3D histological architecture of bone, including an ontogenetic record, crucial for understanding the paleobiology of fossil species, the application of phase-contrast synchrotron tomography to bone at higher resolutions is potentially of great interest. Here we use this technique to provide new 3D insights into the submicron-scale histology of fossil and recent bones, based on the development of new pink-beam configurations, data acquisition strategies, and improved processing tools. Not only do the scans reveal by nondestructive means all of the major features of the histology at a resolution comparable to that of optical microscopy, they provide 3D information that cannot be obtained by any other method.

Phase contrast X-ray synchrotron imaging: opening access to fossil inclusions in opaque amber.

A significant portion of Mesozoic amber is fully opaque. Biological inclusions in such amber are invisible even after polishing, leading to potential bias in paleoecological and phylogenetic studies. Until now, studies using conventional X-ray microtomography focused on translucent or semi-opaque amber. In these cases, organisms of interest were visualized prior to X-ray analyses. It was recently demonstrated that propagation phase contrast X-ray synchrotron imaging techniques are powerful tools to access invisible inclusions in fully opaque amber. Here we describe an optimized synchrotron microradiographic protocol that allowed us to investigate efficiently and rapidly large amounts of opaque amber pieces from Charentes (southwestern France). Amber pieces were imaged with microradiography after immersion in water, which optimizes the visibility of inclusions. Determination is not accurate enough to allow precise phylogenetic studies, but provides preliminary data on biodiversity and ecotypes distribution; phase contrast microtomography remains necessary for precise determination. Because the organisms are generally much smaller than the amber pieces, we optimized local microtomography by using a continuous acquisition mode (sample moving during projection integration). As tomographic investigation of all inclusions is not practical, we suggest the use of a synchrotron for a microradiographic survey of opaque amber, coupled with microtomographic investigations of the most valuable organisms.

A primitive placoderm sheds light on the origin of the jawed vertebrate face

Extant vertebrates form two clades, the jawless Cyclostomata (lampreys and hagfishes) and the jawed Gnathostomata (all other vertebrates), with contrasting facial architectures. These arise during development from just a few key differences in the growth patterns of the cranial primordia: notably, the nasal sacs and hypophysis originate from a single placode in cyclostomes but from separate placodes in gnathostomes, and infraoptic ectomesenchyme migrates forward either side of the single placode in cyclostomes but between the placodes in gnathostomes. Fossil stem gnathostomes preserve cranial anatomies rich in landmarks that provide proxies for developmental processes and allow the transition from jawless to jawed vertebrates to be broken down into evolutionary steps. Here we use propagation phase contrast synchrotron microtomography to image the cranial anatomy of the primitive placoderm (jawed stem gnathostome) Romundina, and show that it combines jawed vertebrate architecture with cranial and cerebral proportions resembling those of cyclostomes and the galeaspid (jawless stem gnathostome) Shuyu. This combination seems to be primitive for jawed vertebrates, and suggests a decoupling between ectomesenchymal growth trajectory, ectomesenchymal proliferation, and cerebral shape change during the origin of gnathostomes.