Publications by authors named "Paul Tafforeau"

109 Publications

The primitive brain of early .

Science 2021 04;372(6538):165-171

Department of Anthropology and Anthropological Museum, University of Zurich, CH-8052 Zurich, Switzerland.

The brains of modern humans differ from those of great apes in size, shape, and cortical organization, notably in frontal lobe areas involved in complex cognitive tasks, such as social cognition, tool use, and language. When these differences arose during human evolution is a question of ongoing debate. Here, we show that the brains of early from Africa and Western Asia (Dmanisi) retained a primitive, great ape-like organization of the frontal lobe. By contrast, African younger than 1.5 million years ago, as well as all Southeast Asian , exhibited a more derived, humanlike brain organization. Frontal lobe reorganization, once considered a hallmark of earliest in Africa, thus evolved comparatively late, and long after first dispersed from Africa.
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http://dx.doi.org/10.1126/science.aaz0032DOI Listing
April 2021

New light shed on the early evolution of limb-bone growth plate and bone marrow.

Elife 2021 Mar 2;10. Epub 2021 Mar 2.

Department of Organismal Biology, Evolution and Development, Uppsala University, Uppsala, Sweden.

The production of blood cells (haematopoiesis) occurs in the limb bones of most tetrapods but is absent in the fin bones of ray-finned fish. When did long bones start producing blood cells? Recent hypotheses suggested that haematopoiesis migrated into long bones prior to the water-to-land transition and protected newly-produced blood cells from harsher environmental conditions. However, little fossil evidence to support these hypotheses has been provided so far. Observations of the humeral microarchitecture of stem-tetrapods, batrachians, and amniotes were performed using classical sectioning and three-dimensional synchrotron virtual histology. They show that Permian tetrapods seem to be among the first to exhibit a centralised marrow organisation, which allows haematopoiesis as in extant amniotes. Not only does our study demonstrate that long-bone haematopoiesis was probably not an exaptation to the water-to-land transition but it sheds light on the early evolution of limb-bone development and the sequence of bone-marrow functional acquisitions.
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http://dx.doi.org/10.7554/eLife.51581DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7924947PMC
March 2021

A parasitic coevolution since the Miocene revealed by phase-contrast synchrotron X-ray microtomography and the study of natural history collections.

Sci Rep 2021 Jan 29;11(1):2672. Epub 2021 Jan 29.

European Synchrotron Radiation Facility, Grenoble, France.

The discovery of a new fossil species of the Caribbeo-Mexican genus Proptomaphaginus (Coleoptera, Leiodidae, Cholevinae) from Dominican amber, associated with a new fossil parasitic fungus in the genus Columnomyces (Ascomycota, Laboulbeniales), triggered an investigation of extant species of Proptomaphaginus and revealed the long-enduring parasitic association between these two genera. This effort resulted in the description of the fossil species †Proptomaphaginus alleni sp. nov., and one fossil and two extant species of Columnomyces, selectively associated with species of Proptomaphaginus: †Columnomyces electri sp. nov. associated with the fossil †Proptomaphaginus alleni in Dominican amber, Columnomyces hispaniolensis sp. nov. with the extant Proptomaphaginus hispaniolensis (endemic of Hispaniola), and Columnomyces peckii sp. nov. with the extant Proptomaphaginus puertoricensis (endemic of Puerto Rico). Based on biogeography, our current understanding is that the Caribbean species of Proptomaphaginus and their parasitic species of Columnomyces have coevolved since the Miocene. This is the first occurrence of such a coevolution between a genus of parasitic fungus and a genus of Coleoptera. The phylogenetic relations among Proptomaphaginus species are also addressed based on a parsimony analysis. Fossil specimens were observed by propagation phase-contrast synchrotron X-ray microtomography (PPC-SRμCT) and extant specimens were obtained through the study of preserved dried, pinned insects, attesting for the importance of (i) technological advancement and (ii) natural history collections in the study of microparasitic relationships.
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http://dx.doi.org/10.1038/s41598-020-79481-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7846571PMC
January 2021

The morphology and evolution of chondrichthyan cranial muscles: A digital dissection of the elephantfish Callorhinchus milii and the catshark Scyliorhinus canicula.

J Anat 2021 May 7;238(5):1082-1105. Epub 2021 Jan 7.

CR2P, Centre de Recherche en Paléontologie-Paris, Muséum national d'Histoire naturelle, Sorbonne Université, Centre National de la Recherche Scientifique, Paris cedex 05, France.

The anatomy of sharks, rays, and chimaeras (chondrichthyans) is crucial to understanding the evolution of the cranial system in vertebrates due to their position as the sister group to bony fishes (osteichthyans). Strikingly different arrangements of the head in the two constituent chondrichthyan groups-holocephalans and elasmobranchs-have played a pivotal role in the formation of evolutionary hypotheses targeting major cranial structures such as the jaws and pharynx. However, despite the advent of digital dissections as a means of easily visualizing and sharing the results of anatomical studies in three dimensions, information on the musculoskeletal systems of the chondrichthyan head remains largely limited to traditional accounts, many of which are at least a century old. Here, we use synchrotron tomographic data to carry out a digital dissection of a holocephalan and an elasmobranch widely used as model species: the elephantfish, Callorhinchus milii, and the small-spotted catshark, Scyliorhinus canicula. We describe and figure the skeletal anatomy of the head, labial, mandibular, hyoid, and branchial cartilages in both taxa as well as the muscles of the head and pharynx. In Callorhinchus, we make several new observations regarding the branchial musculature, revealing several previously unreported or ambiguously characterized muscles, likely homologous to their counterparts in the elasmobranch pharynx. We also identify a previously unreported structure linking the pharyngohyal of Callorhinchus to the neurocranium. Finally, we review what is known about the evolution of chondrichthyan cranial muscles from their fossil record and discuss the implications for muscle homology and evolution, broadly concluding that the holocephalan pharynx is likely derived from a more elasmobranch-like form which is plesiomorphic for the chondrichthyan crown group. This dataset has great potential as a resource, particularly for researchers using these model species for zoological research, functional morphologists requiring models of musculature and skeletons, as well as for palaeontologists seeking comparative models for extinct taxa.
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http://dx.doi.org/10.1111/joa.13362DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8053583PMC
May 2021

The developmental relationship between teeth and dermal odontodes in the most primitive bony fish .

Elife 2020 12 15;9. Epub 2020 Dec 15.

Department of Organismal Biology, Uppsala University, Uppsala, Sweden.

The ontogenetic trajectory of a marginal jawbone of (Late Silurian, 422 Million years old), the phylogenetically most basal stem osteichthyan, visualized by synchrotron microtomography, reveals a developmental relationship between teeth and dermal odontodes that is not evident from the adult morphology. The earliest odontodes are two longitudinal founder ridges formed at the ossification center. Subsequent odontodes that are added lingually to the ridges turn into conical teeth and undergo cyclic replacement, while those added labially achieve a stellate appearance. Stellate odontodes deposited directly on the bony plate are aligned with the alternate files of teeth, whereas new tooth positions are inserted into the files of sequential addition when a gap appears. Successive teeth and overgrowing odontodes show hybrid morphologies around the oral-dermal boundary, suggesting signal cross-communication. We propose that teeth and dermal odontodes are modifications of a single system, regulated and differentiated by the oral and dermal epithelia.
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http://dx.doi.org/10.7554/eLife.60985DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7738188PMC
December 2020

Secondary ossification center induces and protects growth plate structure.

Elife 2020 10 16;9. Epub 2020 Oct 16.

Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden.

Growth plate and articular cartilage constitute a single anatomical entity early in development but later separate into two distinct structures by the secondary ossification center (SOC). The reason for such separation remains unknown. We found that evolutionarily SOC appears in animals conquering the land - amniotes. Analysis of the ossification pattern in mammals with specialized extremities (whales, bats, jerboa) revealed that SOC development correlates with the extent of mechanical loads. Mathematical modeling revealed that SOC reduces mechanical stress within the growth plate. Functional experiments revealed the high vulnerability of hypertrophic chondrocytes to mechanical stress and showed that SOC protects these cells from apoptosis caused by extensive loading. Atomic force microscopy showed that hypertrophic chondrocytes are the least mechanically stiff cells within the growth plate. Altogether, these findings suggest that SOC has evolved to protect the hypertrophic chondrocytes from the high mechanical stress encountered in the terrestrial environment.
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http://dx.doi.org/10.7554/eLife.55212DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7581430PMC
October 2020

Reptile-like physiology in Early Jurassic stem-mammals.

Nat Commun 2020 10 12;11(1):5121. Epub 2020 Oct 12.

Institute of Biotechnology, University of Helsinki, Helsinki, Finland.

Despite considerable advances in knowledge of the anatomy, ecology and evolution of early mammals, far less is known about their physiology. Evidence is contradictory concerning the timing and fossil groups in which mammalian endothermy arose. To determine the state of metabolic evolution in two of the earliest stem-mammals, the Early Jurassic Morganucodon and Kuehneotherium, we use separate proxies for basal and maximum metabolic rate. Here we report, using synchrotron X-ray tomographic imaging of incremental tooth cementum, that they had maximum lifespans considerably longer than comparably sized living mammals, but similar to those of reptiles, and so they likely had reptilian-level basal metabolic rates. Measurements of femoral nutrient foramina show Morganucodon had blood flow rates intermediate between living mammals and reptiles, suggesting maximum metabolic rates increased evolutionarily before basal metabolic rates. Stem mammals lacked the elevated endothermic metabolism of living mammals, highlighting the mosaic nature of mammalian physiological evolution.
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http://dx.doi.org/10.1038/s41467-020-18898-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7550344PMC
October 2020

A broader perspective on estimating dental age for the Xujiayao juvenile, a late Middle Pleistocene archaic hominin from East Asia.

J Hum Evol 2020 Jul 24:102850. Epub 2020 Jul 24.

Department of Anthropology, The Ohio State University, Columbus, OH, 43210, USA; Department of Anthropology/Department of Evolution, Ecology and Organismal Biology, The Ohio State University, Columbus, OH, 43210, USA; School of Anthropology and Conservation, The University of Kent, Canterbury, Kent, CT2 7NR, UK.

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http://dx.doi.org/10.1016/j.jhevol.2020.102850DOI Listing
July 2020

Marginal dentition and multiple dermal jawbones as the ancestral condition of jawed vertebrates.

Science 2020 07;369(6500):211-216

Department of Organismal Biology, Uppsala University, Norbyvägen 18A, SE-752 36, Uppsala, Sweden.

The dentitions of extant fishes and land vertebrates vary in both pattern and type of tooth replacement. It has been argued that the common ancestral condition likely resembles the nonmarginal, radially arranged tooth files of arthrodires, an early group of armoured fishes. We used synchrotron microtomography to describe the fossil dentitions of so-called acanthothoracids, the most phylogenetically basal jawed vertebrates with teeth, belonging to the genera , , and (from the Early Devonian of the Czech Republic). Their dentitions differ fundamentally from those of arthrodires; they are marginal, carried by a cheekbone or a series of short dermal bones along the jaw edges, and teeth are added lingually as is the case in many chondrichthyans (cartilaginous fishes) and osteichthyans (bony fishes and tetrapods). We propose these characteristics as ancestral for all jawed vertebrates.
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http://dx.doi.org/10.1126/science.aaz9431DOI Listing
July 2020

Author Correction: New infant cranium from the African Miocene sheds light on ape evolution.

Nature 2020 Jul;583(7815):E21

Department of Cell and Developmental Biology, University College London, London, WC1E 6BT, UK.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.
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http://dx.doi.org/10.1038/s41586-020-2466-7DOI Listing
July 2020

Development and growth of the pelvic fin in the extant coelacanth Latimeria chalumnae.

Anat Rec (Hoboken) 2021 03 9;304(3):541-558. Epub 2020 Jun 9.

Département Adaptations du Vivant, UMR 7179 MECADEV, MNHN - CNRS, Paris, France.

The ontogeny of the paired appendages has been extensively studied in lungfishes and tetrapods, but remains poorly known in coelacanths. Recent work has shed light on the anatomy and development of the pectoral fin in Latimeria chalumnae. Yet, information on the development of the pelvic fin and girdle is still lacking. Here, we described the development of the pelvic fin and girdle in Latimeria chalumnae based on 3D reconstructions generated from conventional and X-ray synchrotron microtomography, as well as MRI acquisitions. As in other jawed vertebrates, the development of the pelvic fin occurs later than that of the pectoral fin in Latimeria. Many elements of the endoskeleton are not yet formed at the earliest stage sampled. The four mesomeres are already formed in the fetus, but only the most proximal radial elements (preaxial radial 0-1) are formed and individualized at this stage. We suggest that all the preaxial radial elements in the pelvic and pectoral fin of Latimeria are formed through the fragmentation of the mesomeres. We document the progressive ossification of the pelvic girdle, and the presence of a trabecular system in the adult. This trabecular system likely reinforces the cartilaginous girdle to resist the muscle forces exerted during locomotion. Finally, the presence of a preaxial element in contact with the pelvic girdle from the earliest stage of development onward questions the mono-basal condition of the pelvic fin in Latimeria. However, the particular shape of the mesomeres may explain the presence of this element in contact with the girdle.
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http://dx.doi.org/10.1002/ar.24452DOI Listing
March 2021

endocasts suggest ape-like brain organization and prolonged brain growth.

Sci Adv 2020 04 1;6(14):eaaz4729. Epub 2020 Apr 1.

Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637, USA.

Human brains are three times larger, are organized differently, and mature for a longer period of time than those of our closest living relatives, the chimpanzees. Together, these characteristics are important for human cognition and social behavior, but their evolutionary origins remain unclear. To study brain growth and organization in the hominin species more than 3 million years ago, we scanned eight fossil crania using conventional and synchrotron computed tomography. We inferred key features of brain organization from endocranial imprints and explored the pattern of brain growth by combining new endocranial volume estimates with narrow age at death estimates for two infants. Contrary to previous claims, sulcal imprints reveal an ape-like brain organization and no features derived toward humans. A comparison of infant to adult endocranial volumes indicates protracted brain growth in , likely critical for the evolution of a long period of childhood learning in hominins.
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http://dx.doi.org/10.1126/sciadv.aaz4729DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7112758PMC
April 2020

Synchrotron "virtual archaeozoology" reveals how Ancient Egyptians prepared a decaying crocodile cadaver for mummification.

PLoS One 2020 21;15(2):e0229140. Epub 2020 Feb 21.

European Synchrotron Radiation Facility, Grenoble, France.

Although Ancient Egyptians mummified millions of animals over the course of one millennium, many details of these mummification protocols remain unknown. Multi-scale propagation phase-contrast X-ray synchrotron microtomography was used to visualise an ancient Egyptian crocodile mummy housed at the Musée des Confluences (Lyon, France). This state-of-the-art non-destructive imaging technique revealed the complete interior anatomy of the mummy in three dimensions. Here, we present detailed insight into the complex post-mortem treatment of a decaying crocodile cadaver in preparation for mummification. Except for the head and the extremities of the limbs, everything beneath the skin of the crocodile (i.e. organs, muscles, and even most of the skeleton) was removed to cease further putrefaction. This unexpected finding demonstrates that earlier knowledge obtained from textual and other archaeological sources does not sufficiently reflect the diversity of mummification protocols implemented by Ancient Egyptians.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0229140PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7034907PMC
May 2020

Depicting the crystal structure of fibrous ferrierite from British Columbia using a combined synchrotron techniques approach.

J Appl Crystallogr 2019 Dec 14;52(Pt 6):1397-1408. Epub 2019 Nov 14.

Department of Chemical and Geological Sciences, University of Modena and Reggio Emilia, Modena 41121, Italy.

The ferrierite crystal structure has often been subject to discussion because of the possible lowering of symmetry from the space group . It mainly occurs in nature with a fibrous crystal habit, and because of the existence of line/planar defects in the framework, texture and preferred orientation effects it has been difficult to obtain an exact crystallographic model based only on the results from powder diffraction data. Therefore, nano-single-crystal diffraction and tomography data have been combined in order to improve the refinement with a meaningful model. High-quality single-crystal data, providing reliable structural information, and tomography images have been used as input for a Rietveld refinement which took into account a phenomenological description of stacking disorder and the analytical description of the preferred orientation, by means of spherical harmonics for strong texture effects. This is one of the first examples of application of synchrotron nano-diffraction for the structure solution of fibrous minerals of micrometre to nanometre size. The high quality of the crystals allowed collection of single-crystal X-ray diffraction data of up to 0.6 Å resolution, leading to an unambiguous solution and precise anisotropic refinement. Nano-single-crystal diffraction and phase contrast tomography data were collected at ID11 and the high-resolution powder diffraction patterns at ID22 of the European Synchrotron Radiation Facility. This detailed crystallographic characterization provides a basis for understanding the potential of ferrierite for toxicity and carcinogenicity.
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http://dx.doi.org/10.1107/S1600576719013980DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6878881PMC
December 2019

Development and growth of the pectoral girdle and fin skeleton in the extant coelacanth Latimeria chalumnae.

J Anat 2020 03 12;236(3):493-509. Epub 2019 Nov 12.

UMR 7179 MECADEV, MNHN - CNRS, Département Adaptations du Vivant, Muséum National d'Histoire Naturelle, Paris, France.

The monobasal pectoral fins of living coelacanths and lungfishes are homologous to the forelimbs of tetrapods and are thus critical to investigate the origin thereof. However, it remains unclear whether the similarity in the asymmetrical endoskeletal arrangement of the pectoral fins of coelacanths reflects the evolution of the pectoral appendages in sarcopterygians. Here, we describe for the first time the development of the pectoral fin and shoulder girdle in the extant coelacanth Latimeria chalumnae, based on the tomographic acquisition of a growth series. The pectoral girdle and pectoral fin endoskeleton are formed early in development with a radially outward growth of the endoskeletal elements. The visualization of the pectoral girdle during development shows a reorientation of the girdle between the fetus and pup 1 stages, creating a contact between the scapulocoracoids and the clavicles in the ventro-medial region. Moreover, we observed a splitting of the pre- and post-axial cartilaginous plates in respectively pre-axial radials and accessory elements on one hand, and in post-axial accessory elements on the other hand. However, the mechanisms involved in the splitting of the cartilaginous plates appear different from those involved in the formation of radials in actinopterygians. Our results show a proportional reduction of the proximal pre-axial radial of the fin, rendering the external morphology of the fin more lobe-shaped, and a spatial reorganization of elements resulting from the fragmentation of the two cartilaginous plates. Latimeria development hence supports previous interpretations of the asymmetrical pectoral fin skeleton as being plesiomorphic for coelacanths and sarcopterygians.
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http://dx.doi.org/10.1111/joa.13115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7018633PMC
March 2020

Enamel thickness and dental development in Rudapithecus hungaricus.

J Hum Evol 2019 11 19;136:102649. Epub 2019 Sep 19.

Department of Anthropology, University of Toronto, 19 Russell Street, Toronto, ON, M5S 2S2, Canada.

The fossil record of middle and late Miocene Eurasian hominoids has expanded considerably over the past few decades, particularly with the recovery of numerous isolated teeth and jaws. Scholars have turned to assessments of internal tooth structure and growth to make sense of the evolutionary radiations of these primates as well as their affinities to the living great apes (hominids). Here we characterize full-dentition enamel thickness and dental development in several juvenile Rudapithecus hungaricus individuals using multiple imaging modalities. Relative enamel thickness (RET) values for the anterior teeth and premolars of Rudapithecus are broadly akin to those of gorillas and chimpanzees and are thinner than those of orangutans. First molar RET values are most similar to chimpanzees, while posterior molar values are closer to thicker-enameled orangutans. When compared to Miocene hominoids, Rudapithecus shows an intermediate molar RET condition that is especially similar to other dryopithecines. Long-period line periodicity values are comparable to African apes and most Miocene hominoids, and lower than living and fossil orangutans. The mean cuspal daily secretion rate is similar to that of several other Miocene hominoids but is greater than extant great apes. Cusp-specific molar crown formation times generally exceed those of chimpanzees, are lower than those of orangutans, and are broadly like those of other Miocene apes. While Rudapithecus appears to have a somewhat unique pattern of enamel thickness and dental development relative to individual great ape genera, these structural and developmental features are consistent with its designation as a hominid.
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http://dx.doi.org/10.1016/j.jhevol.2019.102649DOI Listing
November 2019

Multiphase progenetic development shaped the brain of flying archosaurs.

Sci Rep 2019 07 25;9(1):10807. Epub 2019 Jul 25.

European Synchrotron Radiation Facility, 71 Avenue des Martyrs, CS-40220, 38043, Grenoble, France.

The growing availability of virtual cranial endocasts of extinct and extant vertebrates has fueled the quest for endocranial characters that discriminate between phylogenetic groups and resolve their neural significances. We used geometric morphometrics to compare a phylogenetically and ecologically comprehensive data set of archosaurian endocasts along the deep evolutionary history of modern birds and found that this lineage experienced progressive elevation of encephalisation through several chapters of increased endocranial doming that we demonstrate to result from progenetic developments. Elevated encephalisation associated with progressive size reduction within Maniraptoriformes was secondarily exapted for flight by stem avialans. Within Mesozoic Avialae, endocranial doming increased in at least some Ornithurae, yet remained relatively modest in early Neornithes. During the Paleogene, volant non-neoavian birds retained ancestral levels of endocast doming where a broad neoavian niche diversification experienced heterochronic brain shape radiation, as did non-volant Palaeognathae. We infer comparable developments underlying the establishment of pterosaurian brain shapes.
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http://dx.doi.org/10.1038/s41598-019-46959-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6658547PMC
July 2019

Neurocranial development of the coelacanth and the evolution of the sarcopterygian head.

Nature 2019 05 17;569(7757):556-559. Epub 2019 Apr 17.

UMR 7179 (MNHN-CNRS) MECADEV, Département Adaptations du Vivant, Muséum National d'Histoire Naturelle, Paris, France.

The neurocranium of sarcopterygian fishes was originally divided into an anterior (ethmosphenoid) and posterior (otoccipital) portion by an intracranial joint, and underwent major changes in its overall geometry before fusing into a single unit in lungfishes and early tetrapods. Although the pattern of these changes is well-documented, the developmental mechanisms that underpin variation in the form of the neurocranium and its associated soft tissues during the evolution of sarcopterygian fishes remain poorly understood. The coelacanth Latimeria is the only known living vertebrate that retains an intracranial joint. Despite its importance for understanding neurocranial evolution, the development of the neurocranium of this ovoviviparous fish remains unknown. Here we investigate the ontogeny of the neurocranium and brain in Latimeria chalumnae using conventional and synchrotron X-ray micro-computed tomography as well as magnetic resonance imaging, performed on an extensive growth series for this species. We describe the neurocranium at the earliest developmental stage known for Latimeria, as well as the major changes that the neurocranium undergoes during ontogeny. Changes in the neurocranium are associated with an extreme reduction in the relative size of the brain along with an enlargement of the notochord. The development of the notochord appears to have a major effect on the surrounding cranial components, and might underpin the formation of the intracranial joint. Our results shed light on the interplay between the neurocranium and its adjacent soft tissues during development in Latimeria, and provide insights into the developmental mechanisms that are likely to have underpinned the evolution of neurocranial diversity in sarcopterygian fishes.
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http://dx.doi.org/10.1038/s41586-019-1117-3DOI Listing
May 2019

First systematic assessment of dental growth and development in an archaic hominin (genus, ) from East Asia.

Sci Adv 2019 01 16;5(1):eaau0930. Epub 2019 Jan 16.

Department of Anthropology, The Ohio State University, Columbus, OH 43210, USA.

Several human dental traits typical of modern humans appear to be associated with the prolonged period of development that is a key human attribute. Understanding when, and in which early hominins, these dental traits first appeared is thus of strong interest. Using x-ray multiresolution synchrotron phase-contrast microtomography, we quantify dental growth and development in an archaic juvenile from the Xujiayao site in northern China dating to 161,000-224,000 years or 104,000-125,000 years before present. Despite the archaic morphology of Xujiayao hominins, most aspects of dental development of this juvenile fall within modern human ranges (e.g., prolonged crown formation time and delayed first molar eruption). For its estimated age-at-death (6.5 years), its state of dental development is comparable to that of equivalently aged modern children. These findings suggest that several facets of modern human dental growth and development evolved in East Asia before the appearance of fully modern human morphology.
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http://dx.doi.org/10.1126/sciadv.aau0930DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6357757PMC
January 2019

Disentangling isolated dental remains of Asian Pleistocene hominins and pongines.

PLoS One 2018 1;13(11):e0204737. Epub 2018 Nov 1.

ESRF-The European Synchrotron, Grenoble, France.

Scholars have debated the taxonomic identity of isolated primate teeth from the Asian Pleistocene for over a century, which is complicated by morphological and metric convergence between orangutan (Pongo) and hominin (Homo) molariform teeth. Like Homo erectus, Pongo once showed considerable dental variation and a wide distribution throughout mainland and insular Asia. In order to clarify the utility of isolated dental remains to document the presence of hominins during Asian prehistory, we examined enamel thickness, enamel-dentine junction shape, and crown development in 33 molars from G. H. R. von Koenigswald's Chinese Apothecary collection (11 Sinanthropus officinalis [= Homo erectus], 21 "Hemanthropus peii," and 1 "Hemanthropus peii" or Pongo) and 7 molars from Sangiran dome (either Homo erectus or Pongo). All fossil teeth were imaged with non-destructive conventional and/or synchrotron micro-computed tomography. These were compared to H. erectus teeth from Zhoukoudian, Sangiran and Trinil, and a large comparative sample of fossil Pongo, recent Pongo, and recent human teeth. We find that Homo and Pongo molars overlap substantially in relative enamel thickness; molar enamel-dentine junction shape is more distinctive, with Pongo showing relatively shorter dentine horns and wider crowns than Homo. Long-period line periodicity values are significantly greater in Pongo than in H. erectus, leading to longer crown formation times in the former. Most of the sample originally assigned to S. officinalis and H. erectus shows greater affinity to Pongo than to the hominin comparative sample. Moreover, enamel thickness, enamel-dentine junction shape, and a long-period line periodicity value in the "Hemanthropus peii" sample are indistinguishable from fossil Pongo. These results underscore the need for additional recovery and study of associated dentitions prior to erecting new taxa from isolated teeth.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0204737PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6211657PMC
April 2019

Wing bone geometry reveals active flight in Archaeopteryx.

Nat Commun 2018 03 13;9(1):923. Epub 2018 Mar 13.

European Synchrotron Radiation Facility, 71 Avenue des Martyrs, CS-40220, 38043, Grenoble Cedex, France.

Archaeopteryx is an iconic fossil taxon with feathered wings from the Late Jurassic of Germany that occupies a crucial position for understanding the early evolution of avian flight. After over 150 years of study, its mosaic anatomy unifying characters of both non-flying dinosaurs and flying birds has remained challenging to interpret in a locomotory context. Here, we compare new data from three Archaeopteryx specimens obtained through phase-contrast synchrotron microtomography to a representative sample of archosaurs employing a diverse array of locomotory strategies. Our analyses reveal that the architecture of Archaeopteryx's wing bones consistently exhibits a combination of cross-sectional geometric properties uniquely shared with volant birds, particularly those occasionally utilising short-distance flapping. We therefore interpret that Archaeopteryx actively employed wing flapping to take to the air through a more anterodorsally posteroventrally oriented flight stroke than used by modern birds. This unexpected outcome implies that avian powered flight must have originated before the latest Jurassic.
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http://dx.doi.org/10.1038/s41467-018-03296-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5849612PMC
March 2018

Synchrotron scanning reveals amphibious ecomorphology in a new clade of bird-like dinosaurs.

Nature 2017 12 6;552(7685):395-399. Epub 2017 Dec 6.

Directorate Earth & History of Life, Royal Belgian Institute of Natural Sciences, B-1000 Brussels, Belgium.

Maniraptora includes birds and their closest relatives among theropod dinosaurs. During the Cretaceous period, several maniraptoran lineages diverged from the ancestral coelurosaurian bauplan and evolved novel ecomorphologies, including active flight, gigantism, cursoriality and herbivory. Propagation X-ray phase-contrast synchrotron microtomography of a well-preserved maniraptoran from Mongolia, still partially embedded in the rock matrix, revealed a mosaic of features, most of them absent among non-avian maniraptorans but shared by reptilian and avian groups with aquatic or semiaquatic ecologies. This new theropod, Halszkaraptor escuilliei gen. et sp. nov., is related to other enigmatic Late Cretaceous maniraptorans from Mongolia in a novel clade at the root of Dromaeosauridae. This lineage adds an amphibious ecomorphology to those evolved by maniraptorans: it acquired a predatory mode that relied mainly on neck hyperelongation for food procurement, it coupled the obligatory bipedalism of theropods with forelimb proportions that may support a swimming function, and it developed postural adaptations convergent with short-tailed birds.
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http://dx.doi.org/10.1038/nature24679DOI Listing
December 2017

Synchrotron imaging and Markov Chain Monte Carlo reveal tooth mineralization patterns.

PLoS One 2017 19;12(10):e0186391. Epub 2017 Oct 19.

Department of Human Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States of America.

The progressive character of tooth formation records aspects of mammalian life history, diet, seasonal behavior and climate. Tooth mineralization occurs in two stages: secretion and maturation, which overlap to some degree. Despite decades of study, the spatial and temporal pattern of elemental incorporation during enamel mineralization remains poorly characterized. Here we use synchrotron X-ray microtomography and Markov Chain Monte Carlo sampling to estimate mineralization patterns from an ontogenetic series of sheep molars (n = 45 M1s, 18 M2s). We adopt a Bayesian approach that posits a general pattern of maturation estimated from individual- and population-level mineral density variation over time. This approach converts static images of mineral density into a dynamic model of mineralization, and demonstrates that enamel secretion and maturation waves advance at nonlinear rates with distinct geometries. While enamel secretion is ordered, maturation geometry varies within a population and appears to be driven by diffusive processes. Our model yields concrete expectations for the integration of physiological and environmental signals, which is of particular significance for paleoseasonality research. This study also provides an avenue for characterizing mineralization patterns in other taxa. Our synchrotron imaging data and model are available for application to multiple disciplines, including health, material science, and paleontological research.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0186391PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5648163PMC
November 2017

New infant cranium from the African Miocene sheds light on ape evolution.

Nature 2017 08;548(7666):169-174

Department of Cell and Developmental Biology, University College London, London WC1E 6BT, UK.

The evolutionary history of extant hominoids (humans and apes) remains poorly understood. The African fossil record during the crucial time period, the Miocene epoch, largely comprises isolated jaws and teeth, and little is known about ape cranial evolution. Here we report on the, to our knowledge, most complete fossil ape cranium yet described, recovered from the 13 million-year-old Middle Miocene site of Napudet, Kenya. The infant specimen, KNM-NP 59050, is assigned to a new species of Nyanzapithecus on the basis of its unerupted permanent teeth, visualized by synchrotron imaging. Its ear canal has a fully ossified tubular ectotympanic, a derived feature linking the species with crown catarrhines. Although it resembles some hylobatids in aspects of its morphology and dental development, it possesses no definitive hylobatid synapomorphies. The combined evidence suggests that nyanzapithecines were stem hominoids close to the origin of extant apes, and that hylobatid-like facial features evolved multiple times during catarrhine evolution.
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http://dx.doi.org/10.1038/nature23456DOI Listing
August 2017

Synchrotron phase-contrast microtomography of coprolites generates novel palaeobiological data.

Sci Rep 2017 06 2;7(1):2723. Epub 2017 Jun 2.

Department of Organismal Biology, Evolutionary Biology Centre, Uppsala University, Norbyvägen 18A, 752 36, Uppsala, Sweden.

Coprolites (fossil faeces) reveal clues to ancient trophic relations, and contain inclusions representing organisms that are rarely preserved elsewhere. However, much information is lost by classical techniques of investigation, which cannot find and image the inclusions in an adequate manner. We demonstrate that propagation phase-contrast synchrotron microtomography (PPC-SRμCT) permits high-quality virtual 3D-reconstruction of coprolite inclusions, exemplified by two coprolites from the Upper Triassic locality Krasiejów, Poland; one of the coprolites contains delicate beetle remains, and the other one a partly articulated fish and fragments of bivalves.
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http://dx.doi.org/10.1038/s41598-017-02893-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5457397PMC
June 2017

Development of cyclic shedding teeth from semi-shedding teeth: the inner dental arcade of the stem osteichthyan .

R Soc Open Sci 2017 May 17;4(5):161084. Epub 2017 May 17.

Department of Organismal Biology, Uppsala University, Norbyvägen 18A, 752 36, Uppsala, Sweden.

The numerous cushion-shaped tooth-bearing plates attributed to the stem group osteichthyan , which are argued here to represent an early form of the osteichthyan inner dental arcade, display a previously unknown and presumably primitive mode of tooth shedding by basal hard tissue resorption. They carry regularly spaced, recumbent, gently recurved teeth arranged in transverse tooth files that diverge towards the lingual margin of the cushion. Three-dimensional reconstruction from propagation phase-contrast synchrotron microtomography (PPC-SRµCT) reveals remnants of the first-generation teeth embedded in the basal plate, a feature never previously observed in any taxon. These teeth were shed by semi-basal resorption with the periphery of their bases retained as dentine rings. The rings are highly overlapped, which evidences tooth shedding prior to adding the next first-generation tooth at the growing edge of the plate. The first generation of teeth is thus diachronous. Successor teeth at the same sites underwent cyclical replacing and shedding through basal resorption, producing stacks of buried resorption surfaces separated by bone of attachment. The number and spatial arrangement of resorption surfaces elucidates that basal resorption of replacement teeth had taken place at the older tooth sites before the addition of the youngest first-generation teeth at the lingual margin. Thus, the replacement tooth buds cannot have been generated by a single permanent dental lamina at the lingual edge of the tooth cushion, but must have arisen either from successional dental laminae associated with the individual predecessor teeth, or directly from the dental epithelium of these teeth. The virtual histological dissection of these Late Silurian microfossils broadens our understanding of the development of the gnathostome dental systems and the acquisition of the osteichthyan-type of tooth replacement.
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http://dx.doi.org/10.1098/rsos.161084DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5451804PMC
May 2017

Thoracic vertebral count and thoracolumbar transition in .

Proc Natl Acad Sci U S A 2017 06 22;114(23):6000-6004. Epub 2017 May 22.

Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637.

The evolution of the human pattern of axial segmentation has been the focus of considerable discussion in paleoanthropology. Although several complete lumbar vertebral columns are known for early hominins, to date, no complete cervical or thoracic series has been recovered. Several partial skeletons have revealed that the thoracolumbar transition in early hominins differed from that of most extant apes and humans. , and all had zygapophyseal facets that shift from thoracic-like to lumbar-like at the penultimate rib-bearing level, rather than the ultimate rib-bearing level, as in most humans and extant African apes. What has not been clear is whether had 12 thoracic vertebrae as in most humans, or 13 as in most African apes, and where the position of the thoracolumbar transitional element was. The discovery, preparation, and synchrotron scanning of the partial skeleton DIK-1-1, from Dikika, Ethiopia, provides the only known complete hominin cervical and thoracic vertebral column before 60,000 years ago. DIK-1-1 is the only known skeleton to preserve all seven cervical vertebrae and provides evidence for 12 thoracic vertebrae with a transition in facet morphology at the 11th thoracic level. The location of this transition, one segment cranial to the ultimate rib-bearing vertebra, also occurs in all other early hominins and is higher than in most humans or extant apes. At 3.3 million years ago, the DIK-1-1 skeleton is the earliest example of this distinctive and unusual pattern of axial segmentation.
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http://dx.doi.org/10.1073/pnas.1702229114DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5468642PMC
June 2017

100-million-year-old conifer tissues from the mid-Cretaceous amber of Charente (western France) revealed by synchrotron microtomography.

Ann Bot 2017 01 10;119(1):117-128. Epub 2016 Dec 10.

European Synchrotron Radiation Facility, 71 avenue des Martyrs, 38000 Grenoble, France.

Background And Aims: Terrestrial plant remains in fossilized tree resin are relatively common. However, histology and preservation of plants entombed in Cretaceous ambers remain poorly known. We report an exquisitely preserved conifer leafy axis from 100-million-year-old opaque amber of western France that is assignable to Glenrosa carentonensis Moreau, Néraudeau, Tafforeau & Dépré. The purpose of this paper is to discuss the taphonomy and the use of microtomography for studies of palaeobotanical remains in amber.

Methods: A leafy axis was examined using propagation phase-contrast X-ray synchrotron microtomography with voxel sizes of 14·9, 1·4, and 0·7 μm.

Key Results: The conifer leafy axis described is preserved in three dimensions. Despite desiccation of the specimen within the surrounding amber, the cuticle, as well as most of inner tissues, is preserved in three dimensions down to the cellular level. Epidermis, palisade parenchyma, spongy parenchyma, transfusion tracheids and vascular bundles are clearly distinguished.

Conclusions: Gross morphology and histology of the specimen were revealed using synchrotron microtomography, allowing an unprecedented resolution for the study of soft-bodied plants entombed in amber. The study reveals a peculiar combination of authigenic and duripartic preservation as well as permineralization, and highlights the complexity of taphonomic processes that can occur in amber inclusions. This fossil demonstrates the difficulty of studying amber-preserved plant remains under certain conditions.
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http://dx.doi.org/10.1093/aob/mcw225DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5218381PMC
January 2017

The stem osteichthyan Andreolepis and the origin of tooth replacement.

Nature 2016 11 17;539(7628):237-241. Epub 2016 Oct 17.

Science for Life Laboratory and Uppsala University, Department of Organismal Biology, Norbyvägen 18A, SE-752 36 Uppsala, Sweden.

The teeth of gnathostomes (jawed vertebrates) show rigidly patterned, unidirectional replacement that may or may not be associated with a shedding mechanism. These mechanisms, which are critical for the maintenance of the dentition, are incongruently distributed among extant gnathostomes. Although a permanent tooth-generating dental lamina is present in all chondrichthyans, many tetrapods and some teleosts, it is absent in the non-teleost actinopterygians. Tooth-shedding by basal hard tissue resorption occurs in most osteichthyans (including tetrapods) but not in chondrichthyans. Here we report a three-dimensional virtual dissection of the dentition of a 424-million-year-old stem osteichthyan, Andreolepis hedei, using propagation phase-contrast synchrotron microtomography, with a reconstruction of its growth history. Andreolepis, close to the common ancestor of all extant osteichthyans, shed its teeth by basal resorption but probably lacked a permanent dental lamina. This is the earliest documented instance of resorptive tooth shedding and may represent the primitive osteichthyan mode of tooth replacement.
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http://dx.doi.org/10.1038/nature19812DOI Listing
November 2016

Comparative biomechanics of Australopithecus sediba mandibles.

J Hum Evol 2016 11;100:73-86

Evolutionary Studies Institute, University of the Witwatersrand, Private Bag 3, Johannesburg 2050, South Africa.

Fossils attributed to Australopithecus sediba are described as having phylogenetic affinities with early Homo to the exclusion of other South African australopiths. With respect to functional anatomy of mastication, one implication of this hypothesis is that A. sediba mandibles should exhibit absolutely and relatively reduced stiffness and strength in comparison to Australopithecus africanus and Paranthropus robustus jaws. Examination of cortical bone distribution in the MH 1 and MH 2 mandibles of A. sediba (evaluated against samples of Pan, early and modern Homo as well as A. africanus and P. robustus) indicate that the A. sediba mandibular corpus was geometrically similar to other South African australopiths. In particular, enhanced torsional rigidity is characteristic of all South African australopiths including A. sediba. These findings are consistent with a hypothesis that masticatory mechanics may have been similar to other australopiths (and distinct from exemplars of early Homo), and as such suggest that A. sediba's mandibles were functionally suited to consume hard and tough objects. Recent mechanical modeling of the A. sediba cranium, however, has been interpreted as indicating that this species was relatively poorly adapted to produce large bite forces and likely experienced relatively modest strains in its facial skeleton. This paradox - that the cranium signals a departure from the australopith morphotype whereas the mandibles conform to a hypodigm of australopith grade - can be resolved, in part, if it is acknowledged that mechanical performance variables offer imperfect insight into what constitutes feeding adaptations.
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http://dx.doi.org/10.1016/j.jhevol.2016.08.006DOI Listing
November 2016