Ingmar Werneburg

University of Tübingen

Author Statistics

Papers

Citation

H-Index

i-10 index

Research Trends

Author Order

Document Type

Co-Authors

Daisuke Koyabu

University of Tsukuba

Marcelo R. Sánchez‐Villagra

University of Zurich

Oleksandr Yaryhin

I.I. Schmalhausen Institute of Zoology

Taro Nojiri

Juntendo University

Vương Tân Tú

Vietnam Academy of Science and Technology

Masaki Takechi

Juntendo University

Dai Fukui

University of Yamanashi

Toshiko Furutera

Juntendo University

Gabriel S. Ferreira

Universidade Federal do Rio de Janeiro

Nikolay Natchev

Shumen University

Cooperative Institutions

John Wiley & Sons (United States)

Hudson Institute

Centro Científico Tecnológico - Patagonia Norte

Liechtenstein Institute

University of Tübingen

University of Zurich

Museum für Naturkunde

Senckenberg Centre for Human Evolution and Palaeoenvironment

Natural History Museum

The University of Tokyo

Author Statistics

Papers

Citation

H-Index

i-10 index

Research Field

Modeling neck mobility in fossil turtles

Journal of Experimental Zoology Part B Molecular and Developmental Evolution (2014)

Ingmar Werneburg Juliane K. Hinz Michaela Gumpenberger Virginie Volpato Nikolay Natchev

ABSTRACT Turtles have the unparalleled ability to retract their heads and necks within their shell but little is known about the evolution of this trait. Extensive analysis of neck mobility in turtles using radiographs, CT scans, and morphometry reveals that basal turtles possessed less mobility in the neck relative to their extant relatives, although the anatomical prerequisites for modern mobility were already established. Many extant turtles are able to achieve hypermobility by dislocating the central articulations, which raises cautions about reconstructing the mobility of fossil vertebrates. A 3D‐model of the Late Triassic turtle Proganochelys quenstedti reveals that this early stem turtle was able to retract its head by tucking it sideways below the shell. The simple ventrolateral bend seen in this stem turtle, however, contrasts with the complex double‐bend of extant turtles. The initial evolution of neck retraction therefore occurred in a near‐synchrony with the origin of the turtle shell as a place to hide the unprotected neck. In this early, simplified retraction mode, the conical osteoderms on the neck provided further protection. J. Exp. Zool. (Mol. Dev. Evol.) 324B: 230–243, 2015 . © 2014 Wiley Periodicals, Inc.

10.1002/jez.b.22557

Cite

Citations (49)

Author response for "Domestication and the comparative embryology of birds"

Gerardo A. Cordero Ingmar Werneburg

Embryology

10.1002/jez.b.23144/v2/response1

Cite

Citations (0)

Morphological association between muscle attachments and ossification sites in the late cartilaginous skull of tuatara embryos

Journal of Morphology (2022)

Zitong Zhang Oleksandr Yaryhin Daisuke Koyabu Ingmar Werneburg

During development, the embryonic cartilaginous skull in most vertebrates is partially replaced by bones with endochondral and perichondral ossifications. Muscle attachments are thought to influence the patterns of ossification and, hence, the differentiation of the skull. To investigate the association between muscle attachments and early ossifications of reptilian embryos, we conducted digital 3D reconstructions of the cranium, the head, and the neck musculature from a histological section series of a late term embryonic tuatara, Sphenodon punctatus, with a total body length of 52 mm. As the sole living rhynchocephalian species, it is an important outgroup in comparative studies of squamate evolution. We found that head and neck muscles are largely associated with early ossification of the basal plate and the palatoquadrate, and with three other ossifications in an older specimen with a total body length of 72 mm. These results suggest that tensile forces resulting from embryonic muscle contraction are largely, but not exclusively, correlated with the area of endochondral ossification in the chondrocranium and palatoquadrate in tuatara. Beyond little-known genetic factors, the complexity of chondrocranial architecture, the progress of its development, and the effect of multiple muscle transmitting forces in the chondrocranium must be considered to provide a more comprehensive discussion of the mechanical properties of the embryonic skull.

Endochondral ossification

Cranial vault

Neurocranium

10.1002/jmor.21474

Cite

Citations (3)

Trifold origin of the reptilian ear ossicle and its relation to the evolutionary modification of the temporal skull region

Journal of Anatomy (2024)

Ingmar Werneburg Mario Bronzati

Abstract Whereas mammals are characterized by the presence of three middle ear ossicles, reptiles have only one, the columella (stapes). Nevertheless, there is a great diversity of columellar anatomy among sauropsids, especially in the unique and cartilaginous “extracolumella”‐portion. Molecular studies revealed the “columella” of chicken and quails to be formed within the second pharyngeal arch, although conflicting evidence exists for the columellar footplate and distal parts of the columella in these birds. We studied columellar development in four turtles, one lizard, and one caiman species and argue, using early blastematous stages, that, distally, the so‐called “extracolumella” in turtles is mainly of quadrate, that is, first pharyngeal arch origin. Differently, the dorsal aspect of the “extracolumella” of the lizard and a part of the “dorsal columella process” of the caiman are likely quadrate‐derived. This indicates only a partial homology of the distal columellar compartments among reptiles. Moreover, we observed in most species that, at early stages, the footplate differentiates from the otic capsule, which confirms widespread experimental findings of mesodermal cells contributing to the proximal part of the columella. We provide a hypothetical framework for the changes in the columella and quadrate morphology in reptilian evolution. Originally, as evidenced by the fossil record, the columella served as a stabilizing brace between the quadrate and braincase. Associated with changes in the feeding mode of late Permian taxa, the quadrate was integrated along the stress flows from biting, and in early development part of the quadrate differentiated to differently contribute to the distal part of the “columella‐complex,” which now contacts the tympanic membrane. In addition, part of the original otic capsule contributes to the footplate of the mobile columella, providing a connection with the inner ear.

Quadrate bone

Columella

Ossicles

Footplate

Amniote

Elasmobranchii

10.1111/joa.14105

Cite

Citations (2)

Sensory Evolution and Ecology of Early Turtles Revealed by Digital Endocranial Reconstructions

Frontiers in Ecology and Evolution (2018)

Stephan Lautenschlager Gabriel S. Ferreira Ingmar Werneburg

In the past few years, new fossil finds and novel methodological approaches have prompted intensive discussions about the phylogenetic affinities of turtles and rekindled the debate on their ecological origin, with very distinct scenarios, such as fossoriality and aquatic habitat occupation, proposed for the earliest stem-turtles. While research has focused largely on the origin of the anapsid skull and unique postcranial anatomy, little is known about the endocranial anatomy of turtles. Here, we provide 3D digital reconstructions and comparative descriptions of the brain, nasal cavity, neurovascular structures and endosseous labyrinth of Proganochelys quenstedti, one of the earliest stem-turtles, as well as other turtle taxa. Our results demonstrate that P. quenstedti had retained a simple tube-like brain morphology with poorly differentiated regions and mediocre hearing and vision, but a well-developed olfactory sense. Endocast shape analysis indicates that an increase in size and regionalization of the brain took place in the course of turtle evolution, achieving an endocast diversity comparable to other amniote groups. Based on the new evidence, we further conclude that P. quenstedti was a highly terrestrial, but most likely not a fossorial taxon

Endocast

Postcrania

Amniote

Fossorial

10.3389/fevo.2018.00007

Cite

Citations (64)

Morphology of the suspensorial, jaw, and opercle musculature of Beloniformes and related species (Teleostei: Acanthopterygii), with a special reference to the m. adductor mandibulae complex

Ingmar Werneburg

The taxon Beloniformes represents a heterogeneous group of teleost fishes that show an extraordinary diversity of jaw morphology. I present new anatomical descriptions of the jaw musculature in six selected beloniforms and four closely related species. A reduction of the external jaw adductor (A1) and a changed morphology of the intramandibular musculature were found in many Beloniformes. This might be correlated with the progressively reduced mobility of the upper and lower jaw bones. The needlefishes and sauries, which are characterised by extremely elongated and stiffened jaws, show several derived characters, which in combination enable the capture of fish at high velocity. The ricefishes are characterised by several derived and many plesiomorphic characters that make broad scale comparisons difficult. Soft tissue characters are highly diverse among hemiramphids and flying fishes reflecting the uncertainty about their phylogenetic position and interrelationship. The morphological findings presented herein may help to interpret future phylogenetic analyses using cranial musculature in Beloniformes.

Teleostei

Morphology

10.7287/peerj.preprints.691v1

Cite

Citations (0)

Dynamic evolutionary interplay between ontogenetic skull patterning and whole-head integration

Zenodo (CERN European Organization for Nuclear Research) (2024)

Joni Ollonen Eraqi R. Khannoon Simone Macrì Vladislav Vergilov Jaakko Kuurne

Data and code for the analysis in Ollonen et al., 2024, Dynamic evolutionary interplay between ontogenetic skull patterning and whole-head integration, Nature Ecology and Evolution. Raw landmark data, R scripts for the analysis and surface files used for the analysis as well as figure visualisations. Cite the original article, not the dataset citation!!!

10.5281/zenodo.8376575

Cite

Citations (0)

Evolution and development of turtles: organogenesis and cranial musculature

Ingmar Werneburg

Two mechanisms can be detected in evolution leading to differentiating ontogenic patterns and adult morphology: Heterochrony, changes in the timing of developmental characters; and heterotopy, displacements of homologous structures in development. To explore aspects of their patterns and their interrelationship, both phenomena were exemplarily studied in land vertebrates, particularly in its most debated taxon, Testudines. In one part of the thesis the organogenesis of different tetrapod taxa was compared. Therefore a standard system to study vertebrate embryos was developed based on clear anatomical definitions of developmental characters. The study includes recommendations on how to use such characters within a phylogenetic framework, how to handle them in embryological collections and how to deal with them in molecular oriented laboratories. In total 104 organogenic characters were compared among embryos of 23 tetrapod species, including 15 turtle species. Using the Parsimov algorithm we were able to detect heterochronic shifts that autapomorphically support particular nodes in alternative topologies. Our embryological data and the analyses performed best support a sistergroup position of Testudines to all remaining living sauropsids, and a basal position of marine turtles within Cryptodira. The heterochronic shifts detected could – with caution – be correlated to differentiating feeding and locomotion behaviours in early life history of mammals and reptiles or to the count of vertebrae in the respective taxa. As this study exclusively deals with a neontological kind of data we could not differentiate whether turtles evolved within “Anapsida” or on the stemline of Sauria within Diapsida. For two amniote species – the turtle Emydura subglobosa and the mammal Tachyglossus aculeatus – organogenetic patterns were exemplarily described in detail and their timing was correlated to ossification, myogenesis or early crawling behaviour. Alternative topologies were tested among Mammalia to detect the robusticity of heterochronic data – resulting in a critical interpretation of this non-independent kind of data for phylogenetic approaches. Another part of the thesis is concerned with the heterotopic aspect of evolution. In the studies mentioned above I recognised several heterochronic shifts to include head-related characters. Uncertainties about the phylogenetic position of turtles within Tetrapoda are mainly based on the arrangement of temporal bones, and studies on organogenesis did not result in a definitive solution. Hence, the anatomy of the cranium associated musculature in turtles was comparatively studied. A clear definition of muscular structures in general and a review on all studies dealing with cranial musculature in turtles are presented. The homology of 88 muscular units are discussed. I focussed on the evolution of jaw musculature within Testudines and performed phylogenetic analyses having several alternative topologies as phylogenetic frameworks. The hardly comparable jaw muscle anatomy within Sauropsida does not suggest a solution for the position of turtles; hence, a non-homologous arrangement of jaw musculature in the major tetrapod taxa and a position of turtles outside of Sauria are proposed. The jaw muscle characters best support the currently most accepted arrangement of turtle subgroups, presuming 1. South American and Australasian chelids (Pleurodira) to be monophyletic groups and 2. soft-shelled turtles (Trionychidae) being the sister taxon to all remaining living cryptodires. The value of soft tissue characters for phylogenetic reconstruction is discussed and a system for muscle development and evolution is proposed that most adequately reflects the plastic behaviour of this structure in time and space. ZUSAMMENFASSUNG In der Evolution konnen zwei Mechanismen beschrieben werden, die zu unterschiedlichen Entwicklungsmustern und zu verschiedener Adultmorphologie fuhren: Heterochronien, Anderungen im zeitlichen Auftreten; und Heterotopien, raumliche Verschiebungen homologer Strukturen. Um einzelne Aspekte und ihre Beziehung zueinander zu untersuchen, wurden beide Phanomene exemplarisch in Landwirbeltieren, insbesondere ihrem am haufigsten diskutieren Taxon, den Testudines, untersucht. In einem Teil der Arbeit wurde die Organogenese verschiedener Tetrapoden verglichen. Basierend auf klar definierten Entwicklungsmerkmalen, wurde dafur ein Standardsystem zur Untersuchung von Wirbeltierembryonen entwickelt. Empfehlungen zur Handhabung dieser Merkmale in phylogenetischen Studien, in embryologischen Sammlungen und in molekularen Laboratorien werden unterbreitet. Bei 23 Landwirbeltierarten, davon 15 Schildkroten, wurden insgesamt 104 Merkmale der Organogenese verglichen. Unter Verwendung des Parsimov Algorithmus’ konnten heterochrone Verschiebungen detektiert werden, die die jeweilige Verzweigungen in alternativen Topologien unterstutzen. Die embryologischen Daten und die verwendete Untersuchungsmethode unterstutzen am besten ein Schwestergruppenverhaltnis Testudines zu allen anderen lebenden Sauropsiden, sowie eine basale Stellung der Meeresschildkroten innerhalb der Cryptodira. Die festgestellten heterochronen Verschiebungen konnten – mit Vorbehalt – mit dem unterschiedlichen Fres- oder Fortbewegungsverhalten im fruhen Lebensabschnitt der Saugetiere und Reptilien oder der Wirbelanzahl der einzelner Gruppen korreliert werden. Da diese Arbeit ausschlieslich neonthologische Daten untersuchte, war es nicht moglich zu unterscheiden, ob Schildkroten innerhalb der „Anapsida“ oder auf der Stammlinie der Sauria innerhalb der Diapsida entstanden sind. Fur zwei Arten der Amniota – fur die Schildkrote Emydura subglobosa und den Sauger Tachyglossus aculeatus – wurde zum ersten Mal die Organentwicklung im Detail beschrieben und ihr zeitliches Muster konnte mit der Verknocherung, der Muskelentwicklung oder dem fruhen Kletterverhalten korreliert werden. Unterschiedliche Verwandtschaftsverhaltnisse der Saugetiere wurden verglichen, um die Aussagekraft heterochroner Daten zu testen. Der Wert dieser unabhangigen Daten fur stammesgeschichtliche Ansatze wird kritisch beurteilt. Ein weiterer Teil der vorliegenden Arbeit befast sich mit heterotopen Aspekten der Evolution. In den oben genannten Untersuchungen wurden zahlreiche heterochrone Verschiebungen festgestellt, die Merkmale der Kopfentwicklung beinhalten. Unklarheiten zur phylogenetischen Stellung der Schildkroten betreffen vor allem die Anordnung der Schadelknochen und die Untersuchungen zur Organogenese konnten keine definitive Stammbaumhypothese liefern. Daher wurde die Anatomie der Cranium-assoziierten Muskulatur der Schildkroten vergleichend untersucht. Hierfur wurden im Allgemeinen klare Definitionen muskularer Strukturen prasentiert und eine Zusammenschau aller bisherigen Veroffentlichungen, die sich mit Kopfmuskeln der Schildkroten beschaftigen, vorgestellt. Die Homologien von 88 Muskeleinheiten (muscular units) werden diskutiert. Die Kiefermuskulatur der Schildkroten wird naher untersucht und, basierend auf verschiedenen Topologien, phylogenetische Analysen durchgefuhrt. Die schwer vergleichbare Anatomie der Kiefermuskulatur in den Sauropsiden last auf keine Losung fur die Stellung der Schildkroten schliesen. Daher wird eine nicht homologe Architektur der Kiefermuskeln innerhalb der Tetrapoden-Gruppen und eine Stellung der Schildkroten auserhalb der Sauria vorgeschlagen. Die Merkmale der Kiefermuskulatur unterstutzen am besten die gegenwartig weitgehend akzeptierte Hypothese zur Verwandtschaft der einzelnen Schildkrotengruppen. Diese nimmt an, das 1. die sudamerikanischen und die australisch-asiatischen Cheliden (Pleurodira) jeweils eine monophyletische Gruppe bilden oder, das 2. die Weichschildkroten (Trionychidae) allen ubrigen lebenden Cryptodiren gegenuberstehen. Der Wert von Weichgewebe fur phylogenetische Rekonstruktionen wird diskutiert und ein System zur Muskelentwicklung und - evolution wird vorgeschlagen, das am adaquatesten das plastische Verhalten dieser Struktur in Raum und Zeit darstellt.

Organogenesis

10.5167/uzh-39844

Cite

Citations (7)

Dentition and feeding in Placodontia: tooth replacement in Henodus chelyops

BMC Ecology and Evolution (2021)

Yannick Pommery Torsten M. Scheyer James M. Neenan Tobias Reich Vincent Fernández

Abstract Background Placodontia is a Triassic sauropterygian reptile group characterized by flat and enlarged crushing teeth adapted to a durophagous diet. The enigmatic placodont Henodus chelyops has numerous autapomorphic character states, including extreme tooth count reduction to only a single pair of palatine and dentary crushing teeth. This renders the species unusual among placodonts and challenges identification of its phylogenetic position. Results The skulls of two Henodus chelyops specimens were visualized with synchrotron tomography to investigate the complete anatomy of their functional and replacement crushing dentition in 3D. All teeth of both specimens were segmented, measured, and statistically compared to reveal that H. chelyops teeth are much smaller than the posterior palatine teeth of other cyamodontoid placodonts with the exception of Parahenodus atancensis from the Iberian Peninsula. The replacement teeth of this species are quite similar in size and morphology to the functional teeth. Conclusion As other placodonts, Henodus chelyops exhibits vertical tooth replacement . This suggests that vertical tooth replacement arose relatively early in placodont phylogeny. Analysis of dental morphology in H. chelyops revealed a concave shape of the occlusal surface and the notable absence of a central cusp. This dental morphology could have reduced dental wear and protected against failure. Hence, the concave teeth of H. chelyops appear to be adapted to process small invertebrate items, such as branchiopod crustaceans. Small gastropods were encountered in the matrix close to both studied skulls.

Autapomorphy

Posterior teeth

10.1186/s12862-021-01835-4

Cite

Citations (6)

Neutron Imaging in Cultural Heritage Research at the FRM II Reactor of the Heinz Maier-Leibnitz Center

Journal of Imaging (2018)

Burkhard Schillinger Amélie Beaudet Anna Fedrigo Francesco Grazzi Ottmar Kullmer

Neutron Imaging is ideally suited for applications in cultural heritage even at small reactors with moderate image resolution. However, recently, high resolution imaging is being increasingly used for advanced studies, especially in paleontology. The special contrast for hydrogen and between neighboring elements in the periodic system allows for new applications that are not accessible for X-rays, like organic material in enclosed containers made of ceramics or metals, fossilized bones in chalk rock or in ferrous “red” beds, and even for animal and hominid teeth. Fission neutrons permit the examination of large samples that otherwise show large attenuation for thermal neutrons.

Center (category theory)

Neutron Imaging

10.3390/jimaging4010022

Cite

Citations (28)