Combing Paleontology and Developmental Biology to Understand Skull Evolution in Turtles

• Applicant: Privatdozent Dr. Ingmar Werneburg
• Subject Area: Palaeontology ; Developmental Biology ; Evolution, Anthropology
• Term: from 2019 to 2024
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 415747545

• Final Report Year: 2025

Final Report Abstract

In this project, we aimed at understanding the evolutionary origin of the diversity in the temporal region of land vertebrate skulls, with an initial focus on turtles. The project successfully generated 68 publications, including contributions to high-impact journals such as Nature Communications and PNAS. The project's findings are categorized into seven main areas: 1. Head/Neck-interface: Using Finite Element Analyses, our research demonstrated a progressive correlation between skull architecture and neck evolution in turtles. 2. General Cranial Anatomy: Several studies explored the complex interplay of various organ systems in the head. Using Anatomical Network Analysis, we identified "functional modules" in the skull and highlighted feeding mode as a major driver of temporal region evolution across diverse land vertebrates. 3. General Cranial Development: Using classical histological and gross morphological observations, a comprehensive research program on the embryonic cartilaginous skull (chondrocranium) was developed, leading to a better understanding of its evolution and the ossification modes of dermal bones, which are formed on the top of the chondrocranium and lay the basics for adult temporal bone architecture. 4. Turtle Cranial Anatomy: The initial focus on turtles continued with studies on neurovascular anatomy, the labyrinth organ, and the hyoid apparatus in extant and fossil species. A significant discovery showed how movements in turtle embryos influence the shaping of the temporal region. 5. The Evolution of the Temporal Region in Land Vertebrates: We analyzed historical hypotheses on the temporal skull region and studied cranial suture anatomy in early amniotes. Novel biomechanical hypotheses were developed to explain temporal skull architecture, relating bite forces to postorbital bone arrangement, which garnered significant scientific and public attention. 6. Theoretical aspects of Developmental Timing: Several papers were published on the timing of developmental characters, aiding in the interpretation of skull development studies. 7. Theoretical aspects of Comparative Anatomy: This part of the project contributed to general questions of comparative anatomy, emphasizing the necessity of analyzing ontogenetic, paleontological, embryological, zoological, and biomechanical approaches in parallel to address morphological questions effectively. This aligns with the 19th-century "Vergleichende Entwicklungsgeschichte" approach of Carl Gegenbaur, now enhanced with modern tools. The results of the present project have opened new avenues for future research, particularly emphasizing the ontogeny of the temporal region. The extensive body of morphological insights generated by this project lays a strong foundation for continued exploration into the intricate evolutionary pathways of skull morphology in vertebrates.

Publications

• Morphofunctional Categories and Ontogenetic Origin of Temporal Skull Openings in Amniotes. Frontiers in Earth Science, 7.
  Werneburg, Ingmar
  
• Feeding biomechanics suggests progressive correlation of skull architecture and neck evolution in turtles. Scientific Reports, 10(1).
  Ferreira, Gabriel S.; Lautenschlager, Stephan; Evers, Serjoscha W.; Pfaff, Cathrin; Kriwet, Jürgen; Raselli, Irena & Werneburg, Ingmar
  
• On the “cartilaginous rider” in the endocasts of turtle brain cavities. Vertebrate Zoology, 71, 403-418.
  Werneburg, Ingmar; Evers, Serjoscha W. & Ferreira, Gabriel
  
• Modeling Skull Network Integrity at the Dawn of Amniote Diversification With Considerations on Functional Morphology and Fossil Jaw Muscle Reconstructions. Frontiers in Ecology and Evolution, 9.
  Werneburg, Ingmar & Abel, Pascal
  
• Skull Sutures and Cranial Mechanics in the Permian Reptile Captorhinus aguti and the Evolution of the Temporal Region in Early Amniotes. Frontiers in Ecology and Evolution, 10.
  Abel, Pascal; Pommery, Yannick; Ford, David Paul; Koyabu, Daisuke & Werneburg, Ingmar
  
• Tetrapod Water-Land Transition: Reconstructing Soft Tissue Anatomy and Function. Frontiers Research Topics. Frontiers Media SA.
  Molnar, Julia L.; Diogo, Rui; Werneburg, Ingmar & Boisvert, Catherine Anne
  
• Evolution of the temporal skull openings in land vertebrates: A hypothetical framework on the basis of biomechanics. The Anatomical Record, 307(4), 1559-1593.
  Werneburg, Ingmar & Preuschoft, Holger
  
• Terrestrialisation and the cranial architecture of tetrapods. Fossil Record, 27(3), 473-497.
  Werneburg, Ingmar
  
• The temporal region of the tetrapod skull: a textbook example on integrative morphology. Revue de Paléobiologie 43(1): 101-118 (Proceedings volume of the fifth international Georges Cuvier symposium in Montbéliard)
  Pascal Abel & Ingmar Werneburg
  
• Trifold origin of the reptilian ear ossicle and its relation to the evolutionary modification of the temporal skull region. Journal of Anatomy, 246(3), 402-414.
  Werneburg, Ingmar & Bronzati, Mario