Evolution and development of the pseudosuchian skull table sutures and its impact on the cranial topology

Abstract

Reorganization (i.e., rearrangement, fusion, or loss) of cranial bones is one of the most striking ways to introduce evolutionary novelties in the cranium. It is accomplished by the co-option (reuse) of pre-existing developmental processes and morphological characteristics. To understand how this process works from both macro-evolutionary and developmental directions, I looked at the cranial reorganization of pseudosuchians, a reptilian lineage that includes crocodiles and their common ancestors. Although only a few modern crocodylians still exist today, extinct pseudosuchians greatly diversified and prospered from the Mesozoic to the Cenozoic era and adapted to multiple ecological niches, such as land, saltwater and freshwater habitats. Their sturdy cranial fossils are often well-preserved and can represent the major evolutionary transitions in the pseudosuchian life history. Following the structure of a typical evo-devo study, I began with exploring the macroevolution of cranial reorganization in pseudosuchians (Chapter 1), compared these characteristics with its sister group, the dinosaurs (Chapter 2), chose a specific feature (i.e. suture anatomy of the frontal and parietal bones) and looked at their morphological changes during development (Chapter 3), and attempted to learn more about their developmental mechanism (Chapter 4). Multiple interdisciplinary techniques were used: computed tomography scan of crocodylian skulls, computer modeling of the cranial arrangement called Anatomical Network Analysis (AnNA), geometric morphometrics to record the diversity of suture shape, and histology, and immunofluorescence to identify key proteins involved in formation of bones. Using AnNA, I showed that pseudosuchians had a smaller reorganization compared to avialans (Chapter 2). This macroevolutionary reorganization manifested as a skull bone reduction from crown pseudosuchians to modern crocodylians and was associated with the fusion of the frontals and parietals (Chapter 1). The frontal and parietal bones and their homologues were identified as the cranial bones with the greatest burden (i.e., highly connected to other bones and subjected to higher levels of constraint) in archosaurs (Chapter 2). Fusion of these bones is an excellent example of heterochrony: the development stage for complete fusion of interfrontal and interparietal suture shifted from juveniles in eusuchian (stem crocodylian) to embryos in crocodylians (Chapter 3). Similarities with other amniotes also revealed a conserved pattern of sutural form: sutures begin from a simple morphotype (i.e., abutting joint) with minimal interdigitations, and then, as they receive mechanical input, diversify in post-embryonic stages by either fusing, maintaining their embryonic form, or increasing interdigitation and joint complexity into their lineage-specific form (Chapter 3). Histology and immunofluorescence showed the ossification of the frontal and parietal bones rely on the mechanosensitive Wnt and BMP signaling pathways and osteoblast-osteoclast balance (Chapter 4). The intertwining signaling pathway and patterns of ossification also show that the interdependent development of the forebrain, skull roof/skull table, and facial bones.