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Lissamphibia: Anura) Ecomorphology, biomechanics and ontogeny of the pectoral girdle in anurans (Lissamphibia: Anura) with emphasis on morphological methods Dissertation with the aim of achieving a doctoral degree at the Faculty of Mathematics, Informatics and Natural Sciences Department of Biology University of Hamburg submitted by Karolin Engelkes Hamburg 2020 Head of examination commission: Prof. Dr. Susanne Dobler, Universität Hamburg Dissertation reviewers: Prof. Dr. Alexander Haas, Universität Hamburg Prof. Dr. Andreas Schmidt-Rhaesa, Universität Hamburg Prof. Dr. John A. Nyakatura, Humboldt Universität zu Berlin Date of oral defense: 19.03.2021 Contents Abstract ...................................................................................................................................... 5 Zusammenfassung ...................................................................................................................... 7 Chapter one: General introduction ............................................................................................. 9 Chapter two: Measurement error in µCT-based three-dimensional geometric morphometrics introduced by surface generation and landmark data acquisition .......... 27 Chapter three: Accuracy of bone segmentation and surface generation strategies analyzed by using synthetic CT volumes ...................................................................... 67 Chapter four: Ecomorphology of the pectoral girdle in anurans (Amphibia, Anura): shape diversity and biomechanical considerations ......................................................... 99 Chapter five: A simple setup for episcopic microtomy and a digital image processing workflow to acquire high-quality volume data and 3D surface models of small vertebrates ..................................................................................................................... 139 Chapter six: Ontogenetic development of the shoulder joint muscles in frogs (Amphibia: Anura) assessed by digital dissection with implications for interspecific muscle homologies and nomenclature ...................................................................................... 167 Chapter seven: General discussion ......................................................................................... 207 Danksagung ............................................................................................................................ 227 Eidesstattliche Versicherung .................................................................................................. 229 Supporting Information .......................................................................................................... 231 3 Abstract Abstract Frogs and toads (Amphibia: Anura) inhabit a wide range of habitats that are each associated with specific modes of locomotion. Despite the generally conserved anuran Bauplan, various anatomical adaptations to locomotor behaviors have been reported in previous studies. Most of these studies, however, focused on the limbs or the pelvic girdle. The pectoral girdle, that is the anatomical complex that connects the forelimbs to the axial skeleton, has rarely been analyzed with regard to its adaptation to and function in locomotion. Various previous studies on the anatomy and evolution of the pectoral girdle skeleton provide a base for ecomorphological and functional analyses of the skeletal girdle elements. The inclusion of the pectoral girdle muscles in such studies is complicated by inconsistencies in the identification and naming of the shoulder joint muscles in literature accounts. Therefore, the aims of this thesis were twofold: The first aim was to analyze the relationships between locomotor mode, skeletal shape variation, and biomechanical function of the anuran pectoral girdle. The second aim was to assess the ontogenetic development and innervation of the shoulder joint muscles in order to resolve the inconsistencies in literature accounts and to thereby provide a base for future studies that could include those muscles in biomechanical analyses or reconstruct muscle evolution. The first aim was approached by assessing whether geometric morphometrics was a valid method to analyze the shape of the anuran pectoral girdle and by optimizing the corresponding workflow. As geometric morphometrics proved to be a suitable approach, it was used to study the shape diversity in the pectoral girdle bones in relation to locomotor behavior within a phylogenetic framework. The analyses were complemented by musculo- skeletal modelling and finite element analyses in order to understand the biomechanical implications of shape differences in the context of locomotion. Digital dissections of volumes that were generated by histological serial sectioning, episcopic microtomy, or micro- computed tomography of larval and adult specimens were performed to approach the second aim. Phylogenetic relationships, size, and locomotor behavior had an effect on the shape of the pectoral girdle in anurans, but the relative impact of these factors varied between bones. Remarkable shape diversity was observed within locomotor groups which indicates many-to- one mapping of form onto function. The girdle shapes of burrowing and non-burrowing 5 Abstract species, and headfirst and backward burrowing species significantly differed from one another. The moment arms of (simulated) humerus retractor muscles crossing the shoulder joint were enlarged in burrowing species by specific pectoral girdle geometries. This potential adaptation to burrowing behavior was achieved by different, species-specific mechanisms. Differences in the pectoral girdle shapes were associated with differences in the reaction of the coracoid to simulated loading by physiologically relevant forces. The anuran shoulder joint muscles were ontogenetically derived from the ventral and the dorsal pre-muscle mass that can be found in all vertebrates. The commonly used names ‘m. coraco-brachialis longus’ and ‘m. deltoideus’ were found to be misleading with regard to the ontogenetic origin of the corresponding muscle units. The mm. scapulohumeralis profundus anterior and posterior, although present in all examined species, have been overlooked in some studies. If present, the portions of the mm. cleidohumeralis, supracoracoideus, and coracobrachialis have occasionally been incorrectly recognized or assigned in previous studies. All other shoulder joint muscles have correctly been identified and named in previous studies. A nomenclature consistent with regard to inter-specific homologies and the ontogenetic origin of muscle units was suggested. Shape variations in the skeletal elements of the pectoral girdle and also of the forelimbs provide the base for various, potentially adaptive configurations of the shoulder joint muscles. 6 Zusammenfassung Zusammenfassung Frösche und Kröten (Amphibia: Anura) leben in vielen verschiedenen Habitaten, in denen sie jeweils spezifische Fortbewegungsweisen verwenden. Trotz des weitestgehend konservierten Bauplans der Anuren haben frühere Studien verschiedene anatomische Anpassungen an die Fortbewegungsweisen gefunden. Die meisten dieser Studien haben sich jedoch auf die Beine und den Beckengürtel konzentriert. Mögliche Anpassungen des Schultergürtel, also des anatomischen Komplexes, der die Vorderbeine mit dem Achsenskelett verbindet, wurden bisher kaum untersucht. Frühere Studien zur Anatomie und Evolution des Schultergürtelskeletts bieten eine Grundlage für weiterführende ökomorphologische und funktionelle Analysen des Skeletts. Die Einbeziehung der Schultergürtelmuskeln in solche Analysen wird jedoch durch die inkonsistente Identifizierung und Benennung der einzelnen Muskeleinheiten in der Literatur erschwert. Darum werden mit dieser Arbeit zwei Ziele verfolgt: Zunächst sollen die Beziehungen zwischen Fortbewegungsweise, Form und Funktion des Schultergürtels der Anuren analysiert werden. Das zweite Ziel besteht darin, die ontogenetische Entwicklung und Innervierung der Muskeln des Schultergelenks zu klären und mit diesen Erkenntnissen die Inkonsistenzen in der Literatur aufzulösen, um damit eine Basis für mögliche zukünftige Studien, die die Schultergürtelmuskulatur in biomechanische Analysen einbeziehen oder die Muskelevolution rekonstruieren könnten, zu schaffen. Um das erste Ziel zu erreichen, wurde zunächst untersucht, ob die Geometrische Morphometrie eine valide Methode ist, um die Form des Schultergürtels der Anuren zu untersuchen, und der Workflow wurde für diesen speziellen Fall optimiert. Da sich die Geometrische Morphometrie als geeignete Methode herausgestellt hat, wurde mit ihrer Hilfe die Formvarianz der Knochen des Schultergürtels im Kontext von Lokomotion und Phylogenie untersucht. Die Untersuchungen wurden durch Muskel-Skelett-Modellierungen und Finite Elemente Analysen ergänzt, um die biomechanischen Auswirkungen von Formunterschieden zu verstehen. Digitale Präparationen von Volumendaten, die durch histologische Serienschnitte, episkopische Mikrotomie und Mikro-Computer Tomographie gewonnen wurde, wurden an larvalen und adulten Individuen durchgeführt, um das zweite Ziel zu erreichen. Phylogenetische Verwandtschaft, Größe und Fortbewegungsweise hatten einen signifikanten Effekt auf die Form des Schultergürtels der Anuren; die Stärke des Einflusses 7 Zusammenfassung dieser Faktoren unterschied sich jedoch zwischen den einzelnen Knochen. Eine bemerkenswerte Formenvielfalt wurde innerhalb der Lokomotionsgruppen beobachtet, was many-to-one mapping der Form
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