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Evolution of the Arthropod Mandible: a Molecular Developmental Perspective

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Evolution of the Arthropod Mandible: a Molecular Developmental Perspective Evolution of the Arthropod Mandible: a molecular developmental perspective Joshua Frederick Coulcher UCL Submitted for the Degree of Doctor of Philosophy September 2011 Declaration I, Joshua Frederick Coulcher, confirm that the work presented in this thesis is my own. Where information has been derived from other sources, I confirm that this has been indicated in the thesis. 2 Abstract The mandible is thought to have evolved once in the ancestor to the mandibulate arthropods; the insects, crustaceans and myriapods. If the mandible is a homologous structure, it suggests that there will be shared developmental genes required to pattern the mandible in different species. As a representative of mandibulate arthropods, the red flour beetle Tribolium castanem was chosen to study genes required to pattern the mandible. This study show that the Tribolium orthologue of cap’n’collar (Tc cnc) patterns the mandible of Tribolium. Loss of Tc cnc function by RNA interference (RNAi) results in a transformation of the mandible to maxillary identity and deletion of the labrum. Analysis of gene expression by in situ hybridisation shows that Tc cnc represses the Tribolium orthologues of the Hox genes proboscipedia (pb) and Deformed (Dfd), which pattern the maxillary appendage. Similar expression patterns of cnc, Dfd and pb homologues in mandibulate arthropods suggests that the functions of these genes are conserved. As the mandible has evolved from a maxilla-like precursor in the ancestor to all mandibulate arthropods, the manner in which Tc cnc differentiates the mandible from a maxilla in Tribolium recapitulates the evolution of the mandible from a maxilla-like precursor. An orthologue of cnc was cloned from the spider Achaearanaea tepidariorum, chosen as an outgroup to the mandibulate arthropods, but no evidence of a developmental role was discovered. Study of the expression of genetic markers for appendage segments shows that the biting edge of the mandible is derived from one endite, and the mandible is divided into a subcoxa and coxa which are also present in the maxillary, labial and leg appendages. There are significant similarities in the expression of genetic markers that presumably indicate serial homology of the subcoxa and coxa of the mandible to the subcoxa and coxa of other appendages. 3 Acknowledgements I would to thank my supervisor Max Telford for all the valuable help and guidance he has given me over the past few years. I would also like to thank Paola Oliveri for all her support she has given me during my PhD. I would like to thank several co-workers, both past and present, in the laboratory that I have been working in over the last four years. I am grateful to Bernhard Egger, Kate Rawlinson, Fraser Simpson, Omar Rota-Stabelli, Andrew Economou, Rob Lanfear for many interesting and lively discussions as well as helping me in the laboratory with my experiments. I would also like to thank Giovanna Vinti for all the help that she has given me during my time at UCL. Many thanks go to Nico Posnien, Andrew Peel and Meriem Takarli for both giving me invaluable advice and demonstrating experimental techniques in Tribolium. Many thanks also go to Nikola-Michael Prpic-Schäper, Alistair Mcgregor, Matthias Pechmann and Viktoria Linne for helping me learn how to maintain a healthy spider culture and also for all their advice on performing experiments on Achaearanea. I would also like to thank Gregor Bucher, Angelika Stollewerk, Michalis Averof and Linda Partridge for kindly inviting me into their laboratory in order to learn experimental techniques and also for allowing me to use their facilities. I am indebted to the Biotechnology and Biological Sciences Research Council (BBSRC) for providing the financial support necessary for me to perform the research which is presented in this thesis. I would like to thank my father, for without his support and encouragement this thesis would never have been possible. Finally, I would like to thank my partner Cécile for being supportive, helping out with my experiments and not least for putting up with my anti-social hermit-like existence for the substantial period of time it took to write this thesis. 4 Table of Contents Abstract ............................................................................................................................. 3 Acknowledgments .................................................................................................... 4 Table of contents ...................................................................................................... 5 List of figures..................................................................................................................... 7 List of tables ........................................................................................................... 11 Chapter 1: Introduction .......................................................................................... 12 1.1 General introduction ................................................................................... 12 1.2 Evolution of the biramous limb .................................................................. 16 1.3 Mandible diversity ...................................................................................... 21 1.4 Arthropod Phylogeny .................................................................................. 28 1.5 Arthropod Fossil Record in the Cambrian ................................................... 32 1.6 Serial homology of the mandible and maxilla ............................................. 37 1.7 Molecular development of the mandible .................................................. 46 1.8 Homology of anterior arthropod segments ................................................ 53 1.9 Mandibular segment patterning genes in Drosophila. ............................... 58 1.10 The red flour beetle Tribolium castaneum ................................................. 60 1.11 Introduction to results chapters ................................................................ 62 Chapter 2: Development of the embryonic mandibular endite in Tribolium ............. 65 2.1: Introduction .................................................................................................. 65 2.2: Results .......................................................................................................... 69 2.3: Discussion ..................................................................................................... 76 Chapter 3: Division of the Tribolium embryonic mandible into a subcoxa and coxa . 80 3.1: Introduction .................................................................................................. 80 3.2: Results .......................................................................................................... 85 3.3: Discussion ..................................................................................................... 99 Chapter 4: Tc cnc differentiates the mandible from a maxilla in Tribolium ............ 110 4.1: Introduction ................................................................................................ 110 4.2: Results ........................................................................................................ 117 4.3: Discussion ................................................................................................... 130 Chapter 5: The protopodite patterning role of Tc Dfd in the maxilla. ..................... 141 5.1: Introduction ................................................................................................ 141 5 5.2: Results ........................................................................................................ 146 5.3: Discussion ................................................................................................... 157 Chapter 6: Investigating the role of mandible patterning genes in non-mandibulate arthropods ........................................................................................................... 162 6.1: Introduction ................................................................................................ 162 6.2: Results ........................................................................................................ 168 6.3: Discussion ................................................................................................... 175 Chapter 7: Discussion ............................................................................................ 180 7.1: General overview of results ...................................................................... 180 7.2: The mandibular subcoxa ............................................................................ 185 7.3: Molecular development of the mandible .................................................. 191 7.4: The role of cnc in the ancestor to all mandibulates ................................... 197 7.5: General Conclusions ................................................................................... 204 Chapter 8: Materials and Methods ........................................................................ 208 8.1: Animal culture ............................................................................................ 208 8.2: Molecular biology techniques. ................................................................... 209 8.3: in situ hybridization protocols. ................................................................... 213 8.4: Microscopy ...............................................................................................
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