The evolution of head structures in Diptera and the phylogeny of the order Dissertation zur Erlangung des akademischen Grades „doctor rerum naturalium“ (Dr. rer. nat.) vorgelegt dem Rat der Biologisch-Pharmazeutischen Fakultät der Friedrich-Schiller-Universität Jena von Dipl. Biol. Katharina Schneeberg geboren am 30.08.1983 in Jena Gutachter: 1. Prof. Dr. Rolf G. Beutel (Friedrich-Schiller-Universität Jena) 2. Prof. Dr. Steffen Harzsch (Ernst Moritz Arndt Universität Greifswald) 3. PD Dr. Thomas Hörnschemeyer (Georg-August-Universität Göttingen) Datum der öffentlichen Verteidigung: 18.7.2014 Table of contents Table of contents 1. Introduction .......................................................................................................................................1 2. Material and techniques.................................................................................................................11 2.1 List of taxa examined ...........................................................................................................11 2.2 Morphological techniques ....................................................................................................14 2.3 Cladistic analyses.................................................................................................................15 3. Published results ............................................................................................................................16 3.1 Study I: Adult head structures of Deuterophlebiidae (Insecta), a highly derived “ancestral” dipteran lineage.................................................................................................17 3.2 Study II: The adult head morphology of the Hessian fly Mayetiola destructor (Diptera, Cecidomyiidae). ....................................................................................................18 3.3 Study III: The adult head morphology of Axymyia furcata (Axymyiidae, Diptera)...........19 3.4 Study IV: The morphology of the larval head of Tipulidae (Diptera, Insecta) – the dipteran groundplan and evolutionary trends.....................................................................20 3.5 Study V: The larvae of Nymphomyiidae (Diptera, Insecta) – ancestral und highly derived? .....................................................................................................................21 3.6 Study VI: The skeletomuscular system of the larva of Drosophila melanogaster (Drosophilidae, Diptera) – a contribution to the morphology of a model organism. ........22 3.7 Study VII: Reconstructing the evolution of Holometabola (Hexapoda) using SRμCT-based morphological data......................................................................................23 3.8 Phylogenetic results .............................................................................................................24 4. Phylogenetically relevant characters ............................................................................................26 5. Discussion.......................................................................................................................................58 5.1 Phylogeny .............................................................................................................................58 5.1.1 The phylogenetic potential of characters of the head of larvae and adults...........58 5.1.2 Phylogenetic implications of the examined characters ..........................................59 5.2 Character transformations ...................................................................................................64 5.2.1 Adult head .................................................................................................................64 5.2.2 Larval head................................................................................................................72 5.3 Conclusion ............................................................................................................................79 6. Summary.........................................................................................................................................81 7. Zusammenfassung.........................................................................................................................86 8. References......................................................................................................................................91 9. Appendix .......................................................................................................................................110 10. Lebenslauf.....................................................................................................................................133 11. Publikationen ................................................................................................................................134 12. Danksagung..................................................................................................................................136 13. Eigenständigkeitserklärung..........................................................................................................138 Introduction 1 Introduction With approximately 170 000 described species Diptera (true flies) are one of the extremely species- riches groups of Holometabola (Pape et al. 2011). Fossil dipterans are known since the Triassic (Krzemiski & Krzemiska 2003). Recent species occur worldwide, on all continents and in all zoogeographic regions (Alexander & Byers 1981). The number of individuals is often extremely high. Diptera are very versatile in their ecology and they also show a considerable variation in their anatomy, especially in their immature stages (Grimaldi & Engel 2005). Nevertheless, their monophyly has never been questioned (see Schneeberg & Beutel 2013). It is supported by the transformation of the hind wings into halteres (Hennig 1973) correlated with a strong enlargement of the mesothorax, which bears the functional wings, whereas the pro- and metathorax are distinctly reduced in size (Hennig 1973). The halteres are equipped with a numerous sensilla and serve as gyroscopic sense organs and stabilize the flight (Faust 1952; Pringle 1948). Another apomorphy of the group is the transformation of the two- segmented labial palps into labellae (Matsuda 1965; Hennig 1973). They are thickened and used to take up liquid food. Male dipterans bear a maximum of seven abdominal spiracles (Hennig 1973). The number of chromosomes is reduced (maximum n = 10, n = 3-6 in most dipteran groups) (Hennig 1973). The larvae of Diptera are legless and called maggots (Hennig 1973). Fig. 1: Proposed phylogenetic relationships among the antliophoran orders to: A, Hennig 1969, 1973, 1981 (morphological data); Kristensen 1999 (morphological data). B, Kristensen 1981, 1991, 1995 (morphological data); Beutel & Gorb 2001 (morphological data, attachment device); Sinclair et al. 2007 (morphological data, male genitalia); Wiegmann et al. 2009 (molecular data, nuclear genes); McKenna & Ferell 2010 (molecular data, nuclear genes); Ishiwata et al. 2011 (molecular data, nuclear genes). C, Beutel et al. 2011 (morphological data). D, Whiting & Wheeler 1994 (modified) (morphological data); Whiting et al. 1997 (modified) (molecular data, 18S and 28S rDNA); Wheeler et al. 2001 (morphological and molecular data, 18S and 28S rDNA); Whiting 2002a (modified) (molecular data, 18S rDNA). E, Grimaldi & Engel 2005 (morphological and paleontological data). F, Whiting 2002b (molecular data, nuclear genes, 18S and 28S rDNA). G, Friedrich & Beutel 2010a (morphological data, thorax). H, Beutel & Baum 2008 (morphological data, head morphology); Beutel et al. 2009 (morphological data, larva). I, Friedrich & Beutel 2010b (morphological data, thorax). J, Wood & Borkent 1989 (morphological data). 1 Introduction The morphology of Diptera is not well known and consequently the groundplan of the group is insufficiently established. This impedes interordinal comparisons and the understanding of the early evolution within the group. Diptera form a monophyletic unit Antliophora (= pump bearers) with Siphonaptera (fleas) and Mecoptera (scorpions flies and hanging flies) (Hinton 1958; Hennig 1969), but the phylogenetic relationships between these groups is still discussed controversially (Beutel & Baum 2008; Beutel et al. 2009; Wiegmann et al. 2009; Friedrich & Beutel 2010a; Beutel et al. 2011; Peters et al. 2014) (Fig. 1). Potential sistergroups of Diptera are Siphonaptera (Wood & Borkent 1989; Friedrich & Beutel 2010b; Beutel et al. 2011) (Figs. 1C, I, J), Mecoptera (Hennig 1969, 1973, 1981; Kristensen 1999) (Fig. 1A), Nannochoristidae (Beutel & Baum 2008; Beutel et al. 2009) (Fig. 1H) or a taxon comprising Mecoptera + Siphonaptera (Kristensen 1981, 1991, 1995; Beutel & Gorb 2001; Sinclair et al. 2007; Wiegmann et al. 2009; McKenna & Farrell 2010; Ishiwata et al. 2011) (Fig. 1B). While the monophyly of Siphonaptera is extremely well supported, the monophyly of Mecoptera was repeatedly questioned (Wood & Borkent 1989; Whiting 2002b; Grimaldi & Engel 2005; Beutel & Baum 2008; Friedrich & Beutel 2010a, b) (Figs. 1E-J). The “Halteria-hypothesis”, i.e. a sister group relationship between Diptera and Strepsiptera, which was mainly supported by 18S rDNA (Whiting et al. 1997; Whiting 1998; Wheeler et al. 2001; Whiting 2002a) (Fig. 1D), has been refuted in recent studies (Wiegmann et al. 2009; Friedrich & Beutel