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The Thorax of Odonata (Insecta) - Including Remarks on Evolution and Phylogeny

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The Thorax of Odonata (Insecta) - Including Remarks on Evolution and Phylogeny The Thorax of Odonata (Insecta) - including remarks on evolution and phylogeny Dissertation zur Erlangung des mathematisch-naturwissenschaftlichen Doktorgrades „Doctor rerum naturalium“ der Georg-August-Universität Göttingen im Promotionsprogramm Biologie der Georg-August-University School of Science (GAUSS) vorgelegt von Sebastian Büsse aus Hildesheim Göttingen, 2013 Gutachter Betreuungsausschuss PD Dr. Thomas Hörnschemeyer JFB Institut für Zoologie & Anthropologie, Abteilung Morphologie, Systematik und Evolutionsbiologie, Georg-August-Universität Göttingen Prof. Dr. Rainer Willmann JFB Institut für Zoologie & Anthropologie, Abteilung Morphologie, Systematik und Evolutionsbiologie, Georg-August-Universität Göttingen Mitglieder der Prüfungskommission Referent: PD Dr. Thomas Hörnschemeyer JFB Institut für Zoologie & Anthropologie, Abteilung Morphologie, Systematik und Evolutionsbiologie, Georg-August-Universität Göttingen Korreferent: Prof. Dr. Rainer Willmann JFB Institut für Zoologie & Anthropologie, Abteilung Morphologie, Systematik und Evolutionsbiologie, Georg-August-Universität Göttingen Weitere Mitglieder der Prüfungskommission: 3: Prof. Dr. Elvira Hörandl, AvH Institut für Pflanzenwissenschaften, Abteilung Systematische Botanik, Georg-August-Universität Göttingen. 4: PD Dr. Mark Maraun, JFB Institut für Zoologie & Anthropologie, Abteilung Tierökologie, Georg-August-Universität Göttingen. 5: PD Dr. Alexander Schmidt, Courant Forschungszentrum Geobiologie, Nachwuchsgruppe „Evolution der Landpflanzen & Entwicklung der terrestrischen Ökosysteme“, Georg-August- Universität Göttingen. 6: Jun. Prof. Dr. Gregor Bucher, JFB Institut für Zoologie & Anthropologie, Abteilung Entwicklungsbiologie (GZMB), Georg-August-Universität Göttingen. Tag der mündlichen Prüfung: 14. August 2013 In Strichen, wo auf trocknem Land Man Jungfraun nur noch selten fand Sind Wasserjungfern, Demoisellen, Libellen häufig festzustellen. So kann der Mensch sich manchmal irren, Sie scheinen reizend, wenn sie schwirren Am Ufer hin, in Schilf und Gräsern Mit ihren Flügeln, schön und gläsern. Doch hat es jedem noch gegraut, Der ihnen ins Gesicht geschaut: Glotzaugen, bös, voll Mordverlangen Und Kiefer, scharf wie Eisenzangen! Eugen Roth Table of Contents iv Table of Contents Gutachter i Table of Contents iv 1. General Introduction 1‘11 1.1. Insecta 1 1.2. Odonata 2 1.3. Thorax Morphology 4 1.4. Phylogeny of Odonata 5 1.5. Aims of the Present Study 11 2. Phylogeographic Analysis Elucidates the Influence of the Ice Ages on 12‘37 the Disjunct Distribution of Relict Dragonflies in Asia 2.1. Contribution to this Publication 12 2.2. Publication (Büsse et al. 2012, PLoS one) 13 3. Homologization of the Flight Musculature of Zygoptera (Insecta: Odonata) 38‘58 and Neoptera (Insecta) 3.1. Contribution to this Publication 38 3.2. Publication (Büsse et al. 2013, PLoS one) 39 4. Analysis System for Taxonomic Identification of Insecta Species 59‘75 Applicable to Strongly Degraded DNA Using the Nuclear 28S-rRNA Gene 4.1. Contribution to this Manuscript 59 4.2. Manuscript (Grumpkow et al submitted, 60 Systematic & Biodiversity) 5. The Thorax Morphology of Zygoptera (Insecta: Odonata) – The Skeletal 75‘97 System 5.1. Contribution to this Manuscript 76 5.2. Manuscript (Genet et al. submitted, 77 Arthropod Structure & Development) 6. The Nymphal Thorax Musculature of Anisoptera (Insecta: Odonata) and Its 98‘143 Evolutionary Relevance 6.1. Contribution to this Manuscript 98 6.2. Manuscript (Büsse & Hörnschemeyer submitted, 99 BMC Evolutionary Biology) 7. A Taxonomic Review of Epiophlebia laidlawi (Insecta: Odonata) – Including 145‘156 Remarks on Phylogeny 7.1. Contribution to this Manuscript 145 7.2. Manuscript (Büsse in preparation) 146 Table of Contents v 8. Final Discussion and Conclusions 157‘171 8.1. Epiophlebia 157 8.1.1. Molecular and Phylogeographic Analysis of Epiophlebia 157 8.1.2. Morphology of Epiophlebia laidlawi 159 8.2. Universal Analysis System for Taxonomic Identification 160 8.3. The Flight Apparatus of Odonata and Homologies with 162 Neoptera 8.3.1. Wing Base Structures 163 8.3.2. Thorax Musculature 164 8.3.3. Generalized Odonata Thorax and the Ground Pattern 166 of Pterygote Insects 8.4. Concluding Remarks 170 Bibliography 173 Summary 187 Zusammenfassung 189 Erklärung 191 Danksagung 192 Supplement 193‘211 Table 1: Attachment Points Generalized Odonata thorax 190 Table 2 : Comparatative Table Thorax Musculature 202 Digital Version of Dissertation: S Büsse 2013 210 Bestätigung der Übereinstimmung 211 1. General Introduction 1 1. General Introduction 1.1. Insecta Insects are by far the richest in species and show an extraordinary variety of forms among living organisms (Figure 1). There are at least one million recent species described and this number increases annually by about 3000 species (Xylander & Günther 2003, Grimaldi & Engel 2005); estimates indicate the planet harbours 10 to 90 million insect species (Groombridge 1992, Wilson 1995). Many insects live together in enormous swarms and communities, e.g. locusts Figure 1 - The diversity of life shown as proportions of named species (Grimaldi & Engel 2005). that occur in swarms ranging in size from 0.7 million to two million individuals (Groll & Günther 2003) or social hymenoptera, the colonies of which can grow to as many as 20 million individuals. The colony of the honeybee (Apis mellifera Linnaeus, 1758) can be made up of as many as 40 thousand to 100 thousand individuals (Dathe 2003a). There are therefore an estimated 10 sextillion (1021) insect specimens currently living on Earth. That implies that there are around two billion insect individuals per human being (Dathe 2003b). Insects are indisputably the most successful group of organisms alive. They are able to adapt to nearly all conceivable living conditions and habitats. Insects remained among the first life forms to conquer land for approximately 400 million years (MY). They may have arisen about 420 million years ago (MYA) in the Late Silurian. At this time, only a few other terrestrial organisms had colonized our world, with the most likely of them being other arthropods as well as plant species (Grimaldi & Engel 2005). In the case of insects, the key to their success and dispersability was the emergence of wings. Insects developed wings at least 90 MY earlier than vertebrates (Engel & Grimaldi 2004) and are the only invertebrates that have wings (Grimaldi & Engel 2005). Recently, the allegedly oldest pterygote insect, † Strudiella devonica (Garrouste, 2012), was discovered and interpreted as a winged devonian insect nymph (Garrouste et al. 2012). However, Hörnschemeyer et al. (2013) disproved this study and showed that † S. devonica was only a poorly preserved Devonian arthropod. The oldest known accepted winged fossil is † Delitzschala bitterfeldensis Brauckmann & Schneider, 1996. 1. General Introduction 2 Figure 2 - Two of the oldest known pterygote insects. A † Delitzschala bitterfeldensis B † Brodioptera strick- lani. (After Bruckmann & Schneider 1996 and Nelson & Tidwell 1988). Dating back to the Lower Carboniferous, or approximately 320 MYA, it was found in Germany (Figure 2; Willmann 2003). Wings nevertheless remain the key to insect evolution and success. They are an indispensable character system that was ‘perfected’ in the Odonata. 1.2. Odonata Odonata are one of the oldest members of this most diverse group of living organisms. This insect group (Figure 3), which includes 5500 recent and approximately 600 fossil species, is distributed worldwide with exception of the circumpolar regions. The greatest diversity is found in the Oriental Region with 1000 species, followed by the Neotropic and Ethiopic ecozones. There are 114 known species for Europe, with 80 Figure 3 - The diversity of recent Insecta as propor- known to be found in Central tions of named species (Grimaldi & Engel 2005). Europe (Xylander & Günther 2003, Grimaldi & Engel 2005). Dragonflies and damselflies are undeniably one of the key arthropod predators. This applies to both nymphs, who live under the water surface and are able to hunt even for vertebrates like small fishes, and adults, which are skilled avian predators (e.g. Corbet 1999). Their wing pairs can be controlled independently and some species are able to even fly backwards (Hatch 1966). The variation between nymph and adult Odonata habitat – nymphs live under water and adults are terrestrial – bears comparison with 1. General Introduction 3 the Holometabola (e.g. Corbet 1999). Nymph and adult hemimetabolous insects generally share a common habitat (e.g. Deckert & Göllner-Scheiding 2003). This superordinate position, a major role in the invertebrate food web, and adaption to totally different habitats of nymphs and adults, as mentioned above, are reflected in a unique morphology. The basic pattern morphology is comparably uniform (Figure 4); some of the most important characters of Odonata are: Adults: • Four long, uniform wings with distal pterostigma and highly derived wing venation. • The prothorax is small and extremely versatile. The mesothorax and metathorax form a functional unit known as the pterothorax or synthorax, which is tilted caudally at 45° in Odonata. • The pleurites are rather enlarged in a dorso-ventral direction, whereas the tergites and sternites are unusually small compared to other pterygotes. • Direct muscle attachment is the mechanism for moving the wing. The dorsal longitudinal thorax musculature is reduced. • Spined legs thrust forward for catching prey. • The abdomen is slender, and can approaches
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