Molecular phylogenetics and taxonomic issues in dragonfly systematics (Insecta: Odonata) Rasmus Hovm¨oller Department of Zoology Stockholm University 2006 Molecular phylogenetics and taxonomic issues in dragonfly systematics (Insecta: Odonata) Doctoral dissertation 2006 Rasmus Hovm¨oller Department of Entomology Swedish Museum of Natural History PO Box 500 07 SE 104 05 Stockholm Sweden [email protected] ISBN 91-7155-282-0 c 2006 Rasmus Hovm¨oller Typeset in Computer Modern with LATEX 2ε. Cover illustration by Andrea Klintbjer Sympetrum sanguineum (M¨uller, 1764) Printed by US-AB, Stockholm List of papers I: Hovm¨oller,, R., K¨allersj¨o,M. and Pape, T., 2004. The Palaeoptera problem: basal pterygote phylogeny inferred from 18S and 28S rDNA sequences. Cladistics 18, 313–323. II: Hovm¨oller, R. and Johansson, F., 2004. A phylogenetic perspec- tive on larval spine evolution in Leucorrhinia (Odonata: Libellulidae) based on ITS1, 5.8S and ITS2 rDNA sequences. Molecular Phyloge- netics and Evolution 30, 653–662. III: Hovm¨oller,, R. Monophyly of Ischnurinae (Odonata: Zygoptera, Coenagrionidae) established from COII and 16S sequences. Manuscript. IV: Hovm¨oller, R. A catalog of species group names in the genus Coenagrion Kirby, 1890 (Odonata: Coenagrionidae). Manuscript. V: Hovm¨oller, R. A proposal to conserve the name Calopteryx Leach, 1815 over Agrion Fabricius, 1775. Manuscript. i ii Contents 1 Clades and classification of the Odonata 1 1.1 Origin and monophyly of Odonata . 1 1.2 Classification and taxonomy - a historical review . 1 1.2.1 Pioneers of dragonfly systematics . 2 1.2.2 Cladistic morphological studies . 3 1.2.3 Molecular studies . 4 2 Life history 7 2.1 Larval stage . 7 2.2 Emergence . 8 2.3 Imago . 8 2.4 Mating system . 8 2.5 Mating rituals and species recognition . 9 2.6 Ovipositing . 10 2.7 Life on the wing . 11 3 Extant clades of Odonata 13 3.1 Zygoptera - damselflies . 13 3.1.1 Calopterygoidea . 13 3.1.2 “Lestinoidea” . 13 3.1.3 Coenagrionoidea . 14 3.1.4 Hemiphleboidea . 14 3.2 Epiprocta: Anisoptera + “Anisozygoptera” . 14 3.2.1 The paraphyletic Anisozygoptera . 15 3.3 Anisoptera . 15 3.3.1 “Aeshnoidea” . 16 3.3.2 Cordulegastroidea . 16 3.3.3 Libelluloidea . 17 4 Odonata – a key group in insect evolution 19 4.1 History of insect flight . 19 4.2 Paranota – a terrestrial origin? . 20 4.3 An aquatic origin? . 20 4.4 Palaeopterous and neopterous wings . 21 4.5 Folding wings – a key event in insect evolution . 21 4.6 Palaeoptera – monophyletic or not? . 21 4.6.1 The Metapterygota hypothesis . 21 4.6.2 The Opistoptera hypothesis . 22 4.6.3 A monophyletic Palaeoptera? . 22 5 Ribosomal sequences in phylogenetic systematics 25 5.1 Structure and function of the ribosome . 25 5.2 Establishing homology in molecular data . 26 5.3 Approaches to multiple sequence alignment . 26 5.3.1 Finding an optimal path . 26 5.4 Multiple sequence alignment . 27 5.4.1 Heuristic multiple alignment . 27 5.5 Optimization methods . 28 iii 5.5.1 Parsimony direct optimization – an example . 28 5.6 Secondary structure alignment . 29 6 A presentation of the articles 31 7 Sammanfattning p˚asvenska 37 7.1 Inledning . 37 7.2 Trollsl¨andors liv och naturhistoria . 37 7.2.1 Klassificering av trollsl¨andor – en historisk ¨oversikt . 37 7.3 En trollsl¨andas livscykel . 39 7.3.1 Larvstadiet . 39 7.3.2 F¨orvandlingen . 39 7.3.3 Imagon – den fullbildade sl¨andan . 39 7.3.4 Parningssystemet . 40 7.3.5 Parningsspel och artigenk¨anning . 40 7.3.6 Aggl¨ ¨aggning . 40 7.3.7 Flyg- och jaktbeteende . 40 7.4 De nu levande trollsl¨andornas diversitet . 41 7.4.1 Zygoptera . 41 7.4.2 Epiprocta . 41 7.4.3 Anisoptera - ¨akta trollsl¨andor . 42 7.5 En nyckelgrupp i insekternas evolution . 42 7.5.1 Vingutveckling p˚aland – paranotalhypotesen . 43 7.5.2 Vingutveckling i vatten – omformade g¨alar? . 43 7.6 Palaeoptera och Neoptera . 44 7.6.1 Ar¨ Palaeoptera en monofyletisk grupp? . 44 7.7 Ribosomala DNA-sekvenser i fylogenetisk systematik . 45 7.7.1 Ribosomers struktur och funktion . 45 7.8 Presentation av artiklarna . 47 8 Acknowledgments 51 iv Preface Dragonflies (Odonata) are one of the instantly recognizable groups of insects. The aerial acrobatics of the true dragonflies, the shimmering wings of the demoi- selles and perhaps even the tiny damselflies are a familiar sight to anyone who has spent an afternoon at a lakeside. Dragonflies are an ancient group of insects, and a key group in understanding the evolution of insects and insect flight. I have studied dragonflies from different phylogenetic perspectives – from the wide view of the systematic placement of dragonflies in the insects, to higher- level phylogeny in Coenagrionid damselflies and a close look at a small group of libellulids in the genus Leucorrhinia. For these papers, I have used molecular methods to obtain phylogenetic hypotheses. In addition to phylogentic stud- ies, I have examined the nomenclature of two groups of damselflies, first in a synonymic catalog of the genus Coenagrion and next in an examination of the history and taxonomic availabilty of the genus name Agrion. The first and second chapters of the introduction are about the natural his- tory of dragonflies and how their phylogeny and life-history evolution has been interpreted. This is followed by a presentation of the extant groups of dragon- flies on a super-familial level. The final historical chapter is a history of insect flight. Next, there is a section on ribosomal genes and different strategies for homologizing DNA data in phylogenetic systematics, and finally a presentation of the five articles included in this thesis. v vi Chapter 1 Clades and classification of the Odonata 1.1 Origin and monophyly of Odonata Dragonflies are one of the most ancient groups of insects alive today. The first known fossils of dragonfly-like insects are from the Upper Carboniferous and belong to the group Protodonata, the extinct sister group of modern Odonata. Included in Protodonata is the largest insect known to have existed: Mega- neuropsis permiana Carpenter, 1939. This species had a wingspan of over 70 cm. Most Protodonata are only known from wings, but a composite picture can be assembled from fragmented evidence (Grimaldi and Engel, 2005): an insect with some striking similarities to modern dragonflies bearing toothed mandibles, large compound eyes and legs angled forward. They were most cer- tainly predators. Although the larvae are unknown, the close relationship to extant dragonflies suggests that they could have been aquatic. True Odonata appeared in the early Permian era, represented by the extinct suborders Protanisoptera, Protozygoptera as well as the species Permagrion falklandicum Tillyard, 1928, which has been interpreted either as a modern zy- gopteran or a representative of the extinct suborder Archizygoptera (Trueman in Silsby, 2001). Modern dragonflies (Odonata sensu stricto) are a well-supported monophyletic group (e.g. Rehn, 2003; Trueman, 1996; Kristensen, 1975; Wheeler et al., 2001). They share several unique characters, most notably the secondary male genitalia and the prehensile labial mask of the larvae. 1.2 Classification and taxonomy - a historical re- view Figure 1.1: Scandinavian besman scale. Illustration from “Nordisk Familjebok” (1905). Dragonflies were originally classified in the genus Libellula within the order Neuroptera (Linnaeus, 1758). Libellula means “small weighing scale”, referring to a type of counterbalanced hanging scales. The linnaean Neuroptera contained all the insect orders with multiple crossveins in the wings: Odonata in Libel- lula; Ephemeroptera in Ephemera; Trichoptera in Phryganea; Plecoptera, Neu- 1 roptera sensu stricto, and Megaloptera in Hemerobius, Mecoptera in Panorpa and Rhaphidioptera in Rhaphidia. Fabricius (1775) divided the genus Libel- lula intro three: Libellula, Aeshna and Agrion. An even finer division of the European genera was suggested by Leach (1815), where such familiar taxa as Lestes, Calopteryx (as Calepteryx), Gomphus and Cordulegaster were described. Leach’s taxonomy was accepted and expanded upon by the francophone odona- tologists Rambur (1842) and de S´elys-Longchamps (e.g. 1850, 1872, 1876).The Belgian entomologist Baron Michel Edmond de S´elys-Longchamps, can be con- sidered the founder of modern odonatology. From 1840 to his death in 1900, he published monographs on every major group of Odonata except the Libel- lulidae. He described over 1000 species as well as erecting, as subfamilies, most of the groups now treated as families. Well into the 20th century Odonata were still usually treated as part of the Neuroptera sensu Linnaeus, although this was often considered an unnatural grouping. In contemporary literature, Odonata were sometimes referred to as Paraneuroptera, and grouped with the other hemimetabolous “Neuroptera” i.e. Ephemeroptera, Psocoptera and Ple- coptera in the Pseudoneuroptera. The classification changed when Martynov (e.g. 1925) reconsidered the group Subulicornes, proposed by Latreille (1807) for Neuroptera with tiny bristle-like antennae and aquatic larvae, under the name Palaeoptera. This was to be a controversial group, as will be explained below. 1.2.1 Pioneers of dragonfly systematics Coenagrionoidea Lestoidea Calopterygoidea Epiophlebia Figure 1.2: Munz (1919) phylogeny for Zygoptera The most notable pre-cladistic phylogenetic studies of the Odonata were performed by Needham (1903) on the entire group, and Zygoptera by Munz (1919). These were mostly based on patterns in the wing venation and the theory that “ontogeny recapitulates phylogeny” (Haeckel, 1866). In Odonata larvae, the growth of tracheae in the wing pads can be followed throughout the instars. The pattern of the growing tracheae follow the pattern of the main veins in the imago, but there are indications that the trachaetion as well as the venation rather follows lacunae in the epidermis that form well before either tracheae or veins migrate in (see Carpenter (1966), for a review).