The thorax musculature of Anisoptera (Insecta: Odonata) nymphs and its evolutionary relevance

BMC Evolutionary Biology

Thomas Hörnschemeyer¹  Sebastian Büsse¹ 

[1] Department of Morphology, Systematic & Evolutionary Biology, J-F-Blumenbach Institute for Zoology & Anthropology, Georg-August-University Göttingen, Göttingen, Germany

关键词: Homologization scheme;    Insect flight apparatus;    Musculature;    Odonata nymphs;    Homology with Neoptera (Insecta);    Dragonflies;   

Others  :  1085378
DOI  :  10.1186/1471-2148-13-237

 received in 2013-06-12, accepted in 2013-10-29,  发布年份 2013

【 摘 要 】

Background

Among the winged insects (Pterygota) the Odonata (dragon- and damselflies) are special for several reasons. They are strictly aerial predators showing remarkable flight abilities and their thorax morphology differs significantly from that of other Pterygota in terms of the arrangement and number of muscles. Even within one individual the musculature is significantly different between the nymphal and adult stage.

Results

Here we present a comparative morphological investigation of the thoracic musculature of dragonfly (Anisoptera) nymphs. We investigated representatives of the Libellulidae, Aeshnidae and Cordulegasteridae and found 71 muscles: 19 muscles in the prothorax, 26 in the mesothorax and 27 in the metathorax. Nine of these muscles were previously unknown in Odonata, and for seven muscles no homologous muscles could be identified in the neopteran thorax.

Conclusion

Our results support and extend the homology hypotheses for the thoracic musculatures of Odonata and Neoptera, thus supplementing our understanding of the evolution of Pterygota and providing additional characters for phylogenetic analyses comprising all subgroups of Pterygota.

【 授权许可】

   
2013 Büsse and Hörnschemeyer; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Asahina S: A morphological study of a relic dragonfly Epiophlebia superstes Selys (Odonata, Anisozygoptera). Japan society for the promotion of science: Tokyo; 1954.
• [2]Hatch G: Structure and mechanics of the dragonfly pterothorax. Ann Entomol Soc Am 1966, 50:702-714.
• [3]Pfau HK: Untersuchungen zur Konstruktion, Funktion und Evolution des Flugapparates der Libellen (Insecta, Odonata). Tijdschr Entomol 1986, 129:35-123.
• [4]Büsse S, Genet C, Hörnschemeyer T: Homologization of the flight musculature of Zygoptera (Insecta: Odonata) and Neoptera (Insecta). PLoS ONE 2013, 8(2):e55787. 10.1371/journal.pone.0055787
• [5]Corbet PS: Dragonflies: behavior and ecology of Odonata. New York: Cornell Univ Press; 1999.
• [6]Snodgrass RE: The dragonfly larva. Smithsonian Miscellaneous Collections 1954, 12(2):38pp.
• [7]Xylander WER, Günther KK: 7. Ordnung Odonata, Libellen. In Lehrbuch der speziellen zoologie, insecta. Edited by Dathe HH. Berlin: Spektrum Akademischer Verlag; 2005:167-172.
• [8]PoletaÏev N: Du développement des muscles d’ailes chez les odonates. Hor Soc Ent 1881, 16:1-10.
• [9]Maloeuf NSR: The postembryonic history of the somatic musculature of the dragonfly thorax. J. Morph. 1935, 58:87-115.
• [10]Whedon AD: Muscular reorganization in the Odonata during metamorphosis. Bio Bull 1929, 56(3):177-193.
• [11]Wittig G: Untersuchungen am Thorax von Perla abdominalis Burm. (Larve und Imago) unter besonderer Berücksichtigung des peripheren Nervensystems und der Sinnesorgane. Zool Jahrb 1955, 74:491-570.
• [12]Willkommen J, Hörnschemeyer T: The homology of wing base sclerites and flight muscles in Ephemeroptera and Neoptera and the morphology of the pterothorax of Habroleptoides confusa (Insecta: Ephemeroptera: Leptophlebiidae). Arthropod Struct Dev 2007, 36:253-269.
• [13]Bechly G: Morphologische Untersuchungen am Flügelgeäder der rezenten Libellen und deren Stammgruppenvertreter (Insecta; Pterygota; Odonnata) unter besonderer Berücksichtigung der Phylogenetischen Systematik und des Grundplanes der Odonata. Petalura 1996, 2:1-402. special volume
• [14]Lohmann H: Das phylogenetische System der Anisoptera (Odonata). Entomol Z 1996, 106:209-266.
• [15]Trueman JWH: A prelimnary cladistic analysis of Odonate wing venation. Odonatologica 1996, 25:59-72.
• [16]Misof B, Rickert AM, Buckley TR, Fleck G, Sauer KP: Phylogenetic signal and its decay in mitochondrial SSU and LSU rRNA gene fragments of Anisoptera. Mol Biol Evol 2001, 18:27-37.
• [17]Rehn AC: Phylogenetic analysis of higher-level relationships of Odonata. Syst Entomol 2003, 28:181-239.
• [18]Bybee SM, Ogden TH, Branham MA, Whiting MF: Molecules, morphology and fossils: a comprehensive approach to odonate phylogeny and the evolution of the odonate wing. Cladistics 2008, 23:1-38.
• [19]Gade G, Simek P, Fescemyer HW: Adipokinetic hormones provide inference for the phylogeny of Odonata. J Insect Physiol 2011, 57:174-178.
• [20]Dumont HJ, Vierstraete A, Vanfleteren JR: A molecular phylogeny of the Odonata (Insecta). Syst Entomol 2010, 35:6-18.
• [21]Clark HW: The adult musculature of the anisopterous dragonfly thorax (Odonata, Anisoptera). J Morph 1940, 67:523-565.
• [22]Ninomiya T, Yoshizawa K: A revised interpretation of the wing base structure in Odonata. Syst Entomol 2009, 34:334-345.
• [23]Grimaldi D, Engel MS: Evolution of the insects. Cambridge: University Press; 2005.
• [24]Snodgrass RE: The thorax of insect and the articulations of the wings. P USA Nat Mus 1909, 36:511-595.
• [25]Bauernfeind E: The mayflies of Greece – a provisional checklist. In Proceedings of the Xth international conference on ephemeroptera; Perugia Edited by Gaino E. 2003, 99-106.
• [26]Ogden TH, Whiting MF: The problem with “the Paleoptera problem:” sense and sensitivity. Cladistics 2003, 19:432-442.
• [27]Ishiwata K, Sasaki G, Ogawa J, Miyata T, Su Z-H: Phylogenetic relationships among insect orders based on three nuclear protein-coding gene sequences. Mol Phylogene Evol 2011, 58(2):169-180.
• [28]Blanke A, Wipfler B, Letsch H, Koch M, Beckmann F, Beutel R, Misof B: Revival of Palaeoptera—head characters support a monophyletic origin of Odonata and Ephemeroptera (insecta). Cladistic 2012, 2012:1-22. 10.1111/j.1096-0031.2012.00405.x
• [29]Blanke A, Greve C, Wipfler B, Beutel R, Holland BR, Misof B: The identification of concerted convergence in insect heads corroborates Palaeoptera. Syst Biol 2012, 1-14. 10.1093/sysbio/sys091
• [30]Martynov AV: Über zwei Grundtypen der Flügel bei den Insekten und ihre Evolution. Z Morpho Ökol Tiere 1925, 4:465-501.
• [31]Hennig W: Die Stammesgeschichte der Insekten. Frankfurt am Main: Waldemar Kramer; 1969.
• [32]Kukalová-Peck J: Origin and evolution of insect wings and their relation to metamorphosis, as documented by the fossil record. J Morph 1978, 156:53-126.
• [33]Kukalová-Peck J: Origin of insect wing and wing articulation from the insect leg. Can J Zool 1983, 61:1618-1669.
• [34]Kukalová-Peck J: Ephemeroid wing venation based upon new gigantic carboniferous mayflies and basic morphology, phylogeny, and metamorphosis of pterygote insects (Insecta, Ephemerida). Can J Zool 1985, 63:933-955.
• [35]Kukalová-Peck J: Fossil history and the evolution of hexapod structures. In The insects of Australia. Edited by CSIRO. Melbourne: Melbourne University Press; 1991:141-179.
• [36]Kukalová-Peck J: Phylogeny of higher taxa in Insecta: finding synapomorphies in the extant fauna and separating them from homoplasies. Evol Biol 2008, 35:4-51.
• [37]Wootton JR: Function, homology and terminology in insect wings. Syst Entomol 1979, 4:81-93.
• [38]Haas F, Kukalová-Peck J: Dermaptera hindwing structure and folding: new evidence for familial, ordinal and superordinal relationships within Neoptera (Insecta). Eur J Entomol. 2001, 98:445-509.
• [39]Rasnitsyn AP: Subclass scarabaeona laicharting, 1781. The winged insects (= pterygota Lang, 1888). In History of insects. Edited by Rasnitsyn AP, Quicke DLJ. Dordrecht: Kluwer Academic Publishers; 2002:75-82.
• [40]Hovmöller R, Pape T, Källersjö M: The Palaeoptera problem: basal pterygote phylogeny inferred from 18S and 28S rDNA sequences. Cladistics 2002, 18:313-323.
• [41]Thomas JA, Trueman JWH, Rambaut A, Welch JJ: Relaxed phylogenetics and the Palaeoptera problem: resolving deep ancestral splits in the insect phylogeny. Syst Biol 2013, 62(2):285-297.
• [42]Börner C: Neue Homologien zwischen Crustaceen und Hexapoden: die Beißmandibel der Insekten und ihre phylogenetische Bedeutung: Archi- und Metapterygota. Zool Anz 1909, 34:100-125.
• [43]Hennig W: Kritische Bemerkungen zum phylogenetischen System der Insekten. Beitr Entom 1953, 3:1-85.
• [44]Kristensen NP: The phylogeny of hexapod “orders”: a critical review of recent accounts. J Zoolog Syst Evol Res 1975, 13:1-44.
• [45]Kristensen NP: Phylogeny of insect orders. Annu Rev Entomol 1981, 26:135-157.
• [46]Staniczek AH: The mandible of silverfish (Insecta: Zygentoma) and mayflies (Ephemeroptera): its morphology and phylogenetic significance. Zool Anz 2000, 239:147-178.
• [47]Staniczek AH: Der Larvenkopf von Oniscigaster wakefieldi McLachlan, 1873 (Insecta: Ephemeroptera: Oniscigastridae). Tübingen, Germany: Ph.D. thesis, University of Tübingen; 2001.
• [48]Wheeler WC, Whiting MA, Wheeler QD, Carpenter JM: The phylogeny of the extant hexapod orders. Cladistics 2001, 17:113-169.
• [49]Willmann R: Die phylogenetischen Beziehungen der Insecta: offene Fragen und Probleme. Düsseldorf, Germany: Löbbecke-Museum und Aquazoo; 2003:1-64. [Verhandlungen Westdeutscher Entomologentag]
• [50]Beutel R, Gorb S: A revised interpretation of the evolution of attachment structures in hexapoda with special emphasis on Mantophasmatodea. Arthro Syst Phyl 2006, 64:3-25.
• [51]Simmons M: Independence of alignment and tree search. Mol Phylogenet Evol 2004, 31:874-879.
• [52]Morgan MJ, Kelchner SA: Inference of molecular homology and sequence alignment by direct optimization. Mol Phylogenet Evol 2010, 56:305-311.
• [53]Yoshizawa K, Johnson KP: Aligned 18S for Zoraptera (Insecta): phylogenetic position and molecular evolution. Mol Phylogenet Evol 2005, 37:572-580.
• [54]Boudreaux HB: Arthropod phylogeny with special reference to insects. New York: Wiley; 1979.
• [55]Carle FL: The wing vein homologies and phylogeny of the Odonata: a continuing debate. Soc Int Odonatol Rapid Comm 1982, 4:66.
• [56]Carle FL: Evolution of the odonate copulatory process. Odonatologica 1982, 11:271-286.
• [57]Kjer KM: Aligned 18S and insect phylogeny. Syst Biol 2004, 53:506-514.
• [58]Yoshizawa K: Direct optimization overly optimizes data. Syst Entomol 2010, 35:199-206.
• [59]Kingsolver J, Koehl M: Selective factors in the evolution of insect wings. Ann Rev Entomol 1994, 39:425-451.
• [60]Hörnschemeyer T: Phylogenetic significance of the wing-base of the Holometabola (Insecta). Zool Scr 2002, 31:17-29.
• [61]Willkommen J: The morphology of the pterothorax of Ephemeroptera, Odonata and Plecoptera (Insecta) and the homology of wing base sklerites and flight muscles. Stutt Beit Naturk n ser A 2008, 1:203-300.
• [62]Friedrich F, Beutel R: The thorax of Zorotypus (hexapoda, zoraptera) and a new nomenclature for the musculature of Neoptera. Arthropod Struc Dev 2008, 37:29-54.
• [63]Yoshizawa K, Ninomiya T: Homology of the wing base sclerites in Ephemeroptera (Insecta: Pterygota) – a reply to Willkommen and Hörnschemeyer. Arthropod Struct Dev 2007, 36:277-279.
• [64]Rüppell G, Hilfert D: The flight of the relict dragonfly Epiophlebia superstes (Selys) in comparison with that of the modern Odonata (Anisozygoptera: Epiophelebiidae). Odonatologica 1993, 22:295-309.
• [65]Blanke A, Beckmann F, Misof B: The head anatomy of Epiophlebia superstes (Odonata: Epiophlebiidae). Org Divers Evol 2013, 13(1):55-66. 10.1007/s13127-012-0097-z
• [66]Snodgrass RE: Principles of insect morphologie. New York: Mc Graw-Hill Book Company; 1935.
• [67]Matsuda R: Morphology and evolution of the insect thorax. The Entomological Society of Canada: Ottawa; 1970.
• [68]Bocharova-Messner OM: Flügelentwicklung in frühen postembyonalen Stadien der Entwicklung von Libellen (ordnung ODONATA). UdSSR: Labor für Morphologie Wirbelloser des Institutes für Tiermorphologie “A. N. Severtsov” der Akademie der Wissenschaften; 1959.
• [69]Kéler SV: Entomologisches Wörterbuch. Berlin: Akademieverlag Berlin; 1963.
• [70]Rieppel O: Semaphoronts, cladograms and the roots of total evidence. Biol J Linn Soc 2003, 80:167-186.
• [71]Rieppel O: Popper and systematics. Syst Biol 2003, 2:259-271.
• [72]Rieppel O: The nature of parsimony and instrumentalism in systematics. J Zool Evol Res 2007, 45:177-183.
• [73]Barlet J: Morphologie du thorax de Lepisma saccharina L. (Apterygote Thysanoure): II. musculature 1. Bull Ann Soc Entomol Belg 1953, 89:214-236.
• [74]Barlet J: Morphologie du thorax de Lepisma saccharina L. (Aptérygote thysanoure): II. musculature 2. Bull Ann Soc Entomol Belg 1954, 90:299-321.
• [75]Barlet J: Squelette et musculature thoraci ques de Lepismachilis y-signata kratochvil (Thysanoures). Bull Ann Soc Entomol Belg 1967, 103:110-157.
• [76]Romeis B: Mikroskopische Technik. Urban und Schwarzenberg: München; 1987.
• [77]Betz O, Wegst U, Weide D, Heethoff M, Helfen L, Lee W-K, Cloetens P: Imaging applications of synchrotron X-ray phase-contrast microtomography in biological morphology and biomaterials science: I. general aspects of the technique and ist advantages in the analysis of millimetre-sized arthropod structure. J Micros 2007, 227:51-71.