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Old method not old-fashioned: parallelism between wing venation and wing-pad tracheation of cockroaches and a revision of terminology

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Abstract

The Comstock–Needham system, the foundation of main vein homology of insects, is grounded in the comparison between wing venation and wing-pad tracheation, particularly that of Plecoptera and Blattodea. However, the trachea-based approach has come into great dispute in recent years. Meanwhile, the terminology used to describe the wing venation of cockroaches requires a revision according to homology and the practical need. These motivated us to examine the wings of cockroaches, comparing the tracheation of nymphs with the tracheation and venation of adults. We find a correspondence between the tracheation and the main vein venation; therefore the trachea-based approach is effective in cockroaches. It is supported that Neopteran insects have six homologous main veins, namely, Sc, R, M, Cu, Pcu and V. We interpret the wing morphology of cockroaches in detail, including veins, furrows, folds and apical folding. RA and RP in hindwing, ScP, CuA and CuP in tegmen and hindwing, are recognized. Hindwing R + M is the only normal venal fusion in cockroaches. In addition, we propose several descriptive terms: cmv, V[1], V[s], pseudostem and characteristic posterior branch. The venation of 41 species (representing 41 genera), and the wing-pad tracheation of four of them including Diploptera punctata, which has unique apical folding, are illustrated.

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References

  • Anisyutkin LN (2015) New and little known Epilamprinae (Dictyoptera: Blaberidae) from the collections of the Muséum d’histoire naturelle de Genève and the Zoological Institute of Saint Petersburg. Part l. Rev Suisse Zool 122:283–296

    Google Scholar 

  • Beccaloni G, Eggleton P (2013) Order Blattodea. In: Zhang ZQ (ed) Animal biodiversity: an outline of higher-level classification and survey of taxonomic richness (Addenda 2013). Zootaxa 3703:1–82, 46–48

  • Béthoux O (2005) Wing venation pattern of Plecoptera (Insecta: Neoptera). Illiesia 1:52–81

    Google Scholar 

  • Béthoux O, Wieland F (2009) Evidence for Carboniferous origin of the order Mantodea (Insecta: Dictyoptera) gained from forewing morphology. Zool J Linn Soc 156:79–113

    Article  Google Scholar 

  • Béthoux O, Schneider JW, Klass K-D (2011) Redesciption of the holotype of Phyloblatta gaudryi (Agnus, 1903) (Pennsylvanian; Commentry, France), an exceptionally well-preserved stem-dictyopteran. Geodiversitas 33:625–635

    Article  Google Scholar 

  • Bourgoin T, Wang R-R, Asche M, Hoch H, Soulier-Perkins A et al (2015) From micropterism to hyperpterism: recognition strategy and standardized homology-driven terminology of the forewing venation patterns in planthoppers (Hemiptera: Fulgoromorpha). Zoomorphology 134:63–77

    Article  Google Scholar 

  • Brannoch SK, Wieland F, Rivera J, Klass K-D, Béthoux O, Svenson GJ (2017) Manual of praying mantis morphology, nomenclature, and practices (Insecta, Mantodea). ZooKeys 696:1–100

    Article  Google Scholar 

  • Breitkreuz LCV, Winterton SL, Engel ES (2017) Wing tracheation in Chrysopidae and other Neuropterida (Insecta): a resolution of the confusion about vein fusion. Am Mus Novit 3890:1–44

    Article  Google Scholar 

  • Bruijning CFA (1947) An account of the Blattidae (Orthoptera) from Celebes, the Moluccas, and New Guinea. Zoologische Mededeelingen 27:205–252

    Google Scholar 

  • Bruijning CFA (1948) Studies of Malayan Blattidae. Zoologische Mededeelingen 29:1–174

    Google Scholar 

  • Brunner von Wattenwyl C (1865) Nouveau Système des Blattaires. G. Braumüller, Vienna

    Google Scholar 

  • Comstock JH (1918) The Wings of Insects. The Comstock Publishing Company, Ithaca

    Google Scholar 

  • Comstock JH, Needham JG (1898) The wings of insects. Am Nat 32:43–48 (81–89, 231–257, 335–340, 413–424, 561–565, 769–777, 903–911)

    Article  Google Scholar 

  • Comstock JH, Needham JG (1899) The wings of insects. Am Nat 33:117–126 (845–860)

    Article  Google Scholar 

  • Djernæs M, Klass K-D, Picker MD, Damgaard J (2011) Phylogeny of cockroaches (Insecta, Dictyoptera, Blattodea), with placement of aberrant taxa and exploration of out-group sampling. Syst Entomol 37:65–83

    Article  Google Scholar 

  • Djernæs M, Klass K-D, Eggleton P (2015) Identifying possible sister groups of Cryptocercidae + Isoptera: a combined molecular and morphological phylogeny of Dictyoptera. Mol Phylogenet Evol 84:284–303

    Article  Google Scholar 

  • Evangelista DA, Djernæs M, Kohli MK (2017) Fossil calibrations for the cockroach phylogeny (Insecta, Dictyoptera, Blattodea), comments on the use of wings for their identification, and a redescription of the oldest Blaberidae. Palaeontol Electron 20:1FC(1–23)

    Google Scholar 

  • Fennah RG (1944) The morphology of the tegmina and wings in Fulgoroidea (Homoptera). Proc Entomol Soc Wash 46:185–199

    Google Scholar 

  • Forbes WTM (1933) The axillary venation of the insects. V Int Congr Entomol 1932:277–284

    Google Scholar 

  • Forbes WTM (1943) The origin of wings and venational types in insects. Am Midl Nat 29:381–405

    Article  Google Scholar 

  • Fristrom D, Wilcox M, Fristrom J (1993) The distribution of PS integrins, laminin A and F-actin during key stages in Drosophila wing development. Development 117:509–523

    CAS  PubMed  Google Scholar 

  • Fristrom D, Gotwals P, Eaton S, Kornberg TB, Sturtevant M, Bier E, Fristrom JW (1994) blistered: a gene required for vein/intervein formation in wings of Drosophila. Development 120:2661–2671

    CAS  PubMed  Google Scholar 

  • Gillott C (2005) Entomology, 3rd edn. Springer, Dordrecht

    Google Scholar 

  • Grandcolas P, Deharveng L (2007) Miroblatta baai, a new very large cockroach species from caves of Borneo (Blattaria: Blaberidae). Zootaxa 1390:21–25

    Article  Google Scholar 

  • Guo Y, Béthoux O, Gu J-J, Ren D (2013) Wing venation homologies in Pennsylvanian ‘cockroachoids’ (Insecta) clarified thanks to a remarkable specimen from the Pennsylvanian of Ningxia (China). J Syst Palaeontol 11:41–46

    Article  Google Scholar 

  • Haas F, Kukalová-Peck J (2001) Dermaptera hindwing structure and folding: New evidence for familial, ordinal and superordinal relationships within Neoptera (Insecta). Eur J Entomol 98:445–509

    Article  Google Scholar 

  • Hamilton KGA (1972) The insect wing, part II. Vein homology and the archetypal insect wing. J Kansas Entomol Soc 45:54–58

    Google Scholar 

  • Holdsworth RP Jr (1941) The wing development of Pteronarcys proteus Newman (Pteronarcidae: Plecoptera). J Morphol 70:431–461

    Article  Google Scholar 

  • Inward D, Beccaloni G, Eggleton P (2007) Death of an order: a comprehensive molecular phylogenetic study confirms that termites are eusocial cockroaches. Biol Lett 3:331–335

    Article  CAS  Google Scholar 

  • Karny H (1921) Zur systematik der Orthopteroiden insecten. Treubia 1:163–269

    Google Scholar 

  • Klass KD, Meier R (2006) A phylogenetic analysis of Dictyoptera (Insecta) based on morphological characters. Entomol Abh 63:3–50

    Google Scholar 

  • Kukalová-Peck J (1978) Origin and evolution of insect wings and their relation to metamorphosis, as documented by the fossil record. J Morphol 156:53–126

    Article  Google Scholar 

  • Kukalová-Peck J (1983) Origin of the insect wing and wing articulation from the arthropodan leg. Can J Zool 61:1618–1669

    Article  Google Scholar 

  • Kukalová-Peck J (1991) Fossil history and the evolution of hexapod structures. In: Naumann ID, Carne PB, Lawrence JF, Nielsen ES, Spradbery JP, Taylor RW, Whitten MJ, Littlejohn MJ (eds) The Insects of Australia, a textbook for students and researchers. Melbourne University Press, Melbourne, pp 141–179

    Google Scholar 

  • Kukalová-Peck J, Lawrence JF (2004) Relationships among coleopteran suborders and major endoneopteran lineages: evidence from hind wing characters. Eur J Entomol 101:95–144

    Article  Google Scholar 

  • Lameere A (1922) Sur la nervation alaire des insects. Bull Acad R Belg Cl Sci 1922:38–149 (on the wing-venation of insects. Psyche 30: 123–132. Translated by Austin M Brues, 1923)

    Google Scholar 

  • Li XR, Huang D (2018a) A new praying mantis from middle Cretaceous Burmese amber exhibits bilateral asymmetry of forefemoral spination (Insecta: Dictyoptera). Cretaceous Res 91:269–273

    Article  Google Scholar 

  • Li XR, Huang D (2018b) A new Cretaceous cockroach with heterogeneous tarsi preserved in Burmese amber (Dictyoptera, Blattodea, Corydiidae). Cretaceous Res 92:12–17

    Article  Google Scholar 

  • Li XR, Wang ZQ (2015) A taxonomic study of the beetle cockroaches (Diploptera Saussure) from China, with notes on the genus and species worldwide (Blattodea: Blaberidae: Diplopterinae). Zootaxa 4018:35–56

    Article  Google Scholar 

  • Li XR, Wang ZQ (2016) Perisphaerinae Brunner von Wattenwyl and Hyposphaeria Lucas are valid names concealed by the unavailable names Perisphaeriinae and Perisphaeria Burmeister (Blattodea: Blaberidae). ZooKeys 574:75–80

    Article  Google Scholar 

  • Li XR, Wang ZQ (2017) Updating the knowledge of assassin bug cockroaches (Blattodea: Blaberidae: Paranauphoeta Brunner von Wattenwyl): Species from China and taxonomic changes. Entomol Sci 20:302–317

    Article  Google Scholar 

  • Li XR, Wang LL, Wang ZQ (2018) Rediscovered and new perisphaerine cockroaches from SW China with a review of subfamilial diagnosis (Blattodea: Blaberidae). Zootaxa 4410:251–290

    Article  Google Scholar 

  • Ma C, Wang YY, Wu C, Kang L, Liu CX (2014) The compact mitochondrial genome of Zorotypus medoensis provides insights into phylogenetic position of Zoraptera. BMC Genom 15:1156

    Article  Google Scholar 

  • Meier R (1993) Book review. The insect of Australia: a textbook for studies and research workers, 2nd edition. Syst Biol 42:588–591

    Google Scholar 

  • Misof B, Liu S, Meusemann K, Peters RS, Donath A et al (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346:763–767

    Article  CAS  Google Scholar 

  • Nivedita M (1982) Histological observations on tracheal growth during wing development in Oncopeltus fasciatus (Dallas) (Heteroptera; Lygaeidae). Proc Indian Acad Sci Anim Sci 91:609–621

    Article  Google Scholar 

  • Prokop J, Pecharová M, Nel A, Hörnschemeyer T (2018) The wing base of the palaeodictyopteran genus Dunbaria Tillyard: where are we now? Arthropod Struct Dev 47:339–351

    Article  Google Scholar 

  • Qiu L, Che YL, Wang ZQ (2017) Contribution to the cockroach genus Ctenoneura Hanitsch, 1925 (Blattodea: Corydioidea: Corydiidae) with descriptions of seven new species from China. Zootaxa 4237:265–299

    Article  Google Scholar 

  • Ragge DR (1955a) The Wing-venation of the Orthoptera Saltatoria with Notes on Dictyopteran Wing-venation. British Museum (Natural History), London

    Google Scholar 

  • Ragge DR (1955b) The wing-venation of the order Phasmida. Trans Entomol Soc Lond 106:375–391

    Article  Google Scholar 

  • Ramsay GW (1990) Mantodea (Insecta), with a review of aspects of functional morphology and biology. Fauna N Zeal 19:1–96

    Google Scholar 

  • Rehn JWH (1951) Classification of the Blattaria as indicated by their wings (Orthoptera). Mem Am Entomol Soc 14:1–134

    Google Scholar 

  • Roth LM (1986) The genus Episymploce Bey-Bienko. III. Species from Laos, North and South Vietnam and Thailand. (Dictyoptera: Blattaria, Blattellidae). Entomol Scand 17:455–474

    Article  Google Scholar 

  • Roth LM (1987) The genus Episymploce Bey-Bienko. V. Species from China. (Dictyoptera: Blattaria, Blattellidae). Entomol Scand 18:125–141

    Google Scholar 

  • Roth LM (1997) The cockroach genera Pseudothyrsocera Shelford, Haplosymploce Hanitsch, and Episymploce Bey-Bienko (Blattaria: Blattelidae, Blattellinae). Tijdschr Entomol 140:67–110

    Google Scholar 

  • Roth LM (2003) Systematics and phylogeny of cockroaches (Dictyoptera: Blattaria). Orient Insects 37:1–186

    Article  Google Scholar 

  • Schneider JW, Lucas SG, Rowland JM (2004) The Blattida (Insecta) fauna of Carrizo Arroyo, New Mexico—biostratigraphic link between marine and nonmarine Pennsylvanian/Permian boundary profiles. In: Lucas SG, Zeigler KE (eds) Carboniferous–Permian transition. New Mex Mus Nat Hist Sci Bull 25:247–262

  • Shelford R (1906) Studies of the Blattidæ. Trans Entomol Soc Lond 1906:231–280

    Google Scholar 

  • Smart J (1951) The wing-venation of the American cockroach Periplaneta americana Linn. (Insecta: Blattidae). Proc Zool Soc Lond 121:501–509

    Article  Google Scholar 

  • Smart J (1953) The wing-venation of the Migratory Locust (Locusta migratoria Linn.) (Insecta: Acridiidae). Proc Zool Soc Lond 123:207–217

    Article  Google Scholar 

  • Smart J (1956) On the wing-venation of Chaeteessa and other mantids (Insecta: Mantodea). Proc Zool Soc Lond 127:545–553

    Article  Google Scholar 

  • Snodgrass RE (1935) Principles of insect morphology. McGraw-Hill Book Company, New York

    Google Scholar 

  • Song N, Li H, Song F, Cai WZ (2016) Molecular phylogeny of Polyneoptera (Insecta) inferred from expanded mitogenomic data. Sci Rep 6:36175

    Article  CAS  Google Scholar 

  • Vršanský P (1997) Piniblattella gen. nov.—the most ancient genus of the family Blattellidae (Blattodea) from the Lower Cretaceous of Siberia. Entomol Probl 28:67–79

    Google Scholar 

  • Waddington CH (1940) The genetic control of wing development in Drosophila. J Genet 41:75–139

    Article  Google Scholar 

  • Wang ZQ, Shi Y, Qiu ZW, Che YL, Lo N (2017) Reconstructing the phylogeny of Blattodea: robust support for interfamilial relationships and major clades. Sci Rep 7:3903

    Article  Google Scholar 

  • Wei D, Ren D (2013) Completely preserved cockroaches of the family Mesoblattinidae from the Upper Jurassic-Lower Cretaceous Yixian Formation (Liaoning Province, NE China). Geol Carpath 64:291–304

    Article  Google Scholar 

  • Wei DD, Béthoux O, Guo YX, Schneider JW, Ren D (2013) New data on the singularly rare ‘cockroachoids’ from Xiaheyan (Pennsylvanian; Ningxia, China). Alcheringa 37:547–557

    Article  Google Scholar 

  • Whitten JM (1962) Homology and development of insect wing tracheae. Ann Entomol Soc Am 55:288–295

    Article  Google Scholar 

  • Wieland F (2008) The genus Metallyticus reviewed (Insecta: Mantodea). Spec Phylogeny Evol 1:147–170

    Google Scholar 

  • Willkommen J (2008) The morphology of the pterothorax of Ephemeroptera, Odonata and Plecoptera (Insecta) and the homology of wing base sclerites and flight muscles. Stutt Beit Natur A Neue Serie 1:203–300

    Google Scholar 

  • Wootton RJ (1979) Function, homology and terminology in insect wings. Syst Entomol 4:81–93

    Article  Google Scholar 

  • Yoshizawa K (2011) Monophyletic Polyneoptera recovered by wing base structure. Syst Entomol 36:377–394

    Article  Google Scholar 

  • Zhang Z, Schneider JW, Hong Y (2013) The most ancient roach (Blattodea): a new genus and species from the earliest Late Carboniferous (Namurian) of China, with a discussion of the phylomorphogeny of early blattids. J Syst Palaeontol 11:27–40

    Article  Google Scholar 

  • Zheng Y, Wang C, Che Y, Wang Z (2016) The species of Symplocodes Hebard (Blattodea: Ectobiidae: Blattellinae) with description of a new species from China. J Nat Hist 50:339–361

    Article  Google Scholar 

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Acknowledgements

Most of the materials examined were collected by Dr. Shun-Hua Gui, Dr. Yan Shi, Dr. Jian-Yue Qiu, Mr. Zhi-Wei Qiu, Mr. Lu Qiu, Mr. Hong-Guang Liu and XRL. We thank our colleagues Ms. Li-Li Wang and Mr. Lu Qiu for drafting several figures in Online Resource 1. We also want to thank Mr. Tie-Xiong Zhao and Dr. Gui-Qiang Huang for collecting and donating the specimens of Spelaeoblatta sp. and Catara rugosicollis, respectively. The reviewers’ constructive comments improved the manuscript. Dr. Han-Qiang Wang (Institute of Plant Physiology and Ecology, SIBS, CAS) made one of the references accessible. This study is financially supported by the National Natural Sciences Foundation of China (nos. 31093430 and 31472026).

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Li, XR., Zheng, YH., Wang, CC. et al. Old method not old-fashioned: parallelism between wing venation and wing-pad tracheation of cockroaches and a revision of terminology. Zoomorphology 137, 519–533 (2018). https://doi.org/10.1007/s00435-018-0419-6

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