Abstract
The fine structures of vasa deferentia and postvesicular vasa deferentia were investigated in the hangingfly Terrobittacus implicatus (Cai et al. 2006) and the scorpionfly Cerapanorpa nanwutaina (Chou 1981) using light and transmission electron microscopy, and schematic diagrams were drawn accordingly. The vasa deferentia of both species comprise muscular layers, a basal lamina, and a mono-layered epithelium, but the postvesicular vasa deferentia contain muscular layers, a basal lamina, a single-layered epithelium, a subcuticular cavity, and an inner cuticle respectively. The vas deferens releases secretions into the lumen directly, probably by means of merocrine production. On the contrary, the cells of the postvesicular vas deferens correspond to class I glandular cells, discharging secretions into the subcuticular cavity first, and then into the lumen through an inner cuticle. The epithelium in both structures of Bittacidae is well developed and contains more microvilli, organelles, and more types of secretions than in Panorpidae. In Panorpidae, the spine of the postvesicular vas deferens may serve as a barricade for the reflow of the sperm and to protect the extraordinarily long structure from being collapsed or injured.
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References
Araújo VA, Zama U, Neves CA, Dolder H, Lino-Neto J (2005) Ultrastructural, histological and histochemical characteristics of the epithelial wall of the seminal vesicle of mature Scaptotrigona xanthotricha Moure males (Hymenoptera, Apidae, Meliponini). Braz J Morphol Sci 22:193–201. http://host-article-assets.s3.amazonaws.com/jms/587cb45b7f8c9d0d058b461c/fulltext.pdf
Bissell TL (1937) Structure of the reproductive system of the pecan weevil (Curculionidae). Ann Entomol Soc Am 30:242–251. https://doi.org/10.1093/aesa/30.2.242
Brito P, Salles FF, Dolder H (2011) Characteristics of the male reproductive system and spermatozoa of Leptophlebiidae (Ephemeroptera). Neotrop Entomol 40:103–107. https://doi.org/10.1590/S1519-566X2011000100015
Brito P, Salles FF, Dolder H (2012) Morphology of male reproductive systems in Ephemeroptera: intrinsic musculature. Neotrop Entomol 41:306–310. https://doi.org/10.1007/s13744-012-0039-7
Byers GW, Thornhill R (1983) Biology of the Mecoptera. Annu Rev Entomol 28:203–228. https://doi.org/10.1146/annurev.en.28.010183.001223
Cai L-J, Huang P-Y, Hua B-Z (2006) Two new Chinese Bittacus Latreille (Mecoptera: Bittacidae) from Michangshan Mountains. Entomotaxonomia 28:127–130.
Chapman RF (2013) The insects: structure and function, 5th edn. Cambridge University Press, Cambridge
Chen J, Tan J-L, Hua B-Z (2013) Review of the Chinese Bittacus (Mecoptera: Bittacidae) with descriptions of three new species. J Nat Hist 47:1463–1480. https://doi.org/10.1080/00222933.2012.763065
Chou I, Ran R-B, Wang S-M (1981) Taxonomic study of the Chinese Mecoptera (I, II). Entomotaxonomia 3:1–22.
Cooper KW (1972) A Southern California Boreus, B. notoperates n. sp. I. Comparative morphology and systematics (Mecoptera: Boreidae). Psyche 79:269–283. https://doi.org/10.1155/1972/56294
Dallacqua RP, Landim CC (2003) Ultrastructure of the ducts of the reproductive tract of males of Melipona bicolor bicolor Lepeletier (Hymenoptera, Apinae, Meliponini). Anat Histol Embryol 32:276–281. https://doi.org/10.1046/j.1439-0264.2003.00484.x
Dallai R, Marchini D, Callaini G (1988) Microtubule and microfilament distribution during the secretory activity of an insect gland. J Cell Sci 91:563–570. http://jcs.biologists.org/content/91/4/563
Dustin P (1985) Microtubules, 2nd edn. Springer-Verlag, New York
Filimonova SA (2016) Morpho-functional variety of the coxal glands in cheyletoid mites (Prostigmata). I. Syringophilidae. Arthropod Struct Dev 45:356–367. https://doi.org/10.1016/j.asd.2016.06.005
Freitas SPC, Gonçalves TCM, Serrão JE, Costa J, Santos-Mallet JR (2010) Male reproductive system structure and accessory glands ultrastructure of two species of Triatoma (Hemiptera, Reduviidae, Triatominae). Micron 41:518–525. https://doi.org/10.1016/j.micron.2010.01.008
Friele A (1930) Die postembryonale Entwicklungsgeschichte der männlichen Geschlechtsorgane und Ausführungswege von Psychoda alternata Say. Z Morph Ökol Tiere 18:249–288. https://doi.org/10.1007/BF00419211.pdf
Gao Q-H, Hua B-Z (2013) Co-evolution of the mating position and male genitalia in insects: a case study of a hangingfly. PLoS One 8:e80651. https://doi.org/10.1371/journal.pone.0080651
Gerber GH, Church NS, Rempel JG (1971) The anatomy, histology, and physiology of the reproductive systems of Lytta nuttalli Say (Coleoptera: Meloidae). I. The internal genitalia. Can J Zool 49:523–533. https://doi.org/10.1139/z71-080
Gomes LF, Badke JP, Zama U, Dolder H, Lino-Neto J (2012) Morphology of the male reproductive system and spermatozoa in Centris Fabricius, 1804 (Hymenoptera: Apidae, Centridini). Micron 43:695–704. https://doi.org/10.1016/j.micron.2012.01.013
Grell KG (1942) Der Genitalapparat von Panorpa communis L. Zool Jb Anat 67:513–588
Huang F, Yu R-X, Chen X-X (2007) Ultrastructure of the male reproductive system of Cotesia vestalis (Hymenoptera: Braconidae) with preliminary characterization of the secretions. Microsc Res Techn 70:563–571. https://doi.org/10.1002/jemt.20435
Karakaya G, Özyurt N, Candan S, Suludere Z (2012) Structure of the male reproductive sytem in Coreus marginatus (L.) (Hemiptera: Coreidae). Türk Entomol Derg 36:193–204. http://dergipark.gov.tr/entoted/issue/5695/76134
Kölsch G (2000) The ultrastructure of glands and the production and function of the secretion in the adhesive capture apparatus of Stenus species (Coleoptera: Staphylinidae). Can J Zool 78:465–475. https://doi.org/10.1139/z99-213
Krüger S, Ferenz H-J, Randall M, Hodgson AN (2014) Structure of the male reproductive accessory glands of Pterostichus nigrita (Coleoptera: Carabidae), their role in spermatophore formation. Invertebr Reprod Dev 58:75–88. https://doi.org/10.1080/07924259.2013.822835
Landim CC, Dallacqua RP (2005) Morphology and protein patterns of honey bee drone accessory glands. Genet Mol Res 4:473–481. https://www.geneticsmr.com/year2005/vol4-3/pdf/gmr0104.pdf
Ledbetter MC, Porter HR (1963) A “microtubule” in plant cell fine structure. J Cell Biol 19:239–250. https://doi.org/10.1083/jcb.19.1.239
Liu N-Y, Wu G-X, Ze S-Z, Yang B, Zhu J-Y (2017) Morphology and ultrastructure of the male reproductive system of the jewel wasp, Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae). J Asia Pac Entomol 20:577–582. https://doi.org/10.1016/j.aspen.2017.03.017
Lyu Q-H, Zhang B-B, Hua B-Z (2018) Ultrastructure and function of the seminal vesicle of Bittacidae (Insecta: Mecoptera). Arthropod Struct Dev 47:173–179. https://doi.org/10.1016/j.asd.2018.02.001
Marchini D, Brundo MV, Sottile L, Viscuso R (2009) Structure of male accessory glands of Bolivarius siculus (Fischer) (Orthoptera, Tettigoniidae) and protein analysis of their secretions. J Morphol 270:880–891. https://doi.org/10.1002/jmor.10727
Matsuda R (1976) Morphology and evolution of the insect abdomen: with special reference to developmental patterns and their bearings upon systematics. Pergamon Press, New York
Miyaké T (1913) Studies on the Mecoptera of Japan. J Coll Agric Tokyo Imp 4:265–400
Moors L, Spaas O, Koeniger G, Billen J (2005) Morphological and ultrastructural changes in the mucus glands of Apis mellifera drones during pupal development and sexual maturation. Apidologie 36:245–254. https://doi.org/10.1051/apido:2005016
Noirot C, Quennedey A (1974) Fine structure of insect epidermal glands. Annu Rev Entomol 19:61–80. https://doi.org/10.1146/annurev.en.19.010174.000425
Özyurt N, Candan S, Suludere Z (2013) The morphology and histology of the male reproductive system in Dolycoris baccarum Linnaeus 1758 (Heteroptera: Pentatomidae)—light and scanning electron micoscope studies. Micron 44:101–106. https://doi.org/10.1016/j.micron.2012.04.017
Özyurt N, Candan S, Suludere Z (2015) Ultrastructure of male reproductive system of Eurydema ventrale Kolenati 1846 (Heteroptera: Pentatomidae). Microsc Res Techn 78:643–653. https://doi.org/10.1002/jemt.22514
Paoli F, Dallai R, Cristofaro M, Arnone S, Francardi V, Roversi PF (2014) Morphology of the male reproductive system, sperm ultrastructure and γ-irradiation of the red palm weevil Rhynchophorus ferrugineus Oliv. (Coleoptera: Dryophthoridae). Tissue Cell 46:274–285. https://doi.org/10.1016/j.tice.2014.06.003
Penny ND, Byers GW (1979) A check-list of the Mecoptera of the world. Acta Amazon 9:365–388. https://doi.org/10.1590/1809-43921979092365
Potter E (1938) The internal anatomy of the order Mecoptera. Trans R Entomol Soc Lond 87:467–501. https://doi.org/10.1111/j.1365-2311.1938.tb00726.x
Quennedey A (1998) Insect epidermal gland cells: ultrastructure and morphgenesis vol Insecta. In: Harrison FW, Locke M (eds) Microscopic anatomy of invertebrates, vol 11A. Wiley-Liss, New York, pp 177–207
Radhakrishnan P, Marchini D, Taylor PW (2009) Ultrastructure of male reproductive accessory glands and ejaculatory duct in the Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae). Arthropod Struct Dev 38:216–226. https://doi.org/10.1016/j.asd.2008.09.004
Riemann JG, Giebultowicz JM (1992) Sperm maturation in the vasa deferentia of the gypsy moth, Lymantria dispar L. (Lepidoptera: Lymantriidae). Int J Insect Morphol Embryol 21:271–284. https://doi.org/10.1016/0020-7322(92)90022-F
Riemann JG, Thorson BJ (1976) Ultrastructure of the vasa deferentia of the Mediterranean flour moth. J Morphol 149:483–505. https://doi.org/10.1002/jmor.1051490404
Satir P, Stuart AM (1965) A new apical microtubule-associated organelle in the sternal gland of Zootermopsis nevadensis (Hagen), Isoptera. J Cell Biol 24:277–283. https://doi.org/10.1083/jcb.24.2.277
Setty LR (1940) Biology and morphology of some North American Bittacidae (Order Mecoptera). Am Midl Nat 23:257–353. https://doi.org/10.2307/2420667
Shen J, Hua B-Z (2013) Fine structures of the ejaculatory sac and sperm pump of the scorpionfly Panorpa liui Hua (Mecoptera: Panorpidae). Micron 51:41–47. https://doi.org/10.1016/j.micron.2013.06.007
Sinclair BJ, Borkent A, Wood DM (2007) The male genital tract and aedeagal components of the Diptera with a discussion of their phylogenetic significance. Zool J Linnean Soc 150:711–742. https://doi.org/10.1111/j.1096-3642.2007.00314.x
Snodgrass RE (1935) Principles of insect morphology. McGraw Hill, New York
Šobotník J, Kutalová K, Vytisková B, Roisin Y, Bourguignon T (2014) Age-dependent changes in ultrastructure of the defensive glands of Neocapritermes taracua workers (Isoptera, Termitidae). Arthropod Struct Dev 43:205–210. https://doi.org/10.1016/j.asd.2014.02.003
Steiner P (1937) Beitrag zur Fortpflanzungsbiologie und Morphologie des Genitalapparates von Boreus hiemalis L. Z Morph Ökol Tiere 32:276–288. https://doi.org/10.1007/BF00403076
Sturm R (2008) Morphology and histology of the ductus receptaculi and accessory glands in the reproductive tract of the female cricket, Teleogryllus commodus. J Insect Sci 8:1–12. https://doi.org/10.1673/031.008.3501
Tan J-L, Hua B-Z (2009) Terrobittacus, a new genus of the Chinese Bittacidae (Mecoptera) with descriptions of two new species. J Nat Hist 43:2937–2954. https://doi.org/10.1080/00222930903359628
Viscuso R, Brundo MV, Sottile L (2005) Ultrastructural organization of the seminal vesicles of Baculum thaii (Phasmida, Phasmatidae) during sexual maturity. Ital J Zool 72:113–119. https://doi.org/10.1080/11250000509356661
Wheeler DE, Krutzsch PH (1992) Internal reproductive system in adult males of the genus Camponotus (Hymenoptera: Formicidae: Formicinae). J Morphol 211:307–317. https://doi.org/10.1002/jmor.1052110308
Wieczorek K, Świątek P (2008) Morphology and ultrastructure of the male reproductive system of the woolly beech aphid Phyllaphis fagi (Hemiptera: Aphididae: Phyllaphidinae). Eur J Entomol 105:707–712. https://doi.org/10.14411/eje.2008.096
Xie S, Hua B-Z (2010) Ultrastructure of the seminal vesicle and sperm storage in Panorpidae (Insecta: Mecoptera). Micron 41:760–768. https://doi.org/10.1016/j.micron.2010.05.012
Zhang B-B, Zhang C-N, Dietrich C, Dai W (2016) Anatomy and ultrastructure of male reproductive system in two leafhoppers Cicadella viridis and Kolla paulula (Hemiptera: Auchenorrhyncha: Cicadellidae). Ann Entomol Soc Am 109:447–462. https://doi.org/10.1093/aesa/saw016
Zhong W, Ding G, Hua B-Z (2015) The role of male’s anal horns in copulation of a scorpionfly. J Zool 295:170–177. https://doi.org/10.1111/jzo.12194
Acknowledgements
We thank Lu Liu and Ying Miao for the assistance in specimen collection and Xiao-Jun Fan, Mi Huo, and Ke-Rang Huang for the assistance in transmission electron microscopy.
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This work was funded by the National Natural Science Foundation of China (grant no. 31672341).
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Lyu, QH., Hua, BZ. Ultrastructure of the vasa deferentia of Terrobittacus implicatus and Cerapanorpa nanwutaina (Insecta: Mecoptera). Protoplasma 256, 883–891 (2019). https://doi.org/10.1007/s00709-019-01346-6
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DOI: https://doi.org/10.1007/s00709-019-01346-6