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Spermatozoa and spermiogenesis of the wolf spider Schizocosa malitiosa (Lycosidae, Araneae) and its functional and phylogenetic implications

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Abstract

The wolf spider Schizocosa malitiosa is a well-known model system for studies on sexual selection in spiders. Despite this, little is known about the morphology of the reproductive system and spermatozoa in this species. In the present study, we investigate the male genital system and sperm cells of S. malitiosa using electron microscopy and provide a computer-based 3D reconstruction of the spermatozoa for the first time for arthropods. In general, the male genital system consists of two long, tube-like testes that lead into convoluted deferent ducts. The ejaculatory duct is enlarged and contains a large quantity of sperm and secretion. As revealed by transmission electron microscopy, only one type of secretion droplet is present in the seminal fluid. The spermatozoa of S. malitiosa resemble an organization known for members of the RTA clade, i.e., with an arrow-shaped acrosomal vacuole partly sunk into the nucleus and a chambered centriolar adjunct (a newly introduced character). This organization provides further support for these characters as potential synapomorphies for the RTA clade. By the end of the spermiogenesis, the nucleus and axoneme coils within the cell and a multi-layered secretion sheath are formed representing cleistospermia. The function of the thick secretion sheath is still unknown, but might be correlated either with the residency time in the female (insemination until oviposition) since female S. malitiosa do not lay eggs before the fourth month after copulation or with the receptivity-inhibiting substances suggested for this species.

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References

  • Aire TA, Ozegbe PC (2012) Components and development of the centriolar complex during and beyond spermiogenesis in a passeridan bird, the masked weaver (Ploceus velatus). Tissue Cell 44:63–67

    Article  PubMed  Google Scholar 

  • Aisenberg A, Costa FG (2005) Females mated without sperm transfer maintain high sexual receptivity level in the wolf spider Schizocosa malitiosa. Ethology 111:545–558

    Article  Google Scholar 

  • Alberti G (1990) Comparative spermatology of Araneae. Acta Zool Fenn 190:17–34

    Google Scholar 

  • Alberti G (2000) Chelicerata. In: Adiyodi KG, Adiyodi RG (eds) Reproductive biology of invertebrates, vol IX B. Wiley, Chichester, pp 311–388

    Google Scholar 

  • Alberti G, Coyle FA (1991) Ultrastructure of the primary male genital system, spermatozoa and spermiogenesis of Hypochilus pococki (Araneae, Hypochilidae). J Arachnol 19:136–149

    Google Scholar 

  • Alberti G, Weinmann C (1985) Fine structure of spermatozoa of some labidognath spiders (Filistatidae, Segestriidae, Dysderidae, Oonopidae, Scytodidae, Pholcidae; Araneae; Arachnida) with remarks on spermiogenesis. J Morphol 185:1–35

    Article  Google Scholar 

  • Alberti G, Afzelius BA, Lucas SM (1986) Ultrastructure of spermatozoa and spermatogenesis in bird spiders (Theraphosidae, Mygalomorphae, Araneae). J Submicr Cytol 18:739–753

    Google Scholar 

  • Baruffaldi L, Costa FG, Rodríguez A, González A (2010) Chemical communication in Schizocosa malitiosa: evidence of a female contact sex pheromone and persistence in the field. J Chem Ecol 36:759–767

    Article  PubMed  CAS  Google Scholar 

  • Bertkau P (1875) Über den Generationsapparat der Araneiden. Arch Naturgesch 41:235–262

    Google Scholar 

  • Bertkau P (1877) Über die Übertragungsorgane und die Spermatozoen der Spinnen. Verh Naturh Ver Preuss Rheinl 34:28–32

  • Breed WG (2005) Evolution of the spermatozoon in muroid rodents. J Morphol 265:271–290

    Article  PubMed  Google Scholar 

  • Burger M, Michalik P (2010) The male genital system of goblin spiders: evidence for the monophyly of Oonopidae (Araneae, Arachnida). Am Mus Novit 3675:1–13

    Google Scholar 

  • Coddington JA, Levi HW (1991) Systematics and evolution of spiders (Araneae). Annu Rev Ecol Syst 22:565–592

    Article  Google Scholar 

  • Coelho L, Aisenberg A, Costa FG (2010) Testing female receptiveness to novel or previous mating partners in a wolf spider. Behaviour 147:383–395

    Article  Google Scholar 

  • Costa FG (1975) El comportamiento precopulatorio de Lycosa malitiosa Tullgren (Araneae: Lycosidae). Rev Brasil Biol 35:359–368

    Google Scholar 

  • Costa FG (1979) Análisis de la cópula y de la actividad postcopulatoria de Lycosa malitiosa Tullgren (Araneae, Lycosidae). Rev Brasil Biol 39:361–376

    Google Scholar 

  • Costa (1991) Fenología de Lycosa malitiosa Tullgren (Araneae, Lycosidae) como componente del criptozoos en Marindia, localidad costera del sur del Uruguay. Bol Soc Zool Uruguay 6:8–21

    Google Scholar 

  • Costa FG, Capocasale RM (1985) La producción de ootecas de Lycosa malitiosa Tullgren (Araneae, Lycosidae). III. Distribución temporal de las oviposiciones. Aracnología 5:1–14

    Google Scholar 

  • Costa-Ayub CLS, Faraco CD (2007) Ultrastructural aspects of spermiogenesis and synspermia in the brown spider Loxosceles intermedia (Araneae: Sicariidae). Arthropod Struct Dev 36:41–51

    Article  PubMed  Google Scholar 

  • Crome W (1951) Die grobe Morphologie des männlichen Genitalapparates einiger Araneen. Deut Zool Z 1:169–186

    Google Scholar 

  • Estramil N, Costa FG (2007) Female sexual receptivity after partial copulations in the wolf spider Schizocosa malitiosa. J Zool 271:148–153

    Article  Google Scholar 

  • Fouquet JP, Kann ML, Combeau C, Melki R (1998) γ-tubulin during the differentiation of spermatozoa in various mammals and man. Mol Hum Reprod 12:1122–1129

    Article  Google Scholar 

  • Fouquet JP, Kann ML, Souès S, Melki R (2000) ARP1 in Golgi organisation and attachment of manchette microtubules to the nucleus during mammalian spermatogenesis. J Cell Sci 113:877–886

    PubMed  CAS  Google Scholar 

  • González M, Costa FG (2008) Persistence of sexual reluctance in mated females and importance of regular copulations in a wolf spider. Ethol Ecol Evol 20:115–124

    Article  Google Scholar 

  • Griswold CE, Ramírez MJ, Coddington JA, Platnick NI (2005) Atlas of phylogenetic data for entelegyne spiders (Araneae: Araneomorphae: Entelegynae) with comments on their phylogeny. Proc Calif Acad Sci 56:1–325

    Google Scholar 

  • Higginson DM, Pitnick S (2011) Intra-ejaculate sperm interactions: do sperm cooperate? Biol Rev 86:249–270

    Article  PubMed  Google Scholar 

  • Jamieson BGM (1987) Ultrastructure and phylogeny of insect spermatozoa. Cambridge University Press, London

    Google Scholar 

  • Jamieson BGM (2007) Avian spermatozoa: structure and phylogeny. In: Jamieson BGM (ed) Reproductive biology and phylogeny of birds. Science Publishers, Enfield New Hampshire, pp 349–511

    Google Scholar 

  • Jamieson BGM, Dallai R, Afzelius BA (1999) Insects: their spermatozoa and phylogeny. Science Publishers, Enfield, New Hampshire

    Google Scholar 

  • Jörger KM, Heß M, Neusser TP, Schrödl M (2009) Sex in the beach: spermatophores, dermal insemination and 3D sperm ultrastructure of the aphallic mesopsammic Pontohedyle milaschewitchii (Acochlidia, Opisthobranchia, Gastropoda). Mar Biol 156:1159–1170

    Article  Google Scholar 

  • Kim JK, Kim TH, Moon MJ (1993) Ultrastructure of the testis in the spider Pardosa astrigera L. Koch. Korean Arachnol 9:43–53

    Google Scholar 

  • Lopez A, Bonaric JC, Boissin L (1983) Etude ultrastructurale de la spermiogenese chez l’araignée Pisaura mirabilis (Clerck, 1858) (Pisauridae). Rev Arachnol 5:55–64

    Google Scholar 

  • Marotta R, Ferraguti M, Erséus C, Gustavsson LM (2008) Combined-data phylogenetics and character evolution of Clitellata (Annelida) using 18S rDNA and morphology. Zool J Linn Soc 154:1–26

    Article  Google Scholar 

  • Michalik P (2007) Spermatozoa and spermiogenesis of Liphistius cf phuketensis (Mesothelae, Araneae, Arachnida) with notes on phylogenetic implications. Arthropod Struct Dev 36:327–335

    Article  PubMed  Google Scholar 

  • Michalik P (2009) The male genital system of spiders (Arachnida, Araneae) with notes on the fine structure of seminal secretions. In: Kropf C, Horak O (eds) Towards a natural history of arthropods and other organisms. In memoriam Konrad Thaler. Contributions to Natural History, Bern, pp 959–972

  • Michalik P, Alberti G (2005) On the occurence of the 9+0 axonemal pattern in the spermatozoa of sheetweb spiders (Linyphiidae, Araneae). J Arachnol 33:569–572

    Article  Google Scholar 

  • Michalik P, Hormiga G (2010) Ultrastructure of the spermatozoa in the spider genus Pimoa: new evidence for the monophyly of Pimoidae plus Linyphiidae (Arachnida: Araneae). Am Mus Novit 3682:1–17

    Article  Google Scholar 

  • Michalik P, Huber BA (2006) Spermiogenesis in Psilochorus simoni (Berland, 1911) (Pholcidae, Araneae): evidence for considerable within-family variation in sperm structure and development. Zoology 109:14–25

    Article  PubMed  Google Scholar 

  • Michalik P, Uhl G (2005) The male genital system of the cellar spider Pholcus phalangioides (Fuesslin, 1775) (Pholcidae, Araneae): development of spermatozoa and seminal secretion. Front Zool 2:1–12

    Article  Google Scholar 

  • Michalik P, Dallai R, Giusti F, Alberti G (2004a) The ultrastructure of the peculiar synspermia of some Dysderidae (Araneae, Arachnida). Tissue Cell 36:447–460

    Article  PubMed  CAS  Google Scholar 

  • Michalik P, Haupt J, Alberti G (2004b) On the occurence of coenospermia in mesothelid spiders (Araneae: Heptathelidae). Arthropod Struct Dev 33:173–181

    Article  PubMed  CAS  Google Scholar 

  • Michalik P, Sacher P, Alberti G (2006) Ultrastructural observations of spermatozoa of several tetragnathid spiders with phylogenetic implications (Araneae, Tetragnathidae). J Morphol 267:129–151

    Article  PubMed  Google Scholar 

  • Miller JA, Carmichael A, Ramírez MJ, Spagna JC, Haddad CR, Řezáč M, Johannesen J, Král J, Wang XP, Griswold CE (2010) Phylogeny of entelegyne spiders: affinities of the family Penestomidae (NEW RANK), generic phylogeny of Eresidae, and asymmetric rates of change in spinning organ evolution (Araneae, Araneoidea, Entelegynae). Mol Phylogenet Evol 55:786–804

    Article  PubMed  Google Scholar 

  • Mottier-Pavie V, Megraw TL (2009) Drosophila bld10 is a centriolar protein that regulates centriole, basal body, and motile cilium assembly. Mol Biol Cell 20:2605–2614

    Article  PubMed  CAS  Google Scholar 

  • Ōsaki H (1969) Electron microscope study on the spermatozoon of the liphistiid spider Heptathela kimurai. Acta Arachnol 22:1–12

    Article  Google Scholar 

  • Ōsaki H (1972) Electron microscope study on spermiogenesis in the spider Oxyopes sertatus. Jap J Zool 16:184–199

    Google Scholar 

  • Platnick NI (2012) The World Spider Catalog, Version 13.0, American Museum of Natural History. http://research.amnh.org/iz/spiders/catalog

  • Platnick NI, Abrahim N, Álvarez-Padilla F, Andriamalala D, Baehr B, Baert L, Bonaldo AB, Brescovit AD, Chousou-Polydouri N, Dupérré N, Eichenberger B, Fannes W, Gaublomme E, Gillespie RG, Grismado CJ, Griswold CE, Harvey MS, Henrard A, Hormiga G, Izquierdo MA, Jocqué R, Kranz-Baltensperger Y, Kropf C, Ott R, Ramírez MJ, Raven RI, Rheims C, Ruiz GRS, Santos AJ, Saucedo A, Sierwald P, Szüts T, Ubick D, Wang X-P (2012) Tarsal organ morphology and the phylogeny of goblin spiders (Araneae, Oonopidae), with notes on basal genera. Am Mus Novit 3736:1–52

    Google Scholar 

  • Reger JF (1970) Spermiogenesis in the spider Pisaurina sp.: a fine structure study. J Morphol 130:421–433

    Article  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as electron-opaque stain in electron microscopy. J Cell Biol 17:208–212

    Article  PubMed  CAS  Google Scholar 

  • Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton

    Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43

    Article  PubMed  CAS  Google Scholar 

  • Useta G, Huber BA, Costa FG (2007) Spermathecal morphology and sperm dynamics in the female Schizocosa malitiosa (Araneae: Lycosidae). Eur J Entomol 104:777–785

    Google Scholar 

  • Wang Z, Zhong X (1993) Origin and function of the centriole adjunct in spermatids of insects. Acta Entomol Sinica 36:419–422

    Google Scholar 

  • Wu XM, Song DX, Chen DY (1997) Ultrastructure of spermatozoa and spermatogenesis in wolf spider Pardosa astrigera (Araneae: Lycosidae). Acta Zool Sinica 43:17–26

    Google Scholar 

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Acknowledgments

We are deeply indebted to Christian Wirkner (Universität Rostock, Germany) for help with the implementation of the 3D pdf. We thank Steffen Harzsch (Ernst-Moritz-Arndt-Universität Greifswald, Germany) who gave us the possibility to use the Amira 5.3 workstation. The first author thanks Gerd Alberti (Ernst-Moritz-Arndt-Universität Greifswald, Germany) for helpful discussion on the sperm structures of the RTA clade. The authors wish to thank Jason Dunlop (Museum für Naturkunde, Berlin, Germany) for improving the English and the anonymous reviewers for the helpful comments on the manuscript. Funding for this research was provided by the German Research Foundation to PM (DFG Mi 1255/5-1).

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Authors and Affiliations

  1. Allgemeine und Systematische Zoologie, Zoologisches Institut und Museum, Ernst-Moritz-Arndt-Universität, J.-S.-Bach-Straße 11/12, 17489, Greifswald, Germany

    Peter Michalik & Elisabeth Lipke

  2. Division of Invertebrate Zoology, American Museum of Natural History, New York City, NY, USA

    Peter Michalik

  3. Laboratorio de Etología, Ecología y Evolución, Instituto de Investigaciones Biológicas Clemente Estable, Montevideo, Uruguay

    Anita Aisenberg & Rodrigo Postiglioni

  4. Sección Entomología, Facultad de Ciencias, UdelaR, Montevideo, Uruguay

    Rodrigo Postiglioni

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  1. Peter Michalik
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  2. Anita Aisenberg
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  4. Elisabeth Lipke
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Correspondence to Peter Michalik.

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Communicated by A. Schmidt-Rhaesa.

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435_2012_166_MOESM1_ESM.pdf

Computer-based 3D reconstruction visualizing the different cell components in a coiled sperm cell in the lumen of the testis. To be able to actively rotate and study the 3D-reconstruction, click on the picture. Use the mouse for navigation. To hide/show different structures, click the tree icon and select from the list. The image stack used for the 3D reconstruction is stored in MorphDBase (https://www.morphdbase.de?P_Michalik_20120706-M-2.1) (PDF 3614 kb)

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Michalik, P., Aisenberg, A., Postiglioni, R. et al. Spermatozoa and spermiogenesis of the wolf spider Schizocosa malitiosa (Lycosidae, Araneae) and its functional and phylogenetic implications. Zoomorphology 132, 11–21 (2013). https://doi.org/10.1007/s00435-012-0166-z

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  • DOI: https://doi.org/10.1007/s00435-012-0166-z

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