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Ultrastructure of spermatozoa of Onthophagus taurus (Coleoptera, Scarabaeidae) exhibits heritable variation

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Abstract

Sperm competition is thought to be an important selective pressure shaping sperm form and function. However, few studies have moved beyond gross examinations of sperm morphology. Sperm length is subject to sexual selection via sperm competition in the scarab beetle Onthophagus taurus. Here, the structure and ultrastructure of spermatozoa in this species were investigated using light and electron microscopy. Spermatozoa were found to be filiform, measuring about 1,200 mm in length. The sperm head consists of a three-layered acrosome and a nuclear region bearing the anterior extension of the centriole adjunct. Acrosome and nuclear regions are bilaterally symmetric, with their axes of symmetry being orthogonal to each other. Head and flagellar structures are connected by a well-developed centriole adjunct. The sperm heads are asymmetrically surrounded by accessory material and embedded into the cytoplasm of the spermatocyst cell. The accessory material is produced inside the spermatids and then transferred to the outside due to a new membrane formed around the sperm’s organelles. The old spermatid membrane separates the accessory material from the cyst cell. The flagellum contains a 9+9+2 axoneme, two accessory bodies, and two mitochondrial derivatives of unequal size. The major mitochondrial derivative is significantly larger than the minor one. The axoneme is arranged in a sinusoidal manner parallel along the major mitochondrial derivative. The spermatozoa show no progressive motility when released in buffer solution which is likely to be the result of the flagellar arrangement and the structure of the major mitochondrial derivative. The cross-sectional area of the minor and the major mitochondrial derivatives show different patterns of genetic variation. The data provide the first estimates of genetic variation in sperm ultrastructure for any species, and give evidence for the persistence of genetic variation in ultrastructure required for the rapid and divergent evolution that characterizes spermatozoa generally.

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References

  • Baccetti B (1972) Insect sperm cells. Adv Insect Physiol 9:315–397

    Article  CAS  Google Scholar 

  • Baccetti B, Daccordi M (1988) Sperm structure and phylogeny of the Chrysomelidae. In: Jolivet P, Petitpierre E, Hsiao TH (eds) Biology of Chrysomelidae. Kluwer Academic, Dordrecht, pp 357–378

    Google Scholar 

  • Baccetti B, Burrini AG, Dallai R, Giusti F, Mazzini M, Renieri T, Rosati F, Selmi G (1973) Structure and function in the spermatozoon of Tenebrio molitor (The spermatozoon of Arthropoda. XX). J Mech Cell Mot 2:149–161

    CAS  Google Scholar 

  • Baccetti B, Dallai R, Rosati F, Giusti F, Bernini F, Selmi G (1974) The spermatozoon of Arthropoda XXVI. The spermatozoon of Isoptera, Embioptera and Dermaptera. J Microsc 21:159–172

    Google Scholar 

  • Baccetti B, Dallai R, Pallini V, Rosati F, Afzelius BA (1977) Protein of insect sperm mitochondrial crystals—Crystallomitin. J Cell Biol 73:594–600

    Article  CAS  PubMed  Google Scholar 

  • Breland OP, Gassner G III, Riess RW, Biesele JJ (1966) Certain aspects of the centriole adjunct, spermiogenesis and the mature sperm of insects. Can J Genet Cytol 8:759–773

    Google Scholar 

  • Burrini AG, Magnano L, Magnano AR, Scala C, Baccetti B (1988) Spermatozoa and phylogeny of Curculionoidea (Coleoptera). Int J Insect Morphol Embryol 17:1–50

    Article  Google Scholar 

  • Dallai R, Afzelius BA (1987) Sperm ultrastructure in the water beetles (Insecta, Coleoptera). Boll Zool 4:301–306

    Google Scholar 

  • Dlugosz J, Harrold JW (1952) The spermatozoon of the spider beetle Ptinus tectus Boieldieu as seen by light and electron microscopy. Proc R Soc Edinb B 64:353–366

    Google Scholar 

  • Emlen DJ, Marangelo J, Ball B, Cunningham CW (2005) Diversity in the weapons of sexual selection: horn evolution in the beetle genus Onthophagus (Coleoptera: Scarabaeidae). Evolution 59:1060–1084

    CAS  PubMed  Google Scholar 

  • Fain-Maurel MA (1966) Aquistitions récentes sur les spermatogenèses atypiques. Ann Biol 4–5:513–564

    Google Scholar 

  • Furieri P (1963) Aspetti morfologici della spermiogenesi di Oryctes grypus Illig. Redia 48:29–40

    Google Scholar 

  • García-González F, Simmons LW (2007) Shorter sperm confer higher competitive fertilization success. Evolution 61:816–824

    Article  PubMed  Google Scholar 

  • Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130:195–204

    CAS  PubMed  Google Scholar 

  • House CM, Simmons LW (2003) Genital morphology and fertilization success in the dung beetle Onthophagus taurus: an example of sexually selected male genitalia. Proc R Soc Lond B 270:447–455

    Article  Google Scholar 

  • House CM, Simmons LW (2005) Relative influence of male and female genital morphology on paternity in the dung beetle Onthophagus taurus. Behav Ecol 16:889–897

    Article  Google Scholar 

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

    Google Scholar 

  • Kubo-Irie M, Miura I, Irie M, Nakazawa T, Mohri H (2000) Spermiogenesis in the stag beetle, Aegus lavicollis Waterhouse (Coleoptera, Lucanidae), with special reference to the centriole adjunct. Invertebr Reprod Dev 37:223–231

    Article  Google Scholar 

  • Lee PE, Wilkes A (1965) Polymorphic spermatozoa in the hymenopterous wasp Dahlbominous. Science 147:1445–1446

    Article  CAS  PubMed  Google Scholar 

  • Lindsey JN, Biesele J (1974) Centriole adjunct development in the grasshopper (Melanoplus differentialis). Cytobios 10:59–81

    Google Scholar 

  • Lino-Neto J, Dolder H (2001a) Redescription of sperm structure and ultrastructure of Trichogramma dendrolimi (Hymenoptera: Chalcidoidea: Trichogrammatidae). Acta Zool 82:159–164

    Article  Google Scholar 

  • Lino-Neto J, Dolder H (2001b) Ultrastructural characteristics of the spermatozoa of Scelionidae (Hymenoptera, Platygastroidea) with phylogenetic considerations. Zool Scr 30:89–96

    Article  Google Scholar 

  • Lino-Neto J, Báo SN, Dolder H (1999) Structure and ultrastructure of the spermatozoa of Bephratelloides pomorum (Fabricius) (Hymenoptera: Eurytomidae). Int J Insect Morphol Embryol 28:253–259

    Article  Google Scholar 

  • Lino-Neto J, Báo SN, Dolder H (2000) Structure and ultrastructure of the spermatozoa of Trichogramma pretiosum Riley and Trichogramma atopovirilia Oatman and Platner (Hymenoptera: Trichogrammatidae). Acta Zool 81:205–211

    Article  Google Scholar 

  • Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, Sunderland

    Google Scholar 

  • Mackie JB, Walker MH (1974) A study of the conjugate sperm of dytiscid water beetles Dytiscus marginalis and Colymbetes fuscus. Cell Tissue Res 148:505–519

    Article  CAS  PubMed  Google Scholar 

  • Mazzini M (1976) Giant spermatozoa in Davales bipustulatus F. (Coleoptera: Cleridae). Int J Insect Morphol Embryol 5:107–115

    Article  Google Scholar 

  • Mencarelli C, Lupetti P, Dallai R (2008) New insights into the cell biology of insect axonemes. In: Jeon KW (ed) International Review of Cell and Molecular Biology, Elsevier, pp 95–145

  • Morrow EH, Gage MJG (2000) The evolution of sperm length in moths. Proc R Soc Lond B 267:307–313

    Article  CAS  Google Scholar 

  • Paccagnini E, Mencarelli C, Mercati D, Afzelius BA, Dallai R (2007) Ultrastructural analysis of the aberrant axoneme morphogenesis in thrips (Thysanoptera, Insecta). Cell Motil Cytoskelet 64:645–661

    Article  Google Scholar 

  • Phillips DM (1969) Exceptions to the prevailing pattern of tubules (9+9+2) in the sperm flagella of certain insect species. J Cell Biol 40:28–43

    Article  CAS  PubMed  Google Scholar 

  • Phillips DM (1970) Insect sperm: their structure and morphogenesis. J Cell Biol 44:243–277

    Article  CAS  PubMed  Google Scholar 

  • Phillips DM (1974) Structural variants in invertebrate sperm flagella and their relationship to motility. In: Sleigh MA (ed) Cilia and flagella. Academic, London, pp 379–402

    Google Scholar 

  • Pitnick S, Miller GT, Schneider K, Markow TA (2003) Ejaculate-female coevolution in Drosophila mojavensis. Proc R Soc Lond B 270:1507–1512

    Article  Google Scholar 

  • Pizzari T, Birkhead TR (2002) The sexually-selected sperm hypothesis: sex-biased inheritance and sexual antagonism. Biol Rev 77:183–209

    Article  CAS  PubMed  Google Scholar 

  • Pomiankowski A, Møller AP (1995) A resolution of the lek paradox. Proc R Soc Lond B 260:21–29

    Article  Google Scholar 

  • Pratt SA (1968) An electron microscope study of Nebenkern formation and differentiation in spermatids of Murgantia histrionica (Hemiptera, Pentatomidae). J Morphol 126:31–66

    Article  CAS  PubMed  Google Scholar 

  • Roff DA (2008) Comparing sire and dam estimates of heritability: jackknife and likelihood approaches. Heredity 100:32–38

    Article  CAS  PubMed  Google Scholar 

  • Simmons LW, García-González F (2008) Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung beetles. Evolution 62:2580–2591

    Article  PubMed  Google Scholar 

  • Simmons LW, Kotiaho JS (2002) Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution 56:1622–1631

    PubMed  Google Scholar 

  • Simmons LW, Kotiaho JS (2007) Quantitative genetic correlation between trait and preference supports a sexually selected sperm process. Proc Natl Acad Sci U S A 104:16604–16608

    Article  CAS  PubMed  Google Scholar 

  • Simmons LW, Moore AJ (2009) Evolutionary quantitative genetics of sperm. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: an evolutionary perspective. Academic, London, pp 405–434

    Google Scholar 

  • Simmons LW, Emlen DJ, Tomkins JL (2007) Sperm competition games between sneaks and guards: a comparative analysis using dimorphic male beetles. Evolution 61:2684–2692

    Article  PubMed  Google Scholar 

  • Simmons LW, House CM, Hunt J, García-González F (2009) Evolutionary response to sexual selection in male genital morphology. Curr Biol 19:1442–1446

    Article  CAS  PubMed  Google Scholar 

  • Taylor VA (1982) The giant sperm of a minute beetle. Tissue Cell 14:113–123

    Article  CAS  PubMed  Google Scholar 

  • Tourmente M, Gomendio M, Roldan ERS, Giojalas LC, Chiaraviglio M (2009) Sperm competition and reproductive mode influence sperm dimensions and structure among snakes. Evolution 63:2513–2524

    Article  PubMed  Google Scholar 

  • Werner G (1965) Untersuchungen über die Spermiogenese beim Sandläufer. Cicindela campestris L Z Zellforsch 66:255–275

    Article  CAS  Google Scholar 

  • Werner G (1976) Entwicklung und Bau der Doppelspermien bei den Dytisciden Acilius sulcatus L., Dytiscus marginalis L. und Hydaticus transversalis Pont. (Coleoptera). Zoomorphologie 83:49–87

    Article  Google Scholar 

  • Werner M, Simmons LW (2008) Insect sperm motility. Biol Rev 83:191–208

    Article  PubMed  Google Scholar 

  • Werner M, Zissler D, Peschke K (1999) Structure and energy pathways of spermatozoa of the rove beetle Aleochara bilineata (Coleoptera, Staphylinidae). Tissue Cell 31:413–420

    Article  CAS  PubMed  Google Scholar 

  • Werner M, Böminghaus A, Zissler D, Peschke K (2001) Comparison of sperm structure and motility between Aleochara tristis and A. clavicornis (Coleoptera, Staphylinidae). Zoology 104(suppl IV):44

    Google Scholar 

  • Werner M, Tscheulin T, Speck T, Zissler D, Peschke K (2002) Ultrastructure and motility pattern of the spermatozoa of Aleochara curtula (Coleoptera, Staphylinidae). Arth Struct Dev 31:243–254

    Article  Google Scholar 

  • Werner M, Gack C, Speck T, Peschke K (2007) Queue up, please! Spermathecal filling in the rove beetle Drusilla canaliculata (Coleoptera, Staphylinidae). Naturwissenschaften 94:837–841

    Article  CAS  PubMed  Google Scholar 

  • West-Eberhard MJ (1983) Sexual selection, social competition, and speciation. Quart Rev Biol 58:155–183

    Article  Google Scholar 

  • West-Eberhard MJ (1984) Sexual selection, competitive communication and species-specific signals in insects. In: Lewis T (ed) Insect communication. Academic, London, pp 283–324

    Google Scholar 

  • Yasuzumi G, Sugioka T, Tsubo I, Yasuzumi F, Matano Y (1970) Spermatogenesis in animals as revealed by electron microscopy. XX Relationship between chromatoid bodies and centriole adjunct in spermatids of grasshopper, Acrida lata. Z Zellforsch 110:231–242

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Minitube, Australia, for the kind donation of the boar semen extender. This research was supported by the Australian Research Council and the West Australian Centres of Excellence in Science and Innovation Program. We acknowledge the facilities, scientific and technical assistance of the Australian Microscopy and Microanalysis Research Facility at the Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, a facility funded by The University, State and Commonwealth Governments.

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  1. Centre for Evolutionary Biology, School of Animal Biology (M092), The University of Western Australia, Crawley, WA, 6009, Australia

    Michael Werner & Leigh W. Simmons

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  1. Michael Werner
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Correspondence to Leigh W. Simmons.

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Werner, M., Simmons, L.W. Ultrastructure of spermatozoa of Onthophagus taurus (Coleoptera, Scarabaeidae) exhibits heritable variation. Naturwissenschaften 98, 213–223 (2011). https://doi.org/10.1007/s00114-011-0763-6

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