The unusual life style of Strepsiptera has presented a long-standing puzzle in establishing its affinity to other insects. Although Strepsiptera share few structural similarities with other insect orders, all members of this order share a parasitic life style with members of two distinctive families in the Coleoptera—the order now considered the most closely related to Strepsiptera based on recent genomic evidence. Among the structural features of several strepsipteran families and other insect families that have been surveyed are the organization of testes and ultrastructure of sperm cells. For comparison with existing information on insect sperm structure, this manuscript presents a description of testes and sperm of a representative of the most primitive extant strepsipteran family Mengenillidae, Eoxenos laboulbenei. We compare sperm structure of E. laboulbenei from this family with that of the three other families of Strepsiptera in the other strepsipteran suborder Stylopidia that have been studied as well as with members of the beetle families Meloidae and Rhipiphoridae that share similar life histories with Strepsiptera. Meloids, Rhipiphorids and Strepsipterans all begin larval life as active and viviparous first instar larvae. This study examines global features of these insects’ sperm cells along with specific ultrastructural features of their organelles.
References
[1]
Dallai, R.; Beani, L.; Kathirithamby, J.; Lupetti, P.; Afzelius, B.A. New findings on sperm ultrastructure of Xenos vesparum (Rossi) (Strepsiptera, Insecta). Tissue Cell 2003, 35, 19–27, doi:10.1016/S0040-8166(02)00099-X.
[2]
Jamieson, B.G.M. The Ultrastructure and Phylogeny of Insect Spermatozoa; Cambridge University Press: Cambridge, UK, 2011.
[3]
Kinzelbach, R.K. Morphologische Befunde an F？cherflüglern und ihre phylogenetische Bedentung Insecta: Strepsiptera; Schwerzerbartsche: Stuttgart, Germany, 1971; p. 256.
[4]
Kathirithamby, J. Host-parasitoid associations in Strepsiptera. Annu. Rev. Ent. 2009, 54, 227–249, doi:10.1146/annurev.ento.54.110807.090525.
[5]
McMahon, D.P.; Hayward, A.; Kathirithamby, J. The first molecular phylogeny of Strepsiptera (Insecta) reveals an early burst of molecular evolution correlated with the transition to endoparasitism. PLoS One 2011, 6, 1–7.
[6]
McKenna, D.D.; Farrell, B.D. 9-genes reinforce the phylogeny of holometabola and yield alternative views on the phylogenetic placement of Strepsiptera. PLoS One 2010, 5, e11887, doi:10.1371/journal.pone.0011887.
[7]
Niehuls, O.; Hartig, G.; Grath, S.; Pohl, H.; Lehmann, J.; Tafer, H.; Donath, A.; Krauss, V.; Eisenhardt, C.; Hertel, J.; et al. Genomic and morphological evidence converge to resolve the enigma of Strepsiptera. Curr. Biol. 2012, 22, 1–5.
[8]
B？ving, A.G.; Craighead, F.C. An illustrated synopsis of the principal larval forms of the order Coleoptera. Entomol. Am. 1931, 11, 1–351.
[9]
Kathirithamby, J. Review of the order Strepsiptera. Syst. Entomol. 1989, 14, 41–92, doi:10.1111/j.1365-3113.1989.tb00265.x.
[10]
Kinzelbach, R.K.; Pohl, H. Ordnung Strepsiptera, F？cherflüger. In Wirbellose Tiere. 5. Teil: Insecta; Dathe, H.H., Ed.; Spektrum Akademischer Verlag: Berlin, Heidelberg, Germany, 2003; pp. 526–539.
[11]
Afzelius, B.A.; Dallai, R. Characteristics of the flagellar axoneme in Neuroptera, Coleoptera and Strepsiptera. J. Morph. 1994, 219, 15–20, doi:10.1002/jmor.1052190104.
[12]
Heming, B.S. Insect Development and Evolution; Cornell University Press: Ithaca, NY, USA, 2003; pp. 6–28.
[13]
Carcupino, M.; Mazzini, M.; Olmi, M.; Kathirithamby, J. The spermatozoon of Halictophagus chilensis Hofmann (Strepsiptera, Halictophagidae). Boll. Zool. 1993, 60, 361–365, doi:10.1080/11250009309355840.
[14]
Kathirithamby, J.; Carcupino, M.; Mazzini, M. Comparative spermatology of four species of Strepsiptera and comparison with a species of primitive Coleoptera (Rhipiphoridae). Int. J. Insect Morph. Embryol. 1993, 22, 459–470, doi:10.1016/0020-7322(93)90024-U.
[15]
Jamieson, B.G.M.; Dallai, R.; Afzelius, B.A. Insects: Their Spermatozoa and Phylogeny; Science Publishers: Enfield, NH, USA, 1999.
[16]
Mazzini, M.; Carcupino, M.; Kathirithamby, J. Fine structure of the spermatozoon of the Strepsipteran Xenos moutoni. Tissue Cell 1991, 23, 199–207, doi:10.1016/0040-8166(91)90074-4.
[17]
Carcupino, M.; Profili, G.; Kathirithamby, J.; Mazzini, M. Sperm ultrastructure of Xenos vesparum (Rossi) and its significance in the taxonomy and phylogeny of Strepsiptera (Insecta). Advances in spermatozoal phylogeny and taxonomy. In Mémoires du Muséum National d’Histoire Naturelle; Jamieson, B.G.M., Ausio, J., Justine, J.-L., Eds.; G. Dufour: Paris, France, 1995; Volume 166, pp. 291–296.
[18]
Kathirithamby, J.; Carcupino, M.; Mazzini, M. Ultrastructure of the spermatozoon of Elenchus japonicus and its bearing on the phylogeny of Strepsiptera. Tissue Cell 1992, 24, 437–442, doi:10.1016/0040-8166(92)90059-G.
[19]
Beani, L.; Giusti, F.; Mercati, D.; Lupetti, P.; Paccagnini, E.; Turillazzi, S.; Dallai, R. Mating of Xenos vesparum (Rossi) (Strepsiptera, Insecta) revisited. J. Morph. 2005, 265, 291–303, doi:10.1002/jmor.10359.
[20]
Silvestri, F. Studi sugli “Strepsiptera” (Insecta). III. Descrizione e biologia di 6 specie italiane di Mengenilla. Boll. Lab. Zool. Gen. Agric. Portici. 1943, 32, 197–282.
[21]
Kathirithamby, J. Morphology of the female Myrmecolacidae (Strepsiptera) including the apron, and an associated structure analogous to the peritrophic matrix. Zool. J. Linn. Soc. 2000, 128, 269–287, doi:10.1111/j.1096-3642.2000.tb00164.x.
[22]
Whiting, M.F.; Carpenter, J.C.; Wheeler, Q.D.; Wheeler, W.C. The Strepsiptera problem: Phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Syst. Biol. 1997, 46, 1–68.
[23]
Ishiwata, K.; Sasaki, G.; Ogawa, J.; Miyata, T.; Su, Z.-H. Phylogenetic relationships among insect orders on three nuclear-coding gene sequences. Mol. Phylogenet. Evol. 2011, 58, 169–180, doi:10.1016/j.ympev.2010.11.001.
[24]
Friedrich, F.; Beutel, R.G. Goodbye Halteria? The thoracic morphology of Endopterygota (Insecta) and its phylogenetic implications. Cladistics 2010, 26, 1–34, doi:10.1111/j.1096-0031.2009.00297.x.
[25]
Longhorn, S.J.; Pohl, H.; Vogler, A.P. Ribosomal protein genes of holometabolan insects reject the Halteria, instead revealing a close affinity of Strepsiptera with Coleoptera. Mol. Phylogenet. Evol. 2010, 55, 846–850, doi:10.1016/j.ympev.2010.03.024.
[26]
Wiegmann, B.M.; Trautwein, M.D.; Kim, J.-W.; Cassel, B.K.; Bertone, M.A.; Winterton, S.L.; Yeates, D.K. Single-copy nuclear genes resolve the phylogeny of the holometabolous insects. BMC Biol. 2009, 7, 34, doi:10.1186/1741-7007-7-34.
[27]
Hayward, D.C.; Truman, J.W.H.; Bastiani, M.J.; Ball, E.E. The structure of the USP/PXR of Xenos pecki indicates that Strepsiptera are not closely related to Diptera. Dev. Genes Evol. 2005, 215, 213–219, doi:10.1007/s00427-004-0461-x.
[28]
Rokas, A.; Kathirithamby, J.; Holland, P.W.H. Intron insertion as a phylogenetic character: The engrailed homeobox of Strepsiptera does not indicate affinity with Diptera. Insect Mol. Biol. 1999, 8, 527–530, doi:10.1046/j.1365-2583.1999.00149.x.
