Traumatic insemination and female counter-adaption in Strepsiptera (Insecta)

Miriam Peinert, Rolf G. Beutel and Hans Pohl

Institut für Spezielle Zoologie und Evolutionsbiologie mit Phyletischem Museum, Entomology Group, FSU Jena, Erbertstrasse 1, 07743 Jena. Email: [email protected]

Introduction Even though Strepsiptera are known since 1793 (Rossi) the first definite proof of their sexual reproduction has been presented by Schrader in 1924. This is mostly due to the unique and enigmatic lifestyle of Strepsiptera, which makes them difficult to collect and to keep in culture. The reproductive biology is strongly influenced by the extreme sexual dimorphism in all known strepsipterans. A highly unusual character complex is the complete loss of the typi- male cal elements of the female genital apparatus, i.e. of the oviposi- tor, vagina, receptaculum seminis, genital chamber, bursa copu- latrix, accessory glands and ovarioles, with eggs floating freely in the hemolymph. The ancestral females of Mengenillidae are free- living but immobilized, whereas those of Stylopidia (ca. 95 % of all species) are permanently endoparasitic. In contrast, males are able to fly right after hatching. Combined with specialized eyes and antennae this allows them to find females within a few hours and to copulate.

Fig 1. Schematic mediosagittal section of a female Strepsiptera showing the possible modes of copulation. Blue = traumatic insemination (hypothesis 1) and red = Usage of the brood canal system (hypothesis 2).

Currently two hypotheses on the copulatory mode exist (Fig. 1): 1. Traumatic insemination: The penis penetrates the body wall of the female and the sperm is inserted directly into the hemo- coel. 2. Usage of the brood canal system: The penis is inserted in the brood canal and the spermatozoa reach the body cavity of the female by moving along the brood canal and birth organs. Several authors addressed this issue with different methodologi- cal approaches. Silvestri (1943) described a traumatic insemina- tion in Mengenillidae based on observations in the laboratory. Lauterbach (1954) did not find spermatozoa in the brood canal host and birth organs using histological sections of recently mated fe- males. He observed darkly pigmented chitinous structures in the female brood canal of females of Stylops (Stylopidae), which were exam- ined one day after copulation or later. He interpreted them as mat- ing signs and therefore concluded traumatic insemination (Fig. 3B). Using histological sections of Xenos vesparum (Xenidae) Beani et al. (2005) could not identify a penetration side and concluded A that sperm injection takes place via the brood canal system.

internal genitalia Methods & Aim of the Study of the male To clarify this issue we documented the mating of Stylops ovinae (Stylopidae) in detail. We used an integrative approach combin- ing different techniques such as video recordings of the copula, histological sections of virgin females and females fixed shortly after copulation, micro-CT scans of fixed copulae, scanning electron microscopy, and three dimensional reconstructions.

Results & Discussion We could demonstrate the presence of an invagination with thickened cuticle directly in front of the birth opening of the fe- male (Fig 3A). The male inserts his penis at this site and the apical part perforates the ventral cuticle (Fig. 2). The sperm is injected into the hemocoel of the female and reaches the oocytes via the hemolymph. The invagination is a secondary genital structure, similar to the spermalege of the common bedbug Cimex lectularius (Heteroptera).

mating sign brood canal invagination of the females egg cephalothorax penis

invagination of the females cephalothorax penetration side B

A B Fig 2.: Volume render of the copulation of S. ovinae based on micro-CT Fig. 3: Histological sections of female S. ovinae. A: Longditudinal section of the cephalothorax of the female. B: Cross section of females cephalotho- scans. A: Overview B: Sections of the male and the female to present the rax in the region of the invagination. penetration side.

References Acknowledgement Beani L., Guisti F., Mercati D., Lupetti P., Paccagnini E., Turillazzi S. & Dallai R. (2005). Mat- Schrader S. H. (1924). Reproduction in Acroschismus wheeleri. Journal of Morphology We thank Wolfgang Rutkies (Osnabrück) for the photograph of Stylops males on the ing of Xenos vesparum (Rossi) (Strepsiptera, Insecta) revisited. Journal of Morphol- 39: 157–205. abdomen of Andrena vaga. ogy 265: 291–303. Silvestri, F. (1943). Studi sugli “Strepsiptera” (lnsecta). III. Descrizione e biologia di 6 Lauterbach G. (1954). Begattung und Larvengeburt bei den Strepsipteren. Zugleich ein specie italiane di Mengenilla. Bolletino del laboratorio di zoologia generale e agraria Beitrag zur Anatomie der Stylops-Weibchen. Zeitschrift für Parasitenkunde 16: 255–297. della Facoltà Agraria in Portici, 32: 197–282.