Subtle effect of Xenos vesparum (Xenidae, Strepsiptera) on the reproductive apparatus of its male host: Parasite or parasitoid?
The present study documents the pace of accessory gland and testes degeneration in the wasp Vespula vulgaris by means of a histological and metric approach, that has not been carried out for social wasps so far. To a certain extent, comparison is made with the degenerative processes of the mucus glands of the honeybee drone. In V. vulgaris, no generative tissue is left by the end of 9 d of age, and so degeneration is a fast process. The three different parts of the accessory glands (muscle layer, gland epithelium, and lumen) change with respect to age. The secretory cells of the epithelium reach their maximum activity during the first days of adult life, which results in a maximally filled gland lumen by 9d. We also provide, for the first time, a histological study of testes degeneration for this species. At eclosion, well-defined cystic structures are still visible, whereas at 9d, it is no longer possible to distinguish different cystic structures. The diameter of the testes decreases with respect to age. Additional key words: reproductive biology, social wasps, mating, ontogeny, male Social insects are well known for their amazing variety of exocrine glands, of which the secretions play a role in numerous aspects of colony organization (Billen & Morgan 1998). As is the case with honeybee drones, male wasps belong to the neglected gender in scientific studies, as is reflected in the few reports on their biology. However, males are also equipped with a number of exocrine glands with variable functions. Examples include sex pheromone production of the mandibular glands in a number of ant species (Hölldobler & Maschwitz 1965), the territorial scent marks from the labial glands of bumblebee males to attract conspecific females for copulation (Kullenberg et al. 1970), and mating sign formation by the secretion of the mucus glands in honeybees (Koeniger 1986, 1991). The male reproductive system consists of paired testes that are responsible for the production of sperm, which is transferred to the females during copulation. Different frommammals, sperm synthesis in males of social hymenopteran species is not continuous, as the testes degenerate before the males become sexually mature. Testes degeneration is actually a remarkable feature in social hymenopterans, although it has never been documented at the histological level in wasps. Zander (1916) and Bishop (1920) mentioned that most of the sperm was found in the seminal vesicle of adult males in honeybees. But in ants, spermatogenesis stops shortly before or after eclosion, and sperm is stored in the seminal vesicle (Forbes 1954; Hölldobler 1966; Ball & Vinson 1984). In wasps of Polistes spp., the maturation of the sperm occurs in the larval stages (Machida 1934). Generally speaking, insects sustain significant levels of sperm competition because of their tendency to keep sperm internally in their spermathecae corresponding with special storage organs (Simmons 2001). The intensity of sperm competition is determined to a considerable extent by the absolute number of different males involved in competition for the ova of a single female (Parker 1998). Genital adaptations for manipulating rival sperm or to influence the duration of copulation are only expected in polyandrous species. Also, holdfast devices associated with the male genital apparatus are to be expected only in species with polyandrous females. In most insects, the male genital system also consists of accessory glands of mesodermal or ectodermal origin, which open into the deferent or ejaculatory ducts, respectively. Among insects, the accessory glands vary notably in size, shape, number, and embryological origin (Adiyodi & Adiyodi 1975; Leopold 1976; Grassé Invertebrate Biology 128(4): 364–371. r 2009, The Author Journal compilation r 2009, The American Microscopical Society, Inc. DOI: 10.1111/j.1744-7410.2009.00178.x Author for correspondence. E-mail: firstname.lastname@example.org 1982; Chapman 1998). Among the functions of the secretions of these glands is the contribution to the seminal fluid and activation of the spermatozoa (Chen 1984; Davey 1985). The secretory cells of these male accessory glands are arranged as a monolayered epithelium and correspond with ‘‘Class-1,’’ according to the classification of Noirot & Quennedey (1974, 1991). A comparative study of the male genital apparatus of 51 bee species, excluding Apis spp., was provided by Ferreira et al. (2004). Among these, the male stingless meliponine bees were characterized by the absence of accessory glands (Dallacqua & Cruz-Landim 2003). In Apis, the accessory glands, called mucus glands, play an important role during sperm transfer (Woyke 1958; Woyke & Ruttner 1958; Koeniger et al. 1989; Koeniger & Hänel 1996). The secretion of the mucus glands, together with the cornual secretion, also contributes to the visibility of the mating sign in honeybees (Koeniger 1991; Koeniger et al. 1996; Colonello & Hartfelder 2005). Moors et al. (2005) described how the morphological structure of the mucus glands in honeybees changes with respect to age. Cruz-Landim & Dallacqua (2005) found that all the secretion of the drone accessory gland is produced before the sexual maturation of the male. They interpret this aspect as justified, because during mating the genital apparatus is lost and the drone dies. Colonello & Hartfelder (2003, 2005) focused on the male accessory gland products and their function in the reproductive biology of social bees. During the first 5 d of the mature drone, the mucus protein content increases enormously (Colonello & Hartfelder 2003). In vespine wasps, mating occurs around noon, preceded by nuptial flights of males, which frequently congregate around prominent vegetation like trees or bushes. Mating occurs mostly while the queen is supported by a substrate (ground, grass, leaves, or branches) instead of during flight (Donisthorpe 1917; Thomas 1960). At the beginning of copulation, the male mounts the queen and inserts his penis into the queen’s sting chamber. Afterwards, he releases the queen and assumes a freehanging position, supported only by their locked genitalia (Post 1980; Ross 1983). Finally, the last phase of the copulation involves reversal of the positions, like the S-position described by Schremmer (1962). Important, but so far unanswered, questions are why testes in males of Vespula spp. mature that early during development, why hooks can occur near the aedeagus tip, and why mucus glands are huge. The answer for multiple mating in those species could be linked to the fact that their window of time for mating is narrow, because males emerge late in the season when winter approaches. In male wasps, the reproductive organ is similar to most insects (El-Deeb et al. 1966). It contains a pair of testes, each linked to a median ejaculatory duct by a vas deferens, that is relatively short and leads into the large seminal vesicles. The seminal vesicles open into the base of the male accessory glands, which are probably associated with sperm maintenance or spermatophore production. Besides these structures, the male genital organ consists of a phallus (Kluge 1895). In this contribution, we report on the development of the male accessory glands and the testes degeneration during sexual maturation in the wasp Vespula vulgaris LINNAEUS 1758, which is the first histological study of testes degeneration in social wasps.