Functional morphology of the female reproductive apparatus of Stephanitis pyrioides (Heteroptera, Tingidae): a novel role for the pseudospermathecae

At mating, female insects generally receive and store sperm in specific organs of their reproductive tract called spermathecae. Some Heteroptera, such as Cimicomorpha, lack a true spermatheca; some have receptacles of novel formation where sperm cells can transit or be stored. In Tingidae, there are two sac-like diverticula, the "pseudospermathecae," each at the base of a lateral oviduct, which previously were considered to function as spermathecae. However, this role has never been documented, either by ultrastructural studies or by observations of sperm transit in the female reproductive tract. In this article, we investigate the morphology and the ultrastructure of the female reproductive apparatus in the economically important tingid species Stephanitis pyrioides, focusing our attention on the functional role of the pseudospermathecae in an evolutionary perspective. Each ovary consists of seven telotrophic meroistic ovarioles, the long pedicels of which enlarge into a bulb-like structure near the terminal oocyte. The ovarioles flow into two long lateral oviducts, which join to form a very short common oviduct. Basally, each lateral oviduct is connected through a short duct to one of two pseudospermathecae. The ultrastructure of the ectodermal epithelium of the pseudospermathecae is dramatically different in sexually immature or mated females. In virgin females, cells delimit a very irregular lumen, filled with a moderately electron-dense granular material. The large nucleus adapts to their irregular shape, which can have long projections in some regions and be flattened in others. After mating, epithelial cells generally elongate and display an apical layer of microvilli extending beneath the cuticle, often containing mitochondria. In the lumen of the pseudospermathecae there is a dense brownish secretion. No sperm cells were ever found inside this organ. After mating, sperm move upward along the lateral oviducts and the ovarioles, accumulating in the bulb-like structure of the pedicels, and proceeding into the distal region between the follicle cells surrounding the oocyte and the ovariole wall. The egg, most likely fertilized in the bulb-like region of the ovariole, moves through the lateral oviduct, entirely enters the pseudospermatheca and is smeared with its secretion just before oviposition. We exclude a function of sperm storage for the pseudospermathecae, and instead suggest a novel role for these organs as reproductive accessory glands