Binucleation of male accessory gland cells in the common bed bug Cimex lectularius

Abstract

The insect male accessory gland (MAG) is an internal reproductive organ responsible for the synthesis and secretion of seminal fluid components, which play a pivotal role in the male reproductive strategy. In many species of insects, the effective ejaculation of the MAG products is essential for male reproduction. For this purpose, the fruit fly Drosophila has evolved binucleation in the MAG cells, which causes high plasticity of the glandular epithelium, leading to an increase in the volume of seminal fluid that is ejaculated. However, such a binucleation strategy has only been sporadically observed in Dipteran insects, including fruit flies. Here, we report the discovery of binucleation in the MAG of the common bed bug, Cimex lectularius , which belongs to hemimetabolous Hemiptera phylogenetically distant from holometabolous Diptera. In Cimex , the cell morphology and timing of synchrony during binucleation are quite different from those of Drosophila . Additionally, in Drosophila , the position of the two nuclei in the adult stage changes as a result of the mating history or the nutrient conditions; however, it remains stable in Cimex . These differences suggest that binucleation in the Cimex MAG plays a unique role in the male reproductive system that is distinct from that of Drosophila .

Morphological and Developmental Traits of the Binucleation of Male Accessory Gland Cells in the Benthic Water Bug, Aphelocheirus vittatus (Hemiptera: Aphelochiridae)

“…We also noticed that after enough feeding, the angles of the lines connecting the two nuclei seemed to be neatly aligned with respect to the PD axis of the tubular shape of the MAGs ( Fig. 3A ), as previously observed in the mesadenial gland of C. lectularius ( Takeda et al 2019 ). Thus, we measured and analyzed these planar angles in 338 epithelial cells of the MAGs.…”

“…At this time, however, an optical longitudinal section of the confocal image showed the apicobasally overlaid positioning of two nuclei ( Fig. 2A ’’) as seen in the nonfeeding state of the fruit fly, Drosophila pseudoobscura ( Takeda et al 2019 ). We then observed the MAG epithelium from an adult at approximately 1 mo after feeding, which induced a drastic growth in the volume of MAGs ( Fig.…”

“…All cells of both cell types are binucleate. The two nuclei change their apicobasal position from vertical to horizontal with respect to the epithelial plane, leading to higher plasticity in the apical area of each cell in order to generate a larger volume of ejaculate ( Taniguchi et al 2012 , 2018 ; Takeda et al 2019 ).…”

“…Despite the merits of cell binucleation in the MAG epithelium for increasing reproductive success, only a few insect taxa other than Drosophila , such as tephritid fruit flies ( Ceratitis capitata [ Marchini et al 2003 ] and Bactrocera tryoni [ Radhakrishnan et al 2009 ]) and cimicid bed bugs ( Cimex lectularius and Cimex hemipterus ; Takeda et al 2019 ), are known to have binucleated cells in their MAG epithelia. Furthermore, in the Cimex accessory gland, which is composed of two organs, the mesadenial gland for production and the mesadenial reservoir for storage, the apicobasal position of the two nuclei is always horizontal to the epithelial plane and does not respond to nutrient intake ( Takeda et al 2019 ). Instead, binucleation was predicted to contribute to forming the proper morphology of each organ; that is, the elongated shape of the binucleate cells is aligned unidirectionally to form the tubular shape of the mesadenial gland, whereas the cell shape is aligned omnidirectionally to form the spherical shape of the mesadenial reservoir.…”

“…Instead, binucleation was predicted to contribute to forming the proper morphology of each organ; that is, the elongated shape of the binucleate cells is aligned unidirectionally to form the tubular shape of the mesadenial gland, whereas the cell shape is aligned omnidirectionally to form the spherical shape of the mesadenial reservoir. Additionally, in the case of the MAG of D. melanogaster , elongated binucleated cells are aligned unidirectionally among the main cells, but not in the secondary cells in local views, whereas they are placed more randomly in global views to form the weakly swollen tubular sac of the MAG of this species ( Takeda et al 2019 ).…”