The bedbug and traumatic insemination

Male bedbugs breach the female's cuticle during copulation and inseminate directly into the female's haemolymph (Usinger, 1966), a mode of insemination that has been shown to be potentially very costly to females (Stutt and Siva-Jothy, 2001). Since the male inserts his aedeagus directly through the female's abdominal cuticle and inseminates into the haemocoel, rather than use the genital tract (Carayon, 1966), any surface microbes (Reinhardt et al., 2005) will be introduced directly into the body cavity. Moreover, this will occur with the simultaneous introduction of a large number of sperm, another form of non-self as far as the female's immune system is concerned. Reinhardt et al. (2003) experimentally revealed that the septic consequences of traumatic insemination formed a large part of the cost base identified by Stutt and Siva-Jothy (2001). Interestingly, male bedbugs direct their mating efforts at females only if they have recently fed (Siva-Jothy, 2006), probably because females cannot prevent mating when engorged with blood (Reinhardt et al, 2009). Nonetheless, mating is so frequent and tightly linked to feeding (Reinhardt and Siva-Jothy, 2007) that mating should be readily predictable when the female leaves her refugium to feed. As might be expected with such a potentially harmful male mating tactic the females have responded in a unique way. Female bedbugs have evolved a discrete immune organ that lies under the cuticle at the place where the male traumatically inseminates (Carayon, 1966). This organ is full of haemocytes (Klein and Kallenborn, 2000) and shows humoral immune activity (M.T. Siva-Jothy, personal observations) that combine to defend the female from the microbes that are introduced during traumatic insemination (Reinhardt et al., 2003). Whereas the evolution of a specialized reproductive immune organ is likely to be restricted to this reproductively unique taxon, its presence and function testifies to the immunological adaptations that can arise as a result of males breaching the female's cuticle during prolonged periods of close contact in insects. Given this predictability, and the fact that mating results in the introduction of microbial pathogens, it is likely that females may benefit from anticipating mating by upregulating antimicrobial effector systems prior to feeding, and the inevitable mating-induced immune insult that follows. Preliminary results suggests such immune anticipation of mating occurs in C. lectu-larius (M.T. Siva-Jothy et al., unpublished results). I predict that similar anticipatory upregulation of induced effector systems will occur in other insect taxa where mating is associated with immuno-logical costs to the female.

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