Abstract
During mating, male bed bugs (Cimicidae) pierce the female abdomen to inject sperm using their needle-like genitalia. Females evolved specialized paragenital organs (the spermalege and associated structures) to receive traumatically injected ejaculates. In Leptocimex duplicatus, the spermalege is duplicated, but the evolutionary significance of this is unclear. In Cimex hemipterus and C. lectularius, in which females normally develop a single spermalege on the right side of the abdomen, similar duplication sometimes occurs. Using these aberrant morphs (D-females) of C. hemipterus, we tested the hypothesis that both of the duplicated spermaleges are functionally competent. Scars on female abdominal exoskeletons indicated frequent misdirected piercing by male genitalia. However, the piercing sites showed a highly biased distribution towards the right side of the female body. A mating experiment showed that when the normal insemination site (the right-side spermalege) was artificially covered, females remained unfertilized. This was true even when females also had a spermalege on the left side (D-females). This result was attributed to handedness in male mating behavior. Irrespective of the observed disuse of the left-side spermalege by males for insemination, histological examination failed to detect any differences between the right-side and left-side spermaleges. Moreover, an artificial insemination experiment confirmed that spermatozoa injected into the left-side spermalege show apparently normal migration behavior to the female reproductive organs, indicating an evolutionary potential for functionally-competent duplicated spermaleges. We discuss possible mechanisms for the evolutionary maintenance of D-females and propose a plausible route to the functionally-competent duplicated spermaleges observed in L. duplicatus.
Highlights
In several animal groups with internal fertilization, females incur wounds from the male intromittent organ piercing the reproductive tract wall or the body wall, with the wound functioning as an entrance for the male ejaculate
Variation in Genitalia and Misdirected Mating Wounds rare, we found a total of 15 D-females, which had the paragenital sinuses on both the right and left sides of the 5th abdominal sternite (Fig. 1D)
Irrespective of the similarity in the histology and spermevacuation process observed in the artificial insemination (AI) experiment between the normal right-side spermaleges and duplicated left-side ones, we detected no sign that the latter is used by males for insemination
Summary
In several animal groups with internal fertilization, females incur wounds from the male intromittent organ piercing the reproductive tract wall or the body wall, with the wound functioning as an entrance for the male ejaculate Such a bizarre mode of sperm transfer, termed traumatic insemination (hereafter, TI), is rare but has evolved multiple times independently, with examples from various animal taxa such as insects, spiders, and flatworms [1,2]. In Primicimex cavernis Baber, Carayon [8] found that many females incurred scars scattered across a wide area of the dorsal side of the abdomen, that were indicative of punctures caused by the male intromittent organs (i.e., they were ‘traces of copulation’) In this species, sperm are directly injected into the female hemocoel and swim to the sperm storage organs, termed seminal conceptacles, that are located at the base of the common oviduct.
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