Damage limitation

Female bedbugs don't take traumatic insemination lying down

Stuart Blackman(stuart.blackman@talk21.com)
Sep 30, 2003

Where there are conflicts of interests there often are evolutionary arms races, an escalation of adaptation. Though well documented between predators and prey (and hostile world powers), arms races have proved difficult to pin down when it comes to another area of life, which theory tells us should be rife with conflicts of interests. But, according to two papers in the Proceedings of the Royal Society of London B, just such a conflict of sexual interests has driven an arms race between male and female bedbugs that has led to the evolution of a unique organ.

The respective interests of prospective mates can conflict with many aspects of reproduction—whether to mate at all, for example, or how many offspring to have. "When the conflict is overt and behavioral, it's much easier to pick up on—like the kind of interaction between predator and prey," said evolutionary biologist Rufus Johnstone of the University of Cambridge. "But a lot of [sexual] conflict goes on once mating has occurred—conflict over fertilization of the egg, for example, or how long [a female] waits before remating. These are much more subtle things to pick up on."

The conflict of interests that occurs between male and female human bedbugs Cimex lectularius is far from subtle, however. Although females have a fully formed reproductive tract through which they lay eggs, they don't use it for copulation. Instead, a male penetrates a female's abdomen with a sharp, intromittent organ called a paramere, and injects his sperm directly into her body cavity, from where they migrate to her ovaries. So-called extragenital traumatic insemination visibly scars females, and a high mating frequency reduces a female's lifespan.

But females have responded with a counteradaptation of their own, described independently by Edward Morrow and Göran Arnqvist from the University of Uppsala and Klaus Reinhardt and colleagues from the University of Sheffield. Both teams studied a structure called a spermalege situated on a female's right flank, where she is most frequently penetrated. It consists of a groove in the outer cuticle that guides the male's paramere through the cuticle into an underlying membrane-bound sac rich in haemocytes.

Morrow and Arnqvist simulated inseminations using needles of similar dimensions to the male's paramere and observed that, compared with females pierced routinely through the spermalege, those pierced in the equivalent area on the left flank died younger and produced half as many eggs (Proceedings of the Royal Society of London B, DOI:10.1098/rspb.2003.25154, September 10, 2003).

Reinhardt et al. also simulated inseminations with a needle and observed a similar effect, but only when using needles that had been contaminated with a culture of bedbug-derived bacteria (Proceedings of the Royal Society of London B, DOI:10.1098/rspb.2003.2515, September 26, 2003).

A role for the spermalege in mitigating the dangers of traumatic insemination seems likely, but how it achieves this is less clear. While Reinhardt et al.'s experiments suggest a role for the spermalege in the control of pathogens introduced during insemination, Morrow and Arnqvist found no effect from needle contamination, which likely reflects a difference between the studies in the degree of experimental contamination. But Morrow and Arnqvist's finding that the spermalege provides protection even without a risk of contamination suggests that the spermalege might also better absorb repeated physical trauma.

Morrow notes that this discrepancy between the studies might reflect a higher background mating rate in his own experiments compared with those of Reinhardt et al. "Females in our experiment were probably 'suffering' more," said Morrow, "so any extra imposed costs… may result in a much more noticeable effect."

But both teams are pleased with the degree of agreement between the papers, which are, said Siva-Jothy, a coauthor of the Reinhardt et al. paper, "as compatible as I would expect them to be, given that we've gone about it in a slightly different way." Together they are "a good, dramatic illustration of this process of adaptation and counteradaptation going on in nature," concludes Johnstone.

Meanwhile, the reason why male bedbugs should have adopted such an unusual insemination technique in the first place remains a mystery. Morrow and Siva-Jothy both look forward to the completion of a molecular phylogeny of the bedbug family (Cimicidae), for clues to how this extragenital system has developed from ancestors with a more conventional sex life.