The cimicids, or bed bugs, belong to a highly specialized hematophagous taxon that parasitizes primarily humans, birds, and bats. Their best-known member is the bed bug, Cimex lectularius. This group demonstrates some bizarre but evolutionarily important biology. All members of the family Cimicidae show traumatic insemination and a suite of female adaptations to this male trait. Cimicids therefore constitute an ideal model system for examining the extreme causes and consequences of sexual selection. Our dual goal in re-examining the extensive literature on this group is to identify issues relevant to pest control, such as dispersal ecology and the recent global spread, and to understand the selective forces that have shaped the unique aspects of this insect's biology.

The frequent wounding of female bedbugs (Cimex lectularius: Cimicidae) during copulation has been shown to decrease their fitness, but how females have responded to this cost in evolutionary terms is unclear. The evolution of a unique anatomical structure found in female bedbugs, the spermalege, into which the male's intromittent organ passes during traumatic insemination, is a possible counteradaptation to harmful male traits. Several functions have been proposed for this organ, and we test two hypotheses related to its role in sexual conflict. We examine the hypotheses that the spermalege functions to (i) defend against pathogens introduced during traumatic insemination; and (ii) reduce the costs of wound healing during traumatic insemination. Our results support the ‘defence against pathogens’ hypothesis, suggesting that the evolution of this unique cimicid organ resulted, at least partly, from selection to reduce the costs of mating-associated infection. We found no evidence that the spermalege reduces the costs of wound healing.

Animal breeding research, reproductive biology, and cellular biogerontology show that fertilization rates and zygote viability critically depend on sperm age. Sexual selection research focuses on differences between male genotypes in sperm performance, such as motility, competitive ability, or compatibility with eggs, but without considering sperm age. A combined view (that the thermodynamically inevitable decline in sperm performance selects for traits in diploid individuals to prevent fertilization with aged sperm) has received very little attention. In this paper, I correct this bias and show that many male and female traits affect sperm aging or the sperm age distribution at any reproductive event. Such traits coincide well with condition-dependent traits considered sexually selected: multiple mating by both sexes, high sperm production rates, the delivery of dense ejaculates containing many sperm (including nonfertilizing types), the packaging of sperm into spermatophores, male and female sperm ejection, sexual coercion, as well as the production of showy antioxidants and various cellular and nuclear repair mechanisms. I conclude that altering the sperm age distribution at any step during reproduction can be an origin of sexually selected traits, and may explain presently observed paternity variation without assuming genetic incompatibility of gametes.

Using basic ecological concepts, we introduce sperm ecology as a framework to study sperm cells. First, we describe environmental effects on sperm and conclude that evolutionary and ecological research should not neglect the overwhelming evidence presented here (both in external and internal fertilizers and in terrestrial and aquatic habitats) that sperm function is altered by many environments, including the male environment. Second, we determine that the evidence for sperm phenotypic plasticity is overwhelming. Third, we find that genotype-by-environment interaction effects on sperm function exist, but their general adaptive significance (e.g., local adaptation) awaits further research. It remains unresolved whether sperm diversification occurs by natural selection acting on sperm function or by selection on male and female microenvironments that enable optimal plastic performance of sperm (sperm niches). Environmental effects reduce fitness predictability under sperm competition, predict species distributions under global change, explain adaptive behavior, and highlight the role of natural selection in behavioral ecology and reproductive medicine.