Bedbugs in Bed

Increased female reproductive rates usually result in accelerated senescence [aging]. This correlation provides a link between the evolutionary conflict of the sexes and aging when ejaculate components elevate female reproductive rates at the cost of future reproduction. It is not clear whether this female cost is manifest as shorter lifespan or an earlier onset or a steeper rate of reproductive senescence. It also is unclear whether beneficial ejaculates release females from reproductive trade-offs and, if so, which senescence parameters are affected. We examined these issues in the bedbug, Cimex lectularius, a long-lived insect that shows reduced female lifespan as well as female reproductive senescence at the male-determined mating frequency. We demonstrate experimentally that, independently of the mating frequency, females receiving more ejaculate show increased reproductive rates and enter reproductive senescence later than females receiving less ejaculate. The rate of reproductive senescence did not differ between treatments, and reproductive rates did not predict mortality. The ejaculate effects were consistent in inter- and intra-population crosses, suggesting they have not evolved recently and are not caused by inbreeding. Our results suggest that ejaculate components compensate for the costs of elevated female reproductive rates in bedbugs by delaying the onset of reproductive senescence. Ejaculate components that are beneficial to polyandrous females could have arisen because male traits that protect the ejaculate have positive pleiotropic effects and/or because female counteradaptations to antagonistic male traits exceed the neutralization of those traits. That males influence female reproductive senescence has important consequences for trade-offs between reproduction and longevity and for studies of somatic senescence. ¹

In polyandrous species, the male optimum for an interacting phenotype is likely to be different from the female's, potentially resulting in an “evolutionary conflict between the individuals of the two sexes” (sexual conflict). ²

During reproduction many interacting phenotypes occur, and sexual conflict may arise from any of these interactions, e.g, the timing or duration of mating, the re-mating rate, the female egg-laying rate, and/or offspring performance. Whenever an interacting phenotype results in net mating costs to one sex, the conflict can be resolved by trade-offs in resource allocations; these trade-offs, in turn, will disturb the existing equilibrium formed by the correlations between other interacting phenotypes. Thus, even if there are no current mating costs to females, there still may be a mosaic of coexisting interacting phenotypes that are, when measured in isolation, costly, neutral, or beneficial to one sex. ³

… several studies have found ejaculate components to be beneficial in several aspects of female reproduction, but it is not known whether such benefits evolved via sexual conflict (e.g., 4, 6, 22) or by traditional female choice. For example, females may have evolved the ability to metabolize manipulative ejaculate substances, or they may choose males that provide the largest direct benefits (e.g., nuptial gifts). In the former case, the metabolism of manipulative substances may be costly initially and so result in trade-offs in females; in the latter case, one would not necessarily expect trade-offs. ⁴

… the ejaculates of C. lectularius have been found to contain antioxidant and antibacterial activity as well as essential amino acids. These substances all have potential fitness benefits for females. ⁵

Candidate traits for the reduction of somatic damage and/or trade-off release are immune effectors, antioxidants, stress-defense substances, and micronutrients in the seminal fluid. Representatives of all 4 types of compound have been found among the >100 components in the semen of bedbugs. ⁶

We did not find the trade-offs predicted by life-history theory and evolutionary models of aging, because increased reproductive rates early in life did not result in earlier reproductive senescence. It is possible that ejaculate components either directly reduce aging damage in the female or release females from trade-offs. ⁷

In conclusion, our data show an important male effect on female fitness and aging patterns and demonstrate that beneficial male postcopulatory traits can evolve alongside harmful male traits. ⁸

That male traits evolve which are beneficial to females may seem surprising in a species that has a high mating frequency that is controlled by males and has last-male sperm precedence: Any newly evolving beneficial ejaculate substance favors competing males that mate subsequently. We envisage 2 possible routes by which such beneficial male effects may have arisen. First, ejaculate traits originally may have had a negative effect on females, as is currently observed for some Drosophila proteins. Consequently, female traits, such as the ability to metabolize ejaculate substances, may be selected for in females. Although the evolution of such female counteradaptations currently is believed merely to neutralize male harm, it may have progressed in bedbugs to benefit females. Alternatively, it is possible that male–male competition does not always have negative side effects on females (pleiotropic sexual antagonism). Instead it may result in male traits that evolved to protect the ejaculate (ejaculate defense traits) having a positive pleiotropic effect on the female such as the antioxidant and the antibacterial activity found in bedbug ejaculates. ⁹