Ejaculate components delay reproductive senescence while elevating female reproductive rate in an insect

Abstract

Increased female reproductive rates usually result in accelerated senescence. 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.

Fig. 1.

Reproductive senescence in female bedbugs in relation to female population origin (A or B), inter- or intra-population cross, and ejaculate exposure rate (low: white background and columns; high: gray background and columns). (A) Event-history plots of individual bedbug females: Within treatment groups, females are ordered by lifespan (46). The color of the squares codes for the weekly reproductive output. The larger number of orange squares in the early weeks in the right-hand plot shows the ejaculate-mediated increased reproductive rate. The longer persistence of orange in the right hand plot and the lower number of green squares illustrates the later onset of reproductive senescence in this treatment group. (B) Parameters of reproductive senescence in female bedbugs. (Top) Egg-laying rate before senescence was higher at the high ejaculate exposure rate than a the low ejaculate exposure rate (t = 2.908, P = 0.004) but did not differ with inter- or intra-population cross (t = 0.697, P = 0.45). The effect of female population did not reach significance (t = −1.923, P = 0.06). No interaction was significant. (Middle) The onset of senescence was delayed by 11.4% in females with a high ejaculate exposure rate compared with females with a low ejaculate exposure rate (t = 2.459, P = 0.015), but there was no effect of female population (t = 1.261, P = 0.3), or inter- or intra-population cross (t = 0.145, P > 0.5). (Bottom) The total number of fertile eggs per female, a close fitness measurement (21), was significantly higher in females in the high ejaculate exposure rate arm (t = 2.963, P = 0.004) and also was influenced by the interaction of female population and by inter- versus intra-population cross (t = 2.115, P = 0.04).