Age‐specific fecundity under pathogenic threat in an insect: Terminal investment versus reproductive restraint

Abstract

1. The terminal investment hypothesis predicts that as an organism's prospects for survival decrease, through age or when exposed to a pathogenic infection, it will invest more in reproduction, which should trade-off against somatic maintenance (including immunity) and therefore future survival. Attempts to test this hypothesis have produced mixed results, which, in addition, mainly rely on the assessment of changes in reproductive effort and often overlooking its impact on somatic defences and survival. Alternatively, animals may restrain current reproduction to sustain somatic protection, increasing the chance of surviving for additional reproductive opportunities.2. We tested both of these hypotheses in females of the yellow mealworm beetle, Tenebrio molitor, an iteroparous insect with reproductive tactics similar to that of long-lived organisms.3. To achieve this, we mimicked pathogenic bacterial infections early or late in the life of breeding females by injecting them with a suspension of inactivated Bacillus cereus, a known natural pathogen of T. molitor, and measured female age-specific fecundity, survival, body mass and immunity.4. Inconsistent with a terminal investment, females given either an early or late-life immune challenge did not exhibit reduced survival or enhance their reproductive output. Female fecundity declined with age and was reduced by the early but not the late immune challenge. Both early and late-life fecundity correlated positively with life expectancy. Finally, young and old females exhibited similar antibacterial immune responses, suggesting that they both restrained reproduction to sustain immunity. 5. Our results clearly demonstrate that age-specific reproduction of T. molitor females under pathogenic threat is inconsistent with a terminal investment. In contrast, our results instead suggest that females used a reproductive restraint strategy to sustain immunity and therefore subsequent reproductive opportunities. However, as infections were mimicked only, the fitness benefit of this reproductive restraint could not be shown.

Senescence of the immune defences and reproductive trade-offs in females of the mealworm beetle, Tenebrio molitor

“…Fecundity declines with age and as a result of an early immune challenge in young females. As previously observed in another study 25 , female fecundity decreased with age and because of the early immunological challenge, both as main effects and as a two-way interaction term (Table 1). According to the early immune challenge and age interaction term, the early immunological challenge only resulted in a reduction in female fecundity at a young age (Fig.…”

“…Previous evidence suggests that females of the mealworm beetle exhibit comparable life history tactics to those of long-lived mammals in that the cost of reproduction is reflected in future reproduction rather than survival 8,12,25 . Furthermore, an immunological challenge simulates an increased likelihood of impending www.nature.com/scientificreports/ infection-related death.…”

“…Furthermore, an immunological challenge simulates an increased likelihood of impending www.nature.com/scientificreports/ infection-related death. However, it has been demonstrated that immunological challenges administered to T. molitor females either early or late in life do not cause them to invest their remaining energy in procreation at the price of their longevity 25 . By contrast, females appear to reduce the cost of current reproduction by restraining it, possibly to gain additional subsequent reproductive opportunities later in life 8,25 .…”

“…This insect is a relatively long-lived insect species with reproductive tactics similar to those of long-lived mammals 8 , in which the cost of current reproduction compromises future reproduction without jeopardizing survival 12 . Furthermore, females exposed to an immune challenge mimicking a microbial infection had their reproductive output reduced without affecting their longevity 25 . While this result is consistent with T. molitor females' reproductive strategy, it also suggests that the cost of the immune response affects reproduction but has a limited impact on somatic defences later in life.…”

Female investment in terminal reproduction or somatic maintenance depends on infection dose

“…For example, snails that have been exposed to a castrating parasite partially compensate for their expected loss of fecundity by increasing egg laying rates [5]. Alternatively, if the danger to future reproduction is less severe, individuals may invest in somatic maintenance, as when mealworm beetles temporarily restrained their reproduction after a relatively avirulent bacterial immune challenge [6] or as when female dung beetles reduced their reproductive output after immune activation [7]. By reducing offspring production in favor of survival and immunity over the short term, individuals gain a longer potential reproductive period.…”