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

Abstract

In the theory of ageing, it has been assumed that ageing is associated with a decline in somatic defences, including the immune system, as a consequence of a trade-off with reproduction. While overall immunity suffers from age-related deterioration (immune senescence), the different components of the immune response appear to age differently. It is also likely that investment among the many arms of the immune system and reproduction with age is finely adjusted to the organisms' reproductive strategy. We investigated this possibility in females of Tenebrio molitor, a species of long-lived insect with reproductive strategies similar to those of long-lived mammals. We specifically tested the effects of immunological challenges imposed early or late in adult life on immune pathway activation as well as fertility early and late in life. We found complex patterns of changes in immune defences with age and age-specific immune challenges with contrasted relationships with female reproduction. While cellular and enzymatic defences showed signs of ageing, they did not trade-off with reproduction. By contrast, the induced antibacterial immune response was found to be unaffected by age and to be highly connected to female fecundity. These findings suggest that these immunological pathways have different functions with regard to female ageing in this insect species.

Figure 1

The experimental protocol used to study the effect of an age-specific immune challenge on the immune defences and reproduction of females of the mealworm beetle (Tenebrio molitor).

Figure 2

Mean number of eggs (± s.e.) produced by females early in life (young: between day 10 and day 30 post eclosion) and late in life (old: between day 40 and day 60 post eclosion) as function of their life time immune treatment: control, immune challenged early only (early), immune challenged late only (late) and immune challenged both early and late in life (early and late). The numbers at the bottom of the bars are the sample size (the number of females involved). Bars topped with the same capital letters denoted groups with non-significant differences (see Table 1).

Figure 3

Summarized immune scores for (a) cellular, (b) enzymatic, and (c) antibacterial defences according to the age at which females were sampled for their haemolymph (young: at 30 days post-eclosion and old: at 60 days post-eclosion) and as a function of their age-specific immune treatment (early control and early challenge at 10 days post-eclosion, and late control and late challenge: at 40 days post-eclosion). The numbers at the bottom of the bars are the sample size (the number of females involved). Bars or groups topped with the same capital letters denoted groups with non-significant differences (see Table 2).

Figure 4

Variation in scores of inducible antibacterial defence as a function of total fecundity (number of eggs laid) the early-life immune treatment. The negative relationship between antibacterial scores and fecundity is significant only among females that were exposed to an early immune challenge (continuous line: F_{1, 62} = 11.77, P = 0.001, r = 0.4). Among controls, the relationship is not statistically significant, and the dashed line is illustrative only.