Intrinsic survival advantage of social insect queens depends on reproductive activation

Abstract

The central trade-off between reproduction and longevity dominates most species' life history. However, no mortality cost of reproduction is apparent in eusocial species, particularly social insects in the order Hymenoptera: one or a few individuals (typically referred to as queens) in a group specialize on reproduction and are generally longer lived than all other group members (typically referred to as workers), despite having the same genome. However, it is unclear whether this survival advantage is due to social facilitation by the group or an intrinsic, individual property. Furthermore, it is unknown whether the correlation between reproduction and longevity is due to a direct mechanistic link or an indirect consequence of the social role of the reproductives. To begin addressing these questions, we performed a comparison of queen and worker longevity in the ant Cardiocondyla obscurior under social isolation conditions. Survival of single queens and workers was compared under laboratory conditions, monitoring and controlling for brood production. Our results indicate that there is no intrinsic survival advantage of queens relative to workers unless individuals are becoming reproductively active. This interactive effect of caste and reproduction on life expectancy outside of the normal social context suggests that the positive correlation between reproduction and longevity in social insect queens is due to a direct link that can activate intrinsic survival mechanisms to ensure queen longevity.

Keywords: Formicidae; ageing; caste; fertility; longevity; social evolution.

Figure 1

The survival of queens and workers of the ant Cardiocondyla obscurior indicating a reversal of the general fecundity-lifespan trade-off. Individuals were kept in isolation under laboratory conditions to compare the intrinsic rates of aging between the castes. A small fraction of queens initiated reproduction, and corresponding workers received equivalent amounts of eggs to control for potential brood effects. Overall survival was not significantly different (not shown) but reproductively active queens were longer-lived than their worker complements, while survival of non-reproductive queens was not significantly different from that of the corresponding workers.

Figure 2

Survival differences in the specific queen-worker dyads that were initially paired based on emergence date and colony source. Subsequently, the worker in a pair received eggs equivalent to what the corresponding queen produced (dyads # 43–48) or remained brood-less when the queen did not produce any eggs (dyads #1–42) to control for potential brood effects. While all of the reproductive queens were longer-lived than the corresponding workers (upper, black bars), only 13 of 42 non-reproductive queens were longer-lived than the corresponding workers (lower, blue bars), which illustrates the significant interaction effect of caste and reproductive status on survival (Fisher’s exact test: p = 0.002).