Kin-selected conflict and the evolution of lifespan and ageing

Lead Research Organisation: University of East Anglia
Department Name: Biological Sciences


Why organisms age, i.e. grow feebler, as they grow old is a central topic in evolutionary ecology. Since bodies self-repair, why cannot every organism constantly renew itself and remain at peak condition despite its chronological age? The evolutionary theory of ageing answers this question with natural selection. Accidents inevitably ensure that there are fewer old individuals than young ones. This means that old individuals make a smaller genetic contribution to future generations. In turn, this means that natural selection values them less highly, or, put another way, that genes with harmful effects are less strongly selected against in older individuals. The result is selection for ageing. However, this conventional view of the evolution of ageing is incomplete, because it omits social effects. Normally an individual's death benefits only the unrelated conspecifics who gain access to the resources it leaves behind. But in a population made up of groups of relatives, death of one individual benefits its related group-mates. This affects the evolution of lifespan and ageing through kin selection, i.e. because relatives share genes in common. An example is the case, common in nature, of a parent whose death releases a resource, such as a nest or territory, required by an offspring to breed (resource inheritance). Eventually this benefits the offspring, creating an incentive for the parent to die prematurely, but there is a twist; parent and offspring do not 'agree' on the exact timing of parental death and resource handover. When the parent dies, it effectively 'trades' its own offspring (relatedness, r, = 0,5) for the less-related offspring of its young, namely its grandoffspring (r = 0.25). But the offspring trades its siblings (r = 0.5) for its own, equally-related offspring (r = 0.5). It follows that, if the parent is declining in fecundity, the offspring favours inheriting the resource before the parent favours yielding it. So, in social systems meeting these conditions, offspring should harass and even kill a parent whose fecundity is declining. If parental fecundity declines sufficiently, the parent gains more fitness by dying and allowing the offspring to reproduce than by remaining alive. Such a parent should rapidly age and die. In this proposal, we aim to test the hypothesis that kin-selected conflict over resource inheritance affects lifespan and ageing using the bumble bee Bombus terrestris as our experimental system. This species is highly suitable for the work because workers inherit the nest from their mother, the queen, and produce their own offspring within it. In addition, B. terrestris workers do sometimes kill their own mother before reproducing (worker matricide). We will test the two central predictions of the hypothesis. The first is that workers harass the queen and commit matricide when they assess that they will gain greater fitness from offspring production than from keeping the queen alive and rearing siblings. The second is that, at or approaching the threshold when the queen is selected to cede control of the nest to workers, queen ageing should be accelerated. To test the first prediction, we will carry out experiments such as comparing the lifespans of queens with and without aggressive, potentially reproductive workers. To test the second, we will confirm that genes known to be indicators of ageing in other social insects act likewise in B. terrestris. We will then test whether, in queens being harassed by workers, these genes show changes in expression level indicating accelerated ageing. The proposed research is novel because the focal hypothesis has not previously been tested, and nor has a combined behavioural and genetic approach to investigating such issues been implemented. It is fundamental because of the theoretical and practical importance of understanding how sociality affects ageing. The work should therefore yield results of value and relevance to several disciplines.


10 25 50
Description In this project, we tested the hypothesis that kin-selected conflict over resource inheritance affects lifespan and ageing using the bumble bee Bombus terrestris. When the mother queen dies, workers of B. terrestris inherit the nest from her and produce their own male offspring inside it. The hypothesis predicts parent-offspring conflict over the exact timing of resource handover. Indeed, workers sometimes kill their own queen before reproducing (worker matricide), supporting the existence of queen-worker conflict over the timing of parental death.

1. We constructed a graphical model of queen-worker conflict over resource inheritance, based on inclusive fitness theory, and experimentally tested it using captive colonies of B. terrestris. We found that, as our model assumed, the workers gain more direct fitness the longer they can reproduce after the queen's death. Moreover, queen fecundity falls with time, which means the threshold for deposing the queen is met first for those workers laying eggs after her death. When we experimentally simulated (by removal of her eggs) the queen losing fecundity, workers increased their rate of harassment of the queen, and aggressive workers were more likely to go on to become egg-layers. This suggests that, as expected, potentially reproductive workers monitor queen fecundity and harass the queen when they perceive her quality to be declining. Overall, these results provide new support for the occurrence of kin-selected conflict over resource inheritance, and, in turn, for such conflict being a key determinant of lifespan in these species (Almond et al. 2019).

2. Using qRT-PCR, we also investigated how expression of genes from ageing-related pathways is affected by queen and worker traits in B. terrestris. We found that four such genes showed higher expression in queen brains with increasing female (queen plus worker) production, with this relationship strengthening as queen age increased, suggesting a link with the positive association of fecundity and longevity found more widely in eusocial insect queens (Lockett et al. 2016). In workers, there was a significant age-related increase in expression of DNA methyltransferase 3 (Dnmt3) in fat body, suggesting a novel association between aging and methylation in B. terrestris. Moreover, ovary activation in workers was associated with significantly higher vitellogenin (vg) expression in fat body and, in younger workers, in brain, consistent with vitellogenin's ancestral role in regulating egg production (Lockett et al. 2016).
Exploitation Route Potentially by commercial bumblebee rearers, who have an interest in understanding the factors that affect bee longevity.
Sectors Agriculture, Food and Drink,Environment