KIN-SELECTED CONFLICT AND THE EVOLUTION OF LIFESPAN AND AGEING

Why organisms age, i.e. grow feebler, as they get 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 the evolution of ageing.

Though it has been highly successful, this conventional version of the evolutionary theory of ageing is incomplete. It omits social effects. An individual's death normally benefits only the unrelated conspecifics who gain resources it leaves behind. But in a social species with populations made up of groups of relatives, an individual's death potentially benefits related group-mates. According to inclusive fitness theory, this should affect the evolution of lifespan and ageing through kin selection, i.e. because relatives share genes.

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. However, because each party is comparatively more related to its own offspring than to those of the other party, there may be parent-offspring conflict over the exact timing of parental death and resource handover (Bourke 2007).

In this project, we tested the hypothesis that kin-selected conflict over resource inheritance affects lifespan and ageing in 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. Workers sometimes kill their own queen before reproducing (worker matricide), which implies the existence of queen-worker conflict over the timing of parental death. We constructed a graphical model of this situation, based on inclusive fitness theory, and experimentally tested it using captive colonies of B. terrestris (Almond et al. 2019).

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 daily removal of her eggs) the queen losing all her 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 in social animals, and, in turn, for such conflict being a key determinant of lifespan in these species (Almond et al. 2019).

Using quantitative PCR, we also investigated how expression of genes from ageing-related pathways is affected by queen and worker traits in B. terrestris. For example, 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). A remaining goal of future work is to investigate more fully how sociality and ageing interact at the genetic level.

The project was carried out by Edd Almond and Tim Huggins in Andrew Bourke's group at UEA, in collaboration with Gabrielle Lockett and Joel Parker, both previously in the School of Biological Sciences, University of Southampton.  The project was funded by NERC.

Almond EJ, Huggins TJ, Crowther LP, Parker JD, Bourke AFG (2019) Queen longevity and fecundity affect conflict with workers over resource inheritance in a social insect. American Naturalist 193: 256-266.

 

Bourke AFG (2007) Kin selection and the evolutionary theory of aging. Annual Review of Ecology, Evolution and Systematics 38: 103-128.

Lockett GA*, Almond EJ*, Huggins TJ, Parker JD, Bourke AFG (2016) Gene expression differences in relation to age and social environment in queen and worker bumble bees. Experimental Gerontology 77: 52-61. *Joint first authors 

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