Social evolution and the evolution of ageing: testing the hypotheses

How and why ageing evolves represent core questions of enduring interest in evolutionary biology. According to the classical evolutionary theory of ageing, the inevitable toll of extrinsic mortality means that natural selection values older individuals less highly than young ones as contributors to future generations. This weakens selection for the expression of beneficial genes in older individuals and, in turn, leads to the degeneration in performance, survivorship or fecundity with time that defines ageing. In addition, limited resources enforce a compromise between selection for reproduction and selection for survival. The result is that reproduction triggers ageing and generates physiological costs that lead to a trade-off, or negative association, between fecundity and longevity.

However, deviations from this classical prediction have increasingly been recognised. A key one occurs when individuals differ in intrinsic quality and/or resources held. High-quality (well-resourced) individuals then both reproduce more and live longer than poor-quality ones. In this case, between-individual comparisons yield a positive association of fecundity and longevity, even though costs of reproduction are not abolished and investments in reproduction and survival are still traded-off within individuals.

Eusocial organisms (ants, bees, wasps and termites with queen and worker castes) are another exception to the classical prediction. Not only are queens very long-lived, but, within the queen caste, the most fecund and productive queens live the longest, i.e. there is a positive fecundity-longevity association. It has therefore been hypothesised that, under eusociality, conventional costs of reproduction are not incurred and that the fecundity-longevity trade-off, along with conventional expression patterns of ageing-related genetic pathways, have been reversed. However, we hypothesise that queens are instead analogous to intrinsically high-quality individuals in non-social organisms, such that costs of reproduction are latent but not usually expressed. Evidence for this hypothesis comes from a recent study of ours showing that, in the eusocial bumblebee Bombus terrestris, when workers are experimentally forced to reproduce, a positive fecundity-longevity association in reproductive workers becomes negative. The workers also live less long. These results suggests that costs of reproduction exist but are not usually expressed by high-quality workers that freely 'choose' to reproduce in unmanipulated colonies. Hence, at least among workers, the reversed fecundity-longevity trade-off may be more apparent than real, calling into fundamental question the field's previous understanding of how eusociality affects ageing.

The proposed project will address the novel questions raised by these findings to establish the full effect of eusociality, and social evolution in general, on the evolution of ageing. We will discriminate between the new hypothesis and the previous hypothesis by: (1) experimentally manipulating costs of reproduction experienced by B. terrestris queens and comparing their longevities; (2) comparing how gene expression profiles (from RNA-Seq data) change with age between queens in this experiment and between workers in a large-scale repeat of the worker experiment outlined above; and (3) comparing changes in gene expression profiles with age between B. terrestris queens (from (1)) and females of the non-social model insect, the fruitfly Drosophila melanogaster, experimentally manipulated (with high-protein larval diet) to be higher quality and to express greater longevity. This last comparison will also reveal whether ageing-associated genetic networks have been radically remodelled in eusocial evolution or reflect quality differences. Through discriminating between two pivotal hypotheses at the intersection of two fundamental fields, i.e. sociality and ageing, this work promises to deliver major advances.

As well as having a substantial academic impact, this research will potentially have key non-academic impacts. Specifically, potential non-academic beneficiaries include commercial bumblebee rearing companies, bee-related NGOs, policy-makers and practitioners in government departments covering biodiversity and agriculture, and the general public.

Many companies worldwide mass-rear bumblebee colonies for the pollination of crops in glasshouses or polytunnels. These companies would potentially benefit from the project because an improved understanding of queen and worker longevity, and the factors that regulate them, might aid in large-scale bee-rearing and in achieving effective, sustainable commercial pollination. The PI will continue ongoing dialogue with the bee-rearing companies to promote relevant results of the new research.

Several organizations, including the Bumblebee Conservation Trust, the British Beekeepers Association and Buglife, are active in conducting and/or promoting the understanding and conservation of bees in the UK. The project would benefit from their aid in disseminating results and impact and they would benefit from having, if they chose, a science-based bee-related 'story' to publicise. The project team will send team members to the Bumblebee Working Group (BWG) meeting, a forum for UK bumblebee conservation held every 1-2 years, which is regularly attended by representatives of relevant NGOs. The PI regularly attends the BWG (and has previously hosted it).

Policy-makers and practitioners in government departments covering biodiversity and agriculture have an interest in understanding the biology of insect pollinators in its broadest sense, especially in view of pollinator declines. This group might benefit from the evidence base that the project will provide as regards bumblebee biology. The PI will seek opportunities to present relevant results to policy-makers and practitioners, building on contacts made at previous workshops and new contacts acquired via Dr Lynn Dicks, an expert at the science-policy interface of bee and pollinator conservation who recently joined AB and TC's School as a NERC Independent Research Fellow and faculty colleague. AB has a record of seeking to maximise the impacts of his research, especially through applying genetic census techniques that he and others have developed for wild bumblebee populations to projects exploring the population biology of declining bumblebee species or testing the effectiveness of agri-environment schemes for bumblebees in the UK. Most recently, results of AB and collaborators' Insect Pollinators Initiative project helped inform details of the Wild Pollinator and Farm Wildlife Package in the new Countryside Stewardship scheme.

Bumblebees are immensely popular organisms with the public, and there is widespread affection for them and appreciation of their pollinating role. In addition, ongoing publicity over declines of honey bees and wild bees has increased awareness of the need to conserve bee populations. The public would benefit from learning the results of the project to satisfy the clear appetite that therefore exists for scientific information on the biology of bees. The project team will engage the public with the results of the research via press releases, dedicated project webpages and events such as exhibitions and public talks. The PI has wide experience of dealing with the media and a demonstrable commitment to interacting with the public in the manner proposed.