Social evolution and the evolution of ageing: testing the hypotheses

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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.