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At first sight, eusocial insects seem to defy the evolutionary theory of ageing. The theory suggests that greater reproduction is paid for by an earlier death, because organisms cannot maximise both fecundity and longevity. However, in the eusocial insects, queens typically live much longer than workers, even though queens are specialised for reproduction and workers are specialised for non-reproductive tasks. In fact, although the differential longevity of queens and workers reveals extraordinary plasticity in the ageing schedules of different phenotypes within a species, it is not a serious problem for the evolutionary theory of ageing. The theory can accommodate this difference, as queens are typically protected from extrinsic mortality by remaining in the safety of the nest and receiving aid from workers, whereas workers undertake risky external tasks such as foraging and nest defence (e.g. Bourke 2007).

The bigger challenge from the eusocial insects to the evolutionary theory of ageing comes from the finding that, within the queen caste, fecundity and longevity are usually positively associated. In other words, queens seem to lack the fecundity-longevity trade-off found in most non-social organisms. This is the case in some ants and, we have found, in the bumble bee Bombus terrestris, in which queens exhibit a positive association between their lifetime reproductive success (lifetime production of new queens and males) and their longevity (Lopez-Vaamonde et al. 2009). Because of such findings, it has been suggested that eusocial insect queens lack costs of reproduction and accordingly may have experienced a remodelling of the genetic pathways that normally underpin the association between reproduction and longevity.

In this project, we tested the relationship between fecundity and longevity in eusocial insects experimentally, but with workers not queens (Blacher et al. 2017). All queens are phenotypically adapted to reproduce, so, in queens, it is hard to generate non-reproductive individuals experimentally. This is not true for workers of species such as B. terrestris, which can produce male offspring by asexual reproduction in a flexible manner depending on social context. We found that, when workers could freely 'choose' whether to activate their ovaries in whole colonies (unmanipulated except that the queen was removed in some to generate a higher number of reproductive workers), workers exhibited a positive fecundity-longevity association as in queens. However, when we experimentally forced randomly-selected workers to become reproductive or non-reproductive (by keeping them in trios with younger and older workers, respectively), workers exhibited a negative fecundity-longevity association. In addition, in this second experiment, ovary-active workers lived less long than ovary-active ones, which was the reverse of the pattern found in whole colonies in the first experiment.

We hadn't expected the results of our second experiment, so they caused us to rethink. Our overall findings suggest that, in B. terrestris workers, costs of reproduction exist but are masked in whole colonies because only high-quality individuals able to overcome them 'choose' to become reproductive. This in turn suggests that costs of reproduction also exist in queens, so there may have been no fundamental remodelling of the genetic pathways underpinning ageing. In fact it has long been recognised that, in non-social organisms, quality differences can generate positive fecundity-longevity associations between individuals. Eusocial insects could be an example of this phenomenon. Finding out whether this is generally true remains an exciting task for the future.

This project was carried out in Andrew Bourke's group at UEA by Pierre Blacher and Tim Huggins. It was funded by the Fyssen Foundation and NERC.

Blacher P, Huggins TJ, Bourke AFG (2017) Evolution of ageing, costs of reproduction and the fecundity-longevity trade-off in eusocial insects. Proceedings of the Royal Society B 284: 20170380.

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

Lopez-Vaamonde C, Raine NE, Koning JW, Brown RM, Pereboom JJM, Ings TC, Ramos-Rodriguez O, Jordan WC, Bourke AFG (2009) Lifetime reproductive success and longevity of queens in an annual social insect. Journal of Evolutionary Biology 22: 983-996.