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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, in eusocial evolution, queens evolve so as to lack costs of reproduction. Accordingly, it has been suggested that queens may have experienced a remodelling of the genetic pathways that normally underpin the association between reproduction and longevity. In the group, we've therefore carried out several projects to investigate the relationship between fecundity and longevity in eusocial insects, and to characterise associated gene expression patterns, with results as follows:

1. Costs of reproduction exist in reproductive worker bumble bees: In the first project, we experimentally tested the relationship between fecundity and longevity in eusocial insects using workers not queens (Blacher et al. 2017). Using workers allowed us to generate non-reproductive individuals experimentally more easily, because, in species such as B. terrestris, workers 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-inactive ones, which was the reverse of the pattern found in whole colonies in the first experiment. These findings, which were unexpected at the time, suggested that costs of reproduction exist in B. terrestris workers but are masked in whole colonies because only high-quality individuals able to overcome them 'choose' to become reproductive. In fact it has long been recognised that, in non-social organisms, quality differences can generate positive fecundity-longevity associations between individuals. Eusocial insects like B. terrestris could therefore represent an example of this phenomenon.


2. Costs of reproduction are present but latent in eusocial bumble bee queens: Given the findings of the previous study, our next step was to test whether queens in annual eusocial insects like B. terrestris experience costs of reproduction (Collins et al. 2023a). We experimentally increased queens' costs of reproduction by removing their eggs, which caused queens to increase their egg-laying rate. Treatment queens lived significantly shorter lives than control queens whose egg-laying rate was not increased. In addition, treatment and control queens differed in age-related gene expression in both their overall expression profiles and the expression of ageing-related genes. Remarkably, these differences appeared to occur principally with respect to relative age (age measured in terms of percentage mortality), not chronological age. Matching our results in workers, these findings suggested that, in queens, costs of reproduction are present but latent, i.e. that positive fecundity-longevity associations in queens of B. terrestris and similar species are condition-dependent. They also raised the possibility that a partial remodelling of genetic and endocrine networks underpinning ageing may have occurred in B. terrestris such that, in unmanipulated conditions, age-related gene expression depends more on chronological than relative age. These findings therefore help illuminate the steps taken in eusocial evolution to achieve the unconditionally positive fecundity-longevity associations, underpinned by a complete remodelling of relevant genetic and endocrine networks, thought to have occurred in advanced eusocial insects.

3. An experiment shows that, in Drosophila, the directionality of fecundity-longevity associations is conditional on larval diet quality: In most eusocial insects, females develop as adult queens or workers depending on the quality and/or quantity of their larval diets. Queen phenotypes might therefore represent females reared on high-quality diets, so helping explain (at the proximate level) why queens typically exhibit positive fecundity-longevity associations. We carried out an experiment using the fruit fly Drosophila melanogaster to test for a general effect of larval diet on the directionality of the fecundity-longevity association in insects (Collins et al. 2023b). We reared D. melanogaster larvae on low (20%), medium (100%), and high (120%) yeast diets, then transferred the adult females developing from these larvae to a common diet. We measured the fecundity and longevity of these adult females individually, and profiled their gene expression changes with age. We found that adult females raised on different larval diets exhibited fecundity-longevity relationships that varied from significantly positive to significantly negative, despite minimal differences in mean life-time fertility or longevity. Females from the different larval diets also differed in age-related gene expression, including for ageing-related genes. This shows that the directionality of the fecundity-longevity relationship in adult insects can be altered and even reversed by changes in larval diet. By extension, larval diet differences may represent a key mechanistic factor underpinning positive fecundity-longevity relationships observed in species such as eusocial insects.  


The worker 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.


The queen and fruit-fly projects were carried out in Andrew Bourke's group at UEA by David Collins, David Prince and Jen Donelan in collaboration with Tracey Chapman.  They were funded by NERC and the sequencing was performed by Edinburgh Genomics.

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.

Collins DH, Prince DC, Donelan JL, Chapman T, Bourke AFG (2023a) Costs of reproduction are present but latent in eusocial bumblebee queens. BMC Biology 21: 153.

Collins DH, Prince DC, Donelan JL, Chapman T, Bourke AFG (2023b) Developmental diet alters the fecundity-longevity relationship and age-related gene expression in Drosophila melanogaster. Journals of Gerontology: Series A

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.

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