Lifetime reproductive success and longevity of workers in a social insect

Lead Research Organisation: University of East Anglia
Department Name: Biological Sciences


The evolution of social behaviour and the evolution of ageing both form major areas of study in evolutionary ecology. The evolution of social behaviour concerns how animal societies such as those of the eusocial insects (ants, bees, wasps and termites) arise and are maintained. The evolution of ageing concerns the factors that affect the longevity of organisms and the pattern of reproduction over their lifetimes. Recently, researchers have realised that these areas are connected, and that orthodox patterns of ageing can be heavily affected by sociality. A key example involves the relationship between lifetime reproductive success (the number of offspring an individual has over its lifetime) and longevity. The standard evolutionary theory of ageing predicts that sources of extrinsic mortality (factors leading to death in the external environment, such as predators, accidents, and so on) select for earlier reproduction, which in turn is paid for by earlier death. This predicts a negative relationship between lifetime reproductive success and longevity, i.e. that individuals producing more offspring have shorter lives. But, in eusocial societies, which contain both breeding and helping individuals, researchers have predicted that the breeders should exhibit a positive relationship between lifetime reproductive success and longevity, i.e. that individuals producing more offspring have longer lives. This is because breeders in eusocial societies are protected against extrinsic mortality by remaining in the nest. The principal investigator's research recently confirmed this prediction by demonstrating for the first time a positive relationship between lifetime reproductive success and longevity in queens of a eusocial insect, the bumble bee Bombus terrestris.

In B. terrestris, as in many other eusocial insects, the workers, which are all daughters of the queen, can produce some offspring of their own. Because of the sex determination system in bees, workers' offspring are always males. Reproductive workers will, like queens, be protected from extrinsic mortality if they tend to remain in the nest, but not if they routinely leave the nest to forage. This allows the hypothesized effect of extrinsic mortality to be isolated, because it leads to the prediction that reproductive workers will exhibit a positive relationship between lifetime reproductive success and longevity if they tend to remain in the nest and a negative relationship if they tend to leave the nest to forage. The aim of this project is to test this hypothesis using B. terrestris as the study organism.

The project is feasible because B. terrestris is an annual eusocial insect, i.e. one completing its colony cycle in a single season and hence one in which queens and workers live in the colony for at most a few months. B. terrestris colonies are also commercially available and are easy to keep and observe in the laboratory. The lifetime reproductive success and longevity of all mother queens and a sample of their reproductive worker daughters will be determined in a set of colonies whose workers have been individually marked. Birth and death dates, time spent in the nest and lifetime reproductive success will be measured across all individuals, with lifetime reproductive success being measured both as egg-production (measured from filming of nests) and from parentage analyses of males using genetic markers.

This research is novel and fundamental because it will test new concepts at the interface of the important areas of social evolution and the evolution of ageing. For this reason, the work will substantially advance our basic understanding of both sociality and ageing in general.

Planned Impact

As well as having an academic impact, this research will potentially benefit two other groups, namely commercial bumble-bee rearing companies and the general public. The commercial culture of bumble bee colonies for the pollination of glasshouse crops is a growing industry worldwide. Ideally the industry should sustainably rear and then market bumble bee species native to the country of use, and there is evidence that several companies are attaining this goal. These companies would potentially benefit from greater knowledge of the social biology of bumble bees, especially as regards colony and individual longevity, since these directly affect the pollinating lifetime of commercial colonies. The PI will build on existing contacts with these companies to explore the application of the research results to enhance their sustainability, effectiveness and competitiveness. In turn, the possibility will be explored of using commercial rearing facilities for experiments on the life history and evolution of social insects on a large scale that is not achievable in other study systems. The PI has a record of seeking to maximise the impacts of his research, for example through applying genetic census techniques that he and colleagues have developed to projects investigating the population biology of declining bumble bee species or testing the effectiveness of agri-environment schemes for bumble bees in the UK.

Many members of the public are fascinated by bumble bees, drawn by their intrinsic attractiveness but also recognizing their importance in the pollination of crops and wild flowers. Bumble bees therefore make great tools with which to engage adults and schoolchildren in both ecology as a discipline and the conservation of ecosystem services as a concept and policy goal. The PI and research technician will seek to engage the public with the results of the research via press releases, dedicated project webpages and engagement events such as exhibitions and public talks. The PI has wide experience of dealing with the media and interacting with the public in this way.


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Description 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.
Exploitation Route Potentially by commercial rearers of bumblebees interested in a better understanding of factors affecting longevity in captivity.
Sectors Agriculture, Food and Drink,Environment