QUEEN-WORKER COADAPTATION AND CONFLICT IN A PRIMITIVELY EUSOCIAL BEE

Lead Research Organisation: University of Sussex
Department Name: Sch of Life Sciences

Abstract

Understanding the conflicts of interest that occur within families has been a major focus of research in evolutionary biology: unless they are genetically identical, the precise evolutionary interests of individual family members often differ. Family conflicts have been particularly well studied in social insects, where there is potential conflict between the queen and her workers over questions such as who should lay the eggs, what sex-ratio of offspring to produce, and the length of tenure of the queen. However, while much is now known about the evolutionary endpoint of these conflicts, little is known about the underlying genetic architecture and the pattern of reciprocal adaptation between queen- and worker-expressed genes. This proposal will investigate queen-worker interactions in the UK social sweat bee Lasioglossum malachurum (Hymenoptera: Halictidae). A key method will be cross-fostering: just before workers reach adulthood, queens will be switched between nests. Because cross-fostered queens no longer share a nest with genetically related workers (which would normally be their own offspring), cross-fostering means that (1) queen and worker influences on offspring characteristics can be separated; (2) any subsequent correlations between the behaviour of a queen and her workers (now in separate nests) must reflect genes inherited by workers from queens rather than effects of the common environment; (3) 'mismatches' between queen and worker characteristics are generated - mismatches of the kind expected during on-going evolutionary conflict, but not normally available to study because evolution has largely eliminated them.

By using a combination of cross-fostering, and DNA fingerprinting to determine whether each offspring was produced by queen or workers, the work will achieve the following objectives.

Objective 1: Test whether evolution has led to a correlation between a queen's ability to prevail in reproductive conflicts with the workers in her new nest, and the ability of her workers to prevail in the same conflicts with an unrelated queen.

Objective 2: Carry out the first direct test of whether queens normally manipulate worker size and number in their own interests, for example by reducing worker size and therefore a worker's ability to compete with the queen over offspring production.

Objective 3: Separate queen influences from worker influences on body size, a key offspring trait, and investigate the underlying genetic architecture theoretically.

Objective 4: Carry out the first direct test of a key hypothesis for the evolution of helping in Hymenoptera: the hypothesis that a larger group of workers leads to a more female-biased sex-ratio of offspring. Because workers are more closely related to female- than male offspring of the queen, such an effect could facilitate helping.

The study system allows exceptionally large sample sizes to be obtained in the field, where natural selection operates. The overall result will be the most comprehensive understanding to date of the process of queen-worker coevolution, including the first tests of several key hypotheses. Empirical work will be carried out at the University of Sussex, and the project will involve collaboration with Project Partner Prof Mathias Kölliker (University of Basel, Switzerland).

Planned Impact

WHO WILL BENEFIT FROM THE RESEARCH?

The project is blue-skies research to investigate fundamental questions about social evolution. Apart from other academics, the main beneficiaries will be the public through public communication activities. Public understanding of science is essential to maintain science funding and scientific literacy.

Activities will be targetted towards:

- students (and their teachers) at schools and further education colleges taking science subjects
- science undergraduates
- viewers of science/natural history programmes on TV

There are at least two reasons why the proposed research should stimulate public interest:

1. Although we will use a social insect model to investigate conflict and manipulation, these are also central features of everyday human interactions, including family interactions.
2. The public are intrinsically curious about social bees, because (a) they are social, (b) they are familiar as crop pollinators and producers of honey, and (c) bees are often seen as being dangerous.

HOW WILL THEY BENEFIT FROM THE RESEARCH?

1. Understanding the science behind their own behaviour.

The success of popular science books on cooperation, such as Rock, Paper, Scissors (Fisher 2009), and TV programmes on human behaviour, such as the BBC's Human Planet, indicate that the general public is very interested in behaviour that can be related to humans, and so would be receptive to learning about topics related to the proposed research. The interactive approach to be implemented via the Pathways to Impact plan seems particularly appropriate to stimulate interest.

2. Understanding the science behind natural history programmes

Although natural history TV programmes are very popular, they rarely show how the science behind the ideas presented is actually carried out. Similarly, many peoples' idea of what a scientist does come from TV dramas which portray scientists as emotionless megalomaniacs or as living an idyllic, stress-free life while consuming glasses of sherry! This is not ideal in the UK, a country that is world-leading in science, and where we should be aiming to encourage students to consider a scientific career as interesting, challenging and worthwhile. By focusing on conflict between genes residing within the same organism, the proposed film would also go beyond the evolution of species, or an organism's form and its adaptive function, which tend to be the perspectives taken in natural history programmes.

3. Learning about social bees.

Although bees pollinate crops and produce honey, many people see them as a nuisance or even dangerous. While most people may be able to recognize a bumblebee, few are aware that there are actually >250 bee species in the UK alone, the vast majority of which are much smaller than bumblebees and often mistaken for 'flies'. By overcoming these misconceptions, and showing that bees make complex decisions about cooperation, we can stimulate curiosity about the natural world, which will ultimately make us better able to conserve it. Furthermore, we can foster future generations of scientists by helping students to understand how even stinging insects such as bees can not only be interesting, but also help us to understand our own behaviour.
Fisher L. 2009. Rock, Paper, Scissors: Game Theory in Everyday Life. New York: Basic Books

Publications

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Related Projects

Project Reference Relationship Related To Start End Award Value
NE/M003191/1 08/01/2015 31/12/2016 £408,251
NE/M003191/2 Transfer NE/M003191/1 01/01/2017 07/08/2018 £164,448
 
Description Understanding the conflicts of interest that occur within families has been a major focus of research in evolutionary biology. In social insects such as bees and wasps there is potential conflict between the queen and her workers over traits such as the sex-ratio and over who produces the male offspring. We investigated queen-worker interactions in primitively eusocial insects such as sweat bees (Halictidae) and paper wasps (Polistes), where physical differences between castes are minimal. A key method we developed was cross-fostering: just before the first workers reached adulthood, we switched queens between nests. Cross-fostering means that (1) 'mismatches' between queen and worker traits are generated - mismatches of the kind expected during on-going evolutionary conflict, but not normally available to study because evolution has largely eliminated them; and (2) queen and worker influences on offspring phenotype can be separated.
One of our main achievements was to carry out a direct test of whether queens normally manipulate worker size and number in their own interests. Social insect queens are nearly always larger than their worker offspring, and queens could benefit in several ways by producing small workers. If she uses aggression to coerce workers, a queen producing small workers might minimize potential conflict with them. In addition, because of the trade-off between the number of workers she is able to produce and their individual size, a queen may produce small workers to optimize colony work effort. In many social insects, the queen provisions the first worker-destined offspring alone, so that she might actively manipulate their attributes by controlling the resources she provides during their development. We used our cross-fostering methodology to create size mismatches between queens and workers. Some of our results were consistent with the idea that queens limit worker size strategically: small workers were no less successful foragers, so that producing a larger number of smaller workers may increase queen fitness. We also found that queens were less likely to attack relatively large workers, perhaps because attempting to coerce them is riskier. However, larger workers were not more aggressive themselves, and did not forage less or invest more in reproduction. Overall there was therefore little evidence that queens limit conflict by producing smaller workers. A key approach in the future might be to induce larger mismatches by manipulating worker size beyond the natural range.
Among our other achievements was to provide empirical support for the group size-sex ratio hypothesis for the evolution of helping in Hymenoptera: the hypothesis that a larger number of workers leads to a more female-biased offspring sex-ratio. Because workers are more closely related to female- than male offspring of the queen, such an effect could facilitate the initial evolution of helping. Beyond our original objectives, we also investigated environmental constraints on the expression of sociality, by transplanting sweat bee foundresses from the south to the far north of the UK. We found that the short season length and harsher conditions further north represent an environmental barrier to the successful expression of sociality.
Exploitation Route The research is primarily of use for other academics in the fields of evolutionary biology/animal behaviour
Sectors Environment

 
Description ERC Advanced Grant
Amount € 2,400,000 (EUR)
Funding ID 695744 
Organisation European Research Council (ERC) 
Sector Public
Country European Union (EU)
Start 01/2017 
End 12/2021