Report

Teaser, summary, work performed and final results

Periodic Reporting for period 2 - CASTECON (SHARING A GENOME: CASTE ANTAGONISM AND COADAPTATION IN SOCIAL INSECTS)

Teaser

SHARING A GENOME: CASTE ANTAGONISM AND COADAPTATION IN SOCIAL INSECTSAs social organisms ourselves, humans have a natural interest in understanding animal societies. Eusociality is arguably the most extreme form of social behaviour, in which some individuals (‘workers’)...

Summary

SHARING A GENOME: CASTE ANTAGONISM AND COADAPTATION IN SOCIAL INSECTS

As social organisms ourselves, humans have a natural interest in understanding animal societies. Eusociality is arguably the most extreme form of social behaviour, in which some individuals (‘workers’) sacrifice their own reproduction to rear the offspring of other individuals (‘queens’). The fundamental feature of eusociality is the division of labour between queen and worker castes: queens are typically long-lived and specialize on egg-laying, while workers are short-lived and specialize on foraging for provisions to feed the offspring. In order to maximize their performance, the two castes therefore need very different characteristics (dimorphism). Yet a remarkable feature of eusociality is that both castes are produced from the same genetic material. This suggests an important constraint, which we refer to as ‘caste antagonism’: a gene that increases performance when expressed in one caste may decrease performance when expressed in the other. For example, a gene that increases fertility may benefit queens, but it may cause workers to use up resources unnecessarily on ovary development at the expense of reduced foraging efficiency. To the extent that equivalent traits in the two castes are controlled by the same sets of genes, caste antagonism means that queens and workers will be constrained from reaching their optimal characteristics. The result will be that the fitness of the population or social group is reduced (Figure 1). Caste antagonism could be resolved through caste-specific gene expression (Figure 1), but genetic barriers may prevent this.
The overall objectives of the CASTECON project are to use wild populations of sweat bees and paper wasps to:
(1) Determine, by analysing gene expression, whether the underlying genetics really does constrain colony performance;
(2) Measure changes in queen-worker antagonism across an environmental gradient;
(3) Use social manipulations and transplants to investigate the mechanisms through which antagonism could be resolved;
(4) Cross-foster individuals between nests to test whether queens manipulate worker body size in their own interests.

Work performed

We have carried out 4 of the 6 planned field experiments, and the associated gene expression analysis is in progress. Three publications have been produced so far. The first publication reported a new set of 24 genetic markers that we developed so that we can determine whether the queen, or one of her workers, has produced each of the immature offspring in a nest (in sweat bees and paper wasps, workers are capable of egg-laying). The second publication was an important and hopefully influential review aimed at stimulating research focussed on caste antagonism. The review characterised caste antagonism, discussed how it might be resolved during evolution, suggested approaches to investigate it and reviewed the empirical evidence. The third publication relates to objective (4) above. In social animals, parents might manipulate characteristics of their offspring in their own interests. In paper wasps, the first offspring produced are smaller than the queen and become workers: instead of founding their own nests, they stay and help their mother to rear new queens and males. We investigated whether paper wasp queens benefit by producing small daughter workers. We used cross-fostering to create size mismatches between queens and their offspring. Before cross-fostering, there was a positive correlation between queen and worker body sizes: larger queens had larger workers. After cross-fostering, the correlation was absent. We then recorded foraging activity, reproductive effort, and aggression on nests. Queens were less likely to attack relatively larger workers, perhaps because attempting to coerce large workers is risky. However, larger workers did not forage less, did not invest more in ovarian development, and were not more aggressive themselves. But because small workers were no less successful foragers, producing a larger number of smaller workers may optimize colony work effort. Thus, queens may limit worker size strategically to optimize foraging, but overall there was limited evidence of size-based queen-worker conflict.

Final results

Our research programme is broadly novel and goes beyond the state of the art by being the first in-depth investigation of genetic constraints on caste evolution. There are possible functional explanations for the dramatic variation in caste dimorphism among social insects, but how dimorphism can evolve, the possibility that its evolution could be limited by genetic constraints, and the processes that could resolve those constraints, are topics that have hardly been considered. Empirically, our work so far is unusual because it uses data collected in the field, where natural selection operates, unlike almost all previous studies of sexual and caste antagonism, which have been conducted in the lab. We are also the first to use cross-fostering to investigate the possibility that queens manipulate worker characteristics.
By the end of the project, I expect all of the planned experiments to have been completed. The overall result will be a new and exciting perspective on queen-worker coevolution.

Website & more info

More info: http://biosciences.exeter.ac.uk/staff/profile/index.php.