Effects of Selection for Honey Bee Worker Reproduction on Foraging Traits

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Abstract
The “reproductive ground plan” hypothesis (RGPH) proposes that reproductive division of labour in social insects had its antecedents in the ancient gene regulatory networks that evolved to regulate the foraging and reproductive phases of their solitary ancestors. Thus, queens express traits that are characteristic of the reproductive phase of solitary insects, whereas workers express traits characteristic of the foraging phase. The RGPH has also been extended to help understand the regulation of age polyethism within the worker caste and more recently to explain differences in the foraging specialisations of individual honey bee workers. Foragers that specialise in collecting proteinaceous pollen are hypothesised to have higher reproductive potential than individuals that preferentially forage for nectar because genes that were ancestrally associated with the reproductive phase are active. We investigated the links between honey bee worker foraging behaviour and reproductive traits by comparing the foraging preferences of a line of workers that has been selected for high rates of worker reproduction with the preferences of wild-type bees. We show that while selection for reproductive behaviour in workers has not altered foraging preferences, the age at onset of foraging of our selected line has been increased. Our findings therefore support the hypothesis that age polyethism is related to the reproductive ground plan, but they cast doubt on recent suggestions that foraging preferences and reproductive traits are pleiotropically linked. In social insects, the evolution of the worker caste and the regulation of reproductive behaviour by workers are poorly understood. Evolution is conservative and often proceeds by adapting an existing gene network to a new function. The “reproductive ground plan” hypothesis (RGPH) suggests that social insects evolved their queen and worker castes by modifying a gene network that once regulated the foraging and reproductive phases of solitary ancestors. In this model, queens retain characteristics of insects in their reproductive phase, whereas workers retain characteristics of the foraging phase. Moreover, the foraging behaviour of workers may also be regulated by the same genes that once controlled the switch between foraging and feeding young in the nest. We evaluated the RGPH by studying a line of honey bees selected for high rates of worker reproduction. We show that in this line workers forage late in life and some may never forage, supporting the idea that genes related to reproduction are also related to foraging. However, we found no support for recent suggestions that genes related to reproduction also regulate the foraging behaviour of individual workers: once they start foraging, our highly reproductive workers forage in the same way that unselected workers do.