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Complex social behaviour derived from maternal reproductive traits

Abstract

A fundamental goal of sociobiology is to explain how complex social behaviour evolves1, especially in social insects, the exemplars of social living. Although still the subject of much controversy2, recent theoretical explanations have focused on the evolutionary origins of worker behaviour (assistance from daughters that remain in the nest and help their mother to reproduce) through expression of maternal care behaviour towards siblings3,4. A key prediction of this evolutionary model is that traits involved in maternal care have been co-opted through heterochronous expression of maternal genes5 to result in sib-care, the hallmark of highly evolved social life in insects6. A coupling of maternal behaviour to reproductive status evolved in solitary insects, and was a ready substrate for the evolution of worker-containing societies3,4,7,8. Here we show that division of foraging labour among worker honey bees (Apis mellifera) is linked to the reproductive status of facultatively sterile females. We thereby identify the evolutionary origin of a widely expressed social-insect behavioural syndrome1,5,7,9, and provide a direct demonstration of how variation in maternal reproductive traits gives rise to complex social behaviour in non-reproductive helpers.

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Figure 1: Distributions of ovariole number and patterns of previtellogenic ovarian activation in worker bees.
Figure 2: Correlations between ovariole number and the social behaviour of wild-type bees.

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Acknowledgements

We thank A.L.O.T. Aase for assistance with dissections, and K. Hartfelder and P. Kukuk for comments. The project was supported by grants from the Norwegian Research Council to G.V.A, and from the National Institute on Aging and the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service to R.E.P.

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Correspondence to Gro V. Amdam or Robert E. Page Jr.

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Supplementary Tables

Supplementary Table 1 and 2. Detailed results on ovary size (number of ovary filaments) and state of ovarian activation in honey bee workers of strains selected for high- or low levels of pollen collection and storage. (DOC 142 kb)

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Amdam, G., Csondes, A., Fondrk, M. et al. Complex social behaviour derived from maternal reproductive traits. Nature 439, 76–78 (2006). https://doi.org/10.1038/nature04340

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