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An invasive social insect overcomes genetic load at the sex locus

Nature Ecology & Evolution volume 1, Article number: 0011 (2017) Cite this article

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Abstract

Some invasive hymenopteran social insects found new populations with very few reproductive individuals. This is despite the high cost of founder effects for such insects, which generally require heterozygosity at a single locus—the complementary sex determiner, csd—to develop as females. Individuals that are homozygous at csd develop as either infertile or subfertile diploid males or not at all. Furthermore, diploid males replace the female workers that are essential for colony function. Here we document how the Asian honey bee (Apis cerana) overcame the diploid male problem during its invasion of Australia. Natural selection prevented the loss of rare csd alleles due to genetic drift and corrected the skew in allele frequencies caused by founder effects to restore high average heterozygosity. Thus, balancing selection can alleviate the genetic load at csd imposed by severe bottlenecks, and so facilitate invasiveness.

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Figure 1: A fragment of the sex locus of the Asian honey bee Apis cerana.
Figure 2: Empirical and simulated data of changes in csd allele frequencies over the course of the A. cerana invasion of Australia.
Figure 3: Expected heterozygosity based on the frequency of alleles in the Australian A. cerana population over eight years of the invasion.
Figure 4: A representation of a model of transmission of csd alleles in a population of honey bees.
Figure 5: Plausible fitness functions for a cost of DMP in honey bees as considered by our model.

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Acknowledgements

We thank the Queensland Department of Agriculture and Fisheries, Queensland Biosecurity, Australian Government Department of Agriculture and Water Resources, Cairns Regional Bee Club, E. Remnant, R. Stephens, R. Swenson, M. Gorton and M. Damon for their assistance. R.G. is supported by a University of Sydney Postdoctoral Fellowship. Research funding came from Australian Research Council DP150101985.

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Authors and Affiliations

  1. Behaviour and Genetics of Social Insects Laboratory, School of Life and Environmental Sciences, Macleay Building A12, University of Sydney, New South Wales, 2006, Australia

    Rosalyn Gloag, Guiling Ding, Joshua R. Christie, Gabriele Buchmann, Madeleine Beekman & Benjamin P. Oldroyd

  2. Key Laboratory of Pollinating Insect Biology of the Ministry of Agriculture, Institute of Apicultural Research, Chinese Academy of Agricultural Sciences, Beijing, 100093, China

    Guiling Ding

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  1. Rosalyn Gloag
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Contributions

B.P.O., M.B. and R.G. conceived the study. R.G., G.D. and G.B. collected samples, designed lab work strategies and performed molecular work. R.G. analysed empirical data. J.R.C. designed and implemented the model and wrote its description. R.G. drafted the manuscript, after which all other authors contributed to revisions. All authors discussed the results and implications of the study at all stages.

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Correspondence to Rosalyn Gloag.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

Supplementary description of modelling, Supplemetary Figures 1 and 2, and Supplementary Tables 1–4. (PDF 1355 kb)

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Gloag, R., Ding, G., Christie, J. et al. An invasive social insect overcomes genetic load at the sex locus. Nat Ecol Evol 1, 0011 (2017). https://doi.org/10.1038/s41559-016-0011

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