Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

An invasive social insect overcomes genetic load at the sex locus

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

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.

References

  1. 1

    Lowe, S. J., Browne, M., Boudjelas, S. & De Poorter, M. 100 of the World’s Worst Invasive Species: a Selection from the Global Invasive Species Database (Invasive Species Specialist Group, Species Survival Commission, World Conservation Union, 2000).

    Google Scholar 

  2. 2

    Foucaud, J. et al. Worldwide invasion by the little fire ant: routes of introduction and eco-evolutionary pathways. Evol. Appl. 3, 363–374 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  3. 3

    Schneider, S. S., DeGrandi-Hoffman, G. & Smith, D. R. The African honey bee: factors contributing to a successful biological invasion. Annu. Rev. Entomol. 49, 351–376 (2004).

    CAS  Article  Google Scholar 

  4. 4

    Beggs, J. R. et al. Ecological effects and management of invasive alien Vespidae. BioControl 56, 505–526 (2011).

    Article  Google Scholar 

  5. 5

    Holway, D. A., Lach, L., Suarez, A. V., Tsutsui, N. D. & Case, T. J. The causes and consequences of ant invasions. Annu. Rev. Ecol. Syst. 33, 181–233 (2002).

    Article  Google Scholar 

  6. 6

    Monceau, K., Bonnard, O. & Thiéry, D. Vespa velutina: a new invasive predator of honeybees in Europe. J. Pest Sci. 87, 1–16 (2013).

    Article  Google Scholar 

  7. 7

    MacIntyre, P. & Hellstrom, J. An Evaluation of the Costs of Pest Wasps (Vespula Species) in New Zealand (Department of Conservation and Ministry for Primary Industries, 2015).

    Google Scholar 

  8. 8

    Heimpel, G. E. & de Boer, J. G. Sex determination in the Hymenoptera. Annu. Rev. Entomol. 53, 209–230 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 9

    Beye, M., Hasselmann, M., Fondrk, M. K., Page, R. E. & Omholt, S. W. The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114, 419–429 (2003).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. 10

    Sakai, A. K. et al. The population biology of invasive species. Annu. Rev. Ecol. Evol. Syst. 32, 305–332 (2001).

    Article  Google Scholar 

  11. 11

    Dlugosch, K. M. & Parker, I. M. Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol. Ecol. 17, 431–449 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12

    Ross, K. G. & Shoemaker, D. D. Estimation of the number of founders of an invasive pest insect population: the fire ant Solenopsis invicta in the USA. Proc. R. Soc. B 275, 2231–2240 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  13. 13

    Zayed, A. & Packer, L. Complementary sex determination substantially increases extinction proneness of haplodiploid populations. Proc. Natl Acad. Sci. USA 102, 10742–10746 (2005).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 14

    van Wilgenburg, E., Driessen, G. & Beukeboom, L. W. Single locus complementary sex determination in Hymenoptera: an “unintelligent” design? Front. Zool. 3, 1 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  15. 15

    Whitehorn, P. R., Tinsley, M. C., Brown, M. J., Darvill, B. & Goulson, D. Impacts of inbreeding on bumblebee colony fitness under field conditions. BMC Evol. Biol. 9, 152 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  16. 16

    Hedrick, P. W., Gadau, J. & Page, R. E. Jr. Genetic sex determination and extinction. Trends Ecol. Evol. 21, 55–57 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17

    Lechner, S. et al. Nucleotide variability at its limit? Insights into the number and evolutionary dynamics of the sex-determining specificities of the honey bee Apis mellifera . Mol. Biol. Evol. 31, 272–287 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  18. 18

    Hasselmann, M. & Beye, M. Signatures of selection among sex-determining alleles of the honey bee. Proc. Natl Acad. Sci. USA 101, 4888–4893 (2004).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. 19

    Oldroyd, B. P. et al. Evolution of mating behaviour in the genus Apis and an estimate of mating frequency in Apis cerana (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 91, 700–709 (1998).

    CAS  Article  Google Scholar 

  20. 20

    Beye, M. et al. Gradual molecular evolution of a sex determination switch through incomplete penetrance of femaleness. Curr. Biol. 23, 2559–2564 (2013).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. 21

    Yokoyama, S. & Nei, M. Population dynamics of sex-determining alleles in honey bees and self-incompatibility alleles of plants. Genetics 91, 609–636 (1976).

    Google Scholar 

  22. 22

    Woyke, J. Population genetic studies on sex alleles in the honeybee using the example of the Kangaroo Island Bee Sanctuary. J. Apicult. Res. 15, 105–125 (1976).

    Article  Google Scholar 

  23. 23

    Cook, J. M. & Crozier, R. H. Sex determination and population biology in the Hymenoptera. Trends Ecol. Evol. 10, 281–286 (1996).

    Article  Google Scholar 

  24. 24

    Woyke, J. Effect of sex allele homo-heterozygosity on honeybee colony populations and on their honey production: 2. Unfavourable development conditions and restricted queens. J. Apicult. Res. 20, 148–155 (1981).

    Article  Google Scholar 

  25. 25

    Woyke, J. Sex determination in Apis cerana indica. J. Apicult. Res. 18, 122–127 (1979).

    Article  Google Scholar 

  26. 26

    Aguilar, A. et al. High MHC diversity maintained by balancing selection in an otherwise genetically monomorphic mammal. Proc. Natl Acad. Sci. USA 101, 3490–3494 (2004).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 27

    Azevedo, L., Serrano, C., Amorim, A. & Cooper, D. N. Trans-species polymorphism in humans and the great apes is generally maintained by balancing selection that modulates the host immune response. Hum. Genom. 9, 21 (2015).

    Article  Google Scholar 

  28. 28

    Goudie, F., Allsopp, M. H. & Oldroyd, B. P. Selection on overdominant genes maintains heterozygosity along multiple chromosomes in a clonal lineage of honey bee. Evolution 68, 125–136 (2014).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. 29

    Hedrick, P. W. What is the evidence for heterozygote advantage selection? Trends Ecol. Evol. 27, 698–704 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  30. 30

    Wenink, P. W., Groen, A. F., Roelke-Parker, M. E. & Prins, H. H. T. African buffalo maintain high genetic diversity in the major histocompatibility complex in spite of historically known population bottlenecks. Mol. Ecol. 7, 1315–1322 (1998).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. 31

    Ross, K. G., Vargo, E. L., Keller, L. & Trager, J. C. Effect of a founder event on variation in the genetic sex-determining system of the fire ant Solenopsis invicta . Genetics 135, 843–854 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. 32

    Zayed, A., Constantin, S. A. & Packer, L. Successful biologial invasion despite a severe genetic load. PLoS ONE 2, e868 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  33. 33

    Koetz, A. H. Ecology, behaviour and control of Apis cerana with a focus on relevance to the Australian incursion. Insects 4, 558–592 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  34. 34

    Hasselmann, M. et al. Evidence for convergent nucleotide evolution and high allelic turnover rates at the complementary sex determiner gene of Western and Asian honeybees. Mol. Biol. Evol. 25, 696–708 (2008).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 35

    Walsh, P. S., Metzger, D. A. & Higuchi, R. Chelex-100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10, 506–513 (1991).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36

    Cho, S., Huang, Z. Y., Green, D. R., Smith, D. R. & Zhang, J. Evolution of the complementary sex-determination gene of honey bees: Balancing selection and trans-species polymorphisms. Genome Res. 16, 1366–1375 (2006).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  37. 37

    Hasselmann, M. et al. Evidence for the evolutionary nascence of a novel sex determination pathway in honeybees. Science 454, 519–523 (2008).

    CAS  Google Scholar 

  38. 38

    Hyink, O., Laas, F. & Dearden, P. K. Genetic tests for alleles of complementary-sex-determiner to support honeybee breeding programmes. Apidologie 44, 306–313 (2012).

    Article  Google Scholar 

  39. 39

    Takahashi, J. et al. Variable microsatellite loci isolated from the Asian honeybee, Apis cerana (Hymenoptera; Apidae). Mol. Ecol. Resour. 9, 819–821 (2009).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. 40

    Solignac, M. et al. Five hundred and fifty microsatellite markers for the study of the honeybee (Apis mellifera L.) genome. Mol. Ecol. Notes 3, 307–311 (2003).

    CAS  Article  Google Scholar 

  41. 41

    Nielsen, R., Tarpy, D. R. & Reeve, H. K. Estimating effective paternity number in social insects and the effective number of alleles in a population. Mol. Ecol. 12, 3157–3164 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  42. 42

    Ruttner, H. & Ruttner, F. Investigations on the flight activity and the mating behaviour of drones. V: drone congration areas and mating distance. Apidologie 3, 203–232 (1972).

    Article  Google Scholar 

  43. 43

    Hinson, E. M., Duncan, M., Lim, J., Arundel, J. & Oldroyd, B. P. The density of feral honey bee (Apis mellifera) colonies in South East Australia is greater in undisturbed than in disturbed habitat. Apidologie 46, 403 (2015).

    Article  Google Scholar 

  44. 44

    Oldroyd, B. P., Thexton, E. G., Lawler, S. H. & Crozier, R. H. Population demongraphy of Australian feral bees (Apis mellifera). Oecologia 111, 381–387 (1997).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. 45

    Abrol, D. P. Asiatic Honeybee Apis cerana Biodiversity Conservation and Agricultural Production Ch. 3 (Springer, 2013).

    Book  Google Scholar 

Download references

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.

Author information

Affiliations

Authors

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.

Corresponding author

Correspondence to Rosalyn Gloag.

Ethics declarations

Competing interests

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)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing