Balancing selection maintains sex determining alleles in multiple-locus complementary sex determination

Jerome J. Weis, Paul J. Ode, George E. Heimpel

Research output: Contribution to journalArticlepeer-review

7 Scopus citations


Hymenopteran species in which sex is determined through a haplo-diploid mechanism known as complementary sex determination (CSD) are vulnerable to a unique form of inbreeding depression. Diploids heterozygous at one or more CSD loci develop into females but diploids homozygous at all loci develop into diploid males, which are generally sterile or inviable. Species with multiple polymorphic CSD loci (ml-CSD) may have lower rates of diploid male production than species with a single CSD locus (sl-CSD), but it is not clear if polymorphism is consistently maintained at all loci. Here, we assess the rate of diploid male production in a population of Cotesia rubecula, a two-locus CSD parasitoid wasp species, approximately 20 years after the population was introduced for biological control. We show that diploid male production dropped from 8–13% in 2005 and 2006 to 3–4% by 2015. We also show from experimental crosses that the population maintained polymorphism at both CSD loci in 2015. We use theory and simulations to show that balancing selection on all CSD alleles promotes polymorphism at several loci in ml-CSD populations. Our study supports the hypothesis that ml-CSD populations have lower diploid male production and are more likely to persist than comparable sl-CSD populations.

Original languageEnglish (US)
Pages (from-to)1246-1257
Number of pages12
Issue number5
StatePublished - May 2017

Bibliographical note

Funding Information:
JJW, PJO, and GEH contributed research ideas and collaborated in writing the manuscript. PJO and GEH provided funding. GEH provided laboratory space and supplies. JJW lead data collection efforts, analyzed data, and wrote code for analyses and simulations. We thank C. Tchida, A. Talbot, and M. Rogers for access to Brassica plantings in Minnesota and Mountain View Farm and Intervale Farm for access to plantings in Massachusetts. We thank R. van Driesche for help coordinating field sampling in Massachusetts. We thank M. Rengstorf, H. Gray, M. Matos, and B. Stevens for help with field and laboratory work. We also thank T. Martin, J. Motl, and the staff at the University Flow Cytometry Resource (University of Minnesota) for assistance with flow cytometry. We thank R. Kraus, A. Bompard, and two anonymous reviewers for helpful comments through Axios Review which improved this manuscript. We conducted all computer simulations through the Minnesota Supercomputing Institute and we thank L. Mills for technical assistance. Funding was provided by a grant from the United States Department of Agriculture (USDA-NIFA 2014-67013-21727) and the University of Minnesota Agricultural Experiment Station. The doi for our data is: 10.5061/dryad.c9d3j.

Publisher Copyright:
© 2017 The Author(s). Evolution © 2017 The Society for the Study of Evolution.


  • Biological control
  • Cotesia rubecula
  • diploid male
  • haplo-diploidy
  • hymenoptera
  • rare allele advantage


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