Population structure, mating system, and sex-determining allele diversity of the parasitoid wasp Habrobracon hebetor

Abstract

Besides haplo-diploid sex determination, where females develop from fertilized diploid eggs and males from unfertilized haploid eggs, some Hymenoptera have a secondary system called complementary sex determination (CSD). This depends on genotypes of a 'sex locus' with numerous sex-determining alleles. Diploid heterozygotes develop as females, but diploid homozygotes become sterile or nonviable diploid males. Thus, when females share sexdetermining alleles with their mates and produce low fitness diploid males, CSD creates a genetic load. The parasitoid wasp Habrobracon hebetor has CSD and displays mating behaviours that lessen CSD load, including mating at aggregations of males and inbreeding avoidance by females. To examine the influence of population structure and the mating system on CSD load, we conducted genetic analyses of an H. hebetor population in Wisconsin. Given the frequency of diploid males, we estimated that the population harboured 10-16 sex-determining alleles. Overall, marker allele frequencies did not differ between subpopulations, but frequencies changed dramatically between years. This reduced estimates of effective size of subpopulations to only N e B20-50, which probably reflected annual fluctuations of abundance of H. hebetor. We also determined that the mating system is effectively monogamous. Models relating sex-determining allele diversity and the mating system to female productivity showed that inbreeding avoidance always decreased CSD loads, but multiple mating only reduced loads in populations with fewer than five sexdetermining alleles. Populations with N e less than 100 should have fewer sex-determining alleles than we found, but high diversity could be maintained by a combination of frequencydependent selection and gene flow between populations.

Effective population size in Hymenoptera with complementary sex determination

“…Hymenopteran species usually exhibit lower levels of genetic variation, when compared to diploid insects (reviewed by Packer and Owen, 2001) even when the confounding effects of haplodiploidy and social behavior are removed (Hedrick and Parker, 1997;Packer and Owen, 2001), consistent with the present analysis. Surprisingly low empirical estimates of N e (5100) for natural hymenopteran populations (Zayed and Packer, 2001;Antolin et al, 2003;Zayed et al, 2004) also lend support to the view that hymenopterans with CSD have lower N e than previously expected.…”

Single-locus complementary sex determination absent in Heterospilus prosopidis (Hymenoptera: Braconidae)

“…However, a minimum level of f/2 developmental mortality is expected under these conditions, so that threshold levels of developmental mortality are required for any given level of secondary sex ratio to be consistent with CSD. These relationships are captured by the expression for secondary sex ratio (r) as a function of the fertilization rate (f) and the rate of diploid male survival (d) under sl-CSD (Cook, 1993a;Heimpel et al, 1999;Antolin et al, 2003): Figure 1 Combinations of developmental mortality and secondary sex ratio that are consistent with sl-CSD under six levels of diploid males survivorship. Gray denotes the parameter space that is consistent with sl-CSD over all possible fertilization rates.…”

Experimental Support for Multiple-Locus Complementary Sex Determination in the Parasitoid Cotesia vestalis

“…Sex determination and inbreeding are intimately related in the Hymenoptera (Hamilton 1967), and population-level conse-quences of CSD are potentially severe (Zayed and Packer 2005). Fundamental knowledge on sex determination could be used to improve the effectiveness with which hymenopterans are used as biological control agents of pest insects and as pollinators (Stouthamer et al 1992;Heimpel et al 1999;Heimpel and Lundgren 2000;Antolin et al 2003;Ode and Hardy 2008). In addition, knowledge of the genetics of sex determination could be used in conservation management of natural populations of pollinating hymenopterans, many of which are declining (Zayed and Packer 2005;Biesmeijer et al 2006).…”