Single-locus complementary sex determination in the inbreeding wasp Euodynerus foraminatus Saussure (Hymenoptera: Vespidae)

Abstract

The Hymenoptera have arrhenotokous haplodiploidy in which males normally develop from unfertilized eggs and are haploid, while females develop from fertilized eggs and are diploid. Multiple sex determination systems are known to underlie haplodiploidy, and the best understood is singlelocus complementary sex determination (sl-CSD) in which sex is determined at a single polymorphic locus. Individuals heterozygous at the sex locus develop as females; individuals that are hemizygous (haploid) or homozygous (diploid) at the sex locus develop as males. sl-CSD can be detected with inbreeding experiments that produce diploid males in predictable proportions as well as sex ratio shifts due to diploid male production. This sex determination system is considered incompatible with inbreeding because the ensuing increase in homozygosity increases the production of diploid males that are inviable or infertile, imposing a high cost on matings between close relatives. However, in the solitary hunting wasp Euodynerus foraminatus, a species suspected of having sl-CSD, inbreeding may be common due to a high incidence of sibling matings at natal nests. In laboratory crosses with E. foraminatus, we find that sex ratios and diploid male production (detected as microsatellite heterozygosity) are consistent with sl-CSD, but not with other sex determination systems. This is the first documented example of sl-CSD in a hymenopteran with an apparent natural history of inbreeding, and thus presents a paradox for our understanding of hymenopteran genetics.

Functionally reproductive diploid and haploid males in an inbreeding hymenopteran with complementary sex determination

“…The information from this handful of examples has been expanded to a general assumption regarding many other species for which data are lacking. The wasp E. foraminatus stands in contrast because it has sl-CSD, high natural levels of inbreeding, and diploid males with normal viability (37,38). Furthermore, in this study we have found that diploid E. foraminatus males have near-normal fertility.…”

“…In unmatched matings, all of a female's fertilized eggs develop as an uninterrupted series of daughters in the innermost part of the nest, but in matched matings, half of the fertilized eggs will develop randomly as diploid males. These diploid males can sometimes be recognized by their ''out-of-order'' nest position if they are followed within the nest by a cell in which a female develops (38).…”

“…Behavioral observations and population genetic data indicate that up to 66% of females mate with a brother at their natal nest before dispersing, and the remaining females mate randomly in the population after dispersal (36,37). However, laboratory breeding experiments confirm that E. foraminatus has sl-CSD and that the resulting diploid males have egg-to-adult viability comparable to haploid males (38). If diploid males in E. foraminatus are the genetic dead end that they are in other species, then this wasp should be suffering a significant sex determination load because of the production of diploid males and possibly an additional loss in fitness to any female that mates with a diploid male and produces sterile triploid offspring.…”

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

“…The genetic load associated with the production of inviable or sterile diploid males makes multiple origins of CSD seem unlikely (Crozier, 1971;Bull, 1981), but it may be that the ancestral status of CSD needs to be reconsidered. In particular, the recent finding of functionally reproductive diploid males in a vespid provides an evolutionary mechanism by which the disadvantages associated with diploid male production can be greatly attenuated Stahlhut and Cowan, 2004). Second, the mode of sex determination may be very evolutionary labile in the Braconidae (and perhaps other taxa) making broad-scale phylogeny a poor predictor of sex determination mechanism.…”

Single-locus sex determination in the parasitoid wasp Cotesia glomerata (Hymenoptera: Braconidae)

“…In Hymenoptera, sl-CSD has been found in at least 20 nonsocial and two social species (Cook, 1993;Butcher et al, 2000a;Beukeboom, 2001;Salin et al, 2004;Stahlhut and Cowan, 2004). The molecular basis of sl-CSD has been revealed in the honeybee, Apis mellifera, in which heterozygotes at the sex-determination locus develop into females and homozygotes or hemizygotes into males (Beye et al, 2003).…”