Feminization and the collapse of haplodiploidy in an asexual parasitoid wasp harboring the bacterial symbiont Cardinium

Abstract

Cardinium is a bacterial symbiont infecting many species of arthropods, and is associated with manipulation of host reproduction. Cardinium is the causal agent of asexual reproduction, or thelytoky, in the chalcidoid parasitoid wasp Encarsia hispida. Feeding antibiotics to the infected adult females results in uninfected male offspring. Here, we show that these males are diploid. Diploid males are extremely unusual in the large hymenopteran superfamily Chalcidoidea, and, to our knowledge, have never before been associated with symbiont infection in this group. These findings indicate that at least in E. hispida, diploidy restoration is a necessary condition but not sufficient to elicit female development. Cardinium is required to feminize diploid male embryos and thus must interact with elements of the host sex determination system. In addition, our data suggest that Cardinium is necessary for the fertility of E. hispida; antibiotic curing of Cardinium reduces offspring production of adult females.

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“…In recent years, another a-proteobacterium, Rickettsia, and the Bacteroidetes Cardinium have also been associated with thelytoky (Hagimori et al, 2006 andZchori-Fein et al, 2004, respectively). The diploid males discovered by Giorgini et al (2009) are a result of antibiotic treatment of E. hispida, which naturally carry a thelytoky-inducing Cardinium. Interestingly, bacteriainduced thelytoky has only been discovered in non-CSD hymenopterans, and the common assumption has been that the symbiont is simply involved in producing females from unfertilized, incipient male eggs by restoring diploidy.…”

“…When a nonimprinted chromosomal set (of paternal origin) is present, it compensates for the imprinted location and the embryo develops into a female (Beukeboom et al, 2007). The report by Giorgini et al (2009) suggests that imprinting present in a restored diploid genome may also allow male development (whatever the mechanism of restoration of diploidy) (Figure 1). Indeed, as stated in the title of the Giorgini et al (2009) study, Cardinium in E. hispida does not restore diploidy but acts as a feminizer of an already diploid product.…”

“…The report by Giorgini et al (2009) suggests that imprinting present in a restored diploid genome may also allow male development (whatever the mechanism of restoration of diploidy) (Figure 1). Indeed, as stated in the title of the Giorgini et al (2009) study, Cardinium in E. hispida does not restore diploidy but acts as a feminizer of an already diploid product. Feminization has been attributed to Cardinium in a haplodiploid mite in a previous study (Weeks et al, 2001).…”

“…Giorgini et al (2009) hypothesized that Cardinium may be involved in the reversal from haplodiploidy to the ancestral state of diplodiploidy. However, a problem with this proposal is that diploid males in Hymenoptera with CSD are in most cases inviable or sterile, and sterility is also the norm amongst antibiotic-induced males.…”

“…Under CSD, fertilized diploid eggs can result in diploid males if they are homozygous at the relevant loci, perhaps due to inbreeding. In this issue, Giorgini et al (2009) present another example of diploid males, in the parasitoid wasp Encarsia hispida of the Chalcidoidea family. But this superfamily does not exhibit CSD, and diploid males were thought to be virtually absent.…”