Diploid males support a two-step mechanism of endosymbiont-induced thelytoky in a parasitoid wasp

Abstract

BackgroundHaplodiploidy, where females develop from diploid, fertilized eggs and males from haploid, unfertilized eggs, is abundant in some insect lineages. Some species in these lineages reproduce by thelytoky that is caused by infection with endosymbionts: infected females lay haploid eggs that undergo diploidization and develop into females, while males are very rare or absent. It is generally assumed that in thelytokous wasps, endosymbionts merely diploidize the unfertilized eggs, which would then trigger female development.ResultsWe found that females in the parasitoid wasp Asobara japonica infected with thelytoky-inducing Wolbachia produce 0.7–1.2 % male offspring. Seven to 39 % of these males are diploid, indicating that diploidization and female development can be uncoupled in A. japonica. Wolbachia titer in adults was correlated with their ploidy and sex: diploids carried much higher Wolbachia titers than haploids, and diploid females carried more Wolbachia than diploid males. Data from introgression lines indicated that the development of diploid individuals into males instead of females is not caused by malfunction-mutations in the host genome but that diploid males are most likely produced when the endosymbiont fails to activate the female sex determination pathway. Our data therefore support a two-step mechanism by which endosymbionts induce thelytoky in A. japonica: diploidization of the unfertilized egg is followed by feminization, whereby each step correlates with a threshold of endosymbiont titer during wasp development.ConclusionsOur new model of endosymbiont-induced thelytoky overthrows the view that certain sex determination mechanisms constrain the evolution of endosymbiont-induced thelytoky in hymenopteran insects. Endosymbionts can cause parthenogenesis through feminization, even in groups in which endosymbiont-diploidized eggs would develop into males following the hosts’ sex determination mechanism. In addition, our model broadens our understanding of the mechanisms by which endosymbionts induce thelytoky to enhance their transmission to the next generation. Importantly, it also provides a novel window to study the yet-poorly known haplodiploid sex determination mechanisms in haplodiploid insects.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0370-9) contains supplementary material, which is available to authorized users.

FeminizingWolbachiaendosymbiont disrupts maternal sex chromosome inheritance in a butterfly species

“…5B). This is similar to the dual role of Wolbachia and Cardinium in haplodiploid parasitoid wasps where they induce thelytokous parthenogenesis in a two-step mechanism, comprising diploidization of the unfertilized egg followed by feminization (Giorgini et al 2009;Ma et al 2015). Here, we develop the potential evolutionary scenario that led to the appearance of both effects in E. mandarina (Fig.…”

“…; Ma et al. ). Here, we develop the potential evolutionary scenario that led to the appearance of both effects in E. mandarina (Fig.…”

Life‐history traits of the Whiting polyploid line of the parasitoid Nasonia vitripennis

“…The offspring sex ratio of those females that mated with the WPL haploid and diploid males in no-choice assays were approximately 0.15, which is not highly divergent from the 0.10 proportion that is possible when mated females have ideal conditions (i.e., low competition, high host quality) (Whiting, 1967). In at least one other non-CSD species (the braconid wasp Asobara japonica Belokobylskij) diploid males are also capable of producing many triploid daughters, although they do not sire as many offspring as haploids (Ma et al, 2015). These CSD species with fertile diploid males are capable of producing daughters.…”

“…Inbreeding does not cause polyploidy in non-CSD species, and polyploidy in non-CSD species may not lead to sterile diploid males (e.g., Whiting, 1960;Ma et al, 2015). Inbreeding does not cause polyploidy in non-CSD species, and polyploidy in non-CSD species may not lead to sterile diploid males (e.g., Whiting, 1960;Ma et al, 2015).…”

Wolbachia Associations with Insects: Winning or Losing Against a Master Manipulator

“…Cardinium, is another symbiont causing similar reproductive alterations as Wolbachia (Giorgini et al, 2009;Ma et al, 2015). In the haplodiploid wasp Encarsia it has been shown that the Cardinium infection doesn't induce, as expected, thelytokous parthenogenesis, but feminization.…”