FeminizingWolbachiaendosymbiont disrupts maternal sex chromosome inheritance in a butterfly species

Abstract

Wolbachia is a maternally inherited ubiquitous endosymbiotic bacterium of arthropods that displays a diverse repertoire of host reproductive manipulations. For the first time, we demonstrate that Wolbachia manipulates sex chromosome inheritance in a sexually reproducing insect. Eurema mandarina butterfly females on Tanegashima Island, Japan, are infected with the wFem Wolbachia strain and produce all‐female offspring, while antibiotic treatment results in male offspring. Fluorescence in situ hybridization (FISH) revealed that wFem‐positive and wFem‐negative females have Z0 and WZ sex chromosome sets, respectively, demonstrating the predicted absence of the W chromosome in wFem‐infected lineages. Genomic quantitative polymerase chain reaction (qPCR) analysis showed that wFem‐positive females lay only Z0 eggs that carry a paternal Z, whereas females from lineages that are naturally wFem‐negative lay both WZ and ZZ eggs. In contrast, antibiotic treatment of adult wFem females resulted in the production of Z0 and ZZ eggs, suggesting that this Wolbachia strain can disrupt the maternal inheritance of Z chromosomes. Moreover, most male offspring produced by antibiotic‐treated wFem females had a ZZ karyotype, implying reduced survival of Z0 individuals in the absence of feminizing effects of Wolbachia. Antibiotic treatment of wFem‐infected larvae induced male‐specific splicing of the doublesex (dsx) gene transcript, causing an intersex phenotype. Thus, the absence of the female‐determining W chromosome in Z0 individuals is functionally compensated by Wolbachia‐mediated conversion of sex determination. We discuss how Wolbachia may manipulate the host chromosome inheritance and that Wolbachia may have acquired this coordinated dual mode of reproductive manipulation first by the evolution of female‐determining function and then cytoplasmically induced disruption of sex chromosome inheritance.

Sex chromosomes control vertical transmission of feminizing Wolbachia symbionts in an isopod

“…Our results show that sex chromosome genotype represents yet another case of host nuclear control over symbiont transmission. Wolbachia symbionts were previously found to prevent sex chromosome transmission in Eurema mandarina butterflies [46]. Here we show that sex chromosomes can prevent Wolbachia transmission in A. nasatum , thereby offering a whole new perspective on the molecular interplay between feminizing symbionts and host sex chromosomes.…”

Persistence of aWolbachia-driven sex ratio bias in an island population ofEuremabutterflies

“…Males were stored at −30°C until DNA extraction. After allowing females to lay eggs in the laboratory for other experiments [21,24], bursa copulatrixes and Malpighian tubules were dissected out from them and the remains were stored at −30°C until DNA extraction.…”

“…It was recently revealed that, like the majority of lepidopteran insects, C females have the WZ karyotype and C males have the ZZ karyotype. In contrast, CF females have the Z0 karyotype [23,24]. By mating with C males, CF females produce embryos that are all Z0, whose Z chromosomes are paternally derived (i.e., Wolbachia -induced disruption of maternal inheritance of the Z chromosome).…”

“…By mating with C males, CF females produce embryos that are all Z0, whose Z chromosomes are paternally derived (i.e., Wolbachia -induced disruption of maternal inheritance of the Z chromosome). In the presence of w Fem, Z0 individuals are determined as female (i.e., Wolbachia -induced feminization), which would otherwise be determined as male in the absence of Wolbachia [24]. The remarkable difference between this phenotype and male killing is that the removal of Wolbachia results in all-male offspring in this phenotype [20,24] but both male and female offspring in other systems where male killing occurs.…”

“…In the presence of w Fem, Z0 individuals are determined as female (i.e., Wolbachia -induced feminization), which would otherwise be determined as male in the absence of Wolbachia [24]. The remarkable difference between this phenotype and male killing is that the removal of Wolbachia results in all-male offspring in this phenotype [20,24] but both male and female offspring in other systems where male killing occurs. Therefore, in CF females, cytoplasmic elements such as mitochondria cannot be transmitted to subsequent generations in the absence of Wolbachia —a state of evolutionary addiction to Wolbachia .…”