Feminizing Wolbachia endosymbiont disrupts maternal sex chromosome inheritance in a butterfly species

Daisuke Kageyama, Mizuki Ohno, Tatsushi Sasaki, Atsuo Yoshido, Tatsuro Konagaya, Akiya Jouraku, Seigo Kuwazaki, Hiroyuki Kanamori, Yuichi Katayose, Satoko Narita, Mai Miyata, Markus Riegler, Ken Sahara

Research output: Contribution to journalArticlepeer-review

37 Citations (Scopus)

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.
Original languageEnglish
Pages (from-to)232-244
Number of pages13
JournalEvolution Letters
Volume1
Issue number5
DOIs
Publication statusPublished - 2017

Open Access - Access Right Statement

©2017 The Authors Evolution Letters published by Wiley Periodicals, Inc. on behalf of Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEB). This is an open access article under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Keywords

  • Wolbachia
  • butterflies
  • sex chromosomes
  • sex determination

Fingerprint

Dive into the research topics of 'Feminizing Wolbachia endosymbiont disrupts maternal sex chromosome inheritance in a butterfly species'. Together they form a unique fingerprint.

Cite this