Feminizing <i>Wolbachia</i> endosymbiont disrupts maternal sex chromosome inheritance in a butterfly species

Kageyama, Daisuke; Ohno, Mizuki; Sasaki, Tatsushi; Yoshido, Atsuo; Konagaya, Tatsuro; Jouraku, Akiya; Kuwazaki, Seigo; Kanamori, Hajime; Katayose, Yūichi; Narita, Satoko; Miyata, Mikio; Riegler, Markus; Sahara, Ken

doi:10.1101/115386

Cited by 11 publications

(17 citation statements)

References 52 publications

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“…However, alternative possibilities still remain such as mitochondrial introgression together with wFem from another yet unknown Eurema species or horizontal transmission of Wolbachia multiple times in E. hecabe but only once in E. mandarina. Unlike the male-killing cases, the appearance of a suppressor against MD in the host would result in all males [2,8], leading to the elimination of Wolbachia as well as the accompanying mtDNA from the population.…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies revealed that E. mandarina C females have the WZ sex chromosome system, whereas CF females have the Z0 sex chromosome system [2,11]. Wolbachia was found to affect female meiosis and prevent the production of Z-bearing oocytes, thereby producing exclusively Z0 embryos that carry a paternal Z.…”

Section: Introductionmentioning

confidence: 99%

“…Wolbachia was found to affect female meiosis and prevent the production of Z-bearing oocytes, thereby producing exclusively Z0 embryos that carry a paternal Z. Moreover, Wolbachia is responsible for female sex determination in Z0 individuals, which would otherwise be determined as males owing to the absence of the female-determining W chromosome [2]. Therefore, the Wolbachia-induced coordinated dual effects (i.e.…”

Section: Introductionmentioning

confidence: 99%

“…Among 30 wild-caught females of E. mandarina (22 CF and eight C females), Z-linked Tpi (430 bp) was polymorphic in 31 nucleotide sites, constituting 24 haplotypes. Because the Z is driven out of Z0 females[2], Tpi is always a marker of paternal origin in CF females. The maximum-likelihood (ML) tree based on Tpi did not show any signs of divergence between CF and C lineages (figure 2a), indicating that CF and C lineages share a common gene pool through males.By contrast, ML trees based on mtDNA exhibited a clear distinction between CF and C (figure 2b).…”

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confidence: 99%

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Wolbachia -induced meiotic drive and feminization is associated with an independent occurrence of selective mitochondrial sweep in a butterfly

et al. 2017

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Maternally inherited endosymbionts manipulate arthropod reproduction in various ways. In the butterfly, a cytoplasmic incompatibility-inducing strainCI and the associated mtDNA haplotypes are known to originate from the sister species , which offered a good case study for microbe-mediated hybrid introgression. BesidesCI, some females with the Z0 karyotype harbour a distinct strainFem, which causes all-female production by meiotic drive and feminization. We report that a considerable proportion of females (65.7%) were infected with bothCI and Fem (CF) on Tanegashima Island. While females singly infected withCI (C) produced offspring at a 1 : 1 sex ratio, CF females produced only females. Although Z-linked sequence polymorphism showed no signs of divergence between C and CF females, mtDNA split into two discrete clades; one consisted of C females and the other CF females, both of which formed a clade with but not with uninfected This suggests that CF matrilines also, but independently, experienced a selective sweep after hybrid introgression from Distinct evolutionary forces were suggested to have caused C and CF matrilines to diverge, which would be irreversible because of the particular phenotype ofFem.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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Wolbachia -induced meiotic drive and feminization is associated with an independent occurrence of selective mitochondrial sweep in a butterfly

et al. 2017

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“…Wolbachia is normally transmitted vertically, from mother to offspring, and can manipulate the host’s reproduction through five mechanisms: cytoplasmic incompatibility, parthenogenesis, male killing, feminization ( Cordaux, Bouchon & Grève, 2011 ) and meiotic drive ( Kageyama et al, 2017 ). However, there is evidence that Wolbachia can be horizontally transmitted ( Vavre et al, 1999 ; Cordaux, Michel-Salzat & Bouchon, 2001 ; Raychoudhury et al, 2009 ; Kraaijeveld et al, 2011 ).…”

Section: Introductionmentioning

confidence: 99%

A bioinformatics approach to identifyingWolbachiainfections in arthropods

Pascar

Chandler

2018

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Wolbachia is the most widespread endosymbiont, infecting >20% of arthropod species, and capable of drastically manipulating the host’s reproductive mechanisms. Conventionally, diagnosis has relied on PCR amplification; however, PCR is not always a reliable diagnostic technique due to primer specificity, strain diversity, degree of infection and/or tissue sampled. Here, we look for evidence of Wolbachia infection across a wide array of arthropod species using a bioinformatic approach to detect the Wolbachia genes ftsZ, wsp, and the groE operon in next-generation sequencing samples available through the NCBI Sequence Read Archive. For samples showing signs of infection, we attempted to assemble entire Wolbachia genomes, and in order to better understand the relationships between hosts and symbionts, phylogenies were constructed using the assembled gene sequences. Out of the 34 species with positively identified infections, eight species of arthropod had not previously been recorded to harbor Wolbachia infection. All putative infections cluster with known representative strains belonging to supergroup A or B, which are known to only infect arthropods. This study presents an efficient bioinformatic approach for post-sequencing diagnosis and analysis of Wolbachia infection in arthropods.

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Mechanistically comparing reproductive manipulations caused by selfish chromosomes and bacterial symbionts

2021

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Insects naturally harbor a broad range of selfish agents that can manipulate their reproduction and development, often leading to host sex ratio distortion. Such effects directly benefit the spread of the selfish agents. These agents include two broad groups: bacterial symbionts and selfish chromosomes. Recent studies have made steady progress in uncovering the cellular targets of these agents and their effector genes. Here we highlight what is known about the targeted developmental processes, developmental timing, and effector genes expressed by several selfish agents. It is now becoming apparent that:(1) the genetic toolkits used by these agents to induce a given reproductive manipulation are simple, (2) these agents target sex-specific cellular processes very early in development, and (3) in some cases, similar processes are targeted. Knowledge of the molecular underpinnings of these systems will help to solve long-standing puzzles and provide new tools for controlling insect pests.

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

Cited by 11 publications

References 52 publications

Wolbachia -induced meiotic drive and feminization is associated with an independent occurrence of selective mitochondrial sweep in a butterfly

Wolbachia -induced meiotic drive and feminization is associated with an independent occurrence of selective mitochondrial sweep in a butterfly

A bioinformatics approach to identifyingWolbachiainfections in arthropods

Mechanistically comparing reproductive manipulations caused by selfish chromosomes and bacterial symbionts

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