A Nightmare for Males? A Maternally Transmitted Male-Killing Bacterium and Strong Female Bias in a Green Lacewing Population

PLoS One. 2016 Jun 15;11(6):e0155794. doi: 10.1371/journal.pone.0155794. eCollection 2016.

Abstract

For maternally transmitted microbes, a female-biased host sex ratio is of reproductive advantage. Here we found a strong female bias in a field population of the green lacewing, Mallada desjardinsi (Insecta; Neuroptera). This bias was attributed to the predominance of individuals harboring a maternally inherited male-killing bacterium that was phylogenetically closely related to the plant-pathogenic Spiroplasma phoeniceum and Spiroplasma kunkelii. Among 35 laboratory-reared broods produced by wild-caught females, 21 broods (60%)-all infected with Spiroplasma-consisted of only females (940 individuals). Among 14 broods consisting of both males and females (516 and 635 individuals, respectively), 4 broods were doubly infected with Spiroplasma and Rickettsia, 6 broods were singly infected with Rickettsia, and 3 broods were uninfected (remaining one brood was unknown). Mortality during embryonic and larval development was prominent in all-female broods but not in normal sex ratio broods. Following antibiotic treatment on all-female broods, mortality was significantly reduced and the sex ratio was restored to 1:1. Strong expression and high prevalence of this male-killer is remarkable considering its low density (~10-5-10-4 cells per host mitochondrial gene copy based on quantitative PCR). In addition, a bacterium closely related to Rickettsia bellii was present in 25 of 34 broods (73.5%), irrespective of the sex ratio, with the infection density comparable to other cases of endosymbiosis (~10-2-10-1 cells per mitochondrial gene copy). Higher density of Rickettsia than Spiroplasma was also demonstrated by electron microscopy which visualized both Spiroplasma-like cells and Rickettsia-like cells inside and outside the ovarian cells.

MeSH terms

  • Animals
  • Anti-Bacterial Agents / pharmacology
  • DNA, Bacterial / chemistry
  • DNA, Bacterial / genetics
  • Female
  • Host-Pathogen Interactions / drug effects
  • Insecta / microbiology*
  • Larva / drug effects
  • Larva / microbiology
  • Male
  • Microscopy, Electron, Transmission
  • Ovary / microbiology
  • Ovary / ultrastructure
  • Phylogeny
  • RNA, Ribosomal, 16S / genetics
  • Rickettsia / classification
  • Rickettsia / genetics
  • Rickettsia / physiology*
  • Sequence Analysis, DNA
  • Sex Factors
  • Sex Ratio
  • Spiroplasma / classification
  • Spiroplasma / genetics
  • Spiroplasma / physiology*
  • Symbiosis
  • Tetracycline / pharmacology

Substances

  • Anti-Bacterial Agents
  • DNA, Bacterial
  • RNA, Ribosomal, 16S
  • Tetracycline

Grant support

This work was financially supported by KAKENHI, a Grant-in-Aid for Scientific Research (https://www.jsps.go.jp/english/e-grants/), grant No. 25450492 for DK, and by internal grants from the National Institute of Agrobiological Sciences and Chiba University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. There was no additional external funding received for this study.