A Nightmare for Males? A Maternally Transmitted Male-Killing Bacterium and Strong Female Bias in a Green Lacewing Population.
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.
Graduate School of Horticulture, Chiba University, Matsudo, Chiba, Japan.
Masayuki
M
Hayashi
Insect Microbe Research Unit, National Institute of Agrobiological Sciences, 1-2 Owashi, Tsukuba, Ibaraki, Japan.
Masaya
M
Watanabe
Insect Microbe Research Unit, National Institute of Agrobiological Sciences, 1-2 Owashi, Tsukuba, Ibaraki, Japan.
Fumiko
F
Yukuhiro
Graduate School of Horticulture, Chiba University, Matsudo, Chiba, Japan.
Masashi
M
Nomura
Insect Microbe Research Unit, National Institute of Agrobiological Sciences, 1-2 Owashi, Tsukuba, Ibaraki, Japan.
Daisuke
http://orcid.org/0000-0002-9026-9825
D
Kageyama
D000818:Animals; D000900:Anti-Bacterial Agents / Q000494:pharmacology; D004269:DNA, Bacterial / Q000737:chemistry / Q000235:genetics; D005260:Female; D054884:Host-Pathogen Interactions / Q000187:drug effects; D007313:Insecta / Q000382:microbiology*; D007814:Larva / Q000187:drug effects / Q000382:microbiology; D008297:Male; D046529:Microscopy, Electron, Transmission; D010053:Ovary / Q000382:microbiology / Q000648:ultrastructure; D010802:Phylogeny; D012336:RNA, Ribosomal, 16S / Q000235:genetics; D012281:Rickettsia / Q000145:classification / Q000235:genetics / Q000502:physiology*; D017422:Sequence Analysis, DNA; D012737:Sex Factors; D012744:Sex Ratio; D013149:Spiroplasma / Q000145:classification / Q000235:genetics / Q000502:physiology*; D013559:Symbiosis; D013752:Tetracycline / Q000494:pharmacology
D000900:Anti-Bacterial Agents; D004269:DNA, Bacterial; D012336:RNA, Ribosomal, 16S; D013752:Tetracycline