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Closely Related Male-Killing and Nonmale-Killing Wolbachia Strains in the Oriental Tea Tortrix Homona magnanima

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Abstract

Wolbachia are inherited intracellular bacteria that cause male-specific death in some arthropods, called male-killing. To date, three Wolbachia strains have been identified in the oriental tea tortrix Homona magnanima (Tortricidae, Lepidoptera); however, none of these caused male-killing in the Japanese population. Here, we describe a male-killing Wolbachia strain in Taiwanese H. magnanima. From field-collected H. magnanima, two female-biased host lines were established, and antibiotic treatments revealed Wolbachia (wHm-t) as the causative agent of male-killing. The wsp and MLST genes in wHm-t are identical to corresponding genes in the nonmale-killing strain wHm-c from the Japanese population, implying a close relationship of the two strains. Crossing the Japanese and Taiwanese H. magnanima revealed that Wolbachia genotype rather than the host genetic background was responsible for the presence of the male-killing phenotype. Quantitative PCR analyses revealed that the density of wHm-t was higher than that of other Wolbachia strains in H. magnanima, including wHm-c. The densities of wHm-t were also heterogeneous between host lines. Notably, wHm-t in the low-density and high-density lines carried identical wsp and MLST genes but had distinct lethal patterns. Furthermore, over 90% of field-collected lines of H. magnanima in Taiwan were infected with wHm-t, although not all host lines harboring wHm-t showed male-killing. The host lines that showed male-killing harbored a high density of Wolbachia compared to the host lines that did not show male-killing. Thus, the differences in the phenotypes appear to be dependent on biological and genetic characteristics of closely related Wolbachia strains.

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Acknowledgments

We thank Dr. Utugi Jimbo (National Museum of Nature and Science, Tokyo, Japan) for morphological identification of Taiwanese population of H. magnanima and Dr. Katsuhiko Ito (Tokyo University of Agriculture and Technology, Tokyo, Japan) for lending us the StepOnePlus™ real-time PCR system (Applied Biosystems, Tokyo, Japan). We also thank Dr. Hisashi Anbutsu (National Institute of Advanced Industrial Science and Technology, Tsukuba, Japan) and Professor Greg Hurst (Institute of Integrative Biology, University of Liverpool, Liverpool, UK) for revising the manuscript.

Data Archiving

The sequence data of wsp and MLST genes of wHm-t were deposited in GenBank under accession numbers LC427375 to LC427380.

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Authors and Affiliations

  1. Department of Applied Biological Science, Graduate School of Agriculture, Tokyo University of Agriculture and Technology, 3-5-8 Saiwai, Fuchu, Tokyo, 183-8509, Japan

    Hiroshi Arai, Madoka Nakai, Yasuhisa Kunimi & Maki N. Inoue

  2. Department of Tea Agronomy Tea Research and Extension Station, 324 Chung-Hsing RD., Yangmei, Taoyuan, Taiwan

    Shiou Ruei Lin

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  1. Hiroshi Arai
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Contributions

In this work, HA conducted field surveys, all experiments, and data analysis. SRL organized to collect insects in Taiwan and contributed to the discussion. MN supported the entire experiments and contributed to the discussion. YK sampled insects in Taiwanese tea field and contributed to the entire discussions of this study. Lastly, MNI had full access to all data and had responsibility for the decision to submit for publication.

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Correspondence to Maki N. Inoue.

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Arai, H., Lin, S.R., Nakai, M. et al. Closely Related Male-Killing and Nonmale-Killing Wolbachia Strains in the Oriental Tea Tortrix Homona magnanima. Microb Ecol 79, 1011–1020 (2020). https://doi.org/10.1007/s00248-019-01469-6

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