Abstract
Male-killing, the death of male offspring induced by maternally transmitted microbes, is classified as early, or late, male-killing. The primary advantage afforded by early male-killing, which typically occurs during embryogenesis, is the reallocation of resources to females, that would have otherwise been consumed by males. Meanwhile, the key advantage of late male-killing, which typically occurs during late larval development, is the maximized potential for horizontal transmission. To date, no studies have reported on the associated developmental and physiological effects of host coinfection with early and late male-killers, which may have a significant impact on the population dynamics of the male-killers. Here we used a lepidopteran tea pest Homona magnanima as a model, which is a unique system wherein an early male-killer (a Spiroplasma bacterium) and a late male-killer (an RNA virus) can coexist in nature. An artificially established matriline, coinfected with both Spiroplasma and RNA virus, exhibited embryonic death (early male-killing) as seen in the host line singly infected with Spiroplasma. Moreover, the coinfected line also exhibited developmental retardation and low pupal weight similar to the host line singly infected with the RNA virus. A series of field surveys revealed that Spiroplasma-RNA virus coinfection occurs in nature at a low frequency. Hence, although the two male-killers are capable of coexisting within the H. magnanima population independently, high associated fitness cost appears to limit the prevalence of male-killer coinfection in the field host population.
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The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
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Acknowledgments
We thank Y. Sato and C. Ishijima (National Agriculture and Food Research Organization, Shimada, Japan) for invaluable help in the field. We also thank Dr. H. Anbutsu (National Institute of Advanced Industrial Science and Technology, Tsukuba, Japan) for kind advice on our research. We also thank four anonymous reviewers for valuable suggestions.
Funding
This work was partially supported by the JSPS KAKENHI grant number JP24580076 and JSPS Research Fellowships for Young Scientists number 19J13123.
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TT conducted characterization of host lines and conducted field surveys. HA conducted field surveys, data analyses, and preparation for the manuscript. TT and HA contributed equally to the present work. NA established the host lines and conducted field surveys. MN supported entire experiments and contributed to discussion. YK supported the works, arranged surveys, and contributed to entire discussions of this study. MNI managed experiments and preparations for the manuscript and contributed to discussions of this study. Corresponding authors HA and MNI have full access to all data and had responsibility for the decision to submit for publication.
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Takamatsu, T., Arai, H., Abe, N. et al. Coexistence of Two Male-Killers and Their Impact on the Development of Oriental Tea Tortrix Homona magnanima. Microb Ecol 81, 193–202 (2021). https://doi.org/10.1007/s00248-020-01566-x
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DOI: https://doi.org/10.1007/s00248-020-01566-x