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Mutualism enhances Wolbachia infection rates in ant-attended Tuberculatus aphid species (Hemiptera: Aphididae)

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Abstract

Some aphid species form close associations with ants: offering them honeydew and obtaining protection from ants in return. However, mutualistic interactions with ants can also have a negative influence on aphid physiological and morphological traits. Wolbachia are intracellular bacteria whose major genotypes are classified into 17 supergroups (A to S except G and R). Aphid species within the genus Tuberculatus feed on Fagaceae leaves and exhibit two contrasting ecological characteristics, ant-attendance and non-attendance. Previous work has found that ant-attended species exhibit lower dispersal and are likely to form aggregated colonies. Considering that host-parasitoid interactions may well be one of the most common horizontal transmission routes of Wolbachia, it is therefore expected that ant associations will be associated with higher Wolbachia infection rate in Tuberculatus aphid species. This study compared Wolbachia infection rates between 11 ant-attended and 12 non-attended Tuberculatus aphid species, which were collected throughout Japan and around Mt. Kariwangsan in South Korea. Mean infection rates of Wolbachia were 30.2% in ant-attended species and 3.1% in non-attended species. The Wolbachia haplotypes detected were classified into supergroups B, M, N, and O. A phylogenetic tree of Tuberculatus aphids constructed from a mitochondrial gene of cytochrome oxidase subunit I and nuclear gene of 18S rRNA was used to examine the correlation between Wolbachia infection rates and ant associations. The phylogenetic comparative analysis showed that Wolbachia infection rates were significantly higher in ant-attended species. Possible Wolbachia infection routes are discussed in terms of the differences in the ecological characteristics between ant-attended and non-attended aphid species. This study shows that the spread of microorganisms is affected by host species interactions, and contributes new insights into the evolution of mutualistic interactions.

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Acknowledgements

I thank S. Sugimoto of Plant Protection Station and the members of SEHU for collecting aphids. I thank K. Yoshizawa, T. Kanbe, S. Suzuki, and S. Akimoto of Hokkaido University for providing help during this study. This work was supported by JSPS Kakenhi Grant Nos. 24570016 and 15K07210 for IY.

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Funding was provided by Japan Society for the Promotion of Science (Grant Nos. 24570016, 15K07210)

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IY conceived the study, collected samples, carried out molecular work, analyzed the data and wrote the manuscript.

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Correspondence to Izumi Yao.

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Yao, I. Mutualism enhances Wolbachia infection rates in ant-attended Tuberculatus aphid species (Hemiptera: Aphididae). Evol Ecol 37, 627–643 (2023). https://doi.org/10.1007/s10682-023-10237-5

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