Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Pathogens are an important driving force for the rapid spread of symbionts in an insect host

Nature Ecology & Evolution volume 7, pages 1667–1681 (2023)Cite this article

Subjects

Abstract

One of the biggest challenges for pathogens invading hosts is microbial symbionts but the role of pathogens in symbionts in nature is unknown. By tracking the dynamics of the entomopathogenic fungal Cordyceps javanica and symbionts in natural populations of the whitefly Bemisia tabaci from 2016 to 2021 across China, we reveal that Rickettsia, a newly invaded symbiont, is positively correlated with the pathogen in both frequency and density. We confirm that applying pathogen pressure can selectively drive Rickettsia to sudden fixation in whiteflies both in the laboratory and in the field. Furthermore, the driving force is elucidated by the Rickettsia-conferred suppression of pathogen infection quantity, proliferation and sporulation, acting as a potential barrier of onward transmission of the pathogen. These results show that pathogens are an important driving force for rapid shifts in host symbionts in the natural niche.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Strong correlation between dynamics of pathogen C. javanica and symbiont Rickettsia in field whiteflies at regional scale.
Fig. 2: Strong correlation between dynamics of pathogen C. javanica and symbiont Rickettsia in field whiteflies at local scale.
Fig. 3: Strong correlation between dynamics of pathogen C. javanica and symbiont Rickettsia in field whiteflies at individual host plant scale.
Fig. 4: Applying pathogen pressure can selectively drive Rickettsia to sudden fixation in whiteflies both in the laboratory and in the field.
Fig. 5: Rickettsia protects whitefly hosts against pathogens by delaying death and suppressing infection quantity and proliferation.
Fig. 6: Rickettsia suppresses the sporulation of C. javanica on whitefly cadavers and acts as a potential barrier of onward transmission of C. javanica.

Similar content being viewed by others

Data availability

Data are available through Zenodo at the following link: https://doi.org/10.5281/zenodo.8011960. Source data are provided with this paper.

References

  1. Cordovez, V., Dini-Andreote, F., Carrión, V. J. & Raaijmakers, J. M. Ecology and evolution of plant microbiomes. Annu. Rev. Microbiol. 73, 68–88 (2019).

    Google Scholar 

  2. King, K. C. Defensive symbionts. Curr. Biol. 29, 78–80 (2019).

    Google Scholar 

  3. Scarborough, C. L., Ferrari, J. & Godfray, H. C. J. Aphid protected from pathogen by endosymbiont. Science 310, 1781–1781 (2005).

    CAS  PubMed  Google Scholar 

  4. Fenton, A., Johnson, K. N., Brownlie, J. C. & Hurst, G. D. D. Solving the Wolbachia paradox: modeling the tripartite interaction between host, Wolbachia, and a natural enemy. Am. Nat. 178, 333–342 (2011).

    PubMed  Google Scholar 

  5. Guo, H. & Qu, Y. Improvement on natural enemies of Bemisia tabaci (Hemiptera: Aleyrodidae) using extracts of Agrimonia pilosa. J. Econ. Entomol. 112, 1581–1586 (2019).

    CAS  PubMed  Google Scholar 

  6. Wu, S. et al. Identification and virulence of Cordyceps javanica strain wf GA17 isolated from a natural fungal population in sweet potato whiteflies (Hemiptera: Aleyrodidae). Environ. Entomol. 50, 1127–1136 (2021).

    CAS  PubMed  Google Scholar 

  7. Himler, A. G. et al. Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332, 254–256 (2011).

    CAS  PubMed  Google Scholar 

  8. Bockoven, A. A. et al. What goes up might come down: the spectacular spread of an endosymbiont is followed by its decline a decade later. Microb. Ecol. 79, 482–494 (2020).

    CAS  PubMed  Google Scholar 

  9. Chu, D. et al. Further insights into the strange role of bacterial endosymbionts in whitefly Bemisia tabaci: comparison of secondary symbionts from biotypes B and Q in China. Bull. Entomol. Res. 101, 477–486 (2011).

    CAS  PubMed  Google Scholar 

  10. Pan, H. et al. Actors affecting population dynamics of maternally transmitted endosymbionts in Bemisia tabaci. PLoS ONE 7, e30760 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Chu, D. et al. The introduction of the exotic Q biotype of Bemisia tabaci from the Mediterranean region into China on ornamental crops. Fla. Entomol. 89, 168–174 (2006).

    Google Scholar 

  12. Pan, H. et al. Further spread of and domination by Bemisia tabaci (Hemiptera: Aleyrodidae) biotype Q on field crops in China. J. Econ. Entomol. 104, 978–985 (2011).

    PubMed  Google Scholar 

  13. Zheng, H. et al. Dynamic monitoring (B versus Q) and further resistance status of Q type Bemisia tabaci in China. Crop Prot. 94, 115–122 (2017).

    Google Scholar 

  14. Zheng, H. et al. Annual analysis of field-evolved insecticides resistance in Bemisia tabaci across China. Pest Manag. 77, 2990–3001 (2021).

    CAS  Google Scholar 

  15. Guo, H., Qu, Y., Liu, X., Zhong, W. & Fang, J. Female-biased symbionts and tomato yellow leaf curl virus infections in Bemisia tabaci. PLoS ONE 9, e84538 (2014).

    PubMed  PubMed Central  Google Scholar 

  16. Zhao, D. X., Zhang, Z. C., Niu, H. T. & Guo, H. F. Win by quantity: a striking Rickettsia-bias symbiont community revealed by seasonal tracking in whitefly Bemisia tabaci. Microb. Ecol. 81, 523–534 (2020).

    PubMed  Google Scholar 

  17. Baas-Becking L. G. M. Geobiologie of Inleiding tot de Milieukunde (in Dutch) (WP Van Stockum & Zoon, 1934).

  18. Hoffmann, A. A., Clancy, D. & Duncan, J. Naturally-occurring Wolbachia infection in Drosophila simulans that does not cause cytoplasmic incompatibility. Heredity 76, 1–8 (1996).

    PubMed  Google Scholar 

  19. Hoffmann, A. A. et al. Cytoplasmic in compatibility in Australian populations of Drosophila melanogaster. Genetics 136, 993–999 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Hedges, L. M. et al. Wolbachia and virus protection in insects. Science 322, 702 (2008).

    CAS  PubMed  Google Scholar 

  21. Brownlie, J. C. & Johnson, K. N. Symbiont-mediated protection in insect hosts. Trends Microbiol. 17, 348–354 (2009).

    CAS  PubMed  Google Scholar 

  22. Fumagalli, M. et al. Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genet. 7, e1002355 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Cagliani, R. & Sironi, M. Pathogen-driven selection in the human genome. Int. J. Evol. Biol. 2013, 204240 (2013).

  24. Manczinger, M. et al. Pathogen diversity drives the evolution of generalist MHC-II alleles in human populations. PLoS Biol. 17, e3000131 (2019).

    PubMed  PubMed Central  Google Scholar 

  25. Carrión, V. J. et al. Pathogen-induced activation of disease-suppressive functions in the endophytic root microbiome. Science 366, 606–612 (2019).

    PubMed  Google Scholar 

  26. King, K. C. et al. Rapid evolution of microbe-mediated protection against pathogens in a worm host. ISME J. 10, 1915–1924 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. King, K. C., Stevens, E. & Drew, G. C. Microbiome: evolution in a world of interaction. Curr. Biol. 30, 265–267 (2020).

    Google Scholar 

  28. Hawkes, C. V., Bull, J. J. & Lau, J. A. Symbiosis and stress: how plant microbiomes affect host evolution. Phil. Trans. R. Soc. B 375, 20190590 (2020).

  29. Jiggins, F. M. & Hurst, G. D. D. Rapid insect evolution by symbiont transfer. Science 332, 185–186 (2011).

    CAS  PubMed  Google Scholar 

  30. Ford, S. A. & King, K. C. In vivo microbial coevolution favors host protection and plastic downregulation of immunity. Mol. Biol. Evol. 38, 1330–1338 (2020).

    PubMed Central  Google Scholar 

  31. Hoffmann, A. A. et al. Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476, 454–457 (2011).

    CAS  PubMed  Google Scholar 

  32. Łukasik, P., Guo, H., van Asch, Ferrari, M. J. & Godfray, H. C. J. Protection against a fungal pathogen conferred by the aphid facultative endosymbionts Rickettsia and Spiroplasma is expressed in multiple host genotypes and species and is not influenced by co-infection with another symbiont. J. Evol. Biol. 26, 2654–2661 (2013).

    PubMed  Google Scholar 

  33. Bernado-Cravo, A. P., Schmeller, D. S., Chatziontas, A., Verdenburg, V. T. & Loyau, A. Environmental factors and host microbiomes shape host-pathogen dynamics. Parasitology 36, 616–633 (2020).

    Google Scholar 

  34. Hellard, E., Fouchet, D., Vavre, F. & Poniter, D. Parasite–parasite interactions in the wild: how to detect them? Trends Parasitol. 31, 640–652 (2015).

    PubMed  Google Scholar 

  35. Ford, A., Kao, D., Williams, D. & King, K. C. Microbe-mediated host defence drivers the evolution of reduced pathogen virulence. Nat. Commun. 7, 13430 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Stevens, E. J., Bates, K. A. & King, K. C. Host microbiota can facilitate pathogen infection. PLoS Pathog. 17, e1009514 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Jaenike, J. et al. Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329, 212–215 (2010).

    CAS  PubMed  Google Scholar 

  38. Oliver, K. M., Campos, J., Moran, N. A. & Hunter, M. S. Population dynamics of defensive symbionts in aphids. Proc. R. Soc. B 275, 293–299 (2008).

    PubMed  Google Scholar 

  39. Drew, G., Stevens, E. J. & King, K. C. Microbial evolution and transitions along the parasite–mutualist continuum. Nat. Rev. Microb. 19, 623–638 (2021).

    CAS  Google Scholar 

  40. Turelli, M. & Hoffmann, A. A. Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353, 440–442 (1991).

    CAS  PubMed  Google Scholar 

  41. Bing, X. L., Yang, J., Zchori-Fein, E., Wang, X. W. & Liu, S. S. Characterization of a newly discovered symbiont of the whitefly Bemisia tabaci (Hemiptera: Aleyrodidae). Appl. Environ. Microb. 79, 568–575 (2012).

    Google Scholar 

  42. Lei, T., Zhao, J., Wang, H., Liu, Y. & Liu, S. Impact of a novel Rickettsia symbiont on the life history and virus transmission capacity of its host whitefly (Bemisia tabaci). Insect Sci. 28, 377–391 (2020).

    PubMed  Google Scholar 

  43. Gottlieb, Y. et al. Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleryodidae). Appl. Environ. Microb. 72, 3646–3652 (2006).

    CAS  Google Scholar 

  44. Wang, H.-L. et al. A newly recorded Rickettsia of the Torix group is a recent intruder and an endosymbiont in the whitefly Bemisia tabaci. Environ. Microbiol. 22, 1207–1221 (2020).

    PubMed  Google Scholar 

  45. Li, T. et al. Cellular tropism, population dynamics, host range and taxonomic status of an aphid secondary symbiont, SMLS (Sitobion miscanthi L type symbiont). PLoS ONE 6, e21944 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Zhang, D. et al. PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol. Ecol. Resour. 20, 348–355 (2019).

    PubMed  Google Scholar 

  47. Singh, S. T. et al. Diversity and phylogenetic analysis of endosymbiontic bacteria from field caught Bemisia tabaci from different locations of North India based on 16S rDNA library screening. Infect. Genet. Evol. 12, 411–419 (2012).

    PubMed  Google Scholar 

  48. Graham, R. I., Grzywacz, D., Mushobozi, W. L. & Wilson, K. Wolbachia in a major African crop pest increases susceptibility to viral disease rather than protects. Ecol. Lett. 15, 993–1000 (2012).

    PubMed  Google Scholar 

  49. Narita, S., Kageyama, D., Nomura, M. & Fukatsu, T. Unexpected mechanism of symbiont-induced reversal of insect sex: feminizing Wolbachia continuously acts on the butterfly Eurema hecabe during larval development. Appl. Environ. Microb. 73, 4332–4341 (2007).

    CAS  Google Scholar 

  50. Ross, P. A. et al. Wolbachia infections in Aedes aegypti differ markedly in their response to cyclical heat stress. PLoS Pathog. 13, e1006006 (2017).

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank X.-L. Ni (Jiangsu Academy of Agricultural Sciences), Z.-W. Song (Guangdong Academy of Agricultural Sciences), M.-Y. Ma (Hunan Academy of Agricultural Sciences), Z.-Y. Ge (Agricultural Committee of Jiulongpo District, Chongqing), Y.-Y. Hou (Jilin Agricultural University), Y. Li (Plant Protection and Inspection Station of Changzhi, Shanxi Province) and X. Liu (Zibo Academy of Agricultural Sciences, Shandong Province) for the help with the collection of whitefly B. tabaci populations. We are very grateful for the funding from the National Natural Science Foundation of China (grant nos. 32172412 for D.Z. and 32172410 for H.G.).

Author information

Authors and Affiliations

  1. Institute of Plant Protection, Jiangsu Academy of Agricultural Sciences, Nanjing, China

    Dongxiao Zhao, Zhichun Zhang, Hongtao Niu & Huifang Guo

Authors
  1. Dongxiao Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhichun Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hongtao Niu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Huifang Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

D.Z. and H.G. conceived of this work. D.Z., Z.Z., H.N. and H.G. developed the methodology. D.Z., Z.Z., H.N. and H.G. carried out the investigations. D.Z., Z.Z., H.N. and H.G. prepared the visualization. D.Z. and H.G. acquired the funding. H.G. supervised the work. D.Z. wrote the original draft while H.G. was involved in reviewing and editing the paper.

Corresponding author

Correspondence to Huifang Guo.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Enric Frago, Jun-Bo Luan and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 The rapid spread of the newly invaded symbiont Rickettsia in natural whitefly populations is driven by the increasing pressure of the pathogen Cordyceps javanica from 2016 to 2020.

The driving force is elucidated by the Rickettsia-conferred suppression of pathogen infection quantity, proliferation and sporulation acting as a potential barrier of onward transmission of the pathogen.

Extended Data Fig. 2 Molecular phylogenetic placement of Rickettsia from whitefly Bemesia tabaci MED collected in 2016 and 2020 across China based on 16 S rRNA, gltA and groEL gene sequences (2328 bp).

Bootstrap values for the Bayesian posterior probabilities (>0.50) are shown at the nodes. The names of hosts are shown in brackets. The sequence accession numbers are shown in Supplementary Table 2. Sequences obtained in this study are labelled by arrows.

Extended Data Table 1 Results of Chi-square test analysis for infection frequencies of Rickettsia and Cordyceps javanica in 2016 and 2020 in the 7 whitefly populations, respectively
Full size table

Supplementary information

Supplementary Information

Supplementary Tables 1 and 2.

Reporting Summary

Source data

Source Data Fig. 1

Statistical source data.

Source Data Fig. 2

Statistical source data.

Source Data Fig. 3

Statistical source data.

Source Data Fig. 4

Statistical source data.

Source Data Fig. 5

Statistical source data.

Source Data Fig. 6

Statistical source data.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhao, D., Zhang, Z., Niu, H. et al. Pathogens are an important driving force for the rapid spread of symbionts in an insect host. Nat Ecol Evol 7, 1667–1681 (2023). https://doi.org/10.1038/s41559-023-02160-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-023-02160-3

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology