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Abstract

Heritable symbionts represent important components of the biology, ecology and evolution of their arthropod hosts. Particular microbial taxa have become common across arthropods as a consequence of their ability to establish in new host species. For a host shift to occur, the symbiont must be exposed to a novel host and then be compatible: it must not cause excess pathology, must have good vertical transmission and must possess a drive phenotype that enables spread. Here we investigate the lability of compatibility to symbiosis with . We used transinfection to establish the protective symbiont from in two closely related novel hosts, and . The had contrasting compatibility in the two species, exhibiting pathology and low vertical transmission but delivering protection from wasp attack in but being asymptomatic and transmitted with high efficiency but with lower protection in . Further work indicated that pathological interactions occurred in two other members of the melanogaster species group, such that was unusual in being able to carry the symbiont without damage. The differing compatibility of the symbiont with these closely related host species emphasizes the rapidity with which host–symbiont compatibility evolves, despite compatibility itself not being subject to direct selection. Further, the requirement to fit three independent components of compatibility (pathology, transmission, protection) is probably to be a major feature limiting the rate of host shifts that will likely impact on the utility of in pest and vector control. Moving forward, the variation between sibling species pairs provides an opportunity to identify the mechanisms behind variable compatibility, which will drive hypotheses as to the evolutionary drivers of compatibility variation.

Funding
This study was supported by the:
  • Horizon 2020 Framework Programme (Award H2020-MSCA-IF-2015, 703379)
    • Principle Award Recipient: MichaelGerth
  • Natural Environment Research Council (Award NE/L002450/1)
    • Principle Award Recipient: JoanneS. Griffin
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2022-12-13
2024-05-22
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References

  1. Moran NA. Symbiosis. Curr Biol 2006; 16:R866–71 [View Article]
    [Google Scholar]
  2. Buchner P. Endosymbioses of Animals with Plant Microorganisms: Interscience Publishers Wiley & Co; 1965
    [Google Scholar]
  3. Dyson EA, Hurst GDD. Persistence of an extreme sex-ratio bias in a natural population. Proc Natl Acad Sci U S A 2004; 101:6520–6523 [View Article] [PubMed]
    [Google Scholar]
  4. Salem H, Kirsch R, Pauchet Y, Berasategui A, Fukumori K et al. Symbiont digestive range reflects host plant breadth in herbivorous beetles. Curr Biol 2020; 30:2875–2886 [View Article] [PubMed]
    [Google Scholar]
  5. Hornett EA, Kageyama D, Hurst GDD. Sex determination systems as the interface between male-killing bacteria and their hosts. Proc Biol Sci 2022; 289:20212781 [View Article] [PubMed]
    [Google Scholar]
  6. Sandström JP, Russell JA, White JP, Moran NA. Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol 2001; 10:217–228 [View Article] [PubMed]
    [Google Scholar]
  7. Werren JH, Windsor D, Guo L. Distribution of Wolbachia among neotropical arthropods. Proc R Soc Lond B 1995; 262:197–204 [View Article]
    [Google Scholar]
  8. Jiggins FM, Hurst GDD. Microbiology. Rapid insect evolution by symbiont transfer. Science 2011; 332:185–186 [View Article]
    [Google Scholar]
  9. Dietel A-K, Kaltenpoth M, Kost C. Convergent evolution in intracellular elements: plasmids as model endosymbionts. Trends Microbiol 2018; 26:755–768 [View Article] [PubMed]
    [Google Scholar]
  10. Ferrari J, Vavre F. Bacterial symbionts in insects or the story of communities affecting communities. Philos Trans R Soc Lond B Biol Sci 2011; 366:1389–1400 [View Article] [PubMed]
    [Google Scholar]
  11. Herren JK, Paredes JC, Schüpfer F, Lemaitre B. Vertical transmission of a Drosophila endosymbiont via cooption of the yolk transport and internalization machinery. mBio 2013; 4:e00532-12 [View Article] [PubMed]
    [Google Scholar]
  12. Clancy DJ, Hoffmann AA. Behavior of Wolbachia endosymbionts from Drosophila simulans in Drosophila serrata, a novel host. Am Nat 1997; 149:975–988 [View Article] [PubMed]
    [Google Scholar]
  13. Russell JA, Moran NA. Horizontal transfer of bacterial symbionts: heritability and fitness effects in a novel aphid host. Appl Environ Microbiol 2005; 71:7987–7994 [View Article]
    [Google Scholar]
  14. Kageyama D, Anbutsu H, Watada M, Hosokawa T, Shimada M et al. Prevalence of a non-male-killing spiroplasma in natural populations of Drosophila hydei. Appl Environ Microbiol 2006; 72:6667–6673 [View Article] [PubMed]
    [Google Scholar]
  15. Tinsley MC, Majerus MEN. Small steps or giant leaps for male-killers? Phylogenetic constraints to male-killer host shifts. BMC Evol Biol 2007; 7:238 [View Article] [PubMed]
    [Google Scholar]
  16. Nakayama S, Parratt SR, Hutchence KJ, Lewis Z, Price TAR et al. Can maternally inherited endosymbionts adapt to a novel host? Direct costs of Spiroplasma infection, but not vertical transmission efficiency, evolve rapidly after horizontal transfer into D. melanogaster. Heredity (Edinb) 2015; 114:539–543 [View Article] [PubMed]
    [Google Scholar]
  17. McGraw EA, Merritt DJ, Droller JN, O’Neill SL. Wolbachia density and virulence attenuation after transfer into a novel host. Proc Natl Acad Sci U S A 2002; 99:2918–2923 [View Article] [PubMed]
    [Google Scholar]
  18. Carrington LB, Hoffmann AA, Weeks AR. Monitoring long-term evolutionary changes following Wolbachia introduction into a novel host: the Wolbachia popcorn infection in Drosophila simulans. Proc Biol Sci 2010; 277:2059–2068 [View Article] [PubMed]
    [Google Scholar]
  19. Gilbert GS, Webb CO. Phylogenetic signal in plant pathogen-host range. Proc Natl Acad Sci U S A 2007; 104:4979–4983 [View Article] [PubMed]
    [Google Scholar]
  20. Streicker DG, Turmelle AS, Vonhof MJ, Kuzmin IV, McCracken GF et al. Host phylogeny constrains cross-species emergence and establishment of rabies virus in bats. Science 2010; 329:676–679 [View Article] [PubMed]
    [Google Scholar]
  21. Longdon B, Hadfield JD, Webster CL, Obbard DJ, Jiggins FM. Host phylogeny determines viral persistence and replication in novel hosts. PLoS Pathog 2011; 7:e1002260 [View Article] [PubMed]
    [Google Scholar]
  22. Longdon B, Brockhurst MA, Russell CA, Welch JJ, Jiggins FM. The evolution and genetics of virus host shifts. PLoS Pathog 2014; 10:e1004395 [View Article] [PubMed]
    [Google Scholar]
  23. Sakaguchi B, Poulson DF. Distribution of “sex-ratio” agent in tissues of Drosophila willistoni. Genetics 1961; 46:1665–1676 [View Article] [PubMed]
    [Google Scholar]
  24. Montenegro H, Solferini VN, Klaczko LB, Hurst GDD. Male-killing Spiroplasma naturally infecting Drosophila melanogaster. Insect Mol Biol 2005; 14:281–287 [View Article] [PubMed]
    [Google Scholar]
  25. Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ. Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 2010; 329:212–215 [View Article] [PubMed]
    [Google Scholar]
  26. Xie JL, Vilchez I, Mateos M. Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS One 2010; 5:e12149 [View Article] [PubMed]
    [Google Scholar]
  27. Xie J, Butler S, Sanchez G, Mateos M. Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps. Heredity (Edinb) 2014; 112:399–408 [View Article] [PubMed]
    [Google Scholar]
  28. Corbin C, Jones JE, Chrostek E, Fenton A, Hurst GDD. Thermal sensitivity of the Spiroplasma-Drosophila hydei protective symbiosis: The best of climes, the worst of climes. Mol Ecol 2021; 30:1336–1344 [View Article] [PubMed]
    [Google Scholar]
  29. Haselkorn TS, Markow TA, Moran NA. Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol Ecol 2009; 18:1294–1305 [View Article] [PubMed]
    [Google Scholar]
  30. Williamson DL, Poulson DF. Sex ratio organisms (Spiroplasmas) of Drosophila. In Whitcomb RF, Tully JG. eds The Mycoplasmas New York: Academic Press; 1979 pp 175–208
    [Google Scholar]
  31. Haselkorn TS, Cockburn SN, Hamilton PT, Perlman SJ, Jaenike J. Infectious adaptation: potential host range of a defensive endosymbiont in Drosophila. Evolution 2013; 67:934–945 [View Article] [PubMed]
    [Google Scholar]
  32. Suvorov A, Kim BY, Wang J, Armstrong EE, Peede D et al. Widespread introgression across a phylogeny of 155 Drosophila genomes. Curr Biol 2022; 32:111–123 [View Article] [PubMed]
    [Google Scholar]
  33. Mateos M, Castrezana SJ, Nankivell BJ, Estes AM, Markow TA et al. Heritable endosymbionts of Drosophila. Genetics 2006; 174:363–376 [View Article] [PubMed]
    [Google Scholar]
  34. Jones JE, Hurst GDD. Symbiont-mediated protection varies with wasp genotype in the Drosophila melanogaster-Spiroplasma interaction. Heredity (Edinb) 2020; 124:592–602 [View Article] [PubMed]
    [Google Scholar]
  35. Walsh PS, Metzger DA, Higuchi R. Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 1991; 10:506–513 [PubMed]
    [Google Scholar]
  36. R core development team R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2013 http://www.R-project.org/
  37. Team R RStudio: Integrated Development Environment for R. Boston, MA: RStudio, PBC; 2015 http://www.rstudio.com/
  38. Goto S, Anbutsu H, Fukatsu T. Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Appl Environ Microbiol 2006; 72:4805–4810 [View Article] [PubMed]
    [Google Scholar]
  39. Yoshida K, Sanada-Morimura S, Huang S-H, Tokuda M. Influences of two coexisting endosymbionts, CI-inducing Wolbachia and male-killing Spiroplasma, on the performance of their host Laodelphax striatellus (Hemiptera: Delphacidae). Ecol Evol 2019; 9:8214–8224 [View Article] [PubMed]
    [Google Scholar]
  40. Fytrou A, Schofield PG, Kraaijeveld AR, Hubbard SF. Wolbachia infection suppresses both host defence and parasitoid counter-defence. Proc Biol Sci 2006; 273:791–796 [View Article] [PubMed]
    [Google Scholar]
  41. Pollmann M, Moore LD, Krimmer E, D’Alvise P, Hasselmann M et al. Highly transmissible cytoplasmic incompatibility by the extracellular insect symbiont Spiroplasma. iScience 2022; 25:104335 [View Article] [PubMed]
    [Google Scholar]
  42. Jaenike J, Polak M, Fiskin A, Helou M, Minhas M. Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol Lett 2007; 3:23–25 [View Article] [PubMed]
    [Google Scholar]
  43. Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L et al. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 2008; 6:27 [View Article] [PubMed]
    [Google Scholar]
  44. Paredes JC, Herren JK, Schüpfer F, Lemaitre B. The role of lipid competition for endosymbiont-mediated protection against parasitoid wasps in Drosophila. mBio 2016; 7:e01006–01016 [View Article] [PubMed]
    [Google Scholar]
  45. Ballinger MJ, Perlman SJ. Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila. PLoS Pathog 2017; 13:e1006431 [View Article] [PubMed]
    [Google Scholar]
  46. Kim-Jo C, Gatti J-L, Poirié M. Drosophila cellular immunity against parasitoid wasps: a complex and time-dependent process. Front Physiol 2019; 10:603 [View Article] [PubMed]
    [Google Scholar]
  47. Pool JE, Wong A, Aquadro CF. Finding of male-killing Spiroplasma infecting Drosophila melanogaster in Africa implies transatlantic migration of this endosymbiont. Heredity (Edinb) 2006; 97:27–32 [View Article] [PubMed]
    [Google Scholar]
  48. Bentley JK, Hind G, Hurst GDD. The male-killing spiroplasmas of Drosophila nebulosa and Drosophila willistoni have identical ITS sequences. Dros Inf Serv 2002; 85:63–65
    [Google Scholar]
  49. Hutchence KJ, Padé R, Swift HL, Bennett D, Hurst GDD. Phenotype and transmission efficiency of artificial and natural male-killing Spiroplasma infections in Drosophila melanogaster. J Invertebr Pathol 2012; 109:243–247 [View Article] [PubMed]
    [Google Scholar]
  50. Gerth M, Martinez-Montoya H, Ramirez P, Masson F, Griffin JS et al. Rapid molecular evolution of Spiroplasma symbionts of Drosophila. Microb Genom 2021; 7: [View Article]
    [Google Scholar]
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