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

Volumn 114, Issue 6, 2015, Pages 539-543

  Nakayama, S ^a,b   Parratt, S R ^a,c   Hutchence, K J ^a   Lewis, Z ^a   Price, T A R ^a   Hurst, G D D ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b KYUSHU UNIVERSITY   (Japan)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DISEASE; ENDOSYMBIONT; FLY; GENE TRANSFER; MATERNAL EFFECT; VERTICAL TRANSMISSION;

ARTHROPODA; DROSOPHILA MELANOGASTER; SPIROPLASMA;

ADAPTATION; ANIMAL; DROSOPHILA MELANOGASTER; EVOLUTION; FEMALE; MALE; MICROBIOLOGY; PHYSIOLOGY; REPRODUCTIVE FITNESS; SPIROPLASMA; STATISTICAL MODEL; SYMBIOSIS;

ADAPTATION, BIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; DROSOPHILA MELANOGASTER; FEMALE; GENETIC FITNESS; LINEAR MODELS; MALE; SPIROPLASMA; SYMBIOSIS;

EID: 84929263615     PISSN: 0018067X     EISSN: 13652540     Source Type: Journal    
DOI: 10.1038/hdy.2014.112     Document Type: Article

References (37)

1. Brownlie JC, Johnson KN. (2009). Symbiont-mediated protection in insect hosts. Trends Microbiol 17: 348-354
2. Carrington LB, Hoffmann AA, Weeks AR. (2010). Monitoring long-Term evolutionary changes following Wolbachia introduction into a novel host: the Wolbachia popcorn infection in Drosophila simulans. Proc R Soc Lond B Biol Sci 277: 2059-2068
3. Clancy DJ, Hoffmann AA. (1997). Behavior of Wolbachia endosymbionts from Drosophila simulans in Drosophila serrata, a novel host. Am Nat 149: 975-988
4. Counce SJ, Poulson DF. (1962). Developmental effects of the sex-ratio agent in embryos of Drosophila willistoni. J Exp Zool 151: 17-31
5. Duron O, Bouchon D, Boutin S, Bellamy L, Zhou LQ, Engelstödter J, et al. (2008). The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 6: 27
6. Gasparich GE, Whitcomb RF, Dodge D, French FE, Glass J, Williamson DL. (2004). The genus Spiroplasma and its non-helical descendants: phylogenetic classification, correlation with phenotype and roots of the Mycoplasma mycoides clade. Int J Syst Evol Microbiol 54: 893-918
7. Haine ER. (2008). Symbiont-mediated protection. Proc R Soc Lond B Biol Sci 275: 353-361
8. Hamilton PT, Leong JS, Koop BF, Perlman SJ. (2014). Transcriptional responses in a Drosophila defensive symbiosis. Mol Ecol 23: 1558-1570
9. Haselkorn TS, Cockburn SN, Hamilton PT, Perlman SJ, Jaenike J. (2013). Infectious adaptation: potential host range of a defensive endosymbiont in Drosophila. Evolution 67: 934-945
10. Haselkorn TS, Markow TA, Moran NA. (2009). Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol Ecol 18: 1294-1305
11. Herren JK, Paredes JC, Schüpfer F, Lemaitre B. (2013). Vertical transmission of a Drosophila endosymbiont via cooption of the yolk transport and internalization machinery. MBio 4: 00532-12
12. Hutchence KJ. (2011). The evolutionary ecology of host-parasite interactions between Drosophila and Spiroplasma. Chapter 3: Phenotype and transmission efficiency of artificial and natural male-killing Spiroplasma infections in Drosophila melanogaster. PhD thesis. University of Liverpool, Liverpool, UK
13. Hutchence KJ, Pade R, Swif HL, Bennet D, Hurst GDD. (2011). Phenotype and transmission efficiency of artificial and natural male-killing of Spiroplasma infections in Drosophila melanogaster. J Invert Pathol 109: 243-247
14. Jaenike J. (2012). Population genetics of beneficial heritable symbionts. Trends Ecol Evol 27: 226-232
15. Jaenike J, Polak M, Fiskin A, Helou M, Minhas M. (2007). Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol Lett 3: 23-25
16. Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ. (2010). Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329: 212-215
17. Jiggins FM, Hurst GDD. (2011). Microbiology. Rapid insect evolution by symbiont transfer. Science 332: 185-186
18. Kageyama D, Anbutsu H, Watada M, Hosokawa T, Shimada M, Fukatsu T. (2006). Prevalence of a non-male-killing Spiroplasma in natural populations of Drosophila hydei. Appl Environ Microbiol 72: 6667-6673
19. Mateos M, Castrezana SJ, Nankivell BJ, Estes AM, Markow TA, Moran NA. (2006). Heritable endosymbionts of Drosophila. Genetics 174: 363-376
20. McGraw EA, Merritt DJ, Droller JN, O'Neill SL. (2002). Wolbachia density and virulence attenuation after transfer into a novel host. Proc Natl Acad Sci USA 99: 2918-2923
21. Montenegro H, Petherwick AS, Hurst GDD, Klaczko LB. (2006). Fitness effects of Wolbachia and Spiroplasma in Drosophila melanogaster. Genetica 127: 207-215
22. Montenegro H, Solferini VN, Klaczko LB, Hurst GDD. (2005). Male-killing Spiroplasma naturally infecting Drosophila melanogaster. Insect Mol Biol 14: 281-288
23. Mouton L, Thierry M, Henri H, Baudin R, Gnankine O, Reynaud B, et al. (2012). Evidence of diversity and recombination in Arsenophonus symbionts of the Bemisia tabaci species complex. BMC Microbiol 12: S10
24. Osaka R, Watada M, Kageyama D, Nomra M. (2013). Detection of Spiroplasma from the mite Macrocheles sp. (Acari: Macrochelidae) ectoparasitic to the fly Drosophila hydei (Diptera; Drosophilidae): a possible route of horizontal transmission? Symbiont 60: 79-84
25. Pool JE, Wong A, Aquadro CF. (2006). Finding of male-killing Spiroplasma infecting Drosophila melanogaster in Africa implies transatlantic migration of this endosymbiont. Heredity 97: 27-32
26. Raychoudhury R, Baldo L, Oliveira DCSG, Werren JH. (2009). Modes of acquisition of Wolbachia: horizontal transfer, hybrid introgression and co-divergence in the Nasonia species complex. Evolution 63: 165-183
27. Rice WR. (1989). Analyzing tables of statistical tests. Evolution 43: 223-225
28. Russell JA, Moran NA. (2005). Horizontal transfer of bacterial symbionts: Heritability and fitness effects in a novel aphid host. Appl Environ Microbiol 71: 7987-7994
29. Sakaguchi B, Poulson DF. (1963). Interspecific transfer of the 'sex-ratio' condition from Drosophila willistoni to D. melanogaster. Genetics 48: 841-861
30. SAS Institute. (2009). JMP 8, SAS Institute Inc.: Cary, NC, USA
31. Tinsley MC, Majerus MEN. (2007). Small steps or giant leaps for male-killers? Phylogenetic constraints to male-killer host shifts. BMC Evol Biol 7: 238
32. Walsh PS, Metzger DA, Higuchi R. (1991). Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10: 506-513
33. Weeks AR, Turelli M, Harcombe WR, Reynolds KT, Hoffmann AA. (2007). From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol 5: 99-1005
34. Williamson DL, Poulson DF. (1979). Sex-ratio organisms (Spiroplasmas) of Drosophila. In: Whitcomb RF, Tully JG (eds) The Mycoplasmas vol. 3, Academic Press: New York, NY, USA. pp 175-208
35. Williamson DL, Sakaguchi B, Hackett KJ, Whitcomb RF, Tully JG, Carle P, et al. (1999). Spiroplasma poulsonii sp. nov., a new species associated with male-lethality in Drosophila willistoni, a neotropical species of fruit fly. Int J Syst Bacteriol 49: 611-618
36. Xie JL, Vilchez I, Mateos M. (2010). Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS ONE 5: 1-7
37. Zug R, Koehncke A, Hammerstein P. (2012). Epidemiology in evolutionary time: the case of Wolbachia horizontal transmission between arthropod host species. J Evol Biol 25: 2149-2160