Effects of bacterial secondary symbionts on host plant use in pea aphids

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1706, 2011, Pages 760-766

  McLean, A H C ^a   Van Asch, M ^a   Ferrari, J ^b   Godfray, H C J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Acyrthosiphon pisum; Aphid; Host specialization; Mutualism; Secondary symbiont

Indexed keywords

APHID; BACTERIUM; CLONE; EVOLUTIONARILY STABLE STRATEGY; FECUNDITY; FITNESS; GENETIC VARIATION; HOST PLANT; LEGUME; MUTUALISM; SPECIALIZATION; SYMBIONT;

ACYRTHOSIPHON PISUM; APHIDIDAE; BACTERIA (MICROORGANISMS); CANDIDATUS HAMILTONELLA DEFENSA; LATHYRUS; LATHYRUS PRATENSIS; VICIA FABA;

EID: 79951777079     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.1654     Document Type: Article

References (44)

1. Moran, N. A. 2001 The coevolution of bacterial endosymbionts and phloem-feeding insects. Ann. Mo. Bot. Gard. 88, 35-44. (doi:10.2307/2666130) (Pubitemid 32437213)
2. Douglas, A. E. 2006 Phloem-sap feeding by animals: problems and solutions. J. Exp. Bot. 57, 747-754. (doi:10.1093/jxb/erj067)
3. Aksoy, S. 1995Wigglesworthia gen. nov. andWigglesworthia glossinidia sp. nov., taxa consisting of the mycetocyteassociated, primary endosymbionts of tsetse flies. Int. J. Syst. Bacteriol. 45, 848-851. (doi:10.1099/00207713-45-4- 848)
4. Werren, J. H. 1997 Biology of Wolbachia. Annu. Rev. Entomol. 42, 587-609. (doi:10.1146/annurev.ento.42.1.587) (Pubitemid 27169561)
5. Moran, N. A., Russell, J. A., Koga, R. & Fukatsu, T. 2005 Evolutionary relationships of three new species of Enterobacteriaceae living as symbionts of aphids and other insects. Appl. Environ. Microbiol. 71, 3302-3310. (doi:10.1128/AEM.71.6.3302-3310.2005) (Pubitemid 40807242)
6. Oliver, K. M., Moran, N. A. & Hunter, M. S. 2006 Costs and benefits of a superinfection of facultative symbionts in aphids. Proc. R. Soc. B 273, 1273-1280. (doi:10.1098/rspb.2005.3436) (Pubitemid 47324464)
7. Tsuchida, T., Koga, R., Shibao, H., Matsumoto, T. & Fukatsu, T. 2002 Diversity and geographic distribution of secondary endosymbiotic bacteria in natural populations of the pea aphid, Acyrthosiphon pisum. Mol. Ecol. 11, 2123-2135. (doi:10.1046/j.1365-294X.2002.01606.x)
8. Moran, N. A. & Dunbar, H. E. 2006 Sexual acquisition of beneficial symbionts in aphids. Proc. Natl Acad. Sci. USA 103, 12 803-12 806. (doi:10.1073/pnas.0605772103) (Pubitemid 44298642)
9. Oliver, K. M., Degnan, P. H., Hunter, M. S. & Moran, N. A. 2009 Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325, 992-994. (doi:10.1126/science.1174463)
10. Scarborough, C. L., Ferrari, J. & Godfray, H. C. J. 2005 Aphid protected from pathogen by endosymbiont. Science 310, 1781-1781. (doi:10.1126/science.1120180) (Pubitemid 41814373)
11. Russell, J. A. & Moran, N. A. 2005 Horizontal transfer of bacterial symbionts: heritability and fitness effects in a novel aphid host. Appl. Environ. Microbiol. 71, 7987-7994. (doi:10.1128/AEM.71.12.7987-7994.2005) (Pubitemid 41803920)
12. Montllor, C. B., Maxmen, A. & Purcell, A. H. 2002 Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol. Entomol. 27, 189-195. (doi:10.1046/j.1365-2311.2002.00393.x) (Pubitemid 34315686)
13. Chen, D. Q., Montllor, C. B. & Purcell, A. H. 2000 Fitness effects of two facultative endosymbiotic bacteria on the pea aphid, Acyrthosiphon pisum, and the blue alfalfa aphid A. kondoi. Entomol. Exp. Appl. 95, 315-323. (doi:10.1023/A:1004083324807) (Pubitemid 30400095)
14. Leonardo, T. E. & Mondor, E. B. 2006 Symbiont modifies host life-history traits that affect gene flow. Proc. R. Soc. B 273, 1079-1084. (doi:10.1098/rspb.2005.3408) (Pubitemid 47324475)
15. Peccoud, J., Ollivier, A., Plantegenest, M. & Simon, J. C. 2009 A continuum of genetic divergence from sympatric host races to species in the pea aphid complex. Proc. Natl Acad. Sci. USA 106, 7495-7500. (doi:10.1073/pnas. 0811117106)
16. Peccoud, J., Simon, J. C., McLaughlin, H. J. & Moran, N. A. 2009 Post-Pleistocene radiation of the pea aphid complex revealed by rapidly evolving endosymbionts. Proc. Natl Acad. Sci. USA 106, 16 315-16 320. (doi:10.1073/pnas.0905129106)
17. Via, S. 1991 The genetic structure of host plant adaptation in a spatial patchwork-demographic variability among reciprocally transplanted pea aphid clones. Evolution 45, 827-852. (doi:10.2307/2409692)
18. Ferrari, J., Via, S. & Godfray, H. C. J. 2008 Population differentiation and genetic variation in performance on eight hosts in the pea aphid complex. Evolution 62, 2508-2524. (doi:10.1111/j.1558-5646.2008.00468.x)
19. Sandström, J. 1996 Temporal changes in host adaptation in the pea aphid, Acyrthosiphon pisum. Ecol. Entomol. 21, 56-62. (doi:10.1111/j.1365-2311. 1996.tb00266.x)
20. Ferrari, J., Godfray, H. C. J., Faulconbridge, A. S., Prior, K. & Via, S. 2006 Population differentiation and genetic variation in host choice among pea aphids from eight host plant genera. Evolution 60, 1574-1584. (Pubitemid 44808251)
21. Hawthorne, D. J. & Via, S. 2001 Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412, 904-907. (doi:10.1038/35091062) (Pubitemid 32821733)
22. Via, S. 1991 Specialized host plant performance of pea aphid clones is not altered by experience. Ecology 72, 1420-1427. (doi:10.2307/1941114)
23. Via, S., Bouck, A. C. & Skillman, S. 2000 Reproductive isolation between divergent races of pea aphids on two hosts. II. Selection against migrants and hybrids in the parental environments. Evolution 54, 1626-1637.
24. Caillaud, M. C. & Via, S. 2000 Specialized feeding behavior influences both ecological specialization and assortative mating in sympatric host races of pea aphids. Am. Nat. 156, 606-621. (doi:10.1086/316991) (Pubitemid 32013276)
25. Darby, A. C., Tosh, C. R., Walters, K. F. A. & Douglas, A. E. 2003 The significance of a facultative bacterium to natural populations of the pea aphid Acyrthosiphon pisum. Ecol. Entomol. 28, 145-150. (doi:10.1046/j.1365-2311. 2003.00492.x) (Pubitemid 36463408)
26. Ferrari, J.,Darby, A. C.,Daniell, T. J., Godfray, H. C. J. & Douglas, A. E. 2004 Linking the bacterial community in pea aphids with host-plant use and natural enemy resistance. Ecol. Entomol. 29, 60-65. (doi:10.1111/j.1365- 2311.2004.00574.x) (Pubitemid 38241752)
27. Leonardo, T. E. & Muiru, G. T. 2003 Facultative symbionts are associated with host plant specialization in pea aphid populations. Proc. R. Soc. Lond. B 270, S209-S212. (doi:10.1098/rsbl.2003.0064) (Pubitemid 37430858)
28. Simon, J. C., Carre, S., Boutin, M., Prunier-Leterme, N., Sabater-Munoz, B., Latorre, A. & Bournoville, R. 2003 Host-based divergence in populations of the pea aphid: insights from nuclear markers and the prevalence of facultative symbionts. Proc. R. Soc. Lond. B 270, 1703-1712. (doi:10.1098/rspb.2003.2430) (Pubitemid 37041291)
29. Tsuchida, T., Koga, R. & Fukatsu, T. 2004 Host plant specialization governed by facultative symbiont. Science 303, 1989-1989. (doi:10.1126/science. 1094611) (Pubitemid 38393267)
30. Leonardo, T. E. 2004 Removal of a specialization associated symbiont does not affect aphid fitness. Ecol. Lett. 7, 461-468. (doi:10.1111/j.1461-0248. 2004.00602.x) (Pubitemid 38693388)
31. Ferrari, J., Scarborough, C. L. & Godfray, H. C. J. 2007 Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids. Oecologia 153, 323-329. (doi:10.1007/s00442-007-0730-2) (Pubitemid 47231250)
32. Koga, R., Tsuchida, T., Sakurai, M. & Fukatsu, T. 2007 Selective elimination of aphid endosymbionts: effects of antibiotic dose and host genotype, and fitness consequences. FEMS Microbiol. Ecol. 60, 229-239. (Pubitemid 46597311)
33. Oliver, K. M., Moran, N. A. & Hunter, M. S. 2005 Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc. Natl Acad. Sci. USA 102, 12 795-12 800. (doi:10.1073/pnas.0506131102) (Pubitemid 41279445)
34. Chandler, S. M., Wilkinson, T. L. & Douglas, A. E. 2008 Impact of plant nutrients on the relationship between a herbivorous insect and its symbiotic bacteria. Proc. R. Soc. B 275, 565-570. (doi:10.1098/rspb.2007.1478) (Pubitemid 351156532)
35. Sandström, J. P., Russell, J. A., White, J. P. & Moran, N. A. 2001 Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol. Ecol. 10, 217-228. (doi:10.1046/j.1365-294X.2001.01189.x) (Pubitemid 32097542)
36. Guay, J.-F., Boudreault, S., Michaud, D. & Cloutier, C. 2009 Impact of environmental stress on aphid clonal resistance to parasitoids: role of Hamiltonella defensa bacterial symbiosis in association with a new facultative symbiont of the pea aphid. J. Insect Physiol. 55, 919-926. (doi:10.1016/j. jinsphys.2009.06.006)
37. Chen, D. Q., Campbell, B. C. & Purcell, A. H. 1996 A new Rickettsia from a herbivorous insect, the pea aphid Acyrthosiphon pisum (Harris). Curr. Microbiol. 33, 123-128. (doi:10.1007/s002849900086) (Pubitemid 26286242)
38. Fukatsu, T., Tsuchida, T., Nikoh, N. & Koga, R. 2001 Spiroplasma symbiont of the pea aphid, Acyrthosiphon pisum (Insecta: Homoptera). Appl. Environ. Microbiol. 67, 1284-1291. (doi:10.1128/AEM.67.3.1284-1291.2001) (Pubitemid 33643573)
39. Sakurai, M., Koga, R., Tsuchida, T., Meng, X. Y. & Fukatsu, T. 2005 (Rickettsia) symbiont in the pea aphid (Acyrthosiphon pisum): novel cellular tropism, effect on host fitness, and interaction with the essential symbiont (Buchnera). Appl. Environ. Microbiol. 71, 4069-4075. (doi:10.1128/AEM.71.7.4069- 4075.2005) (Pubitemid 40980580)
40. Sandström, J. & Pettersson, J. 1994 Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. J. Insect Physiol. 40, 947-955. (doi:10.1016/0022-1910(94)90133-3) (Pubitemid 2161542)
41. Douglas, A. E. & Prosser, W. A. 1992 Synthesis of the essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis. J. Insect Physiol. 38, 565-568. (doi:10.1016/0022-1910(92)90107-O)
42. Koga, R., Tsuchida, T. & Fukatsu, T. 2003 Changing partners in an obligate symbiosis: a facultative endosymbiont can compensate for loss of the essential endosymbiont Buchnera in an aphid. Proc. R. Soc. Lond. B 270, 2543-2550. (doi:10.1098/rspb.2003.2537) (Pubitemid 38082940)
43. Haynes, S., Darby, A. C., Daniell, T. J., Webster, G., van Veen, F. J. F., Godfray, H. C. J., Prosser, J. I. & Douglas, A. E. 2003 Diversity of bacteria associated with natural aphid populations. Appl. Environ. Microbiol. 69, 7216-7223. (doi:10.1128/AEM.69.12.7216-7223. 2003) (Pubitemid 38585372)
44. Oliver, K. M., Degnan, P. H., Burke, G. R. & Moran, N. A. 2010 Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu. Rev. Entomol. 55, 247-266. (doi:10.1146/annurev-ento- 112408-085305)