Independent origins of resistance or susceptibility of parasitic wasps to a defensive symbiont

Ecology and Evolution

Volumn 6, Issue 9, 2016, Pages 2679-2687

  Mateos, Mariana ^a   Winter, Lauryn ^a   Winter, Caitlyn ^a   Higareda Alvear, Victor M ^b   Martinez Romero, Esperanza ^b   Xie, Jialei ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

^b INSTITUTO DE CIENCIAS FÍSICAS   (Mexico)

Author keywords

Drosophila melanogaster; Braconidae; Defensive mutualism; Figitidae; Heritable endosymbiont; Mollicutes

Indexed keywords

EID: 84961282366     PISSN: None     EISSN: 20457758     Source Type: Journal    
DOI: 10.1002/ece3.2085     Document Type: Article

References (63)

1. Asplen, M. K., N. Bano, C. M. Brady, N. Desneux, K. R. Hopper, C. Malouines, et al. 2014. Specialisation of bacterial endosymbionts that protect aphids from parasitoids. Ecol. Entomol. 39:736-739.
2. Ayres, J. S., and D. S. Schneider. 2008. A signaling protease required for melanization in Drosophila affects resistance and tolerance of infections. PLoS Biol. 6:2764-2773.
3. Bensadia, F., S. Boudreault, J. F. Guay, D. Michaud, and C. Cloutier. 2006. Aphid clonal resistance to a parasitoid fails under heat stress. J. Insect Physiol. 52:146-157.
4. Bolaños, L. M., L. E. Servín-Garcidueñas, and E. Martínez-Romero. 2015. Arthropod-Spiroplasma relationship in the genomic era. FEMS Microbiol. Ecol. 91:1-8.
5. Carton, Y., M. Boulétreau, J. J. M. van Alphen, and J. C. van Lenteren. 1986. The Drosophila parasitic wasps. Pp. 347-394 in M. Ashburner, H. L. Carson, and J. N. Thompson, ed. The genetics and biology of Drosophila. Academic Press, London.
6. Carton, Y., F. Frey, and A. J. Nappi. 2009. Parasite-induced changes in Nitric Oxide levels in Drosophila paramelanica. J. Parasitol. 95:1134-1141.
7. Cayetano, L., and C. Vorburger. 2015. Symbiont-conferred protection against Hymenopteran parasitoids in aphids: how general is it? Ecol. Entomol. 40:85-93.
8. Colinet, D., L. Kremmer, S. Lemauf, C. Rebuf, J.-L. Gatti, and M. Poirié. 2014. Development of RNAi in a Drosophila endoparasitoid wasp and demonstration of its efficiency in impairing venom protein production. J. Insect Physiol. 63:56-61.
9. Dion, E., F. Zélé, J. C. Simon, and Y. Outreman. 2011. Rapid evolution of parasitoids when faced with the symbiont-mediated resistance of their hosts. J. Evol. Biol. 24:741-750.
10. Douglas, A. E. 2015. Multiorganismal insects: diversity and function of resident microorganisms. Annu. Rev. Entomol. 60:17-34.
11. Ferguson, N. M., D. T. Kien, H. Clapham, R. Aguas, V. T. Trung, T. N. Chau, et al. 2015. Modeling the impact on virus transmission of Wolbachia-mediated blocking of dengue virus infection of Aedes aegypti. Sci. Transl. Med. 7, 279ra37.
12. Furihata, S., M. Hirata, H. Matsumoto, and Y. Hayakawa. 2015. Bacteria endosymbiont, Wolbachia, promotes parasitism of parasitoid wasp Asobara japonica. PLoS One 10:e0140914.
13. Fytrou, A., P. G. Schofield, A. R. Kraaijeveld, and S. F. Hubbard. 2006. Wolbachia infection suppresses both host defence and parasitoid counter-defence. Proc. R. Soc. Lond. B Biol. Sci. 273:791-796.
14. Gerardo, N. M., and B. J. Parker. 2014. Mechanisms of symbiont-conferred protection against natural enemies: an ecological and evolutionary framework. Curr. Opin. Insect Sci. 4:8-14.
15. Goecks, J., N. T. Mortimer, J. A. Mobley, G. J. Bowersock, J. Taylor, and T. A. Schlenke. 2013. Integrative approach reveals composition of endoparasitoid wasp venoms. PLoS One 8:e64125.
16. Hamilton, P. T., and S. J. Perlman. 2013. Host defense via symbiosis in Drosophila. PLoS Pathog. 9:e1003808.
17. Hamilton, P. T., F. Peng, M. J. Boulanger, and S. J. Perlman. 2016. A ribosome-inactivating protein in a Drosophila defensive symbiont. Proc. Natl Acad. Sci. USA 113:350-355.
18. Haselkorn, T. S. 2010. The Spiroplasma heritable bacterial endosymbiont of Drosophila. Fly 4:80-87.
19. Haselkorn, T. S., and J. Jaenike. 2015. Macroevolutionary persistence of heritable endosymbionts: acquisition, retention and expression of adaptive phenotypes in Spiroplasma. Mol. Ecol. 24:3752-3765.
20. Haselkorn, T. S., T. A. Markow, and N. A. Moran. 2009. Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol. Ecol. 18:1294-1305.
21. Heavner, M. E., G. Gueguen, R. Rajwani, P. E. Pagan, C. Small, and S. Govind. 2013. Partial venom gland transcriptome of a Drosophila parasitoid wasp, Leptopilina heterotoma, reveals novel and shared bioactive profiles with stinging Hymenoptera. Gene 526:195-204.
22. Herren, J. K., J. C. Paredes, F. Schupfer, and B. Lemaitre. 2013. Vertical transmission of a Drosophila endosymbiont via cooption of the yolk transport and internalization machinery. MBio 4: e00532-12. doi:10.1128/mBio.00532-12.
23. Herren, J. K., J. C. Paredes, F. Schüpfer, K. Arafah, P. Bulet, and B. Lemaitre. 2014. Insect endosymbiont proliferation is limited by lipid availability. Elife 3:e02964.
24. Hoskins, R. A., J. W. Carlson, K. H. Wan, S. Park, I. Mendez, S. E. Galle, et al. 2015. The Release 6 reference sequence of the Drosophila melanogaster genome. Genome Res. 25:445-458.
25. Jaenike, J., and T. D. Brekke. 2011. Defensive endosymbionts: a cryptic trophic level in community ecology. Ecol. Lett. 14:150-155.
26. Jaenike, J., M. Polak, A. Fiskin, M. Helou, and M. Minhas. 2007. Interspecific transmission of endosymbiotic Spiroplasma by mites. Biol. Lett. 3:23-25.
27. Jaenike, J., J. K. Stahlhut, L. M. Boelio, and R. L. Unckless. 2010a. Association between Wolbachia and Spiroplasma within Drosophila neotestacea: an emerging symbiotic mutualism? Mol. Ecol. 19:414-425.
28. Jaenike, J., R. Unckless, S. N. Cockburn, L. M. Boelio, and S. J. Perlman. 2010b. Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329:212-215.
29. Kacsoh, B. Z., and T. A. Schlenke. 2012. High hemocyte load is associated with increased resistance against parasitoids in Drosophila suzukii, a relative of D. melanogaster. PLoS One 7:e34721.
30. Kacsoh, B. Z., Z. R. Lynch, N. T. Mortimer, and T. A. Schlenke. 2013. Fruit flies medicate offspring after seeing parasites. Science 339:947-950.
31. Kacsoh, B. Z., J. Bozler, and T. A. Schlenke. 2014. A role for nematocytes in the cellular immune response of the Drosophilid Zaprionus indianus. Parasitology 141:697-715.
32. Kageyama, D., H. Anbutsu, M. Watada, T. Hosokawa, M. Shimada, and T. Fukatsu. 2006. Prevalence of a non-male-killing Spiroplasma in natural populations of Drosophila hydei. Appl. Environ. Microbiol. 72:6667-6673.
33. Keebaugh, E. S., and T. A. Schlenke. 2012. Adaptive evolution of a novel Drosophila lectin induced by parasitic wasp attack. Mol. Biol. Evol. 29:565-577.
34. Keebaugh, E., and T. Schlenke. 2013. Insights from natural host-parasite interactions: The Drosophila model. Dev. Comp. Immunol. 42:111-123.
35. King, G., and L. Zeng. 2001. Logistic regression in rare events data. Polit. Analy. 9:137-163.
36. Kraaijeveld, A. R., H. C. J. Godfray, and P. Genevieve. 2009. Evolution of host resistance and parasitoid counter-resistance. Adv. Parasitol. 70:257-280.
37. Kwiatkowski, M., and C. Vorburger. 2012. Modeling the ecology of symbiont-mediated protection against parasites. Am. Nat. 179:595-605.
38. Kwiatkowski, M., J. Engelstadter, and C. Vorburger. 2012. On genetic specificity in symbiont-mediated host-parasite coevolution. PLoS Comput. Biol. 8:e1002633.
39. Lefevre, T., J. C. de Roode, B. Z. Kacsoh, and T. A. Schlenke. 2012. Defence strategies against a parasitoid wasp in Drosophila: fight or flight? Biol. Lett. 8:230-233.
40. Lukasik, P., M. A. Dawid, J. Ferrari, and H. C. Godfray. 2013. The diversity and fitness effects of infection with facultative endosymbionts in the grain aphid, Sitobion avenae. Oecologia 173:985-996.
41. Martins, A. B., I. Ventura, and L. Klaczko. 2010. Spiroplasma infection in Drosophila melanogaster: what is the advantage of killing males? J. Invertebr. Pathol. 105:145-150.
42. McLean, A. H., and H. C. Godfray. 2015. Evidence for specificity in symbiont-conferred protection against parasitoids. Proc. R. Soc. Lond. B Biol. Sci. 282: 20150977. doi: 10.1098/rspb.2015.0977.
43. Milan, N. F., B. Z. Kacsoh, and T. A. Schlenke. 2012. Alcohol consumption as self-medication against blood-borne parasites in the fruit fly. Curr. Biol. 22:488-493.
44. Montenegro, H., W. N. Souza, D. D. S. Leite, and L. B. Klaczko. 2000. Male-killing selfish cytoplasmic element causes sex-ratio distortion in Drosophila melanogaster. Heredity 85:465-470.
45. Montenegro, H., V. N. Solferini, L. B. Klaczko, and G. D. D. Hurst. 2005. Male-killing Spiroplasma naturally infecting Drosophila melanogaster. Insect Mol. Biol. 14:281-288.
46. Mortimer, N. T. 2013. Parasitoid wasp virulence: a window into fly immunity. Fly 7:31-37.
47. Oliver, K. M., J. Campos, N. A. Moran, and M. S. Hunter. 2008. Population dynamics of defensive symbionts in aphids. Proc. R. Soc. Lond. B Biol. Sci. 275:293-299.
48. Oliver, K. M., K. Noge, E. M. Huang, J. M. Campos, J. X. Becerra, and M. S. Hunter. 2012. Parasitic wasp responses to symbiont-based defense in aphids. BMC Biol. 10:11.
49. Oliver, K. M., A. H. Smith, and J. A. Russell. 2014. Defensive symbiosis in the real world-advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct. Ecol. 28:341-355.
50. Paredes, J. C., J. K. Herren, F. Schüpfer, R. Marin, S. Claverol, C.-H. Kuo, et al. 2015. Genome sequence of the Drosophila melanogaster male-killing Spiroplasma strain MSRO endosymbiont. mBio 6:e02437-14.
51. Paredes-Escobar, J. C. 2014. The useful gate-crasher: molecular interactions between Drosophila and Spiroplasma. Ph.D. diss., École Polytechnique Fédérale De Lausanne.
52. Pool, J. E., A. Wong, and C. F. Aquadro. 2006. Finding of male-killing Spiroplasma infecting Drosophila melanogaster in Africa implies transatlantic migration of this endosymbiont. Heredity 97:27-32.
53. Rouchet, R., and C. Vorburger. 2012. Strong specificity in the interaction between parasitoids and symbiont-protected hosts. J. Evol. Biol. 25:2369-2375.
54. Rouchet, R., and C. Vorburger. 2014. Experimental evolution of parasitoid infectivity on symbiont-protected hosts leads to the emergence of genotype specificity. Evolution 68:1607-1616.
55. Singh, N. D., D. R. Criscoe, S. Skolfield, K. P. Kohl, E. S. Keebaugh, and T. A. Schlenke. 2015. Fruit flies diversify their offspring in response to parasite infection. Science 349:747-750.
56. Ventura, I., A. Martins, M. Lyra, C. Andrade, K. Carvalho, and L. Klaczko. 2012. Spiroplasma in Drosophila melanogaster populations: prevalence, male-killing, molecular Identification, and no association with Wolbachia. Microb. Ecol. 64:794-801.
57. Vorburger, C. 2014. The evolutionary ecology of symbiont-conferred resistance to parasitoids in aphids. Insect Sci. 21:251-264.
58. Wachi, N., F. Y. Nomano, H. Mitsui, N. Kasuya, and M. T. Kimura. 2015. Taxonomy and evolution of putative thelytokous species of Leptopilina (Hymenoptera: Figitidae) from Japan, with description of two new species. Entomol. Sci. 18:41-54.
59. Watts, T., T. S. Haselkorn, N. A. Moran, and T. A. Markow. 2009. Variable incidence of Spiroplasma infections in natural populations of Drosophila species. PLoS One 4:e5703.
60. Xie, J., I. Vilchez, and M. Mateos. 2010. Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS One 5:e12149.
61. Xie, J., B. Tiner, I. Vilchez, and M. Mateos. 2011. Effect of the Drosophila endosymbiont Spiroplasma on parasitoid wasp development and on the reproductive fitness of wasp-attacked fly survivors. Evol. Ecol. 53:1065-1079.
62. Xie, J., S. Butler, G. Sanchez, and M. Mateos. 2014. Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps. Heredity 112:399-408.
63. Xie, J., C. Winter, L. Winter, and M. Mateos. 2015. Rapid spread of the defensive endosymbiont Spiroplasma in Drosophila hydei under high parasitoid wasp pressure. FEMS Microbiol. Ecol. 91:1-11.