Eur. J. Entomol. 117: 149-156, 2020 | DOI: 10.14411/eje.2020.017

Facultative symbionts associated with aphid populations in citrus orchards in northern TunisiaOriginal article

François RENOZ1, Inès PONS1, Christine NOËL1, Kaouthar LEBDI-GRISSA2, Vincent FORAY3, Thierry HANCE1
1 Earth and Life Institute, Biodiversity Research Centre, UC Louvain, ELIB - Croix du sud 4-5 bte L7.07.04, 1348 Louvain-la-Neuve, Belgium; e-mails: francois.renoz@uclouvain.be, ines.pons@uclouvain.be, christine.noel56@hotmail.com, Thierry.hance@uclouvain.be
2 Laboratory of Entomology and Acarology, National Agronomic Institute of Tunisia (INAT) - University of Carthage, 43 Avenue Charles Nicolle, Cité Mahrajène, 1082 Tunis, Tunisia, e-mail: grissak@yahoo.fr
3 Institut de Recherche sur la Biologie de l'Insecte (IRBI), UMR CNRS 7261, 37200 Tours, France; e-mail: vincent.foray@univ-tours.fr

Like many insects, aphids (Hemiptera: Aphididae) can host a wide diversity of symbiotic bacteria that can be important drivers of their evolutionary ecology. In addition to the nutritional obligate symbiont Buchnera aphidicola, these phloem-sap feeding insects can host various facultative symbionts whose functional diversity depends on complex interactions with the host genotype and environmental factors. During sampling in citrus orchards in northern Tunisia, we collected aphids on citrus plants. The specimens belonged either to the cotton-melon aphid Aphis gossypii or the green citrus aphid Aphis spiraecola. We analysed the prevalence of Arsenophonus, Serratia symbiotica, Hamiltonella defensa and Regiella insecticola, four facultative symbionts frequently found in the genus Aphis and potentially associated with phenotypic effects related to nutrition, protection against parasites and tolerance of high temperatures. We found that the diversity and prevalence of facultative symbionts differed between these two aphid species that exploit similar ecological niches. In particular, we found a high prevalence of Arsenophonus in A. gossypii populations and that the defensive symbiont H. defensa was only present in A. spiraecola populations. These results are discussed in light of the ecology and life cycles of each of the species of aphid studied.

Keywords: Hemiptera, Aphididae, Aphis gossypii, Aphis spiraecola, Arsenophonus, Serratia symbiotica, co-infection, 16S rRNA, Citrus, Tunisia

Received: November 22, 2019; Revised: March 19, 2020; Accepted: March 19, 2020; Published online: April 9, 2020  Show citation

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RENOZ, F., PONS, I., NOËL, C., LEBDI-GRISSA, K., FORAY, V., & HANCE, T. (2020). Facultative symbionts associated with aphid populations in citrus orchards in northern Tunisia. EJE, 117, Article 149-156. https://doi.org/10.14411/eje.2020.017
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    References

    1. Arneodo J.D. & Ortego J. 2014: Exploring the bacterial microbiota associated with native South American species of Aphis (Hemiptera: Aphididae). - Environ. Entomol. 43: 589-594. Go to original source...
    2. Ayoubi A., Talebi A.A., Fathipour Y. & Mehrabadi M. 2020: Coinfection of the secondary symbionts, Hamiltonella defensa and Arsenophonus sp. contribute to the performance of the major aphid pest, Aphis gossypii (Hemiptera: Aphididae). - Insect Sci. 27: 86-98. Go to original source...
    3. Blackman R.L. & Eastop V.F. 2000: Aphids on the World's Crops: An Identification and Information Guide. Wiley-Blackwell, New York, 476 pp.
    4. Boukhris-Bouhachem S. 2011: Aphid enemies reported from Tunisian Citrus orchards. - Tunis. J. Plant Prot. 6: 21-28.
    5. Boukhris-Bouhachem S., Ben Fekih I., Nahdi S. & Souissi R. 2017: Capacity assessment of Myzus persicae, Aphis gossypii and Aphis spiraecola (Hemiptera: Aphididae) to acquire and retain PVYNTN in Tunisia. - Arthr.-Plant Interact. 11: 669-674. Go to original source...
    6. Brady C.M. & White J.A. 2013: Cowpea aphid (Aphis craccivora) associated with different host plants has different facultative endosymbionts. - Ecol. Entomol. 38: 433-437. Go to original source...
    7. Brady C.M., Asplen M.K., Desneux N., Heimpel G.E., Hopper K.R., Linnen C.R., Oliver K.M., Wulff J.A. & White J.A. 2014: Worldwide populations of the aphid Aphis craccivora are infected with diverse facultative bacterial symbionts. - Microb. Ecol. 67: 195-204. Go to original source...
    8. Burke G., Fiehn O. & Moran N. 2010: Effects of facultative symbionts and heat stress on the metabolome of pea aphids. - ISME J. 4: 242-252. Go to original source...
    9. Carletto J., Gueguen G., Fleury F. & Vanlerberghe-Masutti F. 2008: Screening the bacterial endosymbiotic community of sap-feeding insects by terminal-restriction fragment length polymorphism analysis. - Entomol. Exp. Appl. 129: 228-234. Go to original source...
    10. Caspi-Fluger A., Inbar M., Mozes-Daube N., Katzir N., Portnoy V., Belausov E., Hunter M.S. & Zchori-Fein E. 2011: Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. - Proc. R. Soc. Lond. (B) 279: 1791-1796. Go to original source...
    11. 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. Lond. (B) 275: 565-570. Go to original source...
    12. Desneux N., Asplen M.K., Brady C.M., Heimpel G.E., Hopper K.R., Luo C., Monticelli L., Oliver K.M. & White J.A. 2018: Intraspecific variation in facultative symbiont infection among native and exotic pest populations: Potential implications for biological control. - Biol. Contr. 116: 27-35. Go to original source...
    13. Douglas A.E. 1998: Nutritional interactions in insect-microbial symbioses: Aphids and their symbiotic bacteria Buchnera. - Annu. Rev. Entomol. 43: 17-37. Go to original source...
    14. Duron O. 2014: Arsenophonus insect symbionts are commonly infected with APSE, a bacteriophage involved in protective symbiosis. - FEMS Microbiol. Ecol. 90: 184-194. Go to original source...
    15. Elhaddad A., ElAmrani A., Fereres A. & Moreno A. 2016: Spatial and temporal spread of Citrus tristeza virus and its aphid vectors in the North western area of Morocco. - Insect Sci. 23: 903-912. Go to original source...
    16. Fakhour S., Ambroise J., Renoz F., Foray V., Gala J.-L. & Hance T. 2018: A large-scale field study of bacterial communities in cereal aphid populations across Morocco. - FEMS Microbiol. Ecol. 94(3): 11 pp. Go to original source...
    17. Ferrari J. & Vavre F. 2011: Bacterial symbionts in insects or the story of communities affecting communities. - Philos. Trans. R. Soc. (B) 366: 1389-1400. Go to original source...
    18. Ferrari J., West J.A., Via S. & Godfray H.C.J. 2012: Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex. - Evolution 66: 375-390. Go to original source...
    19. Gehrer L. & Vorburger C. 2012: Parasitoids as vectors of facultative bacterial endosymbionts in aphids. - Biol. Lett. 8: 613-615. Go to original source...
    20. Gueguen G., Vavre F., Gnankine O., Peterschmitt M., Charif D., Chiel E., Gottlieb Y., Ghanim M., Zchori-Fein E. & Fleury F. 2010: Endosymbiont metacommunities, mtDNA diversity and the evolution of the Bemisia tabaci (Hemiptera: Aleyrodidae) species complex. - Mol. Ecol. 19: 4365-4376. Go to original source...
    21. Halima-Kamel M.B. & Hamouda M.H.B. 2004: Aphids of fruit trees in Tunisia. In Simon J.C., Dedryver C.A., Rispe C. & Hulle M. (eds): Aphids in a New Millennium. INRA, Paris, pp. 119-124.
    22. Henry L.M., Peccoud J., Simon J.-C., Hadfield J.D., Maiden M.J.C, Ferrari J. & Godfray H.C.J. 2013: Horizontally transmitted symbionts and host colonization of ecological niches. - Curr. Biol. 23: 1713-1717. Go to original source...
    23. Henry L.M., Maiden M.C.J., Ferrari J. & Godfray H.C.J. 2015: Insect life history and the evolution of bacterial mutualism. - Ecol. Lett. 18: 516-525. Go to original source...
    24. Jacas J.A., Karamaouna F., Vercher R. & Zappalà L. 2010: Citrus Pest Management in the Northern Mediterranean Basin (Spain, Italy and Greece). In Ciancio A. & Mukerji K.G. (eds): Integrated Management of Arthropod Pests and Insect Borne Diseases, Integrated Management of Plant Pests and Diseases. Springer, Dordrecht, pp. 3-27. Go to original source...
    25. Jones R.T., Bressan A., Greenwell A.M. & Fierer N. 2011: Bacterial communities of two parthenogenetic aphid species cocolonizing two host plants across the Hawaiian Islands. - Appl. Environ. Microbiol. 77: 8345-8349. Go to original source...
    26. Jousselin E., d'Acier A.C., Vanlerberghe-Masutti F. & Duron O. 2013: Evolution and diversity of Arsenophonus endosymbionts in aphids. - Mol. Ecol. 22: 260-270. Go to original source...
    27. Kaneko S. 2018: Seasonal differences in the abundance of an ant-adapted parasitoid, Lysiphlebus japonicus (Hymenoptera: Aphidiidae), in ant-attended colonies of the spirea aphid Aphis spiraecola (Hemiptera: Aphididae) on citrus: comparison for two ant species, Lasius japonicus and Pristomyrmex punctatus (Hymenoptera: Formicidae). - Appl. Entomol. Zool. 53: 315-321. Go to original source...
    28. Karami-Jamour T., Mirmoayedi A., Zamani A. & Khajehzadeh Y. 2018: The impact of ant attendance on protecting Aphis gossypii against two aphidophagous predators and it's role on the intraguild predation between them. - J. Insect Behav. 31: 222-239. Go to original source...
    29. Leclair M., Polin S., Jousseaume T., Simon J.-C., Sugio A., Morlière S., Fukatsu T., Tsuchida T. & Outreman Y. 2016: Consequences of co-infection with protective symbionts on the host phenotype and symbiont titres in the pea aphid system. - Insect Sci. 24: 798-808. Go to original source...
    30. 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. Go to original source...
    31. Limem Sellami E., Delvare G. & Chermiti B. 2013: Parasitoids and hyperparasites of citrus aphids in northern east of Tunisia (Cap Bon). - IOBC/WPRS Bull. 95: 131-139.
    32. £ukasik P., Guo H., van Asch M., Ferrari J. & Godfray H.C.J. 2013: 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. Go to original source...
    33. Mathé-Hubert H., Kaech H., Hertaeg C., Jaenike J. & Vorburger C. 2019: Nonrandom associations of maternally transmitted symbionts in insects: The roles of drift versus biased cotransmission and selection. - Mol. Ecol. 28: 5330-5346. Go to original source...
    34. McLean A.H.C, Asch M., Ferrari J. & Godfray H.C.J. 2011: Effects of bacterial secondary symbionts on host plant use in pea aphids. - Proc. R. Soc. Lond. (B) 278: 760-766. Go to original source...
    35. McLean A.H.C, Godfray H.C.J, Ellers J. & Henry L.M. 2019: Host relatedness influences the composition of aphid microbiomes. - Environ. Microbiol. Rep. 11: 808-816. Go to original source...
    36. Metoui N., Hamrouni L., Dhaoudi F. & Bettaieb T. 2014: Notes ethnobotanique et phytopharmacologique sur la Maltaise de Tunisie. - Phytothérapie 12: 105-108. Go to original source...
    37. 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. Go to original source...
    38. Moran N.A. & Dunbar H.E. 2006: Sexual acquisition of beneficial symbionts in aphids. - Proc. Natl. Acad. Sci. 103: 12803-12806. Go to original source...
    39. Najar-Rodríguez A.J., McGraw E.A., Mensah R.K., Pittman G.W. & Walter G.H. 2009: The microbial flora of Aphis gossypii: Patterns across host plants and geographical space. - J. Invertebr. Pathol. 100: 123-126. Go to original source...
    40. Nyabuga F.N., Outreman Y., Simon J.-C., Heckel D.G. & Weisser W.W. 2010: Effects of pea aphid secondary endosymbionts on aphid resistance and development of the aphid parasitoid Aphidius ervi: a correlative study. - Entomol. Exp. Appl. 136: 243-253. Go to original source...
    41. Oliver K.M., Russell J.A., Moran N.A. & Hunter M.S. 2003: Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. - Proc. Natl. Acad. Sci. 100: 1803-1807. Go to original source...
    42. Oliver K.M., Moran N.A. & Hunter M.S. 2006: Costs and benefits of a superinfection of facultative symbionts in aphids. ‒ Proc. R. Soc. Lond. (B) 273: 1273-1280. Go to original source...
    43. 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. Go to original source...
    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. Go to original source...
    45. Pons I., Renoz F., Noël C. & Hance T. 2019: New insights into the nature of symbiotic associations in aphids: Infection process, biological effects and transmission mode of cultivable Serratia symbiotica bacteria. - Appl. Environ. Microbiol. 85(10): e02445-18, 15 pp. Go to original source...
    46. Rouchet R. & Vorburger C. 2014: Experimental evolution of parasitoid infectivity on symbiont-protected hosts leads to the emergence of genotype specificity. - Evolution 68: 1607-1616. Go to original source...
    47. Russell J.A., Weldon S., Smith A.H., Kim K.L., Hu Y., £ukasik P., Doll S., Anastopoulos I., Novin M. & Oliver K.M. 2013: Uncovering symbiont-driven genetic diversity across North American pea aphids. - Mol. Ecol. 22: 2045-2059. Go to original source...
    48. Russell J.A., Oliver K.M. & Hansen A.K. 2017: Band-aids for Buchnera and B vitamins for all. - Mol. Ecol. 26: 2199-2203. Go to original source...
    49. 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. Go to original source...
    50. Scarborough C.L., Ferrari J. & Godfray H.C.J. 2005. Aphid protected from pathogen by endosymbiont. - Science 310: 1781-1781. Go to original source...
    51. Schmid M., Sieber R., Zimmermann Y.-S. & Vorburger C. 2012: Development, specificity and sublethal effects of symbiont-conferred resistance to parasitoids in aphids. - Funct. Ecol. 26: 207-215. Go to original source...
    52. Simon J.-C., Boutin S., Tsuchida T., Koga R., Le Gallic J.-F., Frantz A., Outreman Y. & Fukatsu T. 2011: Facultative Symbiont infections affect aphid reproduction. - PLoS ONE 6(7): e21831, 10 pp. Go to original source...
    53. Skaljac M., Kirfel P., Grotmann J. & Vilcinskas A. 2018: Fitness costs of infection with Serratia symbiotica are associated with greater susceptibility to insecticides in the pea aphid Acyrthosiphon pisum. - Pest Manag. Sci. 74: 1829-1836. Go to original source...
    54. Tian P.-P., Chang C.-Y., Miao N.-H., Li M.-Y. & Liu X.-D. 2019: The facultative endosymbiont Arsenophonus infections alter aphid (Aphis gossypii) performance on the amino acid-deficient diet. - Appl. Environ. Microbiol. 85(23): e01407-19, 11 pp. Go to original source...
    55. Tsuchida T., Koga R. & Fukatsu T. 2004: Host plant specialization governed by facultative symbiont. - Science 303: 1989. Go to original source...
    56. Tsuchida T., Koga R., Horikawa M., Tsunoda T., Maoka T., Matsumoto S., Simon J.-C. & Fukatsu T. 2010: Symbiotic bacterium modifies aphid body color. - Science 330: 1102-1104. Go to original source...
    57. Tsuchida T., Koga R., Fujiwara A. & Fukatsu T. 2014: Phenotypic effect of "Candidatus Rickettsiella viridis," a facultative symbiont of the pea aphid (Acyrthosiphon pisum), and its interaction with a coexisting symbiont. - Appl. Environ. Microbiol. 80: 525-533. Go to original source...
    58. Vorburger C. 2018: Symbiont-conferred resistance to parasitoids in aphids - Challenges for biological control. - Biol. Contr. 116: 17-26. Go to original source...
    59. Vorburger C., Gehrer L. & Rodriguez P. 2010: A strain of the bacterial symbiont Regiella insecticola protects aphids against parasitoids. - Biol. Lett. 6: 109-111. Go to original source...
    60. Wagner S.M., Martinez A.J., Ruan Y.-M., Kim K.L., Lenhart P.A., Dehnel A.C., Oliver K.M. & White J.A. 2015: Facultative endosymbionts mediate dietary breadth in a polyphagous herbivore. - Funct. Ecol. 29: 1402-1410. Go to original source...
    61. Weldon S.R., Strand M.R. & Oliver K.M. 2013: Phage loss and the breakdown of a defensive symbiosis in aphids. - Proc. R. Soc. (B) 280: 20122103, 7 pp. Go to original source...
    62. Wulff J.A. & White J.A. 2015: The endosymbiont Arsenophonus provides a general benefit to soybean aphid (Hemiptera: Aphididae) regardless of host plant resistance (Rag). - Environ. Entomol. 44: 574-581. Go to original source...
    63. Wulff J.A., Buckman K.A., Wu K., Heimpel G.E. & White J.A. 2013: The endosymbiont Arsenophonus is widespread in soybean aphid, Aphis glycines, but does not provide protectionfrom parasitoids or a fungal pathogen. - PLoS ONE 8(4): e62145, 7 pp. Go to original source...
    64. Xu S., Jiang L., Qiao G. & Chen J. 2019: The bacterial flora associated with the polyphagous aphid Aphis gossypii Glover (Hemiptera: Aphididae) is strongly affected by host plants. - Microb. Ecol. [in press] doi: 10.1007/s00248-019-01435-2. Go to original source...
    65. Zhang S., Luo J., Wang L., Zhang L., Zhu X., Jiang W. & Cui J. 2018: Bacterial communities in natural versus pesticide-treated Aphis gossypii populations in North China. - Microbiol. Open 8: e652, 10 pp. Go to original source...
    66. Zhao Y., Zhang S., Luo J.-Y., Wang C.-Y., Lv L.-M. & Cui J.-J. 2016: Bacterial communities of the cotton aphid Aphis gossypii associated with Bt cotton in northern China. - Sci. Rep. 6: 22958, 8 pp. Go to original source...
    67. Zytynska S.E. & Weisser W.W. 2016: The natural occurrence of secondary bacterial symbionts in aphids. - Ecol. Entomol. 41: 13-26. Go to original source...
    68. Zytynska S.E., Meyer S.T., Sturm S., Ullmann W., Mehrparvar M. & Weisser W.W. 2015: Secondary bacterial symbiont community in aphids responds to plant diversity. - Oecologia 180: 735-747. Go to original source...
    69. Zytynska S.E., Thighiouart K. & Frago E. 2019: A meta-analysis on the benefits and costs of hosting secondary endosymbionts in sap-sucking insects. - bioRxiv URL: https://doi.org/10.1101/563031, 19 pp. Go to original source...

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