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Survey of Heritable Endosymbionts in Southern Mexico Populations of the Fruit Fly Species Anastrepha striata and A. ludens

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Abstract

Heritable endosymbiotic bacteria associated with insects are ubiquitous and taxonomically diverse. Many of these endosymbionts influence the fitness of their hosts and/or manipulate their host reproduction. Exploiting the effects of endosymbionts on hosts for pest control is a growing research area, but requires knowledge of endosymbionts associated with the target pest population. In this study, we used molecular methods to screen southern Mexico populations of two species of tephritid fruit fly pests, Anastrepha ludens and A. striata, for heritable bacteria. The only heritable endosymbiont found was Wolbachia in A. striata. Based on multilocus sequence typing and phylogenetic analyses, this Wolbachia strain is new and belongs to the Wolbachia supergroup B. Wolbachia strains previously reported in members of the genus Anastrepha in South America belong to supergroup A. We discuss the potential implications for pest control of the presence of a different Wolbachia strain in southern Mexico.

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References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  2. Aluja M (1994) Bionomics and Management of Anastrepha. Annu Rev Entomol 39:155–178

    Article  Google Scholar 

  3. Baldo L, Bordenstein S, Wernegreen JJ, Werren JH (2006) Widespread recombination throughout Wolbachia genomes. Mol Biol Evol 23:437–449

    Article  PubMed  CAS  Google Scholar 

  4. Baldo L, Dunning Hotopp JC, Jolley KA, Bordenstein SR, Biber SA, Choudhury RR, Hayashi C, Maiden MCJ, Tettelin H, Werren JH (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 72:7098–7110

    Article  PubMed  CAS  Google Scholar 

  5. Brumin M, Kontsedalov S, Ghanim M (2011) Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci 18:57–66. doi:10.1111/j.1744-7917.2010.01396.x

    Article  Google Scholar 

  6. Bull JJ (1983) Evolution of sex determining mechanisms. Benjamin/Cummings, Menlo Park

    Google Scholar 

  7. Capuzzo C, Firrao G, Mazzon L, Squartini A, Girolami V (2005) ‘Candidatus Erwinia dacicola’, a coevolved symbiotic bacterium of the olive fly Bactrocera oleae (Gmelin). Int J Syst Evol Microbiol 55:1641–1647. doi:10.1099/ijs.0.63653-0

    Article  PubMed  CAS  Google Scholar 

  8. Chen D-Q, Montllor CB, Purcell AH (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

    Article  Google Scholar 

  9. Coscrato VE, Braz AS, Perondini ALP, Selivon D, Marino CL (2009) Wolbachia in Anastrepha fruit flies (Diptera: Tephritidae). Curr Microbiol 59:295–301. doi:10.1007/s00284-009-9433-8

    Article  PubMed  CAS  Google Scholar 

  10. Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev Camb Philos Soc 64:409–434. doi:10.1111/j.1469-185X.1989.tb00682.x

    Article  PubMed  CAS  Google Scholar 

  11. Douglas AE (2009) The microbial dimension in insect nutritional ecology. Funct Ecol 23:38–47

    Article  Google Scholar 

  12. Drosopoulou E, Augustinos A, Nakou I, Koeppler K, Kounatidis I, Vogt H, Papadopoulos N, Bourtzis K, Mavragani-Tsipidou P (2011) Genetic and cytogenetic analysis of the American cherry fruit fly, Rhagoletis cingulata (Diptera: Tephritidae). Genetica 139:1449–1464. doi:10.1007/s10709-012-9644-y

    Article  PubMed  Google Scholar 

  13. Folmer O, Black MB, Hoeh WR, Lutz RA, Vrijenhoek RC (1994) DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    PubMed  CAS  Google Scholar 

  14. Glaser RL, Meola MA (2010) The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS One 5:e11977. doi:10.1371/journal.pone.0011977

    Article  PubMed  Google Scholar 

  15. Haselkorn TS, Markow TA, Moran NA (2009) Multiple introductions of the Spiroplasma bacterial endosymbiont into Drosophila. Mol Ecol 18:1294–1305. doi:10.1111/j.1365-294X.2009.04085.x

    Article  PubMed  CAS  Google Scholar 

  16. Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322:702. doi:10.1126/science.1162418

    Article  PubMed  CAS  Google Scholar 

  17. Hernandez-Ortiz V, Aluja M (1993) Listado de especies del género neotropical Anastrepha (Diptera: Tephritidae) con notas sobre su distribución y plantas hospederas. Folia Entomol Mex 88:89–105

    Google Scholar 

  18. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH (2008) How many species are infected with Wolbachia?–A statistical analysis of current data. FEMS Microbiol Lett 281:215–220. doi:10.1111/j.1574-6968.2008.01110.x

    Article  PubMed  CAS  Google Scholar 

  19. Hurst GDD, Hurst LD, Majerus EN (1997) Cytoplasmic sex ratio distorters. In: O’Neill SL, Hoffmann AA, Werren JH (eds) Influential passengers: inherited microorganisms and arthropod reproduction. Oxford University Press, New York, pp 125–154

    Google Scholar 

  20. 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. doi:10.1126/science.1188235

    Article  PubMed  CAS  Google Scholar 

  21. Jamnongluk W, Kittayapong P, Baimai V, O’Neill SL (2002) Wolbachia infections of tephritid fruit flies: molecular evidence for five distinct strains in a single host species. Curr Microbiol 45:255–260. doi:10.1007/s00284-002-3746-1

    Article  PubMed  CAS  Google Scholar 

  22. Jeyaprakash A, Hoy MA (2000) Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76 % of sixty-three arthropod species. Insect Mol Biol 9:393–405

    Article  PubMed  CAS  Google Scholar 

  23. Jolley K, Chan M-S, Maiden M (2004) mlstdbNet–distributed multi-locus sequence typing (MLST) databases. BMC Bioinformatics 5:86

    Article  PubMed  Google Scholar 

  24. Jurkevitch E (2011) Riding the Trojan horse: combating pest insects with their own symbionts. Microb Biotechnol 4:620–627

    Article  PubMed  CAS  Google Scholar 

  25. Kaltenpoth M, Göttler W, Herzner G, Strohm E (2005) Symbiotic bacteria protect wasp larvae from fungal infestation. Curr Biol 15:475–479

    Article  PubMed  CAS  Google Scholar 

  26. Kellner RLL (2002) Molecular identification of an endosymbiotic bacterium associated with pederin biosynthesis in Paederus sabaeus (Coleoptera, Staphylinidae). Insect Biochem Mol Biol 32:389–395

    Article  PubMed  CAS  Google Scholar 

  27. Kittayapong P, Milne JR, Tigvattananont S, Baimai V (2000) Distribution of the reproduction-modifying bacteria, Wolbachia, in natural populations of tephritid fruit flies in Thailand. ScienceAsia 26:93–103

    Article  Google Scholar 

  28. Kounatidis I, Crotti E, Sapountzis P, Sacchi L, Rizzi A, Chouaia B, Bandi C, Alma A, Daffonchio D, Mavragani-Tsipidou P, Bourtzis K (2009) Acetobacter tropicalis is a major symbiont of the olive fruit fly (Bactrocera oleae). Appl Environ Microbiol 75:3281–3288. doi:10.1128/Aem.02933-08

    Article  PubMed  CAS  Google Scholar 

  29. Kuzina LV, Peloquin JJ, Vacek DC, Miler TA (2001) Isolation and identification of bacteria associated with adult laboratory Mexican fruit flies, Anastrepha ludens (Diptera : Tephritidae). Curr Microbiol 42:290–294

    PubMed  CAS  Google Scholar 

  30. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175

    Google Scholar 

  31. Lauzon CR, McCombs SD, Potter SE, Peabody NC (2009) Establishment and vertical passage of Enterobacter (Pantoea) agglomerans and Klebsiella pneumoniae through all life stages of the Mediterranean fruit fly (Diptera: Tephritidae). Ann Entomol Soc Am 102:85–95

    Article  Google Scholar 

  32. Leonardo TE, Muiru GT (2003) Facultative symbionts are associated with host plant specialization in pea aphid populations. Proc R Soc Lond B Biol Sci 270:S209–S212

    Article  Google Scholar 

  33. Maddison DR, Maddison W (2003) MacClade 4: analysis of phylogeny and character evolution. Sinauer Associates, Sunderland

    Google Scholar 

  34. Marchini D, Rosetto M, Dallai R, Marri L (2002) Bacteria associated with the oesophageal bulb of the medfly Ceratitis capitata (Diptera: Tephritidae). Curr Microbiol 44:120–124

    Article  PubMed  CAS  Google Scholar 

  35. Mateos M, Castrezana S, Nankivell B, Estes A, Markow TA, Moran NA (2006) Heritable endosymbionts of Drosophila. Genetics 174:363–376

    Article  PubMed  CAS  Google Scholar 

  36. Mazzon L, Piscedda A, Simonato M, Martinez-Sanudo I, Squartin A, Girolami V (2008) Presence of specific symbiotic bacteria in flies of the subfamily Tephritinae (Diptera Tephritidae) and their phylogenetic relationships: proposal of ‘Candidatus Stammerula tephritidis’. Int J Syst Evol Microbiol 58:1277–1287. doi:10.1099/ijs.0.65287-0

    Article  PubMed  CAS  Google Scholar 

  37. Montllor CB, Maxmen A, Purcell AH (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195

    Article  Google Scholar 

  38. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190. doi:10.1146/annurev.genet.41.110306.130119

    Article  PubMed  CAS  Google Scholar 

  39. Munson MA, Baumann P, Clark MA, Baumann L, Moran NA, Voegtlin DJ, Campbell BC (1991) Evidence for the establishment of aphid-eubacterium endosymbiosis in an ancestor of four aphid families. J Bacteriol 173:6321–6324

    PubMed  CAS  Google Scholar 

  40. Norrbom AL, Korytkowski CA (2011) New species of and taxonomic notes on Anastrepha (Diptera: Tephritidae). Zootaxa 2740:1–23

    Google Scholar 

  41. O’Neill SL, Karr TL (1990) Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348:178–180

    Article  PubMed  Google Scholar 

  42. Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100:1803–1807

    Article  PubMed  CAS  Google Scholar 

  43. Regassa LB, Gasparich GE (2006) Spiroplasmas: evolutionary relationships and biodiversity. Front Biosci 11:2983–3002

    Article  PubMed  CAS  Google Scholar 

  44. Riegler M, Stauffer C (2002) Wolbachia infections and superinfections in cytoplasmically incompatible populations of the European cherry fruit fly Rhagoletis cerasi (Diptera, Tephritidae). Mol Ecol 11:2425–2434

    Article  PubMed  CAS  Google Scholar 

  45. Rocha LS, Mascarenhas RO, Perondini ALP, Selivon D (2005) Occurrence of Wolbachia in Brazilian samples of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Neotrop Entomol 34:1013–1015

    Article  CAS  Google Scholar 

  46. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  47. Rousset F, Bouchon D, Pintureau B, Juchault P, Solignac M (1992) Wolbachia endosymbionts responsible for various alterations of sexuality in arthropods. Proc R Soc Lond B Biol Sci 250:91–98

    Article  CAS  Google Scholar 

  48. Russell JA, Moran NA (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc R Soc Lond B Biol Sci 273:603–610

    Article  Google Scholar 

  49. Schuler H, Arthofer W, Krumböck S, Köppler K, Vogt H (2009) The bacterial endosymbiont Wolbachia in the invasive cherry fruit fly Rhagoletis cingulata (Diptera, Tephritidae). Mitteilungen der Deutschen Gesellschaft für Allgemeine und Angewandte Entomologie 17:99–101

    Google Scholar 

  50. Schuler H, Arthofer W, Riegler M, Bertheau C, Krumbock S, Koppler K, Vogt H, Teixeira LAF, Stauffer C (2011) Multiple Wolbachia infections in Rhagoletis pomonella. Entomol Exp Appl 139:138–144. doi:10.1111/j.1570-7458.2011.01115.x

    Article  Google Scholar 

  51. Stamatakis A (2006) Phylogenetic models of rate heterogeneity: A high performance computing perspective. In: Proceedings of the IEEE International Parallel & Distributed Processing Symposium, Rhodos

  52. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690. doi:10.1093/bioinformatics/btl446

    Article  PubMed  CAS  Google Scholar 

  53. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML Web servers. Syst Biol 57:758–771. doi:10.1080/10635150802429642

    Article  PubMed  Google Scholar 

  54. Sukumaran J, Holder MT (2010) DendroPy: a Python library for phylogenetic computing. Bioinformatics 26:1569–1571. doi:10.1093/bioinformatics/btq228

    Article  PubMed  CAS  Google Scholar 

  55. Sun X, Cui LW, Li ZH (2007) Diversity and phylogeny of Wolbachia infecting Bactrocera dorsalis (Diptera : Tephritidae) populations from China. Environ Entomol 36:1283–1289

    Article  PubMed  CAS  Google Scholar 

  56. Teixeira L, Ferreira A, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6:2753–2763. doi:10.1371/journal.pbio.1000002

    Article  CAS  Google Scholar 

  57. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  58. Tsuchida T, Koga R, Fukatsu T (2004) Host plant specialization governed by facultative symbiont. Science 303:1989. doi:10.1126/science.1094611

    Article  PubMed  CAS  Google Scholar 

  59. Werren J, O’Neill S (1997) The evolution of heritable symbionts. In: O’Neill S, Hoffmann A, Werren J (eds) Influential passengers: inherited microorganisms and arthropod reproduction. Oxford University Press, Oxford, pp 1–41

    Google Scholar 

  60. Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Micro 6:741–751. doi:10.1038/nrmicro1969

    Article  CAS  Google Scholar 

  61. Xie J, Tiner B, Vilchez I, Mateos M (2011) Effect of the Drosophila endosymbiont Spiroplasma on parasitoid wasp development and on the reproductive fitness of wasp-attacked fly survivors. Evol Ecol 25:1065–1079

    Article  Google Scholar 

  62. Xie J, Vilchez I, Mateos M (2010) Spiroplasma bacteria enhance survival of Drosophila hydei attacked by the parasitic wasp Leptopilina heterotoma. PLoS One 5:e12149

    Article  PubMed  Google Scholar 

  63. Yuval B, Ben-Ami E, Behar A, Ben-Yosef M, Jurkevitch E (2010) The Mediterranean fruit fly and its bacteria—potential for improving sterile insect technique operations. J Appl Entomol. doi:10.1111/j.1439-0418.2010.01555.x

  64. Zabalou S, Apostolaki A, Livadaras I, Franz G, Robinson AS, Savakis C, Bourtzis K (2009) Incompatible insect technique: incompatible males from a Ceratitis capitata genetic sexing strain. Entomol Exp Appl 132:232–240

    Article  Google Scholar 

  65. Zabalou S, Riegler M, Theodorakopoulou M, Stauffer C, Savakis C, Bourtzis K (2004) Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proc Natl Acad Sci USA 101:15042–15045. doi:10.1073/pnas.0403853101

    Article  PubMed  CAS  Google Scholar 

  66. Zindel R, Gottlieb Y, Aebi A (2011) Arthropod symbioses: a neglected parameter in pest- and disease-control programmes. J Appl Ecol 48:864–872. doi:10.1111/j.1365-2664.2011.01984.x

    Article  Google Scholar 

  67. Zwickl DJ (2006) Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation, The University of Texas at Austin

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Acknowledgments

We thank A. Oropeza, R. Bustamante, S. Salgado, E. De Leon, R. Rincón, S. Rodríguez, and G. Rodas for technical assistance at ECOSUR. The Moscafrut (IICA-SAGARPA) facility for providing mass reared A. ludens flies. Funding provided by TAMU-CONACyT grant to Mariana Mateos, Jorge Toledo, Pablo Liedo; NSF grant DEB 0743782 to Mariana Mateos and Luis A. Hurtado. The Texas A&M University Brazos HPC cluster contributed to the research reported here. This is publication No. 216 of the Texas A&M University Center for Biosystematics and Biodiversity. This publication made use of the Wolbachia MLST website (http://pubmlst.org/Wolbachia/) developed by Keith Jolley, hosted at the University of Oxford, and funded by the Wellcome Trust and the US National Science Foundation.

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  1. Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, Texas, USA

    Humberto Martínez & Mariana Mateos

  2. El Colegio de la Frontera Sur, Tapachula, Chiapas, Mexico

    Jorge Toledo & Pablo Liedo

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  1. Humberto Martínez
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Martínez, H., Toledo, J., Liedo, P. et al. Survey of Heritable Endosymbionts in Southern Mexico Populations of the Fruit Fly Species Anastrepha striata and A. ludens . Curr Microbiol 65, 711–718 (2012). https://doi.org/10.1007/s00284-012-0223-3

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