Eur. J. Entomol. 110 (2): 197-204, 2013 | DOI: 10.14411/eje.2013.030

Endosymbiont-free ants: Molecular biological evidence that neither Wolbachia, Cardinium or any other bacterial endosymbionts play a role in thelytokous parthenogenesis in the harvester ant species, Messor barbarus and M. capitatus (Hymenoptera: Formicidae)

Paloma MARTÍNEZ-RODRÍGUEZ1, Jonás SARASA1, Begoña PECO2, Berta M. JAUREGUI3, Desiree RIVERA2, Jose L. BELLA1
1 Departamento de Biología (Genética), Facultad de Ciencias, Universidad Autónoma de Madrid, C/ Darwin 2, E-28049 Madrid, Spain; e-mails: paloma.martinez@uam.es; jonas.sarasa@uam.es; bella@uam.es
2 Departamento de Ecología, Facultad de Ciencias, Universidad Autónoma de Madrid, C/ Darwin 2, E-28049 Madrid, Spain; e-mails: begonna.peco@uam.es; desi.rivera@gmail.com
3 Servicio de I+D+i. Obrascón Huarte Lain S.A., Pº de la Castellana 259D, Torre Espacio, 28046 Madrid, Spain; e-mail: berta7punto@yahoo.es

Thelytokous parthenogenesis is a type of sex determination in which females are produced from unfertilized eggs. Genetic and endosymbiont-induced forms of thelytoky have been described in the Hymenoptera. Our study has revealed that Wolbachia, Cardinium, Spiroplasma and other endosymbionts are probably absent in Iberian populations of harvester ants, Messor barbarus and Messor capitatus (Hymenoptera: Formicidae: Myrmicinae) and are thus not involved as factors in the sex determination of these two species. Our results lend weight to previous suggestions that bacterial parthenogenesis induction in Hymenoptera is probably limited to the reproductive systems of chalcidoid and cynipoid parasitoid wasps (Hymenoptera: Apocrita: Chalcidoidea and Cynipoidea, respectively).

Keywords: Wolbachia, Cardinium, Spiroplasma, endosymbionts, Formicidae, Messor, thelytokous parthenogenesis

Received: June 29, 2012; Accepted: November 26, 2012; Published: April 11, 2013

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References

  1. ADACHI-HAGIMORI T., MIURA K. & STOUTHAMER R. 2008: A new cytogenetic mechanism for bacterial endosymbiont-induced parthenogenesis in Hymenoptera. - Proc. R. Soc. Lond. (B) 275: 2667-2673 Go to original source...
  2. AGOSTI D. 1987: A provisional list of the Balkan ants (Hym. Formicidae) with a key to the worker caste. II. Key to the worker caste, including the European species without the Iberian. - Mitt. Schweiz. Entomol. Ges. 60: 261-293.
  3. AGRAWAL A.F. 2009: Differences between selection on sex versus recombination in red queen models with diploid hosts. - Evolution 63: 2131-2141 Go to original source...
  4. ARTHOFER W., RIEGLER M., SCHULER H., SCHNEIDER D., MODER K., MILLER W.J. & STAUFFER C. 2011: Allele intersection analysis: A novel tool for multi locus sequence assignment in multiply infected hosts. - PloS One 6: e22198 Go to original source...
  5. BALDO L., BORDENSTEIN S., WERNEGREEN J.J. & WERREN J.H. 2006a: Widespread recombination throughout Wolbachia genomes. - Mol. Biol. Evol. 23: 437-449 Go to original source...
  6. BALDO L., HOTOPP J.C.D., JOLLEY K.A., BORDENSTEIN S., BIBER S.A., CHOUDHURY R.R., HAYASHI C., MAIDEN M.C.J., TETTELIN H. & WERREN J.H. 2006b: Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. - Appl. Environ. Microbiol. 72: 7098-7110 Go to original source...
  7. BELL G. 1982: The Masterpiece of Nature: The Evolution and Genetics of Sexuality. University of California Press, Berkeley, 635 pp
  8. BIRKY C.W. & BARRACLOUGH T.G. 2009: Asexual speciation. In Schon K. & Van Dijk P. (eds): Lost Sex: The Evolutionary Biology of Parthenogenesis. Springer, Heidelberg, pp. 201-216
  9. BOLTON B. 1982: Afrotropical species of the myrmicine ant genera Cardiocondyla, Leptothorax, Melissotarsus, Messor and Cataulacus (Formicidae). - Bull. Br. Mus. Nat. Hist. (Entomol.) 45: 307-370
  10. BREEUWER J.A.J. & WERREN J.H. 1990: Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. - Nature 346: 558-560 Go to original source...
  11. CAGNIANT H. 1998: Le genre Messor au Maroc (Hymenoptera: Formicidae). - Ann. Soc. Entomol. Fr. (N.S.). 33: 419-434
  12. COOK J.M. 1993: Sex determination in the Hymenoptera: a review of models and evidence. - Heredity 71: 421-435 Go to original source...
  13. CORDAUX R., BOUCHON D. & GREVE P. 2011: The impact of endosymbionts on the evolution of host sex-determination mechanisms. - Trends Genet. 27: 332-341 Go to original source...
  14. FOUCAUD J., FOURNIER D., ORIVEL J., DELABIE J.H.C., LOISEAU A., LE BRETON J., KERGOAT G.J. & ESTOUP A. 2007: Sex and clonality in the little fire ant. - Mol. Biol. Evol. 24: 2465-2473 Go to original source...
  15. FOURNIER D. & ARON S. 2009: Evolution: No-male's land for an Amazonian ant. - Curr. Biol. 19: R738-R740 Go to original source...
  16. FOURNIER D., ESTOUP A., ORIVEL J., FOUCAUD J., JOURDAN H., LE BRETON J. & LE KELLER L. 2005: Clonal reproduction by males and females in the little fire ant. - Nature 435: 1230-1234 Go to original source...
  17. FROST C.L., FERNANDEZ-MARIN H., SMITH J.E. & HUGHES W.O.H. 2010: Multiple gains and losses of Wolbachia symbionts across a tribe of fungus-growing ants. - Mol. Ecol. 19: 4077-4085 Go to original source...
  18. GASPARICH G.E., WHITCOMB R.F., DODGE D., FRENCH F.E., GLASS J. & WILLIAMSON D.L. 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 Go to original source...
  19. GIORGINI M., BERNARDO U., MONTI M.M., NAPPO A.G. & GEBIOLA M. 2010: Rickettsia symbionts cause parthenogenetic reproduction in the parasitoid wasp Pnigalio soemius (Hymenoptera: Eulophidae). - Appl. Environ. Microbiol. 76: 2589-2599 Go to original source...
  20. GOROPASHNAYA A., FEDOROV V., SEIFERT B. & PAMILO P. 2007: Phylogeography and population structure in the ant Formica exsecta (Hymenoptera, Formicidae) across Eurasia as reflected by mitochondrial DNA variation and microsatellites. - Ann. Zool. Fenn. 44: 462-474
  21. GRASSO D.A., MORI A., LE MOU F., GIOVANNOTTI M. & FANFANI A. 1998: The stridulatory organ of four Messor ant species (Hymenoptera, Formicidae). - Ital. J. Zool. 65: 167-174 Go to original source...
  22. GRASSO D.A., WENSELEERS T., MORI A., LE MOLI F. & BILLEN J. 2000: Thelytokous worker reproduction and lack of Wolbachia infection in the harvesting ant Messor capitatus. - Ethol. Ecol. Evol. 12: 309-314 Go to original source...
  23. HAGIMORI T., ABE Y., DATE S. & KAZUKI M. 2006: The first finding of a Rickettsia bacterium associated with parthenogenesis induction among insects. - Curr. Microbiol. 52: 97-101 Go to original source...
  24. HEIMPEL G.E. & DE BOER J.G. 2008: Sex determination in the Hymenoptera. - Annu. Rev. Entomol. 53: 209-230 Go to original source...
  25. HIMLER A.G., CALDERA E.J., BAER B.C., FERNANDEZ-MARIN H. & MUELLER U.G. 2009: No sex in fungus-farming ants or their crops. - Proc. R. Soc. Lond. (B) 276: 2611-2616 Go to original source...
  26. HONG X.Y., GOTOH T. & NODA H. 2002: Sensitivity comparison of PCR primers for detecting Wolbachia in spider mites. - Appl. Entomol. Zool. 37: 379-383 Go to original source...
  27. HUNTER M.S., PERLMAN S.J. & KELLY S.E. 2003: A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. - Proc. R. Soc. Lond. (B) 270: 2185-2190 Go to original source...
  28. HURST L.D. & PECK J.R. 1996: Recent advances in understanding of the evolution and maintenance of sex. - Trends Ecol. Evol. 11: 46-52 Go to original source...
  29. HURST G.D.D., VON DER SCHULENBURG J.H.G., MAJERUS T.M.O., BERTRAND D., ZAKHAROV I.A., BAUNGAARD J., VOLKL W., STOUTHAMER R. & MAJERUS M.E.N. 1999: Invasion of one insect species, Adalia bipunctata, by two different malekilling bacteria. - Insect Mol. Biol. 8: 133-139 Go to original source...
  30. ITOW T., KOBAYASHI K., KUBOTA M., OGATA K., IMAI H. & CROZIER R. 1984: The reproductive cycle of the queenless ant Pristomyrmex pungens. - Insectes Soc. 31: 87-102 Go to original source...
  31. JIGGINS F.M., HURST G.D., JIGGINS C.D., V. D. SCHULENBURG J.H. & MAJERUS M.E. 2000: The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium. - Parasitology 120: 439-446 Go to original source...
  32. KRONAUER D.J.C., PIERCE N.E. & KELLER L. 2012: Asexual reproduction in introduced and native populations of the ant Cerapachys biroi. - Mol. Ecol. 21: 5221-5235 Go to original source...
  33. LAPEVA-GJONOVA A., ANTONOVA V., RADCHENKO A. & ATANASOVA M. 2010: Catalogue of the ants (Hymenoptera, Formicidae) of Bulgaria. - Zookeys 62: 1-124 Go to original source...
  34. LEGNER E.F. 1987: Transfer of thelytoky to arrhenotokous. Muscidifurax raptor Girault and Sanders (Hymenoptera: Pteromalidae). - Can. Entomol. 119: 265-271 Go to original source...
  35. LENOIR A. & CAGNIANT H. 1986: Role of worker thelytoky in colonies of the ant Cataglyphis cursor (Hymenoptera: Formicidae). - Entomol. Gener. 11: 153-157 Go to original source...
  36. LOFSTROM C., AXELSSON C. & RADSTROM P. 2008: Validation of a diagnostic PCR method for routine analysis of Salmonella spp. in animal feed samples. - Food Anal. Meth. 1: 23-27 Go to original source...
  37. LOMBARDO M. 2008: Access to mutualistic endosymbiotic microbes: an underappreciated benefit of group living. - Behav. Ecol. Sociobiol. 62: 479-497 Go to original source...
  38. LUNT D., IBRAHIM K. & HEWITT G. 1998: mtDNA phylogeography and postglacial patterns of subdivision in the meadow grasshopper Chorthippus parallelus. - Heredity 80: 633-641 Go to original source...
  39. MARCON H.S., COSCRATO V.E., SELIVON D., PARANHOS-PERONDINI A.L. & MARINO C.L. 2011: Variations in the sensitivity of different primers for detecting Wolbachia in Anastrepha (Diptera: Tephritidae). - Brazil. J. Microbiol. 42: 778-785. Go to original source...
  40. MARTINEZ P., DEL CASTILLO P. & BELLA J.L. 2009: Cytological detection of Wolbachia in squashed and paraffin embedded insect tissues. - Biotech. Histochem. 84: 347-353 Go to original source...
  41. MAYNARD S. 1978: The Evolution of Sex. Cambridge University Press, Cambridge, 236 pp
  42. OHKAWARA K., NAKAYAMA M., SATO A., TRINDL A. & HEINZE J. 2006: Clonal reproduction and genetic caste differences in a queen-polymorphic ant, Vollenhovia emeryi. - Biol. Lett. 2: 359-363 Go to original source...
  43. OKAMOTO M. & OHKAWARA K. 2009: Conditional mating tactics in queen of inquiline ant Vollenhovia nipponica. - Ethol. Ecol. Evol. 21: 137-146 Go to original source...
  44. PARKIN E.J. & BUTLIN R.K. 2004: Within- and betweenindividual sequence variation among ITS1 copies in the meadow grasshopper Chorthippus parallelus indicates frequent intrachromosomal gene conversion. - Mol. Biol. Evol. 21: 1595-1601 Go to original source...
  45. PEARCY M., ARON S., DOUMS C. & KELLER L. 2004: Conditional use of sex and parthenogenesis for worker and queen production in ants. - Science 306: 1780-1783 Go to original source...
  46. PEARCY M., HARDY O. & ARON S. 2006: Thelytokous parthenogenesis and its consequences on inbreeding in an ant. - Heredity 96: 377-382 Go to original source...
  47. RABELING R. & KRONAUER D.J.C. 2013: Thelytokous parthenogenesis in eusocial Hymenoptera. - Annu. Rev. Entomol. 58: 273-292 Go to original source...
  48. RABELING C., GONZALES O., SCHULTZ T., BACCI M., GARCIA M.V.B., VERHAAGH M., ISHAK H.D. & MUELLER U.G. 2011: Cryptic sexual populations account for genetic diversity and ecological success in a widely distributed, asexual fungusgrowing ant. - Proc. Nat. Acad. Sci. 108: 12366-12371 Go to original source...
  49. REUTER M., PEDERSEN J.S. & KELLER L. 2004: Loss of Wolbachia infection during colonisation in the invasive Argentine ant Linepithema humile. - Heredity 94: 364-369 Go to original source...
  50. REY O., LOISEAU A., FACON B., FOUCAUD F., ORIVEL J., CORNUET J., ROBERT S., DOBIGNY G., DELABIE J.H.C., FERRERIA MARIANO C.S. & ESTOUP A. 2011: Meiotic recombination dramatically decreased in thelytokous queens of the little fire ant and their sexually produced workers. - Mol. Biol. Evol. 28: 2591-2601 Go to original source...
  51. RUSSELL J.A., MOREAU C.S., GOLDMAN-HUERTAS B., FUJIWARA M., LOHMAN D.J. & PIERCE N.E. 2009: Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. - Proc. Nat. Acad. Sci. U.S.A. 106: 21236-21241 Go to original source...
  52. SCHILDER K., HEINZE J. & HOLLDOBLER B. 1999: Colony structure and reproduction in the thelytokous parthenogenetic ant Platythyrea punctata (F. Smith) (Hymenoptera: Formicidae). - Insectes Soc. 46: 150-158 Go to original source...
  53. SCHLICK-STEINER B.C., STEINER F.M., KONRAD H. & MARKO B. 2006: More than one species of Messor harvester ants (Hymenoptera: Formicidae) in Central Europe. - Eur. J. Entomol. 103: 469-476 Go to original source...
  54. SERBUS L.R., CASPER-LINDLEY C., LANDMANN F. & SULLIVAN W. 2008: The genetics and cell biology of Wolbachia-host interactions. - Annu. Rev. Genet. 42: 683-707 Go to original source...
  55. SHOEMAKER D., ROSS K., KELLER L., VARGO E. & WERREN J. 2000: Wolbachia infections in native and introduced populations of fire ants (Solenopsis spp.). - Insect Mol. Biol. 9: 661-673 Go to original source...
  56. SIMOES P.M., MIALDEA G., REISS D., SAGOT M.F. & CHARLAT S. 2011: Wolbachia detection: an assessment of standard PCR Protocols. - Mol. Ecol. Res. 11: 567-572 Go to original source...
  57. SIMON J.C., DELMOTTE F., RISPE C. & CREASE T. 2003: Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. - Biol. J. Linn. Soc. 79: 151-163 Go to original source...
  58. SIRVIO A. & PAMILO P. 2010: Multiple endosymbionts in populations of the ant Formica cinerea. - BMC Evol. Biol. 10: 335-347 Go to original source...
  59. STOUTHAMER R. 1997: Wolbachia-induced parthenogenesis. In O'Neill S.L., Hoffmann A.A. & Werren J.H. (eds): Influential Passengers: Inherited Microorganisms and Arthropod Reproduction. Oxford University Press, Oxford, pp. 102-122
  60. STOUTHAMER R. & KAZMER D. 1994: Cytogenetics of microbeassociated parthenogenesis and its consequences for gene flow in Trichogramma wasps. - Heredity 73: 317-327 Go to original source...
  61. TSUJI K. 1988: Obligate parthenogenesis and reproductive division of labor in the Japanese queenless ant Pristomyrmex pungens: Comparison of intranidal and extranidal workers. - Behav. Ecol. Sociobiol. 23: 247-255 Go to original source...
  62. VAN BORM S., WENSELEERS T., BILLEN J. & BOOMSMA J.J. 2001: Wolbachia in leafcutter ants: a widespread symbiont that may induce male killing or incompatible matings. - J. Evol. Biol. 14: 805-814 Go to original source...
  63. VAVRE F., DE JONG J.H. & STOUTHAMER R. 2004: Cytogenetic mechanism and genetic consequences of thelytoky in the wasp Trichogramma cacoeciae. - Heredity 93: 592-596 Go to original source...
  64. WEEKS A.R. & BREEUWER J.A.J. 2001: Wolbachia-induced parthenogenesis in a genus of phytophagous mites. - Proc. R. Soc. Lond. (B) 268: 2245-2251 Go to original source...
  65. WEISBURG W., BARNS S., PELLETIER D. & LANE D. 1991: 16S ribosomal DNA amplification for phylogenetic study. - J. Bacteriol. 173: 697-703 Go to original source...
  66. WENSELEERS T. & BILLEN J. 2000: No evidence for Wolbachiainduced parthenogenesis in the social Hymenoptera. - J. Evol. Biol. 13: 277-280 Go to original source...
  67. WENSELEERS T., ITO F., VAN BORM S., HUYBRECHTS R., VOLCKAERT F. & BILLEN J. 1998: Widespread occurrence of the micro-organism Wolbachia in ants. -Proc. R. Soc. Lond. (B) 265: 1447-1452 Go to original source...
  68. WERREN J.H. 1997: Biology of Wolbachia. - Annu. Rev. Entomol. 42: 587-609 Go to original source...
  69. WERREN J.H., ZHANG W. & GUO L.R. 1995: Evolution and phylogeny of Wolbachia - reproductive parasites of arthropods. - Proc. R. Soc. Lond (B) 261: 55-63 Go to original source...
  70. WERREN J.H., BALDO L. & CLARK M.E. 2008: Wolbachia: master manipulators of invertebrate biology. - Nat. Rev. Microbiol. 6: 741-751 Go to original source...
  71. WHITE M.J.D. 1984: Chromosomal mechanisms in animal reproduction. Boll. Zool. 51: 1-23 Go to original source...
  72. WHITING A.R. 1961: Genetics of Habrobracon. - Adv. Genet. 10: 295-348 Go to original source...
  73. WILLIAMS G. 1975: Sex and Evolution. Princeton University Press, Princeton, 210 pp
  74. ZABAL-AGUIRRE M., ARROYO F. & BELLA J.L. 2010: Distribution of Wolbachia infection in Chorthippus parallelus populations within and beyond a Pyrenean hybrid zone. - Heredity 104: 174-184 Go to original source...
  75. ZCHORI-FEIN E. & PERLMAN S.J. 2004: Distribution of the bacterial symbiont Cardinium in arthropods. - Mol. Ecol. 13: 2009-2016 Go to original source...
  76. ZHANG X., NORRIS D.E. & RASGON J.L. 2011: Distribution and molecular characterization of Wolbachia endosymbionts and filarial nematodes in Maryland populations of the lone star tick (Amblyomma americanum). - FEMS Microbiol. Ecol. 77: 50-56 Go to original source...