Eur. J. Entomol. 111 (1): 91-104, 2014 | DOI: 10.14411/eje.2014.011

Endosymbiotic microorganisms of aphids (Hemiptera: Sternorrhyncha: Aphidoidea): Ultrastructure, distribution and transovarial transmission

Anna MICHALIK1, Teresa SZKLARZEWICZ1, Władysława JANKOWSKA1, Karina WIECZOREK2
1 Department of Developmental Biology and Morphology of Invertebrates, Institute of Zoology, Jagiellonian University, Gronostajowa 9, 30-387 Kraków, Poland; e-mails: a.michalik@uj.edu.pl; teresa.szklarzewicz@uj.edu.pl; ada.jankowska@uj.edu.pl
2 Department of Zoology, Faculty of Biology and Environmental Protection, University of Silesia, Bankowa 9, 40-007 Katowice, Poland; e-mail: karina.wieczorek@us.edu.pl

Aphidoidea, endosymbiotic bacteria, bacteriocytes, transovarial transmission of endosymbiotic bacteria The ultrastructure, distribution and transovarial transmission of endosymbiotic bacteria in representatives of six aphid families: Eriosomatidae (Pemphigus spyrothecae, Prociphilus fraxini), Anoeciidae [Anoecia (Anoecia) corni], Drepanosiphidae [Mindarus abietinus, Sipha (Rungsia) maydis, Clethrobius comes, Myzocallis (Lineomyzocallis) walshii], Thelaxidae (Thelaxes dryophila), Aphididae (Delphiniobium junackianum, Aphis viburni, Cavariella theobaldi, Macrosiphoniella tanacetaria) and Lachnidae (Schizolachnus pineti, Eulachnus rileyi) were studied at the ultrastructural level. The ovaries of aphids are accompanied by large organs termed bacteriomes that consist of giant cells termed bacteriocytes. The bacteriocyte cytoplasm is tightly packed with endosymbiotic bacteria. Ultrastructural observations have shown that the bacteria Buchnera aphidicola (primary symbiont of aphids) present in various species are characterized by significant differences in both size and organization of their cytoplasm. In the aphids, Prociphilus fraxini, Sipha (Rungsia) maydis, Thelaxes dryophila, Aphis viburni, Cavariella theobaldi, Macrosiphoniella tanacetaria, Eulachnus rileyi and Schizolachnus pineti, in addition to Buchnera aphidicola, secondary endosymbionts are also present. The bacteriocytes containing secondary endosymbionts are less numerous than those with Buchnera. In Eulachnus rileyi (Lachnidae), in addition to primary and secondary endosymbionts, there is a third type of microorganism. In all species examined both the primary and secondary endosymbionts are transovarially transmitted from mother to offspring.

Keywords: Aphidoidea, endosymbiotic bacteria, bacteriocytes, transovarial transmission of endosymbiotic bacteria dryophila), Aphididae (Delphiniobium junackianum, Aphis viburni, Cavariella theobaldi, Macrosiphoniella tanacetaria) and aphids, Prociphilus fraxini, Sipha (Rungsia) maydis, Thelaxes dryophila, Aphis viburni, Cavariella theobaldi, Macrosiphoniella

Received: March 7, 2013; Revised: July 7, 2013; Accepted: July 7, 2013; Published: January 9, 2014  Show citation

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MICHALIK, A., SZKLARZEWICZ, T., JANKOWSKA, W., & WIECZOREK, K. (2014). Endosymbiotic microorganisms of aphids (Hemiptera: Sternorrhyncha: Aphidoidea): Ultrastructure, distribution and transovarial transmission. EJE, 111(1), 91-104. doi: 10.14411/eje.2014.011
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    References

    1. AKHTAR S. & VAN EMDEN H.F. 1994: Ultrastructure of the symbionts and mycetocytes of bird cherry aphid (Rhopalosiphum padi). - Tiss. Cell 26: 513-522 Go to original source...
    2. AUGUSTINOS A.A., SANTOS-GARCIA D., DIONYSSOPOULOU E., MOREIRA M., PAPANAGIOTOU A., SCARVELAKIS M., DOUDOUMIS V., RAMOS S., AGUIAR A.F., BORGES P.A.V., KHADEM M., LATORRE A., TSIAMIS G. & BOURTZIS K. 2011: Detection and characterization of Wolbachia infections in natural populations of aphids: is the hidden diversity fully unraveled? - PLoS One 6: e28695 Go to original source...
    3. BAUMANN P. 2005: Biology of bacteriocyte-associated endosymbionts of plant sup-sucking insects. - Annu. Rev. Microbiol. 59: 155-189 Go to original source...
    4. BAUMANN P. 2006: Diversity of prokaryote-insect associations within the Sternorrhyncha (psyllids, whiteflies, aphids, mealybugs). In Bourtzis K. & Miller T.A. (eds): Insect Symbiosis. Vol. 2. Contemporary Topics in Entomology Series. CRC Press, Boca Raton, FL, pp. 1-24 Go to original source...
    5. BAUMANN P., BAUMANN L., LAI C.Y., ROUHBAKKSH D., MORAN N.A. & CLARK M.A. 1995: Genetics, physiology, and evolutionary relationships of the genus Buchnera: intracellular symbionts of aphids. - Annu. Rev. Microbiol. 49: 55-94 Go to original source...
    6. BRAENDLE C., MIURA T., BICKEL R., SHINGLETON A.W., KAMBHAMPATI S. & STERN D.L. 2003: Developmental origin and evolution of bacteriocytes in the aphid - Buchnera symbiosis. - PLoS Biol. 1: 70-76 Go to original source...
    7. BROUGH C.N. & DIXON A.F.G. 1990: Ultrastructural features of egg development in oviparae of the vetch aphid, Megoura viciae Buckton. - Tiss. Cell 22: 51-63 Go to original source...
    8. BUCHNER P. 1965: Endosymbiosis of Animals with Plant Microorganisms. Interscience Publishers, New York, London, Sydney, 909 pp
    9. BUCHNER P. 1966: Endosymbiosestudien an Schildlaeusen. VIII. Die Symbiosen der Palaeococcoidea. 1. Teil. - Z. Morphol. Okol. Tiere 56: 275-362 Go to original source...
    10. BUCHNER P. 1967: Endosymbiosestudien an Schildlaeusen. VIII. Die Symbiosen der Palaeococcoidea. 2. Teil. - Z. Morphol. Okol. Tiere 59: 211-317 Go to original source...
    11. BUNING J. 1985: Morphology, ultrastructure and germ cell cluster formation in ovarioles of aphids. - J. Morphol. 186: 209-221 Go to original source...
    12. BURKE G.R., NORMARK B.B., FAVRET C. & MORAN N.A. 2009: Evolution and diversity of facultative symbionts from the aphid subfamily Lachninae. - Appl. Environ. Microbiol. 75: 5328-5335 Go to original source...
    13. CHARLES H. & ISHIKAWA H. 1999: Physical and genetic map of the genome of Buchnera, the primary endosymbiont of the pea aphid Acyrthosiphon pisum. - J. Mol. Evol. 48: 142-150 Go to original source...
    14. 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 Go to original source...
    15. CHEN D.Q. & PURCELL A.H. 1997: Occurrence and transmission of facultative endosymbionts in aphids. - Curr. Microbiol. 34: 220-225 Go to original source...
    16. CHENG D.J. & HOU R.F. 2001: Histological observations on transovarial transmission of a yeast-like symbiote in Nilaparvata lugens (Stal) (Homoptera, Delphacidae). - Tiss. Cell 33: 273-279 Go to original source...
    17. CLARK M.A., MORAN N.A., BAUMANN P. & WERNEGREEN J.J. 2000: Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. - Evolution 54: 517-525 Go to original source...
    18. DARBY A.C., BIRKLE L.M., TURNER S.L. & DOUGLAS A.E. 2001: An aphid-born bacterium allied to the secondary symbionts of whitefly. - FEMS Microbiol. Ecol. 36: 43-50 Go to original source...
    19. VON DOHLEN C.D., SPAULDING K.S., HAVILL N.P., ROSA C. & HOOVER K. 2013: Diversity of proteobacterial endosymbionts in hemlock woolly adelgid (Adelges tsugae) (Hemiptera: Adelgidae) from its native and introduced range. - Environ. Microbiol. 15: 2043-2062 Go to original source...
    20. DOUGLAS A.E. 1989: Mycetocyte symbiosis in insects. - Biol. Rev. 64: 409-434 Go to original source...
    21. 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...
    22. DOUGLAS A.E. 2003: Buchnera bacteria and other symbionts of aphids. In Bourtzis K. & Miller T.A. (eds): Insect Symbiosis. Vol. 1. Contemporary Topics in Entomology Series. CRC Press, Boca Raton, FL, pp. 23-38 Go to original source...
    23. DOUGLAS A.E. & PROSSER W.A. 1992: Synthesis of an essential amino acid tryptophan in the pea aphid (Acyrthosiphon pisum) symbiosis. - J. Insect Physiol. 38: 565-568 Go to original source...
    24. FUKATSU T. & HOSOKAWA T. 2002: Capsule-transmitted gut symbiotic bacterium of the Japanese common plataspid stinkbug, Megacopta punctatissima. - Appl. Environ. Microbiol. 68: 389-396 Go to original source...
    25. FUKATSU T., NIKOH N., KAWAI R. & KOGA R. 2000: The secondary endosymbiotic bacterium of the pea aphid, Acyrthosiphon pisum (Insecta: Homoptera). - Appl. Environ. Microbiol. 66: 2748-2758 Go to original source...
    26. 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 Go to original source...
    27. GOMEZ-VALERO L., SORIANO-NAVARRO M., PEREZ-BROCAL V., HEDDI A., MOYA A., GARCSSA-VERDUGO J.M. & LATORRE A. 2004: Coexistance of Wolbachia with Buchnera aphidicola and a secondary symbiont in the aphid Cinara cedri. - J. Bacteriol. 186: 6626-6633 Go to original source...
    28. GRIFFITHS G.W. & BECK S.D. 1975: Ultrastructure of pea aphid mycetocytes: evidence for symbiote secretion. - Cell Tiss. Res. 159: 351-367 Go to original source...
    29. VAN HAM R.C.H.J., KAMERBEEK J., PALACIOS C., RAUSELL C., ABASCAL F., BASTOLLA U., FERNANDEZ J.M., JIMENEZ L., POSTIGO M., SILVA F.J., TAMAMES J., VIGUERA E., LATORRE A., VALENCIA A., MORAN F. & MOYA A. 2003: Reductive genome evolution in Buchnera aphidicola. - PNAS 100: 581-586 Go to original source...
    30. HINDE R. 1971: The fine structure of the mycetome symbiotes of the aphids Brevicoryne brassicae, Myzus persicae and Macrosiphum rosae. - J. Insect Physiol. 17: 2035-2050 Go to original source...
    31. HOSOKAWA T., KIKUCHI Y., NIKOH N., MENG X.-Y., HIRONAKA M. & FUKATSU T. 2010: Phylogenetic position and peculiar genetic traits of a midgut bacterial symbiont of the stinkbug Parastrachia japonensis. - Appl. Environ. Microbiol. 76: 4130-4135 Go to original source...
    32. HOSOKAWA T., HIRONAKA M., INADOMI K., MUKAI H., NIKOH N. & FUKATSU T. 2013: Diverse strategies for vertical symbiont transmission among subsocial stinkbugs. - PLoS One 8: e65081 Go to original source...
    33. HYPSA V. & NOVAKOVA E. 2009: Insect symbiosis and molecular phylogenetics. In Bourtzis K. & Miller T.A. (eds): Insect Symbiosis. Vol. 3. Contemporary Topics in Entomology Series. CRC Press, Boca Raton, FL, pp. 1-31
    34. ISHIKAWA H. 2003: Insect symbiosis: An introduction. In Bourtzis K. & Miller T.A. (eds): Insect Symbiosis. Vol. 1. Contemporary Topics in Entomology Series. CRC Press, Boca Raton, FL, pp. 1-21 Go to original source...
    35. JOUSSELIN E., DESDEVISES Y. & D'ACIER A.C. 2009: Fine-scale cospeciation between Brachycaudus and Buchnera aphidicola: bacterial genome helps define species and evolutionary relationships in aphids. - Proc. Biol. Sci. 276: 187-196 Go to original source...
    36. KAIWA N., HOSOKAWA T., KIKUCHI Y., NIKOH N., MENG X.Y., KIMURA N., ITO M. & FUKATSU T. 2010: Primary gut symbiont and secondary, Sodalis-allied symbiont of the scutellerid stinkbug Cantao ocellatus. - Appl. Environ. Microbiol. 76: 3486-3494 Go to original source...
    37. KALTENPOTH M., WINTER S.A. & KLEINHAMMER A. 2009: Localization and transmission route of Coriobacterium glomerans, the endosymbiont of pyrrhocorid bugs. - FEMS Microbiol. Ecol. 69: 373-383 Go to original source...
    38. KIKUCHI Y. 2009: Endosymbiotic bacteria in insects: Their diversity and culturability. - Microbes Environ. 24: 195-204 Go to original source...
    39. KLEVENHUSEN F. 1927: Beitraege zur Kenntnis der Aphidensymbiose. - Z. Morphol. Okol. Tiere 41: 97-165 Go to original source...
    40. KOGA R., MENG X.-Y., TSUCHIDA T. & FUKATSU T. 2012: Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. - PNAS 109: E1230-E1237 Go to original source...
    41. 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. Biol. Sci. 270: 2543-2550 Go to original source...
    42. KOLB G. 1963: Die Endosymbiose der Thelaxiden unter besonderer Beruecksichtigung der Hormaphidinen und ihrer Embryonalentwicklung. - Z. Morphol. Okol. Tiere 53: 185-241 Go to original source...
    43. KUECHLER S.M., DETTNER K. & KEHL S. 2010: Molecular characterization and localization of the obligate endosymbiotic bacterium in the birch catkin bug Kleidocerys resedae (Heteroptera: Lygaeidae, Ischnorhynchinae). - FEMS Microbiol. Ecol. 73: 408-418 Go to original source...
    44. KUECHLER S.M., DETTNER K. & KEHL S. 2011: Characterization of an obligate intracellular bacterium in the midgut epithelium of the bulrush bug Chilacis typhae (Heteroptera, Lygaeidae, Artheneinae). - Appl. Environ. Microbiol. 77: 2869-2876 Go to original source...
    45. KUECHLER S.M., RENZ P., DETTNER K. & KEHL S. 2012: Diversity of symbiotic organs and bacterial endosymbionts of lygaeoid bugs of the families Blissidae and Lygaeidae (Hemiptera: Heteroptera: Lygaeoidea). - Appl. Environ. Microbiol. 78: 2648-2659 Go to original source...
    46. KUECHLER S.M., GIBBS G., BURCKHARDT D., DETTNER K. & HARTUNG V. 2013: Diversity of bacterial endosymbionts and bacteria-host co-evolution in Gondwanan relict moss bugs (Hemiptera: Coleorrhyncha: Peloridiidae). - Environ. Microbiol. 15: 2031-2042 Go to original source...
    47. LAI C.-Y., BAUMANN L. & BAUMAN P. 1994: Amplification of trpEG: Adaptation of Buchnera aphidicola to an endosymbiotic association with aphids. - Proc. Natl. Acad. Sci. USA 91: 3819-3823 Go to original source...
    48. LATORRE A. & MOYA A. 2006: Comparative genomics in Buchnera aphidicola, primary endosymbiont of aphids. In Bourtzis K. & Miller T.A. (eds): Insect Symbiosis. Vol. 2. Contemporary Topics in Entomology Series. CRC Press, Boca Raton, FL, pp. 157-174 Go to original source...
    49. LIU L., HUANG X.L., ZHANG R.L., JIANG L.Y. & QIAO G.X. 2013: Phylogenetic congruence between Mollitrichosiphum (Aphididae: Greenideinae) and Buchnera indicates insectbacteria parallel evolution. - Syst. Entomol. 38: 81-92 Go to original source...
    50. MARTINEZ-TORRES D., BUADES C., LATORRE A. & MOYA A. 2001: Molecular systematics of aphids and their primary endosymbionts. - Mol. Phylogenet. Evol. 20: 437-449 Go to original source...
    51. MATSUURA Y., KIKUCHI Y., HOSOKAWA T., RYUICHI K., MENG X.-Y., KAMAGATA. Y., NIKOH N. & FUKATSU T. 2012: Evolution of symbiotic organs and endosymbionts in lygaeid stinkbugs. - ISME J. 6: 397-409 Go to original source...
    52. MICHALIK A., SZKLARZEWICZ T., WEGIEREK P. & WIECZOREK K. 2013: The ovaries of aphids (Hemiptera, Sternorrhyncha, Aphidoidea): morphology and phylogenetic implications. - Inv. Biol. doi: 10.1111/ivb.12026 Go to original source...
    53. MIURA T., BRAENDLE C., SHINGLETON A., SISK G., KAMBHAMPATI S. & STERN D.L. 2003: A comparison of parthenogenetic and sexual embryogenesis of the pea aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). - J. Exp. Zool. (B) 295: 59-81 Go to original source...
    54. MONTLOR 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...
    55. MORAN N.A. & BAUMANN P. 1994: Phylogenetics of cytoplasmically inherited microorganisms of arthropods. - Trends Ecol. Evol. 9: 15-20 Go to original source...
    56. MORAN N.A. & BAUMANN P. 2000: Bacterial endosymbionts in animals. - Curr. Opin. Microbiol. 3: 270-275 Go to original source...
    57. MORAN N.A. & TELANG A. 1998: Bacteriocyte-associated symbionts of insects: a variety of insect groups harbor ancient prokaryotic endosymbionts. - BioScience 48: 295-304 Go to original source...
    58. 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. 1: 3302-3310 Go to original source...
    59. MORAN N.A., MCCUTCHEON J.P. & NAKABACHI A. 2008: Genomics and evolution of heritable bacterial symbionts. - Annu. Rev. Gen. 42: 165-190 Go to original source...
    60. MUNSON M.A., BAUMANN P. & KINSEY M.G. 1991: Buchnera gen. nov. and Buchnera aphidicola sp. nov. a taxon consisting of the mycetocyte-associated, primary endosymbionts of aphids. - Int. J. Syst. Bacteriol. 41: 566-568 Go to original source...
    61. NIZNIK S. & SZKLARZEWICZ T. 2007: Structure and development of hermaphroditic gonad in Icerya purchasi (Insecta, Hemiptera, Coccinea: Monophlebidae). - Zool. Polon. 52: 71-90
    62. NORMARK B.B. 2000: Molecular systematics and evolution of the aphid family Lachnidae. - Mol. Phylogenet. Evol. 14: 131-140 Go to original source...
    63. NOVAKOVA E., HYPSA V. & MORAN N.A. 2009: Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution. - BMC Microbiol. 9: 143 Go to original source...
    64. NOVAKOVA E., HYPSA V., KLEIN J., FOOTTIT R.G., VON DOHLEN C.D. & MORAN N.A. 2013: Reconstructing the phylogeny of aphids (Hemiptera: Aphididae) using DNA of the obligate symbiont Buchnera aphidicola. - Mol. Phylogenet. Evol. 68: 42-54 Go to original source...
    65. OLIVER K.M., RUSSEL 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...
    66. OLIVER K.M., MORAN N.A. & HUNTER M.S. 2006: Cost and benefits of a superinfection of facultative symbionts in aphids. - Proc. R. Soc. (B) 273: 1273-1280 Go to original source...
    67. 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...
    68. PEREZ-BROCAL V., LATORRE A., GIL R. & MOYA A. 2005: Comparative analysis of two genomic regions among four strains of Buchnera aphidicola, primary endosymbiont of aphids. - Gene 345: 73-80 Go to original source...
    69. PEREZ-BROCAL V., GIL R., RAMOS S., LAMELAS A., POSTIGO M., MICHELENA J.M., SILVA F.J., MOYA A. & LATORRE A. 2006: A small microbial genome: the end of a long symbiotic relationship? - Science 314: 312-313 Go to original source...
    70. PEREZ-BROCAL V., GIL R., MOYA A. & LATORRE A. 2011: New insights on the evolutionary history of aphids and their primary endosymbiont Buchnera aphidicola. - Int. J. Evol. Biol. doi: 10.4061/2011/250154 Go to original source...
    71. PRADO S.S., RUBINOFF D. & ALMEIDA R.P.P. 2006: Vertical transmission of a pentatomid caeca-associated symbiont. - Ann. Entomol. Soc. Am. 99: 577-585 Go to original source...
    72. PYKA-FOSCIAK G. 2006: Structure and Development of the Female Gonad in Oviparous and Viviparous Generations of aphid Stomaphis quercus (Hemiptera, Aphidinea: Lachnidae). Ph.D. Thesis, Jagiellonian University, 87 pp. [in Polish]
    73. PYKA-FOSCIAK G. & SZKLARZEWICZ T. 2008: Germ cell cluster formation and ovariole structure in viviparous and oviparous generation of the aphid Stomaphis quercus. - Int. J. Dev. Biol. 52: 259-265 Go to original source...
    74. SACCHI L., GENCHI M., CLEMENTI E., BIGLIARDI E., AVANZATTI A.M., PAJOROI M., NEGRI I., MARZORATI M., GONELLA E., ALMA A., DAFFONCHIO D. & BANDI C. 2008: Multiple symbiosis in the leafhopper Scaphoideus titanus (Hemiptera: Cicadellidae): Details of transovarial transmission of Cardinium sp. and yeast-like endosymbionts. - Tiss. Cell 40: 231-242 Go to original source...
    75. SANDSTROM 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...
    76. SASAKI T. & ISHIKAWA H. 1995: Production of essential amino acids from glutamate by mycetocyte symbiont of the pea aphid Acyrthosiphon pisum. - J. Insect Physiol. 41: 41-46 Go to original source...
    77. SCARBOROUGH C.L., FERRARI J. & GODFRAY H.C.J. 2005: Aphid protected from pathogen by endosymbiont. - Science 310: 1781 Go to original source...
    78. SHIGENOBU S., WATANABE H., HATTORI M., SAKAKI Y. & ISHIKAWA H. 2000: Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. - Nature 407: 81-86 Go to original source...
    79. SWIATONIOWSKA M., OGORZALEK A., GOLAS A., MICHALIK A. & SZKLARZEWICZ T. 2013: Ultrastructure, distribution and transovarial transmission of symbiotic microorganisms in Nysius ericae and Nithecus jacobaeae (Heteroptera: Lygaeidae: Orsillinae). - Protoplasma 250: 325-332 Go to original source...
    80. SZKLARZEWICZ T. & MOSKAL A. 2001: Ultrastructure, distribution, and transmission of endosymbionts in the whitefly Aleurochiton aceris Modeer (Insecta, Hemiptera, Aleyrodinea). - Protoplasma 218: 45-53 Go to original source...
    81. SZKLARZEWICZ T., WNEK A. & BILINSKI S.M. 2000: Structure of ovarioles in Adelges laricis, representative of the primitive aphid Adelgidae. - Acta Zool. (Stockholm) 81: 307-313 Go to original source...
    82. SZKLARZEWICZ T., KEDRA K. & NIZNIK S. 2006: Ultrastructure and transovarial transmission of endosymbiotic microorganisms in Palaeococcus fuscipennis (Burmeister) (Insecta, Hemiptera, Coccinea: Monophlebidae). - Folia Biol. (Krakow) 54: 70-74 Go to original source...
    83. SZKLARZEWICZ T., JANKOWSKA W., WIECZOREK K. & WEGIEREK P. 2009: Structure of the ovaries of the primitive aphids Phylloxera coccinea and Phylloxera glabra (Hemiptera, Aphidinea: Phylloxeridae). - Acta Zool. (Stockholm) 90: 123-131 Go to original source...
    84. SZKLARZEWICZ T., MICHALIK A., CZAJA A. & SZYDLOWSKA S. 2010: Germ cell cluster formation and ovariole structure in Puto albicans and Crypticerya morrilli (Hemiptera: Coccinea). Phylogenetic implications. - Eur. J. Entomol. 107: 589-595. Go to original source...
    85. SZKLARZEWICZ T., KALANDYK-KOLODZIEJCZYK M., KOT M. & MICHALIK A. 2013: Ovary structure and transovarial transmission of endosymbiotic microorganisms in Marchalina hellenica (Insecta, Hemiptera, Coccomorpha: Marchalinidae). - Acta Zool. (Stockholm) 94: 184-192 Go to original source...
    86. THAO M.L. & BAUMANN P. 2004: Evidence for multiple acquisition of Arsenophonus by whitefly species (Sternorrhyncha: Aleyrodidae). - Curr. Microbiol. 48: 140-144 Go to original source...
    87. TOENSHOFF E.R., PENZ T., NARZT T., COLLINGRO A., SCHMITZESSER S., PFEIFER S., KLEPAL W., WAGNER M., WIENMAIER T., RATTEI T. & HORN M. 2012a: Bacteriocyte-associated gammaproteobacterial symbionts of the Adelges nordmannianae/ piceae complex (Hemiptera: Adelgidae). - ISME J. 6: 384-396 Go to original source...
    88. TOENSHOFF E.R., GRUBER D. & HORN M. 2012b: Co-evolution and symbiont replacement shaped the symbiosis between adelgids (Hemiptera: Adelgidae) and their bacterial symbionts. - Environ. Microbiol. 14: 1284-1295 Go to original source...
    89. 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 Go to original source...
    90. TSUCHIDA T., KOGA R., MENG X.-Y., MATSUMOTO T. & FUKATSU T. 2005: Characterization of a facultative endosymbiotic bacterium of the pea aphid Acyrthosiphon pisum. - Microbiol. Ecol. 49: 126-133 Go to original source...
    91. UNTERMAN B.M., BAUMANN P. & MCLEAN D.L. 1989: Pea aphid symbiont relationships established by analysis of 16S rRNAs. - J. Bacteriol. 171: 2970-2974 Go to original source...
    92. 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...
    93. WANG Z., SHEN Z.-R., SONG Y., LIU H.-Y. & LI Z.-X. 2009: Distribution and diversity of Wolbachia in different populations of the wheat aphid Sitobion miscanti (Hemiptera: Aphididae) in China. - Eur. J. Entomol. 106: 49-55 Go to original source...
    94. WILKINSON T.L., FUKATSU T. & ISHIKAWA H. 2003: Transmission of symbiotic bacteria Buchnera to parthenogenetic embryos in the aphid Acyrthosiphon pisum (Hemiptera: Aphidoidea). - Arthr. Struct. Dev. 32: 241-245 Go to original source...

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