Wolbachia – Επαγόμενος αναπαραγωγικός παρασιτισμός και εφαρμογές


Δημοσιευμένα: Ιαν 8, 2009
A. Saridaki
K. Bourtzis
Περίληψη
Οι συμβιωτικές σχέσεις εντόμων-μικροοργανισμών (και ιδιαίτερα βακτηρίων) είναι ένα ευρέως διαδεδομένο φαινόμενο με ποικίλες συνέπειες στη βιολογία του ξενιστή, θετικές ή αρνητικές. Ένα από τα πιο διαδεδομένα και καλά μελετημένα βακτήρια είναι το βακτήριο Wolbachia. Το βακτήριο Wolbachia είναι ένα υποχρεωτικά ενδοκυττάριο και μητρικά κληρονομούμενο βακτήριο που συμβιώνει με ένα μεγάλο εύρος ειδών ασπόνδυλων όπως ακάρεα, αράχνες, ισόποδα, νηματώδεις της φιλαρίασης και κυρίως έντομα. Μελέτες έχουν δείξει ότι το βακτήριο Wolbachia πιθανώς συμβιώνει με το 70% όλων των ειδών των εντόμων, καθιστώντας το ως τον πιο διαδεδομένο συμβιωτικό οργανισμό του πλανήτη. Οι αλληλεπιδράσεις του βακτηρίου με τον ξενιστή κυμαίνονται μεταξύ της αμοιβαίας συμβίωσης και της επαγωγής αναπαραγωγικών ανωμαλιών όπως θηλυκοποίηση, παρθενογένεση, θανάτωση των αρσενικών ατόμων ή κυτταροπλασματική ασυμβατότητα. Παρά την ευρεία εξάπλωση και τις επιδράσεις του βακτηρίου στη βιολογία του ξενιστή, στην ειδογένεση και στην οικολογική ποικιλότητα, λίγα είναι γνωστά για τους μοριακούς μηχανισμούς της αλληλεπίδρασης του ξενιστή με το συμβιωτικό αυτό βακτήριο. Πρόσφατες μελέτες εστιάζουν στη δυνατότητα ανάπτυξης μεθόδων βιολογικού ελέγχου εντόμων γεωργικής, περιβαλλοντικής ή ιατρικής σημασίας, οι οποίες βασίζονται στις ιδιότητες του βακτηρίου Wolbachia.
Λεπτομέρειες άρθρου
  • Ενότητα
  • Articles
Λήψεις
Τα δεδομένα λήψης δεν είναι ακόμη διαθέσιμα.
Αναφορές
Aksoy, S., I. Maudlin, C. Dale, A.S. Robinson and S.L. O'Neill. 2001. Prospects for control of African trypanosomiasis by tsetse vector manipulation. Trends Parasitol. 17: 29- 35.
Arakaki, N., T. Miyoshi and H. Noda. 2001. Wolbachia-mediated parthenogenesis in the predatory thrips Franklinothrips vespiformis (Thysanoptera: Insecta). Proc. R. Soc. Lond. B. Biol. Sci. 268: 1011-1016.
Azzouna, A., P. Greve and G. Martin. 2004. Sexual differentiation traits in functional males with female genital apertures (male symbol fga) in the woodlice Armadillidium vulgare Latr. (Isopoda, Crustacea). Gen. Comp. Endocrinol. 138: 42-49.
Baldo, L., J.C. Dunning Hotopp, K.A. Jolley, S.R. Bordenstein, S.A. Biber, R.R. Choudhury, C. Hayashi, M.C. Maiden, H. Tettelin and J.H. Werren. 2006. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl. Environ. Microbiol. 72: 7098-7110.
Bandi, C., T.J.C. Anderson, C. Genchi and M.L. Blaxter. 1998. Phylogeny of Wolbachia in filarial nematodes. Proc. R. Soc. Lond. B. Biol. Sci. 265: 2407- 2413.
Bandi, C., A.M. Dunn, G.D. Hurst and T. Rigaud. 2001. Inherited microorganisms, sex-specific virulence and reproductive parasitism. Trends Parasitol. 17: 88-94.
Beard, C.B., S.L. O'Neill, R.B. Tesh, F.F. Richards and S. Aksoy. 1993. Modification of arthropod vector competence via symbiotic bacteria. Parasitol. Today 9: 179-183.
Bordenstein, S.R. 2003. Symbiosis and the origin of species. In: Insect symbiosis, vol. 1; eds. K. Bourtzis and T.A. Miller. CRC Press, pp. 283-304.
Bordenstein, S. and R.B. Rosengaus. 2005. Discovery of a novel Wolbachia super group in Isoptera. Curr. Microbiol. 51(6): 393-398.
Bordenstein, S.R., C. Paraskevopoulos, J.C. Hotopp, P. Sapountzis, N. Lo, C. Bandi, H. Tettelin, J.H. Werren and K. Bourtzis. 2009.
Parasitism and mutualism in Wolbachia: what the phylogenomic trees can and cannot say. Mol. Biol. Evol. 26: 231-241.
Bouchon, D., T. Rigaud and P. Juchault. 1998. Evidence for widespread Wolbachia infection in isopod crustaceans: molecular identification and host feminization. Proc. Biol. Sci. 265: 1081-1090.
Bourtzis, K. and S.L. O’Neill. 1998. Wolbachia infections and arthropod reproduction – Wolbachia can cause cytoplasmic incompatibility, parthenogenesis and feminization in many arthropods. Bioscience. 48: 287- 293.
Bourtzis, K., S.L. Dobson, H.R. Braig and S.L. O'Neill. 1998. Rescuing Wolbachia have been overlooked. Nature. 391: 852- 853.
Bourtzis, K. and H.R. Braig. 1999. The many faces of Wolbachia. In: Rickettsiae and rickettsial diseases at the turn of the third millenium; eds. D. Raoult and P. Brouqui. Elsevier, Paris. pp.199-219.
Bourtzis, K., M.M. Pettigrew and S.L. O'Neill. 2000. Wolbachia neither induces nor suppresses transcripts encoding antimicrobial peptides. Insect Mol. Biol. 9: 635-639.
Bourtzis, K., H.R. Braig and T.L. Karr. 2003. Cytoplasmic incompatibility. In: Insect symbiosis, vol. 1; eds. K. Bourtzis and T.A. Miller. CRC Press, pp. 217-246.
Bourtzis, K. and A.S. Robinson. 2006. Insect pest control using Wolbachia and/or radiation. In: Insect Symbiosis, vol. 2; eds. K. Bourtzis and T.A. Miller. CRC Press, pp. 225-246.
Bourtzis, K. 2008. Wolbachia-based technologies for insect pest population control. Adv. Exp. Med. Biol. 627: 104- 113.
Boyle, L., S.L. O'Neill, H.M. Robertson and T.L. Karr. 1993. Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260: 1796-1799.
Braig, H.R., H. Guzman, R.B. Tesh and S.L. O'Neill. 1994. Replacement of the natural Wolbachia symbiont of Drosophila simulans with a mosquito counterpart. Nature 367: 453-455.
Breeuwer, J.A. and J.H. Werren. 1990. Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346: 558-560.
Breeuwer, J.A., R. Stouthamer, S.M. Barns, D.A. Pelletier, W.G. Weisburg and J.H. Werren. 1992. Phylogeny of cytoplasmic incompatibility microorganisms in the parasitoid wasp genus Nasonia (Hymenoptera: Pteromalidae) based on 16S ribosomal DNA sequences. Insect Mol. Biol. 1: 25-36.
Breeuwer, J.A. and G. Jacobs. 1996. Wolbachia: intracellular manipulators of mite reproduction. Exp. Appl. Acarol. 20: 421-434.
Brower, J.H. 1976. Cytoplasmic incompatibility: occurrence in a storedproduct pest Ephestia cautella. Ann. Entomol. Soc. Am. 69: 1011-1015.
Buchner, P. 1965. Endosymbiosis of animals with plant microorganisms. Interscience Publishers. New York. 909 pp.
Cook, P.E., C.J. McMeniman and S.L. O'Neill. 2008. Modifying insect population age structure to control vector-borne disease. Adv. Exp. Med. Biol. 627: 126-140.
Curtis, C.F. and S.P. Sinkins. 1998. Wolbachia as a possible means of driving genes into populations. Parasitology 116: S111–S115.
Dobson, S.L., E.J. Marsland and W. Rattanadechakul. 2002. Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160: 1087-1094.
Dobson, S.L. 2003. Reversing Wolbachiabased population replacement. Trends Parasitol. 19: 128-133.
Dyer, K.A. and J. Jaenike. 2004. Evolutionarily stable infection by a male-killing endosymbiont in Drosophila innubila: molecular evidence from the host and parasite genomes. Genetics 168: 1443-1455.
Fialho, R.F. and L. Stevens. 2000. Malekilling Wolbachia in a flour beetle. Proc. Biol. Sci. 267: 1469-1473.
Foster, J., M. Ganatra, I. Kamal, J. Ware, K. Makarova, N. Ivanova, A. Bhattacharyya, V. Kapatral, S. Kumar, J. Posfai, T. Vincze, J. Ingram, L. Moran, A. Lapidus, M. Omelchenko, N. Kyrpides, E. Ghedin, S. Wang, E. Goltsman, V. Joukov, O. Ostrovskaya, K. Tsukerman, M. Mazur, D. Comb, E. Koonin and B. Slatko. 2005. The Wolbachia genome of Brugia malayi: endosymbiont evolution within a human pathogenic nematode. PLoS Biol. 3: e121.
Fytrou, A., P.G. Schofield, A.R. Kraaijeveld and S.F. Hubbard. 2006. Wolbachia infection suppresses both host defence and parasitoid counter-defence. Proc. Biol. Sci. 273: 791-796.
Hedges, L.M., J.C. Brownlie, S.L. O'Neill and K.N. Johnson. 2008. Wolbachia and virus protection in insects. Science 322: 702.
Hertig, M. and S.B. Wolbach. 1924. Studies on rickettsia-like micro-organisms in insects. J. Med. Res. 44: 329-374.
Hertig, M. 1936. The rickettsia, Wolbachia pipientis (Gen. et Sp. Nov.) and associated inclusions of the mosquito, Culex pipiens. Parasitology 28: 453- 486.
Hilgenboecker, K., P. Hammerstein, P. Schlattmann, A. Telschow and J.H. Werren. 2008. How many species are infected with Wolbachia?--A statistical analysis of current data. FEMS Microbiol. Lett. 281: 215-220.
Hoshizaki, S. and T. Shimada. 1995. PCRbased detection of Wolbachia, cytoplasmic incompatibility microorganisms, infected in natural populations of Laodelphax striatellus (Homoptera: Delphacidae) in central Japan: has the distribution of Wolbachia spread recently? Insect Mol. Biol. 4: 237-243.
Hurst, G.D. 1991. The incidences and evolution of cytoplasmic male killers. Proc. R. Soc. Lond. B. 244: 91-99.
Hurst, G.D., A.P. Johnson, J.H. Schulenburg and Y. Fuyama. 2000. Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics 156: 699-709.
Hurst, G.D., F.M. Jiggins and M.E.N. Majerus. 2003. Inherited microorganisms that selectively kill male hosts: the hidden players of insect evolution? In: Insect symbiosis, vol. 1; eds. K. Bourtzis and T.A. Miller. CRC Press, pp. 177-197.
Ishikawa, H. 1989. Biochemical and molecular aspects of endosymbiosis in insects. Int. Rev. Cytol. 116: 1-45.
Ishikawa, H. 2003. Insect symbiosis: an introduction. In: Insect symbiosis, vol. 1; eds. K. Bourtzis and T.A. Miller. CRC Press, pp. 1-21.
Jayaprakash, A. and M.A. Hoy. 2000. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty three arthropod species. Insect Mol. Biol. 9: 393-405.
Jiggins, F.M., G.D. Hurst and M.E. Majerus. 2000. Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proc. Biol. Sci. 267: 69-73.
Kamoda, S., S. Masui, H. Ishikawa and T. Sasaki. 2000. Wolbachia infection and cytoplasmic incompatibility in the cricket Teleogryllus taiwanemma. J. Exp. Biol. 203(Pt 16): 2503-2509.
Klasson, L., T. Walker, M. Sebaihia, M.J. Sanders, M.A. Quail, A. Lord, S. Sanders, J. Earl, S.L. O'Neill, N. Thomson, S.P. Sinkins and J. Parkhill. 2008. Genome evolution of Wolbachia strain wPip from the Culex pipiens group. Mol. Biol. Evol. 25: 1877-1887.
Klasson, L., J. Westberg, P. Sapountzis, K. Näslund, Y. Lutnaes, A.C. Darby, Z. Veneti, L. Chen, H.R. Braig, R. Garrett, K. Bourtzis and S.G. Andersson. 2009. The mosaic genome structure of the Wolbachia wRi strain infecting Drosophila simulans. Proc. Natl. Acad. Sci. U.S.A. 106: 5725-5730.
Landmann, F., G.A. Orsi, B. Loppin and W. Sullivan. 2009. Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. PLoS Pathog. 5: e1000343.
Lassy, C.W. and T.L. Karr. 1996. Cytological analysis of fertilization and early embryonic development in incompatible crosses of Drosophila simulans. Mech. Dev. 57: 47-58.
Lo, N., M. Casiraghi, E. Salati, C. Bazzocchi and C. Bandi. 2002. How many Wolbachia supergroups exist? Mol. Biol. Evol. 19: 341-346.
Lo, N., C. Paraskevopoulos, K. Bourtzis, S.L. O’Neill, J.H. Werren, S.R. Bordenstein and C. Bandi. 2007. Taxonomic status of the intracellular bacterium Wolbachia pipientis. Int. J. Syst. Evol. Micr. 57: 654-657.
Majerus, M.E., J. Hinrich, G.V. Schulenburg and I.A. Zakharov. 2000. Multiple causes of male-killing in a single sample of the two-spot ladybird, Adalia bipunctata (Coleoptera: coccinellidae) from Moscow. Heredity 84: 605-609.
McGraw, E.A., D.J. Merritt, J.N. Droller and S.L. O'Neill. 2001. Wolbachiamediated sperm modification is dependent on the host genotype in Drosophila. Proc. Biol. Sci. 268: 2565- 2570.
McGraw, E.A., D.J. Merritt, J.N. Droller and S.L. O'Neill. 2002. Wolbachia density and virulence attenuation after transfer into a novel host. Proc. Natl. Acad. Sci. U.S.A. 99: 2918-2923.
McMeniman, C.J., R.V. Lane, B.N. Cass, A.W. Fong, M. Sidhu, Y.F. Wang and S.L. O'Neill. 2009. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323: 141-144.
Merçot H. and D. Poinsot. 1998. Rescuing Wolbachia have been overlooked and discovered on Mount Kilimanjaro. Nature 391: 853.
Michel-Salzat, A., R. Cordaux and D. Bouchon. 2001. Wolbachia diversity in the Porcellionides pruinosus complex of species (Crustacea: Oniscidea): evidence for host-dependent patterns of infection. Heredity 87: 428-434.
Min, K.T. and S. Benzer. 1997. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Natl. Acad. Sci. U.S.A. 94: 10792-10796.
Moreau, J., A. Bertin, Y. Caubet and T. Rigaud. 2001. Sexual selection in an isopod with Wolbachia-induced sex reversal: males prefer real females. J. Evol. Biol. 14: 388-394.
Moreau, J. and T. Rigaud. 2003. Variable male potential rate of reproduction: high male mating capacity as an adaptation to parasite-induced excess of females? Proc. R. Soc. Lond. B. Biol. Sci. 270: 1535-1540.
Moret, Y., P. Juchault and T. Rigaud. 2001. Wolbachia endosymbiont responsible for cytoplasmic incompatibility in a terrestrial crustacean: effects in natural and foreign hosts. Heredity 86(Pt 3): 325-332.
Narita, S., D. Kageyama, M. Nomura and T. Fukatsu. 2007. Unexpected mechanism of symbiont-induced reversal of insect sex: feminizing Wolbachia continuously acts on the butterfly Eurema hecabe during larval development. Appl. Environ. Microbiol. 73: 4332-4341.
Negri, I., M. Pellecchia, P.J. Mazzoglio, A. Patetta and A. Alma. 2006. Feminizing Wolbachia in Zyginidia pullula (Insecta, Hemiptera), a leafhopper with an XX/XO sex-determination system. Proc. R. Soc. Lond. B. Biol. Sci. 273: 2409- 2416.
O'Neill, S.L. and T.L. Karr. 1990. Bidirectional incompatibility between conspecific populations of Drosophila simulans. Nature 348: 178-180.
O'Neill, S.L., R. Giordano, A.M. Colbert, T.L. Karr and H.M. Robertson. 1992. 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc. Natl. Acad. Sci. U.S.A. 89: 2699- 2702.
Paraskevopoulos, C., S.R. Bordenstein, J.J. Wernegreen, J.H. Werren and K. Bourtzis. 2006. Toward a Wolbachia multilocus sequence typing system: discrimination of Wolbachia strains present in Drosophila species. Curr. Microbiol. 53: 388-395.
Poinsot, D., K. Bourtzis, G. Markakis, C. Savakis and H. Merçot. 1998. Wolbachia transfer from Drosophila melanogaster into D. simulans: Host effect and cytoplasmic incompatibility relationships. Genetics 150: 227-237.
Reed, K.M. and J.H. Werren. 1995. Induction of paternal genome loss by the paternal-sex-ratio chromosome and cytoplasmic incompatibility bacteria (Wolbachia): a comparative study of early embryonic events. Mol. Reprod. Dev. 40: 408-418.
Rigaud, T., J. Moreau and P. Juchault. 1999a. Wolbachia infection in the terrestrial isopod Oniscus asellus: sex ratio distortion and effect on fecundity. Heredity 83: 469-475.
Rigaud, T., D. Bouchon, C. Souty-Grosset and R. Raimond. 1999b. Mitochondrial DNA polymorphism, sex ratio distorters and population genetics in the isopod Armadillidium vulgare. Genetics 152: 1669-1677.
Ros, V.I., V.M. Fleming, E.J. Feil and J.A. Breeuwer. 2008. How diverse is the genus Wolbachia? Multiple-gene sequencing reveals a putatively new Wolbachia supergroup recovered from spider mites (Acari: Tetranychidae). Appl. Environ. Microbiol. 75: 1036- 1043.
Rousset, F., D. Vautrin and M. Solignac. 1992. Molecular identification of Wolbachia, the agent of cytoplasmic incompatibility in Drosophila simulans, and variability in relation with host mitochondrial types. Proc. Biol. Sci. 247: 163-168.
Rowley, S.M., R.J. Raven and E.A. McGraw. 2004. Wolbachia pipientis in Australian spiders. Curr. Microbiol. 49: 208-214.
Sasaki, T. and H. Ishikawa. 2000. Transinfection of Wolbachia in the mediterranean flour moth, Ephestia kuehniella, by embryonic microinjection. Heredity 85 (Pt 2): 130-135.
Sinkins, S.P., C.F. Curtis and S.L. O’Neill. 1997. In: Influential passengers: inherited microorganisms and arthropod reproduction; eds. S.L. O’Neill, A.A. Hoffmann and J.H. Werren. Oxford Univ. Press, New York. pp. 155–175.
Sinkins, S.P. and S.L. O’Neill. 2000. Wolbachia as a vehicle to modify insect populations. In: Insect transgenesis. Methods and applications; eds. A.M. Handler and A.A. James. CRC Press. pp. 271-287.
Stouthamer, R., J.A. Breeuwert, R.F. Luck and J.H. Werren. 1993. Molecular identification of microorganisms associated with parthenogenesis. Nature 361: 66-68.
Stouthamer, R., J.A. Breeuwer and G.D. Hurst. 1999. Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu. Rev. Microbiol. 53: 71-102.
Teixeira, L., A. Ferreira and M. Ashburner. 2008. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol. 6: e2.
Telschow, A., P. Hammerstein and J.H. Werren. 2005. The effect of Wolbachia versus genetic incompatibilities on reinforcement and speciation. Evolution 59: 1607-1619.
Tram, U. and W. Sullivan. 2002. Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 296: 1124-1126.
Turelli, M. and A.A. Hoffmann. 1999. Microbe-induced cytoplasmic incompatibility as a mechanism for introducing transgenes into arthropod populations. Insect Mol. Biol. 8: 243– 255.
Wade, M.J. and L. Stevens. 1985. Microorganism mediated reproductive isolation in flour beetles (genus Tribolium). Science 227: 527-528.
Weeks, A.R. and J.A. Breeuwer. 2001. Wolbachia-induced parthenogenesis in a genus of phytophagous mites. Proc. R. Soc. Lond. B. Biol. Sci. 268: 2245- 2251.
Weeks, A.R., M. Turelli, W.R. Harcombe, K.T. Reynolds and A.A. Hoffmann. 2007. From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila. PLoS Biol. 5: e114.
Werren, J.H. 1987. The coevolution of autosomal and cytoplasmic sex ratio factors. J. Theor. Biol. 124: 317-334.
Werren, J.H., D.M. Windsor and L. Guo. 1995. Distribution of Wolbachia among neotropical arthropods. Proc. R. Soc. Lond. B. Biol. Sci. 262: 197-204.
Werren, J.H. 1997. Biology of Wolbachia. Annu. Rev. Entomol. 42: 587-609.
Werren, J.H. 1998. Wolbachia and speciation. In: Endless forms: species and speciation, eds. D.J. Howard and S.H. Berlocher. Oxford University Press, New York. pp.245-260.
Werren, J.H. and D.M. Windsor. 2000. Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc. R. Soc. Lond. B. Biol. Sci. 267: 1277-1285.
Werren, J.H., L. Baldo and M.E. Clark. 2008. Wolbachia: master manipulators of invertebrate biology. Nat. Rev. Microbiol. 6: 741-751.
Wu, M., L.V. Sun, J. Vamathevan, M. Riegler, R. Deboy, J.C. Brownlie, E.A. McGraw, W. Martin, C. Esser, N. Ahmadinejad, C. Wiegand, R. Madupu, M.J. Beanan, L.M. Brinkac, S.C. Daugherty, A.S. Durkin, J.F. Kolonay, W.C. Nelson, Y. Mohamoud, P. Lee, K. Berry, M.B. Young, T. Utterback, J. Weidman, W.C. Nierman, I.T. Paulsen, K.E. Nelson, H. Tettelin, S.L. O'Neill and J.A. Eisen. 2004. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol. 2: 327-341.
Xi, Z., C.C.H. Khoo and S.L. Dobson. 2005. Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310: 326-328.
Yen, J.H. and A.R. Barr. 1973. The etiological agent of cytoplasmic incompatibility in Culex pipiens. J. Invertebr. Pathol. 22: 242-250.
Zabalou, S., M. Riegler, M. Theodorakopoulou, C. Stauffer, C. Savakis and K. Bourtzis. 2004a. Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proc. Natl. Acad. Sci. U.S.A. 101: 15042-15045.
Zabalou, S., S. Charlat, A. Nirgianaki, D. Lachaise, H. Merçot and K. Bourtzis. 2004b. Natural Wolbachia infections in the Drosophila yakuba species complex do not induce cytoplasmic incompatibility but fully rescue the wRi modification. Genetics 167: 827-834.
Zabalou, S. A. Apostolaki, I. Livadaras, G. Franz, A. S. Robinson, C. Savakis and K. Bourtzis. 2009. Incompatible Insect Technique: incompatible males from a Ceratitis capitata (Diptera: Tephritidae) genetic sexing strain. Entomol. Exp. Appl. 132: 232-240.
Zchori-Fein, E., O. Faktor, M. Zeidan, Y. Gottlieb, H. Czosnek and D. Rosen. 1995. Parthenogenesis-inducing microorganisms in Aphytis (Hymenoptera: Aphelinidae). Insect Mol. Biol. 4: 173-178.
Zeh, D.W., J.A. Zeh and M.M. Bonilla. 2005. Wolbachia, sex ratio bias and apparent male killing in the harlequin beetle riding pseudoscorpion. Heredity 95: 41-49.
Zhou, W. F. Rousset and S. O'Neill. 1998. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc. Biol. Sci. 265: 509- 515.