Skip to main content

Advertisement

SpringerLink
Log in

Loss of Wolbachia but not Cardinium in the invasive range of the Australian thrips species, Pezothrips kellyanus

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Many insects are associated with maternally inherited bacterial endosymbionts that manipulate host reproduction or impact other aspects of host fitness. Despite their ecological significance, the role of endosymbionts in biological invasions by their host insects is still poorly understood. In this study, we characterised the genetic diversity of the invasive Kelly’s citrus thrips, Pezothrips kellyanus (Thysanoptera: Thripidae), an important pest of citrus in Australasia and the Mediterranean region. We then surveyed native and invasive populations for the presence of the bacterial endosymbionts Cardinium and Wolbachia. Our analyses of mitochondrial and nuclear genes demonstrated that P. kellyanus originated from Australia. Furthermore, haplotype analysis revealed independent colonisation events for New Zealand and the Mediterranean region. Individuals from Australian populations had both endosymbionts at a high prevalence. In populations from New Zealand and the Mediterranean region, however, Cardinium was fixed and Wolbachia was absent. This may be due to a stochastic loss of Wolbachia prior to the establishment of invasive populations. Alternatively, Wolbachia may have been selected against by environmental factors or due to its potential role as a reproductive parasite that may constrain invasiveness of infected individuals. In contrast, Cardinium remained unaffected by the invasion process. Our study highlights that endosymbionts may be potential factors in the framework of the enemy release hypothesis that predicts success of invasive hosts in the absence of natural enemies. Therefore, the analysis of endosymbiont diversity of invasive insects may improve the understanding of host invasion biology and also deliver new diagnostic markers for biosecurity protocols.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Altizer S, Bartel R, Han BA (2011) Animal migration and infectious disease risk. Science 331:296–302. doi:10.1126/science.1194694

    Article  PubMed  CAS  Google Scholar 

  • Arakaki N, Miyoshi T, Noda H (2001) Wolbachia-mediated parthenogenesis in the predatory thrips Franklinothrips vespiformis (Thysanoptera: Insecta). Proc R Soc B 268:1011–1016. doi:10.1098/rspb.2001.1628

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bagnall R (1916) Brief descriptions of new Thysanoptera VII. Ann Mag Nat Hist 8:213–223

    Article  Google Scholar 

  • Baldo L, Hotopp JCD, 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. doi:10.1128/AEM.00731-06

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Belaam I, Boulahia-Kheder S (2012) Inventory of thrips species in citrus orchards and assessment of scarring fruits in two citrus-producing regions of Tunisia. Tunis J Plant Prot 7:45–53

    Google Scholar 

  • Bhatti J (1969) The taxonomic status of Megalurothrips Bagnall (Thysanoptera: Thripidae). Orient Insects 3:239–244. doi:10.1080/00305316.1969.10433912

    Article  Google Scholar 

  • Bing XL, Ruan YM, Rao Q, Wang XW, Liu SS (2013) Diversity of secondary endosymbionts among different putative species of the whitefly Bemisia tabaci. Insect Sci 20:194–206. doi:10.1111/j.1744-7917.2012.01522.x

    Article  PubMed  CAS  Google Scholar 

  • Blank R, Gill G (1997) Thrips (Thysanoptera: Terebrantia) on flowers and fruit of citrus in New Zealand. N Z J Crop Hortic 25:319–332. doi:10.1080/01140671.1997.9514023

    Article  Google Scholar 

  • Bournier J-P, Mound LA (2000) Inventaire commenté des Thysanoptères de Nouvelle-Calédonie. Bull Soc Entomol Fr 105:231–240

    Google Scholar 

  • Brown A, Huynh LY, Bolender CM, Nelson KG, McCutcheon JP (2014) Population genomics of a symbiont in the early stages of a pest invasion. Mol Ecol 23:1516–1530. doi:10.1111/mec.12366

    Article  PubMed  Google Scholar 

  • Buckman RS, Mound LA, Whiting MF (2012) Phylogeny of thrips (Insecta: Thysanoptera) based on five molecular loci. Syst Entomol 38:123–133. doi:10.1111/j.1365-3113.2012.00650.x

    Article  Google Scholar 

  • Buhay JE (2009) “COI-like” sequences are becoming problematic in molecular systematic and DNA barcoding studies. J Crust Biol 29:96–110. doi:10.1651/08-3020.1

    Article  Google Scholar 

  • Cass BN, Yallouz R, Bondy EC, Mozes-Daube N, Horowitz AR, Kelly SE, Zchori-Fein E, Hunter MS (2015) Dynamics of the endosymbiont Rickettsia in an insect pest. Microb Ecol. doi:10.1007/s00248-015-0565-z

    PubMed  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659. doi:10.1046/j.1365-294x.2000.01020.x

    Article  PubMed  CAS  Google Scholar 

  • Conti F, Tumminelli R, Amico C, Fisicaro R, Frittitta C, Perrotta G, Marullo R (2002) Monitoring Pezothrips kellyanus on citrus in eastern Sicily. In: Marullo R, Mound LA (eds) Thrips and tospoviruses. Proceedings of the 7th international symposium on Thysanoptera. CSIRO, Canberra, pp 207–210

    Google Scholar 

  • Costa L, Mateus C, Strassen R, Franco J, Garcia-Marí F (2006) Thrips (Thysanoptera) associated to lemon orchards in the Oeste region of Portugal. IOBC/WPRS Bull 29:285–291

    Google Scholar 

  • Dao HT, Beattie GAC, Spooner-Hart R, Riegler M, Holford P (2015) Primary parasitoids of red scale (Aonidiella aurantii) in Australia and a review of their introductions from Asia. Insect Sci. doi:10.1111/1744-7917.12275

    PubMed  Google Scholar 

  • Duron O, Bouchon D, Boutin S, Bellamy L, Zhou L, Engelstädter J, Hurst GD (2008a) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 6:27. doi:10.1186/1741-7007-6-27

    Article  PubMed  PubMed Central  Google Scholar 

  • Duron O, Hurst GDD, Hornett EA, Josling JA, Engelstädter JAN (2008b) High incidence of the maternally inherited bacterium Cardinium in spiders. Mol Ecol 17:1427–1437. doi:10.1111/j.1365-294X.2008.03689.x

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform molecular ecology resources population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543. doi:10.1111/j.1365-2311.2011.01318.x

    Article  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    PubMed  CAS  Google Scholar 

  • Froud KJ, Stevens PS, Steven D (2001) Survey of altertative host plants for Kelly’s citrus thrips (Pezothrips kellyanus) in citrus growing regions. N Z Plant Prot 54:15–20

    Google Scholar 

  • Groot TVM, Breeuwer JAJ (2006) Cardinium symbionts induce haploid thelytoky in most clones of three closely related Brevipalpus species. Exp Appl Acarol 39:257–271. doi:10.1007/s10493-006-9019-0

    Article  PubMed  Google Scholar 

  • Hansen A, Jeong G, Paine T, Stouthamer R (2007) Frequency of secondary symbiont infection in an invasive psyllid relates to parasitism pressure on a geographic scale in California. Appl Environ Microbiol 73:7531–7535. doi:10.1128/AEM.01672-07

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hendry TA, Hunter MS, Baltrus DA (2014) The facultative symbiont Rickettsia protects an invasive whitefly against entomopathogenic Pseudomonas syringae strains. Appl Environ Microbiol 80:7161–7168. doi:10.1128/AEM.02447-14

    Article  PubMed  PubMed Central  Google Scholar 

  • Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, Chiel E, Duckworth VE, Dennehy TJ, Zchori-Fein E (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332:254–256. doi:10.1126/science.1199410

    Article  PubMed  CAS  Google Scholar 

  • Hoy MA (2013) Molecular systematics and the evolution of arthropods. In: Insect molecular genetics: an introduction to principles and applications. Elsevier, London, pp 522–579. doi:10.1016/b978-012357031-4/50031-5

  • Hurst GDD, Jiggins FM (2005) Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc R Soc B 272:1525–1534. doi:10.1098/rspb.2005.3056

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Jeschke J, Aparicio LG, Haider S, Heger T, Lortie C, Pyšek P, Strayer D (2012) Support for major hypotheses in invasion biology is uneven and declining. NeoBiota 14:1–20

    Article  Google Scholar 

  • Jolley KA, Chan M-S, Maiden MC (2004) mlstdbNet—distributed multi-locus sequence typing (MLST) databases. BMC Bioinform 5:86. doi:10.1186/1471-2105-5-86

    Article  Google Scholar 

  • Jones CM, Brown MJ (2014) Parasites and genetic diversity in an invasive bumblebee. J Anim Ecol 83:1428–1440. doi:10.1111/1365-2656.12235

    Article  PubMed  PubMed Central  Google Scholar 

  • Kageyama D, Narita S, Watanabe M (2012) Insect sex determination manipulated by their endosymbionts: incidences, mechanisms and implications. Insects 3:161–199. doi:10.3390/insects3010161

    Article  PubMed  PubMed Central  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170. doi:10.1016/S0169-5347(02)02499-0

    Article  Google Scholar 

  • Kern P, Cook JM, Kageyama D, Riegler M (2015) Double trouble: combined action of meiotic drive and Wolbachia feminization in Eurema butterflies. Biol Lett 11:20150095. doi:10.1098/rsbl.2015.0095

    Article  PubMed  Google Scholar 

  • Kumm S, Moritz G (2008) First detection of Wolbachia in arrhenotokous populations of thrips species (Thysanoptera: Thripidae and Phlaeothripidae) and its role in reproduction. Environ Entomol 37:1422–1428. doi:10.1603/0046-225X-37.6.1422

    Article  PubMed  Google Scholar 

  • Lo N, Tokuda G, Watanabe H, Rose H, Slaytor M, Maekawa K, Bandi C, Noda H (2000) Evidence from multiple gene sequences indicates that termites evolved from wood-feeding cockroaches. Curr Biol 10:801–804. doi:10.1016/S0960-9822(00)00561-3

    Article  PubMed  CAS  Google Scholar 

  • Marullo R (2002) Pezothrips kellyanus, parassita degli agrumi nel Mediterraneo e nel mondo. In: Atti XIX Congresso Nazionale Italiano di Entomologia Catania, 10–15 giugno, pp 595–599

  • Marullo R (2009) Host-plant ranges and pest potential: habits of some thrips species in areas of southern Italy. Bull Insectol 62:253–255

    Google Scholar 

  • Monteiro A, Pierce NE (2001) Phylogeny of Bicyclus (Lepidoptera: Nymphalidae) inferred from COI, COII, and EF-1α gene sequences. Mol Phylogenet Evol 18:264–281. doi:10.1006/mpev.2000.0872

    Article  PubMed  CAS  Google Scholar 

  • Moritz G, Mound L, Morris DC, Goldarazena A (2004) Pest thrips of the world on CD-ROM: an identification and information system using molecular and microscopical methods. The University of Queensland, Australia

  • Morrow J, Frommer M, Shearman D, Riegler M (2014) Tropical tephritid fruit fly community with high incidence of shared Wolbachia strains as platform for horizontal transmission of endosymbionts. Environ Microbiol 16:3632–3637. doi:10.1111/1462-2920.12382

    Article  Google Scholar 

  • Morrow JL, Frommer M, Royer JE, Shearman DC, Riegler M (2015) Wolbachia pseudogenes and low prevalence infections in tropical but not temperate Australian tephritid fruit flies: manifestations of lateral gene transfer and endosymbiont spillover? BMC Evol Biol 15:202. doi:10.1186/s12862-015-0474-2

    Article  PubMed  PubMed Central  Google Scholar 

  • Morse JG, Hoddle MS (2006) Invasion biology of thrips. Annu Rev Entomol 51:67–89. doi:10.1146/annurev.ento.51.110104.151044

    Article  PubMed  CAS  Google Scholar 

  • Mound LA, Walker AK (1982) Terebrantia (Insecta: Thysanoptera). Fauna of New Zealand, vol 1. Science Information Division, DSIR, Wellington

    Google Scholar 

  • Mound LA, Tree DJ, Paris D (2012) OZ Thrips–Thysanoptera in Australia. http://www.ozthrips.org/. Accessed 5 April 2012

  • Nakamura Y, Kawai S, Yukuhiro F, Ito S, Gotoh T, Kisimoto R, Yanase T, Matsumoto Y, Kageyama D, Noda H (2009) Prevalence of Cardinium bacteria in planthoppers and spider mites and taxonomic revision of “Candidatus Cardinium hertigii” based on detection of a new Cardinium group from biting midges. Appl Environ Microbiol 75:6757–6763. doi:10.1128/AEM.01583-09

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Navarro-Campos C, Aguilar A, Garcia-Marí F (2011) Population trend and fruit damage of Pezothrips kellyanus in citrus orchards in Valencia (Spain). IOBC/WPRS Bull 62:285–292

    Google Scholar 

  • Nguyen DT, Spooner-Hart RN, Riegler M (2015) Polyploidy versus endosymbionts in obligately thelytokous thrips. BMC Evol Biol 15:23. doi:10.1186/s12862-015-0304-6

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Neill SL, Giordano R, Colbert A, Karrg T, Robertson H (1992) 16S rRNA phylogenetic analysis of the bacterial endosymbionts associated with cytoplasmic incompatibility in insects. Proc Natl Acad Sci USA 89:2699–2702

    Article  PubMed  PubMed Central  Google Scholar 

  • Prenter J, MacNeil C, Dick JTA, Dunn AM (2004) Roles of parasites in animal invasions. Trends Ecol Evol 19:385–390. doi:10.1016/j.tree.2004.05.002

    Article  PubMed  Google Scholar 

  • Puillandre N, Dupas S, Dangles O, Zeddam J-L, Capdevielle-Dulac C, Barbin K, Torres-Leguizamon M, Silvain J-F (2008) Genetic bottleneck in invasive species: the potato tuber moth adds to the list. Biol Invasions 10:319–333. doi:10.1007/s10530-007-9132-y

    Article  Google Scholar 

  • Reuter M, Pedersen JS, Keller L (2004) Loss of Wolbachia infection during colonisation in the invasive Argentine ant Linepithema humile. Heredity 94:364–369. doi:10.1038/sj.hdy.6800601

    Article  Google Scholar 

  • Reuter M, Lehmann L, Guillaume F (2008) The spread of incompatibility-inducing parasites in sub-divided host populations. BMC Evol Biol 8:134. doi:10.1186/1471-2148-8-134

    Article  PubMed  PubMed Central  Google Scholar 

  • Rey O, Estoup A, Facon B, Loiseau A, Aebi A, Duron O, Vavre F, Foucaud J (2013) Distribution of endosymbiotic reproductive manipulators reflects invasion process and not reproductive system polymorphism in the little fire ant Wasmannia auropunctata. PLoS One 8:e58467. doi:10.1371/journal.pone.0058467

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Reynaud P (2010) Thrips (Thysanoptera). In: Roques A et al. (eds) Alien terrestrial arthropods of Europe, vol 4. Pensoft Publishers, pp 767–791. doi:10.3897/biorisk.4.59

  • Riegler M, Sidhu M, Miller WJ, O’Neill SL (2005) Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr Biol 15:1428–1433. doi:10.1016/j.cub.2005.06.069

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  • Roy H, Handley L-JL, Schönrogge K, Poland R, Purse B (2011) Can the enemy release hypothesis explain the success of invasive alien predators and parasitoids? Biocontrol 56:451–468. doi:10.1007/s10526-011-9349-7

    Article  Google Scholar 

  • Rugman-Jones PF, Hoddle MS, Stouthamer R (2007) Population genetics of Scirtothrips perseae: tracing the origin of a recently introduced exotic pest of Californian avocado orchards, using mitochondrial and microsatellite DNA markers. Entomol Exp Appl 124:101–115. doi:10.1111/j.1570-7458.2007.00559.x

    Article  CAS  Google Scholar 

  • Rugman-Jones P, Hoddle M, Amrich R, Heraty J, Stouthamer-Ingel C, Stouthamer R (2012) Phylogeographic structure, outbreeding depression, and reluctant virgin oviposition in the bean thrips, Caliothrips fasciatus (Pergande) (Thysanoptera: Thripidae), in California. Bull Entomol Res 102:698–709. doi:10.1017/S0007485312000302

    Article  PubMed  CAS  Google Scholar 

  • Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332

    Article  Google Scholar 

  • Schuler H, Bertheau C, Egan SP, Feder JL, Riegler M, Schlick-Steiner BC, Steiner FM, Johannesen J, Kern P, Tuba K (2013) Evidence for a recent horizontal transmission and spatial spread of Wolbachia from endemic Rhagoletis cerasi (Diptera: Tephritidae) to invasive Rhagoletis cingulata in Europe. Mol Ecol 22:4101–4111. doi:10.1111/mec.12362

    Article  PubMed  CAS  Google Scholar 

  • Shoemaker DD, Ross KG, Keller L, Vargo E, Werren JH (2000) Wolbachia infections in native and introduced populations of fire ants (Solenopsis spp.). Insect Mol Biol 9:661–673. doi:10.1046/j.1365-2583.2000.00233.x

    Article  PubMed  CAS  Google Scholar 

  • Simões PM, Mialdea G, Reiss D, Sagot MF, Charlat S (2011) Wolbachia detection: an assessment of standard PCR protocols. Mol Ecol Resour 11:567–572

    Article  PubMed  Google Scholar 

  • Song H, Buhay JE, Whiting MF, Crandall KA (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proc Natl Acad Sci USA 105:13486–13491. doi:10.1073/pnas.0803076105

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Stouthamer R, Luck RF, Hamilton W (1990) Antibiotics cause parthenogenetic Trichogramma (Hymenoptera: Trichogrammatidae) to revert to sex. Proc Natl Acad Sci USA 87:2424–2427

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. doi:10.1093/molbev/msr121

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Teksam I, Tunç İ (2009) An analysis of Thysanoptera associated with citrus flowers in Antalya, Turkey: composition, distribution, abundance and pest status of species. Appl Entomol Zool 44:455–464. doi:10.1303/aez.2009.455

    Article  Google Scholar 

  • Tsutsui ND, Kauppinen SN, Oyafuso AF, Grosberg RK (2003) The distribution and evolutionary history of Wolbachia infection in native and introduced populations of the invasive argentine ant (Linepithema humile). Mol Ecol 12:3057–3068. doi:10.1046/j.1365-294X.2003.01979.x

    Article  PubMed  Google Scholar 

  • van der Kooi CJ, Schwander T (2014) Evolution of asexuality via different mechanisms in grass thrips (Thysanoptera: Aptinothrips). Evolution 68:1883–1893. doi:10.1111/evo.12402

    Article  PubMed  Google Scholar 

  • Varikou KN, Birouraki A, Tsitsipis I, Sergentani C (2012) Effect of temperature on the fecundity of Pezothrips kellyanus (Thysanoptera: Thripidae). Ann Entomol Soc Am 105:60–65. doi:10.1603/AN11083

    Article  Google Scholar 

  • Vassiliou VA (2010) Ecology and behavior of Pezothrips kellyanus (Thysanoptera: Thripidae) on citrus. J Econ Entomol 103:47–53. doi:10.1603/ec09114

    Article  PubMed  CAS  Google Scholar 

  • Vassiliou VA (2011) Botanical insecticides in controlling Kelly’s citrus thrips (Thysanoptera: Thripidae) on organic grapefruits. J Econ Entomol 104:1979–1985. doi:10.1603/EC11105

    Article  PubMed  CAS  Google Scholar 

  • Vavre F, Fouillet P, Leury F (2003) Between- and within-host species selection on cytoplasmic incompatibility-inducing Wolbachia in haplodiploids. Evolution 57:421–427. doi:10.1111/j.0014-3820.2003.tb00275.x

    PubMed  Google Scholar 

  • Villablance FX, Roderick GK, Palumbi SR (1998) Invasion genetics of the Mediteranean fruit fly: variation in multiple nuclear introns. Mol Ecol 7:547–560. doi:10.1046/j.1365-294x.1998.00351.x

    Article  Google Scholar 

  • Webster KW, Cooper P, Mound LA (2006) Studies on Kelly’s citrus thrips, Pezothrips kellyanus (Bagnall) (Thysanoptera: Thripidae): sex attractants, host associations and country of origin. Aust J Entomol 45:67–74. doi:10.1111/j.1440-6055.2006.00508.x

    Article  Google Scholar 

  • Weeks AR, Velten R, Stouthamer R (2003) Incidence of a new sex-ratio-distorting endosymbiotic bacterium among arthropods. Proc R Soc Lond B 270:1857–1865. doi:10.1098/rspb.2003.2425

    Article  Google Scholar 

  • Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ (2015) The incidence of bacterial endosymbionts in terrestrial arthropods. Proc R Soc B. doi:10.1098/rspb.2015.0249

    PubMed  Google Scholar 

  • Werren JH, Zhang W, Guo LR (1995) Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc R Soc B 261:55–63. doi:10.1098/rspb.1995.0117

    Article  PubMed  CAS  Google Scholar 

  • White J, Kelly S, Perlman S, Hunter M (2009) Cytoplasmic incompatibility in the parasitic wasp Encarsia inaron: disentangling the roles of Cardinium and Wolbachia symbionts. Heredity 102:483–489. doi:10.1038/hdy.2009.5

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zchori-Fein E, Perlman SJ (2004) Distribution of the bacterial symbiont Cardinium in arthropods. Mol Ecol 13:2009–2016. doi:10.1111/j.1365-294X.2004.02203.x

    Article  PubMed  CAS  Google Scholar 

  • Zchori-Fein E, Perlman SJ, Kelly SE, Katzir N, Hunter MS (2004) Characterization of a ‘Bacteroidetes’ symbiont in Encarsia wasps (Hymenoptera: Aphelinidae): proposal of ‘Candidatus Cardinium hertigii’. Int J Syst Evol Microbiol 54:961–968. doi:10.1099/ijs.0.02957-0

    Article  PubMed  CAS  Google Scholar 

  • Zchori-Fein E, Lahav T, Freilich S (2014) Variations in the identity and complexity of endosymbiont combinations in whitefly hosts. Front Microbiol 5:310. doi:10.3389/fmicb.2014.00310

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou W, Rousset F, O’Neill S (1998) Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc R Soc B 265:509–515. doi:10.1098/rspb.1998.0324

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zug R, Hammerstein P (2014) Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts. Biol Rev 90:89–111. doi:10.1111/brv.12098

    Article  PubMed  Google Scholar 

  • zur Strassen R (1986) Thysanopteren auf Inseln der Nördlichen Sporaden in der Ägäis (Griechenland) (Insecta: Thysanoptera). Senckenberg Biol 67:85–129

    Google Scholar 

  • zur Strassen R (1996) Neue Daten zur Systematik und Verbreitung einiger west-paläarktischer Terebrantia-Arten (Thysanoptera). Entomol Nachr Ber 40:111–118

    Google Scholar 

  • zur Strassen R (2000) Thysanopterologische Notizen (7) (Thysanoptera, Terebrantia). Entomol Nachr Ber 44:25–34

    Google Scholar 

Download references

Acknowledgments

We thank colleagues for supplying thrips specimens (Supplementary Table S1). We also thank Jennifer Morrow, Aidan Hall, Peter Kern and two reviewers for comments on earlier versions of the manuscript. DTN was supported by an Australian Postgraduate Award (International) and MR by research funds from Western Sydney University and HIE.

Author information

Authors and Affiliations

  1. Hawkesbury Institute for the Environment, Western Sydney University, Locked Bag 1797, Penrith, NSW, 2751, Australia

    Duong T. Nguyen, Robert N. Spooner-Hart & Markus Riegler

  2. School of Science and Health, Western Sydney University, Locked Bag 1797, Penrith, NSW, 2751, Australia

    Robert N. Spooner-Hart

Authors
  1. Duong T. Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert N. Spooner-Hart
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Markus Riegler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Markus Riegler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1402 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nguyen, D.T., Spooner-Hart, R.N. & Riegler, M. Loss of Wolbachia but not Cardinium in the invasive range of the Australian thrips species, Pezothrips kellyanus . Biol Invasions 18, 197–214 (2016). https://doi.org/10.1007/s10530-015-1002-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-015-1002-4

Keywords

Search

Navigation