Wolbachia infection dynamics in a natural population of the pear psyllid Cacopsylla pyri (Hemiptera: Psylloidea) across its seasonal generations
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
36192576
PubMed Central
PMC9529970
DOI
10.1038/s41598-022-20968-0
PII: 10.1038/s41598-022-20968-0
Knihovny.cz E-zdroje
- MeSH
- fylogeneze MeSH
- Hemiptera * genetika MeSH
- Pyrus * MeSH
- roční období MeSH
- Wolbachia * genetika MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Wolbachia is one of the most abundant intracellular symbionts of arthropods and has profound effects on host biology. Wolbachia transmission and host phenotypes often depend on its density within the host, which can be affected by multiple biotic and abiotic factors. However, very few studies measured Wolbachia density in natural host populations. Here, we describe Wolbachia in the pear psyllid Cacopsylla pyri from three populations in the Czech Republic. Using phylogenetic analyses based on wsp and multilocus sequence typing genes, we demonstrate that C. pyri harbours three new Wolbachia strains from supergroup B. A fourth Wolbachia strain from supergroup A was also detected in parasitised immatures of C. pyri, but likely came from a hymenopteran parasitoid. To obtain insights into natural Wolbachia infection dynamics, we quantified Wolbachia in psyllid individuals from the locality with the highest prevalence across an entire year, spanning several seasonal generations of the host. All tested females were infected and Wolbachia density remained stable across the entire period, suggesting a highly efficient vertical transmission and little influence from the environment and different host generations. In contrast, we observed a tendency towards reduced Wolbachia density in males which may suggest sex-related differences in Wolbachia-psyllid interactions.
Competence Centre for Plant Health Free University of Bozen Bolzano Bolzano Italy
Department of Botany and Zoology Faculty of Science Masaryk University Brno Czech Republic
Faculty of Science and Technology Free University of Bozen Bolzano Bolzano Italy
Institut Agro INRAE IRHS SFR Quasav University of Angers Angers France
Zobrazit více v PubMed
Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ. The incidence of bacterial endosymbionts in terrestrial arthropods. Proc. R. Soc. B. 2015;282(1807):20150249. doi: 10.1098/rspb.2015.0249. PubMed DOI PMC
Lefoulon E, et al. Breakdown of coevolution between symbiotic bacteria Wolbachia and their filarial hosts. PeerJ. 2016;4:e1840. doi: 10.7717/peerj.1840. PubMed DOI PMC
Zug R, Hammerstein P. Still a host of hosts for Wolbachia: Analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS ONE. 2012;7(6):38544. doi: 10.1371/journal.pone.0038544. PubMed DOI PMC
Werren JH, Baldo L, Clark ME. Wolbachia: Master manipulators of invertebrate biology. Nat. Rev. Microbiol. 2008;6:741–751. doi: 10.1038/nrmicro1969. PubMed DOI
Engelstädter J, Hurst GDD. The ecology and evolution of microbes that manipulate host reproduction. Annu. Rev. Ecol. Evol. Syst. 2009;40:127–149. doi: 10.1146/annurev.ecolsys.110308.120206. DOI
Hurst GDD, Frost CL. Reproductive parasitism: Maternally inherited symbionts in a piparental world. Cold Spring Harb. Perspect. Biol. 2015;7(4):a017699. doi: 10.1101/cshperspect.a017699. PubMed DOI PMC
Bailly-Bechet M, et al. How long does Wolbachia remain on board? Molec. Biol. Evol. 2017;34:1183–1193. doi: 10.1093/molbev/msx073. PubMed DOI
Kaur R, et al. Living in the endosymbiotic world of Wolbachia: A centennial review. Cell Host Microbe. 2021;29:879–893. doi: 10.1016/j.chom.2021.03.006. PubMed DOI PMC
Timmermans MJTN, Ellers J. Wolbachia endosymbiont is essential for egg hatching in a parthenogenetic arthropod. Evol. Ecol. 2009;23:931–942. doi: 10.1007/s10682-008-9282-0. DOI
Hosokawa T, et al. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc. Nation. Acad. Sci. USA. 2010;107:769–774. doi: 10.1073/pnas.0911476107. PubMed DOI PMC
Nikoh N, et al. Evolutionary origin of insect-Wolbachia nutritional mutualism. Proc. Nation. Acad. Sci. USA. 2014;111:10257–10262. doi: 10.1073/pnas.1409284111. PubMed DOI PMC
Balvín O, Roth S, Talbot B, Reinhardt K. Co-speciation in bedbug Wolbachia parallel the pattern in nematode hosts. Sci. Rep. 2018;8(1):1–9. doi: 10.1038/s41598-018-25545-y. PubMed DOI PMC
Manoj RRS, Latrofa MS, Epis S, Otranto D. Wolbachia: Endosymbiont of onchocercid nematodes and their vectors. Parasites Vectors. 2021;14(1):1–24. doi: 10.1186/s13071-021-04742-1. PubMed DOI PMC
Gerth M, Gansauge M-T, Weigert A, Bleidorn C. Phylogenomic analyses uncover origin and spread of the Wolbachia pandemic. Nat. Commun. 2014;5(1):1–7. doi: 10.1038/ncomms6117. PubMed DOI
Brown AMV, et al. Genomic evidence for plant-parasitic nematodes as the earliest Wolbachia hosts. Sci. Rep. 2016;6(1):1–14. doi: 10.1038/srep34955. PubMed DOI PMC
Kajtoch Ł, et al. Using host species traits to understand the Wolbachia infection distribution across terrestrial beetles. Sci. Rep. 2019;9(1):1–15. doi: 10.1038/s41598-018-38155-5. PubMed DOI PMC
Zimmermann BL, et al. Supergroup F Wolbachia in terrestrial isopods: Horizontal transmission from termites? Evol. Ecol. 2021;35:165–182. doi: 10.1007/s10682-021-10101-4. PubMed DOI PMC
Heath BD, Butcher RDJ, Whitfield WGF, Hubbard SF. Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr. Biol. 1999;9:313–316. doi: 10.1016/S0960-9822(99)80139-0. PubMed DOI
Vavre F, Fleury F, Lepetit D, Fouillet P, Bouletreau M. Phylogenetic evidence for horizontal transmission of Wolbachia in host- parasitoid associations. Mol. Biol. and Evol. 1999;16:1711–1723. doi: 10.1093/oxfordjournals.molbev.a026084. PubMed DOI
Jiggins FM, Bentley JK, Majerus MEN, Hurst GDD. Recent changes in phenotype and patterns of host specialization in Wolbachia bacteria. Mol. Ecol. 2002;11:1275–1283. doi: 10.1046/j.1365-294X.2002.01532.x. PubMed DOI
Schuler H, et al. 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. 2013;22:4101–4111. doi: 10.1111/mec.12362. PubMed DOI
Sanaei E, Charlat S, Engelstädter J. Wolbachia host shifts: Routes, mechanisms, constraints and evolutionary consequences. Biol. Rev. 2021;96:433–453. doi: 10.1111/brv.12663. PubMed DOI
Hoffmann AA, Ross PA, Rašić G. Wolbachia strains for disease control: Ecological and evolutionary considerations. Evol. Appl. 2015;8:751–768. doi: 10.1111/eva.12286. PubMed DOI PMC
Chu C-C, Gill TA, Hoffmann M, Pelz-Stelinski KS. Inter-population variability of endosymbiont densities in the Asian citrus psyllid (Diaphorina citri Kuwayama) Microb. Ecol. 2016;71:999–1007. doi: 10.1007/s00248-016-0733-9. PubMed DOI PMC
Nováková E, et al. Mosquito microbiome dynamics, a background for prevalence and seasonality of west nile virus. Front. Microbiol. 2017;8:526. doi: 10.3389/fmicb.2017.00526. PubMed DOI PMC
Krstić O, et al. Wolbachia infection in natural populations of dictyophara Europaea, an alternative vector of grapevine flavescence dorée phytoplasma: Effects and interactions: Effects of wolbachia on phytoplasma vector. Ann. Appl. Biol. 2018;172:47–64. doi: 10.1111/aab.12400. DOI
Gong J-T, et al. Stable introduction of plant-virus-inhibiting Wolbachia into planthoppers for rice protection. Curr. Biol. 2020;30:4837–4845. doi: 10.1016/j.cub.2020.09.033. PubMed DOI
Johnston KL, et al. Anti-Wolbachia drugs for filariasis. Trends. Parasit. 2021;37(12):1068–1081. doi: 10.1016/j.pt.2021.06.004. PubMed DOI
Brelsfoard CL, Dobson SL. Wolbachia-based strategies to control insect pests and disease vectors. Asia-Pac. J. Mol. Biol. Biotech. 2009;17:55–63.
Arora AK, Douglas AE. Hype or opportunity? Using microbial symbionts in novel strategies for insect pest control. J. Insect Phys. 2017;103:10–17. doi: 10.1016/j.jinsphys.2017.09.011. PubMed DOI
Landmann F. The Wolbachia Endosymbionts. Microbiol. Spectr. 2019;7(2):72. doi: 10.1128/microbiolspec.BAI-0018-2019. PubMed DOI PMC
McMeniman CJ, et al. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science. 2009;323:141–144. doi: 10.1126/science.1165326. PubMed DOI
Bourtzis K, et al. Harnessing mosquito-Wolbachia symbiosis for vector and disease control. Acta Trop. 2014;132S:S150–S163. doi: 10.1016/j.actatropica.2013.11.004. PubMed DOI
Schmidt TL, et al. Local introduction and heterogeneous spatial spread of dengue-suppressing Wolbachia through an urban population of Aedes aegypti. PLoS Biol. 2017;15(5):2001894. doi: 10.1371/journal.pbio.2001894. PubMed DOI PMC
Fagen J, et al. Characterization of the relative abundance of the citrus pathogen Ca. Liberibacter Asiaticus in the microbiome of its insect vector, Diaphorina citri, using high throughput 16S rRNA sequencing. Open Microbiol. J. 2012;6:29–33. doi: 10.2174/1874285801206010029. PubMed DOI PMC
Kolora LD, Powell CM, Hunter W, Bextine B, Lauzon CR. Internal extracellular bacteria of diaphorina citri Kuwayama (hemiptera: Psyllidae), the Asian citrus psyllid. Curr. Microbiol. 2015;70:710–715. doi: 10.1007/s00284-015-0774-1. PubMed DOI
Hosseinzadeh S, et al. Distribution and variation of bacterial endosymbiont and “Candidatus Liberibacter asiaticus” titer in the huanglongbing insect vector Diaphorina citri Kuwayama. Microb. Ecol. 2019;78:206–222. doi: 10.1007/s00248-018-1290-1. PubMed DOI
Moussa A, et al. Bacterial microbiota associated with insect vectors of grapevine Bois noir disease in relation to phytoplasma infection. FEMS Microbiol. Ecol. 2020;96(11):fiaa203. doi: 10.1093/femsec/fiaa203. PubMed DOI
Bordenstein SR, O’Hara FP, Werren JH. Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature. 2001;409:707–710. doi: 10.1038/35055543. PubMed DOI
Johnson K. The impact of Wolbachia on virus infection in mosquitoes. Viruses. 2015;7:5705–5717. doi: 10.3390/v7112903. PubMed DOI PMC
López-Madrigal S, Duarte EH. Titer regulation in arthropod-Wolbachia symbioses. FEMS Microbiol. Let. 2019;366(23):fnz232. doi: 10.1093/femsle/fnz232. PubMed DOI
Min K-T, Benzer S. Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc. Nation. Acad. Sci. 1997;94:10792–10796. doi: 10.1073/pnas.94.20.10792. PubMed DOI PMC
Chrostek E, et al. Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: A phenotypic and phylogenomic analysis. PLoS Genet. 2013;9(12):e1003896. doi: 10.1371/journal.pgen.1003896. PubMed DOI PMC
Stacey DA, et al. Genotype and temperature influence pea aphid resistance to a fungal entomopathogen. Physiol. Entomol. 2003;28:75–81. doi: 10.1046/j.1365-3032.2003.00309.x. DOI
Thomas MB, Blanford S. Thermal biology in insect-parasite interactions. Trends in Ecol. Evol. 2003;18:344–350. doi: 10.1016/S0169-5347(03)00069-7. DOI
Jaenike J. Coupled population dynamics of endosymbionts within and between hosts. Oikos. 2009;118:353–362. doi: 10.1111/j.1600-0706.2008.17110.x. DOI
Versace E, Nolte V, Pandey RV, Tobler R, Schlötterer C. Experimental evolution reveals habitat-specific fitness dynamics among Wolbachia clades in Drosophila melanogaster. Mol. Ecol. 2014;23:802–814. doi: 10.1111/mec.12643. PubMed DOI PMC
Corbin C, Heyworth ER, Ferrari J, Hurst GDD. Heritable symbionts in a world of varying temperature. Heredity. 2017;118:10–20. doi: 10.1038/hdy.2016.71. PubMed DOI PMC
Berticat C, Rousset F, Raymond M, Berthomieu A, Weill M. High Wolbachia density in insecticide–resistant mosquitoes. Proc. R. Soc. Lond. B. 2002;269:1413–1416. doi: 10.1098/rspb.2002.2022. PubMed DOI PMC
Mouton L, Henri H, Bouletreau M, Vavre F. Strain-specific regulation of intracellular Wolbachia density in multiply infected insects. Mol. Ecol. 2003;12:3459–3465. doi: 10.1046/j.1365-294X.2003.02015.x. PubMed DOI
Mouton L, Henri H, Charif D, Boulétreau M, Vavre F. Interaction between host genotype and environmental conditions affects bacterial density in Wolbachia symbiosis. Biol. Lett. 2007;3:210–213. doi: 10.1098/rsbl.2006.0590. PubMed DOI PMC
Kondo N, Shimada M, Fukatsu T. Infection density of Wolbachia endosymbiont affected by co-infection and host genotype. Biol. Lett. 2005;1:488–491. doi: 10.1098/rsbl.2005.0340. PubMed DOI PMC
Duron O, et al. High Wolbachia density correlates with cost of infection for insecticide resistant Culex pipiens mosquitoe. Evol. 2006;60:303–314. doi: 10.1111/j.0014-3820.2006.tb01108.x. PubMed DOI
Dittmer J, et al. Host tissues as microhabitats for Wolbachia and quantitative insights into the bacterial community in terrestrial isopods. Mol. Ecol. 2014;23:2619–2635. doi: 10.1111/mec.12760. PubMed DOI
Mouton L, et al. Virulence, multiple Infections and regulation of symbiotic population in the Wolbachia-Asobara tabida symbiosis. Genetics. 2004;168:181–189. doi: 10.1534/genetics.104.026716. PubMed DOI PMC
Goto S, Anbutsu H, Fukatsu T. Asymmetrical interactions between Wolbachia and Spiroplasma endosymbionts coexisting in the same insect host. Appl. Environ. Microbiol. 2006;72:4805–4810. doi: 10.1128/AEM.00416-06. PubMed DOI PMC
Mousson L, et al. Wolbachia modulates Chikungunya replication in Aedes albopictus. Mol. Ecol. 2010;19:1953–1964. doi: 10.1111/j.1365-294X.2010.04606.x. PubMed DOI
Unckless RL, Boelio LM, Herren JK, Jaenike J. Wolbachia as populations within individual insects: Causes and consequences of density variation in natural populations. Proc. R. Soc. B. 2009;276:2805–2811. doi: 10.1098/rspb.2009.0287. PubMed DOI PMC
Tortosa P, et al. Wolbachia age-sex-specific density in Aedes albopictus: A host evolutionary response to cytoplasmic incompatibility? PLoS ONE. 2010;5:e9700. doi: 10.1371/journal.pone.0009700. PubMed DOI PMC
Moretti R, et al. Increased biting rate and decreased Wolbachia density in irradiated Aedes mosquitoes. Paras. Vectors. 2022;15(1):1–16. PubMed PMC
Duron O, Fort P, Weill M. Influence of aging on cytoplasmic incompatibility, sperm modification and Wolbachia density in Culex pipiens mosquitoes. Heredity. 2007;98:368–374. doi: 10.1038/sj.hdy.6800948. PubMed DOI
Shropshire JD, Hamant E, Cooper BS. Male age and Wolbachia dynamics: investigating how fast and why bacterial densities and cytoplasmic incompatibility strengths vary. MBio. 2021;12(6):e02998. doi: 10.1128/mbio.02998-21. PubMed DOI PMC
Zhao D-X, Zhang X-F, Chen D-S, Zhang Y-K, Hong X-Y. Wolbachia-host interactions: host mating patterns affect Wolbachia density dynamics. PLoS ONE. 2013;8(6):e66373. doi: 10.1371/journal.pone.0066373. PubMed DOI PMC
Mouton L, Henri H, Bouletreau M, Vavre F. Effect of temperature on Wolbachia density and impact on cytoplasmic incompatibility. Parasitology. 2006;132:49–56. doi: 10.1017/S0031182005008723. PubMed DOI
Lu W-N, Chiu M-C, Kuo M-H. Host life stage- and temperature-dependent density of the symbiont Buchnera aphidicola in a subtropical pea aphid (Acyrthosiphon pisum) population. J. Asia-Pac. Entomol. 2014;17:537–541. doi: 10.1016/j.aspen.2014.03.012. DOI
Perrot-Minnot M-J, Guo LR, Werren JH. Single and double infections with Wolbachia in the parasitic wasp Nasonia vitripennis effects on compatibility. Genetics. 1996;143:961–972. doi: 10.1093/genetics/143.2.961. PubMed DOI PMC
Van Opijnen T, Breeuwer JAJ. High temperatures eliminate Wolbachia, a cytoplasmic incompatibility inducing endosymbiont, from the two-spotted spider mite. Experim. Appl. Acarol. 1999;23:871–881. doi: 10.1023/A:1006363604916. PubMed DOI
Bordenstein SR, Bordenstein SR. Temperature affects the tripartite interactions between bacteriophage WO, Wolbachia, and cytoplasmic incompatibility. PLoS ONE. 2011;6(12):e29106. doi: 10.1371/journal.pone.0029106. PubMed DOI PMC
Jiang R-X, et al. The Influence of temperature and host gender on bacterial communities in the Asian citrus psyllid. Insects. 2021;12(12):1054. doi: 10.3390/insects12121054. PubMed DOI PMC
Hurst GDD, Jiggins FM, Robinson SJ. What causes ineffcient transmission of male-killing Wolbachia in Drosophila? Heredity. 2001;87:220–226. doi: 10.1046/j.1365-2540.2001.00917.x. PubMed DOI
Hague MTJ, et al. Temperature effects on cellular host-microbe interactions explain continent-wide endosymbiont prevalence. Curr. Biol. 2021;32(4):878–88. doi: 10.1016/j.cub.2021.11.065. PubMed DOI PMC
Sumi T, Miura K, Miyatake T. No seasonal trend in infection of the pale grass blue butterfly, Zizeeria maha (Lepidoptera: Lycaenidae), by Wolbachia. Appl. Entomol. Zool. 2013;48:35–38. doi: 10.1007/s13355-012-0152-4. DOI
Sumi T, Miura K, Miyatake T. Wolbachia density changes seasonally amongst populations of the pale grass blue butterfly, Zizeeria maha (Lepidoptera: Lycaenidae) PLoS ONE. 2017;12(4):e0175373. doi: 10.1371/journal.pone.0175373. PubMed DOI PMC
Cohen C, Toh E, Munro D, Dong Q, Hawlena H. Similarities and seasonal variations in bacterial communities from the blood of rodents and from their flea vectors. ISME J. 2015;9:1662–1676. doi: 10.1038/ismej.2014.255. PubMed DOI PMC
Kriesner P, Conner WR, Weeks AR, Turelli M, Hoffmann AA. Persistence of a Wolbachia infection frequency cline in Drosophila melanogaster and the possible role of reproductive dormancy. Evolution. 2016;70:979–997. doi: 10.1111/evo.12923. PubMed DOI PMC
Overholt WA, Diaz R, Rosskopf E, Green SJ, Overholt WA. Deep characterization of the microbiomes of Calophya spp. (Hemiptera: Calophyidae) gall-inducing psyllids reveals the absence of plant pathogenic bacteria and three dominant endosymbionts. PLoS ONE. 2015;10(7):e0132248. doi: 10.1371/journal.pone.0132248. PubMed DOI PMC
Morrow JL, Hall AAG, Riegler M. Symbionts in waiting: The dynamics of incipient endosymbiont complementation and replacement in minimal bacterial communities of psyllids. Microbiome. 2017;5(1):1–23. doi: 10.1186/s40168-017-0276-4. PubMed DOI PMC
Morrow JL, et al. Characterization of the bacterial communities of psyllids associated with Rutaceae in Bhutan by high throughput sequencing. BMC Microbiol. 2020;20(1):1–6. doi: 10.1186/s12866-020-01895-4. PubMed DOI PMC
Shapoval NA, Nokkala S, Nokkala C, Kuftina GN, Kuznetsova VG. The incidence of Wolbachia bacterial endosymbiont in bisexual and parthenogenetic populations of the psyllid genus Cacopsylla (Hemiptera, Psylloidea) Insects. 2021;12:853. doi: 10.3390/insects12100853. PubMed DOI PMC
Nakabachi A, Inoue H, Hirose Y. Microbiome analyses of 12 psyllid species of the family Psyllidae identified various bacteria including Fukatsuia and Serratia symbiotica, known as secondary symbionts of aphids. BMC Microbiol. 2022;22(1):1–21. doi: 10.1186/s12866-021-02429-2. PubMed DOI PMC
Kruse A, et al. Combining ’omics and microscopy to visualize interactions between the Asian citrus psyllid vector and the Huanglongbing pathogen Candidatus Liberibacter asiaticus in the insect gut. PLoS ONE. 2017;12(6):e0179531. doi: 10.1371/journal.pone.0179531. PubMed DOI PMC
Song X, et al. Composition and change in the microbiome of Diaphorina citri infected with Candidatus Liberibacter asiaticus in China. Int. J. Trop. Insect. Sci. 2019;39:283–290. doi: 10.1007/s42690-019-00036-3. DOI
Nachappa P, Levy J, Pierson E, Tamborindeguy C. Diversity of endosymbionts in the potato psyllid, Bactericera cockerelli (Hemiptera: Triozidae), vector of zebra chip disease of potato. Curr. Microbiol. 2011;62:1510–1520. doi: 10.1007/s00284-011-9885-5. PubMed DOI
Hail D, Dowd SE, Bextine B. Identification and location of symbionts associated with potato psyllid (Bactericera cockerelli) lifestages. Environ. Entomol. 2012;41:98–107. doi: 10.1603/EN11198. PubMed DOI
Cooper WR, et al. Wolbachia infection differs among divergent mitochondrial haplotypes of Bactericera cockerelli (Hemiptera: Triozidae) Ann. Entomol. Soc. Amer. 2015;108:137–145. doi: 10.1093/aesa/sau048. DOI
Fu Z, et al. Host plants and Wolbachia shape the population genetics of sympatric herbivore populations. Evol. Appl. 2020;13:2740–2753. doi: 10.1111/eva.13079. PubMed DOI PMC
Štarhová Serbina L, et al. Microbiome of pear psyllids: a tale about closely-related species sharing their endosymbionts. Environ. Microbiol. 2022 doi: 10.1111/1462-2920.16180. PubMed DOI PMC
Jarausch, B., Tedeschi, R., Sauvion, N., Gross, J. & Jarausch, W. Psyllid Vectors. In: Phytoplasmas: Plant Pathogenic Bacteria - II (eds. Bertaccini, A., Weintraub, P. G., Rao, G. P. & Mori, N.) 53–78 (Springer Singapore, 2019).
Lauterer P. Results of the investigations on Hemiptera in Moravia, made by the Moravian museum (Psylloidea 2) Acta Musei. Morav. Sci. biol. 1999;84:71–151.
Hodkinson ID. Life cycle variation and adaptation in jumping plant lice (Insecta: Hemiptera: Psylloidea): A global synthesis. J. Natur. Hist. 2009;43:65–179. doi: 10.1080/00222930802354167. DOI
Hague MTJ, Mavengere H, Matute DR, Cooper BS. Environmental and genetic contributions to imperfect wMel-like Wolbachia transmission and frequency variation. Genetics. 2020;215:1117–1132. doi: 10.1534/genetics.120.303330. PubMed DOI PMC
Brinker P, Fontaine MC, Beukeboom LW, Falcao Salles J. Host, symbionts, and the microbiome: the missing tripartite interaction. Trends Microbiol. 2019;27:480–488. doi: 10.1016/j.tim.2019.02.002. PubMed DOI
Sinkins SP, et al. Wolbachia variability and host effects on crossing type in Culex mosquitoes. Nature. 2005;436:257–260. doi: 10.1038/nature03629. PubMed DOI
Ant TH, Herd C, Louis F, Failloux AB, Sinkins SP. Wolbachia transinfections in Culex quinquefasciatus generate cytoplasmic incompatibility. Insect Mol. Biol. 2020;29:1–8. doi: 10.1111/imb.12604. PubMed DOI PMC
James AC, Ballard JWO. Expression of cytoplasmic incompatibility in Drosophila simulans and its impact on infection frequencies and distribution of Wolbachia pipientis. Evol. 2000;54:1661–1672. doi: 10.1111/j.0014-3820.2000.tb00710.x. PubMed DOI
Koehncke A, Telschow A, Werren JH, Hammerstein P. Life and death of an influential passenger: Wolbachia and the evolution of CI-modifiers by their hosts. PLoS ONE. 2009;4(2):e4425. doi: 10.1371/journal.pone.0004425. PubMed DOI PMC
Schuler H, et al. Diversity and distribution of Wolbachia in relation to geography, host plant affiliation and life cycle of a heterogonic gall wasp. BMC Evol. Biol. 2018;18(1):1–5. doi: 10.1186/s12862-018-1151-z. PubMed DOI PMC
Bakovic V, Schebeck M, Telschow A, Stauffer C, Schuler H. Spatial spread of Wolbachia in Rhagoletis cerasi populations. Biol. Lett. 2018;14(5):20180161. doi: 10.1098/rsbl.2018.0161. PubMed DOI PMC
Kriesner P, Hoffmann AA, Lee SF, Turelli M, Weeks AR. Rapid sequential spread of two Wolbachia variants in Drosophila simulans. PLoS Pathog. 2013;9(9):e1003607. doi: 10.1371/journal.ppat.1003607. PubMed DOI PMC
Wolfe TM, et al. Comparative genome sequencing reveals insights into the dynamics of Wolbachia in native and invasive cherry fruit flies. Mol. Ecol. 2021;30:6259–6272. doi: 10.1111/mec.15923. PubMed DOI PMC
Jerinić-Prodanović D, Mihajlović L, Stojanović A. Parasitoids of jumping plant-lice (Psylloidea, Hemiptera) from the family Encyrtidae (Hymenoptera, Chalcidoidea) in Serbia. Zootaxa. 2019;4577:29–50. doi: 10.11646/zootaxa.4577.1.2. PubMed DOI
Meyer JM, Hoy MA. Molecular survey of endosymbionts in Florida populations of Diaphorina citri (Hemiptera: Psyllidae) and its parasitoids Tamarixia radiata (Hymenoptera: Eulophidae) and Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae) Flor. Entomol. 2008;91:294–304. doi: 10.1653/0015-4040(2008)91[294:MSOEIF]2.0.CO;2. DOI
Ashraf HJ, et al. Comparative microbiome analysis of Diaphorina citri and its associated parasitoids Tamarixia radiata and Diaphorencyrtus aligarhensis reveals Wolbachia as a dominant endosymbiont. Environ. Microbiol. 2022;24(3):1638–1652. doi: 10.1111/1462-2920.15948. PubMed DOI
Le Goff GJ, et al. Effect of the instar of the pear psyllid Cacopsylla pyri (Hemiptera: Psyllidae) on the behaviour and fitness of the parasitoid Trechnites insidiosus (Hymenoptera: Encyrtidae) Eur. J. Entomol. 2021;118:279–287. doi: 10.14411/eje.2021.028. DOI
Tougeron K, et al. Ecology and biology of the parasitoid Trechnites insidiosus and its potential for biological control of pear psyllids. Pest Manag. Sci. 2021;77(11):4836–47. doi: 10.1002/ps.6517. PubMed DOI
Dedeine F, Ahrens M, Calcaterra L, Shoemaker DD. Social parasitism in fire ants (Solenopsis spp.): A potential mechanism for interspecies transfer of Wolbachia. Mol. Ecol. 2005;14:1543–1548. doi: 10.1111/j.1365-294X.2005.02499.x. PubMed DOI
Gehrer L, Vorburger C. Parasitoids as vectors of facultative bacterial endosymbionts in aphids. Biol. Lett. 2012;8:613–615. doi: 10.1098/rsbl.2012.0144. PubMed DOI PMC
Mascarenhas RO, Prezotto LF, Perondini ALP, Marino CL, Selivon D. Wolbachia in guilds of Anastrepha fruit flies (Tephritidae) and parasitoid wasps (Braconidae) Genet. Mol. Biol. 2016;39:600–610. doi: 10.1590/1678-4685-gmb-2016-0075. PubMed DOI PMC
Ossiannilsson, F. The Psylloidea (Homoptera) of Fennoscandia and Denmark. (Brill, E.J., 1992).
Burckhardt, D. Psyllid-key of Cacopsylla on Rosaceae. https://www.dlr.rlp.de/Psylliden-english (2010).
Braig HR, Zhou W, Dobson SL, O’Neill SL. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J. Bacteriol. 1998;180:2373–2378. doi: 10.1128/JB.180.9.2373-2378.1998. PubMed DOI PMC
Baldo L, et al. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl. Environ. Microbiol. 2006;72:7098–7110. doi: 10.1128/AEM.00731-06. PubMed DOI PMC
Zhou W, Rousset F, O’Neill S. Phylogeny and PCR–based classification of Wolbachia strains using wsp gene sequences. Proc. R. Soc. Lond. B. 1998;265:509–515. doi: 10.1098/rspb.1998.0324. PubMed DOI PMC
Jeffries CL, et al. Diverse novel resident Wolbachia strains in Culicine mosquitoes from Madagascar. Sci. Rep. 2018;8(1):1–5. doi: 10.1038/s41598-018-35658-z. PubMed DOI PMC
Zimmermann, B. L., Bouchon, D., Almerão, M. P. & Araujo, P. B. Wolbachia in Neotropical terrestrial isopods. FEMS Microbiol. Ecol.91, (2015). PubMed
Kawasaki Y, Schuler H, Stauffer C, Lakatos F, Kajimura H. Wolbachia endosymbionts in haplodiploid and diploid scolytine beetles (Coleoptera: Curculionidae: Scolytinae): Wolbachia infection in scolytine beetles. Environ. Microbiol. Rep. 2016;8:680–688. doi: 10.1111/1758-2229.12425. PubMed DOI
Schuler H, et al. Wolbachia in parasitoids attacking native European and introduced Eastern cherry fruit flies in Europe. Environ. Entomoll. 2016;45:1424–1431. doi: 10.1093/ee/nvw137. PubMed DOI
Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molec. Biol. and Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. PubMed DOI PMC
Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res. 2018;3:124. doi: 10.12688/wellcomeopenres.14826.1. PubMed DOI PMC
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J. Molec. Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI
Katoh K, Rozewicki J, Yamada KD. MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Brief. Bioinform. 2019;20:1160–1166. doi: 10.1093/bib/bbx108. PubMed DOI PMC
Trifinopoulos J, Nguyen L-T, von Haeseler A, Minh BQ. W-IQ-TREE: A fast online phylogenetic tool for maximum likelihood analysis. Nucl. Acids Res. 2016;44:W232–W235. doi: 10.1093/nar/gkw256. PubMed DOI PMC
Ronquist F, et al. MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Syste. Biol. 2012;61:539–542. doi: 10.1093/sysbio/sys029. PubMed DOI PMC
Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: More models, new heuristics and parallel computing. Nat. Methods. 2012;9:772–772. doi: 10.1038/nmeth.2109. PubMed DOI PMC
Miller, M. A., Pfeiffer, W. & Schwartz, T. Creating the CIPRES science gateway for inference of large phylogenetic trees. In: 2010 Gateway Computing Environments Workshop (GCE) 1–8 (IEEE, 2010).
Letunic I, Bork P. Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucl. Acids Res. 2021;49:293–296. doi: 10.1093/nar/gkab301. PubMed DOI PMC
Le Clec’h W, et al. High virulence of Wolbachia after host switching: when autophagy hurts. PLoS Pathog. 2012;8(8):e1002844. doi: 10.1371/journal.ppat.1002844. PubMed DOI PMC
Fox J, Weisberg S. An R companion to applied regression. 3. Sage; 2019.
de Mendiburu, F. & Yaseen, M. Agricolae: statistical procedures for agricultural research. R package version 1.4.0. (2020).
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing (2021).
Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag; 2016.