
Ahmed MZ, Breinholt JW, Kawahara AY (2016) Evidence for common horizontal transmission of Wolbachia among butterflies and moths. BMC Evol Biol 16:118
Anbutsu H, Goto S, Fukatsu T (2008) High and low temperatures differently affect infection density and vertical transmission of male-killing Spiroplasma symbionts in Drosophila hosts. Appl Environ Microbiol 74(19):6053–6059
Atyame CM, Delsuc F, Pasteur N, Weill M, Duron O (2011) Diversification of Wolbachia endosymbiont in the Culex pipiens mosquito. Mol Biol Evol 28(10):2761–2772
Bakovic V, Schebeck M, Telschow A, Stauffer C, Schuler H (2018) Spatial spread of Wolbachia in Rhagoletis cerasi populations. Biol Lett 14(5):pii: 20180161
Baldo L, Hotopp JCD, Jolley KA, Bordenstein SR, Biber SA, Choudhury RR et al. (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 72(11):7098–7110
Ballard JWO, Melvin RG (2007) Tetracycline treatment influences mitochondrial metabolism and mtDNA density two generations after treatment in Drosophila. Insect Mol Biol 16(6):799–802
Barton NH, Turelli M (2011) Spatial waves of advance with bistable dynamics: cytoplasmic and genetic analogues of allee effects. Am Nat 178(3):E48–E75
Beckmann JF, Ronau JA, Hochstrasser M (2017) A Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat Microbiol 2(5):17007
Bleidorn C, Gerth M (2018) A critical re-evaluation of multilocus sequence typing (MLST) efforts in Wolbachia. FEMS Microbiol Ecol 94(1):fix163
Bonneau M, Atyame C, Beji M, Justy F, Cohen-Gonsaud M, Sicard M et al. (2018) Culex pipiens crossing type diversity is governed by an amplified and polymorphic operon of Wolbachia. Nat Commun 9:1491
Bordenstein SR, Bordenstein SR (2011) Temperature affects the tripartite interactions between bacteriophage WO, Wolbachia, and cytoplasmic incompatibility. PLoS ONE 6(12):11
Breeuwer JAJ (1997) Wolbachia and cytoplasmic incompatibility in the spider mites Tetranychus urticae and T. turkestani. Heredity 79:41–47
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A et al. (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9(2):378–400
Brown LD, Cai TT, DasGupta A (2001) Interval estimation for a binomial proportion. Stat Sci 16(2):101–117
Carrington LB, Hoffmann AA, Weeks AR (2010) Monitoring long-term evolutionary changes following Wolbachia introduction into a novel host: the Wolbachia popcorn infection in Drosophila simulans. Proc R Soc B 277(1690):2059–2068
Cass BN, Himler AG, Bondy EC, Bergen JE, Fung SK, Kelly SE et al. (2016) Conditional fitness benefits of the Rickettsia bacterial symbiont in an insect pest. Oecologia 180(1):169–179
Cattel J, Nikolouli K, Andrieux T, Martinez J, Jiggins F, Charlat S et al. (2018) Back and forth Wolbachia transfers reveal efficient strains to control spotted wing drosophila populations. J Appl Ecol 55(5):2408–2418
Clancy DJ, Hoffmann AA (1998) Environmental effects on cytoplasmic incompatibility and bacterial load in Wolbachia-infected Drosophila simulans. Entomol Exp Appl 86(1):13–24
Conner WR, Blaxter ML, Anfora G, Ometto L, Rota-Stabelli O, Turelli M (2017) Genome comparisons indicate recent transfer of wRi-like Wolbachia between sister species Drosophila suzukii and D. subpulchrella. Ecol Evol 7(22):9391–9404
Cooper BS, Ginsberg PS, Turelli M, Matute DR (2017) Wolbachia in the Drosophila yakuba complex: pervasive frequency variation and weak cytoplasmic incompatibility, but no apparent effect on reproductive isolation. Genetics 205(1):333–351
Crawley MJ (2007) The R book. John Wiley & Sons, Ltd, Chichester, England
Dobson SL, Marsland EJ, Rattanadechakul W (2002) Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160(3):1087–1094
Duron O, Bouchon D, Boutin S, Bellamy L, Zhou LQ, Engelstadter J et al. (2008) The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol 6:27
Engelstadter J, Hurst GDD (2009) The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst 40:127–149
Engelstadter J, Telschow A (2009) Cytoplasmic incompatibility and host population structure. Heredity 103(3):196–207
Enigl M, Schausberger P (2007) Incidence of the endosymbionts Wolbachia, Cardinium and Spiroplasma in phytoseiid mites and associated prey. Exp Appl Acarol 42(2):75–85
Ferguson LV, Dhakal P, Lebenzon JE, Heinrichs DE, Bucking C, Sinclair BJ (2018) Seasonal shifts in the insect gut microbiome are concurrent with changes in cold tolerance and immunity. Funct Ecol 32(10):2357–2368
Fragata I, Lopes-Cunha M, Barbaro M, Kellen B, Lima M, Faria GS et al. (2016) Keeping your options open: maintenance of thermal plasticity during adaptation to a stable environment. Evolution 70(1):195–206
Fragata I, Simoes P, Lopes-Cunha M, Lima M, Kellen B, Barbaro M et al. (2014) Laboratory selection quickly erases historical differentiation. PLoS ONE 9(5):e96227
Frago E, Dicke M, Godfray HCJ (2012) Insect symbionts as hidden players in insect-plant interactions. Trends Ecol Evol 27(12):705–711
Francuski L, Djurakic M, Ludoski J, Hurtado P, Perez-Banon C, Stahls G et al. (2014) Shift in phenotypic variation coupled with rapid loss of genetic diversity in captive populations of Eristalis tenax (Diptera: Syrphidae): consequences for rearing and potential commercial use. J Econ Entomol 107(2):821–832
Gibson CM, Hunter MS (2010) Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecol Lett 13(2):223–234
Gotoh T, Noda H, Hong XY (2003) Wolbachia distribution and cytoplasmic incompatibility based on a survey of 42 spider mite species (Acari: Tetranychidae) in Japan. Heredity 91(3):208–216
Gotoh T, Noda H, Ito S (2007a) Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 98(1):13–20
Gotoh T, Sugasawa J, Noda H, Kitashima Y (2007b) Wolbachia-induced cytoplasmic incompatibility in Japanese populations of Tetranychus urticae (Acari: Tetranychidae). Exp Appl Acarol 42(1):1–16
Hamilton WD (1967) Extraordinary sex ratios. Science 156(3774):477–488
Hamm CA, Begun DJ, Vo A, Smith CC, Saelao P, Shaver AO et al. (2014) Wolbachia do not live by reproductive manipulation alone: infection polymorphism in Drosophila suzukii and D. subpulchrella. Mol Ecol 23(19):4871–4885
Hancock PA, Godfray HCJ (2012) Modelling the spread of Wolbachia in spatially heterogeneous environments. J R Soc Interface 9(76):3045–3054
Hoffmann AA, Hallas R, Sinclair C, Partridge L (2001) Rapid loss of stress resistance in Drosophila melanogaster under adaptation to laboratory culture. Evolution 55(2):436–438
Hoffmann AA, Iturbe-Ormaetxe I, Callahan AG, Phillips B, Billington K, Axford JK et al. (2014) Stability of the wMel Wolbachia Infection following invasion into Aedes aegypti populations. PLoS Negl Trop Dis 8(9):e3115
Hoffmann AA, Ross PA (2018) Rates and patterns of laboratory adaptation in (mostly) insects. J Econ Entomol 111(2):501–509
Hoffmann AA, Turelli M, Harshman LG (1990) Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126(4):933–948
Hopkins SR, Wojdak JM, Belden LK (2017) Defensive symbionts mediate host-parasite interactions at multiple scales. Trends Parasitol 33(1):53–64
Hurst LD, Atlan A, Bengtsson BO (1996) Genetic conflicts. Q Rev Biol 71(3):317–364
Ishmael N, Hotopp JCD, Ioannidis P, Biber S, Sakamoto J, Siozios S et al. (2009) Extensive genomic diversity of closely related Wolbachia strains. Microbiol-Sgm 155:2211–2222
Jansen VAA, Turelli M, Godfray HCJ (2008) Stochastic spread of Wolbachia. Proc R Soc B 275(1652):2769–2776
Kaur R, Siozios S, Miller WJ, Rota-Stabelli O (2017) Insertion sequence polymorphism and genomic rearrangements uncover hidden Wolbachia diversity in Drosophila suzukii and D. subpulchrella. Sci Rep 7(1):14815
Keller GP, Windsor DM, Saucedo JM, Werren JH (2004) Reproductive effects and geographical distributions of two Wolbachia strains infecting the Neotropical beetle, Chelymorpha alternans Boh. (Chrysomelidae, Cassidinae). Mol Ecol 13(8):2405–2420
Kriesner P, Hoffmann AA, Lee SF, Turelli M, Weeks AR (2013) Rapid sequential spread of two Wolbachia variants in Drosophila simulans. PLoS Pathog 9(9):e1003607
Leftwich PT, Bolton M, Chapman T (2016) Evolutionary biology and genetic techniques for insect control. Evolut Appl 9(1):212–230
LePage DP, Metcalf JA, Bordenstein SR, On JM, Perlmutter JI, Shropshire JD et al. (2017) Prophage WO genes recapitulate and enhance Wolbachia-induced cytoplasmic incompatibility. Nature 543(7644):243–247
Lindsey ARI, Rice DW, Bordenstein SR, Brooks AW, Bordenstein SR, Newton ILG (2018) Evolutionary genetics of cytoplasmic incompatibility genes cifA and cifB in prophage WO of Wolbachia. Genome Biol Evolution 10(2):434–451
Liu Y, Miao H, Hong XY (2006) Distribution of the endosymbiotic bacterium Cardinium in Chinese populations of the carmine spider mite Tetranychus cinnabarinus (Acari: Tetranychidae). J Appl Entomol 130(9–10):523–529
Macke E, Magalhães S, Bach F, Olivieri I (2011) Experimental evolution of reduced sex ratio adjustment under local mate competition. Science 334(6059):1127–1129
Matos M, Simões P, Santos MA, Seabra SG, Faria GS, Vala F et al. (2015) History, chance and selection during phenotypic and genomic experimental evolution: replaying the tape of life at different levels. Front Genet 6:71
Mercot H, Charlat S (2004) Wolbachia infections in Drosophila melanogaster and D. simulans: polymorphism and levels of cytoplasmic incompatibility. Genetica 120(1–3):51–59
Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190
Narita S, Nomura M, Kageyama D (2007) Naturally occurring single and double infection with Wolbachia strains in the butterfly Eurema hecabe: transmission efficiencies and population density dynamics of each Wolbachia strain. FEMS Microbiol Ecol 61(2):235–245
Nguyen TH, Le Nguyen H, Nguyen TY, Vu SN, Tran ND, Le TN et al. (2015) Field evaluation of the establishment potential of wMelPop Wolbachia in Australia and Vietnam for dengue control. Parasite Vector 8:563
Oliver KM, Smith AH, Russell JA (2014) Defensive symbiosis in the real world -advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct Ecol 28(2):341–355
Perlman SJ, Kelly SE, Hunter MS (2008) Population biology of cytoplasmic incompatibility: maintenance and spread of Cardinium symbionts in a parasitic wasp. Genetics 178(2):1003–1011
Perrot-Minnot MJ, Cheval B, Migeon A, Navajas M (2002) Contrasting effects of Wolbachia on cytoplasmic incompatibility and fecundity in the haplodiploid mite Tetranychus urticae. J Evol Biol 15(5):808–817
Poinsot D, Bourtzis K, Markakis G, Savakis C, Mercot H (1998) Wolbachia transfer from Drosophila melanogaster into D. simulans: Host effect and cytoplasmic incompatibility relationships. Genetics 150(1):227–237
Rasgon JL, Scott TW (2003) Wolbachia and cytoplasmic incompatibility in the california Culex pipiens mosquito species complex: Parameter estimates and infection dynamics in natural populations. Genetics 165(4):2029–2038
Raychoudhury R, Baldo L, Oliveira D, Werren JH (2009) Modes of acquisition of Wolbachia: horizontal transfer, hybrid introgression, and codivergence in the Nasonia species complex. Evolution 63(1):165–183
Reuter M, Lehmann L, Guillaume F (2008) The spread of incompatibility-inducing parasites in sub-divided host populations. BMC Evol Biol 8:134
Reynolds KT, Hoffmann AA (2002) Male age, host effects and the weak expression or nonexpression of cytoplasmic incompatibility in Drosophila strains infected by maternally transmitted Wolbachia. Genetical Res 80(2):79–87
Ros VID, Breeuwer JAJ (2009) The effects of, and interactions between, Cardinium and Wolbachia in the doubly infected spider mite Bryobia sarothamni. Heredity 102(4):413–422
Ros VID, Fleming VM, Feil EJ, Breeuwer JAJ (2012) Diversity and recombination in Wolbachia and Cardinium from Bryobia spider mites. BMC Microbiol 12(Suppl 1):S13
Ross PA, Axford JK, Richardson KM, Endersby-Harshman NM, Hoffmann AA (2017a) Maintaining Aedes aegypti mosquitoes infected with Wolbachia. J Vis Exp (126):e56124. https://doi.org/10.3791/56124
Ross PA, Wiwatanaratanabutr I, Axford JK, White VL, Endersby-Harshman NM, Hoffmann AA (2017b) Wolbachia infections in Aedes aegypti differ markedly in their response to cyclical heat stress. PLoS Pathog 13(1):17
Schmidt TL, Barton NH, Rasic G, Turley AP, Montgomery BL, Iturbe-Ormaetxe I et al. (2017) Local introduction and heterogeneous spatial spread of dengue-suppressing Wolbachia through an urban population of Aedes aegypti. PLoS Biol 15(5):e2001894
Sousa V, Zélé F, Rodrigues LR, Godinho DP, Charlery M, Magalhães S (2019) Rapid host-plant adaptation in the herbivorous spider mite Tetranychus urticae occurs at low cost. Curr Opin Insect Sci 36:82–89
Staudacher H, Schimmel BCJ, Lamers MM, Wybouw N, Groot AT, Kant MR (2017) Independent effects of a herbivore’s bacterial symbionts on its performance and induced plant defences. Int J Mol Sci 18(1):182
Suh E, Sim C, Park J-J, Cho K (2015) Inter-population variation for Wolbachia induced reproductive incompatibility in the haplodiploid mite Tetranychus urticae. Exp Appl Acarol 65(1):55–71
Sumi T, Miura K, Miyatake T (2017) Wolbachia density changes seasonally amongst populations of the pale grass blue butterfly, Zizeeria maha (Lepidoptera: Lycaenidae). PLoS ONE 12(4):10
Sun JX, Guo Y, Zhang X, Zhu WC, Chen YT, Hong XY (2016) Effects of host interaction with Wolbachia on cytoplasmic incompatibility in the two-spotted spider mite Tetranychus urticae. Biol J Linn Soc 119(1):145–157
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(10):2731–2739
Toju H, Fukatsu T (2011) Diversity and infection prevalence of endosymbionts in natural populations of the chestnut weevil: relevance of local climate and host plants. Mol Ecol 20(4):853–868
Turelli M, Hoffmann AA (1995) Cytoplasmic incompatibility in Drosophila simulans—dynamics and parameter estimates from natural-populations. Genetics 140(4):1319–1338
Vala F, Van Opijnen T, Breeuwer JAJ, Sabelis MW (2003) Genetic conflicts over sex ratio: mite-endosymbiont interactions. Am Nat 161(2):254–266
Vala F, Weeks A, Claessen D, Breeuwer JAJ, Sabelis MW (2002) Within- and between-population variation for Wolbachia-induced reproductive incompatibility in a haplodiploid mite. Evolution 56(7):1331–1339
Van Opijnen T, Breeuwer JAJ (1999) High temperatures eliminate Wolbachia, a cytoplasmic incompatibility inducing endosymbiont, from the two-spotted spider mite. Exp Appl Acarol 23(11):871–881
Vavre F, Fleury F, Lepetit D, Fouillet P, Bouletreau M (1999) Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol Biol Evol 16(12):1711–1723
Vavre F, Fleury F, Varaldi J, Fouillet P, Bouletreau M (2000) Evidence for female mortality in Wolbachia-mediated cytoplasmic incompatibility in haplodiploid insects: epidemiologic and evolutionary consequences. Evolution 54(1):191–200
Vavre F, Fleury F, Varaldi J, Fouillet P, Bouletreau M (2002) Infection polymorphism and cytoplasmic incompatibility in Hymenoptera-Wolbachia associations. Heredity 88:361–365
Weeks AR, Reynolds KT, Hoffmann AA, Mann H (2002) Wolbachia dynamics and host effects: what has (and has not) been demonstrated? Trends Ecol Evol 17(6):257–262
Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ (2015) The incidence of bacterial endosymbionts in terrestrial arthropods. Proc R Soc Lond 282(1807):20150249
Werren JH, Beukeboom LW (1998) Sex determination, sex ratios, and genetic conflict. Annu Rev Ecol Syst 29:233–261
Xie RR, Chen XL, Hong XY (2011) Variable fitness and reproductive effects of Wolbachia infection in populations of the two-spotted spider mite Tetranychus urticae Koch in China. Appl Entomol Zool 46(1):95–102
Xie RR, Zhou LL, Zhao ZJ, Hong XY (2010) Male age influences the strength of Cardinium-induced cytoplasmic incompatibility expression in the carmine spider mite Tetranychus cinnabarinus. Appl Entomol Zool 45(3):417–423
Yu MZ, Zhang KJ, Xue XF, Hong XY (2011) Effects of Wolbachia on mtDNA variation and evolution in natural populations of Tetranychus urticae Koch. Insect Mol Biol 20(3):311–321
Zeh JA, Bonilla MM, Adrian AJ, Mesfin S, Zeh DW (2012) From father to son: transgenerational effect of tetracycline on sperm viability. Sci Rep 2:375
Zélé F, Santos I, Olivieri I, Weill M, Duron O, Magalhães S (2018a) Endosymbiont diversity and prevalence in herbivorous spider mite populations in South-Western Europe. FEMS Microbiol Ecol 94(4):fiy015
Zélé F, Santos JL, Godinho DP, Magalhães S (2018b) Wolbachia both aids and hampers the performance of spider mites on different host plants. FEMS Microbiol Ecol 94(12):fiy187
Zélé F, Weill M, Magalhães S (2018c) Identification of spider-mite species and their endosymbionts using multiplex PCR. Exp Appl Acarol 74:123–138
Zhang YK, Chen YT, Yang K, Qiao GX, Hong XY (2016) Screening of spider mites (Acari: Tetranychidae) for reproductive endosymbionts reveals links between co-infection and evolutionary history. Sci Rep 6:27900
Zhang YK, Ding XL, Zhang KJ, Hong XY (2013a) Wolbachia play an important role in affecting mtDNA variation of Tetranychus truncatus (Trombidiformes: Tetranychidae). Environ Entomol 42(6):1240–1245
Zhang YK, Zhang KJ, Sun JT, Yang XM, Ge C, Hong XY (2013b) Diversity of Wolbachia in natural populations of spider mites (genus Tetranychus): Evidence for complex infection history and disequilibrium distribution. Microb Ecol 65(3):731–739
Zhao DX, Chen DS, Ge C, Gotoh T, Hong XY (2013a) Multiple infections with Cardinium and two strains of Wolbachia in the spider mite Tetranychus phaselus Ehara: revealing new forces driving the spread of Wolbachia. PLoS ONE 8(1):e54964
Zhao DX, Zhang XF, Hong XY (2013b) Host-symbiont interactions in spider mite Tetranychus truncates doubly infected with Wolbachia and Cardinium. Environ Entomol 42(3):445–452
Zhu LY, Zhang KJ, Zhang YK, Ge C, Gotoh T, Hong XY (2012) Wolbachia strengthens Cardinium-induced cytoplasmic incompatibility in the spider mite Tetranychus piercei McGregor. Curr Microbiol 65(5):516–523
Zhu Y-X, Song Y-L, Zhang Y-K, Hoffmann AA, Zhou J-C, Sun J-T et al. (2018) Incidence of facultative bacterial endosymbionts in spider mites associated with local environment and host plant. Appl Environ Microbiol 84(6):e02546–02517
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