Endosymbiont diversity in natural populations of Tetranychus mites is rapidly lost under laboratory conditions

Abstract

Although the diversity of bacterial endosymbionts in arthropods is well documented, whether and how such diversity is maintained remains an open question. We investigated the temporal changes occurring in the prevalence and composition of endosymbionts after transferring natural populations of Tetranychus spider mites from the field to the laboratory. These populations, belonging to three different Tetranychus species (T. urticae, T. ludeni and T. evansi) carried variable infection frequencies of Wolbachia, Cardinium, and Rickettsia. We report a rapid change of the infection status of these populations after only 6 months of laboratory rearing, with an apparent loss of Rickettsia and Cardinium, while Wolbachia apparently either reached fixation or was lost. We show that Wolbachia had variable effects on host longevity and fecundity, and induced variable levels of cytoplasmic incompatibility (CI) in each fully infected population, despite no sequence divergence in the markers used and full CI rescue between all populations. This suggests that such effects are largely dependent upon the host genotype. Subsequently, we used these data to parameterize a theoretical model for the invasion of CI-inducing symbionts in haplodiploids, which shows that symbiont effects are sufficient to explain their dynamics in the laboratory. This further suggests that symbiont diversity and prevalence in the field are likely maintained by environmental heterogeneity, which is reduced in the laboratory. Overall, this study highlights the lability of endosymbiont infections and draws attention to the limitations of laboratory studies to understand host–symbiont interactions in natural populations.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1
Fig. 2: Wolbachia effects on oviposition of T. urticae females.
Fig. 3: Summary of the development of T. urticae eggs and cytoplasmic incompatibility (CI) levels in intra-population crosses between Wolbachia-infected and uninfected mites.
Fig. 4: Summary of the development of T. urticae eggs and cytoplasmic incompatibility (CI) levels in inter-population crosses using Wolbachia-infected mites.
Fig. 5: Expected invasion of Wolbachia based on its phenotypic effects in each population.

Data availability

Full datasets have been deposited in the Dryad data repository (https://doi.org/10.5061/dryad.pk0p2ngjg).

References

  1. Ahmed MZ, Breinholt JW, Kawahara AY (2016) Evidence for common horizontal transmission of Wolbachia among butterflies and moths. BMC Evol Biol 16:118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 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

    Article  Google Scholar 

  5. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Beckmann JF, Ronau JA, Hochstrasser M (2017) A Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility. Nat Microbiol 2(5):17007

    Article  PubMed  PubMed Central  Google Scholar 

  9. Bleidorn C, Gerth M (2018) A critical re-evaluation of multilocus sequence typing (MLST) efforts in Wolbachia. FEMS Microbiol Ecol 94(1):fix163

  10. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bordenstein SR, Bordenstein SR (2011) Temperature affects the tripartite interactions between bacteriophage WO, Wolbachia, and cytoplasmic incompatibility. PLoS ONE 6(12):11

    Article  CAS  Google Scholar 

  12. Breeuwer JAJ (1997) Wolbachia and cytoplasmic incompatibility in the spider mites Tetranychus urticae and T. turkestani. Heredity 79:41–47

    Article  Google Scholar 

  13. 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

    Article  Google Scholar 

  14. Brown LD, Cai TT, DasGupta A (2001) Interval estimation for a binomial proportion. Stat Sci 16(2):101–117

    Google Scholar 

  15. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. 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

    Article  PubMed  PubMed Central  Google Scholar 

  17. 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

    Article  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. 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

    Article  PubMed  PubMed Central  Google Scholar 

  20. 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

    Article  PubMed  PubMed Central  Google Scholar 

  21. Crawley MJ (2007) The R book. John Wiley & Sons, Ltd, Chichester, England

    Google Scholar 

  22. Dobson SL, Marsland EJ, Rattanadechakul W (2002) Mutualistic Wolbachia infection in Aedes albopictus: accelerating cytoplasmic drive. Genetics 160(3):1087–1094

    PubMed  PubMed Central  Google Scholar 

  23. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Engelstadter J, Hurst GDD (2009) The ecology and evolution of microbes that manipulate host reproduction. Annu Rev Ecol Evol Syst 40:127–149

    Article  Google Scholar 

  25. Engelstadter J, Telschow A (2009) Cytoplasmic incompatibility and host population structure. Heredity 103(3):196–207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 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

    Article  PubMed  PubMed Central  Google Scholar 

  27. 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

    Article  Google Scholar 

  28. 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

    Article  PubMed  PubMed Central  Google Scholar 

  29. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Frago E, Dicke M, Godfray HCJ (2012) Insect symbionts as hidden players in insect-plant interactions. Trends Ecol Evol 27(12):705–711

    Article  PubMed  PubMed Central  Google Scholar 

  31. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 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

    Article  PubMed  PubMed Central  Google Scholar 

  33. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Gotoh T, Noda H, Ito S (2007a) Cardinium symbionts cause cytoplasmic incompatibility in spider mites. Heredity 98(1):13–20

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. 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

    Article  PubMed  PubMed Central  Google Scholar 

  36. Hamilton WD (1967) Extraordinary sex ratios. Science 156(3774):477–488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. 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

    Article  PubMed  PubMed Central  Google Scholar 

  38. Hancock PA, Godfray HCJ (2012) Modelling the spread of Wolbachia in spatially heterogeneous environments. J R Soc Interface 9(76):3045–3054

    Article  PubMed  PubMed Central  Google Scholar 

  39. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 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

    Article  PubMed  PubMed Central  Google Scholar 

  41. Hoffmann AA, Ross PA (2018) Rates and patterns of laboratory adaptation in (mostly) insects. J Econ Entomol 111(2):501–509

    Article  PubMed  PubMed Central  Google Scholar 

  42. Hoffmann AA, Turelli M, Harshman LG (1990) Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans. Genetics 126(4):933–948

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Hopkins SR, Wojdak JM, Belden LK (2017) Defensive symbionts mediate host-parasite interactions at multiple scales. Trends Parasitol 33(1):53–64

    Article  PubMed  PubMed Central  Google Scholar 

  44. Hurst LD, Atlan A, Bengtsson BO (1996) Genetic conflicts. Q Rev Biol 71(3):317–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. 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

    Article  CAS  Google Scholar 

  46. Jansen VAA, Turelli M, Godfray HCJ (2008) Stochastic spread of Wolbachia. Proc R Soc B 275(1652):2769–2776

    Article  PubMed  PubMed Central  Google Scholar 

  47. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Leftwich PT, Bolton M, Chapman T (2016) Evolutionary biology and genetic techniques for insect control. Evolut Appl 9(1):212–230

    Article  CAS  Google Scholar 

  51. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. 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

    Article  CAS  Google Scholar 

  53. 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

    Article  CAS  Google Scholar 

  54. 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

  55. 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

  56. 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

    Article  PubMed  PubMed Central  Google Scholar 

  57. Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. 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

    Article  Google Scholar 

  60. 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

    Article  Google Scholar 

  61. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. 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

    Article  Google Scholar 

  63. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  64. 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

    PubMed  PubMed Central  Google Scholar 

  65. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  67. 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

    Article  Google Scholar 

  68. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. 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

    Article  PubMed  PubMed Central  Google Scholar 

  70. 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

  71. 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

    Article  CAS  Google Scholar 

  72. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. 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

    Article  PubMed  PubMed Central  Google Scholar 

  74. 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

    Article  CAS  Google Scholar 

  75. 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

    Article  PubMed  PubMed Central  Google Scholar 

  76. 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

    Article  CAS  Google Scholar 

  77. 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

    Article  Google Scholar 

  78. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. 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

    Article  PubMed  PubMed Central  Google Scholar 

  80. Turelli M, Hoffmann AA (1995) Cytoplasmic incompatibility in Drosophila simulans—dynamics and parameter estimates from natural-populations. Genetics 140(4):1319–1338

    CAS  PubMed  PubMed Central  Google Scholar 

  81. Vala F, Van Opijnen T, Breeuwer JAJ, Sabelis MW (2003) Genetic conflicts over sex ratio: mite-endosymbiont interactions. Am Nat 161(2):254–266

    Article  PubMed  PubMed Central  Google Scholar 

  82. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. 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

    Article  PubMed  PubMed Central  Google Scholar 

  84. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. 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

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Vavre F, Fleury F, Varaldi J, Fouillet P, Bouletreau M (2002) Infection polymorphism and cytoplasmic incompatibility in Hymenoptera-Wolbachia associations. Heredity 88:361–365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. 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

    Article  Google Scholar 

  88. 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

    Article  Google Scholar 

  89. Werren JH, Beukeboom LW (1998) Sex determination, sex ratios, and genetic conflict. Annu Rev Ecol Syst 29:233–261

    Article  Google Scholar 

  90. 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

    Article  Google Scholar 

  91. 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

    Article  Google Scholar 

  92. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. 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

  95. 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

  96. Zélé F, Weill M, Magalhães S (2018c) Identification of spider-mite species and their endosymbionts using multiplex PCR. Exp Appl Acarol 74:123–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. 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

    Article  PubMed  PubMed Central  Google Scholar 

  100. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. 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

    Article  PubMed  PubMed Central  Google Scholar 

  102. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. 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

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We are grateful to Joaquin Calatayud, Salomé Clémente, Diogo Godinho and Leonor Rodrigues for their help in collecting data from the intra-population crosses; to André Alves, Catarina Bota, Jéssica Paulo, José Leitão, Andreia Oliveira and Luís Silva for the inter-population crosses. We also thank Patrick Makoundou for his attempts to amplify cidA and cidB gene fragments from T. urticae. Finally, we thank Olivier Duron, Inês Fragata, Michael Turelli and Filipa Vala for useful discussions and suggestions. This work was funded by an FCT-ANR project (FCT-ANR//BIA-EVF/0013/2012) to SM and Isabelle Olivieri, and by an FCT-Tubitak project (FCT-TUBITAK/0001/2014) to SM and Ibrahim Cakmak. FZ was funded through an FCT Post-Doc fellowship (SFRH/BPD/125020/2016). Funding agencies did not participate in the design or analysis of experiments.

Author information

Affiliations

Authors

Contributions

Designed the project: FZ and SM, with discussions with MM, MW and FV. Designed experiments: FZ, SM; population maintenance: IS; molecular analyses: FZ, MW; performed the experiments: FZ and IS; statistical analyses and model application: FZ; paper writing: FZ, FV and SM with input from all authors. All authors read and approved the final version of the manuscript.

Corresponding author

Correspondence to Flore Zélé.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zélé, F., Santos, I., Matos, M. et al. Endosymbiont diversity in natural populations of Tetranychus mites is rapidly lost under laboratory conditions. Heredity 124, 603–617 (2020). https://doi.org/10.1038/s41437-020-0297-9

Download citation

Search