ФИЗИОЛОГИЧЕСКИЕ АСПЕКТЫ ВЗАИМООТНОШЕНИЙ WOLBACHIA PIPIENTIS–DROSOPHILA MELANOGASTER
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Ключевые слова

Wolbachia
Drosophila melanogaster
симбиоз
приспособленность
эндокринология насекомых

Аннотация

Внутриклеточная бактерия Wolbachia pipientis является одним из самых распространенных прокариотических симбионтов беспозвоночных. Известно, что она способна влиять на репродуктивную функцию вида-хозяина, что способствует распространению бактерии в его популяциях за счет увеличения численности зараженных самок. Но если основные эффекты Wolbachia достаточно хорошо описаны, то механизмы вызываемых ею репродуктивных аномалий и позитивного влияния на приспособленность хозяина, остаются в значительной степени малоизученными. Данный обзор посвящен обсуждению различных аспектов влияния Wolbachia на физиологию и приспособленность хозяина. Детально рассматривается симбиотическая система Wolbachia pipientis – Drosophila melanogaster, в том числе – влияние бактерии на гормональный статус хозяина и его устойчивость к различным видам стресса и вирусам, плодовитость и продолжительность жизни.

https://doi.org/10.31857/S0044452922020024
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Литература

Hertig M (1936) The Rickettsia, Wolbachia pipientis (gen. et sp.n.) and associated inclusions of the mosquito, Culex pipiens. Parasitology 28(4): 453–486. https://doi.org/10.1017/S0031182000022666

Kriesner P, Conner WR, Weeks AR, Turelli M, Hoffmann AA (2016) Persistence of a Wolbachia infection frequency cline in Drosophila melanogaster and the possible role of reproductive dormancy. Evolution 70(5):979–997. doi: 10.1111/evo.12923

Dobson SL, Bourtzis K, Braig HR, Jones BF, Zhou W, Rousset F, O'Neill SL (1999) Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem Molec Biol 29(2):153–160. doi: 10.1016/s0965-1748(98)00119-2

Stouthamer R, Breeuwer JA, Hurst GD 1999 Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53:71–102. doi: 10.1146/annurev.micro.53.1.71

Werren, JH, Baldo L, Clark ME (2008) Wolbachia: Master manipulators of invertebrate biology. Nat Rev Microbiol 6(10):741–751. https://doi.org/10.1038/nrmicro1969

Hoffmann AA, Turelli M (1997) Cytoplasmic incompatibility in insects. In: O’Neill S, Hoffmann AA, Werren JH, editors. Influential passengers: Inherited microorganisms and arthropod reproduction. Oxford: Oxford University Press. 42–80.

Sinkins, SP, Walker T, Lynd AR, Steven AR, Makepeace BL, Godfray HC, Parkhill J (2005) Wolbachia variability and host effects on crossing type in Culex mosquitoes. Nature 436(7048):257–260. doi: 10.1038/nature03629

Clark ME, Veneti Z, Bourtzis K, Karr TL (2003) Wolbachia distribution and cytoplasmic incompatibility during sperm development: The cyst as the basic cellular unit of CI expression. Mech Dev 120(2):185–198. doi: 10.1016/s0925-4773(02)00424-0

Veneti Z, Clark ME, Zabalou S, Karr TL, Savakis C, Bourtzis K (2003) Cytoplasmic incompatibility and sperm cyst infection in different Drosophila-Wolbachia associations. Genetics 164(2):545–552. doi: 10.1093/genetics/164.2.545

Pinto SB, Stainton K, Harris S, Kambris Z, Sutton ER, Bonsall MB, Parkhill J, Sinkins SP (2013) Transcriptional regulation of Culex pipiens mosquitoes by Wolbachia influences cytoplasmic incompatibility. PLoS Pathog 9(10):e1003647. https://doi.org/10.1371/journal.ppat.1003647

Boyle L, O’Neill SL, Robertson HM, Karr TL (1993) Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260(5115):1796–1799. doi: 10.1126/science.8511587

Bourtzis K, Nirgianaki A, Markakis G, Savakis C (1996) Wolbachia infection and cytoplasmic incompatibility in Drosophila species. Genetics 144(3):1063–1073. doi: 10.1093/genetics/144.3.1063

Noda H, Koizumi Y, Zhang Q, Deng K (2001) Infection density of Wolbachia and incompatibility level in two planthopper species, Laodelphax striatellus and Sogatella furcifera. IBMB 31(6-7):727–737. doi: 10.1016/s0965-1748(00)00180-6

Noda H, Miyoshi T, Zhang Q, Watanabe K, Deng K, Hoshizaki S (2001) Wolbachia infection shared among planthoppers (Homoptera: Delphacidae) and their endoparasite (Strepsiptera: Elenchidae): A probable case of interspecies transmission. Mol Ecol 10(8):2101–2106. doi: 10.1046/j.0962-1083.2001.01334.x

McGraw EA, Merritt DJ, Droller JN, O’Neill SL (2002) Wolbachia density and virulence attenuation after transfer into a novel host. Proc Natl Acad Sci U S A 99(5):2918–2923. doi: 10.1073/pnas.052466499

Lu P, Bian G, Pan X, Xi Z (2012) Wolbachia induces density-dependent inhibition to Dengue Virus in mosquito cells. PLoS Negl Trop Dis 6(7):e1754. doi: 10.1371/journal.pntd.0001754

Early AM, Clark AG (2013) Monophyly of Wolbachia pipientis genomes within Drosophila melanogaster: Geographic structuring, titre variation and host effects across five populations. Mol Ecol 22(23):5765–5778. doi: 10.1111/mec.12530

Osborne SE, Iturbe-Ormaetxe I, Brownlie JC, O’Neill SL, Johnson KN (2012) Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Appl Environ Microbiol 78(19):6922–6929. doi: 10.1128/AEM.01727-12

Martinez J, Ok S, Smith S, Snoeck K, Day JP, Jiggins FM (2015) Should symbionts be nice or selfish? Antiviral effects of Wolbachia are costly but reproductive parasitism is not. PLoS Pathog 11(7): e1005021. doi: 10.1371/journal.ppat.1005021

Detcharoen M, Arthofer W, Jiggins FM, Steiner FM, Schlick-Steiner BC (2020) Wolbachia affect behavior and possibly reproductive compatibility but not thermoresistance, fecundity, and morphology in a novel transinfected host, Drosophila nigrosparsa. Ecol Evol 10:4457–4470. doi: 10.1002/ece3.6212

Moghadam, NN, Thorshauge PM, Kristensen TN, de Jonge N, Bahrndorff S, Kjeldal H, Nielsen JL (2018) Strong responses of Drosophila melanogaster microbiota to developmental temperature. Fly 12(1):1–12. doi: 10.1080/19336934.2017.1394558

Hurst GDD, Johnson AP, Schulenburg JHG, Fuyama Y (2000) Male-killing Wolbachia in Drosophila: a temperature-sensitive trait with a threshold bacterial density. Genetics 156(2):699–709. https://doi.org/10.1093/genetics/156.2.699

Serbus LR, White PM, Silva JP, Rabe A, Teixeira L, Albertson R, Sullivan W (2015) The impact of host diet on Wolbachia titer in Drosophila. PLoS Pathog 11(3):e1004777. doi: 10.1371/journal.ppat.1004777

Chrostek E, Teixeira L (2015) Mutualism breakdown by amplification of Wolbachia genes. PLoS Biol 13(2):e1002065. https://doi.org/10.1371/journal.pbio.1002065

Yamada R, Floate KD, Riegler M, O’Neill SL (2007) Male development time influences the strength of Wolbachia induced cytoplasmic incompatibility expression in Drosophila melanogaster. Genetics 177(2):801–808. doi: 10.1534/genetics.106.068486

Unckless RL, Boelio LM, Herren JK, Jaenike J (2009) Wolbachia as populations within individual insects: Causes and consequences of density variation in natural populations. Proc Biol Sci 276(1668):2805–2811. doi: 10.1098/rspb.2009.0287

Tortosa P, Charlat S, Labbé P, Dehecq JS, Barré H, Weill M (2010) Wolbachia age-sex-specific density in Aedes albopictus: A host evolutionary response to cytoplasmic incompatibility? PLoS One 5(3):e9700. doi: 10.1371/journal.pone.0009700

Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J, Jiggins FM, Teixeira L (2013) Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: A phenotypic and phylogenomic analysis. PLoS Genetics 9(12):e1003896. doi: 10.1371/journal.pgen.1003896

Zhao R, Xuan Y, Li X, Xi R (2008) Age-related changes of germline stem cell activity, niche signaling activity and egg production in Drosophila. Aging Cell 7(3):344–354. doi: 10.1111/j.1474-9726.2008.00379.x

Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42(1):587–609. doi: 10.1146/annurev.ento.42.1.587

Frydman, HM, Li JM, Robson DN, Wieschaus E (2006) Somatic stem cell niche tropism in Wolbachia. Nature 441(7092):509–512. doi: 10.1038/nature04756

Ote M, Yamamoto D (2020) Impact of Wolbachia infection on Drosophila female germline stem cells. Curr Opin Insect Sci 37:8–15. https://doi.org/10.1016/j.cois.2019.10.001

Guo Y, Hoffmann AA, Xu XQ, Zhang X, Huang HJ, Ju JF, Gong JT, Hong XY (2018) Wolbachia-induced apoptosis associated with increased fecundity in Laodelphax striatellus (Hemiptera: Delphacidae). Insect Mol Biol 27(6):796–807. doi: 10.1111/imb.12518

Okayama K, Katsuki M, Sumida Y, Okada K (2016) Costs and benefits of symbiosis between a bean beetle and Wolbachia. Animal Behaviour 119:19–26. https://doi.org/10.1016/j.anbehav.2016.07.004

Teixeira L, Ferreira Á, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6(12):e2. https://doi.org/10.1371/journal.pbio.1000002

Hedges LM, Brownlie JC, O'Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322(5902):702. https://doi.org/10.1126/science.1162418

Osborne SE, San Leong Y, O’Neill SL, Johnson KN (2009) Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog 5(11):e1000656. https://doi.org/10.1371/journal.ppat.1000656

Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT, Hedges LM, Rocha BC, Hall-Mendelin S, Day A, Riegler M, Hugo LE, Johnson KN, Kay BH, McGraw EA, van den Hurk AF, Ryan PA, O'Neill SL (2009) Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139(7):1268–1278. https://doi.org/10.1016/j.cell.2009.11.042

Johnson KN (2015) Bacteria and antiviral immunity in insects. Curr Opin Insect Sci 8:97–103. https://doi.org/10.1016/j.cois.2015.01.008

Glaser RL Meola MA (2010) The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS ONE 5:e11977. https://doi.org/10.1371/journal.-pone.0011977

van den Hurk, AF, Hall-Mendelin S, Pyke AT, Frentiu F D, McElroy K, Day A, Higgs S, O'Neill SL (2012) Impact of Wolbachia on infection with Chikungunya and Yellow Fever Viruses in the mosquito vector Aedes aegypti. PLOS Negl Trop Dis 6(11):e1892. https://doi.org/10.1371/journal.pntd.0001892

Braquart-Varnier C, Lachat M., Herbinière J, Johnson M, Caubet Y, Bouchon D, Sicard M 2008 Wolbachia mediate variation of host immunocompetence, PLoS One 3(9):e3286. https://doi.org/10.1371/journal.pone.0003286

Martinez J, Longdon B, Bauer S, Chan YS, Miller WJ, Bourtzis K, Teixeira L, Jiggins FM (2014) Symbionts commonly provide broad spectrum resistance to viruses ininsects: a comparative analysis of Wolbachia strains. PloS Pathog 10:e1004369. doi: 10.1371/journal.ppat.1004369

Chrostek E, Martins NE, Marialva MS, Teixeira L (2020) Wolbachia-conferred antiviral protection is determined by developmental temperature. mBio 12(5):e0292320. https://doi.org/10.1101/2020.06.24.169169

Pan X, Zhou G, Wu J, Bian G, Lu P, Raikhel AS, Xi Z (2012) Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. Proc Natl Acad Sci U S A 109(1):E23–E31. https://doi.org/10.1073/pnas.1116932108

McMeniman CJ, Lana RV, Cass BN, Fong AWC, Sidhu M, Wang YF, O'Neill SL (2009) Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 323(5910):141–144. doi: 10.1126/science.1165326

Hussain M, Frentiu FD, Moreira LA, O'Neill SL, Asgari S (2011) Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti. Proc Natl Acad Sci U S A 108(22):9250–9255. https://doi.org/10.1073/pnas.1105469108

Zhang G, Hussain M, O'Neill SL, Asgari S (2013) Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti. Proc Natl Acad Sci U S A 110(25):10276–10281. doi: 10.1073/pnas.1303603110

Pimentel AC, Cesar CS, Martins M, Cogni R (2021) The antiviral effects of the symbiont bacteria Wolbachia in insects. Front immunol 11:626329. https://doi.org/10.3389/fimmu.2020.626329

Martinez J, Tolosana I, Ok S, Smith S, Snoeck K, Day JP, Jiggins FM (2017) Symbiont strain is the main determinant of variation in Wolbachia-mediated protection against viruses across Drosophila species. Mol Ecol 26:4072–4084. https://doi.org/10.1111/mec.14164

Graham RI, Grzywacz D, Mushobozi WL, Wilson K (2012) Wolbachia in a major African crop pest increases susceptibility toviral disease rather than protects. Ecol Lett 15:993–1000. https://doi.org/10.1111/j.1461-0248.2012.01820.x

Александров ИД, Александрова МВ, Горячева ИИ, Рощина НВ, Шайкевич ЕВ, Захаров ИА (2007) Удаление эндосимбионта Wolbachia специфически снижает конкурентоспособность и продолжительность жизни самок и конкурентоспособность мух лабораторной линии Drosophila melanogaster. Генетика 43(10):1372–1378. [Alexandrov ID, Alexandrova MV, Goryacheva II, Rochina NV, Shaikevich EV, Zakharov IA (2007) Removing endosymbiotic Wolbachia specifically decreases lifespan of females and competitiveness in a laboratory strain of Drosophila melanogaster. Genetika 43(10):1147–1152. (In Russ)]. https://doi.org/10.1134/S1022795407100080

Вайсман НЯ, Илинский ЮЮ, Голубовский МД (2009) Популяционно-генетический анализ продолжительности жизни Drosophila melanogaster: сходные эффекты эндосимбионта Wolbachia и опухолевого супрессора lgl в условиях температурного стресса. ЖОБ 70(5):438–447. [Vaĭsman NI, Ilinskiĭ II, Golubovskiĭ MD (2009) Population genetic analysis of D. melanogaster longevity: Similar effects of endosymbiont Wolbachia and tumor suppressor Igl under conditions of temperature stress. Zh Obshch Biol 70(5):438–447. (In Russ)].

Min KT, Benzer S (1997) Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci U S A 94(20):10792–10796. https://doi.org/10.1073/pnas.94.20.10792

Strunov AA, Ilinskii YY, Zakharov IK, Kiseleva EV (2013) Effect of high temperature on survival of Drosophila melanogaster infected with pathogenic strain of Wolbachia bacteria. Russ J Genet: Applied Research 3(6):435–443. doi:10.1134/S2079059713060099

Fry AJ, Rand DM (2002) Wolbachia interactions that determine Drosophila melanogaster survival. Evolution 56(10):1976–1981. https://doi.org/10.1111/j.0014-3820.2002.tb00123.x

Fry AJ, Palmer MR, Rand DM (2004) Variable fitness effects of Wolbachia infection in Drosophila melanogaster. Heredity 93(4):379–389. doi: 10.1038/sj.hdy.6800514

Libert S, Chao Y, Chu X, Pletcher SD (2006) Trade-offs between longevity and pathogen resistance in Drosophila melanogaster are mediated by NFkappaB signaling. Aging Cell 5(6):533–543. doi: 10.1111/j.1474-9726.2006.00251.x

Pragya P, Shukla AK, Murthy RC, Abdin MZ, Kar Chowdhuri D (2014) Over-expression of superoxide dismutase ameliorates Cr(VI) induced adverse effects via modulating cellular immune system of Drosophila melanogaster. PLoS ONE 9(2):e88181. https://doi.org/10.1371/journal.pone.0088181

Capobianco F, Nandkumar S, Parker JD (2018) Wolbachia affects survival to different oxidative stressors dependent upon the genetic background in Drosophila melanogaster. Physiol Entomol 43:239–244. https://doi.org/10.1111/phen.12252

Hosamani R, Muralidhara (2013) Acute exposure of Drosophila melanogaster to paraquat causes oxidative stress and mitochondrial dysfunction. Arch Insect Biochem Physiol 83(1):25–40. https://doi.org/10.1002/arch.21094

Palmer RM, Rees DD, Ashton DS, Moncada S (1988) L-arginine is the physiological precursor for the formation of nitric oxide in endothelium-dependent relaxation. Biochem Biophys Res Commun 153(3):1251–1256. https://doi.org/10.1016/s0006-291x(88)81362-7.

Luckhart S, Vodovotz Y, Ciu L, Rosenberg R (1998) The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc Natl Acad Sci U S A 95(10):5700–5705. https://doi.org/10.1073/pnas.95.10.5700

Kraaijeveld AR, Elrayes NP, Schuppe H, Newland PL (2011) L-arginine enhances immunity to parasitoids in Drosophila melanogaster and increases NO production in lamellocytes. Dev Comp Immunol 35(8):857–864. https://doi.org/10.1016/j.dci.2011.03.019

Bruckdorfer R (2005) The basics about nitric oxide. Mol Aspects Med 26(1-2):3–31. https://doi.org/10.1016/j.mam.2004.09.002

Serga SV, Maistrenko OM, Rozhok AI, Mousseau TA, Kozeretska IA (2014) Fecundity as one of possible factors contributing to the dominance of the wMel genotype of Wolbachia in natural populations of Drosophila melanogaster. Symbiosis 63(1):11–17. https://doi.org/10.1007/s13199-014-0283-1

Gruntenko NE, Ilinsky YY, Adonyeva NV, Burdina EV, Bykov RA, Menshanov PN, Rauschenbach IY (2017) Various Wolbachia genotypes differently influence host Drosophila dopamine metabolism and survival under heat stress conditions. BMC Evol Biol 17(2):252. https://doi.org/10.1186/s12862-017-1104-y

Gruntenko NE, Karpova EK, Adonyeva NV, Andreenkova OV, Burdina EV, Ilinsky YY, Bykov RA, Menshanov PN, Rauschenbach IY (2019) Drosophila female fertility and juvenile hormone metabolism depends on the type of Wolbachia infection. J Exp Biol 222(4):jeb195347. https://doi.org/10.1242/jeb.195347

Rauschenbach IY, Adonyeva NV, Karpova EK, Ilinsky YY, Gruntenko NE (2018) Effect of gonadotropic hormones on stress resistance of Drosophila melanogaster females infected with different Wolbachia pipientis genotypes. Russ J Genet 54(7):871–873. https://doi.org/10.1134/S1022795418070128

Burdina EV, Bykov RA, Menshanov PN, Ilinsky YY, Gruntenko NЕ (2021) Unique Wolbachia strain wMelPlus increases heat stress resistance in Drosophila melanogaster. Arch Insect Biochem Physiol 106(4):e21776. https://doi.org/10.1002/arch.21776

Brownlie JC, Cass BN, Riegler M, Witsenburg JJ, Iturbe-Ormaetxe I, McGraw EA, O’Neill SL (2009) Evidence for metabolic provisioning by a common invertebrate endosymbiont, Wolbachia pipientis, during periods of nutritional stress. PLoS Pathog 5(4):e1000368. doi: 10.1371/journal.ppat.1000368

Kremer N, Voronin D, Charif D, Mavingui P, Mollereau B, Vavre F (2009) Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog 5(10):e1000630. doi: 10.1371/journal.ppat.1000630

Hosokawa T, Koga R, Kikuchi Y, Meng X Y, Fukatsu T (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci U S A 107(2):769–774. doi: 10.1073/pnas.09114 76107

Koukou K, Pavlikaki H, Kilias G, Werren JH, Bourtzis K, Alahiotis SN (2006) Influence of antibiotic treatment and Wolbachia curing on sexual isolation among Drosophila melanogaster cage populations. Evolution 60(1):87–96. doi: 10.1554/05-374.1

Miller WJ, Ehrman L, Schneider D (2010) Infectious speciation revisited: Impact of symbiont-depletion on female fitness and mating behavior of Drosophila paulistorum. PLoS Path 6(12):e1001214. doi: 10.1371/journal.ppat.1001214

Пантелеев ДЮ, Горячева ИИ, Андрианов БВ, Резник НЛ, Лазебный ОЕ, Куликов АМ (2007) Эндосимбиотическая бактерия Wolbachia повышает неспецифическую устойчивость к энтомопатогенам и изменяет поведение Drosophila melanogastrer. Генетика 43(9):1277–1280. [Panteleev DY, Goryacheva II, Andrianov BV, Reznik NL, Lazebny OE, Kulikov AM (2007) The endosymbiotic bacterium Wolbachia enhances the nonspecific resistance to insect pathogens and alters behavior of Drosophila melanogaster. Genetika 43(9):1277–1280. (In Russ)].

Okayama K, Katsuki M, Sumida Y, Okada K (2016) Costs and benefits of symbiosis between a bean beetle and Wolbachia. Animal Behaviour 119(19–26). https://doi.org/10.1016/j.anbehav.2016.07.004

Evans O, Caragata EP, McMeniman CJ, Woolfit M, Green DC, Williams CR, Franklin CE, O'Neill SL, McGraw EA (2009) Increased locomotor activity and metabolism of Aedes aegypti infected with a life-shortening strain of Wolbachia pipientis. J Exp Biol 212(10):1436–1441. https://doi.org/10.1242/jeb.028951

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

Илинский ЮЮ, Захаров ИК (2007) Эндосимбионт Wolbachia в евразийских популяциях Drosophila melanogaster. Генетика 7(43):905-915. [Ilinsky Y, Zakharov I (2007) The endosymbiont Wolbachia in Eurasian populations of Drosophila melanogaster. Genetika 43(7):905–915. (In Russ)].

Nunes M, Notle V, Schlotterer C (2008) Nonrandom Wolbachia infection status of Drosophila melanogaster strains with different mtDNA haplotypes. Mol Biol Evol 25:2493–2498. https://doi.org/10.1093/molbev/msn199

Ilinsky Y (2013) Coevolution of Drosophila melanogaster mtDNA and Wolbachia genotypes. PLoS ONE 8:e54373. https://doi.org/10.1371/journal.pone.0054373.

Bykov RA, Yudina MA, Gruntenko NE, Zakharov IK, Voloshina MA, Melashchenko ES, Danilova MV, Mazunin IO, Ilinsky YY (2019) Prevalence and genetic diversity of Wolbachia endosymbiont and mtDNA in Palearctic populations of Drosophila melanogaster. BMC Evol Biol 19(1):48. https://doi.org/10.1186/s12862-019-1372-9

Ilinskii YY, Zakharov IK (2007) Infection of the Uman’ population of Drosophila melanogaster with the cytoplasmic endosymbiont Wolbachia. Dokl Biol Sci 413(4):166–168. https://doi.org/10.1134/S0012496607020238

Riegler M, Iturbe-Ormaetxe I, Woolfit M, Miller WJ, O’Neill SL (2012) Tandem repeat markers as novel diagnostic tools for high resolution fingerprinting of Wolbachia. BMC Microbiol 12(1):S12. https://doi.org/10.1186/1471-2180-12-S1-S12

Zhukova MV, Kiseleva E (2012). The virulent Wolbachia strain wMelPop increases the frequency of apoptosis in the female germline cells of Drosophila melanogaster. BMC Microbiol 12(1):S15. https://doi.org/10.1186/1471-2180-12-S1-S15

McGraw EA, Merritt DJ, Droller JN, O’Neill SL (2001) Wolbachia-mediated sperm modification is dependent on the host genotype in Drosophila. Proc Biol Sci 268(1485):2565–2570. https://doi.org/10.1098/rspb.2001.1839

Suh E, Mercer DR, Fu Y, Dobson SL (2009) Pathogenicity of life-shortening Wolbachia in Aedes albopictus after transfer from Drosophila melanogaster. Appl Environ Microbiol 75(24):7783–7788. https://doi.org/10.1128/AEM.01331-09

Duarte EH, Carvalho A, Verde UDC, Lisboa U (2020) Forward genetics in Wolbachia: Regulation of Wolbachia proliferation by the amplification and deletion of an addictive genomic island. PLoS Genet 17(6):e1009612. https://doi.org/10.1371/journal.pgen.1009612

Hoffmann AA, Clancy DJ, Merton E (1994) Cytoplasmic incompatibility in Australian populations of Drosophila melanogaster. Genetics 136(3):993–999. https://doi.org/10.1093/genetics/136.3.993.

Hoffmann AA, Hercus M, Dagher H (1998) Population dynamics of the Wolbachia infection causing cytoplasmic incompatibility in Drosophila melanogaster. Genetics 148(1):221–231. https://doi.org/10.1093/genetics/148.1.221

Verspoor RL, Haddrill PR (2011) Genetic diversity, population structure and Wolbachia infection status in a worldwide sample of Drosophila melanogaster and D. simulans populations. PLoS One 6(10):e26318. https://doi.org/10.1371/journal.pone.0026318

Richardson MF, Weinert LA, Welch JJ, Linheiro RS, Magwire MM, Jiggins FM, Bergman CM (2012) Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster. PLoS Biol 8:e1003129. doi: 10.1371/journal.pgen.1003129

Starr DJ, Cline TW (2000) A host parasite interaction rescues Drosophila oogenesis defects. Nature 418(6893):76–79. https://doi.org/10.1038/nature00843

Ikeya T, Broughton S, Alic N (2009) The endosymbiont Wolbachia increases insulin/IGF-like signaling in Drosophila. Proc R Soc B 276(1674):3799—3807. doi: 10.1098/rspb.2009.0778

Илинский Ю. Ю., Захаров И. К., 2009. Цитоплазматическая несовместимость у Drosophila melanogaster, обусловленная различными генотипами Wolbachia. Симбиогенетика 7(2):11–18. [Ilinskii YY, Zakharov IK (2009) Cytoplasmic incompatability in Drosophila melanogaster due to different Wolbachia genotypes. Ecological Genetics 7(2):11–18. (In Russ)]. https://doi.org/10.17816/ecogen7211-18

Gruntenko NE, Rauschenbach IY (2008) Interplay of JH, 20E and biogenic amines under normal and stress conditions and its effect on reproduction. J Insect Physiol 54(6):902–908. https://doi.org/10.1016/j.jinsphys.2008.04.004

Johnson EC, White MP (2009) Stressed-out insects: Hormonal actions and behavioral modifications. Hormones, brain and behavior. Elsevier Academic Press P. 1069–1096.

Even N, Devaud JM, Barron AB (2012) General stress responses in the honey bee. Insects 3(4):1271–1298. https://doi.org/10.3390/insects3041271

Jones BE (2005) From waking to sleeping: neuronal and chemical substrates. Trends Pharmacol Sci 26(11):578–586. https://doi.org/10.1016/j.tips.2005.09.009

Liu Q, Liu S, Kodama L, Driscoll MR, Wu MN (2012) Two dopaminergic neurons signal to the dorsal fan-shaped body to promote wakefulness in Drosophila. Curr. Biol 22(22):2114–2123. https://doi.org/10.1016/j.cub.2012.09.008

Zimmerman JE, Chan MT, Lenz OT, Keenan BT, Maislin G, Pack AI (2017) Glutamate is a wake active neurotransmitter in Drosophila melanogaster. Sleep 40(2):zsw046. https://doi.org/10.1093/sleep/zsw046

Adonyeva NV, Burdina EV, Bykov RA, Gruntenko NE, Rauschenbach IY (2019) Genotype of Wolbachia pipientis endosymbiont affects octopamine metabolism in Drosophila melanogaster females. Russ J Genet 55(5):653–655. https://doi.org/10.1134/S1022795419050028

Rohrscheib CE, Bondy E, Josh P, Riegler M, Eyles D, van Swinderen B, Weible MW, Brownlie JC (2015) Wolbachia influences the production of octopamine and affects Drosophila male aggression. Appl Environ Microbiol 81(14):4573–4580. https://doi.org/10.1128/AEM.00573-15

Bi J, Sehgal A, Williams JA, Wang YF (2018) Wolbachia affects sleep behavior in Drosophila melanogaster. J Insect Physiol 107:81–88. https://doi.org/10.1016/j.jinsphys.2018.02.011

Negri I, Pellecchia M, Gre`ve P, Daffonchio D, Bandi C, Alma A (2010) Sex and stripping: the key to the intimate relationship between Wolbachia and host. Commun Integr Biol 3(2):110–115. https://doi.org/10.4161/cib.3.2.10520

Negri I (2011) Wolbachia as an ‘‘infectious’’ extrinsic factor manipulating host signaling pathways. Front Endocrinol 2:115. https://doi.org/10.3389/fendo.2011.00115

Simon AF, Shih C, Mack A, Benzer S (2003) Steroid control of longevity in Drosophila melanogaster. Science 299(5611):1407–1410. https://doi.org/10.1126/science.1080539

Negri I, Pellecchia M (2012) Sex steroids in insects and the role of the endosymbiont Wolbachia: a new perspective. In: Raghvendra KD (ed) Sex hormones, InTech publisher, p 353–374.

Liu C, Wang JL, Zheng Y, Xiong EJ, Li JJ, Yuan LL, Yu XQ, Wang YF (2014) Wolbachia-induced paternal defect in Drosophila is likely by interaction with the juvenile hormone pathway. Insect Biochem Mol Biol 49:49–58. https://doi.org/10.1016/j.ibmb.2014.03.014

Richard DS, Jones JM, Barbarito MR, Cerula S, Detweiler JP, Fisher SJ, Brannigan DM, Scheswohl DM (2001) Vitellogenesis in diapausing and mutant Drosophila melanogaster: further evidence for the relative roles of ecdysteroids and juvenile hormones. J Insect Physiol 47(8):905–913. https://doi.org/10.1016/S0022-1910(01)00063-4

Flatt T, Tu MP, Tatar M (2005) Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. Bioessays 27(10):999–1010. https://doi.org/10.1002/bies.20290

Li M, Mead EA, Zhu J (2011) Heterodimer of two bHLH-PAS proteins mediates juvenile hormone-induced gene expression. Proc Natl Acad Sci U S A 108(2):638–643. https://doi.org/10.1073/pnas.1013914108

Hiruma K, Kaneko Y (2013) Hormonal regulation of insect metamorphosis with special reference to juvenile hormone biosynthesis. Curr Top Dev Biol 103:73–100. https://doi.org/10.1016/B978-0-12-385979-2.00003-4

Simpson SJ, Raubenheimer D (2012) The nature of nutrition: a unifying framework from animal adaptation to human obesity. Princeton University Press, Princeton.

Ponton F, Wilson K, Holmes A, Raubenheimer D, Robinson KL, Simpson SJ (2015) Macronutrients mediate the functional relationship between Drosophila and Wolbachia. Proc Biol Sci 282(1800):20142029. https://doi.org/10.1098/rspb.2014.2029

Lee KP, Simpson SJ, Clissold FJ, Brooks R, Ballard JW, Taylor PW, Soran N, Raubenheimer D (2008) Lifespan and reproduction in Drosophila: new insights from nutritional geometry. Proc Natl Acad Sci U S A 105(7):2498–2503. https://doi.org/10.1073/pnas.0710787105

Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R, Brownlie JC, McGraw EA, Martin W, Esser C, Ahmadinejad N, Wiegand C, Madupu R, Beanan MJ, Brinkac LM, Daugherty SC, Durkin AS, Kolonay JF, Nelson WC, Mohamoud Y, Lee P, Berry K, Young MB, Utterback T, Weidman J, Nierman WC, Paulsen IT, Nelson KE, Tettelin H, O'Neill SL, Eisen JA (2004) Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2(3):E69. https://doi.org/10.1371/journal.pbio.0020069

Caragata EP, Rancès E, Hedges LM, Gofton AW, Johnson KN, O'Neill SL, McGraw EA (2013) Dietary cholesterol modulates pathogen blocking by Wolbachia. PLoS Pathog 9(6):e1003459. https://doi.org/10.1371/journal.ppat.1003459

Markov AV, Zakharov-Gezekhus IA (2006) The parasitic bacterium Wolbachia and the origin of the eukaryotic cell. Paleontol J 40:115–124. https://doi.org/10.1134/S0031030106020018

Henrichfreise B, Schiefer A, Schneider T, Nzukou E, Poellinger C, Hoffmann TJ, Johnston KL, Moelleken K, Wiedemann I, Pfarr K, Hoerauf A, Sahl HG (2009) Functional conservation of the lipid II biosynthesis pathway in the cell wall-less bacteria Chlamydia and Wolbachia: why is lipid II needed? Mol Microbiol 73(5):913–923. https://doi.org/10.1111/j.1365-2958.2009.06815.x

Vollmer J, Schiefer A, Schneider T, Jülicher K, Johnston KL, Taylor MJ, Sahl HG, Hoerauf A, Pfarr K (2013) Requirement of lipid II biosynthesis for cell division in cell wall-less Wolbachia, endobacteria of arthropods and filarial nematodes. Int J Med Microbiol 303(3):140–149. https://doi.org/10.1016/j.ijmm.2013.01.002

Nӓssel DR, Liu Y, Luo J (2015) Insulin/IGF signaling and its regulation in Drosophila. Gen Comp Endocrinol 221:255–266. https://doi.org/10.1016/j.ygcen.2014.11.021

Junnila RK, List EO, Berryman DE, Murrey JW, Kopchick JJ (2013) The GH/IGF-1 axis in ageing and longevity. Nat Rev Endocrinol 9(6):366–376. https://doi.org/10.1038/nrendo.2013.67

Sadagurski M, White MF (2013) Integrating metabolism and longevity through insulin and IGF1 signaling. Endocrinol Metab Clin North Am 42(1):127–148. https://doi.org/10.1016/j.ecl.2012.11.008

Wang L, Karpac J, Jasper H (2014) Promoting longevity by maintaining metabolic and proliferative homeostasis. J Exp Biol 217(1):109–118. https://doi.org/10.1242/jeb.089920

Grönke S, Clarke DF, Broughton S, Andrews TD, Partridge L (2010) Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet 6(2):e1000857. https://doi.org/10.1371/journal.pgen.1000857