Abstract
The intracellular bacterium Wolbachia pipientis is one of the most common prokaryotic symbionts of invertebrates. It is able to affect host species reproduction, thus contributing to the spread of the bacteria in host populations via increasing the number of infected females. However, while the main effects of Wolbachia are well documented, the mechanisms of reproductive anomalies it evokes and positive effects it exerts on the host fitness remain largely understudied. This review addresses various aspects of Wolbachia effects on host physiology and fitness with a special focus on the symbiotic system Wolbachia pipientis–Drosophila melanogaster, specifically Wolbachia influence on host hormonal status and host resistance to stress, viral infection, fecundity, and lifespan.
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INTRODUCTION
Wolbachia pipientis [1] is an intracellular, maternally inherited alpha-proteobacterium that occurs in approximately 40–60% of arthropod species [2], including Drosophila melanogaster, and is one of the most common prokaryotic symbionts of invertebrates (Fig. 1). Wolbachia has been dubbed a master manipulator because it is able to control the biology, morphology, and even some aspects of its host’s behavior. At the same time, the host in turn can gain an advantage over uninfected individuals in its adaptability.
Natural occurrence of the endosymbiotic bacterium Wolbachia pipientis in insects, arachnids and nematodes.
EFFECT OF WOLBACHIA ON HOST’S REPRODUCTION
The co-evolution of W. pipientis and host species has led to the development of a variety of mutual adaptations. In the host organism, most evident adaptations concern a modification of the reproductive function. The four basic phenotypes known to date are cytoplasmic incompatibility (CI), feminization, androcide (selective death of males during embryogenesis or larval development), and thelytokous parthenogenesis [3–5]. Among these effects, CI is the most studied [5, 6].
In insects, CI arises when Wolbachia-infected males mate with uninfected females or those carrying another Wolbachia strain, which leads to embryo death [6]. As a result, Wolbachia-infected females that are protected against CI gain a reproductive advantage over uninfected females. Another variant of CI, bidirectional CI, occurs when crossing parents that carry different bacterial strains. It has been hypothesized that such a type of CI can contribute to host speciation by causing reproductive barriers [7]. The CI level depends on many factors. For example, a high level of sperm infection causes a high CI level [8, 9]. Another discovery has been made when studying a Wolbachia wPip strain that infects the mosquitoes Culex pipiens. The genome of these bacteria has been found to contain a transcription regulator that affects the expression of the host’s grau gene responsible for CI manifestation [10]. A high CI level positively correlates with a high Wolbachia titer [11–14]. The Wolbachia titer in the host organism depends on various factors. One and the same Wolbachia strain may have different titers in different host genotypes [15–17], and within the same host, the titer varies from tissue to tissue, e.g., reproductive tissues show higher titers compared to somatic tissues [18, 19]. In addition, Wolbachia titer may depend on the ambient temperature. For example, D. nigrosparsa raised at temperatures below 19°C had a higher Wolbachia titer compared to individuals grown at high temperatures [20]. Also, D. melanogaster individuals raised at 13°C were found to have a higher Wolbachia density compared to those raised at 31°C [21]. By changing the Wolbachia titer in eggs, temperature also affects the degree of androcid manifestation in D. bifasciata [22]. In D. melanogaster, Wolbachia density varies depending on a diet [23]: flies raised on sucrose-enriched food were shown to have an increased bacterial titer in oogenesis, while those raised on yeast-enriched food had a decreased one. The mortality rate in D. melanogaster infected with the Wolbachia wMelPop strain positively correlates with the bacterial titer [24]. The titer can also change with host age, as observed in many arthropods, including Drosophila spp. [15, 25–28]. Since it has previously been shown that in D. melanogaster females, the division of germline stem cell declines with age [29], while Wolbachia is most represented in host’s reproductive tissues [30–32], the decrease in Wolbachia titer in flies approaching four weeks of age can be explained by a decrease in germline stem cell division.
EFFECT OF WOLBACHIA ON HOST FITNESS
Depending on specific host-bacteria interactions, macrosymbionts can benefit from the Wolbachia symbiont. For example, D. melanogaster infected with wMel had higher fecundity and mating rates compared to uninfected individuals [2]. The cicadas Laodelphax striatellus infected with the wStri strain also had a higher fecundity than uninfected insects [33]. The beetles Callosobruchus chinensis infected with Wolbachia wBruCon, wBruOri, and wBruAus strains were reported to have larger body size and lifespan [34]. At the same time, the infection of D. nigrosparsa with Wolbachia wMel had no effect on fly fecundity level and their heat and cold stress tolerance, although increasing their motor activity [20].
In D. melanogaster and D. simulans, Wolbachia titer positively correlates with host antiviral resistance [19, 35–39], including an increase in insect resistance to viruses dangerous to humans (Dengue, yellow fever, and West Nile fever viruses) [28, 35, 40, 41]. The presence of Wolbachia in Drosophila and mosquitoes leads to increased host resistance to the malaria pathogen (Plasmodium vivax) [38]. As shown in various Drosophila species and the woodlouse Armadillidium vulgare, the symbiont’s impact on host immunocompetence and survival varied significantly within the same population, depending on the host-infecting Wolbachia strain [42, 43], which suggests an actively ongoing evolutionary process in the formation of Wolbachia-host system’s resistance to various pathogens. Recent studies [44] have shown that temperature is a strong modulator of the antiviral protection provided by Wolbachia in D. melanogaster infected with Drosophila C virus (DCV). Drosophila development at 25°C leads to strong antiviral protection in terms of survival and DCV resistance, while the development at 18°C strongly reduces or even negates such a protection. This has been observed with different D. melanogaster genotypes, Wolbachia variants (wMel and wMelCS), and viruses, and may therefore represent a common phenomenon [44].
To shed light on the mechanism underlying these changes, Pan et al. [45] conducted studies on the mosquitoes Aedes aegypti, which transmit a number of severe human diseases, including those caused by yellow fever and Dengue viruses (YFV and DENV). The authors investigated how Wolbachia infection affects the host (Ae. aegypti) and elicits DENV resistance. It was shown that in Wolbachia-infected Ae. aegypti, the transcription of genes related to the regulation of immune responses and redox reactions is activated. The infection with this bacterium induces oxidative stress and increases reactive oxygen species (ROS) levels in the host mosquito. An increase in ROS production is due to the activation of the Toll signaling pathway, which is required to mediate antioxidant expression and counteract oxidative stress. This immune pathway is also responsible for the activation of the antimicrobial peptides defensins and cecropins. There is evidence that these antimicrobial peptides are involved in the suppression of DENV proliferation in Wolbachia-infected mosquitoes. These results show that the symbiotic bacterium can manipulate the host defense system to facilitate its own persistent infection, which results in a reduced ability of mosquitoes to be infected with pathogens dangerous to humans [45].
In another study of the mechanism of antiviral protection associated with Wolbachia infection and also performed on Ae. aegypti, the mosquitoes were infected in laboratory conditions with the Drosophila-specific pathogenic wMelPop strain [46]. It turned out that in the presence of Wolbachia, the synthesis level of miRNAs involved in the regulation of the density of distribution of these bacteria in Ae. aegypti tissues increases. These short single-stranded RNAs encode no proteins, but are implicated in the regulation of a large number of genes. For this reason, they play a crucial role in many vital processes, including immune defense, programmed cell death, etc. The same microRNAs increase mosquito DENV resistance [47, 48].
However, wMelPop is a strain that was only identified in the laboratory. The natural Wolbachia strains, commonly used in antiviral protection studies, are wMel and wMelCS isolated from D. melanogaster, wAu, isolated from D. simulans, wAlbB isolated from Ae. albopictus, and wStri isolated from the cicadas L. striatellus [49]. Martinez et al. [50] analyzed the antiviral protection of many natural Wolbachia strains drived from different Drosophila species after transferring them to the same genetic background of D. simulans. It was found that the protection is determined by not the host genotype but the Wolbachia strain [50]. It is noteworthy that most studies showing the ability of different Wolbachia strains to protect insect hosts against many RNA viruses were carried out under laboratory conditions, and only little evidence has been obtained thus far for the existence of Wolbachia antiviral effect in nature.
In addition, there have been described cases when Wolbachia infection did not protect the host from viruses and, on the contrary, contributed to further infection [51]. In their work, Graham et al. [51] provided data on field populations of the dangerous crop pest, African moth Spodoptera exempta, which show that the prevalence and intensity of infection with nuclear polyhedrosis virus (SpexNPV) positively correlate with the infection with three Wolbachia strains. The authors also demonstrated that the infection with one of these strains increases SpexNPV-induced host mortality by a factor of 6–14. These data suggest that, instead of protecting their lepidopteran hosts from viral infection, Wolbachia makes them more susceptible thereto.
Wolbachia infection has been repeatedly shown to affect Drosophila lifespan. These effects, however, are contradictory and include both increases [19, 52, 53] and decreases [19, 54, 55] in longevity.
The lifespan-regulating effects of Wolbachia may depend on the host genetic background [56, 57]. Fry and Rand [56] used reciprocal hybrid crosses between the two D. melanogaster strains, one of which (Z53), when infected with Wolbachia, lives longer and the other (Z2) does not, and noted that Wolbachia can increase fly longevity by reducing its fecundity. The positive effect of Wolbachia infection on fly longevity was far more pronounced in hybrids of these strains than in the parental line Z53. Moreover, this favorable effect of infection was more evident when females and males were kept separately, which excluded courtship and mating. Under these conditions, almost all Wolbachia-infected insects lived longer than uninfected flies.
The longevity of an organism can be influenced by the genetic background and the environment. The two most common factors that affect longevity and hence arouse great interest are oxidative stress caused by various abiotic exposures and infections [58, 59]. Capobianco et al. [60] investigated how different combinations of Wolbachia infection and oxidative stressors affect lifespan in two wild-caught D. melanogaster strains, Burlington and Plattsburgh. Naturally Wolbachia-infected and cured Burlington and Plattsburgh strains were treated with paraquat or L-arginine to induce two different types of oxidative stress. Both paraquat and L-arginine affect the ROS pathway inside D. melanogaster. Paraquat produces free oxygen radicals when it is metabolized in the cytoplasm. Thus, paraquat is a proven and useful tool for to elevate the superoxide anion content in cells [61]. Feeding on the nitric oxide precursor L-arginine [62] induces nitric oxide, which can enhance the insect immune response to plasmodium [63] and parasitoid infection [64]. Nitric oxide is a small molecule that plays multiple roles in biological processes, including signal transduction and the ability to react with superoxide anions to form peroxynitrite (ONOO-) [65]. Peroxynitrite, a potent and toxic oxidant, is relatively slow to react with most biological molecules. The authors found that the removal of Wolbachia infection shortens the lifespan of flies with one genetic background but not with the other. Wolbachia infection makes only one of the strains more paraquat-sensitive. However, it was the strain uninfluenced by Wolbachia when treated with paraquat that proved to be protected by this infection against L-arginine-induced stress [60]. Consequently, Wolbachia modifies the protection against free radicals via two different mechanisms that depend on the host genetic background. This supports the idea that the factors able to regulate aging (infection and oxidative stress) are not universal, but specific to the genetic structure of the individual.
It has also been shown that the effect of Wolbachia on host fitness also depends to some extent on the genotype of the endosymbiont [66–69]. Serga et al. [66] demonstrated that D. melanogaster females infected with wMelCS have lower fecundity compared to those infected with wMel, which, in the authors’ opinion, may be the reason for the predominance of wMel in D. melanogaster populations.
However, when studying the effect of different Wolbachia genotypes on D. melanogaster survival under heat stress, it was found that one of the wMelCS genotype isolates, wMelPlus strain, provides the host insect with increased stress tolerance [67, 70] and fecundity [68] in comparison with the wMel genotype and other strains of the wMelCS genotype.
Apart from fecundity, longevity, and antiviral protection, Wolbachia influences other aspects of host insect vital activity: in D. melanogaster and D. simulans, the bacterium affects dietary iron metabolism. When the fruit flies were placed on food with a deficiency or excess of iron salts, uninfected individuals laid fewer eggs compared to the infected [71, 72]. In bed bugs Cimex lectularius, it has been shown that Wolbachia wCle can provide an insect host with vitamin B, which is essential for its development [73]. There are also data on the ability of Wolbachia to influence the behavior of its hosts. For example, in D. paulistorum and D. melanogaster it was shown that females and males infected with different Wolbachia strains avoid crossing that leads to CI [74, 75]. Wolbachia-infected D. melanogaster females also demonstrate changes in oviposition substrate preference, while Wolbachia-infected males are more competitive than uninfected ones [76]. The beetles Callosobruchus chinensis infected with Wolbachia wBruCon and wBruOri are significantly more active than uninfected ones, which increases their mating success [77]. Ae. aegypti artificially infected with wMelPop are 2.5-fold more active compared to uninfected ones [78].
All these data indicate that the physiological and behavioral features of Wolbachia-infected insects, which can be observed both under laboratory conditions and in nature, are provided by an entanglement of different genetically determined mechanisms of interaction between the two organisms. Of course, these complicated insect-bacteria interrelationships require further in-depth study.
THE DROSOPHILA MELANOGASTER–WOLBACHIA PIPIENTIS SYSTEM
Particular attention is paid now to the symbiotic D. melanogaster–Wolbachia pipientis system. Analysis of the Wolbachia genomes detected in D. melanogaster revealed six genotypes of monophyletic origin: wMel, wMel2, wMel3, wMel4, wMelCS, and wMelCS2 (Fig. 2), with two of them (wMel and wMelCS) being ubiquitous and the wMel genotype occurring in the vast majority of infected individuals [79–83]. The wMel2 and wMel4 genotypes have been detected in D. melanogaster populations only in the Asian regions [17, 79, 80, 82], wMelCS2—in Eastern Europe and Central Asia, the Caucasus and the Altai [79, 80, 82, 84], and wMel3—only in a single laboratory D. melanogaster strain [79]. A pathogenic wMelCS variant, the wMelPop (from the word “popcorn”) strain, was also isolated in the laboratory and so dubbed for its ability to reproduce unrestrainedly in cells of the Drosophila organism, leading to cell rupture and, as a consequence, degradation of nervous and muscle tissues, as well as premature fly death [54]. As a genetic marker, it is indistinguishable from wMelCS [85]; however, it reduces insect lifespan approximately by half even at optimal temperature (25°C), and by another half when temperature is increased to 29°C [15, 54]. The wMelPop genotype also has a negative effect on host fitness, reducing host survival under stress yet before the onset of its premature death, which wMelPop induces on day 9–10 [67], and increasing the frequency of programmed cell death in the developing Drosophila ovarian follicles [86]. At the same time, the transfer of wMelPop-infected flies kept at 29°C to lower-temperature conditions (16°C) can partially restore their lifespan [55]. In addition, wMelPop was observed to be more pathogenic when transfected in D. simulans and Ae. albopictus compared to its natural host, D. melanogaster [87, 88]. A study of the dynamics of Drosophila brain cell colonization with bacteria of the wMelPop strain showed that they get there at the early stages of insect development, however begin to divide actively only at the imago stage, gradually destroying the host nervous system, with the rate of bacterial cell division increasing as temperature rises [55].
Recently, Duarte et al. [89] developed a novel forward genetic screen and identified new overproliferative Wolbachia variants. The authors provided a comprehensive characterization of two of the obtained mutants, wMelPop2 and wMelOctoless, and determined the genetic substrate of their overproliferation. The wMelPop2 genotype has an amplification of the Octomom region containing eight Wolbachia genes, which, as previously shown, leads to overproliferation in the case of wMelPop [24, 28]. In wMelOctoless, by contrast, the same Octomom region was deleted. A detailed phenotypic characterization of these strains showed that both Wolbachia variants reduced host lifespan and increased its antiviral protection. Moreover, the authors demonstrated that the Wolbachia proliferation rate in D. melanogaster depends on the interaction between the number of Octomom copies, host developmental stage, and temperature. These findings confirm and further develop the ideas on the ambiguous role of this genomic region in the control of Wolbachia proliferation.
A unique Wolbachia wMelPlus strain has also been recently found to increase the stress resistance of D. melanogaster [67, 68, 70]. This strain represents a variant of the wMelCS genotype and is indistinguishable therefrom as a genetic marker.
Numerous studies have shown that the Wolbachia infection rate in natural D. melanogaster populations varies from 30 to 60% across the entire distribution range of the species [2, 80–83, 90–93]. The reasons for such a wide distribution of the symbiont are still not fully elucidated. However, the studies of this symbiosis have yielded extremely interesting results. For example, the symbiont can restore fertility in females of a certain genotype [94], influence the fertility level of Drosophila females by changing their hormonal background [68], increase the fitness of flies with a reduced production of the insulin-like growth factor [95], or rescue flies infected in laboratory conditions with high doses of RNA viruses [35]. However, these and other known facts cannot fully explain why the infection in D. melanogaster populations is ubiquitously maintained at a high level [2, 66, 82]. It should be noted that the CI phenomenon, which could explain the spread and maintenance of Wolbachia in populations, is manifested in D. melanogaster at a high level only under special laboratory conditions, while under conditions approximating the natural, it is extremely low or undetected at all [90, 91].
In 2009, Ilinskii and Zakharov [96] evaluated the CI level in D. melanogaster caused by the three most common Wolbachia genotypes, wMel, wMelCS and wMelCS2. They showed that wMel and wMelCS genotypes are able to elicit a weak CI (< 10%), whereas Wolbachia wMelCS2 lacks this ability.
Chromosomal maps of the six different Wolbachia pipientis genotypes isolated from Drosophila melanogaster (after Riegler et al., 2005, with additions). The genotypes differ by a single large chromosomal inversion, two loci with a variable number of tandem repeats (VNTR-105 and VNTR-141), and two different IS5 transposon insertion sites (WD1310 and WD0516/7).
EFFECT OF WOLBACHIA ON DROSOPHILA MELANOGASTER HORMONAL STATUS
Effect on catecholamines
In insects, catecholamines, dopamine and octopamine, are stress hormones, along with juvenile hormone (JH), 20-hydroxyecdysone (20HE), insulin and adipokinetic hormone, which are directly involved in the control of adaptation [97–99]. Dopamine, apart from being involved in stress development, also plays an important role in controlling sleep quality and quantity. In the mammalian mesencephalic tegmentum, dopamine-containing neurons are important for excitation [100]. Like in mammals, dopamine in flies promotes wakefulness [101], indicating that this and other neurotransmitter pathways [102] share common functions in sleep regulation in both insects and different mammalian species.
The effect of Wolbachia genotype on Drosophila survival under heat stress is mediated by changes in catecholamine metabolism in the latter [67, 103]. The dependence of Wolbachia effect on the level and biosynthesis of octopamine in D. melanogaster on endosymbiont genotype was also shown by Rohrscheib et al. [104].
Transcriptional analysis of the dopamine biosynthesis pathway showed that its two main genes, Pale and Ddc, were significantly activated in Wolbachia-infected flies [105]. A study of the effect of Wolbachia on sleep duration and quality showed that it elicited an increase in total sleep time in both male and female D. melanogaster. Such an increase in sleep duration was due to an increase in the number of nocturnal sleep episodes, but not to an increase in the duration of individual sleep episodes. Accordingly, Wolbachia infection also reduced the excitation threshold in their host flies. However, Wolbachia infection affected neither the circadian rhythm nor post-deprivation sleep recovery. Taken together, these results indicate that Wolbachia mediates the expression of dopamine-related genes and reduces the sleep quality in host insects [105].
Effect on 20-hydroxyecdysone signaling pathway
Drosophila lifespan is well known to be largely dependent on the 20HE signaling pathway, in which 20HE is a steroid hormone acting as the main regulator of insect development and reproduction. This pathway is also involved in the manifestation of Wolbachia-induced reproductive phenotypes [106, 107].
Drosophila with heterozygous mutation in the EcR V559fs gene encoding the 20HE receptor, have an increased lifespan and stress resistance with no obvious locomotor and fertility deficits [108]. Female flies of the DTS-3/+ strain carrying a mutation in the molting defective (mld) gene involved in 20E biosynthesis, also demonstrate increased longevity when cultured at 29°C. It has been suggested that Wolbachia produces specific regulators able to interact both directly and indirectly with the 20E receptor, thus modulating signaling therethrough [109]. These findings confirm that the ecdysteroid pathway may be involved in the lifespan modulation provided by Wolbachia in D. melanogaster.
Effect on juvenile hormone signaling pathway
Wolbachia is able to stimulate gene expression of the juvenile hormone (JH) signaling pathway and influence the JH metabolic level in D. melanogaster [68, 110]. JH is known to be related with ecdysteroid pathways [111–114] and insulin signaling [112]. Liu et al. [110] showed that in D. melanogaster, Wolbachia infection leads to a significant activation of the Jhamt and Met genes encoding the enzyme of JH synthesis and its receptor, playing a key role in the JH signaling pathway. The results of this study suggest that Wolbachia can enhance JH signaling in Drosophila.
Effect on protein-carbohydrate metabolism
Drosophila lifespan is highly dependent on nutritional conditions, such as the balance between dietary proteins and carbohydrates [115]. Ponton et al. [116] demonstrated that Wolbachia modulates the effect of the protein to carbohydrate (P/C) ratio on D. melanogaster lifespan. Flies, whose dietary P/C ratio was 1 : 16, lived longer compared to those with a 1 : 1 P/C ratio, while flies there were allowed to choose between the two food supplements (pure yeast or sucrose solution) had a medium lifespan. This is consistent with the previous results [117] showing that, when offered a choice of dietary supplements, flies regulated the intake of macronutrients to maximize not their longevity but egg-laying capacity. No differences were observed between the survival curves of infected and uninfected insects fed with a P/C 1 : 16 mixture or allowed to choose between the two dietary supplements. However, among the insects fed with a P/C 1 : 1 diet, uninfected flies lived longer compared to the infected. It has been suggested that these results may reflect host-symbiont competitiveness for carbohydrates and explain why infection has a negative effect on host longevity. Wolbachia has a limited number of metabolic pathways [118] and is thus highly dependent on its host for metabolic support [38, 118, 119]. For example, Wolbachia utilizes host sugars not only for glycolysis [120], but also for lipid II synthesis [121, 122], which the authors suggest to be essential for bacterial division. In the same study, the infected flies raised on a P/C 1 : 1 diet had a higher reproduction rate compared to their uninfected counterparts. If flies were allowed to choose between yeast and sucrose solutions, uninfected flies consumed more protein than infected flies. Carbohydrate intake was almost indistinguishable in infected versus uninfected flies. The average P/C ratio preferred by infected and uninfected flies was 1 : 20 and 1 : 9, respectively. Ponton et al. hypothesized that changing the feeding behavior of Wolbachia-infected flies may diminish the lifespan-shortening effect of infection by decreasing the reproduction [116].
Effect on insulin/insulin-like growth factor signaling pathway
The linkage between the fly feeding type and their lifespan is probably mediated by the insulin/insulin-like growth factor 1 (IGF-1) signaling (IIS) pathway, which is known to play a decisive role in the regulation of nutrient uptake and metabolism [123]. In addition, numerous studies have shown that the IIS pathway plays a pivotal role in the regulation of growth, reproduction, stress tolerance, and lifespan in all multicellular organisms, including D. melanogaster [124–126].
There is evidence that Wolbachia boosts the activity of the insulin signaling system [95, 127]. When studying how Wolbachia interacts with the D. melanogaster IIS pathway, Grönke et al. [127] found that the loss of insulin-like proteins produced in the brain significantly increases lifespan, but only in the presence of Wolbachia.
Ikeya et al. [95] explored the effect of Wolbachia infection on a number of IIS-related phenotypes in control and IIS-mutant D. melanogaster. They showed that in the presence of Wolbachia, the ubiquitous expression of a dominant negative form of the Drosophila insulin receptor (InRDN) led to a moderate dwarfism, reduced fecundity and increased longevity in females, i.e. to all phenotypes typical for decreased IIS. In the absence of Wolbachia, the moderate effects of InRDN expression were enhanced, resulting in the emergence of flies with phenotypes characteristic of pronounced IIS deficiency, including extreme dwarfism, sterility, increased fat content, and decreased longevity. The absence of Wolbachia in mutant flies led to a reduction in fecundity and weight of adult insects compared to infected flies of the same genotypes, but had no effect on lifespan [95]. In other words, it can be assumed that Wolbachia partially compensated for the defects caused in the host organism by impaired insulin signaling.
CONCLUSION
The impact of Wolbachia on intraspecific host competition is mediated through changes in the hormonal status of the latter. Wolbachia controls many pathways and processes that are required for the viability of its host, such as stress resistance, immune responses, energy metabolism, protection against oxidative stress, and other key survival functions. By all appearances, the effect of Wolbachia is generally aimed at increasing host fitness by increasing its fecundity and tolerance to environmental factors, which is not always accompanied by an increase in lifespan, and sometimes even shortens it.
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ACKNOWLEDGMENTS
The authors would like to thank the members of the Insect Genetics Department of the Institute of Cytology and Genetics (Siberian Branch of the Russian Academy of Sciences) for fruitful scientific discussions while writing the review, and Olga Shishkina in person for her help in preparing the illustrations.
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This work was supported by the Russian Science Foundation; grant no. 21-14-00090.
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Translated by A. Polyanovsky
Russian Text © The Author(s), 2022, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2022, Vol. 58, No. 2, pp. 71–83https://doi.org/10.31857/S0044452922020024.
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Burdina, E.V., Gruntenko, N.E. Physiological Aspects of Wolbachia pipientis–Drosophila melanogaster Relationship. J Evol Biochem Phys 58, 303–317 (2022). https://doi.org/10.1134/S0022093022020016
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DOI: https://doi.org/10.1134/S0022093022020016