TY - JOUR
AU - Hoffmann, Ary, A
AB - Abstract Wolbachia-infected Aedes aegypti (L.) mosquitoes for control of dengue transmission are being released experimentally in tropical regions of Australia, south-east Asia, and South America. To become established, the Wolbachia Hertig (Rickettsiales: Rickettsiaceae) strains used must induce expression of cytoplasmic incompatibility (CI) in matings between infected males and uninfected females so that infected females have a reproductive advantage, which will drive the infection through field populations. Wolbachia is a Rickettsia-like alphaproteobacterium which can be affected by tetracycline antibiotics. We investigated whether exposure of Wolbachia-infected mosquitoes to chlortetracycline at environmentally relevant levels during their aquatic development resulted in loss or reduction of infection in three strains, wAlbB, wMel, and wMelPop. Wolbachia density was reduced for all three strains at the tested chlortetracycline concentrations of 5 and 50 µg/liter. Two of the strains, wMel and wMelPop, showed a breakdown in CI. The wAlbB strain maintained CI and may be useful at breeding sites where tetracycline contamination has occurred. This may include drier regions where Ae. aegypti can utilize subterranean water sources and septic tanks as breeding sites. tetracycline, chlortetracycline, cytoplasmic incompatibility, dengue The alphaproteobacterium, Wolbachia pipientis, is the focus of international control programs for dengue virus (Iturbe-Ormaetxe et al. 2011, Hoffmann et al. 2014, Flores and O’Neill 2018). Wolbachia has been introduced artificially to populations of the dengue vector mosquito, Aedes aegypti (L.), where it can suppress dengue virus replication and transmission (Moreira et al. 2009, Bian et al. 2010, Walker et al. 2011). The main premise of using Wolbachia-infected mosquitoes for control of dengue transmission is to release these mosquitoes into districts where they will replace the resident population of dengue-transmitting Ae. aegypti, by means of cytoplasmic incompatibility (CI; McMeniman et al. 2009). One method of clearing the Wolbachia infection from mosquito lines and other arthropods for experimental comparisons on similar genetic backgrounds is to use tetracycline antibiotics (Yen and Barr 1974, Hoffmann et al. 1986, Li et al. 2014, Sylvia et al. 2014). Tetracyclines are broad-spectrum antibiotics that show activity against a wide range of bacterial types as well as protozoans and are used extensively in human health and animal husbandry (Chopra and Roberts 2001). Their extensive use has led to release of antimicrobial compounds into the environment and contamination by antibiotics has been under increasing scrutiny since the mid-1990s (Watkinson et al. 2009). Antibiotic contamination of waterways is becoming a major problem throughout the world as it encourages the development and spread of antibiotic resistance in microbes (Gillings 2015) and has potential to disrupt key ecological processes in the aquatic environment (Watkinson et al. 2009). Our concern here is that the presence of antibiotics in water could also have a detrimental effect on the Wolbachia in mosquitoes being used in dengue control programs, thereby reducing their invasion potential and their dengue blocking effect. In the field, eggs of Ae. aegypti may hatch in water contaminated by antibiotics and the larvae could be exposed to these compounds throughout their development. The main sources of antibiotic contamination are animal production waste water, antibiotic production factory waste water, sewerage system waste water, waste water from treatment plants, use of manure or sewage as crop fertilizer, and hospital waste water (Campagnolo et al. 2002, Heberer 2002, Karthikeyan and Meyer 2006, Sarmah et al. 2006, Gillings 2015). In many circumstances, immature Ae. aegypti would not come into contact with contaminated water due to the fact that it is mainly a container-breeding species (Christophers 1960) and the containers would likely be filled by rain water or from domestic drinking supplies. However, Ae. aegypti is known, under particular circumstances, to inhabit drains or underground water sources particularly in regions which have a distinct dry season and it is in situations like this that developing mosquitoes could be exposed to antibiotic contamination. Development of Ae. aegypti in underground sources of water is known from northern Queensland, Australia (Russell et al. 2002, Montgomery et al. 2004); Cuba (Marquetti et al. 2005); Salvador, Brazil (Paploski et al. 2016), and from Mexico (Manrique-Saide et al. 2013, Arana-Guardia et al. 2014) and is likely to be common. Subterranean habitats for Ae. aegypti include wells, sewers, service manholes, pits, stormwater drains, and kitchen sumps (Kay et al. 2000). Infestation of septic tanks by Ae. aegypti is also a known phenomenon and these containers can be significant sources of developing mosquitoes (Barrera et al. 2008) and potential sites of antibiotic accumulation (Lundborg and Tamhankar 2017). A rough estimate of an average contamination level of the fresh water on earth is given by Gillings (2015) as 1.4 µg/liter. In effect, levels of antibiotic contamination vary dramatically and are highest closest to the source. Treated drinking water in the United States, United Kingdom, and Australia shows only rare detections of pharmaceuticals and any detection is normally <0.05 µg/liter (WHO 2011). In contrast, levels of tetracycline antibiotics in animal waste storage ponds can be as high as 1,000 µg/liter (Campagnolo et al. 2002) and cases of contamination of river water from agricultural runoff in China have been recorded up to a maximum concentration of 68.9 µg/liter (chlortetracycline in the Hai River system; Chen et al. 2018). The tetracycline concentration used to clear a mosquito of Wolbachia infection in the laboratory is around 1.0 to 5.0 × 106 µg/liter and is most often administered via the adult mosquito’s source of sucrose over multiple generations until a cure is effected (Li et al. 2014). Less is known about concentrations of tetracycline required to cure a Wolbachia infection in mosquito larvae and published results often demonstrate a lack of success (Dobson and Rattanadechakul 2001, Li et al. 2014). We aimed to study the effects of chlortetracycline environment-level contamination on three different Wolbachia infections in Ae. aegypti by exposing the aquatic stages of the mosquito (egg to pupa) to the antibiotic as might occur in nature. A supplementary aim was to determine a concentration–response curve for chlortetracycline, the response in this case being the reduction of Wolbachia infection in emerging adult mosquitoes. Data generated are potentially useful for dengue control programs that rely on dengue blocking in Wolbachia-infected mosquitoes following replacement of natural mosquito populations as initiated several years ago (Hoffmann et al. 2011). Materials and Methods Antibiotic Concentrations Serial dilution of chlortetracycline hydrochloride (VETRANAL, analytical standard, Sigma–Aldrich, Castle Hill, NSW Australia) was conducted to produce the following concentrations in 144 ml of RO water: 0, 0.0005, 0.005, 0.05, 0.5, 5.0, and 50 µg/liter. Four replicates of each concentration were made in plant culture dishes (Cat. No. SPL310100, PS, 100 × 40 mm, SPL Life Sciences, Gyeonggi-do, Korea) that were to serve as hatching containers for mosquito eggs and subsequent rearing of aquatic stages. Mosquito and Wolbachia Strains Strains of Ae. aegypti mosquito used in the study were the same as those studied by Ross et al. (2017): TSV – an uninfected line originally collected in Townsville, Queensland, Australia wAlbB (Xi et al. 2005) wMel (Walker et al. 2011) wMelPop-CLA (McMeniman et al. 2009) Note that these strains had been backcrossed to Townsville lines to control for genetic background and both the wMel and wMelPop strains were derived from field-collected material following Queensland releases (Hoffmann et al. 2011, Nguyen et al. 2015). Antibiotic Exposure Mosquito colonies were reared according to the protocol of Axford et al. (2016). Mosquito eggs sourced from three colonies of Ae. aegypti infected with different Wolbachia strains (wMelPop, wMel, and wAlbB) were hatched into reverse osmosis (RO) water containing antibiotic (chlortetracycline hydrochloride) as might occur in the field. TSV (uninfected) eggs were also hatched in the same way. Eggs were brushed off a sandpaper ovistrip into a glass vial using a fine paintbrush. Eggs were then tipped onto a 150-mm diameter filter paper (Whatman Filter Paper No. 1, GE Healthcare Life Sciences, Parramatta, NSW Australia) folded in half, to align the eggs, single file, along the inside crease. This arrangement allowed easy counting of eggs under a dissecting microscope. About 112 batches of 70 eggs were added to 1.7-ml centrifuge tubes (Axygen, Corning Life Sciences, Tewksbury, MA). Eggs were hatched directly into each antibiotic treatment by pipetting the solution into each tube before submerging the tube into a hatching container. Four replicates for each concentration were set up for the TSV, wMel, and wAlbB strains. Three replicates were set up for wMelPop. Water in the hatching containers was deoxygenated with active dried yeast (~0.02 mg/liter) to stimulate hatching of eggs and one crushed TetraMin fish food tablet (Tetra, Melle, Germany) was supplied. Larvae were fed with extra fish food as required and allowed to develop to the adult stage in the same container. All individuals that developed and survived to adulthood were stored in absolute ethanol, except for 10 males from each container, which were kept alive and crossed to uninfected female mosquitoes (TSV) to test for CI. CI Test Ten male mosquitoes emerging from each treatment container were crossed to uninfected females in 3-liter cages. Female mosquitoes were allowed to oviposit on sandpaper and eggs were conditioned as described by Axford et al. (2016). After counting under a dissecting microscope, eggs were submerged in reverse osmosis water containing yeast and the proportion of viable eggs was ascertained by counting larvae. Wolbachia Screening Mosquitoes that had developed in antibiotic solutions were screened for presence and relative density of Wolbachia using a high-resolution melt (HRM) assay (Lee et al. 2012) run with a Roche LightCyler 480, under the following conditions: 11 female mosquitoes were screened for Wolbachia in each of the seven antibiotic concentrations for each of the four replicates of the three Wolbachia-infected lines (wMelPop, wMel, and wAlbB) using the primers TMIS5_F/TM1310_R (CTC ATC TTT ACC CCG TAC TAA AAT TTC/TCT TCC TCA TTA AGA ACC TCT ATC TTG) (Yeap et al. 2014; Riegler et al. 2005, unpublished data), w1 (AAA ATC TTT GTG AAG AGG TGA TCT GC/GCA CTG GGA TGA CAG GAA AAG G) (Lee et al. 2012), and AlbB1 A/AlbB1 B (CCT TAC CTC CTG CAC AAC AA/ GGA TTG TCC AGT GGC CTT A) (Joubert et al. 2016) to detect each of the infections, respectively. Three technical replications of each sample were made for each of the three markers used in the HRM assay (mRpS6, mosquito-specific; aRpS6, Ae. aegypti-specific; and the relevant Wolbachia strain primer). Relative Wolbachia density was estimated as the difference in Cp (crossing point) values obtained from the aRpS6 marker and the relevant Wolbachia strain primers. Cp value is the cycle where the fluorescence level emitted due to PCR amplification exceeds the background fluorescence level. Data were transformed and reported as 2ΔCp(aRpS6-Wolbachia). A QX100 Droplet Digital PCR (ddPCR) system (Bio-Rad Laboratories Pty., Ltd., Hercules, CA) with a hydrolysis probe assay (PrimePCR, Bio-Rad Laboratories, Inc., Cat. No. 10031261) was used for ddPCR according to Richardson et al. (2018) on a subset of the male and female mosquitoes to obtain absolute quantification of Wolbachia copies per microliter of DNA. Seven to ten male mosquitoes taken from the 0, 0.5, 5.0, and 50 µg/liter chlortetracycline treatments were also screened for Wolbachia density using ddPCR. Results were analyzed with Quantasoft Analysis Pro 1.0.596.0525, Bio-Rad Laboratories, Inc. Analysis Statistical tests (Generalized Linear Model and post hoc tests) were conducted using IBM SPSS Statistics Version 24, Release 24.0.0.0. Normality was tested with Kolmogorov–Smirnov tests and, where data were non-normal, additional tests were undertaken with transformation. Results Effect on Development Time and Survival The highest concentration of antibiotic (50 µg/liter) had an obvious phenotypic effect on the Ae. aegypti larvae from all lines except wAlbB, causing them to develop more slowly than those exposed to the lower concentrations, thus leading to a delay in the time for the first pupa (male) to develop (F(3,11) = 53.927, P < 0.0001). There was also a slight difference in time to first pupa at 0.005 and 0.0005 µg/liter between the TSV strain and the wMel strain, with wMel larvae being quicker to develop (F(3, 11) = 5.785, P = 0.013; Fig. 1). Fig. 1. View largeDownload slide Time to first pupa (days) for three strains of Wolbachia mosquitoes (Ae. aegypti) and an uninfected line hatched and reared in chlortetracycline hydrochloride. The first pupae to develop were always male. Fig. 1. View largeDownload slide Time to first pupa (days) for three strains of Wolbachia mosquitoes (Ae. aegypti) and an uninfected line hatched and reared in chlortetracycline hydrochloride. The first pupae to develop were always male. The number of adults that emerged from each antibiotic concentration did not fit a normal distribution according to a one-sample Kolmogorov–Smirnov test (P = 0.044). Antibiotic concentration had no significant impact on number of adults that emerged (F(6, 77) = 1.258, P = 0.287), but there was a significant effect of mosquito line (F(3, 77)= 9.777, P < 0.001) on this variable, with more adult mosquitoes emerging from the TSV line than from both the wAlbB line (P = 0.001) and the wMelPop line (P < 0.0001) and more emerging from the wMel line than from wMelPop (P = 0.024; post hoc Tukey’s HSD test after Bonferroni correction; Fig. 2). The same conclusions emerged when data were log-transformed for normality before analysis. Fig. 2. View largeDownload slide Mean number (with standard error) of Ae. aegypti adults emerging from each chlortetracycline treatment replicate. Fig. 2. View largeDownload slide Mean number (with standard error) of Ae. aegypti adults emerging from each chlortetracycline treatment replicate. Effect on CI The number of eggs laid by uninfected female mosquitoes crossed with males reared in antibiotic solutions was normally distributed (P = 0.20) and did not show a significant difference among concentrations (F(6, 77) = 1.729, P = 0.125) and there was no effect of mosquito line (F(3, 77) = 0.326, P = 0.807; Fig. 3). The effect of interaction between line and concentration on numbers of eggs approached significance (F(18, 77) = 1.716, P = 0.054). Fig. 3. View largeDownload slide Mean number of Ae. aegypti eggs laid by Wolbachia-uninfected females crossed with males from four strains reared at seven concentrations of chlortetracycline hydrochloride in a test of CI. Fig. 3. View largeDownload slide Mean number of Ae. aegypti eggs laid by Wolbachia-uninfected females crossed with males from four strains reared at seven concentrations of chlortetracycline hydrochloride in a test of CI. Without antibiotic treatment, only the eggs from the TSV (uninfected) cross would be expected to be viable, as all other crosses should result in CI due to the presence of Wolbachia in the males. However, a loss of CI induction is apparent in wMelPop males exposed to ≥5-µg/liter chlortetracycline and wMel exposed to 50 µg/liter with respect to the proportion of viable eggs (Fig. 4a) and number of larvae (Fig. 4b). In contrast, mosquitoes infected with wAlbB exhibited no loss of CI at the same concentrations. Fig. 4. View largeDownload slide (a) Proportion of viable eggs of Ae. aegypti eggs from crosses between untreated, uninfected females with TSV (uninfected), wAlbB, wMel, or wMelPop males exposed to chlortetracycline hydrochloride throughout their aquatic development. (b) Number of larvae resulting from crosses between untreated, uninfected females with TSV (uninfected), wAlbB, wMel, or wMelPop males exposed to chlortetracycline hydrochloride. Fig. 4. View largeDownload slide (a) Proportion of viable eggs of Ae. aegypti eggs from crosses between untreated, uninfected females with TSV (uninfected), wAlbB, wMel, or wMelPop males exposed to chlortetracycline hydrochloride throughout their aquatic development. (b) Number of larvae resulting from crosses between untreated, uninfected females with TSV (uninfected), wAlbB, wMel, or wMelPop males exposed to chlortetracycline hydrochloride. Effect on Wolbachia Density Overall Wolbachia density differences in female and male Ae. aegypti adults reared without antibiotic were demonstrated between Wolbachia strains: wMelPop > wAlbB > wMel (Supp Fig. 1 [online only]). There was a distinct threshold in HRM Wolbachia relative density scores between the 0.5- and 5-µg/liter chlortetracycline treatments of female mosquitoes (density is constant up to and including the 0.5-µg/liter treatment and then drops at 5 µg/liter; Fig. 5). Fig. 5. View largeDownload slide Effect of chlortetracycline rearing concentration on relative density of Wolbachia in female Ae. aegypti. Fig. 5. View largeDownload slide Effect of chlortetracycline rearing concentration on relative density of Wolbachia in female Ae. aegypti. Density of each Wolbachia strain in adult mosquitoes was reduced in the 5-µg/liter treatment compared with untreated mosquitoes or those exposed to lower concentrations of chlortetracycline, but almost all female individuals still scored as positive in the HRM Wolbachia assay. Wolbachia density was reduced further in mosquitoes exposed to 50-µg/liter chlortetracycline, but Wolbachia was not completely removed from the insects. For most strains, female mosquitoes exposed to 50-µg/liter chlortetracycline had Wolbachia Cp values of >35 cycles which would exclude them from a positive diagnosis if Cp were used as the sole measure, but the melting temperature of the PCR amplicons was consistent with that of the specific Wolbachia strain and individuals in this category were included in the calculations of density. For the wAlbB strain, some individuals from the 50-µg/liter chlortetracycline treatment scored as positive due to Cp values less than 35 and ΔCp (CpaRpS6 – CpwAlbB1) more than −3. Most other individuals had a Cp value less than 35, but they were given an inconclusive diagnosis because ΔCp (CpaRpS6 – CpwAlbB1) was −3 or less, which would generally indicate that the sample cannot be definitively categorized as positive for Wolbachia. Once again, however, the Tm value of these samples is consistent with that of the strain-specific Wolbachia amplicon, indicating that the assay is detecting low titer infections. Absolute quantification of Wolbachia density as copy number per microliter in DNA from male Ae. aegypti adults (Fig. 6) showed a similar threshold of decrease in density between the rearing concentration of 0.5- and 5-µg/liter chlortetracycline. Also, apparent was a differential decrease in number of copies of Wolbachia between strains, with the largest decrease occurring in the wMelPop strain. Density of Wolbachia in male Ae. aegypti after exposure to 50-µg/liter chlortetracycline was lowest for the wMel strain and highest in wAlbB. Variation in Wolbachia copy number between individual male mosquitoes was very high (Fig. 6). Fig. 6. View largeDownload slide Comparison of number of Wolbachia copies between three Wolbachia strains at different rearing concentrations of chlortetracycline in adult male Ae. aegypti. Fig. 6. View largeDownload slide Comparison of number of Wolbachia copies between three Wolbachia strains at different rearing concentrations of chlortetracycline in adult male Ae. aegypti. Discussion High concentrations (5–50 µg/liter) of chlortetracycline antibiotic in the laboratory had adverse effects on Wolbachia density for three strains that have been considered for replacement releases for dengue control (wAlbB, wMel, and wMelPop). In wMel and wMelPop, these reductions in density result in some loss of CI which would have the effect of making mosquitoes containing these strains more difficult to establish in the field for a dengue control program. Strong CI is an important requirement for successful invasion of Wolbachia into field mosquito populations (Yeap et al. 2016), particularly when there are deleterious host fitness effects associated with the infection (Caspari and Watson 1959, Hoffmann and Turelli 1997). The question of how often Ae. aegypti would encounter these concentrations of antibiotic contamination in its larval habitats is not straightforward, but previous records of the species developing in sources of underground water and in septic tanks (Russell et al. 2002, Montgomery et al. 2004, Manrique-Saide et al. 2013, Paploski et al. 2016) highlight the likelihood of this scenario. A comparison of some of the tetracycline contamination levels recorded in the literature suggests that some exposure of Ae. aegypti to detrimental levels of this type of antibiotic is possible (Fig. 7). Fig. 7. View largeDownload slide Experimental concentrations of tetracycline compared with examples of environmental contamination. Fig. 7. View largeDownload slide Experimental concentrations of tetracycline compared with examples of environmental contamination. An environmental impact assessment conducted prior to release of a different type of modified Ae. aegypti as part of Oxitec’s control program (Oxitec_Ltd 2016) concluded that the developing mosquitoes in the proposed release area would not encounter the level of antibiotic concentration that would allow survival of their genetically modified mosquitoes by activating the nonlethal mechanism. The level required is around 1,000-µg/liter tetracycline and figures quoted in the Oxitec study as recorded field maxima in containers are 0.10–0.97 µg/liter. This is clearly quite a different scenario from that of Wolbachia mosquitoes, which are more likely to be detrimentally affected by environmental levels of tetracycline concentration in underground water and septic tanks. However, the question of whether Wolbachia-infected mosquitoes would be affected by antibiotics in their aquatic habitat may also depend on exposure periods and degradation rates of the antibiotic. The half-life of chlortetracycline will vary based on pH, UV exposure, temperature, and organic matter content of the water. The closest estimate of antibiotic half-life for the laboratory conditions used in our experiment is around 7 d based on data for oxytetracycline at 25°C, water, pH 7 with an organic matter substrate of fish food (Doi and Stoskopf 2000). The response of the wAlbB strain to chlortetracycline shows that this strain might have an innate stability which buffers the effect of a reduction of its density on CI. The wAlbB strain in Ae. aegypti has already shown that it is a robust infection in the face of exposure to heat in comparison with the wMel and wMelPop strains and its density is not reduced when exposed to a cyclical temperature regime of 26–37°C (Ross et al. 2017). Clancy and Hoffmann (2003) showed that CI in Drosophila simulans was mediated by environmental factors including temperature, nutrition, and aging as well as by exposure to tetracycline and that Wolbachia density was influenced by some, but not necessarily all of these factors. An asymmetry between sexes in effect of tetracycline and an opposite asymmetry in effect of heat suggests that the interaction between environmental factors and Wolbachia density could be complex (Clancy and Hoffmann 2003) and a result of selection for strong maternal transmission at the expense of CI (Richardson et al. 2018). Several studies on other insects identify host genotype as an additional factor of influence (Mouton et al. 2007). Variability in CI expression which is independent of Wolbachia density in the testes has been identified in D. melanogaster (Yamada et al. 2007) and a strain of Wolbachia in D. pseudotakahashii has been shown to induce CI when present at very low levels in male flies (Richardson et al. 2018). Bio-accumulation of chlortetracycline can occur in Ae. aegypti under mass rearing experiments with a peak in concentration in third-instar larvae (Curtis et al. 2015). It would, therefore, be of benefit to screen for Wolbachia at different life stages of the mosquito to confirm that the bioaccumulated concentration of the antibiotic, which becomes higher than that in the rearing water (Curtis et al. 2015), correlates with a reduction in Wolbachia density at the peak concentration. It is possible for Wolbachia densities to recover from low levels after antibiotic exposure is removed as shown in Drosophila (Clancy and Hoffmann 2003), which means that a reduction in density in a larva could still result in a recovered density in an adult mosquito. Future experiments could further define the threshold between 0.5 and 5 µg/liter to further characterize the concentrations that affect Wolbachia density and ability to induce CI. Concentrations of chlortetracycline >50 µg/liter could be tested to define the rate that confers complete clearance of the Wolbachia strains tested as we found very few individual mosquitoes that had completely lost the infection. It will also be important to model the effects of different proportions of the Wolbachia-mosquito population coming into contact with antibiotics to predict impact on rate of spread of the infection during a new release and impact on Wolbachia-infection frequency if the antibiotic exposure occurs in an established Wolbachia-mosquito population. In conclusion, it is recommended that, when investigating a site for release of Wolbachia-infected mosquitoes, consideration be given to the possibility of mosquitoes breeding in underground water and septic tanks. Given the findings of our study, antibiotic screening of water in known and potential breeding sites of Ae. aegypti could be useful, especially when using strains of Wolbachia-infected mosquitoes that are sensitive to levels of tetracycline contamination. As an alternative, our study shows that it is possible to find strains of Wolbachia which can still confer CI despite a tetracycline-induced reduction in density which could maximize the stability of dengue control programs at sites where underground and cryptic breeding sites are common. Data Availability Statement Data from this study are available from the Dryad Digital Repository (Endersby-Harshman et al. 2019). Acknowledgments We thank our international colleagues Dayanath Meegoda and Itsanun Wiwatanaratanabutr for assistance in the practical work involved in running this experiment. Ashley Callahan performed the HRM assays on the female mosquitoes. Tristan Stevens provided technical assistance for other molecular aspects. The study was funded by the National Health and Medical Research Council through their Program and Fellowship schemes. References Cited Arana-Guardia , R. , C. M. Baak-Baak , M. A. Loroño-Pino , C. Machain-Williams , B. J. Beaty , L. Eisen , and J. E. 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TI - Environmental Concentrations of Antibiotics May Diminish Wolbachia infections in Aedes aegypti (Diptera: Culicidae)
JF - Journal of Medical Entomology
DO - 10.1093/jme/tjz023
DA - 2019-06-27
UR - https://www.deepdyve.com/lp/oxford-university-press/environmental-concentrations-of-antibiotics-may-diminish-wolbachia-eL8hJAiXgs
SP - 1078
VL - 56
IS - 4
DP - DeepDyve
ER -