School of BioSciences - Research Publications

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    Fungicides have transgenerational effects on Rhopalosiphum padi but not their endosymbionts
    Chirgwin, E ; Yang, Q ; Umina, PA ; Gill, A ; Soleimannejad, S ; Gu, X ; Ross, P ; Hoffmann, AA (JOHN WILEY & SONS LTD, 2022-11)
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    Characterization of the first Wolbachia from the genus Scaptodrosophila, a male-killer from the rainforest species S.claytoni
    Richardson, KM ; Schiffer, M ; Ross, PA ; Thia, JA ; Hoffmann, AA (WILEY, 2022-10)
    The Scaptodrosophila genus represents a large group of drosophilids with a worldwide distribution and a predominance of species in Australia, but there is little information on the presence and impacts of Wolbachia endosymbionts in this group. Here we describe the first Wolbachia infection from this group, wClay isolated from Scaptodrosophila claytoni (van Klinken), a species from the east coast of Australia. The infection is polymorphic in natural populations, occurring at a frequency of around 6%-10%. wClay causes male killing, producing female-biased lines; most lines showed 100% male killing, though in 1 line it was <80%. The lines need to be maintained through the introduction of males unless the infection is removed by tetracycline treatment. wClay is transmitted at a high fidelity (98.6%) through the maternal lineage and has been stable in 2 laboratory lines across 24 generations, suggesting it is likely to persist in populations. The infection has not been previously described but is closely related to the male-killing Wolbachia recently described from Drosophila pandora based on multilocus sequence typing and the wsp gene. Male-killing Wolbachia are likely to be common in drosophilids but remain difficult to detect because the infections can often be at a low frequency.
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    Fitness costs of Wolbachia shift in locally-adapted Aedes aegypti mosquitoes
    Ross, PA ; Hoffmann, AA (WILEY, 2022-12)
    Aedes aegypti mosquito eggs can remain quiescent for many months before hatching, allowing populations to persist through unfavourable conditions. A. aegypti infected with the Wolbachia strain wMel have been released in tropical and subtropical regions for dengue control. wMel reduces the viability of quiescent eggs, but this physiological cost might be expected to evolve in natural mosquito populations that frequently experience stressful conditions. We found that the cost of wMel infection differed consistently between mosquitoes collected from different locations and became weaker across laboratory generations, suggesting environment-specific adaptation of mosquitoes to the wMel infection. Reciprocal crossing experiments show that differences in the cost of wMel to quiescent egg viability were mainly due to mosquito genetic background and not Wolbachia origin. wMel-infected mosquitoes hatching from long-term quiescent eggs showed partial loss of cytoplasmic incompatibility and female infertility, highlighting additional costs of long-term quiescence. Our study provides the first evidence for a shift in Wolbachia phenotypic effects following deliberate field release and establishment and it highlights interactions between Wolbachia infections and mosquito genetic backgrounds. The unexpected changes in fitness costs observed here suggest potential tradeoffs with undescribed fitness benefits of the wMel infection.
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    Wolbachia inhibits ovarian formation and increases blood feeding rate in female Aedes aegypti
    Lau, M-J ; Ross, PA ; Endersby-Harshman, NM ; Yang, Q ; Hoffmann, AA ; Bowen, RA (PUBLIC LIBRARY SCIENCE, 2022-11)
    Wolbachia, a gram-negative endosymbiotic bacterium widespread in arthropods, is well-known for changing the reproduction of its host in ways that increase its rate of spread, but there are also costs to hosts that can reduce this. Here we investigated a novel reproductive alteration of Wolbachia wAlbB on its host Aedes aegypti, using studies on mosquito life history traits, ovarian dissection, as well as gene expression assays. We found that an extended period of the larval stage as well as the egg stage (as previously shown) can increase the proportion of Wolbachia-infected females that become infertile; an effect which was not observed in uninfected females. Infertile females had incomplete ovarian formation and also showed a higher frequency of blood feeding following a prior blood meal, indicating that they do not enter a complete gonotrophic cycle. Treatments leading to infertility also decreased the expression of genes related to reproduction, especially the vitellogenin receptor gene whose product regulates the uptake of vitellogenin (Vg) into ovaries. Our results demonstrate effects associated with the development of infertility in wAlbB-infected Ae. aegypti females with implications for Wolbachia releases. The results also have implications for the evolution of Wolbachia infections in novel hosts.
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    Genomic and Phenotypic Comparisons Reveal Distinct Variants of Wolbachia Strain wAlbB
    Martinez, J ; Ross, PA ; Gu, X ; Ant, TH ; Murdochy, SM ; Tong, L ; Filipe, ADS ; Hoffmann, AA ; Sinkins, SP ; Buan, NR (AMER SOC MICROBIOLOGY, 2022-11-22)
    The intracellular bacterium Wolbachia inhibits virus replication and is being harnessed around the world to fight mosquito-borne diseases through releases of mosquitoes carrying the symbiont. Wolbachia strains vary in their ability to invade mosquito populations and suppress viruses in part due to differences in their density within the insect and associated fitness costs. Using whole-genome sequencing, we demonstrate the existence of two variants in wAlbB, a Wolbachia strain being released in natural populations of Aedes aegypti mosquitoes. The two variants display striking differences in genome architecture and gene content. Differences in the presence/absence of 52 genes between variants include genes located in prophage regions and others potentially involved in controlling the symbiont's density. Importantly, we show that these genetic differences correlate with variation in wAlbB density and its tolerance to heat stress, suggesting that different wAlbB variants may be better suited for field deployment depending on local environmental conditions. Finally, we found that the wAlbB genome remained stable following its introduction in a Malaysian mosquito population. Our results highlight the need for further genomic and phenotypic characterization of Wolbachia strains in order to inform ongoing Wolbachia-based programs and improve the selection of optimal strains in future field interventions. IMPORTANCE Dengue is a viral disease transmitted by Aedes mosquitoes that threatens around half of the world population. Recent advances in dengue control involve the introduction of Wolbachia bacterial symbionts with antiviral properties into mosquito populations, which can lead to dramatic decreases in the incidence of the disease. In light of these promising results, there is a crucial need to better understand the factors affecting the success of such strategies, in particular the choice of Wolbachia strain for field releases and the potential for evolutionary changes. Here, we characterized two variants of a Wolbachia strain used for dengue control that differ at the genomic level and in their ability to replicate within the mosquito. We also found no evidence for the evolution of the symbiont within the 2 years following its deployment in Malaysia. Our results have implications for current and future Wolbachia-based health interventions.
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    A wMel Wolbachia variant in Aedes aegypti from field-collected Drosophila melanogaster with increased phenotypic stability under heat stress
    Gu, X ; Ross, PA ; Rodriguez-Andres, J ; Robinson, KL ; Yang, Q ; Lau, M-J ; Hoffmann, AA (WILEY, 2022-04)
    Mosquito-borne diseases remain a major cause of morbidity and mortality. Population replacement strategies involving the wMel strain of Wolbachia are being used widely to control mosquito-borne diseases. However, these strategies may be influenced by temperature because wMel is vulnerable to heat. wMel infections in Drosophila melanogaster are genetically diverse, but few transinfections of wMel variants have been generated in Aedes aegypti. Here, we successfully transferred a wMel variant (termed wMelM) originating from a field-collected D. melanogaster into Ae. aegypti. The new wMelM variant (clade I) is genetically distinct from the original wMel transinfection (clade III), and there are no genomic differences between wMelM in its original and transinfected host. We compared wMelM with wMel in its effects on host fitness, temperature tolerance, Wolbachia density, vector competence, cytoplasmic incompatibility and maternal transmission under heat stress in a controlled background. wMelM showed a higher heat tolerance than wMel, likely due to higher overall densities within the mosquito. Both wMel variants had minimal host fitness costs, complete cytoplasmic incompatibility and maternal transmission, and dengue virus blocking under laboratory conditions. Our results highlight phenotypic differences between Wolbachia variants and wMelM shows potential as an alternative strain in areas with strong seasonal temperature fluctuations.
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    Sex-specific distribution and classification of Wolbachia infections and mitochondrial DNA haplogroups in Aedes albopictus from the Indo-Pacific
    Yang, Q ; Chung, J ; Robinson, KL ; Schmidt, TL ; Ross, PA ; Liang, J ; Hoffmann, AA ; Kittayapong, P (PUBLIC LIBRARY SCIENCE, 2022-04)
    The arbovirus vector Aedes albopictus (Asian tiger mosquito) is common throughout the Indo-Pacific region, where most global dengue transmission occurs. We analysed population genomic data and tested for cryptic species in 160 Ae. albopictus sampled from 16 locations across this region. We found no evidence of cryptic Ae. albopictus but found multiple intraspecific COI haplotypes partitioned into groups representing three Asian lineages: East Asia, Southeast Asia and Indonesia. Papua New Guinea (PNG), Vanuatu and Christmas Island shared recent coancestry, and Indonesia and Timor-Leste were likely invaded from East Asia. We used a machine learning trained on morphologically sexed samples to classify sexes using multiple genetic features and then characterized the wAlbA and wAlbB Wolbachia infections in 664 other samples. The wAlbA and wAlbB infections as detected by qPCR showed markedly different patterns in the sexes. For females, most populations had a very high double infection incidence, with 67% being the lowest value (from Timor-Leste). For males, the incidence of double infections ranged from 100% (PNG) to 0% (Vanuatu). Only 6 females were infected solely by the wAlbA infection, while rare uninfected mosquitoes were found in both sexes. The wAlbA and wAlbB densities varied significantly among populations. For mosquitoes from Torres Strait and Vietnam, the wAlbB density was similar in single-infected and superinfected (wAlbA and wAlbB) mosquitoes. There was a positive association between wAlbA and wAlbB infection densities in superinfected Ae. albopictus. Our findings provide no evidence of cryptic species of Ae. albopictus in the region and suggest site-specific factors influencing the incidence of Wolbachia infections and their densities. We also demonstrate the usefulness of ddRAD tag depths as sex-specific mosquito markers. The results provide baseline data for the exploitation of Wolbachia-induced cytoplasmic incompatibility (CI) in dengue control.
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    A decade of stability for wMel Wolbachia in natural Aedes aegypti populations
    Ross, PP ; Robinson, KM ; Yang, Q ; Callahan, AA ; Schmidt, T ; Axford, J ; Coquilleau, MA ; Staunton, K ; Townsend, M ; Ritchie, S ; Lau, M-J ; Gu, X ; Hoffmann, A ; Dimopoulos, G (PUBLIC LIBRARY SCIENCE, 2022-02-23)
    Mosquitoes carrying Wolbachia endosymbionts are being released in many countries for arbovirus control. The wMel strain of Wolbachia blocks Aedes-borne virus transmission and can spread throughout mosquito populations by inducing cytoplasmic incompatibility. Aedes aegypti mosquitoes carrying wMel were first released into the field in Cairns, Australia, over a decade ago, and with wider releases have resulted in the near elimination of local dengue transmission. The long-term stability of Wolbachia effects is critical for ongoing disease suppression, requiring tracking of phenotypic and genomic changes in Wolbachia infections following releases. We used a combination of field surveys, phenotypic assessments, and Wolbachia genome sequencing to show that wMel has remained stable in its effects for up to a decade in Australian Ae. aegypti populations. Phenotypic comparisons of wMel-infected and uninfected mosquitoes from near-field and long-term laboratory populations suggest limited changes in the effects of wMel on mosquito fitness. Treating mosquitoes with antibiotics used to cure the wMel infection had limited effects on fitness in the next generation, supporting the use of tetracycline for generating uninfected mosquitoes without off-target effects. wMel has a temporally stable within-host density and continues to induce complete cytoplasmic incompatibility. A comparison of wMel genomes from pre-release (2010) and nine years post-release (2020) populations show few genomic differences and little divergence between release locations, consistent with the lack of phenotypic changes. These results indicate that releases of Wolbachia-infected mosquitoes for population replacement are likely to be effective for many years, but ongoing monitoring remains important to track potential evolutionary changes.
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    Differential toxicological effects of natural and synthetic sources and enantiomeric forms of limonene on mosquito larvae
    Ross, PA ; Nematollahi, N ; Steinemann, A ; Kolev, SD ; Hoffmann, AA (SPRINGER, 2022-01)
    Abstract Common fragranced consumer products, such as cleaning supplies and personal care products, emit chiral compounds such as limonene that have been associated with adverse effects on human health. However, those same compounds abound in nature, and at similar concentrations as in products, but without the same apparent adverse human health effects. We investigated whether different types of limonene may elicit different biological effects. In this study, we investigated the mortality rate of mosquito larvae in response to changes in their environment. Specifically, we tested different sources of naturally occurring R-limonene and chemically synthetized limonene, containing one of its enantiomeric forms (R-, S-) in mortality bioassays with Aedes aegypti mosquito larvae. We found that a natural source of limonene extracted from oranges induced lower mortality of mosquito larvae compared to synthetic sources at the same concentration. However, enantiomeric forms did not differ in their effects on mortality. Our results provide novel evidence that natural sources of a chemical can cause lower rates of mortality than synthetic sources.
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    Limonene Emissions: Do Different Types Have Different Biological Effects?
    Nematollahi, N ; Ross, PA ; Hoffmann, AA ; Kolev, SD ; Steinemann, A (MDPI, 2021-10)
    Limonene is one of the most abundant pollutants indoors, and it contributes to the formation of additional pollutants, such as formaldehyde and photochemical smog. Limonene is commonly used in fragranced consumer products, such as cleaning supplies and air fresheners, which have also been associated with health problems. Limonene can exist in different enantiomeric forms (R-limonene and S-limonene) and be derived from different sources. However, little is known about whether different forms and sources of limonene may have different effects. This research explored whether different types of limonene, at the same concentrations, could elicit different biological effects. To investigate this question, the study employed Aedes aegypti mosquitoes, which have sophisticated olfactory abilities, in olfactometer tests of repellency/attraction. The results indicate that a synthetic source of R-limonene is more repellent than a natural source of R-limonene. In addition, synthetic sources of both R-limonene and S-limonene are not significantly different in repellency. These findings can contribute to our understanding and further exploration of the effects of a common fragrance compound on air quality and health.