Efficient production of male Wolbachia-infected Aedes aegypti mosquitoes enables large-scale suppression of wild populations

Crawford, Jacob E.; Clarke, David W; Criswell, Victor; Desnoyer, Mark; Cornel, Devon; Deegan, Brittany; Gong, Kyle; Hopkins, Kaycie C.; Howell, Paul; Hyde, Justin S; Livni, Josh; Behling, Charlie; Benza, Renzo; Chen, Willa; Dobson, Karen L; Eldershaw, Craig; Greeley, Daniel; Han, Yi; Hughes, Bridgette; Kakani, Evdoxia G.; Karbowski, Joe; Kitchell, Angus; Lee, Erika; Lin, Teresa; Liu, Jianyi; Lozano, Martin; Macdonald, W. W.; Mains, James W.; Metlitz, Matty; Mitchell, Sara N.; Moore, David J.; Ohm, Johanna R.; Parkes, Kathleen; Porshnikoff, Alexandra; Robuck, Chris; Sheridan, Martin; Sobecki, Robert; Smith, Peter H.; Stevenson, Jessica; Sullivan, Jordan; Wasson, Brian; Weakley, Allison M.; Wilhelm, Mark; Won, Joshua; Yasunaga, Ari; Chan, William C; Holeman, Jodi; Snoad, Nigel; Upson, Linus; Zha, Tiantian; Dobson, Stephen L.; Mulligan, F Steven; Massaro, Peter; White, Bradley J.

doi:10.1038/s41587-020-0471-x

Cited by 248 publications

(299 citation statements)

References 40 publications

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“…For example, there is a more than 200-fold range in Wolbachia titer across Drosophila melanogaster samples, consistent with previous estimates of titer in another Drosophila species [61]. Similarly, our results are in the range of previous estimates of Wolbachia titer in Aedes Aegypti [62]. To determine the degree to which host species influences variation in titer, we fit a generalized linear model to the data (Supplementary Table S14).…”

Section: Comparative Study Of Titer Across Symbiont Taxasupporting

confidence: 88%

Deep data mining reveals variable abundance and distribution of microbial reproductive manipulators within and among diverse host species

Medina

Russell

Aswadhati

et al. 2019

Preprint

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Bacterial symbionts that manipulate the reproduction of their hosts to increase their successful transmission are important factors in invertebrate ecology and evolution. In light of their use as a biological control agent, studying the genomic and phenotypic diversity of reproductive manipulators can improve efforts to control infectious diseases and contribute to our understanding of host-symbiont evolution. Despite the vast genomic and phenotypic diversity of reproductive manipulators, only a handful of Wolbachia strains are used as biological control agents because little is known about the broad scale infection frequencies of these bacteria in nature. Here we develop a data mining approach to quantify the number of arthropod and nematode host species available on the Sequence Read Archive (SRA) that are infected with Wolbachia and other reproductive manipulators such as Rickettsia and Spiroplasma. Across the entire database, we found reproductive manipulators infected 1733 arthropod and 103 nematode samples, representing 121 and 10 species, respectively. We estimated that Wolbachia infects approximately 24% of all arthropod species and 20% of all nematode species. In contrast, we estimated other reproductive manipulators infect 0-8% of arthropod and nematode species. We show that relative Wolbachia density within hosts, titer, is significantly lower than the titer of the other reproductive manipulators. Considering the fitness costs of high titers, low titer may contribute to enabling Wolbachia's high prevalence across hosts species and mitigate impacts on host biology compared with other reproductive manipulator taxa. Our study demonstrates that data mining is a powerful tool for understanding host-symbiont coevolution and opens an array of previously inaccessible questions for further analysis. IntroductionBacterial symbionts of eukaryotic hosts exhibit an impressive array of phenotypes that interact with host biology. Included among these symbionts are bacteria that alter host reproduction in order to increase their likelihood of transmission to the next host generation [1-4], a strategy termed reproductive manipulation. Depending on the nature of host reproduction, reproductive manipulators are generally transmitted vertically by associating with either the oocyte or developing embryos [5]. Manipulative phenotypes range from strategies that prevent the survival of uninfected offspring, such as cytoplasmic incompatibility, to strategies such as feminization, male killing, and parthenogenesis, that actually change the sex ratio to favor females for overall increased infection rates [1][2][3][4]. These drastic manipulations to normal host biology mean that reproductive manipulators can induce reproductive isolation, drive changes in sexuality, and alter reproductive ecology in their hosts [6][7][8].

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Section: Comparative Study Of Titer Across Symbiont Taxasupporting

confidence: 88%

Deep data mining reveals variable abundance and distribution of microbial reproductive manipulators within and among diverse host species

Medina

Russell

Aswadhati

et al. 2019

Preprint

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“…Whole genomic DNA from individual adult mosquito samples was extracted using the QIAGEN Blood and Tissue kit (Qiagen, Hilden, Germany) following the manufacturer's instructions. PCR-free sequencing libraries were prepared using a custom pipeline including the TruSeq DNA PCR-Free kit (Illumina) [65]. Samples were sequenced on the Illumina HiSeqX sequencing platform pooling 32 samples per flowcell at Verily Life Sciences (South San Francisco, CA) resulting in an average of 100 million 150-bp reads per sample as previously described [12].…”

Section: Mosquito Samples and Dna Preparationmentioning

confidence: 99%

Improved reference genome of the arboviral vector Aedes albopictus

et al. 2020

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Background: The Asian tiger mosquito Aedes albopictus is globally expanding and has become the main vector for human arboviruses in Europe. With limited antiviral drugs and vaccines available, vector control is the primary approach to prevent mosquito-borne diseases. A reliable and accurate DNA sequence of the Ae. albopictus genome is essential to develop new approaches that involve genetic manipulation of mosquitoes. Results: We use long-read sequencing methods and modern scaffolding techniques (PacBio, 10X, and Hi-C) to produce AalbF2, a dramatically improved assembly of the Ae. albopictus genome. AalbF2 reveals widespread viral insertions, novel microRNAs and piRNA clusters, the sex-determining locus, and new immunity genes, and enables genome-wide studies of geographically diverse Ae. albopictus populations and analyses of the developmental and stage-dependent network of expression data. Additionally, we build the first physical map for this species with 75% of the assembled genome anchored to the chromosomes. Conclusion: The AalbF2 genome assembly represents the most up-to-date collective knowledge of the Ae. albopictus genome. These resources represent a foundation to improve understanding of the adaptation potential and the epidemiological relevance of this species and foster the development of innovative control measures.

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“…This has led to inundative field-releases of Wb -infected mosquitoes as a potential control strategy for Ae. aegypti , either by population suppression ( Crawford et al 2020 ) or by population replacement ( World Mosquito Program 2017 , Nazni et al 2019 , Ryan et al 2019 ).…”

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confidence: 99%

Wolbachia in Native Populations of Aedes albopictus (Diptera: Culicidae) From Yucatan Peninsula, Mexico

Puerta-Guardo

Contreras-Perera

Pérez-Carrillo

et al. 2020

Journal of Insect Science

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This study reports the results of a molecular screening for Wolbachia (Wb) infection in Aedes albopictus (Skuse) populations recently established in the Yucatan Peninsula, Mexico. To do so, collections of free-flying adults with BG traps and emerged adults from eggs after ovitrap field collections were performed in three suburban localities of the city of Merida, Yucatan. Overall, local populations of Ae. albopictus present a natural Wb infection rate of ~40% (18 of 45). Wb infection was detected in both field-collected adults (76.5%, 13 of 17) and eggs reared (17.8%, 5 of 28) and in 37.9% (11/29) of females and 43.7% (7/16) of male Ae. albopictus mosquitoes. An initial screening for Wolbachia strain typing showed that native Ae. albopictus were naturally coinfected with both wAlbA and wAlbB strains. The knowledge of the prevalence and diversity of Wolbachia strains in local populations of Aedes mosquitoes is part of the baseline information required for current and future Wolbachia-based vector control approaches to be conducted in Mexico.

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Efficient production of male Wolbachia-infected Aedes aegypti mosquitoes enables large-scale suppression of wild populations

Cited by 248 publications

References 40 publications

Deep data mining reveals variable abundance and distribution of microbial reproductive manipulators within and among diverse host species

Deep data mining reveals variable abundance and distribution of microbial reproductive manipulators within and among diverse host species

Improved reference genome of the arboviral vector Aedes albopictus

Wolbachia in Native Populations of Aedes albopictus (Diptera: Culicidae) From Yucatan Peninsula, Mexico

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