Incompatible and sterile insect techniques combined eliminate mosquitoes

Zheng, Xiaoying; Zhang, Dongjing; Li, Yongjun; Yang, Cui; Yu, Weiwu; Xiao, Liang; Liang, Yongkang; Pan, Xiaoling; Hu, Linchao; Sun, Qiang; Wang, Xiaohua; Wei, Yingyang; Zhu, Jian; Qian, Wei; Zeng, Yan; Parker, Andrew G.; Gilles, Jérémie; Bourtzis, Kostas; Bouyer, Jérémy; Tang, Moxun; Zheng, Baodong; Yu, Jianshe; Liu, Julian; Zhuang, Jiajia; Hu, Zhigang; Zhang, Meichun; Gong, Jun-Tao; Hong, Xia; Zhang, Zhoubing; Lin, Lifeng; Liu, Qiyong; Hu, Zhiyong; Wu, Zhongdao; Baton, Luke Anthony; Hoffmann, Ary A.; Xi, Zhiyong

doi:10.1038/s41586-019-1407-9

Cited by 515 publications

(587 citation statements)

References 51 publications

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“…pipiens (Laven, 1967) by exploiting the natural variation in Wolbachia infection types between mosquitoes from different locations (Atyame et al, 2014). Other releases have used Wolbachia from a closely related species through introgression (O'Connor et al, 2012) and novel Wolbachia transinfections generated through microinjection (Mains, Brelsfoard, Rose, & Dobson, 2016;Zheng et al, 2019).…”

Section: Rele a S E S Of Novel Wolbach Ia Infec Ti On S For Vec Tormentioning

confidence: 99%

An elusive endosymbiont: DoesWolbachiaoccur naturally inAedes aegypti?

Ross

Callahan

Yang

et al. 2020

Ecology and Evolution

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Wolbachia are maternally inherited endosymbiotic bacteria found within many insect species. Aedes mosquitoes experimentally infected with Wolbachia are being released into the field for Aedes‐borne disease control. These Wolbachia infections induce cytoplasmic incompatibility which is used to suppress populations through incompatible matings or replace populations through the reproductive advantage provided by this mechanism. However, the presence of naturally occurring Wolbachia in target populations could interfere with both population replacement and suppression programs depending on the compatibility patterns between strains. Aedes aegypti were thought to not harbor Wolbachia naturally but several recent studies have detected Wolbachia in natural populations of this mosquito. We therefore review the evidence for natural Wolbachia infections in A. aegypti to date and discuss limitations of these studies. We draw on research from other mosquito species to outline the potential implications of natural Wolbachia infections in A. aegypti for disease control. To validate previous reports, we obtained a laboratory population of A. aegypti from New Mexico, USA, that harbors a natural Wolbachia infection, and we conducted field surveys in Kuala Lumpur, Malaysia, where a natural Wolbachia infection has also been reported. However, we were unable to detect Wolbachia in both the laboratory and field populations. Because the presence of naturally occurring Wolbachia in A. aegypti could have profound implications for Wolbachia‐based disease control programs, it is important to continue to accurately assess the Wolbachia status of target Aedes populations.

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Section: Rele a S E S Of Novel Wolbach Ia Infec Ti On S For Vec Tormentioning

confidence: 99%

An elusive endosymbiont: DoesWolbachiaoccur naturally inAedes aegypti?

Ross

Callahan

Yang

et al. 2020

Ecology and Evolution

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“…Of these phenotypes, two in particular have current or potential use in arthropod pest and vector control efforts and are important to the basic biology of both host and microbe, making them the subject of diverse research interest. CI, the most widespread phenotype, is currently deployed in Aedes albopictus and A. aegypti mosquitoes to reduce the incidence of vector-borne diseases (5)(6)(7)(8). These efforts have achieved early success (5,8,9), but there are potential challenges for widespread applications of CI-based vector control, including potential difficulty in spreading CI-Wolbachia strains to recalcitrant host species (10)(11)(12).…”

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confidence: 99%

Transgenic Testing Does Not Support a Role for Additional Candidate Genes in Wolbachia Male Killing or Cytoplasmic Incompatibility

2020

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Endosymbiotic bacteria in the genus Wolbachia remarkably infect nearly half of all arthropod species. They spread in part because of manipulations of host sexual reproduction that enhance the maternal transmission of the bacteria, including male killing (death of infected males) and unidirectional cytoplasmic incompatibility (CI; death of offspring from infected fathers and uninfected mothers). Recent discoveries identified several genes in prophage WO of Wolbachia (wmk, cifA, and cifB) that fully or partially recapitulate male killing or CI when transgenically expressed in Drosophila melanogaster. However, it is not yet fully resolved if other gene candidates contribute to these phenotypes. Here, we transgenically tested 10 additional gene candidates for their involvement in male killing and/or CI. The results show that despite sequence and protein architecture similarities or comparative associations with reproductive parasitism, transgenic expression of the candidates does not recapitulate male killing or CI. Sequence analysis across Wmk and its closest relatives reveals amino acids that may be important to its function. In addition, evidence is presented to propose new hypotheses regarding the relationship between wmk transcript length and its ability to kill a given host, as well as copy number of wmk homologs within a bacterial strain, which may be predictive of host resistance. Together, these analyses continue to build the evidence for identification of wmk, cifA, and cifB as the major genes that have thus far been shown to cause reproductive parasitism in Wolbachia, and the transgenic resources provide a basis for further functional study of phage WO genes. IMPORTANCE Wolbachia are widespread bacterial endosymbionts that manipulate the reproduction of diverse arthropods to spread through a population and can substantially shape host evolution. Recently, reports identified three prophage WO genes (wmk, cifA, and cifB) that transgenically recapitulate many aspects of reproductive manipulation in Drosophila melanogaster. Here, we transgenically tested 10 additional gene candidates for CI and/or male killing in flies. The results yield no evidence for the involvement of these gene candidates in reproductive parasitism, bolstering the evidence for identification of the cif and wmk genes as the major factors involved in their phenotypes. In addition, evidence supports new hypotheses for prediction of male-killing phenotypes or lack thereof based on wmk transcript length and copy number. These experiments inform efforts to understand the full basis of reproductive parasitism for basic and applied purposes and lay the foundation for future work on the function of an interesting group of Wolbachia and phage WO genes.

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“…Recently, the use of an artificial triple- Wolbachia infection combined with the sterile insect technique (SIT) for population suppression interventions demonstrated a successful reduction of Ae. albopictus population density in open field trials in China (38). Additionally, positive results of IIT (Incompatible Insect Technique) for population suppression were also obtained after preliminary trials in Italy of released of Ae.…”

Section: Discussionmentioning

confidence: 99%

WolbachiastrainwAu efficiently blocks arbovirus transmission inAedes albopictus

Mancini

Herd

Ant

et al. 2019

Preprint

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10 11 The global incidence of arboviral diseases transmitted by Aedes mosquitoes, including dengue, 12 chikungunya, yellow fever, and Zika, has increased dramatically in recent decades. The release 13 of Aedes aegypti carrying the maternally inherited symbiont Wolbachia as an intervention to 14 control arboviruses is being trialled in several countries. However, these efforts are 15 compromised in many endemic regions due to the co-localization of the secondary vector 16 Aedes albopictus, the Asian tiger mosquito. Ae. albopictus has an expanding global distribution 17 following incursions into a number of new territories. To date, only the wMel and wPip strains 18 of Wolbachia have been reported to be transferred into and characterized in this vector. A 19 Wolbachia strain naturally infecting Drosophila simulans, wAu, was selected for transfer into 20 a Malaysian Ae. albopictus line to create a novel triple-strain infection. The newly generated 21 line showed self-compatibility, moderate fitness cost and complete resistance to Zika and 22 dengue infections. 23 24 Author summary 25 Aedes albopictus, the invasive Asian tiger mosquito, is responsible for numerous outbreaks of 26 important viruses such as dengue and Zika in various regions of the world. The need for 27 alterative control interventions propelled the development of a novel approach that exploits a 28 natural insect symbiont, Wolbachia; when transferred into non-native hosts, these maternally-29 inherited bacteria are able to interfere with the transmission of mosquito-borne viruses, and 30 also provide reproductive advantages to the host, offering a promising tool for self-sustaining 31 field applications. Currently, several field trials are ongoing for the primary vector of dengue 32 and several other arboviruses, Aedes aegypti, providing encouraging results. In this study, Ae.33 albopictus has been targeted for a similar approach: this mosquito species naturally carries two 34 strains of Wolbachia. The artificial introduction of a third, non-native strain made this line less 35 able to transmit dengue and Zika viruses and had an impact on its fitness. 37Introduction 38 The Asian tiger mosquito Aedes albopictus is an increasingly prominent vector of arboviruses.39 This anthropophilic and peridomestic mosquito species is an aggressive daytime biter with a 40 capacity to invade both temperate and tropical areas by adapting to different climates and 41 producing overwintering eggs. It originates in Asia, but is now widely distributed across 42 Europe, Africa, the Americas and the Pacific, and the identified transboundary mechanisms 43 involved in its expansion contribute to a high invasiveness and ever-increasing geographic 44 range (1, 2). 45 Ae. albopictus has been incriminated as a vector of more than 20 arboviruses (3); it acted as 46 the primary vector of some lineages of chikungunya virus (CHIKV) during outbreaks in La 47 Reunion (4, 5) and Italy (6). It is also a well-characterized secondary vector of dengue virus 48 (DENV) (7), with similar compe...

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Incompatible and sterile insect techniques combined eliminate mosquitoes

Cited by 515 publications

References 51 publications

An elusive endosymbiont: DoesWolbachiaoccur naturally inAedes aegypti?

An elusive endosymbiont: DoesWolbachiaoccur naturally inAedes aegypti?

Transgenic Testing Does Not Support a Role for Additional Candidate Genes in Wolbachia Male Killing or Cytoplasmic Incompatibility

WolbachiastrainwAu efficiently blocks arbovirus transmission inAedes albopictus

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