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The current review of the Sterile Insect Technique (SIT) is motivated by new technologies and the recent renaissance of male release field trials, which is driving an evolution in mosquito control and regulation. Practitioners that are releasing male mosquitoes would do well to learn from past successes and failures, including political and public engagement complications. With examples that include nuanced integrations of the different technologies, e.g., combinations of Wolbachia and irradiation, it is critical that scientists understand and communicate accurately about the technologies, including their evolving management by different regulatory agencies in the USA. Some male release approaches are considered 'pesticides' and regulated by federal and state agencies, while other male release approaches are unregulated. It is important to consider how the new technologies fit with the more 'traditional' chemical applications of adulticides and larvicides. The economics of male release programs are substantially different from traditional control costs, which can be a challenge to their adoption by abatement districts. However, there is substantial need to overcome these complications and challenges, because the problem with invasive mosquitoes grows ever worse with factors that include insecticide resistance, globalization and climate change., (© The Author(s) 2021. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

The range of the mosquito Aedes aegypti continues to expand, putting more than two billion people at risk of arboviral infection. The sterile insect technique (SIT) has been used to successfully combat agricultural pests at large scale, but not mosquitoes, mainly because of challenges with consistent production and distribution of high-quality male mosquitoes. We describe automated processes to rear and release millions of competitive, sterile male Wolbachia-infected mosquitoes, and use of these males in a large-scale suppression trial in Fresno County, California. In 2018, we released 14.4 million males across three replicate neighborhoods encompassing 293 hectares. At peak mosquito season, the number of female mosquitoes was 95.5% lower (95% CI, 93.6-96.9) in release areas compared to non-release areas, with the most geographically isolated neighborhood reaching a 99% reduction. This work demonstrates the high efficacy of mosquito SIT in an area ninefold larger than in previous similar trials, supporting the potential of this approach in public health and nuisance-mosquito eradication programs.

As part of the response to autochthonous Zika transmission in the United States, the City of South Miami implemented a 6-mo period in which Wolbachia-infected WB1 Aedes aegypti (L.) males were released into an ~170-acre area. Intracellular Wolbachia bacteria infections in Ae. aegypti cause early embryonic arrest (known as cytoplasmic incompatibility [CI]) and egg hatch failure, and inundative introductions have been suggested as a potential control tool. Throughout the release period, the Ae. aegypti population was monitored within both the release area and an equivalent area that did not receive WB1 male releases. The results show a significant reduction in egg hatch at the area receiving WB1 males, which is consistent with expectations for CI. Similarly, the number of Ae. aegypti was significantly reduced at the area receiving WB1 males, relative to the untreated area. The observed population reduction and results encourage additional work and replication of the Wolbachia biopesticide approach against Ae. aegypti, as an additional tool to be integrated with existing control tools for the control of this medically important vector and nuisance pest., (© The Author(s) 2019. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

Background: The auto-dissemination approach has been shown effective at treating cryptic refugia that remain unaffected by existing mosquito control methods. This approach relies on adult mosquito behavior to spread larvicide to breeding sites at levels that are lethal to immature mosquitoes. Prior studies demonstrate that 'dissemination stations,' deployed in mosquito-infested areas, can contaminate adult mosquitoes, which subsequently deliver the larvicide to breeding sites. In some situations, however, preventative measures are needed, e.g., to mitigate seasonal population increases. Here we examine a novel approach that combines elements of autocidal and auto-dissemination strategies by releasing artificially reared, male mosquitoes that are contaminated with an insecticide., Methodology: Laboratory and field experiments examine for model-predicted impacts of pyriproxyfen (PPF) directly applied to adult male Aedes albopictus, including (1) the ability of PPF-treated males to cross-contaminate females and to (2) deliver PPF to breeding sites., Principal Findings: Similar survivorship was observed in comparisons of PPF-treated and untreated males. Males contaminated both female adults and oviposition containers in field cage tests, at levels that eliminated immature survivorship. Field trials demonstrate an ability of PPF-treated males to transmit lethal doses to introduced oviposition containers, both in the presence and absence of indigenous females. A decline in the Ae. albopictus population was observed following the introduction of PPF-treated males, which was not observed in two untreated field sites., Conclusions/significance: The results demonstrate that, in cage and open field trials, adult male Ae. albopictus can tolerate PPF and contaminate, either directly or indirectly, adult females and immature breeding sites. The results support additional development of the proposed approach, in which male mosquitoes act as vehicles for insecticide delivery, including exploration of the approach with additional medically important mosquito species. The novelty and importance of this approach is an ability to safely achieve auto-dissemination at levels of intensity that may not be possible with an auto-dissemination approach that is based on indigenous females. Specifically, artificially-reared males can be released and sustained at any density required, so that the potential for impact is limited only by the practical logistics of mosquito rearing and release, rather than natural population densities and the self-limiting impact of an intervention upon them.

Mosquito species, members of the genera Aedes, Anopheles and Culex, are the major vectors of human pathogens including protozoa (Plasmodium sp.), filariae and of a variety of viruses (causing dengue, chikungunya, yellow fever, West Nile). There is lack of efficient methods and tools to treat many of the diseases caused by these major human pathogens, since no efficient vaccines or drugs are available; even in malaria where insecticide use and drug therapies have reduced incidence, 219 million cases still occurred in 2010. Therefore efforts are currently focused on the control of vector populations. Insecticides alone are insufficient to control mosquito populations since reduced susceptibility and even resistance is being observed more and more frequently. There is also increased concern about the toxic effects of insecticides on non-target (even beneficial) insect populations, on humans and the environment. During recent years, the role of symbionts in the biology, ecology and evolution of insect species has been well-documented and has led to suggestions that they could potentially be used as tools to control pests and therefore diseases. Wolbachia is perhaps the most renowned insect symbiont, mainly due to its ability to manipulate insect reproduction and to interfere with major human pathogens thus providing new avenues for pest control. We herein present recent achievements in the field of mosquito-Wolbachia symbiosis with an emphasis on Aedes albopictus. We also discuss how Wolbachia symbiosis can be harnessed for vector control as well as the potential to combine the sterile insect technique and Wolbachia-based approaches for the enhancement of population suppression programs., (Copyright © 2013 International Atomic Energy Agency 2013. Published by Elsevier B.V. All rights reserved.)

Methoprene is a juvenile hormone analog commonly used for the control of mosquito larvae. It acts through interference with normal metamorphosis, resulting in mortality prior to and during adult emergence. Methoprene is not commonly used for the control of adult mosquitoes, due to an absence of acute effects. Here, we have evaluated for chronic effects caused by the exposure of adult Aedes aegypti mosquitoes to methoprene. We applied methoprene to adults, both through 1) topical application to the abdomen and 2) as an aerosol, examining for treatment effects on ovary development, adult longevity, and fecundity. The results demonstrate that relatively high doses are required to affect adult survivorship. In contrast, significant impacts on both fecundity and egg hatch were observed in females treated at the lower dosages. We discuss the results in relation to autocidal strategies for mosquito control in which the release of fecund females is to be avoided.

Recent releases of mosquitoes infected with different Wolbachia types into Australia have led to conditions that have not been observed naturally and that have not been considered theoretically. In an ongoing public health campaign, two Wolbachia infection types have been introduced, and the infections differ in their fitness cost imposed on the host mosquito. The dynamics of each infection type as it interacts with the indigenous uninfected host population have been previously examined via models and empirical tests. Here we conduct a modeling analysis to predict the dynamics when the two infection types do not remain geographically isolated. The results demonstrate the potential replacement and loss of the more costly infection type, which may not be the desired public health outcome.

Background: Aedes polynesiensis is the primary vector of Wuchereria bancrofti in the South Pacific and an important vector of dengue virus. An improved understanding of the mosquito population genetics is needed for insight into the population dynamics and dispersal, which can aid in understanding the epidemiology of disease transmission and control of the vector. In light of the potential release of a Wolbachia infected strain for vector control, our objectives were to investigate the microgeographical and temporal population genetic structure of A. polynesiensis within the Society Islands of French Polynesia, and to compare the genetic background of a laboratory strain intended for release into its population of origin., Methods: A panel of eight microsatellite loci were used to genotype A. polynesiensis samples collected in French Polynesia from 2005-2008 and introgressed A. polynesiensis and Aedes riversi laboratory strains. Examination of genetic differentiation was performed using F-statistics, STRUCTURE, and an AMOVA. BAYESASS was used to estimate direction and rates of mosquito movement., Results: FST values, AMOVA, and STRUCTURE analyses suggest low levels of intra-island differentiation from multiple collection sites on Tahiti, Raiatea, and Maupiti. Significant pair-wise FST values translate to relatively minor levels of inter-island genetic differentiation between more isolated islands and little differentiation between islands with greater commercial traffic (i.e., Tahiti, Raiatea, and Moorea). STRUCTURE analyses also indicate two population groups across the Society Islands, and the genetic makeup of Wolbachia infected strains intended for release is similar to that of wild-type populations from its island of origin, and unlike that of A. riversi., Conclusions: The observed panmictic population on Tahiti, Raiatea, and Moorea is consistent with hypothesized gene flow occurring between islands that have relatively high levels of air and maritime traffic, compared to that of the more isolated Maupiti and Tahaa. Gene flow and potential mosquito movement is discussed in relation to trials of applied autocidal strategies.

Background: Lymphatic filariasis (LF) is a globally significant disease, with 1.3 billion persons in 83 countries at risk. A coordinated effort of administering annual macrofilaricidal prophylactics to the entire at-risk population has succeeded in impacting and eliminating LF transmission in multiple regions. However, some areas in the South Pacific are predicted to persist as transmission sites, due in part to the biology of the mosquito vector, which has led to a call for additional tools to augment drug treatments. Autocidal strategies against mosquitoes are resurging in the effort against invasive mosquitoes and vector borne disease, with examples that include field trials of genetically modified mosquitoes and Wolbachia population replacement. However, critical questions must be addressed in anticipation of full field trials, including assessments of field competitiveness of transfected males and the risk of unintended population replacement., Methodology/principal Findings: We report the outcome of field experiments testing a strategy that employs Wolbachia as a biopesticide. The strategy is based upon Wolbachia-induced conditional sterility, known as cytoplasmic incompatibility, and the repeated release of incompatible males to suppress a population. A criticism of the Wolbachia biopesticide approach is that unintended female release or horizontal Wolbachia transmission can result in population replacement instead of suppression. We present the outcome of laboratory and field experiments assessing the competitiveness of transfected males and their ability to transmit Wolbachia via horizontal transmission., Conclusions/significance: The results demonstrate that Wolbachia-transfected Aedes polynesiensis males are competitive under field conditions during a thirty-week open release period, as indicated by mark, release, recapture and brood-hatch failure among females at the release site. Experiments demonstrate the males to be 'dead end hosts' for Wolbachia and that methods were adequate to prevent population replacement at the field site. The findings encourage the continued development and extension of a Wolbachia autocidal approach to additional medically important mosquito species.

Adult numbers and sizes of mosquitoes were monitored for 2 yr in neighboring habitats on the western coast of Raiatea (Society Archipelago) in anticipation of testing new vector control technologies. Aedes polynesiensis Marks females comprised the overwhelming majority (approximately 99%) of the three species of mosquitoes captured in Biogent Sentinel traps placed at fixed sites on three small satellite islands (motus) of the western lagoon and on the shoreline of Raiatea. Aedes polynesiensis males, Aedes aegypti (L.), and Culex quinquefasciatus Say rarely were collected. Numbers of Ae. polynesiensis females per collection differed among trapping dates and locations, with the majority of females captured on two motus, Horea and Toamaro. Shoreline and Horea females had significantly longer mean wing lengths than females from Tiano and Toamaro. Thus, wing lengths were influenced more by local developmental conditions than overall numbers of adults. Significantly more females were captured during the wet season than the dry season. Nonetheless, at least on the two highly productive motus, dry-season females had larger wing lengths than their wet season counterparts. Local weather patterns predicted about half the variation in mosquito numbers. Differences in vector abundance observed when comparing neighboring motus are likely because of differences in human activity and mosquito suppression.

Background: Lymphatic filariasis (LF), a global public health problem affecting approximately 120 million people worldwide, is a leading cause of disability in the developing world including the South Pacific. Despite decades of ongoing mass drug administration (MDA) in the region, some island nations have not yet achieved the threshold levels of microfilaremia established by the World Health Organization for eliminating transmission. Previously, the generation of a novel Aedes polynesiensis strain (CP) infected with an exogenous type of Wolbachia has been described. The CP mosquito is cytoplasmically incompatible (i.e., effectively sterile) when mated with wildtype mosquitoes, and a strategy was proposed for the control of A. polynesiensis populations by repeated, inundative releases of CP males to disrupt fertility of wild females. Such a strategy could lead to suppression of the vector population and subsequently lead to a reduction in the transmission of filarial worms., Methodology/principal Findings: CP males and F1 male offspring from wild-caught A. polynesiensis females exhibit near equal mating competitiveness with F1 females under semi-field conditions., Conclusions/significance: While laboratory experiments are important, prior projects have demonstrated the need for additional testing under semi-field conditions in order to recognize problems before field implementation. The results reported here from semi-field experiments encourage forward progression toward small-scale field releases.

Background: Lymphatic filariasis (LF) is a leading cause of disability in South Pacific regions, where >96% of the 1.7 million population are at risk of LF infection. As part of current global campaign, mass drug administration (MDA) has effectively reduced lymphatic filiariasis prevalence, but mosquito vector biology can complicate the MDA strategy. In some regions, there is evidence that the goal of LF elimination cannot be attained via MDA alone. Obligate vector mosquitoes provide additional targets for breaking the LF transmission cycle, but existing methods are ineffective for controlling the primary vector throughout much of the South Pacific, Aedes polynesiensis., Methodology/principal Findings: Here we demonstrate that interspecific hybridization and introgression results in an A. polynesiensis strain ('CP' strain) that is stably infected with the endosymbiotic Wolbachia bacteria from Aedes riversi. The CP strain is bi-directionally incompatible with naturally infected mosquitoes, resulting in female sterility. Laboratory assays demonstrate that CP males are equally competitive, resulting in population elimination when CP males are introduced into wild type A. polynesiensis populations., Conclusions/significance: The findings demonstrate strategy feasibility and encourage field tests of the vector elimination strategy as a supplement to ongoing MDA efforts.

Genetic strategies that reduce or block pathogen transmission by mosquitoes are being investigated as a means to augment current control measures. Strategies of vector suppression and replacement are based upon intracellular Wolbachia bacteria, which occur naturally in many insect populations. Maternally inherited Wolbachia have evolved diverse mechanisms to manipulate host insect reproduction and promote infection invasion. One mechanism is cytoplasmic incompatibility (CI) through which Wolbachia promotes infection spread by effectively sterilizing uninfected females. In a prior field test, releases of Wolbachia-infected males were used to suppress a field population of Culex pipiens. An additional strategy would employ Wolbachia as a vehicle to drive desired transgenes into vector populations (population replacement). Wolbachia-based population suppression and population replacement strategies require an ability to generate artificial Wolbachia associations in mosquitoes. Here, we demonstrate a technique for transferring Wolbachia (transfection) in a medically important mosquito species: Aedes albopictus (Asian tiger mosquito). Microinjection was used to transfer embryo cytoplasm from a double-infected Ae. albopictus line into an aposymbiotic line. The resulting mosquito line is single-infected with the wAlbB Wolbachia type. The artificially generated infection type is not known to occur naturally and displays a new CI crossing type and the first known example of bidirectional CI in Aedes mosquitoes. We discuss the results in relation to applied mosquito control strategies and the evolution of Wolbachia infections in Ae. albopictus.

Aedes aegypti continues to spread globally and remains a challenge to control, in part due to its 'cryptic behavior' in that it often deposits eggs (oviposits) in larval habitats that are difficult to find and treat using traditional methods. Auto-dissemination strategies target these cryptic breeding sites by employing mosquitoes to deliver lethal doses of insecticide. This report describes the initial field trials of an application known as Autodissemination Augmented by Males (ADAM), utilizing A. aegypti males dusted with pyriproxyfen (PPF). Findings presented here are drawn from both caged and field trial studies. Together, these trials examined for the ability of A. aegypti males to disseminate PPF and to impact field populations. PPF-dusted males were able to effectively deliver lethal doses of PPF to oviposition sites under the conditions tested. Results from field trials in Florida and California demonstrated reduced A. aegypti populations in treated areas, compared to areas where PPF-treated males were not released. These results indicate that the release of PPF-dusted A. aegypti males can impact A. aegypti populations as measured by both reduced larval survival and lower numbers of adult female A. aegypti. We propose the ADAM approach as an addition to existing mosquito control techniques targeting A. aegypti and other mosquitoes that utilize cryptic larval habitats.

The mosquito family Culicidae is divided into 2 subfamilies named the Culicinae and Anophelinae. Nix , the dominant male-determining factor, has only been found in the culicines Aedes aegypti and Aedes albopictus , 2 important arboviral vectors that belong to the subgenus Stegomyia. Here we performed sex-specific whole-genome sequencing and RNAseq of divergent mosquito species and explored additional male-inclusive datasets to investigate the distribution of Nix. Except for the Culex genus, Nix homologs were found in all species surveyed from the Culicinae subfamily, including 12 additional species from 3 highly divergent tribes comprising 4 genera, suggesting Nix originated at least 133 to 165 million years ago (MYA). Heterologous expression of 1 of 3 divergent Nix open reading frames (ORFs) in Ae. aegypti resulted in partial masculinization of genetic females as evidenced by morphology and doublesex splicing. Phylogenetic analysis suggests Nix is related to femaleless (fle), a recently described intermediate sex-determining factor found exclusively in anopheline mosquitoes. Nix from all species has a conserved structure, including 3 RNA-recognition motifs (RRMs), as does fle. However, Nix has evolved at a much faster rate than fle. The RRM3 of both Nix and fle are distantly related to the single RRM of a widely distributed and conserved splicing factor transformer-2 (tra2). The RRM3-based phylogenetic analysis suggests this domain in Nix and fle may have evolved from tra2 or a tra2 -related gene in a common ancestor of mosquitoes. Our results provide insights into the evolution of sex determination in mosquitoes and will inform broad applications of mosquito-control strategies based on manipulating sex ratios toward nonbiting males. [ABSTRACT FROM AUTHOR]

Prior studies have demonstrated that Wolbachia, a commonly occurring bacterium capable of manipulating host reproduction, can affect life history traits in insect hosts, which in turn can have population‐level effects. Effects on hosts at the individual level are predicted to impact population dynamics, but the latter has not been examined empirically. Here, we describe a biological model system based on Aedes albopictus (Asian tiger mosquito) that allows for measurement of population dynamics, which has not been accomplished in prior field trials or laboratory designs. The results demonstrate the studied populations to be robust and allow for persistent, closed populations with overlapping generations, which are regulated solely through density‐dependent, intraspecific competition for limited resources. Using a novel experimental design, we compare populations that are either uninfected or infected with Wolbachia. The results show differences that include population size, eclosion rates, adult survivorship, and fecundity. The aposymbiotic populations were generally larger and adults longer lived relative to the infected populations. The outcome is discussed in context with naturally occurring Wolbachia invasions, proposed autocidal strategies, and the utility of the developed system as a biological platform for hypothesis testing and improved parameterization. [ABSTRACT FROM AUTHOR]

Simple Summary: The release of Wolbachia trans-infected mosquitoes to the environment has demonstrated promising results in reducing the target mosquito populations. The use of boric acid toxic sugar bait is another successful and upcoming technique in mosquito control. However, the potential complementary use of the two techniques had not been evaluated. This study demonstrates the significant mortality impact of boric acid toxic sugar bait on Wolbachia trans-infected Aedes albopictus Skuse mosquitoes, thus giving important insight to program planners. The field release of Wolbachia trans-infected male mosquitoes, as well as the use of toxic sugar baits, is a novel and promising candidate technique for integrated mosquito management programs. However, the methods of action of the two techniques may not be complementary, because the Wolbachia method releases mosquitoes into the environment expecting a wild population reduction in subsequent generations while the toxic baits are intended to reduce the wild population by killing mosquitoes. This laboratory study was conducted to evaluate the effectiveness of boric acid toxic sugar baits on Wolbachia trans-infected male Aedes albopictus, relative to wild-type Ae. albopictus males. Wolbachia trans-infected (ZAP male®) and the wild-type Ae. albopictus males were exposed separately to 1% boric acid in a 10% sucrose solution in BugDorms. In the control test, the two groups were exposed to 10% sucrose solution without boric acid. Percent mortalities were counted for 24 h, 48 h and 72 h post exposure periods. The results show that 1% boric acid toxic sugar bait can effectively kill ZAP males under laboratory conditions, and the effectiveness was significantly higher after 24 h and 48 h, compared to wild-type male Ae. albopictus. This finding will help in planning and coordinating integrated mosquito management programs, including both Wolbachia trans-infected mosquito releases and the use of toxic sugar baits against Ae. albopictus. [ABSTRACT FROM AUTHOR]

Recent efforts in controlling mosquito-borne diseases focus on biocontrol strategies that incapacitate pathogens inside mosquitoes by altering the mosquito's microbiome. A case in point is the introduction of Wolbachia into natural mosquito populations in order to eliminate Dengue virus. However, whether this strategy can successfully control vector-borne diseases is debated; particularly, how artificial infection affects population dynamics of hosts remains unclear. Here, we show that natural Wolbachia infections are associated with unstable mosquito population dynamics by contrasting Wolbachia -infected versus uninfected cage populations of the Asian tiger mosquito ( Aedes albopictus ). By analyzing weekly data of adult mosquito abundances, we found that the variability of the infected populations is significantly higher than that of the uninfected. The elevated population variability is explained by increased instability in dynamics, as quantified by system nonlinearity (i.e., state-dependence). In addition, predictability of infected populations is substantially lower. A mathematical model analysis suggests that Wolbachia may alter mosquito population dynamics by modifying larval competition of hosts. These results encourage examination for effects of artificial Wolbachia establishment on mosquito populations, because an enhancement of population variability with reduced predictability could pose challenges in management. Our findings have implications for application of microbiome alterations in biocontrol programs. [ABSTRACT FROM AUTHOR]