The sterile insect technique (SIT) and the incompatible insect technique (IIT) are emerging and potentially revolutionary tools for controlling Aedes aegypti (L.), a prominent worldwide mosquito vector threat to humans that is notoriously difficult to reduce or eliminate in intervention areas using traditional integrated vector management (IVM) approaches. Here we provide an overview of the discovery, development, and application of SIT and IIT to Ae. aegypti control, and innovations and advances in technology, including transgenics, that could elevate these techniques to a worldwide sustainable solution to Ae. aegypti when combined with other IVM practices.

Aedes aegypti (L.) is a prominent worldwide human disease vector that consistently eludes escalating and intensive population reduction and elimination efforts by public health vector control agencies. A principal foundation of the difficulty of control of Ae. aegypti populations is the ubiquity of and reliance on traditional integrated vector management (IVM) measures that apply pesticides to control this species. Cryptic peri-domestic habitats exploited by Ae. aegypti for immature development and adult resting (Harwood et al. 2016) are difficult or impossible to reach with standard adulticide and larvicide applications and can evoke strong opposition to chemical-based control by residents in the intervention area. Skip oviposition behavior (Reiter 2007) and asynchronous egg development or hatching (Gillett 1955) compound and complicate the spatial and temporal scope of larvicide treatments. Furthermore, increasing resistance to pesticide active ingredients approved by the US Environmental Protection Agency (EPA) and escalating deregistration of approved pesticides (Burkett et al. 2013) is rapidly and severely constricting the arsenal of chemical control options available to mosquito control operators. The effects of resistance and deregistration are intensified because of glacial development and registration of new effective chemical control measures, including essential oil and other EPA-exempt active ingredients (Avant 2012), which lag substantially below the rate of expansion and establishment of Ae. aegypti populations.

Fortunately, a suite of biological control techniques broadly including the sterile insect technique (SIT) and the incompatible insect technique (IIT) are gaining widespread research attention as well as increasing pilot and operational implementation across nearly every continent (Tables 1 and 2) to control populations of Ae. aegypti in support of IVM. The SIT involves what many consider a classical approach of directly sterilizing males, using either irradiation or exposure to a chemical sterilant, damaging gametic tissue. The IIT involves rendering males incompatible through either genetic manipulation (including transgenics), hybridization, or microbiota (i.e., Wolbachia) that doesn’t sterilize the males, thus leaving them able to copulate with their conspecifics under the proper conditions. The difference between the two techniques is that for the classical SIT, the males and/or females are rendered sterile from the treatment, which may also damage somatic tissue. For IIT, it is the combination of incompatible heritable factors (i.e., genes or microbiota) that alters female fertility or the successful development of immatures into adulthood.

Table 1.

The first area-wide programs, conducted in the 1960s and 1970s, implemented the sterile insect technique (SIT) to control Aedes aegypti. These programs failed and were abandoned because of limitations in the understanding of radiation dose and lack of public support.

The first area-wide programs, conducted in the 1960s and 1970s, implemented the sterile insect technique (SIT) to control Aedes aegypti. These programs failed and were abandoned because of limitations in the understanding of radiation dose and lack of public support.
The first area-wide programs, conducted in the 1960s and 1970s, implemented the sterile insect technique (SIT) to control Aedes aegypti. These programs failed and were abandoned because of limitations in the understanding of radiation dose and lack of public support.
Table 2.

Implemented and planned area-wide programs conducted since 2010 after an approximately 35-yr hiatus that apply the sterile insect technique (SIT) or the incompatible insect technique (IIT) to control Aedes aegypti populations around the world.

Implemented and planned area-wide programs conducted since 2010 after an approximately 35-yr hiatus that apply the sterile insect technique (SIT) or the incompatible insect technique (IIT) to control Aedes aegypti populations around the world.
Implemented and planned area-wide programs conducted since 2010 after an approximately 35-yr hiatus that apply the sterile insect technique (SIT) or the incompatible insect technique (IIT) to control Aedes aegypti populations around the world.

Both SIT and IIT, with some exceptions, center on releasing overwhelming numbers of colony-reared males that are attractive to wild-type females but have been sterilized (SIT) or are otherwise reproductively incompatible (IIT) with those females, leading to reduction in egg production or production of inviable eggs or offspring, which eventually suppresses or even eliminates the target Ae. aegypti population. Conspecific males are used, so the biology of the target organism itself is exploited to locate females specifically. No pesticides are used, so no resistance to pesticide should evolve, although some data exist on evolution of wild-type females to avoid or downselect sterile males (Hibino et al. 1991). Depending on the technique, SIT, IIT, or combined SIT/IIT programs can be developed and implemented with few or no regulatory obstacles, but all techniques share the requirement of a long view (of population elimination or replacement), funding, and support for as long as a defined human population needs to be protected from Ae. aegypti. In this overview we present a brief history of the discovery and development of SIT and IIT, their advantages and disadvantages, case studies of historical and recent pilot or operational implementations, and our view of the way forward to elevate these tools to increasingly higher efficacy to complement and address the weaknesses of IVM.

Discovery and early development:

The SIT grew from the extension of seminal discoveries on the effect of x-ray radiation on mammalian fertility (Albers-Schönberg 1903) into investigations of the impact of radiation on insects. Early work exposing houseflies, Musca domestica L. (Axenfeld 1896) or the European ant, Formica sanguinea Latreille (Forel and Dufour 1902) to x-rays resulted in no observed life history effects. Hunter (1912) conducted several experiments exposing a variety of arthropods to x-rays, including vectors of human and veterinary diseases such as Dermacentor andersoni Stiles (as Dermacentor venustus), Argas miniatus Koch, Rhipicephalus annulatus (Say) (as Margaropus annulatus), and Culex pipiens L., which yielded no conclusive evidence that radiation affected fertility as had been observed in mammals. Students of Hunter’s continued this work with cigarette beetles, Lassioderma serricorne (Fabricius) in Tampa, FL, but similarly found no evidence of reproductive impact (Morgan and Runner 1913). However, a key turning point in the technology was reached when a more stable x-ray tube was used that delivered consistent output and produced sterility in the cigarette beetles (Runner 1916). The mechanism of x-ray–induced sterility was teased out by H. J. Muller, who identified dominant lethal mutations generated in Drosophila melanogaster Meigen in somatic cells (Muller 1927) and gametes after exposure to radiation, causing a lack of development in zygotes (Muller 1954). The radiation broke chromosomes and created sticky ends that would reattach and generate deleterious mutations.

Use of radiation for control of insect pests by damaging gametic chromosomes through radiation exposure was first proposed by Serebrovsky (1940); however, he was not able to fully explore the possibility of his hypothesis before his death in 1948.

First application of x-ray sterilization to insect control:

The first application of radiation-based sterilization was conducted on Sanibel Island, FL, in 1951 against the New World screwworm fly, Cochliomyia hominivorax (Coquerel). However, these efforts fell short and only ca. 80% eradication was achieved (Bushland 1960). The first successful broad application eradication of a population from an area using radiation-based sterilization was conceived of and executed by E. F. Knipling from the US Department of Agriculture (USDA) targeting C. hominivorax on the island of Curaçao in 1954 (Baumhover et al. 1955). The concept of this new technique—now called the sterile insect technique (SIT)—consisted of the release of multiple cohorts of colony-reared screwworm flies that had been sterilized by exposure to x-ray radiation per Muller’s (1927) findings. The hypothesized outcome of screwworm population reduction and eventual eradication depended on successful and numerically overwhelming competition by these sterile males with fertile wild males for mating opportunities with fertile wild female screwworm flies, thus reducing the number of fertile eggs. In the absence of migration of wild types into the treated area–minimized or eliminated by conducting the study on an island–repeated releases of overwhelming numbers of sterile males were hypothesized to reduce or eliminate the target population in that area, which was observed during the 1954 investigation (Baumhover et al. 1955). Following this successful demonstration and additional positive results from field releases of sterilized screwworm fly males on Florida’s Sanibel Island and Captiva Island (Lindquist 1955), stakeholders in the livestock industry and in the USDA solicited a full area-wide SIT program to eradicate screwworm from the southern USA (Lindquist 1963), which expanded to successful eradication of this severe agricultural pest from the entire USA by 1966 (Baumhover 2001). Following elimination in the USA, plans were put in place to coordinate control efforts with Mexico to eliminate screwworm there and continue pushing the elimination zone farther south, with a new barrier being established at the narrow Darien Gap in the Isthmus of Panama (Baumhover 2001), which has persisted with few breaches to the present day.

In light of the success of area-wide control of the screwworm fly using SIT, the technique was evaluated against Ae. aegypti in an effort to expand the arsenal of control options beyond traditional IVM. Early SIT programs targeting Ae. aegypti were initiated in the 1960s and 1970s, as outlined in Table 1, but halted because of complications that prevented the success of the programs. Chief among them were lack of public support, ineffective radiation dose calibration, and poor tracking and monitoring of mosquito populations and dispersal of released irradiated males (Dame et al. 2009). It was not until 2016 that SIT was revisited to control Ae. aegypti populations (Table 2), which will be discussed later in this review.

Beyond x-rays: Other methods of sterilization:

Methods of irradiation of mosquitoes to achieve sterilization are not limited to x-ray exposure. Other methods include exposure of male mosquitoes to ionizing radiation (i.e., gamma radiation) generated from radioactive isotope sources (Darrow 1968, Bourtzis et al. 2016) or exposure to optical radiation such as through the use of an argon laser by focusing 514.5-nm wavelength microbeams for less than a second on the mosquito gonadal region (Rodriguez et al. 1989).

Other means to induce male sterility in mosquitoes such as chemosterilization have been investigated, which consists of exposing mosquitoes to chemical agents such as tepa, thiotepa, and apholate (Weidhaas and Schmidt 1963, Gato et al. 2014). Chemical sterilants function in a number of ways, for example, by causing deleterious mutations in DNA or even internal cellular damage within actively dividing somatic cells (Campion 1972). Chemical sterilization, although unlikely to disrupt male competitiveness, was primarily discontinued following concerns of sterilant bioaccumulation and nontarget sterilization (Bracken and Dondale 1972). However, de Castro Poncio et al. (2021) demonstrated a novel form of SIT that they termed natural vector control (NVC), which combined RNAi and the chemical sterilant thiotepa with the goal of reducing or eliminating the residue of the chemical sterilant in the released adults. Their experiment was successful in producing thiotepa residue-free, sterile male Ae. aegypti. Subsequent field trials in Jacarezinho, a neighborhood of Rio de Janeiro, Brazil, using the SIT NVC process resulted in a 14× reduction of human dengue incidence cases in the area compared to the control.

Why use SIT to control Ae. aegypti?:

Several advantages for incorporating SIT in IVM have been identified. First, males from local Ae. aegypti strains may be readily colonized and reared in the laboratory for sterilization and release, and will be more likely to survive in the local environment to compete with nonsterilized males compared to existing laboratory strains that may need to be purchased or otherwise obtained (Oliva et al. 2021). Sterilization of colony-reared mosquitoes is a nonregulated and nonproprietary technology, with perpetual availability limited only by funding, rearing space, and sterilization source, with no need for permits for release as can be the case with genetically modified organisms (Mains et al. 2016). When SIT is implemented with careful and routine surveillance, there is no known nontarget impact or evolution of insecticide resistance.

What factors may limit the efficacy of SIT to control Ae. aegypti?:

Several considerations need to be highlighted to understand the limits of SIT in an IVM program. For SIT to be implemented with lasting success, sustained funding and local facilities are essential to generate high numbers of healthy and competitive sterilized males over extended periods of time that are for all intents and purposes indefinite, as exemplified by the screwworm fly SIT program. In the case of radiation-based SIT, a radiation source must be purchased or leased and maintained, permitted, and available throughout the program. In addition, specialized training for operators may also require a personnel screening process for special access to equipment. Also, a hidden cost inefficiency to producing colony-reared males is that of producing and separating out females that are not needed for the next generation and will not be released in the control program. Although sterilization through radiation can be optimized to retain life history qualities of males that increase competitiveness (i.e., survivorship, longevity, energy stores, and fertility), radiation may nevertheless impact male competitiveness through disruption of somatic cells and tissue development (El-Gazzar and Dame 1983). Despite intensive and sustained release of SIT males in a prescribed area, seasonal or point immigration of the target species from adjacent or disconnected untreated areas can occur and reestablish the population (Yasuno et al. 1978).

The IIT may be considered a variation of the SIT, because the objective of both techniques is to force wild-type females to produce unfertilized or inviable eggs, reduced numbers of eggs, or inviable progeny. In contrast to SIT, which relies strictly on the release of males sterilized by radiation or chemicals to interrupt production of the next generation, IIT relies upon a variety of heritable genetic or biological phenomena that create a barrier to reproduction, such as hybridization and satyrization, cytoplasmic incompatibility, or genetic modification (such as the insertion of dominant lethal genes). Like SIT, a successful IIT program depends on long-term rearing and release of large numbers of colony-produced male mosquitoes; however, the variety of IIT approaches also present a mosaic of advantages and disadvantages that must be considered.

IIT through hybridization:

Hybridization-based IIT is accomplished with the release of males of a closely related but reproductively incompatible species capable of competing for females against males of the target species but generating inviable hybrid eggs or offspring, thus reducing the target population over time. In the first successful demonstration of this technique, Vanderplank (1947) was able to control a small population of the tsetse fly Glossina swynnertoni Austen by releasing male pupae of the closely related but reproductively incompatible species G. morsitans morsitans Westwood in G. swynnertoni habitat. This habitat is not ideal for G. m. morsitans; therefore the released individuals survived only long enough to mate with G. swynnertoni females, which was sufficient to suppress this local population. However, hybridization-based IIT is likely not appropriate for a species such as Ae. aegypti because of the challenge of identifying a closely related species that is capable of successful copulation with Ae. aegypti females followed by the production of inviable hybrid eggs or sterile hybrid offspring that can also be mass-reared in colony and be sufficiently compatible with the habitat in the intervention area.

IIT through satyrization:

Satyrization is a specific form of interspecific reproductive incompatibility in which the act of mating sterilizes females of the target species (Ribeiro 1988). The satyrization effect had been proposed as a mechanism for the displacement of Ae. aegypti by Ae. albopictus Skuse from the southeastern USA, including Texas, Louisiana, Mississippi, Alabama, and Florida in the 1980s by Nasci et al. (1989) and Tripet et al. (2011). Satyrization was proposed as an enhancement to SIT-based population control by Honma et al. (2019), and later executed by Maiga et al. (2020a) in the release of irradiated male Ae. albopictus to reduce both local Ae. albopictus and Ae. aegypti on La Réunion island. However, closer laboratory analysis revealed that the Ae. aegypti population on La Réunion had become resistant to satyrization by male Ae. albopictus.

IIT through cytoplasmic incompatibility:

The cytoplasmic incompatibility (CI) -based approach to IIT centers on a group of maternally inherited intracellular endosymbiotic bacteria from the genus Wolbachia that can be found in approximately two-thirds of insect species (Werren et al. 2008) and has been applied to Ae. aegypti population control. Wolbachia spp. can cause sterility through CI, a complex bacterial toxin-antidote system that rescues sperm to fertilize eggs harboring the same species and strain of Wolbachia (Beckmann et al. 2017). If a female does not have a Wolbachia infection or harbors a different Wolbachia strain than the male, the sperm is not rescued, and the egg is not fertilized (Chen et al. 2019). Therefore CI-based IIT consists of releasing in the intervention area large cohorts of conspecific males of the target species that harbor an incompatible strain of Wolbachia that will overwhelmingly mate with target females and potentially disrupt the target population.

Additionally, Wolbachia leveraged in an IIT program can be used for population replacement instead of population reduction. For example, successive releases of both male and female Ae. aegypti carrying a novel strain of Wolbachia into the Australian towns of Yorkey’s Knob and Gordonvale gradually replaced the wild Wolbachia strain in the local Ae. aegypti population (Hoffmann et al. 2011). As a consequence of this demonstration, the incidence of dengue decreased in and around the release locations because the novel Wolbachia strain reduced the vector competence for dengue virus in the local Ae. aegypti population (Hoffmann et al. 2011). This same technology and techniques were repeated in Yogyakarta, Indonesia, by Utarini et al. (2021), and the results were similar to those of Hoffman et al. (2011) with a reduction in virologically confirmed dengue by 77% in treatment area populations compared to control area populations. Although population replacement obviously did not eradicate the population of Ae. aegypti in the area, it reduced the risk of dengue transmission.

IIT through genetic modification:

Genetic modification–based IIT may be used to interrupt the production of a generation in Ae. aegypti mosquitoes. The most prominent example of this IIT approach is Release of Insects carrying a Dominant Lethal gene (RIDL). As described by Alphey et al. (2013), RIDL is a genetics-based tool that inserts a dominant lethal transgene that can be artificially repressed—for example, by rearing larvae in the presence of tetracycline—to allow for laboratory colonization, but when allowed to express naturally (i.e., without tetracycline) induces mortality in offspring. For example, when RIDL-modified male or female Ae. aegypti mate with wild conspecifics, their offspring inherit the dominant lethal allele, and though eggs develop and eclose, immatures did not survive past the L4 larval stage. However, a new modification of the RIDL technology allows only males to survive to the adult stage without added tetracycline (Spinner et al. 2022). This can be an advantage over traditional SIT—which would not lead to the production of larvae because eggs are inviable—in populations where larval density in immature habitat is a key limiting factor (Alphey et al. 2008).

Another form of IIT that uses genetic modification is the introduction of transgenes into a population that promote the production of homing endonucleases that lead to population elimination by destroying female chromosomes. For example, the ribosomal DNA repeat sequences found on the X chromosome can be targeted by the homing endonuclease I-PpoI from Anopheles gambiae Giles, and, by combining it with a b2t promoter and expressed in the testes, all sperm carrying an X chromosome are destroyed, leading to extremely male-biased progeny (Galizi et al. 2014).

Pros and cons of IIT:

Similar to SIT, implementing IIT allows specific targeting of a mosquito species such as Ae. aegypti with no impact on nontargets. However, unlike SIT, IIT can be developed to induce mortality in a specific life stage, as seen with RIDL, which targets late-stage larvae, allowing larval competition among conspecifics (Phuc et al. 2007, Alphey et al. 2013), or as seen with Wolbachia, which can target adult survivorship to allow procreation supporting population replacement with reduced vector competence (Hoffmann et al. 2011), and it can disrupt or limit the development of pathogens commonly transmitted by mosquitoes (Moreira et al. 2009).

Some disadvantages to the use of IIT include the difficulty of winning public support and obtaining regulatory agency licensing for genetically modified organisms or introduced novel microbiota (Alphey et al. 2002, Mains et al. 2016). Additionally, the relatively higher complexity of IIT modifications to colony-reared mosquitoes compared to those in an SIT program may require commercial production at distant facilities that do not incorporate strains local to the intervention area. Nonlocal laboratory strains may not express the same feeding, mating, and resting behaviors as the local population, thus compromising their competitiveness (Carvalho et al. 2022). Furthermore, transport of adult IIT mosquitoes from a centralized production location to distant release locations may compromise survivorship and competitiveness (Sasmita et al. 2021).

Early investigations and applications: The 1960s and 1970s:

The earliest recorded effort to apply SIT to control local populations of Ae. aegypti was conducted by Morlan et al. (1962), when they irradiated colonized male Ae. aegypti with 11,000–18,000 roentgen (equal to 96–158 Gy) from a cobalt 60 gamma source and released them in Pensacola, FL, in 1960. In 1961 Morlan et al. (1963) repeated the experiment, this time with a locally colonized Ae. aegypti strain. Unfortunately, both attempts failed to demonstrate a difference in the number of mosquitoes collected between the treatment and control sites from 1960 and 1961. It is possible that the attempts made by Morlan et al. (1962) may have been successful had they used a lower radiation exposure level, given that a dose of 50 Gy returned 99% sterile but more competitive males (i.e., longer survival rates) than those irradiated at higher doses (Chen et al. 2023).

Following the failed attempt by Morlan et al. (1962), Fay and Craig (1969) released Ae. aegypti genetically marked with autosomal variants in Meridian, MS, to investigate dispersal of released males and the acceptance of released males by wild females. Similar additional studies were conducted by Bond et al. (1970) and Hausermann et al. (1971) to investigate dispersal of genetically marked male and female Ae. aegypti. These studies were important in understanding Ae. aegypti dispersal and how to exploit their movement behavior to better release SIT mosquitoes. Bond et al. (1970) and Hausermann et al. (1971) examined the same mosquito strain in Meridian and identified socioeconomic and topographical factors in dispersal patterns of male and female Ae. aegypti documenting their propensity both to fly between 100 and 200 m and to disperse to the edge of the release area rather than remain at the release site.

Asman et al. (1981) reviewed early efforts to control wild Ae. aegypti populations using the SIT and IIT from three separate projects. The first and largest was led by the World Health Organization (WHO) and the Indian Council for Medical Research (ICMR) in New Delhi, India. The second project was led by the International Centre for Insect Physiology and Ecology (ICIPE) in Mombasa, Kenya, and the third by the USDA Agricultural Research Service laboratory in Gainesville, FL.

The ICMR program consisted of several project releases. The first release was conducted in August 1971 with colony-reared male Ae. aegypti carrying a dominant mutant marker expressing a silver lyre marking to assess whether a genetic variant strain could be successfully introduced and propagated in the field (Rai et al. 1973). Positive results from the first release supported execution of a second release later that month of the first set of heterozygous translocated male Ae. aegypti in an effort to control the population. Further attempts by the ICMR program evaluated chemosterilized males and males from additional transgenic strains for their mating competitiveness (Grover et al. 1976): In 1974, 18,000 chemosterilized males were released over six nights (3,000 per night), and chemosterilized males accounted for 90% of mates for the wild female population. However, although mating success of genetically translocated males was lower than the chemosterilized males (28–57%), males with a population distorter gene had higher mating success (46–155%) than only genetically translocated males. Overall, males with a population distorter gene and those males that were chemosterilized were as competitive with respect to mating as wild males, unlike the genetically translocated males.

The IIT program initiated by ICIPE in Kenya engineered Ae. aegypti to carry a heritable genetic translocation mechanism induced by radiation exposure and maintained by crossing to a multiple marker stock which yielded a fertility rate of 25% (McDonald et al. 1977). Several releases were carried out across three villages totaling nearly 64,000 pupae, resulting in a dramatic drop in fertility rates of eggs from 97% to 36% in one village. Lorimer et al. (1976) released Ae. aegypti with a T3–sex-linked translocation homozygote on chromosomes 1 and 3 induced from a population originating from New Delhi, India, for population replacement in Kenya in 1974–75 at the same locations investigated by McDonald et al. (1977). Lorimer et al. (1976) demonstrated released female populations of Ae. aegypti T3 had a significantly lower egg hatch rate (75%) versus the wild-type females (93%), and that the T3 females preferred to oviposit in ovitraps placed to monitor oviposition rather than within the clay water storage pots in homes in the intervention area. However, the T3 homozygote compared unfavorably with the wild-type Ae. aegypti in several measures of fitness and was unsuccessful in replacing the local population and in establishing itself in a village without wild-type Ae. aegypti (Lorimer et al. 1976).

The two investigations conducted by the USDA in Florida tested competitiveness in the field of male Ae. aegypti carrying a T1:2-26–male-linked translocation carrying markers for red eye (re), spot (s), and black tarsi (blt) on chromosomes 1, 2, and 3, respectively. The first trial was conducted in July 1972 on an island artificially populated with the VOYLE strain, a wild-type stock generated from hundreds of field-collected mosquitoes from Gainesville, FL (Seawright et al. 1975). The T1:2-26 Ae. aegypti strain was found to be competitive against VOYLE males in mating, indicated by the reduction fertility in VOYLE females from 96.8% to 36.2% (Seawright et al. 1975). The second trial also used males carrying a single or double genetic translocation released in a cypress/pine forest 10 km north of Gainesville, FL against VOYLE Ae. aegypti (Seawright et al. 1976). The latter trial yielded similar results to Seawright et al. (1975), indicating that males carrying genetic translocations could be competitive against a form of wild-type males and reduce fertility in a form of wild-type females.

Efforts to control Ae. aegypti using SIT and/or IIT from 2010 to the present:

Following an approximately 35-yr gap, efforts resumed starting in 2010 to attempt to control Ae. aegypti using SIT and/or IIT approaches. A RIDL-based IIT investigation was conducted on Grand Cayman Island in 2010 with transgenic OX513A Ae. aegypti developed by Oxitec (Oxitec Ltd, Abingdon, United Kingdom). Approximately 3.3 million transgenic male mosquitoes were released over 56 releases and reduced the Ae. aegypti population in the intervention area by 80% compared to the control plot. Following the positive results from the investigation on Grand Cayman Island, Oxitec released RIDL Ae. aegypti (OX513A) in Brazil, Malaysia, Panama, and India (Table 2).

A new version of Ae. aegypti OX513A was later developed, termed the “friendly™ mosquito,” Ae. aegypti OX5034, that unlike its predecessor was designed to mate with wild female cohorts allowing only male offspring surviving to adulthood (Spinner et al. 2022). The original OX513A strain males could not produce offspring that survive to the adult stage unless tetracycline was added to the water to rescue the larvae (Berube 2020, Spinner et al. 2022). In 2021 Oxitec cooperated with the Florida Keys Mosquito Control District to release Ae. aegypti OX5034 to evaluate its efficacy and public reception (Micu 2020); however, the results have not yet been published.

The World Mosquito Program (WMP; formerly Eliminate Dengue: Our Problem) organized a release of Ae. aegypti infected with a novel Wolbachia endosymbiont in Yorkey’s Knob and Gordonville, Australia, in 2011 for control of dengue transmission by Ae. aegypti through population replacement as described earlier (Table 2), (Moreira 2019). Colonized male and female Ae. aegypti infected with Wolbachia wMel, isolated from Drosophila melanogaster and transferred into embryos of Ae. aegypti (Walker et al. 2011), were released to mate with wild cohorts and drive the endosymbiont into the local population by exploiting CI. Their efforts were successful and led to 100% and 90% population replacement in Yorkey’s Knob and Gordonville, respectively (Hoffman et al. 2011). These successes spurred the World Mosquito Program to develop additional novel Wolbachia infection lines in Ae. aegypti to drive pathogen-refractory Ae. aegypti into more communities to reduce disease transmission. The World Mosquito Program has collaborated with organizations and governments for additional releases in Australia, Vietnam, Indonesia, Colombia, Vanuatu, Mexico, Fiji, New Caledonia, Kiribati, and Sri Lanka and plans to release in Laos (Table 2; WMP 2021, 2022a–j). Overall, their ongoing efforts have resulted in effective population replacement followed by disease suppression (Table 2; WMP 2021, 2022a–j).

Efforts by additional groups continue to develop IIT approaches to protect public health through suppression of Ae. aegypti. MosquitoMate (MosquitoMate, Inc., Lexington, KY) partnered with Verily (South San Francisco, CA) in 2017 to develop a WolbachiawAlbB-infected Ae. aegypti strain for population suppression in Fresno, CA. Twenty million colony-reared Wolbachia-infected male Ae. aegypti were released, leading to a 68% reduction in wild-type Ae. aegypti (Table 2; Gilbert and Melton 2018). The trial was repeated in 2018 with nearly 14 million males released, leading to a 95.5% reduction in wild-type female Ae. aegypti (Table 2; Crawford et al. 2020). The MosquitoMate technique experienced additional successes in Miami, FL (Table 2; Mains et al. 2019), Key West, FL (Schairer et al. 2021), and Houston, TX (Table 2; Lozano et al. 2022).

A new SIT approach called boosted SIT, or bSIT, discussed further below, was developed for a 2016 Ae. aegypti control effort in Chachoengsao Province, Thailand (Table 2; Kittayapong et al. 2019). Briefly, the bSIT approach in this investigation consisted of releasing 437,980 males treated with a combination of gamma radiation and Wolbachia wAlbA and wAlbB over 24 wk, which led to a 97.3% reduction in the wild population (Table 2). Additional variations of bSIT-treated males targeting Ae. aegypti were developed and deployed in Yucatan, Mexico, as well as Singapore (Table 2; Ng 2021, Martín-Park et al. 2022), both projects returning successful vector control or reduction in pathogen transmission.

Mass production technology:

Both SIT and IIT depend on extensive production of quality incompatible or sterile males, and sometimes females, to be released in intervention areas. In the past, mosquito colony production demanded vast amounts of lab space and water (Morlan et al. 1963). However, the IAEA developed a protocol (Maiga et al. 2020b) and a larval-rearing apparatus to generate large numbers of mosquitoes in less space (Mamai et al. 2020). Each IAEA larval-rearing apparatus occupies 0.6 m2 and can rear approximately 300,000 ± 20,000 male mosquitoes across 5 d of pupation (Mamai et al. 2020). By contrast, an equivalent number of mosquitoes reared in a standard laboratory colony would require more than 200 41 cm × 30 cm × 8 cm plastic trays, each with 3.0 liters of deionized water and 5 m2 of floor space (Balestrino et al. 2014).

Sexing technology:

A significant and heavily targeted bottleneck of SIT and IIT programs is separation of males from females. Traditional separation techniques exploit the sexual dimorphism of Aedes spp. pupae to separate them into small (male) and large (female) cohorts using a variety of mechanisms. One separation instrument designed by Sharma et al. (1972) that consisted of square holes of a fixed width of 1,400 µm was used by Bellini et al. (2013) to separate Aedes albopictus at 24–30 h after pupation. Male Ae. aegypti have been separated by size using a device with adjustable louvered slits of aluminum sheets to allow only pupae of a certain size or smaller to pass through (McCray 1961). Another design consists of flat plate glass panels that create an adjustable wedge-shaped space capturing smaller male pupae in the narrow portion and larger female pupae in the wide portion (Fay and Morlan 1959). Importantly, variables such as larval-rearing density, temperature, or food can affect pupal cephalothorax size, making it critical to follow strict culture conditions so a given device can consistently separate males (Papathanos et al. 2009).

Sex separation of colony-reared mosquitoes has also been achieved by exploiting adult behavior. For example, adult female mosquitoes can be eliminated from a cohort by being presented a toxic (or “spiked”) bloodmeal containing boric acid or ivermectin that males will not be able to consume (Yamada et al. 2013, Gunathilaka et al. 2019). However, separation at the adult stage using this method may be compromised if pupae are irradiated because several strains of irradiated female Ae. aegypti pupae do not readily blood feed (Aldridge et al. 2020, Cunningham et al. 2020, Chen et al. 2023), although other strains may have increased blood-feeding behavior following irradiation (Moretti et al. 2022).

Computer techniques for discrimination between male and female pupae could be applied to sex-specific dimorphism separation methods (Zacarés et al. 2018). However, combining computer supported sorting with genetically modified strains shows enormous potential in production of male mosquitoes for SIT and IIT programs. For example, generation of transgenic lines containing a fluorescent protein marker linked to sex chromosomes as demonstrated by Catteruccia et al. (2005) has allowed separation of male and females visually at any stage: first instar An. gambiae larvae with a sex-linked green fluorescent protein have been sorted by sex with 100% accuracy using the complex parametric analyzer and sorter system with a flow cytometry machine, abbreviated as COPAS (Marois et al. 2012).

Genetic sorting systems have also been developed to produce strains of female-specific flightless adults that allow flight-capable males to be automatically separated from females (Fu et al. 2010). This technique was used by Labbé et al. (2012) to generate flightless Ae. albopictus and by O’Leary and Adelman (2020) to generate flightless Ae. aegypti.

Drug-induced separation of transgenic mosquitoes is another method of sex separation that we mentioned earlier: the RIDL technique (Thomas et al. 2000). Here we go into greater detail. A successful example of this technique is described by Phuc et al. (2007) where Ae. aegypti are engineered to carry a dominant, repressible, non-sex-specific, late-acting, and heritable lethal genetic system, together with an Act5C-DsRed2 fluorescent marker. If reared in the presence of 30 µg/ml tetracycline the lethal gene is repressed; tetracycline therefore acts as an “antidote” or repressor of the lethal system to allow the RIDL strain to be reared under defined conditions (Massonnet-Bruneel et al. 2013) so that they can be released and mate with wild types and produce offspring that will develop without tetracycline in the wild and die in the larval stage. In the wild, tetracycline does not occur naturally and therefore would not rescue the developing larvae from the expression of the lethal gene. More detailed information on sex sorting technologies and techniques is provided in reviews by Gilles et al. (2014) and Papathanos et al. (2018).

Drone dispersal:

Uncrewed aircraft systems (UASs) or drones have already been operationalized by mosquito and vector control districts for mosquito surveillance and applications of adulticide space sprays and solid and liquid larvicides (Aragao et al. 2020, Carrasco-Escobar et al. 2022). These devices have recently been investigated and are beginning to be operationalized for dispersal of mosquitoes for SIT and IIT programs (Bouyer et al. 2020) for both areawide and pinpoint (or “hotspot”) targeting (Garcia et al. 2022). SIT or IIT mosquitoes may be compressed into a dense puck, allowing a greater payload for release (Culbert et al. 2017). Drone dispersal of SIT and IIT mosquitoes overcomes a major barrier to ground-level dispersal of Ae. aegypti, a species that will not readily fly across roads (Russell et al. 2005, Hemme et al. 2010). Despite the many advantages of incorporating drones into SIT and IIT programs, more work needs to be done identifying, for example, optimal height for releases of mosquitoes, optimal rearing conditions to support the unique stressors of this method of dispersal, and understanding effects of drift at various heights, wind speeds, and flight velocities.

Chilling and compaction:

Optimization of packaging and preparation of mosquitoes prior to release can improve both survival during transport and performance upon release. Aedes albopictus that were chilled and compacted prior to transport showed differences in mating performance and survivorship: chilling to 5°C or 10°C for >3 h resulted in lowered competitive performance against wild males, and males chilled for >3 h demonstrated lower levels of glucose than those chilled for <3 h (Zhang et al. 2020). One strategy to mitigate the impact of chilling, compaction, and transportation is to provide a sugar meal prior to these processes (Bellini et al. 2014).

Hormesis:

Hormesis is a biological dose-response phenomenon in which exposure to a small quantity of a stressor improves subsequent performance, whereas exposure to larger quantities of the same stressor will decrease subsequent performance (i.e., low dose stimulation, high dose inhibition; Costantini et al. 2010). Furthermore, mild exposure to one stressor can induce greater protection to subsequent exposure of other stressors, known as cross-tolerance (Boardman et al. 2011). Hormesis and cross-tolerance can be leveraged to improve males reared for irradiation in an SIT program: severe hypoxia of Ae. aegypti can lead to increases in longevity following radiation exposure by reducing the number of free radicals generated due to the low oxygen atmosphere, an increase in the amount of radiation needed to achieve >95% sterility, and significantly increased competitiveness compared to wild, nonirradiated males (Tussey et al. 2022). Unfortunately, Tussey et al. (2022) did not examine hormetic effects on female Ae. aegypti; however, we speculate that female Ae. aegypti would have greater median survivorship following anoxic treatment prior to irradiation due to the disposable soma hypothesis (Kirkwood 2002), where cellular resources are diverted from reproduction to survivorship in the event reproduction has been compromised as observed in the female Caribbean fruit fly Anastrepha suspensa (Loew) (López-Martínez and Hahn 2014), the codling moth Cydia pomonella (L.) (White and Hutt 1970), and the lubber grasshopper Romalea microptera (Palisot de Beauvois) (Hatle et al. 2008).

Boosted SIT (bSIT):

SIT used in conjunction with either an enhancement of the SIT-treated organism or with another management strategy, or both, is called boosted SIT (bSIT). One example of bSIT with enhancement of the SIT organism is rearing irradiated sterile males with a probiotic diet to enhance competitiveness. Although this enhancement has not yet been applied to mosquitoes, probiotic diets that supplement gut microbiota have improved competitiveness of irradiated Tephritid fruit flies (Kyritsis et al. 2017). An example of bSIT centered on enhancing the effect of SIT-treated males with a layered management strategy is to coat males with a juvenile hormone analogue larvicide such as pyriproxyfen. Matings with wild females will hypothetically contaminate them with the larvicide, passively disseminating the formulation to cryptic immature habitats to disrupt the growth of immature mosquitoes (Bouyer and Lefrancois 2014), which models suggest could result in rapid reduction of the population (Pleydell and Bouyer 2019).

An SIT program centered on irradiated males can also be boosted by combining it with an IIT program. For example, given that female Ae. aegypti have a higher sensitivity to radiation than males (Aldridge et al. 2020), Kittayapong et al. (2019) and Zheng et al. (2019) combined SIT/IIT programs by applying radiation to sterilize mosquitoes reared for an IIT program so that incidentally released females would be more likely to be sterile. Also, as the density of mosquitoes to be irradiated increases, the amount of radiation necessary to penetrate the mass and successfully sterilize males on the interior of the irradiator chamber increases, rendering males on the exterior less competitive due to a higher dose of radiation (Yamada et al. 2019). Therefore, combining IIT males (unirradiated) with SIT irradiated males in a program potentially provides a numerical buffer for sufficient competitive males (Baton et al. 2021).

Microbiota and diet:

Variation in time to pupation, adult size, and longevity are factors documented to be influenced by microbiota of developing larvae (Souza et al. 2019). Mosquito larvae possessing no microbiome (axenic) reared in an axenic environment did not survive more than 5 days after hatching (Coon et al. 2014). By supplementing developing or adult mosquito diets with nutrients such as vitamins and minerals (Phasomkusolsil et al. 2017) or microbiota as seen in Mediterranean fruit flies (Ceratitis capitata [Wiedemann]) released for SIT (Ami et al. 2010), male performance could be optimized for SIT as mentioned earlier, providing a competitive advantage over wild-type males. Moreover, supplementing adult mosquito colony diet with a multivitamin may enhance longevity as observed in Anopheles campestris Reid, An. dirus Peyton & Harrison, and An. sawadwongporni Rattanarithikul & Green by Phasomkusolsil et al. (2017). Furthermore, microbiota have been demonstrated to indirectly influence vector competence by potentially influencing the Toll pathway tied to the innate immune system of the mosquito (Xi et al. 2008). Consequently, a notable feature of Wolbachia is that in some instances it can disrupt infection by viruses such as dengue, chikungunya, Zika, West Nile, and yellow fever viruses in the mosquito host as observed by Moreira et al. (2009), Van Den Hurk et al. (2012), and Dutra et al. (2016) and reviewed by Caragata et al. (2019), which is the primary motivation behind population replacement. But Wolbachia has also been shown to positively influence infection of West Nile virus in Culex tarsalis Coquillett (Dodson et al. 2014).

Improving SIT with models: Wave/pulse releases and buffer/corridor zones:

Optimization to a threshold level of both the number of release sites and frequency of releases can have a mathematically profound influence on the predictive efficacy of SIT programs for Ae. aegypti (Oléron Evans and Bishop 2014), due to balances among forces of recolonization of low-density mosquito areas from high-density mosquito areas and density-dependent mortality associated with large groups of released sterile males. One model suggests distribution of large single batches of sterile males into multiple smaller release sites could be beneficial, but releasing above the optimal ratio of sterile:wild males provided no benefit to control and instead leads to costly and ineffective overproduction of sterile males (Oléron Evans and Bishop 2014).

Mathematically modeled releases of mosquitoes for SIT have also identified that releasing massive numbers of sterile males within a corridor between the intervention area and an adjacent nonintervention area, while maintaining small releases within the intervention area, will mitigate immigration of wild populations that would enter the targeted intervention area (Anguelov et al. 2020).

Education/community engagement:

Successful SIT or IIT programs depend on effective engagement and education of the community where the intervention will take place (Dame et al. 2009). Without community involvement SIT or IIT programs can rapidly fail because community opinion and perception can positively or negatively shape the outcome of the program. For example, a news article authored by Dr. K. S. Jayaraman in India in 1974 accused the World Health Organization (WHO) and the US government of conducting germ warfare under the guise of scientific research in vector control through SIT (Oh, New Delhi; oh, Geneva 1975). This accusation fomented political backlash by the Indian government, and local communities were no longer receptive to the SIT projects, and the WHO did not renew tenure of the Genetic Control of Mosquitoes Research Unit facility (Tomiche 1975).

Although some programs invested heavily in community involvement and engagement to win community stakeholders, there are unfortunately examples in which successful practices for community engagement in one country may not carry over to another country and lessons from the past need to be revisited. For example, Oxitec successfully employed a community engagement program prior to the release of genetically modified Ae. aegypti in Brazil (Capurro et al. 2016), but when releases were initially attempted in Key Haven, FL, the release program stalled because of intense public pressure and had to be revised as explained by Taylor (2020). However, this project has been restarted in the Florida Keys, approved by a majority of the precincts of Monroe County (31 out of 33) and permitted by the EPA for 2021, with additional projects approved by the EPA for Florida and California in 2022 (Waltz 2022).

The priority in an SIT or IIT program is community engagement (Moreira 2019) and should be accounted for in developing the program budget. SIT program leaders should interact with the affected population, their local institutions including health clinics and schools, and their community leaders for disseminating accurate, transparent, and easily accessible information about the program. Transparency should be exemplified by a frank discussion of advantages and disadvantages compared to other approaches, as well as benefits, and risks, of the proposed program. Initially, surveys should be conducted to measure existing understanding of and acceptance by the local population. In addition, a community reference group should be organized: a local committee that monitors all actions conducted by the program and is the first to be informed by SIT/IIT program leaders so that communication channels established with the community, including telephone, e-mail, face-to-face interactions, and social media, can be engaged (Moreira 2019). Finally, a postrelease survey or questionnaire should be distributed to allow the community to provide feedback on the performance of the program (Capurro et al. 2016).

Traditional IVM and other optimizations prior to SIT/IIT release:

Proper preparation of the target area must be part of the SIT/IIT program. For example, some programs may pretreat the target area through conventional adulticide or larvicide actions prior to initial SIT/IIT releases, to bestow released cohorts the greatest chance to numerically outcompete surviving wild-type males. Another mode of optimization is to leverage findings from long-term and ongoing mosquito surveillance by local mosquito and vector control districts so that the SIT/IIT program can be ramped up and implemented early in the anticipated season for the target species, when populations are at their lowest and the released mosquitoes can be the most numerically overwhelming. However, consideration of seasonal conditions should also inform release timing and balance findings from target population level monitoring so that colony-reared mosquitoes are not negatively stressed by the release environment. It should be emphasized that given the current capabilities and ongoing development of SIT and IIT—i.e., they are not perfected and may not be successful for all targets in all places—these biological control approaches should be integrated into the full picture of IVM and not considered a panacea to mosquito control (Pleydell and Bouyer 2019, Martín-Park and Che-Mendoza 2022).

The inadequacy of traditional chemical-based IVM control techniques targeting Ae. aegypti means that it is critical we continue to develop and refine novel control strategies such as SIT and IIT. Deregistration of pesticides (Rose 2001, Usta 2013), slow development of new pesticides (Roush and Tabashnik 2012), evolution of pesticide resistance (Vontas et al. 2012), loss of funding for traditional control programs (NACCHO 2017), hesitancy or lack of support from the public toward pesticide use (Piltch-Loeb et al. 2019), and the difficulty of finding, accessing, and eliminating oviposition sources (Reiter et al. 1995) are a constellation of factors that will limit the role of traditional IVM in long-term sustainable control of Ae. aegypti populations. However, the increasing attention focused on SIT and IIT as a potential alternative or supplement to traditional IVM may steer more funding and research towards improving the techniques and expanding their operational use. In 2020 a joint commission by the IAEA and WHO generated a comprehensive guidance framework for preparing a complete SIT program and evaluating its performance for suppression of Aedes-borne diseases (WHO and IAEA 2020).

The 2010 revival of investigations and operations focused on SIT and IIT for the control of Ae. aegypti is very timely because of new technology and a public receptive to alternatives to traditional chemical control (Alphey et al. 2008, 2010). Public support can be better developed by including specific budgets for coordinated outreach and education in SIT programs (Alphey et al. 2010). Better quality radiation doses are now possible because of more efficient irradiators and calibration equipment (Klassen and Curtis 2005). Capabilities for tracking and monitoring Ae. aegypti populations and dispersal of released males in the intervention area may now be greatly enhanced with GPS and GIS technology (Klassen and Curtis 2005). Also, radiation-based SIT releases can be enhanced by combining with IIT-based strains of Ae. aegypti designed to reduce disease transmission and/or populations of the vector (Alphey et al. 2010). In addition to these new capabilities, a suite of innovations—some of which have yet to be adapted to target Ae. aegypti—is positioned to further optimize SIT and IIT approaches to the point of widespread operational implementation.

Aedes aegypti is a prominent worldwide disease vector threat that consistently eludes formidable efforts by public health vector control agencies because of the difficulty of aligning expected pesticide-based control efficacy with the unique bionomics and evolving resistance of this species. Fortunately, biological control techniques such as SIT and IIT can be used in place of or alongside pesticides and/or other traditional IVM techniques to significantly improve Ae. aegypti control programs. Both SIT and IIT are species-specific, exploiting conspecifics to seek out females, and so may overcome the limitations of pesticide applications that attempt to target Ae. aegypti in cryptic habitat or resistant populations. Release of mosquitoes sterilized by radiation does not require EPA approval and cannot be deregistered. Technological advancements continue to improve the efficacy of SIT and IIT through, for example, advancements in genetic modifications, sex sorting, movement and dispersal tracking using GIS and GPS data, refinement in radiation calibration to preserve male competitiveness, optimization of mosquito rearing conditions to increase production, performance, and survivorship, and timing releases to exploit environmental conditions that maximize performance of Wolbachia endosymbionts.

  1. Early development of radiation-based SIT was hindered by problems with radiation dose calibration and irradiation equipment malfunction.

  2. SIT has been used extensively to control a variety of veterinary and medically significant vector and pest species. With continued development, we hypothesize that additional species such as Ae. aegypti can be controlled.

  3. Bionomic, resistance, and standard IVM challenges to Ae. aegypti control may be mitigated with the SIT; however, technological and scientific breakthroughs are needed for 1) more efficient, consistent, and benign sterilization of Ae. aegypti males, 2) better tracking of dispersal and survival of released sterile males, and 3) more precise monitoring of target population dynamics, which includes detecting immigration from adjacent or disparate locations.

Albers-Schönberg
HE.
1903
.
Über eine bisher unbekannte Wirkung der Röntgenstrahlen auf den Organismus der Tiere
.
Munch Med Wochenschr
50
:
1859
1860
.
Aldridge
RL,
Kline
J,
Coburn
JM,
Britch
SC,
Boardman
L,
Hahn
DA,
Linthicum
KJ.
2020
.
Gamma-irradiation reduces survivorship, feeding behavior, and oviposition of female Aedes aegypti
.
J Am Mosq Control Assoc
36
:
152
160
.
Alphey
L,
Beard
CB,
Billingsley
P,
Coetzee
M,
Crisanti
A,
Curtis
C,
Eggleston
P,
Godfray
C,
Hemingway
J,
Jacobs-Lorena
M,
James
AA.
2002
.
Malaria control with genetically manipulated insect vectors
.
Science
298
(
5591
):
119
121
.
Alphey
L,
Benedict
M,
Bellini
R,
Clark
GG,
Dame
DA,
Service
MW,
Dobson
SL.
2010
.
Sterile-insect methods for control of mosquito-borne diseases: an analysis
.
Vector Borne Zoonotic Dis
10
:
295
311
.
Alphey
L,
McKemey
A,
Nimmo
D,
Neira Oviedo
M,
Lacroix
R,
Matzen
K,
Beech
C.
2013
.
Genetic control of Aedes mosquitoes
.
Pathogens Glob Health
107
:
170
179
.
Alphey
L,
Nimmo
D,
O’Connell
S,
Alphey
N.
2008
.
Insect population suppression using engineered insects
.
Adv Exp Med Biol
627
:
93
103
.
Ami
EB,
Yuval
B,
Jurkevitch
E.
2010
.
Manipulation of the microbiota of mass-reared Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) improves sterile male sexual performance
.
ISME J
4
:
28
37
.
Anguelov
R,
Dumont
Y,
Djeumen
IVY.
2020
.
On the use of traveling waves for pest/vector elimination using the sterile insect technique. arXiv [math.AP]
Available from: http://arxiv.org/abs/2010.00861.
Aragao
FV,
Zola
FC,
Marinho
LHN,
de Genaro Chiroli
DM,
Junior
AB,
Colmenero
JC.
2020
.
Choice of unmanned aerial vehicles for identification of mosquito breeding sites
.
Geospatial Health
15
[Internet] [accessed January 25, 2024]. Available from: https://www.geospatialhealth.net/index.php/gh/article/view/810.
Asman
SM,
McDonald
PT,
Prout
T.
1981
.
Field studies of genetic control systems for mosquitoes
.
Annu Rev Entomol
26
:
289
318
.
Avant
S.
2012
.
DWFP: A battle plan to protect US troops from harmful insects
.
Agric Res
60
:
4
14
.
Axenfeld
D.
1896
.
Die röntgen’schen Strahlen dem Arthropodenauge sichtbar
.
Centralblatt für Physiologie 10:147
.
Balestrino
F,
Puggioli
A,
Gilles
JRL,
Bellini
R.
2014
.
Validation of a new larval rearing unit for Aedes albopictus (Diptera: Culicidae) mass rearing
.
PloS ONE
9
:
e91914
.
Baton
LA,
Zhang
D,
Li
Y,
Xi,
Z.
2021
. Combining the incompatible and sterile insect techniques for pest and vector control. In:
Hendrichs
J,
Pereira
R,
Vreysen
MJB
, eds.
Area-wide integrated pest management
.
Boca Raton, FL
:
CRC Press
. p
367
404
.
Baumhover
AH.
2001
.
A personal account of programs to eradicate the screwworm, Cochliomyia hominivorax, in the United States and Mexico with special emphasis on the Florida program
.
Fla Entomol
84
:
1
52
.
Baumhover
AH,
Graham
AJ,
Hopkins
DE,
Dudley
PH,
New
WD,
Bushland
RC.
1955
.
Control of screw-worms through release of sterilized flies
.
J Econ Entomol
48
:
4
462
.
Beckmann
JF,
Ronau
JA,
Hochstrasser
M.
2017
.
A Wolbachia deubiquitylating enzyme induces cytoplasmic incompatibility
.
Nat Microbiol
2
:
17007
.
Beebe
NW,
Pagendam
D,
Trewin
BJ,
Boomer
A,
Bradford
M,
Ford
A,
Liddington
C,
Bondarenco
A,
De Barro
PJ,
Gilchrist
J,
Paton
C,
Staunton
KM,
Johnson
B,
Maynard
A,
Devine
GJ,
Hugo
LE,
Rasic
G,
Cook
H,
Massaro
P,
Snoad
N,
Crawford
JE,
White
BJ,
Xi
Z,
Ritchie
SA.
2021
.
Releasing incompatible males drives strong suppression across populations of wild and Wolbachia-carrying Aedes aegypti in Australia
.
Proc Natl Acad Sci USA
118
:
1
12
. https://doi.org/10.1073/pnas.2106828118
Bellini
R,
Medici
A,
Puggioli
A,
Balestrino
F,
Carrieri
M.
2013
.
Pilot field trials with Aedes albopictus irradiated sterile males in Italian urban areas
.
J Med Entomol
50
:
317
325
.
Bellini
R,
Puggioli
A,
Balestrino
F,
Brunelli
P,
Medici
A,
Urbanelli
S,
Carrieri
M.
2014
.
Sugar administration to newly emerged Aedes albopictus males increases their survival probability and mating performance
.
Acta Trop
132
:
116
123
.
Berube
DM.
2020
. Mosquitoes bite: A Zika story of vector management and gene drives. In:
Trump
BD,
Cummings
CL,
Kuzma
J,
Linkov
I
, eds.
Synthetic biology 2020: frontiers in risk analysis and governance
.
Cham, Switzerland
:
Springer International Publishing
. p
143
163
.
Boardman
L,
Sørensen
JG,
Johnson
SA,
Terblanche
JS.
2011
.
Interactions between controlled atmospheres and low temperature tolerance: a review of biochemical mechanisms
.
Front Physiol
2
:
92
.
Bond
HA,
Craig
GB,
Fay
RW.
1970
.
Field mating and movement of Aedes aegypti
.
Mosq News
30
:
394
402
.
Bourtzis
K,
Lees
RS,
Hendrichs
J,
Vreysen
MJB.
2016
.
More than one rabbit out of the hat: radiation, transgenic and symbiont-based approaches for sustainable management of mosquito and tsetse fly populations
.
Acta Tropica
157
:
115
130
.
Bouyer
J,
Culbert
NJ,
Dicko
AH,
Pacheco
MG,
Virginio
J,
Pedrosa
MC,
Garziera
L,
Pinto
ATM,
Klaptocz
A,
Germann
J,
Wallner
T,
Herranz
GS,
Argiles Herrero
R,
Yamada
H,
Balestrino
F,
Vreysen
MJB.
2020
.
Field performance of sterile male mosquitoes released from an uncrewed aerial vehicle
.
Sci Robot
5
. https://doi.org/10.1126/scirobotics.aba6251
Bouyer
J,
Lefrançois
T.
2014
.
Boosting the sterile insect technique to control mosquitoes
.
Trends Parasitol
30
:
271
273
.
Bracken
GK,
Dondale
CD.
1972
.
Fertility and survival of Achaearanea tepidariorum (Araneida: Theridiidae) on a diet of chemosterilized mosquitoes
.
Can Entomol
104
:
1709
1712
.
Burkett
DA,
Cope
SE,
Strickman
DA,
White
GB.
2013
.
The Deployed Warfighter Protection (DWFP) research program: developing new public health pesticides, application technologies, and repellent systems
.
J Integr Pest Manag
4
:
1
7
.
Bushland
RC.
1960
. Male sterilization for the control of insects. In:
Metcalf
RL
, ed.
Advances in pest control research
. Volume
III
.
New York, NY
:
Interscience Publishers
. p
1
25
.
Campion
DG.
1972
.
Insect chemosterilants: a review
.
Bull Entomol Res
61
:
577
635
.
Capurro
ML,
Carvalho
DO,
Garziera
L,
Pedrosa
MC.
2016
.
Description of social aspects surrounding releases of transgenic mosquitoes in Brazil
.
J Recent Sci Res
7
:
10363
10369
.
Caragata
EP,
Tikhe
CV,
Dimopoulos
G.
2019
.
Curious entanglements: interactions between mosquitoes, their microbiota, and arboviruses
.
Curr Opin Virol
37
:
26
36
.
Carrasco-Escobar
G,
Moreno
M,
Fornace
K,
Herrera-Varela
M,
Manrique
E,
Conn
JE.
2022
.
The use of drones for mosquito surveillance and control
.
Parasites Vectors
15
:
473
.
Carvalho
DO,
McKemey
AR,
Garziera
L,
Lacroix
R,
Donnelly
CA,
Alphey
L,
Malavasi
A,
Capurro
ML.
2015
.
Suppression of a field population of Aedes aegypti in Brazil by sustained release of transgenic male mosquitoes
.
PloS Negl Trop Dis
9
:
e0003864
.
Carvalho
DO,
Morreale
R,
Stenhouse
S,
Hahn
DA,
Gomez
M,
Lloyd
A,
Hoel
D.
2022
.
A sterile insect technique pilot trial on Captiva Island: defining mosquito population parameters for sterile male releases using mark–release–recapture
.
Parasites Vectors
15
:
1
4
.
Catteruccia
F,
Benton
JP,
Crisanti
A.
2005
.
An Anopheles transgenic sexing strain for vector control
.
Nature Biotechnol
23
:
1414
1417
.
Chen
C,
Aldridge
RL,
Gibson
S,
Kline
J,
Aryaprema
V,
Qualls
W,
Xue
RD,
Boardman
L,
Linthicum
KJ,
Hahn
DA.
2023
.
Developing the radiation‐based sterile insect technique (SIT) for controlling Aedes aegypti: identification of a sterilizing dose
.
Pest Manag Sci
79
:
1175
1183
.
Chen
H,
Ronau
JA,
Beckmann
JF,
Hochstrasser
M.
2019
.
A Wolbachia nuclease and its binding partner provide a distinct mechanism for cytoplasmic incompatibility
.
Proc Natl Acad Sci USA
116
:
22314
22321
.
Coon
KL,
Vogel
KJ,
Brown
MR,
Strand
MR.
2014
.
Mosquitoes rely on their gut microbiota for development
.
Mol Ecol
23
:
2727
2739
.
Costantini
D,
Metcalfe
NB,
Monaghan
P.
2010
.
Ecological processes in a hormetic framework
.
Ecol Lett
13
:
1435
1447
.
Crawford
JE,
Clarke
DW,
Criswell
V,
Desnoyer
M,
Cornel
D,
Deegan
B,
Gong
K,
Hopkins
KC,
Howell
P,
Hyde
JS,
Livni
J,
Behling
C,
Benza
R,
Chen
W,
Dobson,
KL,
Eldershaw
C,
Greeley
D,
Han
Y,
Hughes
B,
Kakani
E,
Karbowski
J,
Kichell
A,
Lee
E,
Lin
T,
Liu
J,
Lozano
M,
MacDonald
W,
Mains
JW,
Metlitz
M,
Mitchell
SN,
Moore
D,
Ohm
JR,
Parkes
K,
Proshnikoff
A,
Robuck
C,
Sheridan
M,
Sobecki
R,
Smith
P,
Stevenson
J,
Sullivan
J,
Wasson
B,
Weakley
AM,
Wilhelm
M,
Won
J,
Yasunaga
A,
Chan
WC,
Holeman
J,
Snoad
N,
Upson
L,
Zha
T,
Dobson
SL,
Mulligan
FS,
Massaro
P,
White
BJ.
2020
.
Efficient production of male Wolbachia-infected Aedes aegypti mosquitoes enables large-scale suppression of wild populations
.
Nat Biotechnol
38
:
482
492
.
Culbert
NJ,
Lees
RS,
Vreysen
MJB,
Darby
AC,
Gilles
JRL.
2017
.
Optimised conditions for handling and transport of male Anopheles arabiensis: effects of low temperature, compaction, and ventilation on male quality
.
Entomol Exp Appl
164
:
276
283
.
Cunningham
CA,
Aldridge
RL,
Kline
J,
Bibbs
CS,
Linthicum
KJ,
Xue
RD.
2020
.
Effects of radiation on blood-feeding activity of Aedes aegypti (Diptera: Culicidae)
.
J Vector Ecol
45
:
135
136
.
Dame
DA,
Curtis
CF,
Benedict
MQ,
Robinson
AS,
Knols
BGJ.
2009
.
Historical applications of induced sterilization in field populations of mosquitoes
.
Malar J
8
(
Suppl 2)
:
S2
.
Darrow
DI.
1968
.
The effect of gamma irradiation on reproduction and life span of the mosquito Culex tarsalis Coquillett
.
Mosq News
28
:
21
24
.
de Castro Poncio
L,
dos Anjos
FA,
de Oliveira
DA,
Rebechi
D,
de Oliveira
RN,
Chitolina
RF,
Fermino
ML,
Bernardes
LG,
Guimarães
D,
Lemos
PA,
Silva
MNE,
Silvestre
RGM,
Bernardes
ES,
Paldi
N.
2021
.
Novel sterile insect technology program results in suppression of a field mosquito population and subsequently to reduced incidence of dengue
.
J Infect Dis
224
:
1005
1014
.
DMVCD [Delta Mosquito and Vector Control District]
.
2023
.
Oxitec announces 2022 US pilot plans for mosquito technology [Internet
].
Visalia, CA
:
Delta Mosquito and Vector Control District
[accessed September 23, 2023]. Available from: https://deltamvcd.org/oxitec-announces-2022-us-pilot-plans-for-mosquito-technology/.
Dodson
BL,
Hughes
GL,
Paul
O,
Matacchiero
AC,
Kramer
LD,
Rasgon
JL.
2014
.
Wolbachia enhances West Nile virus (WNV) infection in the mosquito Culex tarsalis
.
PloS Negl Trop Dis
8
:
e2965
.
Dutra
HL,
Rocha
MN,
Dias
FB,
Mansur
SB,
Caragata
EP,
Moreira
LA.
2016
.
Wolbachia blocks currently circulating Zika virus isolates in Brazilian Aedes aegypti mosquitoes
.
Cell Host Microbe
19
:
771
774
.
El-Gazzar
LM,
Dame
DA.
1983
.
Effects of combinations of irradiation and chemosterilization on mating competitiveness of Culex quinquefasciatus Say
.
J Econ Entomol
76
:
1331
1334
.
Fay
RW,
Craig
J.
1969
.
Genetically marked Aedes aegypti in studies of field populations
.
Mosq News
29
:
121
127
.
Fay
RW,
Morlan
HB.
1959
.
A mechanical device for separating the developmental stages, sexes and species of mosquitoes
.
Mosq News
19
:
144
147
.
Forel
A,
Dufour
H.
1902
. Ueber die Empfindlichkeit der Ameisen für Ultra-violett und Röntgen’sche Strahlen.
Zoolog Jahrbuch
17
:
335
338
.
Fu
G,
Lees
RS,
Nimmo
D,
Aw
D,
Jin
L,
Gray
P,
Berendonk
TU,
White-Cooper
H,
Scaife
S,
Kim Phuc
H,
Marinotti
O.
2010
.
Female-specific flightless phenotype for mosquito control
.
Proc Natl Acad Sci USA
107
:
4550
4554
.
Galizi
R,
Doyle
LA,
Menichelli
M,
Bernardini
F,
Deredec
A,
Burt
A,
Stoddard
BL,
Windbichler
N,
Crisanti
A.
2014
.
A synthetic sex ratio distortion system for the control of the human malaria mosquito
.
Nat Commun
5
:
3977
.
Garcia
M,
Maza
I,
Ollero
A,
Gutierrez
D,
Aguirre
I,
Viguria
A.
2022
.
Release of sterile mosquitoes with drones in urban and rural environments under the European Drone Regulation. NATO Advanced Science Institutes Series E
.
Appl Sci
12
:
1250
.
Garziera
L,
Pedrosa
MC,
de Souza
FA,
Gómez
M,
Moreira
MB,
Virginio
JF,
Capurro
ML,
Carvalho
DO.
2017
.
Effect of interruption of over-flooding releases of transgenic mosquitoes over wild population of Aedes aegypti: two case studies in Brazil
.
Entomol Exp Appl
164
:
327
339
.
Gato
R,
Companioni
A,
Bruzón
RY,
Menéndez
Z,
González
A,
Rodríguez
M.
2014
.
Release of thiotepa sterilized males into caged populations of Aedes aegypti: life table analysis
.
Acta Tropica
132
(
Suppl
):
S164
169
.
Gato
R,
Menéndez
Z,
Prieto
E,
Argilés
R,
Rodríguez
M,
Baldoquín
W,
Hernández
Y,
Pérez
D,
Anaya
J,
Fuentes
I,
Lorenzo
C.
2021
.
Sterile insect technique: successful suppression of an Aedes aegypti field population in Cuba
.
Insects
12
. https://doi.org/10.3390/insects12050469
Gesto
JSM,
Pinto
SB,
Dias
FBS,
Peixoto
J,
Costa
G,
Kutcher
S,
Montgomery
J,
Green
BR,
Anders
KL,
Ryan
PA,
Simmons
CP.
2021a
.
Large-scale deployment and establishment of Wolbachia into the Aedes aegypti population in Rio de Janeiro, Brazil
.
Front Microbiol
12
:
711107
.
Gesto
JSM,
Ribeiro
GS,
Rocha
MN,
Dias
FBS,
Peixoto
J,
Carvalho
FD,
Pereira
TN,
Moreira
LA.
2021b
.
Reduced competence to arboviruses following the sustainable invasion of Wolbachia into native Aedes aegypti from Southeastern Brazil
.
Sci Rep
11
:
10039
.
Gilbert
JA,
Melton
L.
2018
.
Verily project releases millions of factory-reared mosquitoes
.
Nat Biotechnol
36
:
781
782
.
Gilles
JRL,
Schetelig
MF,
Scolari
F,
Marec
F,
Capurro
ML,
Franz
G,
Bourtzis
K.
2014
.
Towards mosquito sterile insect technique programmes: exploring genetic, molecular, mechanical and behavioural methods of sex separation in mosquitoes
.
Acta Tropica
132
(
Suppl
):
S178
187
.
Gillett
JD.
1955
.
Variation in the hatching-response of Aedes eggs (Diptera: Culicidae)
.
Bull Entomol Res
46
:
241
254
.
Glandorf
DCM.
2017
.
Technical evaluation of a potential release of OX513A Aedes aegypti mosquitoes on the island of Saba [Internet]
. Available from: https://rivm.openrepository.com/handle/10029/620888.
Gorman
K,
Young
J,
Pineda
L,
Márquez
R,
Sosa
N,
Bernal
D,
Torres
R,
Soto
Y,
Lacroix
R,
Naish
N,
Kaiser
P.
2016
.
Short-term suppression of Aedes aegypti using genetic control does not facilitate Aedes albopictus
.
Pest Manag Sci
72
:
618
628
.
Grover
KK,
Suguna
SG,
Uppal
DK,
Singh
KRP,
Ansari
MA,
Curtis
CF,
Singh
D,
Sharma
VP,
Panicker
KN.
1976
.
Field experiments on the competitiveness of males carrying genetic control systems for Aedes aegypti
.
Entomol Exp Appl
20
:
8
18
.
Gunathilaka
N,
Ranathunge
T,
Udayanga
L,
Wijegunawardena
A,
Gilles
JRL,
Abeyewickreme
W.
2019
.
Use of mechanical and behavioural methods to eliminate female Aedes aegypti and Aedes albopictus for sterile insect technique and incompatible insect technique applications
.
Parasites Vectors
12
:
148
.
Harris
AF,
McKemey
AR,
Nimmo
D,
Curtis
Z,
Black
I,
Morgan
SA,
Oviedo
MN,
Lacroix
R,
Naish
N,
Morrison
NI,
Collado
A.
2012
.
Successful suppression of a field mosquito population by sustained release of engineered male mosquitoes
.
Nat Biotechnol
30
:
828
830
.
Harwood
JF,
Helmey
WL,
Turnwall
BB,
Justice
KD,
Farooq
M,
Richardson
AG.
2016
.
Controlling Aedes aegypti in cryptic environments with manually carried ultra-low volume and mist blower pesticide applications
.
J Am Mosq Control Assoc
32
:
217
223
.
Hatle
JD,
Paterson
CS,
Jawaid
I,
Lentz
C,
Wells
SM,
Fronstin
RB.
2008
.
Protein accumulation underlying lifespan extension via ovariectomy in grasshoppers is consistent with the disposable soma hypothesis but is not due to dietary restriction
.
Exp Gerontol
43
:
900
908
.
Hausermann
W,
Fay
RW,
Hacker
CS.
1971
.
Dispersal of genetically marked female Aedes aegypti in Mississippi
.
Mosq News
31
:
37
51
.
Hemme
RR,
Thomas
CL,
Chadee
DD,
Severson
DW.
2010
.
Influence of urban landscapes on population dynamics in a short-distance migrant mosquito: evidence for the dengue vector Aedes aegypti
.
PLoS Negl Trop Dis
4
:
e634
.
Hibino
Y,
Iwahashi
O.
1991
.
Appearance of wild females unreceptive to sterilized males on Okinawa island in the eradication programme of the melon fly, Dacus cucurbitae Coquillett (Diptera: Tephritidae)
.
Appl Entomol Zool
26
:
265
270
.
Hien
NT,
Anh
DD,
Le
NH,
Yen
NT,
Phong
TV,
Nam
VS,
Duong
TN,
Nguyen
NB,
Huong
DTT,
Hung
LQ,
Trinh
CN.
2021
.
Environmental factors influence the local establishment of Wolbachia in Aedes aegypti mosquitoes in two small communities in central Vietnam
.
Gates Open Research [Internet
]
5
:
147
. https://doi.org/10.12688/gatesopenres.13347.2
Hoffmann
AA,
Montgomery
BL,
Popovici
J,
Iturbe-Ormaetxe
I,
Johnson
PH,
Muzzi
F,
Greenfield
M,
Durkan
M,
Leong
YS,
Dong
Y,
Cook
H.
2011
.
Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission
.
Nature
476
:
454
457
.
Honma
A,
Kumano
N,
Noriyuki
S.
2019
.
Killing two bugs with one stone: a perspective for targeting multiple pest species by incorporating reproductive interference into sterile insect technique
.
Pest Manag Sci
75
:
571
577
.
Hossain
MF,
Ghosh
A,
Sultana
N,
Momen
M,
Hossain
MA,
Khan
SA,
Seheli
K.
2021
.
Optimization of irradiation sterility dose of the male Aedes aegypti (Linnaeus) Mosquito: a laboratory study in Bangladesh
.
Int J Trop Insect Sci
42
:
1421
1428
.
Hunter
WD.
1912
.
Results of experiments to determine the effect of Roentgen rays upon insects
.
J Econ Entomol
5
:
188
193
.
Indriani
C,
Tantowijoyo
W,
Rancès
E,
Andari
B,
Prabowo
E,
Yusdi
D,
Ansari
MR,
Wardana
DS,
Supriyati
E,
Nurhayati
I,
Ernesia
I.
2020
.
Reduced dengue incidence following deployments of Wolbachia-infected Aedes aegypti in Yogyakarta, Indonesia: a quasi-experimental trial using controlled interrupted time series analysis
.
Gates Open Res
4
:
50
.
Kirkwood
TBL.
2002
.
Evolution of ageing
.
Mech Ageing Dev
123
:
737
745
.
Kittayapong
P,
Ninphanomchai
S,
Limohpasmanee
W,
Chansang
C,
Chansang
U,
Mongkalangoon
P.
2019
.
Combined sterile insect technique and incompatible insect technique: the first proof-of-concept to suppress Aedes aegypti vector populations in semi-rural settings in Thailand
.
PloS Negl Trop Dis
13
:
e0007771
.
Klassen
W,
Curtis
CF.
2005
. History of the sterile insect technique. In:
Dyck
VA,
Hendrichs
J,
Robinson
AS
, eds.
Sterile insect technique: principles and practice in area-wide integrated pest management
.
Dordrecht, the Netherlands
:
Springer Netherlands
. p
3
36
.
Kyritsis
GA,
Augustinos
AA,
Cáceres
C,
Bourtzis
K.
2017
.
Medfly gut microbiota and enhancement of the sterile insect technique: similarities and differences of Klebsiella oxytoca and Enterobacter sp. AA26 probiotics during the larval and adult stages of the VIENNA 8D53+ genetic sexing strain
.
Front Microbiol
8
:
2064
.
Labbé
GMC,
Scaife
S,
Morgan
SA,
Curtis
ZH,
Alphey
L.
2012
.
Female-specific flightless (fsRIDL) phenotype for control of Aedes albopictus
.
PloS Negl Trop Dis
6
:
e1724
.
Lacroix
R,
McKemey
AR,
Raduan
N,
Kwee Wee
L,
Hong Ming
W,
Guat Ney
T,
Rahidah AA
S,
Salman
S,
Subramaniam
S,
Nordin
O,
Hanum
AT.
2012
.
Open field release of genetically engineered sterile male Aedes aegypti in Malaysia
.
PLoS ONE
7
:
e42771
.
Lindquist
AW.
1955
.
The use of gamma radiation for control or eradication of the screw-worm
.
J Econ Entomol
48
:
467
469
.
Lindquist
AW.
1963
.
Insect population control by the sterile-male technique. Technical Report Series 21 (Report of Panel, Vienna, 16–19 October 1962)
.
Vienna, Austria
:
IAEA
. Available from: https://inis.iaea.org/collection/NCLCollectionStore/_Public/25/009/25009347.pdf.
López-Martínez
G,
Hahn
DA.
2014
.
Early life hormetic treatments decrease irradiation-induced oxidative damage, increase longevity, and enhance sexual performance during old age in the Caribbean fruit fly
.
PloS ONE
9
:
e88128
.
Lorimer
N,
Lounibos
LP,
Petersen
JL.
1976
.
Field trials with a translocation homozygote in Aedes aegypti for population replacement
.
J Econ Entomol
69
:
405
409
.
Lozano
S,
Pritts
K,
Duguma
D,
Fredregill
C,
Connelly
R.
2022
.
Independent evaluation of Wolbachia infected male mosquito releases for control of Aedes aegypti in Harris County, Texas, using a Bayesian abundance estimator
.
PloS Negl Trop Dis
16
:
e0010907
.
Maiga
H,
Gilles
JR,
Lees
RS,
Yamada
H,
Bouyer
J.
2020a
.
Demonstration of resistance to satyrization behavior in Aedes aegypti from La Réunion island
.
Parasite
27
:
22
. https://doi.org/10.1051/parasite/2020020
Maiga
H,
Mamai
W,
Yamada
H,
Argilés Herrero
R.
2020b
.
Guidelines for mass-rearing of Aedes mosquitoes. Version 1 [Internet]
[accessed February 2, 2023]. Available from: https://inis.iaea.org/search/search.aspx?orig_q=RN:51066763.
Mains
JW,
Brelsfoard
CL,
Rose
RI,
Dobson
SL.
2016
.
Female adult Aedes albopictus suppression by Wolbachia-infected male mosquitoes
.
Sci Rep
6
:
33846
.
Mains
JW,
Kelly
PH,
Dobson
KL,
Petrie
WD,
Dobson
SL.
2019
.
Localized control of Aedes aegypti (Diptera: Culicidae) in Miami, FL, via inundative releases of Wolbachia-infected male mosquitoes
.
J Med Entomol
56
:
1296
1303
.
Mamai
W,
Maiga
H,
Somda
NSB,
Wallner
T,
Konczal
A,
Yamada
H,
Bouyer
J.
2020
.
Aedes aegypti larval development and pupal production in the FAO/IAEA mass-rearing rack and factors influencing sex sorting efficiency
.
Parasite
27
:
43
.
Marina
CF,
Liedo
P,
Bond
JGR,
Osorio
A,
Valle
J,
Angulo-Kladt
R,
Gómez-Simuta
Y,
Fernández-Salas
I,
Dor
A,
Williams
T.
2022
.
Comparison of ground release and drone-mediated aerial release of Aedes aegypti sterile males in southern Mexico: efficacy and challenges
.
Insects
13
. https://doi.org/10.3390/insects13040347
Marois
E,
Scali
C,
Soichot
J,
Kappler
C,
Levashina
EA,
Catteruccia
F.
2012
.
High-throughput sorting of mosquito larvae for laboratory studies and for future vector control interventions
.
Malar J
11
:
302
.
Martín-Park
A,
Che-Mendoza
A.
2022
.
Pilot trial using mass field-releases of sterile males produced with the incompatible and sterile insect techniques as part of integrated Aedes aegypti control in Mexico
.
PloS Negl Trop Dis
. Available from: https://journals.plos.org/plosntds/article?id=10.1371/journal.pntd.0010324.
Massonnet-Bruneel
B,
Corre-Catelin
N,
Lacroix
R,
Lees
RS,
Hoang
KP,
Nimmo
D,
Alphey
L,
Reiter
P.
2013
.
Fitness of transgenic mosquito Aedes aegypti males carrying a dominant lethal genetic system
.
PLoS ONE
8
:
e62711
.
McCray
EM
Jr.
1961
.
A mechanical device for the rapid sexing of Aedes aegypti pupae
.
J Econ Entomol
54
:
819
.
McDonald
PT,
Hausermann
W,
Lorimer
N.
1977
.
Sterility introduced by release of genetically altered males to a domestic population of Aedes aegypti at the Kenya coast
.
Am J Trop Med Hyg
26
:
553
561
.
Micu
A.
2020
.
Millions of genetically-modified mosquitoes will be deployed to save Floridians from bites [Internet]
. Available from: https://www.zmescience.com/science/genetically-modifiedmosqito-262345.
Moreira
LA.
2019
.
When a bacterium fights arboviruses
.
Comptes Rendus Biol
342
:
267
268
.
Moreira
LA,
Iturbe-Ormaetxe
I,
Jeffery
JA,
Lu
G,
Pyke
AT,
Hedges
LM,
Rocha
BC,
Hall-Mendelin
S,
Day
A,
Riegler
M,
Hugo
LE,
Johnson
KN,
Kay
BH,
McGraw
EA,
van den Hurk
AF,
Ryan
PA,
O’Neill
SL.
2009
.
A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and Plasmodium
.
Cell
139
:
1268
1278
.
Moretti
R,
Lampazzi
E,
Damiani
C,
Fabbri
G,
Lombardi
G,
Pioli
C,
Desiderio
A,
Serrao
A,
Calvitti
M.
2022
.
Increased biting rate and decreased Wolbachia density in irradiated Aedes mosquitoes
.
Parasites Vectors
15
:
67
.
Morgan
AC,
Runner
GA.
1913
.
Some experiments with Roentgen rays upon the cigarette beetle, Lasioderma serricorne Fabr
.
J Econ Entomol
6
:
226
230
.
Morlan
HB,
Hayes
RO,
Schoof
HF.
1963
.
Methods for mass rearing of Aedes aegypti (L.)
.
Public Health Rep
78
:
711
719
.
Morlan
HB,
McCray
EM
Jr,
Kilpatrick
JW.
1962
.
Field tests with sexually sterile males for control of Aedes aegypti
.
Mosq News
22
:
295
300
.
Muller
HJ.
1927
.
Artificial transmutation of the gene
.
Science
66
:
84
87
.
Muller
HJ.
1954
.
The nature of the genetic effects produced by radiation
.
Radiation Biol
1
:
351
473
.
NACCHO [National Association of County and City Health Officials].
2017
.
Mosquito control capabilities in the U.S. Washington, DC: NACCHO
[accessed January 24, 2024]. Available from: https://www.naccho.org/uploads/downloadable-resources/Mosquito-control-in-the-U.S.-Report.pdf
Nasci
RS,
Hare
SG,
Willis
FS.
1989
.
Interspecific mating between Louisiana strains of Aedes albopictus and Aedes aegypti in the field and laboratory
.
J Am Mosq Control Assoc
5
:
416
421
.
Nazni
WA,
Hoffmann
AA,
NoorAfizah
A,
Cheong
YL,
Mancini
MV,
Golding
N,
Kamarul
GMR,
Arif
MAK,
Thohir
H,
NurSyamimi
H,
ZatilAqmar
MZ,
NurRuqqayah
M,
NorSyazwani
A,
Faiz
A,
Irfan
FRMN,
Rubaaini
S,
Nuradila
N,
Nizam
NMN,
Irwan
SM,
Endersby-Harshman
NM,
White
VL,
Ant
TH,
Herd
CS,
Hasnor
AH,
AbuBakar
R,
Hapsah
DM,
Khadijah
K,
Kamilan
D,
Lee
SC,
Paid
YM,
Fadzilah
K,
Topek
O,
Gill
BS,
Lee
HL,
Sinkins
SP.
2019
.
Establishment of Wolbachia strain wAlbB in Malaysian populations of Aedes aegypti for dengue control
.
Curr Biol
29
:
4241
4248.e5
.
Ng
LC,
Wolbachia-Singapore Consortium P
.
2021
.
Wolbachia-mediated sterility suppresses Aedes aegypti populations in the urban tropics [Internet
]. Available from: https://www.medrxiv.org/content/10.1101/2021.06.16.21257922.abstract.
Nguyen
TH,
Nguyen
HL,
Nguyen
TY,
Vu
SN,
Tran
ND,
Le
TN,
Vien
QM,
Bui
TC,
Le
HT,
Kutcher
S,
Hurst
TP.
2015
.
Field evaluation of the establishment potential of wMelPop Wolbachia in Australia and Vietnam for dengue control
.
Parasites & Vectors
8
:
563
. https://doi.org/10.1186/s13071-015-1174-x
O’Leary
S,
Adelman
ZN.
2020
.
CRISPR/Cas9 knockout of female-biased genes AeAct-4 or myo-fem in Ae. aegypti results in a flightless phenotype in female, but not male mosquitoes
.
PloS Negl Trop Dis
14
:
e0008971
.
Oh, New Delhi; oh, Geneva
.
1975
. Nature
256
:
355
357
. https://doi.org/10.1038/256355a0
Oléron Evans
TP,
Bishop
SR.
2014
.
A spatial model with pulsed releases to compare strategies for the sterile insect technique applied to the mosquito Aedes aegypti
.
Math Biosci
254
:
6
27
.
Oliva
CF,
Benedict
MQ,
Collins
CM,
Baldet
T,
Bellini
R,
Bossin
H,
Bouyer
J,
Corbel
V,
Facchinelli
L,
Fouque
F,
Geier
M.
2021
.
Sterile Insect Technique (SIT) against Aedes species mosquitoes: a roadmap and good practice framework for designing, implementing and evaluating pilot field trials
.
Insects
12
. http://doi.org/10.3390/insects12030191
Papathanos
PA,
Bossin
HC,
Benedict
MQ,
Catteruccia
F,
Malcolm
CA,
Alphey
L,
Crisanti
A.
2009
.
Sex separation strategies: past experience and new approaches
.
Malar J
8
(
Suppl 2
):
S5
.
Papathanos
PA,
Bourtzis
K,
Tripet
F,
Bossin
H,
Virginio
JF,
Capurro
ML,
Pedrosa
MC,
Guindo
A,
Sylla
L,
Coulibaly
MB,
Yao
FA,
Epopa
PS,
Diabate
A.
2018
.
A perspective on the need and current status of efficient sex separation methods for mosquito genetic control
.
Parasites Vectors
11
:
654
. https://doi.org/10.1186/s13071-018-3222-9
Patil
PB,
Dasgupta
SK,
KV
SR,
Char
B,
Zehr
UB,
Barwale
SR.
2020
.
Surveillance of Aedes mosquito species in villages of Jalna district, Maharashtra, India
.
J Entomol Zool Stud
8
:
669
677
.
Patil
PB,
Yadav
KK,
Dasgupta
SK,
Zehr
UB,
Barwale
SR,
Char
B.
2021
. Evaluation of transgenic Aedes aegypti L. strain in India: a friendly mosquito. In:
Tyagi
BK
, ed.
Genetically modified and other innovative vector control technologies: eco-bio-social considerations for safe application
.
Singapore
:
Springer Singapore
. p
89
118
.
Phasomkusolsil
S,
Pantuwatana
K,
Tawong
J,
Khongtak
W,
Kertmanee
Y,
Monkanna
N,
Khaosanorh
S,
Wanja
EW,
Davidson
SA.
2017
.
Sugar and multivitamin diet effects on the longevity and mating capacity of laboratory-reared male anopheline mosquitoes
.
J Am Mosq Control Assoc
33
:
175
183
.
Phuc
HK,
Andreasen
MH,
Burton
RS,
Vass
C,
Epton
MJ,
Pape
G,
Fu
G,
Condon
KC,
Scaife
S,
Donnelly
CA,
Coleman
PG.
2007
.
Late-acting dominant lethal genetic systems and mosquito control
.
BMC Biol
5
:
1
11
.
Piltch-Loeb
R,
Merdjanoff
AA,
Bhanja
A,
Abramson
DM.
2019
.
Support for vector control strategies in the United States during the Zika outbreak in 2016: the role of risk perception, knowledge, and confidence in government
.
Prev Med
119
:
52
57
.
Pleydell
DR,
Bouyer
J.
2019
.
Biopesticides improve efficiency of the sterile insect technique for controlling mosquito-driven dengue epidemics
.
Commun Biol
2
:
1
11
.
Rai
KS,
Grover
KK,
Suguna
SG.
1973
.
Genetic manipulation of Aedes aegypti: incorporation and maintenance of a genetic marker and a chromosomal translocation in natural populations
.
Bull World Health Org
48
:
49
56
.
Ranathunge
T,
Harishchandra
J,
Maiga
H,
Bouyer
J,
Gunawardena
YINS,
Hapugoda
M.
2022
.
Development of the sterile insect technique to control the dengue vector Aedes aegypti (Linnaeus) in Sri Lanka
.
PloS ONE
17
:
e0265244
.
Reiter
P.
2007
.
Oviposition, dispersal, and survival in Aedes aegypti: implications for the efficacy of control strategies
.
Vector Borne Zoonotic Dis
7
:
261
273
.
Reiter
P,
Amador
MA,
Anderson
RA,
Clark
GG.
1995
.
Dispersal of Aedes aegypti in an urban area after blood feeding as demonstrated by rubidium-marked eggs
.
Am J Trop Med Hyg
52
:
177
179
.
Ribeiro
JM.
1988
.
Can satyrs control pests and vectors
?
J Med Enomol
25
:
431
440
.
Rodriguez
PH,
Hamm
WJ,
Garcia
F,
Garcia
M,
Schirf
V.
1989
.
Reduced productivity in adult yellow fever mosquito (Diptera: Culicidae) populations
.
J Econ Entomol
82
:
519
523
.
Rose
RI.
2001
.
Pesticides and public health: integrated methods of mosquito management
.
Emerg Infect Dis
7
:
17
23
.
Roush
R,
Tabashnik
BE.
2012
.
Pesticide resistance in arthropods
.
New York, NY
:
Springer Science & Business Media
.
Runner
GA.
1916
.
Effect of Röntgen rays on the tobacco, or cigarette beetle and the results of experiments with a new form of Röntgen tube
.
J Agric Res
6
:
383
388
.
Russell
RC,
Webb
CE,
Williams
CR,
Ritchie
SA.
2005
.
Mark-release-recapture study to measure dispersal of the mosquito Aedes aegypti in Cairns, Queensland, Australia
.
Med Vet Entomol
19
:
451
457
.
Ryan
PA,
Turley
AP,
Wilson
G,
Hurst
TP,
Retzki
K,
Brown-Kenyon
J,
Hodgson
L,
Kenny
N,
Cook
H,
Montgomery
BL,
Paton
CJ.
2019
.
Establishment of wMel Wolbachia in Aedes aegypti mosquitoes and reduction of local dengue transmission in Cairns and surrounding locations in northern Queensland, Australia
.
Gates Open Res
3
:
1547
.
Sasmita
HI,
Ernawan
B,
Sadar
M,
Nasution
IA,
Indarwatmi
M,
Tu
W-C,
Neoh
K-B.
2021
.
Assessment of packing density and transportation effect on sterilized pupae and adult Aedes aegypti (Diptera: Culicidae) in non-chilled conditions
.
Acta Tropica
226
:
106243
.
Schairer
CE,
Najera
J,
James
AA,
Akbari
OS,
Bloss
CS.
2021
.
Oxitec and MosquitoMate in the United States: lessons for the future of gene drive mosquito control
.
Pathog Glob Health
115
:
365
376
.
Schmidt
TL,
Barton
NH,
Rašić
G,
Turley
AP,
Montgomery
BL,
Iturbe-Ormaetxe
I,
Cook
PE,
Ryan
PA,
Ritchie
SA,
Hoffmann
AA,
O’Neill
SL.
2017
.
Local introduction and heterogeneous spatial spread of dengue-suppressing Wolbachia through an urban population of Aedes aegypti
.
PloS Biol
15
:
e2001894
.
Seawright
JA,
Kaiser
PE,
Dame
DA,
Willis
NL.
1975
.
Field competitiveness of males of Aedes aegypti (L.) heterozygous for a translocation
.
Mosq News
35
:
30
33
.
Seawright
JA,
Kaiser
PE,
Willis
NL,
Dame
DA.
1976
.
Field competitiveness of double translocation heterozygote males of Aedes aegypti (L.)
.
J Med Entomol
13
:
208
211
.
Serebrovsky
AS.
1940
.
On the possibility of a new method for the control of insect pests
. In: Sterile-male technique for eradication or control of harmful insects. No. STI/PUB/224.
Vienna, Austria
:
International Atomic Energy Agency
[1969]. p
123
137
.
Sharma
VP,
Patterson
RS,
Ford
HR.
1972
.
A device for the rapid separation of male and female mosquito pupae
.
Bull World Health Organ B
47
:
429
432
.
Souza
RS,
Virginio
F,
Riback
TIS,
Suesdek
L,
Barufi
JB,
Genta
FA.
2019
.
Microorganism-based larval diets affect mosquito development, size and nutritional reserves in the yellow fever mosquito Aedes aegypti (Diptera: Culicidae)
.
Front Physiol
10
. https://doi.org/10.3389/fphys.2019.00152
Spinner
SA,
Barnes
ZH,
Puinean
AM,
Gray
P,
Dafa’alla
T,
Phillips
CE,
Nascimento de Souza
C,
Frazon
TF,
Ercit
K,
Collado
A,
Naish
N
, Sulston E, Phillips GCL, Greene KK, Poletto M, Sperry BD, Warner SA, Rose NR, Frandsen GK, Verza NC, Gorman KJ, Matzen KJ.
2022
.
New self-sexing Aedes aegypti strain eliminates barriers to scalable and sustainable vector control for governments and communities in dengue-prone environments
.
Front Bioeng Biotechnol
10
. https://doi.org/10.3389/fbioe.2022.975786
Tantowijoyo
W,
Andari
B,
Arguni
E,
Budiwati
N,
Nurhayati
I,
Fitriana
I,
Ernesia
I,
Daniwijaya
EW,
Supriyati
E,
Yusdiana
DH,
Victorius
M.
2020
.
Stable establishment of wMel Wolbachia in Aedes aegypti populations in Yogyakarta, Indonesia
.
PloS Negl Trop Dis
14
:
e0008157
.
Taylor
C.
2020
.
Making sense of public scientific controversy: a case study examining science communication and public engagement surrounding genetically modified mosquitoes in the Florida Keys
[Ph.D. dissertation].
University of Rhode Island, Kingston, RI
.
Thomas
DD,
Donnelly
CA,
Wood
RJ,
Alphey
LS.
2000
.
Insect population control using a dominant, repressible, lethal genetic system
.
Science
287
:
2474
2476
.
Tomiche
FJ.
1975
.
The WHO and mosquitoes
.
Nature
257
:
175
.
Tripet
F,
Lounibos
LP,
Robbins
D,
Moran
J,
Nishimura
N,
Blosser
EM.
2011
.
Competitive reduction by satyrization? Evidence for interspecific mating in nature and asymmetric reproductive competition between invasive mosquito vectors
.
Am J Trop Med Hyg
85
:
265
.
Tussey
DA,
Linthicum
KJ,
Hahn
DA.
2022
.
Does severe hypoxia during irradiation of Aedes aegypti pupae improve sterile male performance
?
Parasites Vectors
15
:
446
.
Usta
C.
2013
.
Microorganisms in biological pest control—a review (bacterial toxin application and effect of environmental factors)
. In:
Silva-Opps
M
ed.
Current Progress in Biological Research
.
London, United Kingdom: InTechOpen
. p.
287
317
. https://doi.org/10.5772/55786
Utarini
A,
Indriani
C,
Ahmad
RA,
Tantowijoyo
W,
Arguni
E,
Ansari
MR,
Supriyati
E,
Wardana
DS,
Meitika
Y,
Ernesia
I,
Nurhayati
I,
Prabowo
E,
Andari
B,
Green
BR,
Hodgson
L,
Cutcher
Z,
Rancès
E,
Ryan
PA,
O’Neill
SL,
Dufault
SM,
Tanamas
SK,
Jewell
NP,
Anders
KL,
Simmons
CP.
2021
.
Efficacy of Wolbachia-infected mosquito deployments for the control of dengue
.
N Engl J Med
384
:
2177
2186
.
Van Den Hurk
AF,
Hall-Mendelin
S,
Pyke
AT,
Frentiu
FD,
McElroy
K,
Day
A,
Higgs
S,
O’Neill
SL.
2012
.
Impact of Wolbachia on infection with chikungunya and yellow fever viruses in the mosquito vector Aedes aegypti
.
PLoS Negl Trop Dis
6
:
e1892
.
Vanderplank
FL.
1947
.
Experiments in the hybridisation of tsetse-flies (Glossina, Diptera) and the possibility of a new method of control
.
Trans Royal Entomolo Soc London
98
:
1
18
+ 2 plates (
pt. 1
).
Vontas
J,
Kioulos
E,
Pavlidi
N,
Morou
E,
della Torre
A,
Ranson
H.
2012
.
Insecticide resistance in the major dengue vectors Aedes albopictus and Aedes aegypti
.
Pestic Biochem Physiol
104
:
126
131
.
Walker
T,
Johnson
PH,
Moreira
LA,
Iturbe-Ormaetxe
I,
Frentiu
FD,
McMeniman
CJ,
Leong
YS,
Dong
Y,
Axford
J,
Kriesner
P,
Lloyd
AL,
Ritchie
SA,
O’Neill
SL,
Hoffmann
AA.
2011
.
The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations
.
Nature
476
:
450
453
.
Waltz
E.
2022
.
First results from us trial of genetically modified mosquitoes
.
Nature
604
:
608
609
.
Weidhaas
DE,
Schmidt
CH.
1963
.
Mating ability of male mosquitoes, Aedes aegypti (L.), sterilized chemically or by gamma radiation
.
Mosq News
23
:
32
34
.
Werren
JH,
Baldo
L,
Clark
ME.
2008
.
Wolbachia: master manipulators of invertebrate biology
.
Nat Rev Microbiol
6
:
741
751
.
White
LD,
Hutt
RB.
1970
.
Effects of gamma irradiation on longevity and oviposition of the codling moth
.
J Econ Entomol
63
:
866
869
.
WHO and IAEA
.
2020
.
Guidance framework for testing the sterile insect technique as a vector control tool against Aedes-borne diseases
.
Geneva, Switzerland
:
World Health Organization and the International Atomic Energy Agency
.
WMP [World Mosquito Program]
.
2021
.
WMP Mexico factsheet [Internet]
.
WMP [World Mosquito Program]
.
2022a
.
WMP Kiribati factsheet
.
WMP [World Mosquito Program].
2022b
. WMP Vanuatu factsheet
.
WMP [World Mosquito Program]
.
2022c
.
WMP New Caledonia factsheet
.
WMP [World Mosquito Program]
.
2022d
. WMP Fiji factsheet
.
WMP [World Mosquito Program]
.
2022e
.
WMP Vietnam factsheet
.
WMP [World Mosquito Program].
2022f
.
WMP Sri Lanka factsheet [Internet
] .
WMP [World Mosquito Program]
.
2022g
.
WMP Laos factsheet
.
WMP [World Mosquito Program]
.
2022h
.
WMP Indonesia factsheet
.
WMP [World Mosquito Program]
.
2022
i.
WMP Colombia factsheet [Internet
] .
WMP [World Mosquito Program]
.
2022
j.
WMP Brazil factsheet [Internet]
.
Xi
Z,
Ramirez
JL,
Dimopoulos
G.
2008
.
The Aedes aegypti Toll pathway controls dengue virus infection
.
PLoS Pathog
4
:
e1000098
.
Yamada
H,
Maiga
H,
Juarez
J,
De Oliveira Carvalho
D,
Mamai
W,
Ali
A,
Bimbile-Somda
NS,
Parker
AG,
Zhang
D,
Bouyer
J.
2019
.
Identification of critical factors that significantly affect the dose-response in mosquitoes irradiated as pupae
.
Parasites Vectors
12
:
435
.
Yamada
H,
Soliban
SM,
Vreysen
MJ,
Chadee
DD,
Gilles
JR.
2013
.
Eliminating female Anopheles arabiensis by spiking blood meals with toxicants as a sex separation method in the context of the sterile insect technique
.
Parasites Vectors
6
:
1
10
.
Yasuno
M,
Macdonald
WW,
Curtis
CF,
Grover
KK,
Rajagopalan
PK,
Sharwa
LS,
Sharma
VP,
Singh
D,
Singh
KRP,
Agarwal
HV,
Kazmi
SJ.
1978
.
A control experiment with chemosterilized male Culex pipiens fatigans Wied. in a village near Delhi surrounded by a breeding-free zone
.
Med Entomol Zool
29
:
325
343
.
Zacarés
M,
Salvador-Herranz
G,
Almenar
D,
Tur
C,
Argilés
R,
Bourtzis
K,
Bossin
H,
Pla
I.
2018
.
Exploring the potential of computer vision analysis of pupae size dimorphism for adaptive sex sorting systems of various vector mosquito species
.
Parasites Vectors
11
:
656
.
Zhang
D,
Xi
Z,
Li
Y,
Wang
X,
Yamada
H,
Qiu
J,
Liang
Y,
Zhang
M,
Wu
Y,
Zheng
X.
2020
.
Toward implementation of combined incompatible and sterile insect techniques for mosquito control: optimized chilling conditions for handling Aedes albopictus male adults prior to release
.
PloS Negl Trop Dis
14
:
e0008561
.
Zheng
X,
Zhang
D,
Li
Y,
Yang
C,
Wu
Y,
Liang
X,
Liang
Y,
Pan
X,
Hu
L,
Sun
Q,
Wang
X.
2019
.
Incompatible and sterile insect techniques combined eliminate mosquitoes
.
Nature
572
:
56
61
.

Author notes

United States Department of Agriculture, Agricultural Research Service Center for Medical, Agricultural, and Veterinary Entomology, 1600 SW 23rd Drive, Gainesville, FL 32608