Release Of Sterile Males Research Articles

Cross-Mating Compatibility and Competitiveness among Aedes albopictus Strains from Distinct Geographic Origins - Implications for Future Application of SIT Programs in the South West Indian Ocean Islands.

The production of large numbers of males needed for a sustainable sterile insect technique (SIT) control program requires significant developmental and operational costs. This may constitute a significant economic barrier to the installation of large scale rearing facilities in countries that are undergoing a transition from being largely dependent on insecticide use to be in a position to integrate the SIT against Aedes albopictus. Alternative options available for those countries could be to rely on outsourcing of sterile males from a foreign supplier, or for one centralised facility to produce mosquitoes for several countries, thus increasing the efficiency of the mass-rearing effort. However, demonstration of strain compatibility is a prerequisite for the export of mosquitoes for transborder SIT applications. Here, we compared mating compatibility among Ae. albopictus populations originating from three islands of the South Western Indian Ocean, and assessed both insemination rates and egg fertility in all possible cross-mating combinations. Furthermore, competitiveness between irradiated and non-irradiated males from the three studied strains, and the subsequent effect on female fertility were also examined. Although morphometric analysis of wing shapes suggested phenoptypic differences between Ae. albopictus strains, perfect reproductive compatibility between them was observed. Furthermore, irradiated males from the different islands demonstrated similar levels of competitiveness and induced sterility when confronted with fertile males from any of the other island populations tested. In conclusion, despite the evidence of inter-strain differences based on male wing morphology, collectively, our results provide a new set of expectations for the use of a single candidate strain of mass-reared sterile males for area-wide scale application of SIT against Ae. albopictus populations in different islands across the South Western Indian Ocean. Cross-mating competitiveness tests such as those applied here are necessary to assess the quality of mass reared strains for the trans-border application of sterile male release programs.

Challenges and options for disease vector control

The ongoing Zika virus outbreak, which briefly threatened to put a stop to the 2016 Olympic Games in Brazil, has again focused attention on the threat of vector‐borne diseases. One efficient strategy to battle such diseases, now underway in Brazil to fight the Zika virus, is to kill the insects that carry the pathogen. Vector control has been practised with varying effectiveness for at least half a century, especially for malaria; the Brazil outbreak again highlights the need for integrating existing methods including the use of insecticides, vaccines, drugs and low technology such as sanitation to keep insect vectors at bay. In addition, new approaches are being developed based on sophisticated methods such as genome editing of the insect vector and deliberate infection of mosquitoes with the Wolbachia bacteria. However, attempts to scale up these new methods from field trials to deployment have been slowed down or halted by environmental concerns or public resistance against genetically modified organisms. The Zika outbreak in South America has stimulated cross‐border collaboration of public health authorities and increased pressure to use new integrative approaches that are essential for combatting vector‐borne diseases. The irony is that the Zika virus itself has a minimal global impact compared with other insect‐borne pathogens, but it has attracted enormous publicity because of the risk of causing microcephaly in unborn children, combined with the coincidence of the outbreak during the Olympic year. The exact risk for the foetus is as yet unknown [1], but it is clear that Zika is otherwise a relatively mild disease with no symptoms in the majority of cases (http://www.cdc.gov/zika/symptoms/index.html). By contrast, other mosquito‐borne diseases, including malaria, yellow fever, dengue and chikungunya (CHIKV), are major causes of both mortality and morbidity, responsible for hundreds of millions of cases each year and millions of deaths …

Tetracycline-suppressible female lethality and sterility in the Mexican fruit fly, Anastrepha ludens.

The sterile insect technique (SIT) involves the mass release of sterile males to suppress insect pest populations. SIT has been improved for larval pests by the development of strains for female-specific tetracycline-suppressible (Tet-off) embryonic lethal systems for male-only populations. Here we describe the extension of this approach to the Mexican fruit fly, Anastrepha ludens, using a Tet-off driver construct with the Tet-transactivator (tTA) under embryo-specific Anastrepha suspensa serendipity α (As-sry-α) promoter regulation. In the absence of tetracycline, tTA acts upon a Tet-response element linked to the pro-apoptotic cell death gene lethal effector, head involuation defective (hid), from A. ludens (Alhid(Ala2) ) that contains a sex-specific intron splicing cassette, resulting in female-specific expression of the lethal effector. Parental adults double-homozygous for the driver/effector vectors were expected to yield male-only progeny when reared on Tet-free diet, but a complete lack of oviposited eggs resulted for each of the three strains tested. Ovary dissection revealed nonvitellogenic oocytes inall strains that was reversible by feeding females tetracycline for 5 days after eclosion, resulting in male-only adults in one strain. Presumably the sry-α promoter exhibits prezygotic maternal expression as well as zygotic embryonic expression in A. ludens, resulting in a Tet-off sterility effect in addition to female-specific lethality.

Establishment of a satellite rearing facility to support the release of sterile Aedes albopictus males. I. Optimization of mass rearing parameters

The vector species Aedes albopictus (Skuse, 1894) was recorded in Turkey for the first time, near the Greek border, in 2011 and a high risk of expansion towards Aegean and Mediterranean coasts of Turkey was estimated. A preliminary study was planned to evaluate the possibility of creating a satellite mass rearing facility for this species and manage a larval rearing procedure by using the new mass-rearing technology proposed by the International Atomic Energy Agency (IAEA). For this purpose, the effects of different larval densities (1, 2, 3 and 4 larvae per ml) on the preimaginal development were evaluated by observing pupal, adult and male productivity using life cycle trials. Geometric morphometric analyses were also performed to define all phenotypic differences that occurred on the wing size and shape morphology of adult stage at the four different rearing conditions tested. A high pupation productivity was obtained with a larval density of 2 larvae/ml while adult emergence ratio was not affected by the densities tested. No significant difference was observed in shape of the wings among different densities in males and females. Nevertheless, a significant difference in female’s centroid sizes was observed between the treatment groups 1–2 and 3–4 larvae/ml and in males centroid size reared at 1 larvae/ml versus the other densities.

Approximating Optimal Release in a Deterministic Model for the Sterile Insect Technique

Cost/benefit analyses are essential to support management planning and decisions before launching any pest control program. In particular, applications of the sterile insect technique (SIT) are often prevented by the projected economic burden associated with rearing processes. This has had a deep impact on the technique development and its use on insects with long larval periods, as often seen in beetles. Under the assumptions of long adult timespan and multiple mating, we show how to find approximate optimal sterile release policies that minimize costs. The theoretical framework proposed considers the release of insects by pulses and finds approximate optimal release sizes through stochastic searching. The scheme is then used to compare simulated release strategies obtained for different pulse schedules and release bounds, providing a platform for evaluating the convenience of increasing sterile male release intensity or extending the period of control.

Determination of the sterile release rate for stopping growing age-structured populations

ABSTRACTA freely-growing age-structured population was modeled for growth and control by sterile male releases. Equilibrium populations yield critical sterile male release rates that would hold the population at equilibrium. It is shown here that these rates may be different from the release rates required to stop a growing population and bring it to an equilibrium. A computer simulation was constructed of this population and a parameter sensitivity analysis graphed the effects on the required sterile male release rate of fertility, mating delay in adult females, net juvenile survivorship, three adult survivorship curves, the time spent in the juvenile stages, and total life span. The adult survivorship curves had the greatest effect on the required sterile release rate for population elimination. The required release rate was also determined for Ceratitis capitata (Wiedemann) using survivorship and fertility data from a laboratory strain. The concepts of over-flooding ratio and release ratio were discussed and quantified for the cases above.

Re-examination of sea lamprey control policies for the St. Marys River: completion of an adaptive management cycle

The St. Marys River (SMR) historically has been a major producer of sea lampreys (Petromyzon marinus) in the Laurentian Great Lakes. In the early 2000s, a decision analysis (DA) project was conducted to evaluate sea lamprey control policies for the SMR; this project suggested that an integrated policy of trapping, sterile male releases, and Bayluscide treatment was the most cost-effective policy. Further, it concluded that formal assessment of larval sea lamprey abundance and distribution in the SMR would be valuable for future evaluation of control strategies. We updated this earlier analysis, adding information from annual larval assessments conducted since 1999 and evaluating additional control policies. Bayluscide treatments continued to be critical for sea lamprey control, but high recruitment compensation minimized the effectiveness of trapping and sterile male release under current feasible ranges. Because Bayluscide control is costly, development of strategies to enhance trapping success remains a priority. This study illustrates benefits of an adaptive management cycle, wherein models inform decisions, are updated based on learning achieved from those decisions, and ultimately inform future decisions.

Modeling ephemeral mating encounters in insects: The emergence of mate-finding Allee effects and applications to theoretical models of sterile release

Lack of successful mating encounters in two-sex insect populations is a mechanism that might trigger reproductive Allee effects. In this paper I examine a function that models ephemeral mating encounters through the expected density of pairs formed by individuals of both sexes at any time. When this function is incorporated in a general system of differential equations for a two-sex population the solutions exhibit the emergence of an Allee effect for low population densities. Compared with current conceptual models for mate-finding Allee effects, the proposed pairing function does not include a parameter that quantifies the Allee effect strength, a feature that might be useful when information to parameterize Allee effects is unavailable. The mating function is then used to numerically explore how mate-finding Allee effects are enhanced by the release of sterile males in theoretical models where (i) the initial sex ratio is skewed, (ii) sterile males are released in pulses and (iii) partial female remating is allowed.

Mapping the benefit-cost ratios of interventions against bovine trypanosomosis in Eastern Africa

This study builds upon earlier work mapping the potential benefits from bovine trypanosomosis control and analysing the costs of different approaches. Updated costs were derived for five intervention techniques: trypanocides, targets, insecticide-treated cattle, aerial spraying and the release of sterile males. Two strategies were considered: continuous control and elimination. For mapping the costs, cattle densities, environmental constraints, and the presence of savannah or riverine tsetse species were taken into account. These were combined with maps of potential benefits to produce maps of benefit-cost ratios.The results illustrate a diverse picture, and they clearly indicate that no single technique or strategy is universally profitable. For control using trypanocide prophylaxis, returns are modest, even without accounting for the risk of drug resistance but, in areas of low cattle densities, this is the only approach that yields a positive return. Where cattle densities are sufficient to support it, the use of insecticide-treated cattle stands out as the most consistently profitable technique, widely achieving benefit-cost ratios above 5. In parts of the high-potential areas such as the mixed farming, high-oxen-use zones of western Ethiopia, the fertile crescent north of Lake Victoria and the dairy production areas in western and central Kenya, all tsetse control strategies achieve benefit-cost ratios from 2 to over 15, and for elimination strategies, ratios from 5 to over 20. By contrast, in some areas, notably where cattle densities are below 20per km2, the costs of interventions against tsetse match or even outweigh the benefits, especially for control scenarios using aerial spraying or the deployment of targets where both savannah and riverine flies are present. If the burden of human African trypanosomosis were factored in, the benefit-cost ratios of some of the low-return areas would be considerably increased.Comparatively, elimination strategies give rise to higher benefit-cost ratios than do those for continuous control. However, the costs calculated for elimination assume problem-free, large scale operations, and they rest on the outputs of entomological models that are difficult to validate in the field. Experience indicates that the conditions underlying successful and sustained elimination campaigns are seldom met.By choosing the most appropriate thresholds for benefit-cost ratios, decision-makers and planners can use the maps to define strategies, assist in prioritising areas for intervention, and help choose among intervention techniques and approaches. The methodology would have wider applicability in analysing other disease constraints with a strong spatial component.

Long-term Effects of Carbohydrate Availability on Mating Success of Newly Eclosed Aedes albopictus (Diptera: Culicidae) Males.

Sugar availability varies greatly in nature, and determining how this affects male mosquito fitness is essential for understanding population dynamics. We allowed male Aedes albopictus (Skuse) carbohydrate access for increasing intervals of time immediately after eclosion and we evaluated their fitness by comparing mortality, mating success, and sperm transfer. We compared individual male Ae. albopictus, which were offered water or 20% sucrose solution for 24, 48, or 72 h. As predicted, there were significant increases in fitness for each additional day of sucrose access. Following sugar exposure, we allowed males daily access to three virgin females. We assessed mating success through observation of spermatozoa in the female spermathecae. When individuals of the same age were compared, males with sugar access exhibited significantly greater mating success than water-treated males in all treatments. The total number of spermathecae filled by males with sugar access in the 48- and 72-h treatments was also significantly greater on some days; these were 3-5 d posteclosion in the 48-h treatment and 5-6 d posteclosion in the 72-h treatment. We conclude that extended sugar access at eclosion is important for maximizing fitness in male Ae. albopictus and should be applicable to sterile male release efforts, especially when laboratory-reared males suffered from other disadvantages. We recommend retaining adult males for 3 d posteclosion prior to release to improve their mating success in male release initiatives.

Seasonal variation in size estimates of Aedes albopictus population based on standard mark–release–recapture experiments in an urban area on Reunion Island

The implementation of the sterile insect technique for area-wide vector control requires that natural population density be accurately estimated to determine both the appropriate time to treat and the adequate number of sterile males for release. Herein, we used mark–release–recapture (MRR) to derive seasonal abundance estimates of Aedes albopictus population sizes within a delimited geographical area in Reunion Island. Population size of Ae. albopictus was estimated through four mark–release–recapture experiments carried out separately in different seasons. Marked males and females were released each time, and recaptured using BG sentinel traps for six consecutive days. Data were used to estimate the population size using a conceptual model that incorporates the variation in daily mortality rates. The likely influence of environmental factors on the magnitude of catches and on population fluctuation was analyzed. A total of 2827 mosquitoes (1914 males and 913 females) were marked and released on four occasions during dry and wet seasons. After release, 138 males (7.21%) and 86 females (9.41%) of the marked specimens were recaptured in subsequent samplings. The effectiveness of the daily captures of wild and released mosquitoes was significantly influenced by meteorological conditions such as temperature, rainfall, wind speed and light intensity. The estimates of Ae. albopictus population size obtained with our model estimator ranged from 298 to 1238 males and 604 to 2208 females per ha, with seasonal variability – higher population size in the humid season. The presented results will be essential in designing more effective sterile male release strategies for long-term suppression of wild Ae. albopictus populations.

Silencing the buzz: a new approach to population suppression of mosquitoes by feeding larvae double-stranded RNAs.

BackgroundMosquito-borne diseases threaten over half the world’s human population, making the need for environmentally-safe mosquito population control tools critical. The sterile insect technique (SIT) is a biological control method that can reduce pest insect populations by releasing a large number of sterile males to compete with wild males for female mates to reduce the number of progeny produced. Typically, males are sterilized using radiation, but such methods can reduce their mating competitiveness. The method is also most effective if only males are produced, but this requires the development of effective sex-sorting methods. Recent efforts to use transgenic methods to produce sterile male mosquitoes have increased interest in using SIT to control some of our most serious disease vectors, but the release of genetically modified mosquitoes will undoubtedly encounter considerable delays as regulatory agencies deal with safety issues and public concerns.MethodsTestis genes in the dengue vector Aedes aegypti were identified using a suppression subtractive hybridization technique. Mosquito larvae were fed double-stranded RNAs (dsRNAs) that targeted both the testis genes and a female sex determination gene (doublesex) to induce RNA interference (RNAi) -mediated sterility and inhibition of female development. Fertility and mating competiveness of the treated males were assessed in small-scale mating competition experiments.ResultsFeeding mosquito larvae dsRNAs targeting testis genes produced adult males with greatly reduced fertility; several dsRNAs produced males that were highly effective in competing for mates. RNAi-mediated knockdown of the female-specific isoform of doublesex was also effective in producing a highly male-biased population of mosquitoes, thereby overcoming the need to sex-sort insects before release.ConclusionsThe sequence-specific gene-silencing mechanism of this RNAi technology renders it adaptable for species-specific application across numerous insect species. We envisage its use for traditional large-scale reared releases of mosquitoes and other pest insects, although the technology might also have potential for field-based control of mosquitoes where eggs deposited into a spiked larval site lead to the release of new sterile males.

Male-specific Y-linked transgene markers to enhance biologically-based control of the Mexican fruit fly, Anastrepha ludens (Diptera: Tephritidae).

BackgroundReliable marking systems are critical to the prospective field release of transgenic insect strains. This is to unambiguously distinguish released insects from wild insects in the field that are collected in field traps, and tissue-specific markers, such as those that are sperm-specific, have particular uses such as identifying wild females that have mated with released males. For tephritid fruit flies such as the Mexican fruit fly, Anastrepha ludens, polyubiquitin-regulated fluorescent protein body markers allow transgenic fly identification, and fluorescent protein genes regulated by the spermatocyte-specific β2-tubulin promoter effectively mark sperm. For sterile male release programs, both marking systems can be made male-specific by linkage to the Y chromosome.ResultsAn A. ludens wild type strain was genetically transformed with a piggyBac vector, pBXL{PUbnlsEGFP, Asβ2tub-DsRed.T3}, having the polyubiquitin-regulated EGFP body marker, and the β2-tubulin-regulated DsRed.T3 sperm-specific marker. Autosomal insertion lines effectively expressed both markers, but a single Y-linked insertion (YEGFP strain) expressed only PUbnlsEGFP. This insertion was remobilized by transposase helper injection, which resulted in three new autosomal insertion lines that expressed both markers. This indicated that the original Y-linked Asβ2tub-DsRed.T3 marker was functional, but specifically suppressed on the Y chromosome. The PUbnlsEGFP marker remained effective however, and the YEGFP strain was used to create a sexing strain by translocating the wild type allele of the black pupae (bp+) gene onto the Y, which was then introduced into the bp- mutant strain. This allows the mechanical separation of mutant female black pupae from male brown pupae, that can be identified as adults by EGFP fluorescence.ConclusionsA Y-linked insertion of the pBXL{PUbnlsEGFP, Asβ2tub-DsRed.T3} transformation vector in A. ludens resulted in male-specific expression of the EGFP fluorescent protein marker, and was integrated into a black pupae translocation sexing strain (T(YEGFP/bp+), allowing the identification of male adults when used in sterile male release programs for population control. A unique observation was that expression of the Asβ2tub-DsRed.T3 sperm-specific marker, which was functional in autosomal insertions, was specifically suppressed in the Y-linked insertion. This may relate to the Y chromosomal regulation of male-specific germ-line genes in Drosophila.

Pest persistence and eradication conditions in a deterministic model for sterile insect release

The release of sterile insects is an environment friendly pest control method used in integrated pest management programmes. Difference or differential equations based on Knipling's model often provide satisfactory qualitative descriptions of pest populations subject to sterile release at relatively high densities with large mating encounter rates, but fail otherwise. In this paper, I derive and explore numerically deterministic population models that include sterile release together with scarce mating encounters in the particular case of species with long lifespan and multiple matings. The differential equations account separately the effects of mating failure due to sterile male release and the frequency of mating encounters. When insects spatial spread is incorporated through diffusion terms, computations reveal the possibility of steady pest persistence in finite size patches. In the presence of density dependence regulation, it is observed that sterile release might contribute to induce sudden suppression of the pest population.

Male reproductive biology of Aedes mosquitoes

Among Aedes mosquitoes are species responsible for transmission of serious pathogens to humans. To cope with the current threats to long-term effectiveness of the traditional vector control methods, non-conventional control strategies are being developed. These include autocidal control such as the release of sterile males (sterile insect technique) and the release of Wolbachia-infected males to induce sexual sterility (incompatible insect technique) and pathogen-refractory strain replacement variations using Wolbachia. Sterile male types of techniques particularly depend on released males’ ability to successfully mate with wild females. For that reason, a good understanding of male mating biology, including a thorough understanding of the reproductive system and mating capacity, increases the likelihood of success of such genetic vector control programmes. Here we review the literature concerning the reproduction of Aedes mosquitoes with an emphasis on the male biology. We consider sexual maturation, mate finding, insemination, male reproductive capacity, and the occurrence of multiple matings. We also discuss which parameters are of greatest importance for the successful implementation of autocidal control methods and propose questions for future research.

Review: Improving our knowledge of male mosquito biology in relation to genetic control programmes

The enormous burden placed on populations worldwide by mosquito-borne diseases, most notably malaria and dengue, is currently being tackled by the use of insecticides sprayed in residences or applied to bednets, and in the case of dengue vectors through reduction of larval breeding sites or larviciding with insecticides thereof. However, these methods are under threat from, amongst other issues, the development of insecticide resistance and the practical difficulty of maintaining long-term community-wide efforts. The sterile insect technique (SIT), whose success hinges on having a good understanding of the biology and behaviour of the male mosquito, is an additional weapon in the limited arsenal against mosquito vectors. The successful production and release of sterile males, which is the mechanism of population suppression by SIT, relies on the release of mass-reared sterile males able to confer sterility in the target population by mating with wild females. A five year Joint FAO/IAEA Coordinated Research Project brought together researchers from around the world to investigate the pre-mating conditions of male mosquitoes (physiology and behaviour, resource acquisition and allocation, and dispersal), the mosquito mating systems and the contribution of molecular or chemical approaches to the understanding of male mosquito mating behaviour. A summary of the existing knowledge and the main novel findings of this group is reviewed here, and further presented in the reviews and research articles that form this Acta Tropica special issue.

Transient Population Dynamics of Mosquitoes during Sterile Male Releases: Modelling Mating Behaviour and Perturbations of Life History Parameters

The release of genetically-modified or sterile male mosquitoes offers a promising form of mosquito-transmitted pathogen control, but the insights derived from our understanding of male mosquito behaviour have not fully been incorporated into the design of such genetic control or sterile-male release methods. The importance of aspects of male life history and mating behaviour for sterile-male release programmes were investigated by projecting a stage-structured matrix model over time. An elasticity analysis of transient dynamics during sterile-male releases was performed to provide insight on which vector control methods are likely to be most synergistic. The results suggest that high mating competitiveness and mortality costs of released males are required before the sterile-release method becomes ineffective. Additionally, if released males suffer a mortality cost, older males should be released due to their increased mating capacity. If released males are of a homogenous size and size-assortative mating occurs in nature, this can lead to an increase in the abundance of large females and reduce the efficacy of the population-suppression effort. At a high level of size-assortative mating, the disease transmission potential of the vector population increases due to male releases, arguing for the release of a heterogeneously-sized male population. The female population was most sensitive to perturbations of density-dependent components of larval mortality and female survivorship and fecundity. These findings suggest source reduction might be a particularly effective complement to mosquito control based on the sterile insect technique (SIT). In order for SIT to realize its potential as a key component of an integrated vector-management strategy to control mosquito-transmitted pathogens, programme design of sterile-male release programmes must account for the ecology, behaviour and life history of mosquitoes. The model used here takes a step in this direction and can easily be modified to investigate additional aspects of mosquito behaviour or species-specific ecology.

Analysis of the genitalia rotation in the male Anopheles funestus (Diptera: Culicidae)

Anopheles funestus is a major malaria vector in Africa. Insecticide resistance has developed in populations of this species in several African countries, prompting the need to develop additional vector control methods such as the sterile insect technique (SIT). This technique requires an understanding of those underlying physiological events that lead to sexual maturity of An. funestus males, the rotation of their genitalia in particular. The aim of this study was to qualitatively and quantitatively describe genital rotation in An. funestus males as it is an essential function of sexual maturation. Genital rotation of all the males reached its final rotation stage (135–180° rotation) 36h post emergence at 23±1°C in laboratory colonised An. funestus males. These males had a comparable rotation rate to wild caught An. funestus at the same temperature setting. A temperature change (either 18±1°C or 29±1°C versus 23±1°C) significantly influenced the genital rotation rate such that this rate increased with increasing temperature. This information enhances our knowledge of the An. funestus male biology. This is important in terms of applying the sterile insect technique as the understanding and manipulation of the rate of sexual maturation in males has implications for the timing of sterile male release.

Transcriptome analysis in Ceratitis capitata to unveil genes involved in ageing-maturation process

The sterile insect technique (SIT) is widely used in integrated programmes against the Mediterranean fruit fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). Information on the age distribution of insects, and more particularly, the knowledge of wild female reproductive status (mature or not) at the time of the sterile male release is one of the key factors for the success of the SIT. In recent years, sequencing analysis has become an important tool in molecular biology. In this work we present a genome-wide expression analysis based on SSH (substractive sequence hybridization) and EST (expressed sequence tag) sequencing and macroarray expression analysis to identify signature genes related to the ageing-maturing process in C. capitata, leading to the successful identification of new putative candidate genes of reproductive status in medfly that would serve as molecular markers for ageing. We have sorted out 94 unigenes from 873 single-pass ESTs, of which 57% have homology with known genes. Ageing-maturing process in C. capitata presents a marked expression pattern accompanied by the increase of transcription level of genes involved in reproduction (vitellogenins, chorion proteins and male-specific serum proteins). Other identified cDNAs (43%) with a differential expression pattern would be also candidates but deserve further studies, as they belong to the unknown function class.

Male mosquitoes make waves in paradise

Invited Commentary on ‘Open release of male mosquitoes infected with a Wolbachia biopesticide: field performance and infection containment’, O’Connor et al. While the ‘neglected’ mosquito-borne tropical diseases dengue and chikungunya often dominate attention, lymphatic filariasis continues to be a threat to over a billion people. The obvious subdivision provided by islands of the south Pacific provide what is arguably low-hanging fruit for a progressive mass-drug-administration program to eliminate this endemic disease, but this has met with surprising difficulty.1 The usual hurdles of ensuring compliance and consistent program implementation contribute, but these are exacerbated by what is apparently a very efficient vector, even at low densities, Aedes polynesiensis. Often hiding in crab holes and rat-gnawed coconut shells, Ae. polysiensis is protected from exposure to insecticides, so unconventional approaches to control are being considered including methoprene-impregnated baits that the crabs ‘auto-disseminate’ to their burrows2 and fabric resting targets.3 Isolated island mosquito populations have traditionally been favorite targets for genetic control strategies, so the combination of a stubborn vector, a significant disease and hundreds of islands makes the south Pacific a perfect target. Stephen Dobson’s lab at the University of Kentucky has exploited this opportunity to explore sexual sterility for control by infecting Ae. polynesiensis with particular Wolbachia endosymbionts. Unlike the population replacement goal of the Australia Ae. aegypti Wolbachia program,4 Dobson’s lab is using Wolbachia solely for the male sterility that occurs when infected males mate with uninfected wild females. A similar approach has been used previously, most dramatically against Culex quinquefasciatus.5 O’Conner et al.6 have now reported the results of a field release of male Ae. polynesiensis infected (via introgression) with an Ae. riversi Wolbachia. This endosymbiont causes bidirectional sexual sterility when mated to wild Ae. polynesiensis. By releasing approximately 100 000 carefully selected males, they were able to demonstrate population suppression on Toamaro atoll (French Polynesia) relative to two control sites. They also demonstrated that the likelihood of males transfering Wolbachia to Ae. polynesiensis, Ae. Aegypti, or Ae. albopictus is, at best, extremely low. Essential to this approach is that females cannot be released (at least in large numbers) since they can cause population replacement rather than elimination. On the scale of production of this experiment, they were able to accomplish this and argue that replacement is not likely regardless. All results were good preliminary demonstrations of safety and efficaciousness. In spite of arguments that population replacement is not likely, stringent removal of females will continue to be necessary until their inability to establish is demonstrated to be a fact. Considering this requirement, the main advantage of bi-directional sexual incompatibility over classical irradiation-based sterile male release may be good mating competitiveness: this was demonstrated. This project revives an approach whose performance must compete head-to-head with other options for producing similar sterile-male effects: classical sterile insect technique and transgenesis. Critical to further development of the technology is the ability to successfully eliminate females on a large scale during production, a technology that is not yet available. However, continued development of such methods as this team has demonstrated should move ahead until their potential in area-wide programs is soundly assessed.