Open Release of Male Mosquitoes Infected with a Wolbachia Biopesticide: Field Performance and Infection Containment

Abstract

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

Genetic control ofAedesmosquitoes

“…However, it is clear that here, as for conventional genetic engineering of mosquitoes, the relevant research groups have worked hard to clarify and then to comply with all applicable regulations. 8,57,[108][109][110][111] For any self-sustaining genetic system, key questions relate to the initial ability to spread and confer the desired phenotype, and the possibility that evolutionary responses will compromise this, or have some other undesirable effect. Though in principle the large-scale use of such systems may be reversible by further genetic intervention, restoring the status quo ante is at best uncertain; this irreversibility has been a major discussion point in respect of gene drive systems.…”

“…polynesiensis; specific characteristics of this vector may have contributed to the failure of drug-based control programmes in the region. 7,8 A vaccine has long been available for yellow fever, but remains some way off for dengue, following disappointing results from a recent large trial of the leading candidate. 9,10 With no licensed vaccine or specific drug (whether prophylactic or therapeutic), dengue control focuses on the major mosquito vector, Ae.…”

Gene drives and the management of agricultural pests

“…Although organisms carrying local gene drives may still escape from islands, the isolation provided by islands may add an extra level of containment (O'Connor et al 2012). Local gene drives could also be restricted by functioning only on specialized pests (e.g.…”

Wolbachia endosymbionts and human disease control

“…The male Wolbachia phenotype cannot invade the population due to the induced male sterility and strict maternal inheritance [97,122,123]. This IIT approach has been used in Burma, where bi-directional CI was successful in reducing a C. quinquefasciatus population [101] and field trials are underway with these approaches [122,124] with respect to filariasis and dengue and work is underway for the use of IIT against additional insects and diseases, such as malaria and filariasis [12]. What makes IIT compelling as a method of reducing insect population is that traditional approaches, such as the use of insecticides, biological control and larval habitat removal, sometimes fail to affect a substantial proportion of the population, resulting in quick population recovery following treatments.…”