Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control

Abstract

C ytoplasmic incompatibility (CI) is the most widespread and, perhaps, the most prominent feature that Wolbachia endosymbionts impose on their hosts (1, 2). CI results in embryonic mortality (EM) in matings between insects of the same species with different Wolbachia infection status (3, 4). It can be either unidirectional or bidirectional. Unidirectional CI is typically expressed when an infected male mates with an uninfected female. The reciprocal mating is fully compatible, as are matings between infected individuals. Bidirectional CI usually occurs in matings between infected individuals harboring different strains of Wolbachia. Although the mechanism of CI has not yet been elucidated on the molecular level, several lines of evidence suggest that Wolbachia somehow modifies the paternal chromosomes during spermatogenesis (mature sperm does not contain the bacteria). This modification influences their behavior during the first mitotic divisions and results in loss of mitotic synchrony (5, 6). Even before the etiological connection between Wolbachia and CI was revealed in mosquitoes (7), attempts were made to exploit CI as a method to suppress natural populations of arthropod pests in a way analogous to the sterile insect technique (S.I.T.) (8). These early attempts involved the mass production and release of incompatible male insects to control wild populations of disease vectors such as the mosquito Culex pipiens (9) and of agricultural pests such as the European cherry fruit fly, Rhagoletis cerasi (10) and, at a smaller scale, the almond moth Cadra (Ephestia) cautella (11).The Mediterranean fruit fly (medfly) Ceratitis capitata is a worldwide pest that infests Ͼ250 fruit varieties of economic importance (12). Extensive screenings of both laboratory and natural populations of medfly have shown that this insect pest is not infected with Wolbachia (13). However, at the time of this writing, ongoing experimental work suggests that some Brazilian natural populations of medfly may be infected with Wolbachia (D. Selivon, personal communication). To determine whether the medfly can support Wolbachia infections and express CI, we used conventional embryonic cytoplasmic injections (14-17) for transfer of natural bacterial symbionts from a related species, R. cerasi (Diptera, Tephritidae) (18), to an uninfected laboratory strain of medf ly C. capitata (Diptera, Tephritidae), the Benakeion strain.Previous studies have demonstrated high levels of incompatibility between natural populations of R. cerasi (10,19), the basis of which was recently shown to be Wolbachia (18). Populations of R. cerasi are either infected by a single Wolbachia variant, wCer1, or coinfected by two variants, wCer1 and wCer2. Incompatibility occurs between males from doubly infected populations and females from singly infected populations, suggesting the wCer2 infection as the cause of CI (18). Additionally, transfer of wCer2 in Drosophila simulans also resulted to the induction of CI (17). An additional, yet uncharacterized, Wolbachia strain (wCer...

Mosquito vector‐associated microbiota: Metabarcoding bacteria and eukaryotic symbionts across habitat types in Thailand endemic for dengue and other arthropod‐borne diseases

“…albopictus have been developed and released into Ae. albopictus populations with naturally occurring Wolbachia for population suppression (Atyame et al., 2016; Mains, Brelsfoard, Rose, & Dobson, 2016) by way of a mechanism known as cytoplasmic incompatibility (CI), where matings between males and females with different strains of Wolbachia experience mortality of the developing embryos (Zabalou et al., 2004). Thus, naturally occurring Wolbachia incompatible with introduced transfected strains could interfere with virus suppression and could also lead to local Ae.…”

Unique clade of alphaproteobacterial endosymbionts induces complete cytoplasmic incompatibility in the coconut beetle

“…A simple technique is to release males infected with CI-inducing Wolbachia into target uninfected populations to suppress population growth of the target, as in the sterile insect technique (SIT) (9). Guaranteeing the sterility of males is essential in SIT, and strong CI expression can effectively suppress a target population.…”

Longicorn beetle that vectors pinewood nematode carries manyWolbachiagenes on an autosome

“…In theory, if maternally transmitted genetic elements that co-inherit with a CI-inducing Wolbachia, such as the Wolbachia itself or other co-infecting endosymbionts, are transformed with a gene of interest, such as a gene that confers resistance of the insect against the pathogen infection, the genetic trait is expected to be spread and fixed in the insect population, driven by the symbiont-induced reproductive phenotype (Beard et al 1993;Durvasula et al 1997;Sinkins et al 1997;Dobson 2003;Sinkins & Gould 2006;McMeniman et al 2009). Mass introduction of males infected with CI-inducing Wolbachia has been proposed as a means for suppressing agricultural and medical pest insect populations (Zabalou et al 2004;Xi et al 2006). In this context, Wolbachia infections in pest insects are potentially of practical utility.…”