Male‐killing bacteria as agents of insect pest control

Abstract

Summary Continual effort is needed to reduce the impact of exotic species in the context of increased globalization. Any innovation in this respect would be an asset. We assess the potential of combining two pest control techniques: the well‐established sterile insect technique (SIT) and a novel male‐killing technique (MKT), which comprises inoculation of a pest population with bacteria that kill the infected male embryos. Population models are developed to assess the efficiency of using the MKT for insect pest control, either alone or together with the SIT. We seek for conditions under which the MKT weakens requirements on the SIT. Regarding the SIT, we consider both non‐heritable and inherited sterility. In both cases, the MKT and SIT benefit one another. The MKT may prevent the SIT from failing when not enough sterilized males are released due to high production costs and/or uncertainty on their mating ability following a high irradiation dose. Conversely, with already established SIT, pest eradication can be achieved after introduction of male‐killing bacteria with lower vertical transmission efficiency than if the MKT was applied alone. For tephritid fruit flies with non‐heritable sterility, maximal impact of the SIT is achieved when the released males are fully sterile. Conversely, for lepidopterans with inherited sterility, maximal impact of the SIT is achieved for intermediate irradiation doses. In both cases, increasing vertical transmission efficiency of male‐killing bacteria benefits the SIT; high enough vertical transmission efficiency allows for pest eradication where the SIT is absent or induces only pest suppression when used alone. Synthesis and applications. While both techniques can suppress or eliminate the pest on their own, combined application of the male‐killing technique and the sterile insect technique substantially increases pest control efficiency. If male‐killing bacteria are already established in the pest, any assessment of the sterile insect technique needs to account for their presence; otherwise, management recommendations could be exaggerated and unnecessarily costly.

A cascade of destabilizations: Combining Wolbachia and Allee effects to eradicate insect pests

“…Moreover, our results suggest that the two tactics act synergistically: the decrease in population size obtained when CI and mating disruption are combined is higher than the cumulative decrease obtained with each tactic applied separately. Our model therefore supports previous studies that highlight the potential benefit of simultaneously using multiple complementary management tactics (Berec et al., ; Blackwood et al., ; Suckling et al., ). If different tactics benefit from one another, additional methods for controlling a pest population should also be considered.…”

“…Additionally, while our focus was on cytoplasmic incompatibilities, there is evidence that Wolbachia and other bacteria are capable of other reproductive manipulations including male-killing (Dyer & Jaenike, 2004;Richardson, Schiffer, Griffin, Lee, & Hoffman, 2016). Similar conclusions were also made in the recent modelling study of Berec et al (2016), who suggest that SIT is improved when combined with male-killing bacteria. This suggests the existence of additional avenues for utilizing Wolbachia in the context of pest management.…”

“…Braig, Guzman, Tesh, & Oneill, 1994;Hoffmann et al, 2011). At the population level, the conceptual underpinnings for mass releases of incompatible males do not depart from that of SIT, for which interactions with the Allee effect have already been thoroughly analysed (Barclay, 1982;Barclay & Mackauer, 1980;Berec, Maxin, & Bernhauerová, 2016;Boukal & Berec, 2009;Fauvergue, 2013;Lewis & Van Den Driessche, 1993;Yamanaka & Liebhold, 2009).…”

Transgenic Testing Does Not Support a Role for Additional Candidate Genes in Wolbachia Male Killing or Cytoplasmic Incompatibility

“…In addition, male killing is a potential adjunctive or standalone control method. Although it has not yet been tested empirically in arthropods, population modeling suggests that male killing could be especially useful in a two-pronged approach alongside CI or sterile insect technique (SIT) (13). CI and male killing also have important consequences for host evolution and ecology.…”

Wolbachiainfection in Argentinean populations ofAnastrepha fraterculus sp1: preliminary evidence of sex ratio distortion by one of two strains

“…For example, it has been shown that the Incompatible Insect Technique (IIT), which is based on the mechanism of Wolbachia-induced CI, can be used alone or in combination with the Sterile Insect Technique (SIT) to suppress populations of insect pests of agricultural, veterinary or human health importance [58,[62][63][64][65][66][67]. Wolbachia-induced MK has also been suggested as a tool for insect pest control [68,69].…”