Dual effects of insect fecundity overdispersion on the Wolbachia establishment and the implications for epidemic biocontrol

The utilization of the most prevalent endosymbionts Wolbachia spp. to tackle insect-borne viral diseases is growing rapidly. Understanding how and how often Wolbachia establish in a local population is fundamental to replacement releases but remains unclear. Previous models make the prediction of poor performance of Wolbachia at low frequencies that contradicts the natural ubiquity of those endosymbionts, and the prediction of almost certain fixation of Wolbachia at high frequencies that cannot explain the large fluctuations and collapses of infection in field releases. Here, we investigated whether those paradoxes can be reconciled by the stochasticity originating from fecundity overdispersion within host insects. We first reanalysed published data sets and showed that fecundity was mostly overdispersed in insects. To understand the effects of host fecundity variation on Wolbachia establishment, we further constructed a model accounting for cytoplasmic incompatibility and fecundity cost on infected hosts. Based on the empirical results of fecundity overdispersion, the model predicted not only a biologically relevant probability for Wolbachia to establish from a single infection, but also a large uncertainty of fixation at high frequencies. These findings will enable a better understanding of endosymbiont-insect dynamics and help to design sustainable strategies to control arboviral diseases.