Reciprocal Host–Wolbachia Interactions Shape Infection Persistence Upon Loss of Cytoplasmic Incompatibility in Haplodiploids

Abstract

Maternally transmitted symbionts such as Wolbachia spread within host populations by mediating reproductive phenotypes. Cytoplasmic incompatibility (CI) is a reproductive phenotype that interferes with embryonal development when infected males fertilize uninfected females. Wolbachia-based pest control relies on strong CI to suppress or replace pest populations. Host genetic background determines CI strength, and host suppressors that cause weak CI threaten the efficacy of Wolbachia-based pest control programs. In haplodiploids, CI embryos either die (Female Mortality, FM-CI) or develop into uninfected males (Male Development, MD-CI). The reciprocal spread of host suppressors and infection, as well as the interaction with the two CI outcomes in haplodiploids, remains poorly understood. The contribution of sex allocation distortion (Sd), an independent Wolbachia-mediated reproductive phenotype that causes a female-biased sex ratio, to infection persistence in haplodiploids is also poorly understood, especially with imperfect maternal transmission. To address these issues, we developed individual-based simulations and validated this computational tool by tracking Wolbachia spread in experimental Tetranychus urticae populations and by contrasting infection dynamics with deterministic mathematical models. Within ⁓14 host generations, we found that deterministic models inflate infection frequencies relative to simulations by ⁓8.1% and overestimate the driving potential of CI, particularly under low initial infection frequencies. Compared to MD-CI, we show that FM-CI strongly extends infection persistence when nuclear suppressors are segregating in the population. We also quantify how maternal transmission modulates the reciprocal spread of suppressors and infection. Upon loss of CI, we show that hypomorphic expression of Sd (~5%) is sufficient for a stable persistence of infection. We derive a mathematical expression that approximates the stable polymorphic infection frequencies that can be maintained by Sd. Collectively, our results advance our understanding of how symbiosis with CI-inducing Wolbachia and haplodiploid hosts might evolve and inform CI-based pest control programs of potential future risks.