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 modifier systems have been identified that suppress CI strength, threatening 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 persistency in haplodiploids is also poorly understood, especially with imperfect maternal transmission. To address these issues, we developed individual-based simulations grounded in the haplodiploid Tetranychus urticae pest system. We validated our simulations by tracking Wolbachia spread in experimental T. urticae populations and by contrasting the predictions of deterministic models. Within [~]15 host generations, we found that deterministic models inflate final infection frequencies by [~]8.1%, and significantly overestimate the driving potential of CI, particularly under low initial infection frequencies. Compared to MD-CI, we show that FM-CI strongly extends infection persistency when suppressors are segregating in the population. We also quantify how maternal transmission and CI outcome modulate 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 closed-form 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 might evolve and inform CI-based pest control programs of potential future risks.