Both maternal and paternal genotypes modulate Wolbachia-induced cytoplasmic incompatibility in graham bean beetles

Abstract

Cytoplasmic incompatibility (CI) is a phenomenon where embryonic development is disrupted–often leading to complete failure–when the female parent lacks the symbiont strain carried by the male parent. This mechanism, employed by maternally transmitted symbionts such as Wolbachia, facilitates their rapid spread within a host population. CI has significant potential as a tool for achieving population replacement or suppression, particularly targeting disease vectors and agricultural pests. While complete expression of CI is ideal for such applications, its intensity can vary. Despite extensive research on the symbiont genotypes, the influence of host genetic background on CI expression remains poorly understood. Here, we found that in the bean beetle Callosobruchus analis, the Wolbachia strain wCana2 induces weak CI in its native nuclear background but strong CI in a previously unassociated nuclear background. Crossing experiments reveal that the nuclear backgrounds of both male and female parents can significantly affect CI expression independent of Wolbachia titres in C. analis. These findings uncover novel perspectives on the host-symbiont interactions underlying CI and highlight the complexities to be addressed for its practical application.