The saboteur's tools: Common mechanistic themes across manipulative symbioses

Insects and other arthropods often harbour intracellular bacterial associates. These bacterial symbionts cannot survive outside their host and rely on vertical transmission from infected mothers to their progeny. Thus, symbiont success is tied directly to reproductive success of female hosts. As a result of this intimate relationship, these heritable symbionts have evolved numerous strategies to increase the likelihood of their own transmission, some of which involve the direct manipulation of host reproduction to increase production or fitness of female progeny. These manipulations often come at the expense of male hosts or uninfected individuals, and include strategies such as inducing crossing incompatibilities that increase infected female fitness relative to uninfected females (cytoplasmic incompatibility), killing or feminizing male hosts, and inducing asexual production of female progeny (parthenogenesis). In the past decade, there has been substantial interest in the applied use of these manipulative bacteria in control of pest species, including suppressing disease carried by mosquito vectors of human pathogens. This, along with developments in molecular tools and techniques, has spurred major advances in understanding the mechanisms by which symbiont lineages manipulate their insect hosts, culminating with the identification of the bacterial genes responsible for key manipulations. Here, we review the major research advances in the mechanisms of symbiont-induced reproductive manipulation and compare the mechanisms of a number of common reproductive manipulators.