The diversity of inherited parasites of insects: the male-killing agent of the ladybird beetle Coleomegilla maculata is a member of the Flavobacteria

Abstract

Many species of insects bear maternally inherited bacteria which contribute to the physiology and metabolism of their host whereas others bear inherited bacteria which are regarded as parasitic. Parasitic behaviours centre on disruption of the production, survival or fertility of male hosts, through which the microbe is not transmitted. One of the most common of these is early male-killing, where the bacteria kill male embryos they enter. The question arises as to why all inherited symbionts are not male-killers. The male-killing agents identified to date derive from two groups: the Proteobacteria and the Mollicutes. However, bacteria from other groups (Spirochaetes, Flavobacteria) are found to be inherited in insects, but contain no incidence of male-killing. We show here an association of male-killing with a bacterium from one of these groups. The bacterium causing male-killing behaviour in the ladybird Coleomegilla maculata is most closely related to Blattabacterium, a host-beneficial Flavobacteria found in cockroaches and some termites. This result indicates there is little if any taxonomic bar to the evolution of male-killing behaviour. This pattern severely contrasts with the evolution of two other parasitic symbiont behaviours, cytoplasmic incompatibility and the induction of host parthenogenesis, which have been found to be associated exclusively with bacteria from one group: Wolbachia. The result is briefly discussed in the light of the incidence of parasitic and beneficial cytoplasmic elements among insects.