Evidence that Rickettsia manipulate the reproduction of Quadrastichus mendeli, a parasitoid of the Eucalyptus invasive pest Leptocybe invasa recently recorded in Italy

The blue-gum chalcid Leptocybe invasa is a pest of Eucalyptus, likely native to Australia that over the past 15 years has invaded 39 countries on all continents where eucalypts are grown. A recent survey in Australia pointed out three species of parasitoids, the most promising of which, Quadrastichus mendeli, has been released into some Mediterranean countries. At present, the Italian legislation forbids the release of non-native parasitoids; nevertheless in 2014 Q. mendeli was recorded in Southern Italy, probably due to its release in neighbouring countries. After just one year, Q. mendeli has showed a strong impact on Italian populations of L. invasa causing, in some areas, the almost complete disappearance of galls. Q. mendeli is uniparental like its host. As we have recently shown that the thelytokous reproduction of its host (L. invasa) is due to a Rickettsia symbiont, we hypothesised that Rickettsia could be involved also in the thelytoky of Q. mendeli, which may have acquired this symbiont by horizontal transmission. We found evidences that a Parthenogenesis-Inducing (PI) Rickettsia is involved in Q. mendeli’s thelytoky, that is, the symbiont is densely present in the reproductive apparatus and is vertically transmitted. However, despite the close contact inside the gall and a presumably long coevolutionary history due to the parasitoid’s host specificity, host and parasitoid do not share the same Rickettsia. Indeed, phylogenetic analyses of three regions (16S-rRNA, gltA and rpmE-tRNAfMet) showed that Q. mendeli harbours a Rickettsia belonging to the ancestral group, subgroup limoniae. This is the first finding of a PI Rickettsia of this clade infecting a hymenopteran, and represents the fourth instance of PI Rickettsia. Remarkably, all PI Rickettsia discovered so far infect wasps of the hymenopteran family Eulophidae, and belong to three different phylogenetic groups, suggesting multiple independent evolution of the PI phenotype in the genus Rickettsia.