Diversity and evolution of bacterial symbionts in the gut symbiotic organ of jewel stinkbugs (Hemiptera: Scutelleridae)

The majority of plant-sucking stinkbugs of the superfamily Pentatomoidea possess numerous crypts in the midgut as the symbiotic organ, where specific and beneficial symbiotic bacteria are harbored extracellularly. The host–symbiont relationships are co-speciating in the families Plataspidae, Acanthosomatidae and Urostylididae, but promiscuous in the families Pentatomidae and Cydnidae. As for the family Scutelleridae, only a few species have been examined for their gut symbiotic bacteria. Here, we comprehensively investigated Japanese scutellerid stinkbugs representing 6 genera, 8 species, and 24 individuals. Molecular phylogenetic analysis revealed that the scutellerid gut symbionts are polyphyletic, consisting of at least seven distinct phylogenetic groups in the Gammaproteobacteria. In four of the seven groups, the symbionts were closely related to each other, to the pentatomid gut symbionts, and to environmental bacteria of the genus Pantoea. These results strongly suggest that the scutellerid gut symbionts are of multiple evolutionary origins, presumably entailing repeated symbiont acquisitions, replacements and/or horizontal transfers in a promiscuous manner. Elimination of the gut symbionts from Lampromicra miyakona resulted in high mortality without adult emergence, confirming that the gut symbionts are of beneficial nature. In conclusion, the host–symbiont associations in the Scutelleridae seem to be similar to those in the Pentatomidae and Cydnidae.