Scientists have discovered a new kind of symbiotic organ on the hind legs of the adult female Japanese dinidorid stinkbug Megumenum gracilicorne.
The enlarged hind leg structures were previously thought to be ‘tympanal organs’ for sensing sound, which have evolved in many insect species, including cicadas, grasshoppers, moths and mantises.
But a closer look at adult female stinkbugs collected from different locations in Japan has revealed their actual purpose is far stranger.
“We found that, in reproductively mature females, the tympanum was covered with fibrous white material, resembling fungal hyphae,” the researchers write in a study presenting the findings in the journal Science.
The organ consists of a porous cuticle with fungus “luxuriantly growing from the pores”.
“We observed that the gravid females laid eggs in a row, and when each egg was deposited, the females rhythmically scratched the fungus-covered hindleg organ with the tarsal claws of the opposite hindleg and rubbed the egg surface, smearing the fungi onto the eggs,” the authors write.
“Within a few days, the fungal hyphae grew to cover the entire egg mass. On hatching, the hyphae attached to the body surface of newborn nymphs, although the fungi were subsequently lost as the nymphs moulted and grew.”
While most of the fungi belonged to the family Cordycipitaceae, which includes ‘entomopathogenic’ fungi such as Cordyceps and Beauveria that infect and kill insects, many did not belong to highly pathogenic lineages.
“Notably, within and between collection localities, and between years, fungal composition often markedly differed between individuals,” the authors report.
“These patterns indicated that although M. gracilicorne transmits hindleg-associated fungi to eggs vertically, the fungi are lost during nymphal development and have to be newly acquired by adult females from the environment every generation.”
The researchers found that in the field more than half of the stinkbugs’ eggs were parasitised by the wasp Trissolcus brevinotaulus.
Experiments in the lab later confirmed that while the female wasps approached eggs both covered in fungus or with it removed, they could not lay eggs into the fungus-covered ones.
“If eggs were sparsely coated with fungus, the female wasps were able to compress hyphae by antennal drumming and sometimes succeeded in oviposition [egg laying],” the authors write.
The fungi did not infect the wasps. This suggests they are cultured on the female’s hindleg and transferred to her eggs to act as a physical defence against parasitic wasp attack, rather than as a chemical or pathogenic deterrent.
“We speculate that the female-specific hindleg organ evolved for smearing secretions onto eggs for chemical defense or camouflage, but environmental fungi colonised the organ and exploited the secretion, and the insects co-opted the fungi for egg defense,” the authors conclude.
“Future studies should focus on what molecular mechanisms underpin the development of the dinidorid symbiotic organ and how the specific fungal lineages are selected and cultivated by the insect.”