Mothers never miss the moment: a fine-tuned mechanism for vertical symbiont transmission in a subsocial insect

Abstract

In a subsocial stinkbug Parastrachia japonensis, mature adult females lay both fertile eggs and trophic eggs in an underground nest, guard the egg mass for 15–20 days, and collect and provide food fruits for the nymphs. We investigated the vertical transmission of this species’ obligate gut symbiont ‘Candidatus Benitsuchiphilus tojoi’ from mother to offspring. We observed that the mothers started to excrete a copious amount of symbiont-containing white mucus from the anus onto the egg mass at around 45 min before egg hatching; the excretion continued for approximately 40 min, and about 5 min later, fertile eggs in the egg mass started to hatch synchronously. The newborn nymphs immediately ingested the mucous secretion and the trophic eggs, which were completely consumed within 24 h. Mother removal and anal-sealing experiments confirmed that vertical symbiont transmission was mediated by the nymphs’ exploitation of the mother-derived mucous secretion. Mother removal also resulted in asynchronous egg hatching, suggesting maternal involvement in the egg-hatching synchrony. These results indicate that vertical symbiont transmission in P. japonensis is finely tuned to the timing of egg hatching through intricate mother–offspring behavioural interactions, and highlight how sociality can evolutionarily affect symbiosis and vice versa.