Background Monoculture farming poses significant disease challenges, but fungus-farming termites are able to successfully keep their monoculture crop free from contamination by other fungi. It has been hypothesised that obligate gut passage of all plant substrate used to manure the fungal symbiont is key to accomplish this. Here we refute this hypothesis in the fungus-farming termite species Macrotermes bellicosus. Results We first used ITS amplicon sequencing to show that plant substrate foraged on by termite workers harbour diverse fungal communities, which potentially could challenge the farming symbiosis. Subsequently, we cultivated fungi from dissected sections of termite guts to show that fungal diversity does not decrease during gut passage. Therefore, we investigated if healthy combs harboured these undesirable fungal genera, and whether the presence of workers affected fungal diversity within combs. Removal of workers led to a surge in fungal diversity in combs, implying that termite defences must be responsible for the near-complete absence of other fungi in functioning termite gardens. Conclusions The rapid proliferation of some of these fungi when colonies are compromised indicates that some antagonists successfully employ a sit-and-wait strategy that allows them to remain dormant until conditions are favourable. Although this strategy requires potentially many years of waiting, it prevents these fungi from engaging in an evolutionary arms race with the termite host, which employs a series of complementary behavioural and chemical defences that may prove insurmountable.

Fungus-growing termites (Isoptera: Macrotermitinae) dominate African savannah ecosystems where they play important roles in ecosystem functioning. Their ecological dominance in these ecosystems has been attributed to living in an ectosymbiosis with fungi of the genus Termitomyces (Lyophyllaceae). Evolutionary theory predicts that the transmission mode of a symbiont determines cooperation and conflict between host and symbiont with vertical transmission (co-transmission of host and symbiont offspring to the next generation) leading to less conflict than horizontal transmission (symbionts are acquired by the host from the environment). Thus, one can hypothesize associations with vertical transmission to be ecological more successful than those with horizontal transmission. We tested this by analyzing whether there is an association between transmission mode and fungus-growing termite species abundance and distribution in West-African savannah and forest ecosystems. We used data from a total of 78 study sites comprising protected National Parks as well as anthropogenically disturbed ecosystems, covering Benin, Côte d'Ivoire, and Togo. Our results showed that, in contrast to expectation, species with horizontal symbiont transmission were more common. We encountered more often species with horizontal than vertical transmission. This result might be due to the fact that only five out of the 25 identified fungus-growing termite species had vertical transmission. Yet, species with horizontal transmission also had higher relative abundances within study sites than those with vertical transmission. Thus, transmission mode is unlikely to explain abundance differences between fungus-growing termite species.

An amendment to this paper has been published and can be accessed via the original article.