Among biologists who study social insects, the development of sophisticated fungus agriculture in leafcutter ants and some termites is considered one of the landmark events in social insect evolution. In the most advanced species, the insects organize massive foraging trips for vegetation, converting it into a suitable medium on which fungal gardens proliferate. In exchange, the fungi compose the main diet of their gardeners, supporting vast nests of hundreds of thousands of individuals. We continue to make interesting discoveries on the ecology and evolution of these mutualisms, even though we’ve studied these systems to death in the past few decades. As it turns out, other animals as ecologically and phylogenetically diverse as bark beetles, sea snails, and damselfish have evolved ‘farming’ of some kind.
Being mainly subterranean insects that live in dark, humid nests, it would make sense that ant and termite lineages would have coevolved ancient and advanced partnerships with equally specialized fungi over millions of years. But what about other social insects? In The Insect Societies (1971), E.O. Wilson, noting that social bees and wasps seem to lack the accompanying communities of inquiline insects (highly specialized freeloaders) that inhabit ant and termite nests, proposed that this might be because bees and wasps tend to build more tightly sealed and inaccessible nests, sanitize nests more thoroughly of detritus, use more durable materials to build their nests, and construct them in arboreal environments rather than underground. I suspect that Wilson would have extended this hypothesis to microorganisms as well. Aside from my humble opinion that this explanation is excessively reductive and hand-wavy, Wilson’s observation is true. After all, the bees, despite their overall uniform ecology as nectar feeders and pollen hoarders, have spawned eusocial lineages just as advanced and varied as the ants and termites, so we ought to expect that some of these lineages have likewise evolved intimate associations with fungi in a convergent matter. Thus, my excitement at the news that we now have our first fungus-cultivating bee, as described by Menezes et al. in Current Biology.
Scaptotrigona depilis, an already known and rather well-studied tropical stingless bee, has a fairly typical social life compared to its relatives in the Meliponini. The colony’s home life is centered on the nest, a complex structure built out of cerumen, a mixture of wax secreted by young workers and resin brought in from outside. It is this cerumen that is used to build individual cells to store food and house bee larvae, which will develop into the next generation of adult workers. Cerumen is recycled throughout the hive to build and repair various other structures, and when a new queen leaves the mother colony to found a new colony elsewhere, a swarm of workers uses cerumen from the old hive to begin construction on the new nest. Atypically, however, the fungus, an unidentified species in the genus Monascus, also inhabits the cerumen, and as the bees reuse and transport cerumen, they spread the fungus throughout the nest and disperse it to new sites. In fact, the fungus seems to be so dependent on bees for propagating it that the authors found no evidence of the fungus producing conidia, the durable clonal spores generated by normal fungi. Instead, it grows exclusively as a webby mass of active growing cells called mycelium.
Also like other social bees, after a new brood cell is completed, S. depilis workers fill it with a barfed-up soup of pollen and honey, enough to fuel the development of one bee larva to maturity. After the enormous queen deposits a single egg on the mess and shuffles away, the cell is completely sealed off; the baby bee hatches literally swimming in its own exclusive food mass. As Monascus grows on the food–in fact, the brood cells are the only place where the fungal mycelium actively grows–the larva actively consumes the fungus as well, so that nothing remains in the cell by the time the larva matures and begins spinning its cocoon. To test the importance of the fungus to bee larva survival, the researchers grew 300 S. depilis larvae in the lab on either UV-sterilized food or sterilized food that was then retreated with the fungus. While 76% of larvae fed food containing the fungus survived, only a piddling 8% of larvae fed sterilized food did the same.
Clearly, the fungus was playing a key role in bee development. But what was it doing? During the lab experiments, they found that sterilized bee food quickly spoiled, but food containing Monascus stayed fresh. Incidentally, other species of Monascus are known to secrete antimicrobial agents, and the fungus has been long used by human cultures to preserve and ferment food. However, when Menezes et al. tested the effectiveness of bee food against E. coli and staph bacteria compared to the antibiotics penicillin and streptomycin, they found it was not effective all. (Newly made bee food was as effective as the antibiotics in inhibiting growth, but this was probably due to properties independent of the fungus, similar to the way that honey in your cupboard doesn’t spoil). Perhaps the fungus is only effective in excluding other microbes more specialized in growing on the bee food or plays another role entirely.
Overall, this paper’s main significance was in providing the first proof of a bee relying on a close association with a fungal ectosymbiont, and in this respect the authors did demonstrate that bee larvae require the fungus to develop. However, the results were preliminary, and I was dissatisfied that no experiments were performed to better confirm the mutualistic nature of this relationship. I would have liked to know how well the fungus grows outside of S. depilis hives and on media besides bee larva food, or if larval mortality without the fungus does result in decreased worker recruitment and lower colony fitness. I was also personally skeptical of the comparison of the bee-fungus mutualism with advanced agriculture in ants and termites, since the bees’ adaptations to inoculate the fungus, cultivate it, and utilize it in their diet were either not proven or not noticeably different from other stingless bees in general. I agree with the authors that the disappointing lack of obvious and elaborated anatomic and behavioral adaptations is more akin to other examples of proto-farming.
Of course, these problems can be addressed in the many interesting and potentially fruitful future directions that can be taken with this research. I’d especially like to know if the unknown Monascus in question is a distinct species exclusively associated with S. depilis bees, or a unique form of an unknown that grows facultatively lives alongside other bee species or in other environments. I’m also confident that we will uncover more examples of fungal ‘agriculture’ in the large genus Scaptotrigona, among the diverse meliponine bees, and in other social bee lineages in general. The lesson is that when we don’t know about species natural history in ‘well-studied’ groups, we are prone to overgeneralizations and overlooking major discoveries. In this respect, this paper deserves to generate more buzz among scientists.