Nature is full of impostors, and many of them are found in the insect world. Certain species, such as the bee fly or the ant spider, are experts at misdirection and their ability to confuse predators or prey is on a par with that of John Travolta in Face/Off and Arya Stark in Game of Thrones. However, never before has a blow fly been observed successfully living in cognito among termites.
Now, for the first time ever, an international study led by the Institute of Evolutionary Biology ( IBE ), a joint centre of the Consejo Superior de Investigaciones Científicas (CSIC) (the Spanish National Research Council (CSIC) ) and Pompeu Fabra University (UPF) , in conjunction with the Botanical Institute of Barcelona (IBB, CSIC-CMCNB), has discovered a species of blow fly (family Calliphoridae) whose larvae infiltrate colonies of harvester termites.
Published in Current Biology, the discovery was made in the Anti-Atlas mountain range in southern Morocco, and reveals unique morphological and chemical adaptations. The research sheds light on the evolution of flies and the adaptations of termite-related species.
"This is a chance finding. In our research group we mainly study butterflies and ants. As it had rained a lot and the butterflies were not flying, we looked for ants. When we lifted a stone we found a termite mound with three fly larvae that we had never seen before. The water had probably flooded the deeper layers of the nest and the larvae had emerged onto the surface", says Roger Vila, the IBE researcher who led the study. "It must be an extremely rare species, because we have made three more expeditions in that area and, despite lifting hundreds of stones, we found only two more flies, together, in another termite mound.
A "termite mask" on the tail aids infiltration
The team has described the morphological adaptations of this species of blow fly. In particular, the larvae of this calliphorid have developed a unique disguise to help them infiltrate termite mounds.
On the back of the body, the larvae display a "termite mask": a non-functional "head" with antennae and palps the same size as those of a large harvester termite. They also have two false eyes, which are actually the larvae's breathing holes.
"Most termites live several metres deep and have no visual perception. However, harvester termites come out at dusk to collect grass, so they have functional eyes that the larvae are able to mimic with their spiracles", says Vila.
In addition, the larvae have unusual "tentacles" around their bodies that mimic termite antennae in great detail, which the team was able to demonstrate using scanning electron microscopy. The numerous tentacles surrounding the body of the larvae facilitate simultaneous communication with several termites.
The larvae also mask themselves with the smell of their nest mates
Inside the nest, everything is dark, so the termites recognise each other using their antennae, with which they detect the shape and smell of their siblings. All the members of the nest share this scent, and the soldier termites attack and dismember any intruders from other colonies. These maggots, however, also manage to mimic the distinctive odour of their hosts.
"We quantified the chemical composition of these larvae and the result is surprising: they are indistinguishable from the termites in the colony where they live; they smell exactly the same. In addition, the larvae and termites in a particular colony have slight differences in their chemical profile that differentiate them from other termite mounds. This odour is key to interacting with the termites and benefiting from their communal life. It is a chemical disguise."
Termites tend and groom the intruding maggots
When the team found the larvae in Morocco, they were occupying the termite mound's food chambers. Once in the laboratory, they observed that the fly larvae tended to settle in the most populated areas of the nest, where they received constant attention from the termites, which preened them using their mouthparts.
Although the team was unable to reveal their diet, they were able to observe trophallaxis-like behaviour: the termites appeared to transmit food to the larvae using their mouths. "The larvae are not only tolerated, but they constantly communicate with the termites through contact with their antenna-like tentacles. The termites even seem to feed them, although this has not yet been unequivocally demonstrated", explains Vila.
The team stresses the difficulty of keeping these insects in the laboratory, as it involves maintaining colonies of desert termites, which live in very special conditions. "The larvae we studied eventually died without metamorphosing, so there may be elements of the nest and the symbiotic relationship between the termites and the flies that we were unable to transfer to the laboratory. Their diet is currently unknown, and their adult form remains a mystery", adds Vila.
The "termite mask" is an evolutionary leap for blow flies
The relationship between the blow fly larvae and termites appears to be a form of social parasitism or symbiosis. The most similar case is found in humpback flies. However, in humpback flies it is the adults, not the larvae, that mimic termites, representing a case of independent evolution of a relationship with termites, or termitophilia.
"The common ancestor of blow flies and humpback flies dates back more than 150 million years, much further than that which separates humans from mice. We are therefore confident that we have discovered a new case of social integration evolution", explains Vila.
The team used phylogenomic studies to prove that the fly they have discovered belongs to the genus Rhyncomya. Since none of the known species of this genus share the unusual lifestyle or the incredible morphology of the newly discovered fly, the study suggests that this new species must have evolved very quickly.
"This discovery invites us to reconsider the limits and potential of symbiotic relationships and social parasitism in nature. But, above all, we should realise how much we still do not know about the vast diversity and specialisation of insects, which are essential organisms in ecosystems", concludes Vila.
This international study is the result of a collaborative effort between the Institute of Evolutionary Biology (IBE) and the Botanical Institute of Barcelona (IBB, CSIC-CMCNB) in Barcelona, together with the University of Florence in Italy, the University of Minnesota and North Carolina State University in the United States, and the Natural History Museum Denmark.
Reference article: Schär S, Talavera G, Dapporto L, et al. Blow fly larvae socially integrate termite nests through morphological and chemical mimicry. Current Biology. 2024; https://doi.org/10.1016/j.cub.2025.01.007
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