Vanishing act: the disappearance of ancient nutritional symbioses in ants

Figure 1: An Ant Feeds from an Extrafloral Nectary

If you’ve ever been to a magic show, you may have seen a trick where the magician makes an object miraculously disappear. The mystery draws you in, where could it have gone? However, these sorts of mysteries are not confined only to the realm of stage magic, but can also occur in nature. Our new articledescribes a mysterious vanishing act of an ancient mutualism, created not by magicians but by ants.  

Ants are one of the most successful and widespread insects on the planet. They flourish on every continent except Antarctica. This might lead us to wonder why ants are so widespread when other insects are restricted to certain regions or climates. It is believed that at least part of this success can be explained by the partnerships they form with symbiotic microbes. For example, certain groups of ants have formed symbiotic relationships with bacteria that provide them with nitrogen-based nutrients, such as amino acids, that keep their colonies healthy when proteins are scarce2,3. By relaxing their need for protein, these symbiotic ant lineages have been able to colonize protein-limited ecological niches, such as forest canopies where they feed predominantly on plant-based food sources (Fig 1)4,5. This has allowed these ants to rise to become some of the most abundant and diverse animal groups in tropical rainforests.

Figure 2. Top: An illustration of the ant gut alongside a florescent in-situ hybridisation image of a dissected ant midgut. Host DNA is in fluorescent blue while the bacteriocyte-associated symbiont is in fluorescent red. 
Bottom: Pictures of ants from the four ant genera of interest. (From left: Camponotus, Formica, Cardiocondyla, Plagiolepis)
All images except the illustration also appear in our publication "Convergent evolution of a labile nutritional symbiosis in ants".

While ant symbioses are diverse in their manifestation, we chose to focus on one particularly intimate type, called a bacteriocyte-associated symbiosis. In these cases, the host has evolved a specialized organ called the bacteriome that is made up of large cells called bacteriocytes that house the symbiont (Fig 2). These symbioses are characteristic of the ancient nutritional mutualisms found in sap and blood-feeding insects, where the host is completely reliant on the bacteria to provision nutrients missing in their diets6. It is less clear, however, why predominantly omnivorous insects such as ants would evolve these symbioses.

To better understand the critical role of symbionts in ants, we compared the bacteriocyte-associated symbionts that had independently evolved in four ant lineages (Fig 2B). Studying the symbiont genomes revealed the only function that they have retained is the capacity to synthesize the amino acid tyrosine, which is an important component of insect cuticles. This suggests that ants have convergently formed partnerships with microbes to provision tyrosine to help thicken their cuticle when proteins are scarce. However, it also uncovered a fascinating mystery.

As part of our project, we screened hundreds of ants from the genera Formica and Cardiocondyla for their bacteriocyte-associated symbionts. What we discovered is that not all the queens carried the symbiont, and appeared perfectly healthy! In many types of symbiotic relationships this would not be an unexpected finding as facultative symbionts can come and go in host populations. However, this was a completely unprecedented for a bacteriocyte-associated symbiosis, which are normally always present in reproductive individuals. Our research indicated these symbionts have been associated with their ant hosts for tens of millions of years and have been strictly transmitted to offspring through host generations. Herein lies the vanishing act of ants. How can a symbiont, whose sole means of transmission is from mother to offspring, disappear from the matriline and yet still be maintained for millions of years?

It will probably take some time to fully understand how ants manage this trick, but we have a theory as to what could be happening. We hypothesize that the symbiosis may be held in a cost-benefit balance where the symbionts is retained in the long term for its nutritive benefits, but occasionally lost in the short term due to the cost of maintaining the relationship. In this scenario, the symbiont would be lost when key nutrients such as tyrosine are plentiful. This in combination with diet flexibility from an omnivorous lifestyle may make it so that ant colonies can persist with uninfected queens in some contexts. However, asymbiotic individuals would eventually be purged from the population when these nutrients are scarce resulting in the long-term maintenance of the symbiosis.

Whatever the answer to this mystery, our project has helped us understand how ants use microbes to solve common dietary problems. But it has also shown us that these mutualisms that were once thought to be essential and inseparable from their hosts in can breakdown, as is the case of the vanishing symbionts of ants.

  

References

  1. Jackson, R. et al. Convergent evolution of a labile nutritional symbiosis in ants. ISME J (2022).
  2. Feldhaar, H. et al. Nutritional upgrading for omnivorous carpenter ants by the endosymbiont Blochmannia. BMC Biol. 5, 48 (2007).
  3. Hu, Y. et al. Herbivorous turtle ants obtain essential nutrients from a conserved nitrogen-recycling gut microbiome. Nat. Commun. 9, 964 (2018).
  4. Davidson, D. W., Cook, S. C., Snelling, R. R. & Chua, T. H. Explaining the abundance of ants in lowland tropical rainforest canopies. Science (80-. ). 300, 969–972 (2003).
  5. Russell, J. A. et al. Bacterial gut symbionts are tightly linked with the evolution of herbivory in ants. Proc. Natl. Acad. Sci. U. S. A. 106, 21236–21241 (2009).
  6. Moran, N. A., McCutcheon, J. P. & Nakabachi, A. Genomics and Evolution of Heritable Bacterial Symbionts. Annu. Rev. Genet. 42, 165–190 (2008).