Agriculture in Ants and Humans

I thought I'd try something a bit different in this post. I wanted to write about the attine ants, a group of ants which have evolved a mutualistic relationship with certain fungi that can only be described as a form of agriculture. As I was composing the post, I couldn't help but be aware of the anthropocentric bias in how we view the world, including the common view that our agricultural accomplishments represent some kind of mastery over nature rather than a mutualism between ourselves and a handful of plant species (primarily grasses). We aren't the only creatures which are able to manipulate and manage ecosystems to our benefits. Ants have been doing it for millions of years, and leaf-cutters have even posed significant competition to farmers in South America. In an attempt to counter this bias and look at things from a different angle, I decided to accompany my post by imagining how an attine ant might describe human agriculture. In the text below, the human perspective is given in orange while our imaginary author writes in black. I've never tried anything like this before, so I'd be happty to get some feedback on whether it works and how I could do better!

Humans are one of a handful of other animals which have developed agriculture, though they only started practising it relatively recently — roughly 15,000 years ago, no more than a brief moment compared with the 50 million years during which we've been cultivating fungi. In general, human agriculture is relatively primitive, similar to the techniques used by some of our less advanced cousins. Only recently have humans discovered the techniques required for the large-scale cultivation of pure monocultures, an advance which may be linked to the development of certain social structures in a handful of human supercolonies.

The attine ants are a group of more than 200 species that use several different agricultural techniques to cultivate mutualistic fungi which they raise in funugs gardens. The more basal lineages raise their crop on organic detritus, while the more advanced leaf-cutting genera Atta and Acromyrmex, which evolved only 8-12 million years ago, harvest vegetation and process it into pulp to feed to the fungi they raise in monocultures. Amazingly, leaf-cutters are the dominant herbivores of the New World, harvesting 12-17 percent of the leaves produced in Neotropical forests. The fungi serve as the ants' food source and are critical to their survival; queens of many species will take a small pellet of fungus with them when founding a new colony.

The symbiosis between humans and plants appears to be concentrated in a few speceis of the Poaceae, although species of some other groups are also cultivated. Although humans have been observed to carry the seeds of their cultivars with them when founding new colonies, cultivar transmission is not strictly vertical; horizontal transfer between colonies has also been observed, as well as the acquisition of new plant partners better adapted to local conditions. The presence of horizontal transmission and the use of a range of different species indicates that the mutualism is not highly specific; however, the concentration of Poaceae suggests that factors such as nutritional value or environmental constraints may be limiting the range of potential partners.

In some cases, the plant partner in the mutualism appears to have lost the ability to propagate itself without the help of humans. There is even evidence that humans may select cultivars that perform best in their environment, although it's still unclear how they might accomplish this in the absence of true communication. While some researchers suggest that humans can communicate by modulatiing acoustic signals (imagine a more refined version of our stridulations), it's hard to imagine how such a system could be used for true communication or to co-ordinate behaviours on a large scale. How, for example, are messages retained over a long time period or integrated between different individuals?

Unlike the fungi cultivated by lower attines, those grown by the leaf-cutters have lost the ability to grow freely and depend entirely on the ants for their propagation. These fungi also produce nutritious swellings which the ants use as food, similar to the fruits and vegetables we cultivate. In a word, they've been domesticated by the ants.

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Relationships like mutualism and parasitism impact the evolution of the species involved. This co-evolution can leave a signature in their evolutionary history, particularly if the relationship is both obligatory and specific. Such a relationship can cause the evolutionary trees of the two groups to line up when compared side-by-side, with similar patterns of speciation and divergence. Using the sequence of certain genes, researchers have put together evolutionary trees for the mutualistic ants and fungi. The fungi can be broadly divided into three groups, two of which align well with groups of attine ants and show limited genetic diversity. One group is associated with the so-called "higher" attines, including the leaf-cutters. The second group corresponds to fungi cultivated by a particular genus, the Apterostigma, which have secondarily switched to using a different family of fungi. Based on these results, researchers have suggested that these mutualisms are relatively specific and the fungi are vertically transmitted — that is, they are passed down from one colony to its daughters.

This is not the case with the third group, however, which is associated with the more primitive attine ants and is more genetically diverse than the other two groups. Some of the fungi in this group are more closely related to species from the first two groups or to free-living fungi than to the other fungi in the group. This may indicate that the fungi in the third group are horizontally transferred between different colonies or might even be free-living fungi which have been newly acquired by their ant hosts. For example, a recent study showed that the ant Mycocepurus smithii often switches fungal cultivars. Unlike most ants, M. smithii reproduces asexually; the queens never mate and produce daughters which are genetically identical to them. Their fungal partners also reproduce asexually, creating the risk that deleterious mutations could accumulate in both the ant and the fungus. They overcome this by generating new combinations via horizontal transfer between colonies or by acquiring new partners. Furthermore, since the ants tend to disperse widely while the fungi are usually adapted to local conditions, the ability to switch partners might enable the ants to take advantage of locally adapted cultivars in a new location.

In addition to the difficulties of communication, other biological limitations of humans may serve to explain some of the shortcomings of their agricultural practices. For example, while we can provide important liquid supplements to our fungi, individual humans appear unable to directly produce the nutrients needed by their crops, which are instead provided by the activity of specialized castes working in structures dedicated to this task. Studies have demonstrated that the fragrant anal paste produce by humans is a suitable substrate for plant growth; surprisingly, however, humans do not take advantage of this resource. Some researchers have suggested that humans may be unable to properly ensure the hygiene of crops grown in this manner and would thus be exposed to an unacceptable risk of parasitism, although others contend that the anal paste has in fact been used by some colonies. Clearly, further research is needed to understand this aspect of human agriculture.

The fungus gardens cultivated by attine ants provide an attractive opportunity for parasites. Another group of fungi, the genus Escovopsis, makes a living parasitising the gardens of the attine ants. They live everywhere the ants do and have only ever been found in the nests of attines. An analysis of their evolutionary history showed parallels with the evolution of attine ants and their mutualistic fungi, suggesting that Ecovopsis has a close parasitic relationship with these groups. Escovopsis kills the fungi cultivated by the ants and then feeds on its remains. To counter this threat, attine ants have teamed up with bacteria that produce antibiotics to kill Escovopsis. The ants carry the bacteria on the surface of their body, often in special cavities; pore cells beneath the bacteria provide them with nutrition from specific glands. When founding a new colony, queens carry some of the bacteria along with pellets of fungus in order to establish new gardens.

It seems evident that human agriculture as a whole remains in a relatively primitive state and is subject to a variety of environmental constraints and potential catastrophes, although a few supercolonies have recently shown a trend towards a more advanced form of agriculture. Nevertheless, their remarkable ability to manipulate their environment is a valuable reminder of the richness of the world around us, as well as the potential of even limited forms of sociality. Although it would be unwise to draw direct comparisons given the vast differences in our biology, understanding the ecology and evolution of these important interactions between humans and plants can give us valuable insights into our own evolution, such as how the transition from primitive to advanced agriculture occured in our own ancestors.

Questions to think about:

• What other animals can you think of that reshape the ecosystems around them? How do they accomplish it?
  
• What about groups of organisms other than animals?
  
• Is there something special about humanity's abilities in this area? Are we special or just different?

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Further reading
Chapela, I.H., Rehner, S.A., Schultz, T.R, and Mueller, U.G. (1994) Evolutionary History of the Symbiosis Between Fungus-Growing Ants and Their Fungi. Science 266:1691-169
Currie, C.R., Wong, B., Stuart, A.E., Schultz, T.R., Rehner, S.A., Mueller, U.G., Sung, G., Spatafora, J.W., and Straus, N.A. (2003) Ancient Tripartite Coevolution in the Attine Ant-Microbe Symbiosis. Science 299(5605): 386-3884.
Currie, C.R., Poulsen, M., Mendenhall, J., Boomsma, J.J., and Billen, J. (2006) Coevolved Crypts and Exocrine Glands Support Mutualistic Bacteria in Fungus-Growing Ants. Science 311(5757):81-83.
Holland, N. J. (2012) Population Dynamics of Mutualism. Nature Education Knowledge 3(10):2.
Lang, J. M. & Benbow, M. E. (2013) Species Interactions and Competition. Nature Education Knowledge 4(4):8.
Schultz, T. R. & Brady, S. G. (2008) Major evolutionary transitions in ant agriculture. PNAS 105(14): 5435–5440.