Humans developed agriculture after the last ice age, which ended around twelve thousand years ago. Farming was only possible based on technological advances and organizational skills that could be passed down the generations, setting these Neolithic farmers apart from earlier humans. Against this short history of human farming it is a surprise that some ants and termites figured out how to farm fungi for food tens of millions of years ago. This innovation was so successful that insect farmers diversified into many species that dominate savannas and rain forests across the world to this day. A new study, published today in Nature Communications, reveals the genetic changes that enabled these farming ants and their cultivars to be so successful.
An international team of researchers, led by the Centre for Social Evolution in Copenhagen (CSE), China National GeneBank (CNGB) and BGI-Shenzhen analyzed the genome sequences of seven farming ant species and their fungus crops. These represent the entire scale-range of fungus-farming: Some species practice small-scale subsistence farming, with miniature farms the size of golf-balls hidden under the forest floor; others have moved on to industrial-scale farming in colonies with millions of workers – the leaf-cutter ant colonies whose highways bustle with thousands of workers carrying leaves, which can hardly fail to escape the attention of any tourist visiting Latin America. As CSE’s Dr Sanne Nygaard explains: “These ants have resolved many challenges that human agriculture continues to struggle with, such as superb hygiene, effective pest management and the production and application of fungicides and antibiotics that have not made their diseases resistant as time went by. They have done this not through science and technology, but by evolution by natural selection”.
The study shows that the building blocks of the fungus-farming ant genomes were shuffled around over evolutionary time at a rate higher than that of any animal groups for which genome sequences are currently available. This is reminiscent of many plants and animals domesticated by humans that have had elevated rates of evolutionary change because of selective breeding by farmers. Nygaard et al. also show that the origins of ant farming, and later transitions in crop domestication, are older than so far suspected: the ancestor of these ants started to farm fungi nearly 60 million years ago, shortly after the dinosaurs went extinct.
Crop changes also played a crucial role: the large-scale ant farmers have fungal crops that must always be asexually propagated, similar to most modern human crops. When this transition happened, the ants needed to feed their fungus gardens better quality compost, so they started harvesting fresh leaves. This in turn made their cultivars lose many of the cellulose- and lignin-degrading enzymes that are typically found in the less specialized ancestral crops of small subsistence farmers. Guojie Zhang, who is co-senior author and coordinated the genome analysis work, elaborates: “During mutual domestication, both the ants and their crop fungi underwent dramatic changes which precluded that they could ever return to independent life. Comparative genomics is a powerful tool to track these evolutionary processes.”
The most crucial adaptation in both the ants and cultivars, however, was evolving the ability to produce and process chitin – the main component of fungal cell walls – in large quantities. As Nygaard et al. show, the genomes of farming ants and their crops carry many signatures of past natural selection, accumulating novel genetic traits that likely facilitated the large-scale and massively successful ant fungus farms we see today.
The study’s senior author, Professor Jacobus (Koos) Boomsma, comments: “Ant fungus-farming is an intriguing example of stable mutualistic cooperation that realized huge potential by slow and gradual improvements – so much in fact that the leaf-cutting ants are now serious agricultural pests throughout Latin America because of their efficiency in defoliating human crops. Ant farming appears to be more sustainable than human farming in almost all respects that have been studied. The only human achievement that really stands out is that we created industrial-scale farming much faster, but our farming practices are rarely as thorough as those achieved by slow natural selection in farming insect societies”.