Extant species of Atta leaf-cutting ants may have benefited from expansion of the Cerrado

These ants emerged some 8.5 million years ago and underwent an intense speciation process between 1 million and 3 million years ago, when the Brazilian savanna was expanding. The recent advance of agriculture in the region, however, appears to be reducing this biodiversity and selecting species that damage crops.

By André Julião  |  Agência FAPESP – A study conducted by researchers working in Brazil, Argentina and the United States suggests that the Cerrado, Brazil’s Neotropical savanna biome, may have been a center for the emergence of new species of Atta leaf-cutting ants in the last million years. However, the recent expansion of agriculture in the region appears to be having a negative effect on species diversity among Atta there and to be favoring species considered agricultural pests.

The results of the study, reported in an article published in Systematic Entomology, suggested that the common ancestor of all extant Atta species first emerged some 8.5 million years ago somewhere in Mesoamerica, the historical region comprising present-day southern Mexico, Central America and northwestern Colombia. They then spread through South America, mainly from the Cerrado outward. An explosion of new species appears to have occurred between 1 million and 3 million years ago, precisely when the Cerrado was expanding.

“The expansion of the Cerrado appears to have favored these ant species by providing more food diversity and more open environments, to which they adapted very well. They became specialists in these different habitats and differentiated into new species,” said Corina Barrera, first author of the article. The study was conducted while she was a PhD candidate at São Paulo State University’s Institute of Biosciences (IB-UNESP) in Rio Claro.

“If the Cerrado disappears, they may shrink again in terms of biodiversity, as has happened in the past to other species. That may already be happening to them because of the introduction of extensive agriculture in the region. We haven’t measured the magnitude of this phenomenon yet. We know a major Atta population explosion is under way, but with low biological diversity, due to the expansion of agriculture. The few species that benefit from crops like soybeans and sugarcane, for example, become pests. Forest-dwelling species, which don’t adapt to crops, could undergo mass extinction,” said Maurício Bacci Júnior, a professor at IB-UNESP and last author of the article.

The study was part of two projects (19/24470-2 and 19/03746-0 supported by FAPESP and led by Bacci. The latter is funded in partnership by the US National Science Foundation (NSF) and the FAPESP Research Program on Biodiversity Characterization, Conservation, Restoration and Sustainable Use (BIOTA-FAPESP).

The researchers first collected samples from 865 colonies in 19 countries, and in 25 Brazilian states. They then selected 224 specimens for DNA extraction and sequencing of 2,340 ultra-conserved elements (UCEs), which are DNA regions identical in at least two species. Scientists can determine evolutionary relations with significant precision by comparing UCEs.

Farmer ants

To humans, leaf-cutting ants are agricultural pests, but these insects have practiced agriculture since before Homo sapiens appeared on the planet.

Most ant species are omnivorous hunter-gatherers, preying on a multitude of organisms. Leaf-cutters, however, are part of a subtribe called Attina that began producing its own food between 50 million and 60 million years ago.

“Agriculture was invented by ants and by some groups of termites and beetles,” said Bacci, who is affiliated with IB-UNESP’s Center for Studies of Social Insects (CEIS). “They began by feeding on fungi and evolved into fungus farmers. They grow fungi in their nests on some kind of substrate. In the case of leaf-cutting ants, the substrate is made up of leaves and other plant remains. They have a source of food that’s available in all seasons of the year, and this gives them a degree of food security.”

Ants have practiced agriculture for such a long time that they have learned to produce their own pesticides. In the case of an even older group than leaf-cutters, for example, this takes the form of a mutualism with bacteria, which protect the fungi they eat against pathogens.

However, while these more ancient ants use fallen flowers and leaves as a substrate on which to grow fungi, leaf-cutters such as Atta, Acromyrmex and Amoimyrmex actually cut leaves off plants and take them back to their nests, thereby potentially damaging crops and being considered pests.

The very earliest leaf-cutting ant species emerged some 19 million years ago. The most recent genera, Atta and Acromyrmex, differentiated about 16.5 million years ago. Leaf-cutters are the newest fungus-growing species of ants. Some emerged only 1 million to 300,000 years ago. An example of the latter is Atta robusta (common name saúva-preta).

This relative newcomer is already threatened with extinction. Restricted to coastal areas of Rio de Janeiro and Espírito Santo states, A. robusta is classified as “vulnerable” by federal environmental agency ICMBio in its Red Book of Endangered Brazilian Fauna. A possible explanation for this vulnerability is an inability to adapt to other habitats.

Other species successfully expand their habitats as human activity spreads. An example is A. sexdens, or saúva-limão. The “lemon” in its common name comes from the odor it releases when crushed, but it is a notorious agricultural pest and can destroy an entire crop overnight.

“Any plant not native to South America, as are the main crops grown in Brazil, will always be a magnet for leaf-cutting ants,” Bacci said.

He is currently mapping the genes present in leaf-cutters in search of traits (genetic signatures) that may explain their success or proximity to extinction. Besides contributing to a deeper understanding of natural selection in the group, this genetic analysis could serve as a basis for the development of more targeted formicides capable of attacking only genes of species that harm crops and are expanding, while sparing those of inoffensive ants, as well as fish, birds and mammals.

The article “Phylogenomic reconstruction reveals new insights into the evolution and biogeography of Atta leaf-cutting ants (Hymenoptera: Formicidae)” is at: onlinelibrary.wiley.com/doi/10.1111/syen.12513.