Potatoes may have shaped genetic makeup of Indigenous Andeans

BUFFALO, N.Y. — The Indigenous people of the Andes were the first to domesticate the potato, making the starch-rich crop a dietary staple for this high-altitude population long before it spread to the rest of the world.

Today, their descendants in Peru carry the highest known numbers of genes involved in starch digestion of any population in the world.

This is no accident, according to a new study co-led by the University at Buffalo and UCLA and published today (May 5) in Nature Communications. 

Evolutionary biologists and anthropologists found that natural selection favored Indigenous Andeans who had an unusually high number of salivary amylase genes (AMY1) starting around 6,000 to 10,000 years ago — the same period when potatoes were first grown in the Andean highlands, 

People with a high number of AMY1 copies tend to produce more of the amylase enzyme in their saliva, which begins breaking down starch in the mouth, and, thus, are thought to digest starch more effectively.

“Biologists have long suspected that different groups of humans have evolved genetic adaptations in response to their diets, but there are very few cases where the evidence is this strong,” says the study’s co-corresponding author, Omer Gokcumen, PhD, professor of biological sciences in the UB College of Arts and Sciences.

The study collected DNA from Peruvian Andean Quechua speakers — data that was then compared with genomic databases containing thousands of DNA samples from dozens of modern human populations. 

It could open the door to wider research into the lives of people who live at high altitudes — populations that deal with limited foodstuffs and extreme exposure to cold temperatures and ultraviolet rays.

“The high altitude Andes region is known for being a very rich geographic region for understanding human evolutionary adaptation to hypoxia, where tissues do not get enough oxygen,” says co-corresponding author Abigail Bigham, PhD, associate professor of anthropology at UCLA, who studies populations in the Peruvian Andes and the Himalayas of Nepal. “But I think this research highlights how the Andes are very useful for understanding human evolutionary adaptation to other environmental selective pressures like diet adaptation.”

The work builds on Gokcumen’s prior research showing that the initial duplication of AMY1 in humans occurred at least 800,000 years ago, as well as Bigham’s prior research showing evidence of selection in the starch digestion pathway among Peruvian Andeans that corresponds to the period of potato domestication.  

Ancestors of Indigenous Andeans likely already carried both the lower and higher copy numbers of AMY1 before they settled into the highlands and domesticated potatoes. However, when they did begin growing potatoes, those with higher copy numbers gained an evolutionary advantage. 

Starting after about 10,000 years ago, those with roughly 10 copies or more had a 1.24% survival or reproductive advantage per generation.

“Evolution is chiseling a sculpture, not constructing a building,” Gokcumen says. “It’s not as if Indigenous Andeans gained additional AMY1 copies once they started eating potatoes. Instead, those with lower copy numbers were eliminated from the population over time, perhaps because they had less number of offspring, and the ones with the higher copy numbers remained.” 

The result? Indigenous people living in Peru today carry an average of 10 AMY1 copies, approximately two to four more than any of 83 populations examined in the study.

On average, Indigenous people in Peru carry more copies (10 vs. six) than the Maya — an Indigenous population in Mexico with shared evolutionary history but without a tradition of potato farming.

“This direct comparison is one of the major reasons why we think their high number of AMY1 copies in the Peruvians did not evolve just by chance but instead linked to their long history of eating potatoes,” says Luane Landau, a PhD student in Gokcumen’s lab and the joint first author of the study.

However, they still had to account for the dramatic decline in the Indigenous population of the Americas following contact with Europeans in the 15th century, which resulted in disease, famine, violence, conflict and a rapid loss of genetic diversity in a short period of time.

Was it possible that this population bottleneck — rather than natural selection — could have disproportionately removed individuals with lower AMY1 copy numbers? Disentangling the two factors was a major challenge.

In the end, state-of-the-art ultra-long DNA sequencing technologies, along with newly available comparative datasets, allowed the researchers to demonstrate that high numbers of copies of the gene rose in frequency in the Andes several thousand years before Europeans appeared on the scene.

“We saw that the signal of natural selection was also much older, leading us to distinguish it from the population bottleneck,” says the study’s other first author, Kendra Scheer, a PhD student in Gokcumen’s lab. 

The ultra-long DNA sequencing technologies also provided unprecedented resolution that made it possible to investigate the mutational mechanisms responsible for exceptionally high AMY1 copy numbers.

Better understanding our genome could inform our dietary choices. In the future, people with fewer AMY1 copies could avoid eating too many potatoes or prepare them in a different way. 

“There could come a day when our diets are personalized according to our DNA,” Gokcumen says.

It also raises questions about how humans will evolve from modern diets.

“For most of human history, people ate the same thing their ancestors had eaten for thousands of years. You quite literally needed to migrate across the world to change your diet. So what does it mean now that we eat food from all over the world?” Scheer says. “And now that we’ve demonstrated the natural selection forces at play from eating potatoes, what does it mean now that the whole world eats french fries?”

While some think humans are adapted to the Paleolithic environment and not suited to eat foods that came post domestication, Bigham says their research shows that human populations have responded and evolved to changing food conditions within the last 10,000 years.

“Our metabolic pathways are not simply a product of that Paleolithic past,” she says. 

Other collaborators on the research include the University of Kansas, Penn State University, the University of Pennsylvania, the University of Puerto Rico at Cayey, Syracuse University, Cayetano Heredia University (Peru) and Bilkent University (Turkey).

The work was supported by the National Science Foundation, National Institutes of Health and the Leakey Foundation.