Behavioral adaptation precedes morphological change in human evolution

As early humans spread from lush African forests into grasslands, their need for ready sources of energy led them to develop a taste for grassy plants, especially grains and the starchy plant tissue hidden underground.

But a new Dartmouth-led study shows that hominins began feasting on these carbohydrate-rich foods before they had the ideal teeth to do so. The study provides the first evidence from the human fossil record of behavioral drive, wherein behaviors beneficial for survival emerge before the physical adaptations that make it easier, the researchers report in Science.

The study authors analyzed fossilized hominin teeth for carbon and oxygen isotopes left behind from eating plants known as graminoids, which includes grasses and sedges. They found that ancient humans gravitated toward consuming these plants far earlier than their teeth evolved to chew them efficiently. It was not until 700,000 years later that evolution finally caught up in the form of longer molars like those that let modern humans easily chew tough plant fibers.

The findings suggest that the success of early humans stemmed from their ability to adapt to new environments despite their physical limitations, says Luke Fannin, a postdoctoral researcher at Dartmouth and lead author of the study.

We can definitively say that hominins were quite flexible when it came to behavior and this was their advantage. As anthropologists, we talk about behavioral and morphological change as evolving in lockstep. But we found that behavior could be a force of evolution in its own right, with major repercussions for the morphological and dietary trajectory of hominins."

Luke Fannin, postdoctoral researcher at Dartmouth

Nathaniel Dominy, the Charles Hansen Professor of Anthropology at Dartmouth and senior author of the study, says isotope analysis overcomes the enduring challenge of identifying the factors that caused the emergence of new behaviors-behavior doesn't fossilize.

"Anthropologists often assume behaviors on the basis of morphological traits, but these traits can take a long time-a half-million years or more––to appear in the fossil record," Dominy says.

"But these chemical signatures are an unmistakable remnant of grass-eating that is independent of morphology," he says. "They show a significant lag between this novel feeding behavior and the need for longer molar teeth to meet the physical challenge of chewing and digesting tough plant tissues."

The team analyzed the teeth of various hominin species, beginning with the distant human relative Australopithecus afarensis, to track how the consumption of different parts of graminoids progressed over millennia. For comparison, they also analyzed the fossilized teeth of two extinct primate species that lived around the same time-giant terrestrial baboon-like monkeys called theropiths and small leaf-eating monkeys called colobines.

All three species veered away from fruits, flowers, and insects toward grasses and sedges between 3.4 million to 4.8 million years ago, the researchers report. This was despite lacking the teeth and digestive systems optimal for eating these tougher plants.

Hominins and the two primates exhibited similar plant diets until 2.3 million years ago when carbon and oxygen isotopes in hominin teeth changed abruptly, the study found. This plummet in both isotope ratios suggests that the human ancestor at the time, Homo rudolfensis, cut back on grasses and consumed more oxygen-depleted water.

The researchers lay out three possible explanations for this spike, including that these hominins drank far more water than other primates and savanna animals, or that they suddenly adopted a hippopotamus-like lifestyle of being submerged in water all day and eating at night.

The explanation most consistent with what's known about early-human behavior, they report, is that later hominins gained regular access to underground plant organs known as tubers, bulbs, and corms. Oxygen-depleted water also is found in these bulging appendages that many graminoids use for storing large amounts of carbohydrates safely away from plant-eating animals.

The transition from grasses to these high-energy plant tissues would make sense for a species growing in population and physical size, Fannin says. These underground caches were plentiful, less risky than hunting, and provided more nutrients for early humans' expanding brains. Having already adopted stone tools, ancient humans could dig up tubers, bulbs, and corms while facing little competition from other animals.

"We propose that this shift to underground foods was a signal moment in our evolution," Fannin says. "It created a glut of carbs that were perennial-our ancestors could access them at any time of year to feed themselves and other people."

Measurements of hominin teeth showed that while they became consistently smaller-shrinking about 5% every 1,000 years-molars grew longer, the researchers report. Hominins' dietary shift toward graminoids outpaced that physical change for most of their history.

But the study found that the ratio flipped about 2 million years ago with Homo habilis and Homo ergaster, whose teeth exhibited a spurt of change in shape and size more suited to eating cooked tissues, such as roasted tubers.

Graminoids are ubiquitous across many ecosystems. Wherever they were, hominins would have been able to maximize the nutrients derived from these plants as their teeth became more efficient at breaking them down, Dominy says.

"One of the burning questions in anthropology is what did hominins do differently that other primates didn't do? This work shows that the ability to exploit grass tissues may be our secret sauce," Dominy says.

"Even now, our global economy turns on a few species of grass––rice, wheat, corn, and barley," he says. "Our ancestors did something completely unexpected that changed the game for the history of species on Earth."