Anthropogenic seed dispersal: rethinking the origins of plant domestication


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The plants we consume for food have changed drastically in the 10,000 years since humans began practicing agriculture, but hominids have been intensively interacting with the plants and animals around them since before the dawn of our species. As humans became aware of the ability to modify crops through selective breeding, the evolution of new traits in plants greatly increased. However, plants have been evolving in response to human selective pressures since long before people began consciously altering them through breeding.

Anthropogenic seed dispersal: rethinking the origins of plant domestication
A photo of an ear from a wild barley plant, with the ripe seeds naturally shattering off due to the brittle rachis or stem
structure at their base. In the wild, this brittle rachis allows the plant to spread its seed up to two meters from the
parent plant, which is a rather weak dispersal mechanism and not characteristic of the other crop progenitor plants.
The barley that we eat today evolved tougher rachises as part of the mutualistic relationship they evolved
with humans. Humans have dispersed barley plants all over the world [Credit: Robert Spengler]

In a new study published in Trends in Plant Science, Dr. Robert Spengler examines these evolutionary responses and theorizes that all of the earliest traits to evolve in the wild relatives of modern domesticated crops are linked to human seed dispersal and the evolutionary need for a plant to spread its offspring.

Domestication syndrome and the emergence of similar traits

Many of the earliest traits of domestication in plants are similar across different crop species, a phenomenon evolutionary biologists refer to as parallel evolution. For example, in all large-seeded grass crops – e.g. wheat, barley, rice, oats – the first trait of domestication is a toughening of the rachis (the individual stem that holds a cereal grain to the ear). Likewise, in all large-seeded legumes, such as peas, lentils, fava beans, and kidney beans, the earliest trait of domestication is a non-shattering pod.

Anthropogenic seed dispersal: rethinking the origins of plant domestication
A wild barley grain with a zoomed in image of the base of the rachis. In this wild form, the rachis cleanly snaps
off of the ear of barley when it is ripe. In the domesticated form, the rachis has to be forcibly pulled off of
the ear causing a jagged break. Archaeobotanists look for specimens with the jagged break as the first
indication of plants evolving in response to human cultivation practices [Credit: Robert Spengler]

Archaeobotanists studying early plant domestication agree that the evolution of tougher rachises in cereal crops was a result of humans using sickles to harvest grains. During a harvest, the specimens with the most brittle rachises lost their seeds, whereas the plants with tougher rachises benefited from having their seeds protected and saved for the following year. Humans then cleared away competitive plants (weeding), tilled soil, sowed seeds, and maintained the crops until the next harvest. We can assume that the same process occurred for legumes.

For nearly a century, scholars have been aware of the fact that this parallel evolution was the result of similar selective pressures from people in different centers of domestication around the world, leading to what many researchers call “domestication syndrome.” In the simplest biological sense, Spengler suggests, humans provide better seed-dispersal services for food crops than those plants would have had in the wild, causing them to evolve traits that facilitated agriculture and improved their own chances of reproduction.

The evolution of seed-dispersal traits in crops

Archaeobotanists have studied seed-dispersal traits in the wild relatives of cereal and legume crops, but few have discussed how the wild relatives of other crops dispersed their seeds. In this manuscript, Spengler steps away from the heavy focus on these few plants and looks at the wild seed-dispersal processes in other crops.

Anthropogenic seed dispersal: rethinking the origins of plant domestication
The wild progenitors of domesticated legumes, such as this wild relative of grass peas (Lathyrus), explode and shoot
 out their seeds when they are ripe. The first steps towards domestication included a loss of this trait in favour
 of retaining seeds in their pods for humans to collect. Humans then became the obligate dispersers
for these domesticated legumes [Credit: Robert Spengler]

Spengler notes that before the last Ice Age, megafaunal mammals, including humans, were key for the evolution of larger fruits in the wild. While some plants have mechanical methods of seed dispersal, the most common way plants spread their seeds is by recruiting animals to do it for them. Bright red cherries, for example, have evolved to entice birds with red-green color vision. The birds consume the sugary fruit, then fly to a new area and deposit the seed from the cherry. Larger fruits, however, require larger animals to distribute them, meaning the progenitor plants for most of the fruits in our produce markets today evolved to be spread by large mammals. Paleontologists have previously noted the parallel evolution of larger fruits to entice larger animals in many unrelated plant families, a process that Spengler reveals to be mirrored in the evolution of crops cultivated by humans.

Spengler also theorizes that megafaunal mammals may have been key to the dispersal of seeds in the progenitors of small-seeded grains, such as quinoa, millets, and buckwheat. With smooth, hard-shelled seeds that grow at the top of the plant, no secondary defensive compounds or thorns, and a rapid rate of growth, the foliage of these plants are the perfect food for grazing animals. The small size of these wild seeds may have been an evolutionary adaptation that allowed them to pass successfully through the digestive systems of hooved mammals, which often only allow seeds smaller than 2mm to pass. Conceptualizing domestication as seed-dispersal based evolution, as Spengler proposes, explains why the first traits of domestication in all of the small-seeded annual crops were thinning of the seed coat, an increase in seed size, and breaking of dormancy – a reversal of the traits that allowed for seed dispersal by grazing mammals. The domestication process severed the mutualistic ties these plants had with their wild seed dispersers and made them dependent upon humans for dispersal.

Understanding plant domestication as seed-dispersal-based mutualism

During the Early and Mid-Holocene, plants in specific locations around the world started to evolve new traits in response to human cultivation practices. As human populations increased in size and became more concentrated, the selective pressures that people placed on these plants increased. In the wild, plants often evolve mutualistic relationships in response to heavy herbivory pressures. The same evolutionary responses, Spengler argues, can be seen in farmers’ fields during the early steps towards domestication, with plants developing traits to better use humans as seed dispersers.

Anthropogenic seed dispersal: rethinking the origins of plant domestication
A farmer in Uzbekistan burning the stubble in his field to reduce the weeds and insects before planting a new rotation
of crops. The seeds that farmers save to plant for the following year have a strong chance of survival, whereas
seeds that are dropped from the plant can be consumed by birds or insects, or killed by winter frosts.
Therefore, plants evolved ways to retain their seeds in order to have them collected by humans
rather than dispersed on the ground [Credit: Robert Spengler]

“Humans are the best seed dispersers that have ever existed, dispersing plant species all over the world,” Spengler says. “We are currently removing all competitive plant species across the Amazon to spread soybean seeds – a plant that originally evolved traits for a mutualistic relationship with humans in East Asia. Likewise, most of the prairies of the American Midwest have been removed in order to grow maize, a crop that evolved to recruit humans in tropical southern Mexico. Humans are powerful seed dispersers and plants will readily evolve new traits to spread their seeds and colonize new areas more successfully.”

Dr. Spengler is the director of the archaeobotanical laboratories at the Max Planck Institute for the Science of Human History in Jena, Germany. “It is important look at the domestication of plants from an evolutionary ecology perspective and seek to find parallels between the evolution of plants in the wild and during early cultivation,” says Spengler. “By modeling domestication as an equivalent process to evolution in the wild and setting aside the idea of conscious human innovation, we can more effectively study the questions of why and how this process occurred.”

Source: Max Planck Institute for the Science of Human History [February 27, 2020]



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