Humans and plants have a complex shared evolution. The most obvious example is our selection and expansion of specific plants during the agricultural revolution. What’s less obvious is the role that plants had in the selection of humans.
Farmers and gardeners have long known that some plants, such as basil and tomato, pair well together because of how they keep predators such as worms and beetles away from each other, and help each other grow1,2. Such productive interrelationships result from chemical feedback between species, termed allelopathy, and are often the sum of millions of years of co-evolution. More specifically, allelochemical interactions refer to the phenomenon where plants secrete secondary metabolites that affect the growth and development of other plants, insects, and mammals around them3.
Allelochemicals can be classified into three types, based on how they allow the host plant to interact with its environment. Synomones result in mutualistic symbiotic relationships between the host plant and recipient, such that both species benefit from the relationship4. At the other end of the allelochemical spectrum are kairomones, which harm the host species and benefit others. An example would be allelochemicals released by spruce trees that attract bark beetles, which are then eaten by checkered beetles that are also attracted to the spruce trees’ allelochemicals. Both beetles have developed specific sensory neurons that detect and draw them toward such secondary metabolites, but for different purposes4. The third type of allelochemical, allomones, are often cited as a defense mechanism because they deter predators, usually without harming them, as with pine trees that repel the same bark beetles that are attracted to other conifers5. These three types of allelochemical relationships have allowed plants and animals to co-exist and co-evolve over millennia, each relying on the other for survival, growth, and development.
It is important to note that allelochemical interactions are rarely single events; rather in fully developed ecosystems, such as forest environments, the relationships can become quite complex. There can be third-party interactions where plants outside a food chain can affect plants and predators in other food chains with seemingly no gain whatsoever4. This complexity is heightened by the variety of secondary metabolites that play a role in allelopathy. Some of the most important of these secondary metabolites are the terpenes, which are common allelochemicals produced by all plants. These terpenes are powerful on a global scale. As an example, terpene aerosols above forests seed clouds, suggesting that forests can influence their own rainfall6. Terpenes also affect nearby plants by influencing their allelochemical production and toxicity, and affecting their growth by mediating factors such as soil moisture, mycorrhizal function, and insect and bacterial growth3,7,8.
As with other allelochemicals, terpenes not only affect plants but animals as well. Terpenes control insects and harmful invasive species through allelochemical relationships9–11. For example, phytophagous insects, or those that feed on green plants, maximize their fitness by using their highly developed sensory systems to identify terpenes emitted by suitable plants10. In turn, such plants have developed a fine-tuned mechanism to release molecules to deter these insects10. Plants have similar relationships with mammals. Many plants are selectively browsed by mammals based on the terpenes and other secondary metabolites produced by the plant12,13. As such, these mammals have co-evolved with and are reliant on allelochemicals.
Perhaps the most striking example of co-evolution is that of plants and humans. For millions of years, humans foraged and put selective pressure on certain plants, resulting in cultivated plant communities. However, it would be deceptive to say that specific plants were passively chosen based on artificial selection pressures; rather, entire plant communities have co-evolved and adapted to the human environment14. A common example of such a relationship can be seen with the introduction of tubers in the human diet and the number of amylase gene copies in the human genome. About ten thousand years ago, humans learned how to cook their food. Tubers such as yams and potatoes were now appealing in taste and texture, though they had been bitter and inedible when raw. To digest the starch, humans needed more amylase, a protein responsible for starch hydrolysis. At the time, the human genome contained only one or two copies of the amylase gene15. To match with the increase in starch intake, humans with more copies of the amylase gene were positive selected, leading to an overall increase in the number of genes in the population15. Today, there are six amylose genes in the average human genome, as compared to one or two in the human genome ten thousand years ago15. These starchy foods came with substantial increase in calories, and more importantly, glucose, which is the brain’s primary source of energy. This increase in glucose availability allowed for increases in brain size and rapid cognitive evolution. In turn, it provided a selection advantage for tubers, which were now cultivated by the humans. It has been hypothesized that this increase in starch consumption is what ultimately led to the evolutionary split between Neanderthals and humans, marking the evolution of a higher-order species.
There are also more subtle effects that humans and plants have on each other. A striking example is the relationship of fava bean consumption and glucose-6-phosphate-dehydrogenase (G6PD) deficiency16–19. People living in the Mediterranean consume a large amount of fava beans, which are an excellent source of protein. Fava beans are also known to have strong oxidative qualities, and as a result, those who have a G6PD deficiency and consume fava beans can develop a type of anemia commonly known as favism16. This disease can be lethal but the polymorphism that results in the deficiency has persisted for many generations16. This may seem counterintuitive, but the same oxidative mechanism that causes favism also allows individuals who have the G6PD deficiency to fight malarial infections16. As a result, people who consume fava beans have evolved to withstand malaria.
Another example of co-evolution stems from mammals’ use of plants with psychoactive properties. Mammals from chimpanzees21 to humans22 have sought plants with allelochemicals that produce psychoactive effects. This dual-natured relationship is based on the similarity between the allelochemicals and endogenous neurotransmitters in the brain, and serves as evidence of the co-evolution of psychotropic plants and mammals22,23. In this way, plants have “cultivated” mammals by producing allelochemicals that replicate the effects of neurotransmitters in the brain. In turn, as humans developed a liking for such plants, they began cultivating them, increasing their evolutionary success. Perhaps the most commonly cultivated of these psychoactive plants is tobacco which contains nicotine that acts on the acetylcholine and nicotinic receptors in the brain23. Another example is the cacao plant whose caffeine and theobromine molecules act on the adenosine receptor amongst others23. Mammals also consume psychoactive plants that affect streams of consciousness, as evidenced from multiple species of mammals on the African plains that consume fermented fruit or jaguars that consume yage. A less obvious example is that opium, whose constituents act on opioid receptors, producing psychedelic effects in addition to its more obvious analgesic properties22. By ingesting these plants, mammals altered their neural functioning, and changed their cognition. For humans, these changes in cognition may have resulted in the burst of creative art and invention that coincided with the appearance and subsequent use of psychedelic plants24, a remarkable coincidence to say the least. Some researchers have hypothesized that plant secondary metabolites allowed, or perhaps caused modern civilization24,25.
Another example of how plants affect human physiology and consciousness can be seen in the practice of forest therapy. Also known as ‘forest bathing,’ forest therapy is based on the Japanese practice of Shinrin-yoku which means “taking in the forest atmosphere through all of our senses,26” , referring to the act of using a forest environment to improve one’s mind and body27. Large studies in humans show that walking in a forest environment reduces anxiety, lowers blood pressure, decreases heart rate, and promotes overall cardiovascular relaxation27–29. One possible explanation for the positive health effects of forest therapy experiments lies in the physical activity of walking itself. However, subsequent studies showed that people performing the same physical activities had significant improvements in stress parameters in urban forests when compared to urban participants in adjacent non-forested areas29. In addition, laboratory studies revealed that inhalation of forest terpenes lowered stress in rats30. Participants in forest therapy groups also showed significant increases in immunity, including heightened natural killer (NK) cell activity, and decreased depression and pain after two days of a forest therapy program27,31,32. Though the forest therapy effects on immunity are likely multifactorial, other research has linked specific terpenes from the forest to NK cell activity in a laboratory setting27,33.
Terpenes are one of the most prevalent and important allelochemicals found in forests, and have been associated with the restorative effects of forest therapy. However, in our modern urban world, access to forests is not always possible. A surrogate for forest terpene exposure may exist in the form of essentials oils, which have been shown to deliver many of the benefits of forest therapy27,34,35. Essential oils are concentrated, volatile, aromatic liquids that are extracted from plants and are rich in terpenes, among other compounds. Inhalation of essential oils of certain trees such as cypress33 and perilla36 has been shown to have strong olfactory stimulation and physiological effects similar to forest therapy,27 suggesting that humans can receive some of the positive effects of forest therapy by breathing in terpenes from essential oils of plants commonly found in forests.
As humans have evolved, we have driven the evolution of plants by carefully selecting and cultivating them for their medicinal, dietary, and health properties. Likewise, plants have driven human adaptations such as our ability to metabolize certain compounds. However, in mankind’s increasingly urbanized and digital society, modern humans have been disconnected from the forests in which our species evolved, resulting in what experts have coined “technostress”27. As more humans move away from rural areas and our innate relationships with plants, further escalations in levels of stress and anxiety may ensue. Is it possible that humans may ameliorate the physiological and psychological problems caused by technostress through olfactory immersion in natural environments via essential oils? Through inhalation of specific combinations of terpenes humans can reap the restorative benefits of forest therapy anywhere and harness the physiological interrelationship with plants that has been so central to our evolution and success as a species.
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