Plant chemicals in the evolution of mammals and humans

Modern Ayurveda

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The relation between primates and fleshy fruits was established in the early-mid Eocene (55 to 48 million years bp) when the tropical forests reached their maximum latitudinal extent (Collinson and Hooker, 1991). Plants have formed a significant part of the diet throughout human evolution and there can be no doubt that a wide range of plant chemicals was thereby ingested. Although there is evidence to suggest that the evolution of plant secondary compounds was closely influenced by their interaction with insect pollinators, there is no evidence that mammals have had any impact on the distribution of these compounds but have adapted to them (Lindroth, 1988). The whole of hominid evolution may have taken place against a backdrop of plant secondary compounds similar to those existing today. Recently a chemical from an Australian legume of interest in AIDS (acquired immune deficiency syndrome) research was found in morphologically similar species from S. America. The common ancestor of both groups was believed to have spanned the land bridge which linked present day Australasia and S. America during the break-up of the Gondwanaland land mass 100 to 50 million years bp (Fellows et al., 1992) providing some support for the view that the current range of plant secondary compounds was established early and was not greatly influenced by mammalian herbivory.

The lines leading to modern humans and the chimpanzees, our nearest primate relatives, diverged 6-10 million years bp, but fully modern humans did not emerge until c. 100000 years ago (Diamond, 1989). Modern chimpanzees eat a wide range of plant material with the occasional intake of meat. The diet of emerging humans almost certainly included a high proportion of meat (Blumenschine, 1991), but until the start of farming c. 10 000 years ago also a wide range of plant species. With farming came an increase in the proportion of plant material in the diet relative to meat, but a reduction in the range of plant species, and therefore in the range of plant chemicals, consumed (Schoeninger, 1982). Excavations at a site in Syria dated to the time of the conversion to agriculture revealed a reduction from about 200 to 20 in the range of species eaten (Hillman et al., 1989). These changes were associated with increased levels of malnutrition and disease (Garn and Leonard, 1989; Ulijasek, 1991). The practice of herbal medicine may have been an attempt to replace plant chemicals which had been lost from the diet, but whose ingestion had long-term and subtle benefits for human physiology. It is interesting that in the ancient Indian tradition of ayurvedic medicine cookery and pharmacology are not considered as separate. The use of herbs in the modern practice of this system is seen as a way of replacing those factors which, in the past, would have been normal constituents of the diet (Ballentine, 1978).

Despite a demonstrable defensive role of many plant secondary compounds, the existence of plant-eating animals is proof that those defences are seldom absolute. Lindroth (1988) suggests that one consequence of the evolution of chemical defences in plants has been to enforce the generalist feeding pattern of most mammalian herbivores. Further factors which ensure that the generalist approach to feeding is, for most herbivores, the optimal strategy include availability of food, which is frequently seasonal in nature, and its security, which is often threatened by climatic factors. A consequence of this approach is that their detoxification systems must remain flexible enough to cope with low levels of a plethora of compounds. These may easily be overloaded if restricted to a few food items. As mammals have evolved overall because of, rather than in spite of, green plants, it may not be fanciful to suppose that low levels of potentially toxic chemicals may actually be beneficial at low concentration and in the presence of adequate nutrients. This might go some way to explaining why it is that many natural medicinal agents are toxic at high doses. Toxicity is relative. As Janzen (1978) has pointed out, animals will not necessarily prefer to feed on plants with low levels of plant secondary compounds if they can feed on those with higher levels whose negative effects are offset by high concentrations of nutrients.

Many plant secondary compounds which appeared to be neither nutritive nor toxic to mammalian predators, for example the ubiquitous flavonoids, are now believed to have subtle beneficial effects in the diet, including a role as scavengers of reactive oxygen species (ROS) and modulators of the immune system. They may have evolved originally in plants to protect them from the effects of ROS generated inter alia through exposure to excess UV light. In mammals ROS are generated as a side reaction of respiration and are normally destroyed by the body's own defences, e.g. by glutathione. They are produced in excess as part of the primary disease process and then go on to cause further tissue injury. A chronic lack of plant-derived antioxidant defences in the modern human diet may be responsible for the rise in many intractable conditions, such as cancer and even AIDS (Halliwell and Cross, 1991).

The influence of oxygen may hold the clue to many of the unanswered questions concerning evolution, for example what has triggered bursts of species diversification at different points in geological time? Gottlieb (1989) suggests that major land plant diversifications corresponded with peaks in the concentration of atmospheric oxygen. He also points out that there is a broad correlation with increased complexity of some plant secondary compounds and their oxygen content.

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