Coevolution

When two kinds of organisms exert natural selection on each other so they influence each other's evolution, they are undergoing coevolution. Any two organisms may exert selective pressure on each other. Herbivores exert selection on plants favoring the evolution of defenses, and plant defenses exert selection on herbivores to overcome them. Competitors exert selection on each other favoring superior competitive ability. Pollinating insects exert selection on flowering plants to provide attractants and rewards, and plants exert selection on pollinators for superior pollination service. This reciprocal natural selection is the core concept in coevolution. It may produce ongoing evolutionary "warfare," in which the participants constantly change their weapons or tools, or it may produce a relationship that benefits both participants. When the outcome is beneficial to both, it is called mutualism.

In 1964 entomologist Paul Ehrlich and botanist Peter Raven suggested that these reciprocal changes in physical, chemical, or behavioral traits could be great enough to generate new species. Theoretically, as selection favors changes in each partner, the altered partner could differ from its ancestor enough to become isolated as a new species. For example, if a plant gains protection from its parents' enemies (disease or insects) by producing novel defenses, and if this protection is lost by sharing genes with the parental plant types, then selection should eventually eliminate mating between these two types, resulting in two species where before there was one. Natural selection may then favor enemies capable of colonizing the new plant species, with subsequent reproductive isolation and the formation of additional enemy species. New enemy and plant species are thus formed. Ehrlich and Raven claimed that coevolution may be the major kind of interaction generating the diversity of species on land. While many scientists are skeptical of that statement, the evidence of coevolution is all around us, and many fascinating relationships in nature have arisen from it.

Evidence of Coevolution

Most plants and animals experience natural selection from many sources at once. So it seems unlikely that one organism would be the sole or even the primary selective influence on another. Nonetheless, there are good examples of tightly coevolved relationships (the two participants have a highly specialized interaction). In these cases, the selective advantages gained by responding to one source of selection (the other participant) must outweigh many other factors.

For example, butterflies in the cabbage butterfly family (Pieridae) feed primarily on plants in the cabbage family (Brassicaceae). Members of the cabbage family (cabbage, broccoli, mustards) all share a common set of chemical defenses, called glucosinolates, that are found in very few other plant families. Species in the cabbage butterfly family are capable of feeding on these toxins without harm. According to the coevolutionary view, a mutation long ago in a cabbage ancestor provided that plant with the ability to make glucosinolates, which allowed it to escape the pests plaguing its glucosinolate-free ancestors. But soon natural selection favored butterflies with mutations allowing them to feed on glucosinolates, and these butterflies were able to eat the new plants. Additional mutations in the plants produced new glucosinolates, protecting those plants but selecting for butterflies that could overcome the new chemistry, and so on. In the coevolution scenario, the ability to produce glucosinolates and stepwise responses to evolving enemies resulted in the cabbage family as well as the cabbage butterfly family. If we were to draw cladograms, or evolutionary trees, for co-evolved insects and their host plants, they would be near-mirror images, since each chemical change and speciation event among the plants should have produced one in the insects, and each change in the insects should have produced one in the plants.

Factors Inhibiting Coevolution

Closely matched trees are said to be concordant, an indication of co-evolution between two sets of organisms. Scientists have thus far found few concordant trees involving plants and insects, for at least four reasons. First, it is very difficult to construct such trees, especially for insects, because the fossil record (and even current knowledge about insect diets) is so incomplete. Diets are not preserved in the fossil record. Second, insect and plant evolution are influenced by many things. Most plants are attacked by many different kinds of enemies, and a single defense is unlikely to work equally well against all. And insect success is dependent not only on food, but on weather, escape from predators and disease, and other factors. So plants may not be the single greatest influence on insects or vice versa.

Third, these selective factors interact. The susceptibility of insects to predators, parasites, and disease is also influenced by plant defenses, sometimes in a direction opposite to the way chemistry influences growth and reproduction. For example, gypsy moths grow larger and produce many more eggs when feeding on aspen leaves than on oak. But they are killed readily by a viral disease when they feed on aspen and are protected by oak leaves. So there are conflicting selective forces acting on the insects. The net result is that gypsy moth caterpillars do not distinguish between oaks and aspens consistently. Similarly, plant defenses against their own diseases sometimes inhibit production of defenses against herbivores. This would make coevolution between plants and herbivores very unlikely.

Fourth, herbivores usually do not exert enough selection to favor major changes in the plants. They rarely consume more than a small fraction of their plant food and seldom kill plants outright. Compared with other factors, like obtaining water, nutrients, and light, herbivores are seldom the strongest evolutionary influence on plants. Similarly, competitors infrequently exert the kind of influence on plant neighbors that would produce coevolutionary patterns. Plants exhibit adaptations to competition, including growth responses to the green light reflected from neighbors, and perhaps the production of chemicals toxic to competitors (allelopathy). But there are few, if any, clear cases of mutual adaptation among plant competitors.

But diseases do kill plants frequently and so exert strong selection on plants favoring defense responses specific to the attacking microbe. Scientists have documented many gene-for-gene interactions between plants and pathogens in which a single gene difference between two plants can determine susceptibility to a given microbe. A single gene difference between two microbes can determine which can successfully attack a given plant. One can clearly see evidence of coevolution in these cases, where plants have responded to pressure from microbes with successive genetic and biochemical modifications and the microbes have responded in kind to those changes. A few similar examples do exist for plants and insects, in plant species (e.g., conifer trees, parsnips) with defenses strongly influenced by genes (and less by environment) and insects that can kill them.

Mutually Beneficial Coevolution

Perhaps the most striking examples of coevolution involve mutualisms, in which the participants have exerted selection that makes their relationship increasingly beneficial to each of them. In mutualisms natural selection has favored traits in each participant that strengthen or improve the relationship and its benefits. These interactions contrast with those described above, in which each organism participates at the other's expense.

For example, insects and other animals that transfer pollen among flowers (pollen vectors ) provide a crucial service to the plant while receiving a reward, usually nectar and pollen itself. Because it is disadvantageous for a plant's pollen to be deposited on the flower of another species, natural selection has favored the evolution of traits to reduce these "errors," usually by narrowing the range of species attracted and moving pollen. For example, flowers may produce nectar guides, patterns that reflect ultraviolet wavelengths, making them visible only to certain insects. Others may provide a long, tubular entrance accessible only to night-flying moths with long tongues. The length of a flower's corolla tube is often matched to a particular moth having the same tongue length. This ensures that the pollen will be carried only to other flowers with the same tube length, presumably of the same species. Some flowers provide necessary resources for specific insects, such as oils needed to cement a bee's nest or for mating purposes. In each case, there presumably has been a series of evolutionary changes in the flower (such as corolla tube length) that exerted selection-favoring changes in the pollen vector (tongue length, for example), fine tuning the interaction to mutual benefit.

The evolution of mutualism provides opportunities for deception. For example, many species of orchids produce colorful flowers and odors but provide no reward. They depend on mistakes made by inexperienced bees to get their pollen onto a vector. To ensure that a mistake pays off, the orchid is constructed so that any visiting bee necessarily carries away the pollen in sticky packets called pollinia deposited on its body. The flower is constructed so that when the bee makes a second mistake the pollinium is removed and deposited on the stigma of the second flower. Pollen transfer has to be efficient; terrestrial orchids in temperate North America may only be visited once in a decade.

Some tropical orchids improve their chances of being visited by producing volatile chemicals that are collected by certain bees and used as mating signals. Some orchids may produce an odor that mimics a bee's mating signal, attracting bees that are then disappointed in finding no mate, but carry away a pollinium. In more elaborate coevolved interactions the orchid flowers actually look like a female bee or wasp, with which males attempt to mate. In yet others the flower resembles a male bee, and territorial males attack it. In these latter situations, the pollinia are deposited on the bee when it contacts the flower to mate or fight. All of these deceptive floral adaptations produce a very dependable relationship between the plant and insect (pollinator constancy), but at the insects' expense.

Plants may form mutualisms with potential enemies as well. A limiting step in the nitrogen cycle is the capture of inorganic nitrogen from the air and its incorporation into organic forms plants can use. Bacteria have developed this ability, called nitrogen fixation, and are a critical link in this cycle. Legumes and some other plants have formed associations with certain bacteria, particularly the genus Rhizobium, in which the bacteria live in swellings, or nodules, on the plant roots. But since many bacteria are enemies (pathogens) of plants, plants and Rhizobium have had to reach a coevolved accommodation. Through coevolution, they have developed a specialized interaction that depends on manipulating expression of each other's genes. Rhizobium produces signals that turn off plant defense responses and identify it as friendly to the plant. Host plants produce chemical signals that turn on genes in the bacteria that produce signals directing the plant root to produce a nodule. The bacteria then invade the nodule, where the plant provides necessary nutrients in return for nitrogen. It is clear that this relationship has evolved from a battle between enemies, host and pathogen, to a mutualism.

Unanswered Questions

Scientists are divided about how many species have been shaped by coevolution. Several important questions need to be answered before this issue will be resolved. If insects exert relatively little pressure on plants, how often would plant defenses change? Do insects make mistakes in selecting plants as food or oviposition sites? If not, how do they ever begin feeding on a new plant type? How great a change is necessary to provoke a response in the coevolutionary partner; for example, how much change in the shape of an orchid is necessary to provide improved visitation by an insect? And how can we evaluate the importance of the coevolutionary partner versus other factors that influence the evolution of plants, animals, and microbes?

see also Evolution of Plants; Interactions, Plant-Fungal; Interactions, Plant-Plant; Interactions, Plant-Vertebrate; Pollination Biology.

Jack C. Schultz

Bibliography

Price, Peter W. Insect Ecology. New York: John Wiley & Sons, Inc. 1997.

Schoonhoven, L. M., T. Jermy, and J. J. A. van Loon. Insect-Plant Biology. London: Chapman and Hall, 1998.

Thompson, John N. The Coevolutionary Process. Chicago, IL: University of Chicago Press, 1994.

——, and John J. Burdon. "Gene-for-Gene Coevolution Between Plants and Parasites." Nature 360 (1992): 121-25.

FIGS AND FIG WASPS

More than nine hundred species of figs (Ficus ) are pollinated by figs wasps (family Agaonidae) in rela tionships that exhibit closely coe volved characteristics. The hollow fig inflorescence is formed by a swollen flower receptacle (base) and is lined inside with flowers that go through five stages:

1. Prefemale , in which the fig is closed to wasps as flowers de velop;
2. Female , in which tiny wasps crawl inside the inflorescence through a special pore and lay eggs in the mature flowers;
3. Interfloral , during which wasp lar vae develop inside some female flowers while others produce seed;
4. Male , in which male flowers ma ture, producing pollen, while the new generation of wasps emerges from female flowers. Female wasps mate, collect pollen, and exit through escape holes bored by males; and
5. Postfloral , in which seeds ripen, and the fruit becomes attractive to animals that disperse it.

The escaped females invade new fig flowers on other trees, repeating the cycle. The figs provide special ized flowers in which the wasps lay eggs, sacrificing these as a reward, and the timing of male and female flower production is designed to match the wasps' development. The wasps are specifically adapted for life in the fig, and cannot lay eggs or feed anywhere else. Usually only one wasp species can live in one fig species. A natural consequence of this system is that the figs we eat contain some of the minute wasps that do not escape.