Many evolutionary adaptations can only be understood as evolution of one species in response to another species, a process known as coevolution. Coevolution can modify general interactions such as herbivory or predation, or it can result in very close symbiotic relationships between two species. In coevolution, the evolution of each species is influenced not by the mere presence, but by the evolution, of the other species. To understand an adaptation that results from coevolution between two partners, one has to at least know the identity of the other partner. But what happens if one of the partners has become extinct? The other species may continue manifesting its adaptations, perhaps for thousands of years, even though the adaptations are now meaningless. The adaptations of the surviving species now become puzzling, because the other spe- cies has become one of the “ghosts of evolution.”
In order for symbiotic adaptations to continue being expressed, even when the other partner is a ghost, the adaptations must not be detrimental to the organism, otherwise its cost would be so great that natural selection would get rid of the adapta- tions or the species that has them. Furthermore, the extinction of one species should have been relatively recent, otherwise natural selection, operating over long periods of time, would presumably eliminate the adaptations.
One of the types of symbiotic interaction is parasitism, in which the parasite benefits at the expense of the host. Coevolution favors hosts that resist parasites. If the parasite becomes extinct, the host may continue defending against it. Some observers main- tain that some human blood proteins are examples of defenses against bacterial parasites that are now rare. A mutated form of the CCR5 protein, which is on the surfaces of some human white blood cells, may have conferred resistance to bubonic and pneumonic plague, which would explain why it is most prevalent (even though it is still less common than the normal CCR5 protein) in northern European countries. Calculations of the rate of evolution of this mutant protein suggest that it originated at about the time of the Black Death of 1347–50, and it may help to explain why subsequent outbreaks of the plague were less severe than the Black Death. The plague bacillus, Yersinia pestis, is not actually a ghost; it still exists. However, it is sufficiently rare—mainly because it is spread by rat fleas, and public health measures now keep rats and humans from as close contact as occurred in the Middle Ages—that it is almost a ghost. The CCR5 protein has recently become a subject of intense interest, as it appears to be one of the proteins that HIV uses to gain entry into certain white blood cells (see AIDS, evolution of). It has also been suggested that the mutant form of the cell membrane chloride transport protein, a mutation that causes cystic fibrosis, was once favored by natural selection because it conferred resis- tance to diseases. This would explain why the mutation is so com- mon: one in 25 Americans of European descent carry the mutation. Since the adaptations carry little cost, and the parasites have only recently become uncommon, the adaptations persist. Another type of symbiotic interaction is mutualism, in which both species benefit. One major category of examples of ghosts of evolution is certain types of fruits. The function of a fruit is to get the seeds within it dispersed to a new location. Some fruits have parachute-like structures or wings that allow the wind to disperse the seeds to new locations. Other fruits use animal dispersers. Spiny fruits cling to the fur of mammals. These fruits have probably not coevolved with specific mammalian species; any furry mammal can carry a cocklebur fruit and scatter its seeds. But coevolution is likely to occur between animals and plants with fruits that are soft, sweet, fragrant, and colorful. All four of these adaptations are costly to the plant that produces them, and specific to a relatively small group of animals that eat the fruits. A fruit may appeal to one kind of animal, but its particular characteristics, especially flavor, may be uninteresting or even disgusting to other animals. Therefore if a species of animal that eats fruits becomes extinct, the seeds in those particular fruits may no longer be dispersed to new locations. If this should happen, the species of plant will not necessarily become extinct, although it will probably suffer a reduced popula- tion because fewer seeds are dispersed to suitable new locations. The fruits will simply fall to the ground near the parent and grow there. Some seeds will not germinate right away unless they have passed through an animal intestine; however, these seeds often germinate eventually even without this treatment. The result will be clumps of unhealthy, competing plants, but at least they will not immediately die. Another species of animal may become attracted to the fruit, but they are unlikely to be as effective as the original species of animal with which the plant species coevolved. Con- sider an example, in which a large animal consumes the fruits of a species of tree. The animal chews and digests the fruits but does not chew the seeds. The seeds, with hard coats, pass through the digestive tract intact and can germinate. This animal is an effec- tive dispersal agent. If this large animal species becomes extinct, a smaller animal species may consume the fruits. However, the smaller animal may not swallow the whole fruit and may either pick out the seeds or actually crush and eat them. In either case, the smaller animal is not acting as an effective dispersal agent, the way the large animal did. In some extreme cases, the fruits pile up on the ground and rot.
North America has an impressive number of plant species that produce fruits that seem to have no animals that disperse them, often because they are too large for any extant animal spe- cies to eat. Their dispersers would appear to be ghosts of evolu- tion. North America had many large mammal species, until the end of the last Ice Age, when two-thirds of the genera of large animals became extinct. This included mastodons, mammoths, horses, and giant sloths. It is unclear to what extent this was caused by the cli- mate changes that were occurring at that time, or by overhunting by the newly arrived humans (see pleistocene extinction). These animals are probably the ghosts. South America also suffered a wave of extinctions, about the same time as North America. North America has many more ghosts of evolution than Eurasia, and it also suffered a far larger number of large mammal Pleistocene extinctions than Eurasia. Ecologists Daniel Janzen and Paul Martin first suggested that this phenomenon is widespread in North and South America.
Scientists cannot identify ghost dispersers with certainty, because nobody knows whether any of these animals actually would have eaten the fruits. If scientists hypothesize that mast- odons dispersed certain fruits, the best that they can do is to see
whether elephants eat any of these fruits. This tells the scientists little, because elephants are similar to but not the same as mast- odons, and because animals eat not just what their species can eat but what they have learned to eat from their parents. Even if inves- tigators could train elephants to eat some of these fruits, this would not prove that, in the wild, mammoths or mastodons ate them. Among the examples of North American ghosts of evolution are: • Bois-d’arcs. These are small trees, noted for their very strong
wood, that have been planted widely across North America as fencerow windbreaks. Like other trees in the mulberry family, Ma- clura pomifera has separate male and female trees; and the fe- males produce composite fruits that consist of a cluster of berries. While mulberries are small, sweet, and edible by many species of birds and mammals (including humans), the fruits of the bois-d’arc are large (about seven inches, or 15 cm, in diameter), green, hard, and sticky. (These trees are also called Osage oranges, because the fruits look a little bit like oranges and grow wild in the tribal lands of the Osage tribe; and hedge-apples, because the fruits look a little bit like apples and the trees were planted as hedges.) While not highly poisonous, the fruits are definitely repulsive and diffi- cult to digest. There appears to be no animal that eats the fruits. Squirrels consume the seeds, but this is not dispersal; it kills the seeds rather than dispersing them. The fruits commonly fall to the ground and rot; several of the fruit’s dozens of seeds grow, result- ing in a clump of trunks that have grown together. In some cases the trunks have fused to form what appears to be a single trunk. It is rare to see a single-trunked bois-d’arc tree in the wild. (Single- trunked bois-d’arc trees are common in the countryside, but these were planted in fields that were subsequently abandoned and are not really wild trees.) Another consequence of the absence of a disperser is that wild bois-d’arcs are found only in river valleys of Oklahoma, Texas, Arkansas, and nearby areas. Without dispers- ers, the only direction for such large fruits to roll is downhill, into river valleys. Had they not been planted widely across eastern North America, they might eventually have become extinct as the last fruit rolled into the sea.
• Avocados. Wild avocados (Persea americana) are not nearly as large as the ones in supermarkets, but they are still large enough that no extant species of animal swallows them whole. Many ani- mals can nibble at the nutritious fruit, but the seeds are simply left near the parent in most cases. Which large animal might have eaten these fruits in the past?
• Honey locusts. Gleditsia triacanthos, a tree in the bean family, pro- duces very long, spiral seed pods. No native species of mammal regularly eats these pods, even though they are juicy and sweet. Once cattle were introduced to North America, many of them would eat these pods when available. Like bois-d’arcs, honey locust trees have a recent native range confined largely to river valleys. Today they have spread again, because they have been widely planted as urban trees and have escaped again into the wild. There appears to be a similar lack of dispersal in the mes- quite, a bush in the bean family that also produces sweet pods, though much smaller than those of honey locust. Other examples that have been suggested include papayas, man- gos, melons, gourds, and watermelons. The idea that North and South America have many fruits that are ghosts of evolution is corroborated by African and Asian ana- logs. There are numerous fruits in Africa and Asia that are con- sumed, and the seeds dispersed, by animals (such as elephants) that are similar to the ones that became extinct in the Americas. Some of the ghost fruits are inedible to most animals, but the now-extinct specialist dispersers may have had, as African and Asian fruit dis- persers do today, intestinal bacteria that break down otherwise toxic products. Elephants eat clay, which adsorbs toxins from the digestive system. Might mammoths and mastodons have had similar adaptations that allowed them to consume fruits such as bois-d’arc?
Fruits are not the only examples of the ghosts of evolution. Other examples include flowers and stems.
• Flowers. Pawpaws (Asimina triloba), small wild fruit trees of the eastern deciduous forest of North America, persist primarily by the spread and resprouting of roots and underground stems. No native pollinator appears to be reliable. Although there has been no recent wave of pollinator extinctions as great as that of the Pleistocene extinction of fruit dispersers, apparently the pollinator of this tree has become extinct. Recently, native pollinator populations have precipitously declined, which threatens many native plant species with ultimate extinction. This may especially be true of large cacti in the deserts of southwestern North America, which rely on bats to pollinate their flowers. Thus very soon the bats that pollinate these cacti might become ghosts of evolution.
• Stems. The bois-d’arc also has large thorns, widely spaced on the branches, which appear totally ineffective at defending the leaves against the animals that today eat them, such as deer. Per- haps the thorns as well as the fruits are the leftover responses to the now-extinct ghosts of evolution. Wild honey locust trees have three-pointed thorns (hence the name tri-acanthos) bristling from their trunks. Hawthorns (genus Crataegus) have thorns even longer, and more widely spaced, then those of bois-d’arc. Evo- lutionary biologists estimate that 10 percent of the woody plant species in New Zealand have a particularly tangled method of branching that may have protected them at one time from brows- ing by moas, giant birds that were driven into extinction by the first Maori inhabitants. Other revolutionary biologists, such as C. J. Howell, disagree.
Thirteen thousand years is not long enough for the trees to evolve some other mechanism of dispersal. One would expect that, eventually, the unnecessarily large fruits would no longer be produced, as mutant forms of the trees produced fruits that could be easily dispersed by wind or water. This may have happened in the case of the honey locust. An apparently new species of locust, the swamp locust Gleditsia aquatica has evolved in southern North America, perhaps from a Gleditsia triacanthos ancestor. It produces much smaller pods that float easily in water.
The main point of this essay is that species are “designed” by evolution not to live in their current environments but in those of their immediate ancestors—and if that environment changes, there can be a considerable lag time before evolution designs a response. The result is, as ecologist Paul Martin wrote, “We live on a conti- nent of ghosts, their prehistoric presence hinted at by sweet-tasting (continues)
from not harming the host; if the parasite kills the host, it has killed its habitat, and must find another. Natural selec- tion often favors the evolution of milder and milder para- sites. This does not happen with parasites such as cholera
bacteria, that disperse to new hosts rapidly or impersonally (in the case of cholera, through sewage). But when a para- site must disperse to a new host by personal contact among hosts (as with smallpox), the parasite benefits when the host remains well enough to walk around and infect other people. The Ebola virus is one of the deadliest diseases known to humankind, but it is so deadly that it never has had a chance to spread through more than a small group of people at any one time.
Coevolution, therefore, can cause host species to become more resistant, and parasite populations to become milder. Many diseases, such as smallpox, were evolving toward milder forms even before the introduction of mod- ern medical practices. Some diseases have, in fact, disap- peared, perhaps because the parasitic relationship evolved into a completely commensalistic one. This process, also called balanced pathogenicity, has been directly measured during the course of a disease outbreak in rabbits. Commen- salism can be produced by coevolution, but once it has been attained, does not involve coevolution any longer. Natural selection may prevent the relationship from slipping back into parasitism.
Coevolution Leading to Mutualism
Another kind of symbiosis is mutualism, in which both spe- cies benefit. In some cases, the activities of commensals can evolve into mutualism. Most human intestinal bacteria are commensals. Some of them are mutualists because they pro- vide a benefit to humans. The presence of some kinds of intestinal bacteria may prevent the growth of parasitic bacte- ria. Some of the mutualistic bacteria may even produce vita- min B which is to them a waste product. Bacteria on the skin and in body orifices may prevent infection by parasitic bac- teria and fungi. Nonhuman examples of beneficial internal microbes abound. Cows cannot digest grass; it is the bacteria in their stomachs that digest it (and get food for themselves in the process). Many termites cannot digest wood; it is the microbes in their intestines that digest it. The microbes in
pods of mesquite [and] honey locust …” As the destruction of wild habitats by humans continues at a rapid pace, humans may be inau- gurating the sixth of the mass extinctions in the history of the world. Sometimes, when two species are partners, human activities cause the extinction of one partner but not the other. Starting with the 19th century, scientists began to understand that the present is the key to understanding the past. To understand what happened in the past, look at what is happening today in the natural world. However, it is just as true that the past is the key to understanding the present. This is just one of the many meanings that emerge from the brilliant statement made by one of the founders of modern evolutionary sci-
ence (see dobzhansky, theodosius): “Nothing makes sense except in the light of evolution.”
Further Reading
Barlow, Connie. The Ghosts of Evolution: Nonsensical Fruit, Missing Partners, and Other Ecological Anachronisms. New York: Basic Books, 2000.
Buchmann, Stephen L., and Gary Paul Nabhan. The Forgotten Pol- linators. Washington, D.C.: Island Press, 1996. Howell, C. J., et al. “Moa ghosts exorcised? New Zealand’s divari- cate shrubs avoid photoinhibition.” Functional Ecology 16 (2002): 232–240. Janzen, Daniel H., and Paul S. Martin. “Neotropical anachronisms: the fruits the gomphotheres ate.” Science 215 (1982): 19–27.