Beetles Versus Plants: a 300‑Million‑Year War

The coevolutionary struggle between enemies may produce much more than exquisite poisons and sophisticated antidotes. It may be a driving force behind the diversity of life itself.

The possibility that coevolution could have such a profound effect was first raised in 1964 by two ecologists, Paul Ehrlich and Peter Raven. Ehrlich and Raven pointed out that while pollinating plants may be on friendly terms with insects, many wage all‑out war. Insects make their living by chewing leaves, boring through wood, feasting on fruit, and otherwise ravaging plants. By eating leaves, the insects deprive them of photosynthesis. By nibbling on their roots, they cut off their supply of water and nutrients. If they chew away too much, they can kill plants outright. Even if insects limit themselves to a plant’s seeds, they deprive it of its genetic legacy.

Plants have evolved physical and chemical defenses to ward off these hungry bugs. Holly plants have evolved leaves with sharp teeth along their edges that protect them from chewing insects. (If you clip off the teeth, bugs can quickly strip the leaves.) Some plants respond to insect bites by creating poisons in their tissues. Some defend themselves with a network of tubes in their leaves and stems full of sticky resin or gooey latex. When an insect chewing on the plant ruptures one of the tubes, a flood of resin or latex comes pouring out. It engulfs the insect, perhaps to entomb it in a lump of amber or trap it in a rubbery plug of latex. Other plants defend themselves by calling for help. In response to the bite of a caterpillar, they release chemicals that attract parasitic wasps. The wasps lay their larvae inside the attackers, devouring them from within.

Ehrlich and Raven suggested that any lineage of plants that happened to evolve a way to escape its pests might be able to grow aggressively and spread its range. It would become less likely to go extinct and more likely to branch off into new species. Over time, its descendants would be more diverse than other lineages of plants that hadn’t managed to escape their pests.

To the insects, these new plants would be like a continent rising out of the ocean, just waiting for them to explore. But to reach it, they would have to evolve a way to overcome the plants’ new defenses. Any lineage of insects that managed to find a way would be able to colonize the plants, and without any competition from other insects, they would thrive and diversify. This coevolution–a series of escapes and captures and fresh escapes–might account for the different levels of diversity among plants and among insects.

Ehrlich and Raven’s hypothesis was alluring, but it was difficult to test. Scientists couldn’t replay the past 300 million years and watch the coevolution of plants and their insect enemies play out. But by the early 1990s, a Harvard entomologist named Brian Farrell had figured out how to use the diversity of living plants and insects to see whether Ehrlich and Raven were right.

In his first test, he set out to see if the evolution of a new defense really does trigger an explosion of diversity in plants. As his test case, he chose the evolution of canals of latex or resin, which drown feeding insects. Farrell found that this defense arose independently in 16 lineages of plants. He counted up the number of species each lineage had given rise to and then compared it to the number of species in closely related lineages that lacked canals. In 13 out of the 16 cases, the groups with canals were far more diverse than their relatives without them. The gingko tree and conifers share a close common ancestor, for instance, but gingkoes, which lack canals, consist of a single species. Meanwhile, conifers evolved canals and have since produced 559 species, ranging from pines to yews. Daisies and dandelions belong to a diverse group of canal‑bearing plants called Asterales, which has 22,000 species in its ranks. Its closest relative without canals, an obscure group called the Calyceraceae, has only 60. By evolving defensive canals, these plants have lived up to Ehrlich and Raven’s prediction: they have thrived by fighting off their enemies.

Farrell then looked at the second part of Ehrlich and Raven’s hypothesis: when insects manage to colonize these new lineages of plants, they experience bursts of diversity of their own. He chose a particularly diverse bunch of insects for his study: beetles. The biologist J. S. B. Haldane liked to say that if biology had taught him anything about the nature of the Creator, it was that he had “an inordinate fondness for beetles.” While insects may be the most diverse group of animals, beetles, with 330,000 known species, are the most diverse group of insects. Farrell set out to figure out how they had become so diverse.

He first built himself an evolutionary tree of beetles. He found that the insects did not start out as plant eaters. The most primitive beetles had a diet that consisted of fungus and smaller insects. A few species of living beetles such as weevils carry on this primitive way of life today. But about 230 million years ago, a new branch of beetles shifted its diet to plants. Many of the plants we are most familiar with had not yet evolved. There were no flowering plants, for example. These early plant‑eating beetles specialized on the plants that already existed, known as gymnosperms (the group that includes conifers, gingkoes, and sago palms). By feeding on gymnosperms, these new branches of beetles diversified into many more species than their fungus‑and insect‑eating cousins.

About 120 million years ago, flowering plants began to emerge and proved to be far more diverse than gymnosperms. As they diversified, five separate lineages of beetles managed to make the leap from gymnosperms to these new plants. Farrell found that in all five cases the beetles that shifted to flowering plants consistently became more diverse than their cousins who stayed behind, surviving on gymnosperms. In some cases the diversity of the new beetles has multiplied more than a thousand times. As Ehrlich and Raven had predicted, the newer beetles explored new ways of making a living on the plants. The beetles that feed on gymnosperms specialize on pinecones or similar seed‑bearing structures. The beetles that moved to flowering plants began branching out to different kinds of food, such as bark, leaves, and roots.

Although no one has done such careful studies of other insects, the same pattern probably holds: coevolution with flowering plants was their secret to success. And like all good research, Farrell’s work points to a new puzzle still to be solved: Why are there so many flowering plants? Again, at least part of the answer probably has to do with coevolution. As insects invented new ways to devour flowering plants, the plants were under intense pressure to find ways to hold them at bay. At the same time, some insects such as bees were coevolving more benign partnerships, helping flowering plants spread their pollen, which may have helped them fight against extinction and branch into more species. Diversity, scientists have found, begets diversity.

Man Versus Bug

Beetles and other insects have been coevolving with the plants they eat for hundreds of millions of years. In the past few thousand years, we humans have suddenly altered their coevolution by domesticating plants and trying to keep insects from eating them. For the most part, we’ve tried stopping insects without taking the reality of coevolution into consideration, with the result that much of our effort backfires. The swift development of resistance to pesticides is one of the most graphic cases of coevolution in action.

Humans began domesticating crops around 10,000 years ago. As the first farmers planted fields with crops like lentils and bulgur, insects fed on them just as they had on their wild ancestors. At first humans could do nothing but plead to the gods. Sometimes they would even take insects to court. In 1478 beetles were ravaging the crops around the Swiss city of Berne, and in response the mayor appointed a lawyer to go to an ecclesiastical court and demand punishment. “With grievous wrong, they do detriment to the ever‑living God,” they complained. A lawyer was appointed for the beetles, and defendant and plaintiff made their cases to the court. After hearing both sides, the bishop ruled in favor of the farmers, declaring that the beetles were incarnations of devils. “We charge and burden them with our curse,” he declared, “and command them to be obedient and anathematize them in the name of the Father, the Son and the Holy Ghost, that they turn away from all fields, grounds, enclosures, seeds, fruits and produce, and depart.”

The beetles did not depart. They went on eating their crops as before. It was then decided that the beetles were not devils but a punishment that God was visiting on farmers for their sins. Once the farmers gave a tithe to the Church from what little harvest they could manage, the beetles disappeared. Or perhaps when the beetles used up their food supply their population crashed naturally.

When court cases and invocations to the gods have failed, farmers have resorted to poisons. The Sumerians began putting sulfur on their crops 4,500 years ago; pitch and grease were popular in ancient Rome. Ancient farmers discovered that some plants contained substances that could help their crops ward off insects. The Greeks soaked their seeds in cucumber extract before planting them. In the 1600s, Europeans began to extract chemicals from plants such as tobacco that proved even more powerful than old potions. From an Armenian daisy in 1807 came pyrethrum, which farmers still use today.

At the same time that Europeans were discovering better pesticides, they were also building huge farms both at home and in their new colonies. For insects it was as if someone had laid out a vast banquet table. Epidemics of insects raced across entire countries. Farmers began resorting to harsher kinds of pesticides, such as cyanide, arsenic, antimony, and zinc; they mixed copper and lime into a concoction known as paris green. With the invention of airplanes and spray nozzles, entire farms could be blanketed with pesticides, and by 1934 American farmers were using 30 million pounds of sulfur, 7 million pounds of arsenic‑based pesticides, and 4 million pounds of paris green.

Around 1870, a little fruit‑eating insect arrived in San Jose, California, on some nursery stock shipped from China. The pest, which became known as the San Jose scale, quickly spread through the United States and Canada, killing orchard trees as it went. Farmers found that the best way to control the scale was to spray their orchards with a mixture of sulfur and lime. Within a few weeks of spraying a tree, the insect vanished completely.

Around the turn of the century, however, farmers began to notice that the sulfur‑lime mixture wasn’t working all that well. A handful of scales would survive a spraying and eventually rebound to their former numbers. In Clarkston Valley in Washington state, orchard growers became convinced that manufacturers were adulterating their pesticide. They built their own factory to guarantee a pure poison, which they drenched over their trees, yet the scale kept spreading uncontrollably. An entomologist named A. L. Melander inspected the trees and found scales living happily under a thick crust of dried spray.

Melander began to suspect that adulteration was not to blame. In 1912 he compared how effective the sprays were in different parts of Washington. In Yakima and Sunnyside, he found that sulfur‑lime could wipe out every last scale on a tree, while in Clarkston between 4 and 13 percent survived. On the other hand, the Clarkston scales were annihilated by a different pesticide made from fuel oil, just as the insects in other parts of Washington were. In other words, the scales of Clarkston had a peculiar resistance to sulfur‑lime.

Melander wondered why. He knew that if an individual insect eats small amounts of certain poisons, such as arsenic, it can build up an immunity. But San Jose scales bred so quickly that no single scale experienced more than a single spray of sulfur‑lime, giving them no chance to develop immunity.

A radical idea occurred to Melander. Perhaps mutations made a few scales resistant to sulfur‑lime. When a farmer sprayed his trees, these resistant scales survived, as well as a few nonresistant ones that hadn’t received a fatal dose. The surviving scales would then breed, and the resistant genes would become more common in the following generations. Depending on the proportions of the survivors, the trees might become covered by resistant or nonresistant scales. In the Clarkston Valley region farmers had been using sulfur‑lime longer than anywhere else in the Northwest and were desperately soaking their trees with the stuff. In the process, they were driving the evolution of more resistant scales.

Melander offered his ideas in 1914, but no one paid much attention to him; they were too busy discovering even more powerful pesticides. In 1939 the Swiss chemist Paul Muller found that a compound of chlorine and hydrocarbons could kill insects more effectively than any previous pesticide. Dubbed DDT, it looked like a panacea. Cheap and easy to make, it could kill many species of insects and was stable enough to be stored for years. It could be used in small doses, and it didn’t seem to pose any health risks to humans. Between 1941 and 1976,4.5 million tons of DDT was produced–more than a pound for every man, woman, and child alive today. DDT was so powerful and cheap that farmers gave up old‑fashioned ways of controlling pests, such as draining standing water or breeding resistant strains of crops.

DDT and similar pesticides created the delusion that pests could be not merely controlled but eradicated. Farmers began spraying pesticides on their crops as a matter of course, rather than to control outbreaks. Meanwhile, public health workers saw in DDT the hope of controlling mosquitoes, which spread diseases such as malaria. In his 1955 book, Man’s Mastery of Malaria , Paul Russell of Rockefeller University promised that “for the first time it is economically feasible for nations, however underdeveloped and whatever the climate, to banish malaria completely from their borders.”

DDT certainly saved a great many lives and crops, but even in its early days some scientists saw signs of its doom. In 1946, Swedish scientists discovered houseflies that could no longer be killed with DDT. Houseflies in other countries became resistant as well in later years, and soon other species could withstand it. Melander’s warning was becoming a reality. By 1992 more than 500 species were resistant to DDT, and the number is still climbing. As DDT began to fail, farmers at first just applied more of it; when more no longer worked, they switched to newer pesticides, like malathion; when those started to fail, they looked for newer ones.

The quest to eradicate pests with DDT and similar poisons has been a colossal failure. Each year more than 2 million tons of pesticides are used in the United States alone. Americans use 20 times more pesticides today than they did in 1945, even though the newest pesticides are up to 100 times more toxic. And yet the fraction of crops lost to insects has risen from 7 percent to 13 percent–thanks in large part to the resistance insects have evolved.

The failure of DDT has been an unplanned experiment in evolution, as compelling as Darwin’s finches or the guppies of Trinidad. As Ehrlich and Raven pointed out in 1964, plants have been producing natural pesticides for hundreds of millions of years, and insects have coevolved resistance to them. In the last few thousand years, insects encountered some new man‑made poisons on the plants they’ve been eating, and they’ve been doing what they’ve always done: evolving their way around them. Coevolution has entered the age of humans.

The first time a pesticide is sprayed on a field, it kills most of the insects. A few insects survive because they don’t get a fatal dose. Others survive because they have rare mutant genes that happen to protect them from the pesticide. These mutations might have arisen from time to time during the species’ life‑time, but normally they put insects at a disadvantage. As the mutants were outcompeted, their mutation would disappear. The balance between new mutations and their eradication from the gene pool leaves a population of insects at any given moment with a few mutants in their ranks. At the moment that the pesticides arrive, the mutants suddenly are more fit than their counterparts.

There are many ways that mutant insects can resist pesticides. They may be born with thick cuticles covering their bodies, shielding them from the chemical. They may make a mutant protein that can cut a pesticide molecule into pieces. They may get irritable when they come into contact with the pesticide, flying away before they can receive a lethal dose.

After a spraying, the surviving insects are free from competitors. They may even be liberated from their parasites and predators, if the pesticide wipes them out as well. With few rival pests to eat their food, and without enemies to keep their numbers in check, they explode. As they mate with one another, or with surviving nonresistant insects, their mutant genes quickly spread. If farmers spray relentlessly, enough, the nonresistant forms may disappear almost completely.

Pesticides are a clumsy substitute for coevolution. Plants and insects can evolve new attacks against each other from one generation to the next. But chemists need years to discover new pesticides, and as they search, the resistance insects evolve takes a heavy toll. Resistant insects require farmers to spend more money to buy new pesticides. Unlike the natural defenses that plants produce, pesticides may also kill earthworms and other subterranean creatures that are essential for creating new soil out of organic matter. Some pesticides kill bees and other pollinators. They can linger in the environment for years and travel for thousands of miles. Pesticides may also kill humans, directly poisoning farmhands, and there is some disturbing–although hotly disputed–evidence of a relationship between exposure to pesticides and some types of cancer.

Agribusiness has recently offered a solution to the pesticide crisis, in the form of genetically altered crops. Eight million hectares of farmland are now planted with crops carrying genes from bacteria that let them make their own pesticides. The genes come from Bacillus thuringiensis, a bacterium that lives in the soil and artacks butterflies and moths. In order to feed on its hosts, B. thuringiensis uses these genes to produce a protein that destroys an insect’s gut cells. Cultures of the bacteria (known as Bt) have been kept since the 1960s, and the protein is sprayed just about everywhere, from organic farms to forests. It doesn’t harm mammals, and it quickly breaks down in sunlight. Now biochemists have been able to insert Bt genes into plants such as cotton, corn, and potatoes, and these plants now produce Bt in their own tissues. Insects that attack the transgenic plants eat the Bt and die.

The Environmental Protection Agency is hoping that Bt‑producing crops won’t become another victim of coevolution. If a cotton farmer plants his entire farm with Bt‑producing crops, the insects that live there will encounter vast expanses of plants all producing the same poison, and they’ll evolve resistance. The EPA is mandating that farmers plant ordinary crops on 20 percent or more of their fields. These patches will become refuges where nonresistant insects can survive; they’ll mate with resistant insects, the reasoning goes, and keep those resistance genes from becoming too common.

This approach depends on the cooperation of farmers, who will have to sacrifice some of the crops in their refuges to insects. But their grim experiences with pesticides will probably keep many of them from planting only Bt crops. If these crops succeed over the long term, it will be thanks to a proper understanding of coevolution. But if resistance does break out, farmers may have to buy new kinds of modified plants that produce a new kind of toxin–in other words, they will have to jump off the pesticide treadmill only to jump onto a transgenic treadmill.

Coevolution offers some hints about other ways to fight pests. Insects would be less harmful if farmers stopped growing vast carpets of monoculture. Growing a combination of different crops makes it harder for the specialist pests to build up the reproductive momentum they need to cause an outbreak. And consumers can help as well. When you shop for fruit, you probably pass over ones that are blemished. Fruit growers know this and go to great lengths to deliver spotless produce to supermarkets–a feat that requires using lots of pesticides to kill insects. In fact, a slightly blemished fruit is perfectly safe to eat. If consumers were more willing to buy less‑than‑perfect fruit, farmers could use substantially fewer pesticides. As a result, they would relax the evolutionary pressure on insects to resist the pesticides.