The Beak of the Finch: A Story of Evolution in Our Time

by Jonathan Weiner

  That is why Rosemary and Peter put the word dynamic in the title of the first book they wrote together: Evolutionary Dynamics of a Natural Population. “It’s important to keep in mind,” says Rosemary: “Species don’t stand still. You can’t ‘preserve’ a species.” Every species is, as the Grants write in the last words of their book, “constantly changing and capable of further change.”

  All of which brings home a “bitter-sweet message,” as Peter Boag wrote in Nature on the centenary of Darwin’s death: “much less is known about evolution in the Galápagos than most people think, but Galápagos populations and communities are probably now changing faster than ever.”

  Chapter 18

  The Resistance Movement

  Let a man profess to have discovered some new Patent Powder Pimperlimplimp, a single pinch of which being thrown into each corner of a field will kill every bug throughout its whole extent, and people will listen to him with attention and respect. But tell them of any simple common-sense plan, based upon correct scientific principles, to check and keep within reasonable bounds the insect foes of the farmer, and they will laugh you to scorn.

  —BENJAMIN WALSH,

  The Practical Entomologist (1866)

  All summer long, messengers from Federal Express deliver large white parcels to a laboratory down on Moffett C-Level. The parcels come from hamlets in Louisiana, Southern California, and many states in between: the swath of North America that is often called the Cotton Belt, or the Bible Belt.

  As these parcels come in, a postdoc in the laboratory sets them on his lab bench, slits the FedEx seals, and lifts the insulated lids. Inside, each box is molded in the shape of a white crater. In the bottom of the crater, lying on a bed of dry ice, amid a faint rising cloud of vapor, are a dozen gray moths.

  The postdoc, Martin Taylor, lifts out the moths one by one with a tweezers. One by one he grinds them in a mortar and pestle, like an old fashioned pharmacist, to extract their DNA. He is watching these moths from his laboratory bench the way Peter Boag is watching Darwin’s finches. Some of the greatest opposition to evolution comes from the farmers of the Cotton Belt, and that is where Taylor is seeing one of the most dramatic cases of evolution in action on this planet.

  There was a time, not so long ago, when this particular species of moth, Heliothis virescens, lived a life of obscurity, probably in forests and hedgerows, where it ate weeds. But in the year 1940, cotton farmers began spraying their fields with the chemical compound dichlorodiphenyltrichloroethane, better known as DDT. These first insecticidal sprays killed so many insects, and killed so many of the birds that ate the insects, that in biological terms the cotton fields were left standing virtually vacant, like an archipelago of newborn islands—and out of the woods and hedgerows fluttered Heliothis virescens.

  Some of these moths were able to tolerate DDT. They lived long enough to lay their eggs in the cotton bolls. Their eggs hatched into larvae, and the larvae began devouring the cotton.

  In the next few optimistic years, pesticide manufacturers assaulted Heliothis with bigger and bigger doses of DDT. They also brought out more poisons from the same chemical family: aldrin, chlordane. The aim was nothing less than the control of nature, and pesticide manufacturers believed that control was within their grasp. The annual introduction of new pesticides rose from the very first product, DDT, in 1940, to great waves of chemical invention in the 1960s and 1970s. In those decades, dozens of new herbicides and insecticides were brought to market each year. Heliothis became one of the most heavily sprayed species in what amounted to a biological world war. Through it all, the moths clung to the cotton.

  At the moment, most farmers in the Cotton Belt are spraying their fields with pyrethroids, which are sold under brand names as optimistic as ever: two of the more popular are Scout and Karate. When these pyrethroids were first introduced, they improved cotton yields by about a quarter, sometimes as much as a third. But in the year 1980, there were reports from California’s Imperial Valley of moths with fifty-fold resistance to pyrethroids. This resistance movement spread like the others.

  “Right now Heliothis is throwing the cotton industry in Louisiana in a panic,” says Bruce Black, an entomologist at American Cyanamid, the pesticide giant, which is based in Princeton. “The moths have become almost absolutely resistant to all pesticides, from your cyclodienes to your organophosphates to your carbamates, and most of your pyrethroids. And these pyrethroids are literally the last bastion to prevent the cotton industry from collapsing. In Louisiana, in the fields, they have insects that are two-hundred-fold resistant to pyrethroids. Farmers are saying they can’t grow a crop next year. The bugs will wipe them out.”

  Martin Taylor has a grant from American Cyanamid to watch Heliothis evolve.

  WHEN HE LECTURES about Heliothis, Taylor usually begins with a transparency on which he has printed, in tall, spindly, Victorian characters:

  THE VARIATION OF ANIMALS AND PLANTS

  UNDER DOMESTICATION

  with special reference to resistance

  of insects to pesticides

  By Charles Darwin. MA, FRS, &c.

  “It’s an extraordinarily potent example of evolution going on under our eyes,” Taylor says. “Visible evolution.”

  A pesticide applies selection pressure as surely as a drought or flood. The poison selects against traits that make a species vulnerable to it, because the individuals that are most vulnerable are the ones that die first. The poison selects for any trait that makes the species less vulnerable, because the least vulnerable are the ones that survive longest and leave the most offspring. In this way the invention of pesticides in the twentieth century has driven waves of evolution in insects all over the planet. Heliothis is only one case in hundreds. Flying scale insects have evolved strong resistance to buquinolate in only six generations. Nematode worms in the guts of sheep have evolved strong resistance to thiabendazole in three generations. Sheep ticks have evolved strong resistance to HCH-dieldrin in just two generations. In 1967, a distinguished entomologist announced in Scientific American the discovery of a “resistance-proof” family of insecticides. The poisons were variants of some of the insects’ hormones. How could insects escape their own hormones? Yet within five years, flies had evolved one-hundred-fold resistance.

  “This seemed to surprise people,” says Taylor. “It would not have surprised an evolutionary biologist. But it surprised pesticide sprayers and the manufacturers of chemical compounds endlessly.”

  “If you look through the literature,” says Linda Hall of Cornell University, who specializes in the study of pesticide resistance, “you’ll find people saying, ‘Resistance will not develop for pyrethroids.’ That was incredibly naive. Almost anything you give an insect, almost any way you find to kill it, it will find a way not to be killed. That’s the whole bit about evolution: no matter what you choose for your killing method, it will find a way not to be killed. Yet people from various companies were standing up at American Chemical Society meetings and saying, ‘Insects should not develop resistance to pyrethroids.’ I don’t know,” she says. “I don’t understand it at all.”

  When evolutionists study these worldwide resistance movements, they see four classes of adaptations arising, because an insect under attack has four possible routes to survival.

  First, it can simply dodge. Strains of malarial mosquitoes in Africa used to fly into a hut, sting someone, and then land on the hut wall to digest their meals. In the 1950s and 1960s health workers began spraying hut walls with DDT. Unfortunately in every village there were always a few mosquitoes that would fly in through the window, bite, and fly right back out. Millions of mosquitoes died, but these few survived and multiplied. Within a short time almost all of the mosquitoes in the villages were hit-and-run mosquitoes.

  Second, if an insect cannot dodge, it can evolve a way to keep the poison from getting under its cuticle. Some diamondback moths, if they land on a leaf that is tainted with pyrethroids, will fly off and le
ave their poisoned legs behind, an adaptive trick known as “leg-drop.”

  Third, if the insect can’t keep the poison out, it may evolve an antidote. A mosquito species called Culex pipiens can now survive massive doses of organophosphate insecticides. The mosquitoes actually digest the poison, using a suite of enzymes known as esterases. The genes that make these esterases are known as alleles B1 and B2. Many strains of Culex pipiens now carry as many as 250 copies of the B1 allele and 60 copies of B2.

  Because these genes are virtually identical, letter by letter, from continent to continent, it seems likely that they come from a single lucky mosquito. The mutant, the founder of this particular resistance movement, is thought to have lived in the 1960s, somewhere in Africa or Asia. Its descendants apparently hitched rides around the world in airplanes. The genes first appeared in Californian mosquitoes in 1984, in Italian mosquitoes in 1985, and in French mosquitoes in 1986.

  Finally, if the insect can’t evolve an antidote, it can sometimes find an internal dodge. The poison has a target somewhere inside the insect’s body. The insect can shrink this target, or move it, or lose it. Of the four types of adaptations, the four survival strategies, this is the hardest for evolution to bring off—but Taylor thinks this is how Heliothis is evolving now.

  “It always seems amazing to me that evolutionists pay so little attention to this kind of thing,” says Taylor. “And that cotton growers are having to deal with these pests in the very states whose legislatures are so hostile to the theory of evolution. Because it is evolution itself they are struggling against in their fields each season. These people are trying to ban the teaching of evolution while their own cotton crops are failing because of evolution. How can you be a Creationist farmer any more?”

  Heliothis can evolve resistance to pyrethroids in the course of a single growing season. In Arkansas in May 1987 only about 6 percent of the moths survived a certain fixed dose of the poison. But by that September, several moth generations later, 61 percent survived that same dose. The same rapid evolution has been observed in cotton fields in Louisiana, Oklahoma, Texas, and Mississippi.

  Years ago, when DDT resistance first appeared, geneticists studied the problem in the laboratory with house flies. Flies that survived doses of DDT often carried a certain mutant gene on the third chromosome, a mutant that came to be called kdr, for knockdown resistance. This single gene conferred resistance to DDT and all its variants.

  Today, every postmodern, well-equipped house fly carries not only kdr but also a mutant gene called pen, which reduces its uptake of insecticides. On the fly’s fourth chromosome it carries a mutant gene called dld-r, which gives it resistance to dieldrin and dieldrin’s family of poisons. On its second chromosome it carries a mutant gene known as AChE-R, which protects it from organophosphates and carbamates.

  Flies were astonishingly quick to evolve resistance to pyrethroids, and many investigators think they coped so well because they had already evolved in the right direction with DDT. The same kdr that fought DDT seems to have fought pyrethroids too. If a lucky fly’s parents both carry kdr, so that it inherits one copy from the mother and one copy from the father, it will often display one-thousand-fold resistance to pyrethroids.

  According to current thinking, DDT and pyrethroids both attack the same target in the fly: microscopic doorways in the membranes of the fly’s nerve cells. These doorways, sodium channels, open and close to allow nerve signals to pass through the cell. Both DDT and pyrethroids are thought to jam the channels open, triggering repetitive, uncontrolled discharges in the nerve cells. If enough of the channels get locked open, a fly goes into convulsions, then paralysis, and dies.

  The structure of the sodium channel is almost identical in animals as far apart on the evolutionary tree as flies, eels, rats, and human beings. This suggests that the structure evolved far back in evolutionary time, before the split in the tree between invertebrates and vertebrates. In the sodium channel, then, the poison is attacking a structure that is old, vital, and universally fixed in its design throughout the animal kingdom. One would think it would be extremely hard for a fly to change such a venerable design. But flies have done just that. They have modified the genes that make the channels in a way that somehow saves the flies from the jamming action of the poison.

  The sodium channel gene has been completely sequenced in Drosophila melanogaster. That is, all of the invisible characters that make up the gene have been deciphered and published. So Taylor and his advisor, Marty Kreitman, decided, on a hunch, to go into the DNA of the moth and look for the same gene. Although the Heliothis genome is unusually big for an insect—it is bigger than a chicken’s, approaching the size of a human being’s, a billion letters long—Taylor knew exactly how to go about finding the gene. With the new molecular techniques the procedure is reasonably easy to do.

  The Drosophila gene goes ATCGAGAAGTACTTCGTGT … and so on. Taylor went to a small machine along the wall of the laboratory, a DNA synthesizer, which is standard equipment for a molecular evolutionist. Standing at this synthesizer, as nonchalantly as if he were typing on a keyboard, he instructed the machine to assemble the matching sequence of letters: a fragment of artificial DNA. Then he ground up bits and pieces of Heliothis moths in a mortar and pestle, extracted the moths’ DNA, and mixed in the artificial DNA.

  If the moth did carry the same gene as the fly, Taylor’s DNA fragment would find it, and bind to it. The small strand of artificial DNA would stick to the long strand of moth DNA. To see if they did stick together, he bathed all of the DNA in a special enzyme solution, which chopped the strands into pieces, and he sifted through the pieces.

  (“It’s very robust stuff, DNA,” Taylor says. “You can do all this grinding and it won’t break. The only risks to it are from enzymes.”)

  After months of work, Taylor found a fragment in the genome of the moth that matched part of the gene in the fly. The moth gene went ATCGAGAAGTACTTCGTGT … and so on for 184 of Darwin’s invisible characters. Almost two hundred letters, and they differed by only a single letter between Heliothis and Drosophila. The moth carries almost exactly the same gene as the fly.

  Now Taylor is searching through the moth’s sodium channel gene for changes that might protect the moth from pyrethroids. Which letters have flipped along the length of the DNA, and saved the day for Heliothis? This part of the search is much more laborious. It may take as little as a single letter-flip, a single point substitution, as it is called, to make the moth resist the poison. And the whole gene consists of many thousands of letters.

  Yet the pesticide manufacturers once thought they would wipe out pests once and for all with pyrethroids. “People don’t like to have their categories threatened,” says Taylor. “They like to think, That’s a moth, and That’s a fly. Fixed categories. They don’t like to think of lots of hybridizing and change all the time in every line of moths and flies, lots of evolution in action all the time around them.

  “Even people who think they understand Darwin tend not to think about this, because they are schooled in Darwin’s gradualism.

  “It is hard enough to control pests even if we know what is going on. But you can’t control them if you don’t realize the target you are aiming at can move.”

  BECAUSE WE DO not think this way, we make the same tactical errors again and again. Resistance movements are not only out in the cotton fields. They are also closer to home. During the past fifty years while we have been throwing poisons at the pests in our fields, we have also been throwing larger and larger quantities of chemicals at the pests within our own bodies. Here too scientists are now watching evolution in action.

  Western hospitals started to use antibiotics regularly in the 1950s, and resistance appeared within a year or two. One out of three patients in every Western hospital is now on antibiotics, and antibiotic resistance is increasing so rapidly that many physicians are calling it a global epidemic.

  This kind of resistance tends to follow the same cycle as pesticide
resistance: big companies, big medicine, blanket treatment, followed by almost immediate disappointment.

  “It’s generally the case that these chemical companies are not familiar with evolution,” says Martin Taylor.

  In the U.S. the Centers for Disease Control and Prevention (C.D.C.P.) in Atlanta has instituted a national surveillance for drug resistance. “When these new drug-resistance strains become endemic in hospitals,” one doctor told the editor of Science recently, “you will be safer staying home than going to a hospital unless you have a truly dread disease.”

  It is easy to start a resistance movement in the most common bacteria in the human gut, E. coli. First one establishes a colony of E. coli in a Petri dish. The bacteria multiply so rapidly that a single microscopic cell can grow into a visible pile of ten million E. coli between morning and mid-afternoon. To the eye, ten million E. coli look like a tiny heap of salt.

  Next, one doses the colony with an antibiotic. As fast as it grew, the colony disappears. Only a few cells in the colony have survived—the two or three cells that carry a rare resistance gene for that antibiotic. These several survivors multiply and pass their successful gene to their descendants. Soon there is a new colony in the dish, a colony in which virtually every member cell is resistant to the antibiotic.

  “Darwin would have loved to watch that simple experiment,” says one molecular evolutionist. “That’s exactly what he said natural selection is. And it can happen in a day or two.”

  Bruce Levin, a microbiologist who is now at Emory University, in Atlanta, once teamed up with several colleagues to watch the evolution of E. coli in his own gut. Every few days when he went to the john he would take a sample. (A single wipe of toilet paper comes away with as many as two trillion individuals of the Bacteroides species, twenty billion individual enterobacteria, and dozens of other species that have never been named by science.)