When Endler analyzed his surveys he discovered a pattern. The spots on each guppy look chaotic, but the spots of all of the populations of guppies in a stream, taken together, from the headwaters down to the base, have a kind of order. The spots on each population of guppies bear a simple relationship to the number of guppy eaters in their part of the stream. The more numerous the guppies’ enemies, the smaller and fainter the guppies’ spots. The fewer their enemies, the larger and brighter their spots.
The lucky guppies in the headwaters wear sporty coats of many colors, and each color is represented by big clownish splotches. Many of their spots are blue. These blue spots are iridescent, like the Day-Glo patches that cyclists wear; they flash as the fish swim, and they can be seen a great distance through the clear water.
Meanwhile the guppies downstream tend to wear conservative pin dots of black and red. The spots are almost vanishingly small. Most wear only a tiny amount of blue.
Endler looked at his data from stream after stream. In every one of them, the size and number of spots ran steeply downhill. And Endler drew the same sort of conclusion that Lack did when he noticed the patterns of beaks in the Galápagos. Endler thought he could see the hand of natural selection at work among the guppies. The greater the pressure from their predators, the more camouflage they wear; the less the pressure, the slighter the camouflage.
Of course, that interpretation did not explain why guppies are colorful at all. If they are in some danger everywhere, even in the headwaters, then why doesn’t natural selection favor the best-camouflaged guppy everywhere?
The answer is that a male guppy has more to do in life than merely survive. It also has to mate. To survive it has to hide among the colored gravel at the bottom of its stream and among the other guppies of its school. But to mate it has to stand out from the gravel and stand out from the school. It has to elude the eyes of the cichlid or the prawn while catching the eyes of the female guppy.
The gaudier the male, the better his sex life. He is more popular among females, and he gets many chances to pass on his gaudy genes—as long as he lives. In a quiet spot near the headwaters of the stream his life is likely to be long and happy and he may father innumerable gaudy children. But in a spot near the base of the stream he may not father a single guppy before he vanishes down the gullet of a cichlid.
The quieter the colors of a male, the less luck he has in courting females. On the other hand he is likely to have more time to try, because the less he stands out among his own kind, the less he stands out among his enemies.
This is not just a problem for Trinidadian guppies. Wherever males court females, or females court males, whether the signals are a bright splash of color, as in guppies or red-winged blackbirds, or loud far-carrying songs, as in frogs and crickets, their broadcasts are always in danger of being intercepted by the enemy. Strong colors or loud calls can attract a mate from one side and a predator from the other. Every bullfrog calling in the night is in the dangerous spot of Romeo calling out beneath the balcony of the house of Capulet. A few species have found ways to finesse this problem. Among fish, some wrasses change color only very briefly, to flash a sexual signal in dangerous waters—the equivalent of a sexy whisper, pssst!
Looking at his guppy data, Endler read into them a struggle between two contending forces. Everywhere in the stream the gaudier fish produce gaudier young—pushing the next generation toward loud colors and self-advertisement. And everywhere in the stream the quieter fish produce quieter young, pushing the next generation toward modesty. In the relative safety of the headwaters the gaudier guppies live long enough to win many females before they are eaten, so the population evolves in the direction of greater and greater gaudiness, and almost every male wears a coat of many colors. But in the dangerous waters at the base of the mountain the gaudy guppies live such a short time that they are outreproduced by the modest guppies. So the whole population evolves in the direction of greater and greater drabness. Males court females at distances of 2 to 4 centimeters, and from there the little spots are visible; but from farther away the males blend into the gravel. So the small-spotted guppies can blend into the background in the eyes of their predators, Endler says, “yet still be visible and stimulating to females.”
When Endler first began studying the guppy streams, he was in the same position as David Lack after the Galápagos. Endler could see patterns that strongly suggested the forces of selection at work. He did not actually see selection shaping the patterns, but the closer he looked the more he was sure that the hand that shaped the patterns really was the hand of natural selection. Within the broad patterns he kept finding curious subsidiary patterns. For instance in a few of the headwaters there are prawns. In these headwaters the guppies favor red spots. This red shift makes sense because although guppies and other fish see more or less the same colors that humans do, prawns and shrimp are red-blind—they cannot see the last band in our rainbows. So in those particular headwaters, male guppies with big red spots can show off to female guppies while hiding from the prawns.
Back in the 1940s, Lack made his selectionist argument about Darwin’s finches without trying to measure it in the field to see if he was right. But Endler went the extra step: he decided to test the predictions of his theory by trying to detect these processes in action. He built ten ponds in a greenhouse at Princeton University. Four of the ponds were about as wide, deep, and long as the low-water territories of Crenicichla alta. The other six ponds were about the size of the headwater streams with the comparatively mild-mannered Rivulus hartii. Endler put black, white, green, blue, red, and yellow gravel in the bottom of his artificial ponds and pumped water through them to give them a current, like the streams in the wild.
Meanwhile, Endler collected guppies from up and down a dozen streams in Trinidad and Venezuela. In some places he took guppies that lived with just one predator, in some places guppies that lived with two predators, and so on up to the maximum, seven. He wanted stocks of wild guppies that had evolved under the whole spectrum of guppy menace, that were coping in the wild with every level of danger. He bred each stock in a separate aquarium.
When the artificial streams were ready for his guppies, Endler took five pairs at random from each stock and put them all together into two of his ponds to let them breed and mingle and get used to their new homes. Guppies can give birth at the age of five or six weeks, and a female guppy can spawn a lot of baby guppies, so it did not take long for the populations to double. After a month he took guppies from those two ponds and used them to stock two more ponds. A month after that, he had enough guppies to seed each of his ten ponds with two hundred fish per pond.
What he had done, in effect, was to shuffle and reshuffle the deck. He now had a highly heterogeneous assortment of guppies. They had all kinds of spots, and their spots were completely random with respect to the gravel at the bottom of their homes.
He let these guppies breed in their new streambeds for months. Then he added a few of their natural enemies to the streams, according to a careful plan. The evolutionary experiment had begun.
According to his prediction, the guppies should now evolve rapidly. The guppies in each tank should begin to look more like guppies that live with that same set of predators in the wild, they should come to look more like the gravel in their particular stream, and those in the most dangerous tanks should come to mimic the gravel more closely than those in the safer tanks.
After five months, Endler took his first census. He drained each stream, counting every male’s spots and noting their position, anesthetizing them, photographing them, as he had done in the wild, and then starting up the stream again. Nine months later he took a second census. By that time nine or ten generations had passed in the lives of his guppies.
Some of the guppies were safe, with no enemies. These guppies got gaudier between the foundation of the colony and the first census, and they got gaudier still by the time of the second census. The males evolved more and more s
pots, bigger and bigger spots, wilder and wilder palettes of spots.
Meanwhile males in tanks with the dangerous cichlids evolved fewer and fewer, smaller and smaller spots. They were still visible to females, but they got less and less visible to cichlids, who strike from 20 to 40 centimeters away. These guppies mostly dropped the blue and the iridescent spots, their Day-Glo patches, just like guppies that live with cichlids in the wild. Endler measured these differences as meticulously as the Grants measure finch beaks. “Spot height, spot area, total area, and total spot area relative to body area also decreased significantly with increased predation intensity,” he reports. The fish themselves changed size, too. Full-grown guppies in the dangerous tanks were smaller, while mature guppies in the safe waters were larger—again, just as in the wild.
Each tank had a different bottom: different mixes of gravel colors and different gravel sizes. In the pools with no predators the guppies did not change their spots to match the gravel—the opposite. Their spots evolved to be smaller than the big gravel and larger than the small gravel, making the males easier and easier to see, like chameleons in reverse. They carried more iridescent spots, and a wider palette of colors per fish, and generation after generation they looked less and less like their background, all of which is just what we would expect if they were competing for attention. Sexual selection was operating to make males as different from the gravel bottom as possible.
If only one force or the other had been operating, just natural selection or just sexual selection, the guppies would not have evolved in this remarkable way. Without natural selection all of the fish would have gotten gaudier. Without sexual selection none of them would have gotten gaudier. But the safe ones did get much more colorful, adding, in particular, blue spots. It is probably not a coincidence that guppies’ retinas are exquisitely sensitive to blue. Almost all males carry some blue somewhere, even in the most dangerous waters—it may be a sine qua non of courtship.
The fish had evolved in Endler’s greenhouse until they replicated the patterns that they display in nature, and they had done so in a very short time. Of course, Endler’s streams were artificial. He had not seen natural selection in the wild. A skeptic could still argue that Endler was wrong about his explanation for the pattern in the wild. So Endler figured out a way to run the same sort of evolutionary experiment in nature.
Early in his fieldwork he had found a Trinidadian stream that contained the guppy eater Rivulus hartii, but no guppies. About 2 kilometers away was a second stream that contained both guppy eaters and guppies. Endler took a random sample of about two hundred guppies from one of the high-danger zones in the second river. He measured each and every one, as usual, and then he transferred them to the safe place in the first river. He took a sample of their descendants more than a year later, after a passage of fifteen generations.
The males in the safe stream were now much gaudier than their immediate ancestors, who were still living in the stream next door and coping with many enemies. The immigrant males wore bigger spots, and more of them, and each male sported a wider assortment of colors. Natural selection had acted just as predicted. Evolution had run as fast in the wild as in the greenhouse.
Everywhere in those streams, daily and hourly, natural selection in the form of cichlids and prawns is not just metaphorically but literally scrutinizing the male guppies. The result of enemy predations on each generation keeps pushing the males to blend in with the stream bottom. At the same time, daily and hourly, sexual selection in the form of female guppies is scrutinizing those same males. The result of their choices is that generation after generation of males is pushed to stand out.
Now it is clear why there is such virtually infinite range of variation in the way each individual male guppy is spotted. Many different random patterns of splotches will be equally good camouflage, because the streambed patterns are random too. It would not help the guppies to sport the same pattern as all the others, and in fact it would hurt them. If the guppy males all looked alike, their enemies could develop a search image—an inner template. They would search for that pattern, as we search for the face of a friend in a crowd. The rare misfit would have a great advantage. Meanwhile the females would go for the unusual males, too, and that would drive more and more diversity of patterns. So in this respect natural selection and sexual selection cease to oppose each other and push in the same direction: toward almost infinite diversity.
We see here an example of what Darwin saw in the wide world. He understood that his simple process can lead to the most bewildering and chaotic-looking diversification and variety—but underneath, the driver is as simple and plain and commonsense as ever, “small consequences of one general law leading to the advancement of all organic beings,—namely, multiply, vary, let the strongest live and the weakest die.” The guppy experiments suggested to Endler what Darwin’s finches were suggesting at about the same time to the Galápagos finch watchers: that natural selection can be swift and sure. The process is flowing along, all around us, much faster than Darwin ever dreamed.
Endler’s study is leading him into deeper and deeper waters. He now suspects that the guppies’ spots, their mating habits, and their color vision are all evolving simultaneously, with change in any one of these factors driving change in all the others. To measure variations in the guppies’ retinas, Endler is collaborating with physiologists. These “hard science” types often remind him how “soft” the science of evolution is perceived to be by the outside world—even by biologists. “I was talking with someone in vision physiology the other day,” Endler says, “and he told me, ‘Wow, I had no idea that the subject was so rigorous. I had no idea that you actually did experiments.’
“We have a serious public-relations problem,” Endler says. “People don’t realize this is real science.”
AS TREVOR PRICE’S WATCH DREW to a close, the members of the Finch Unit had logged almost a decade on Daphne Major. When they looked back, they saw this: in 1977, evolution by natural selection had made the birds bigger. In the wet season of 1978, evolution by sexual selection made them even bigger. Then one or the other or both pressures acting together made the birds on the island bigger yet in ’79, ’80, ’81, and ’82. The sum total of all the varied pressures of life on Daphne Major seemed to be pushing the finches in a single direction. At this rate, the birds would go on shooting into the future like a searchlight, growing larger and larger.
So the results of the finch watch presented a paradox. If there is strong selection for large size, year after year, why don’t all the small finches turn into large ones? Why is there a small ground finch, a medium ground finch, and a large ground finch? Why doesn’t every small become a medium and every medium a large? Or were they doing just that—had the course of evolution taken off in a new direction on this island just as the Grants and their students arrived to watch?
It did not seem likely that the trend would keep going like this. Surely the Grants had not begun to watch just at the moment that Darwin’s finches were in the middle of a radical transformation. That would have been like training a new telescope on a distant star and watching it explode into a supernova before your eyes.
Something had to happen soon. The trend had to break. Some force had to whirl down upon the birds and force them back in the other direction.
Trevor Price was positive that with the next heavy wet season he would see something new. In the next solid rain he would detect the pull to oppose the push, the event that would reverse the trend he had seen in the run of dry years.
In 1980 Trevor had two bouts of rain. But that was not enough. It did not trigger much breeding. He needed just one good breeding bout.
Price got as desperate for rain as Boag had been on the watch before him. He paced the island for months on end, waiting for rain. Then he’d come into town—the fishing village of Puerto Ayora on the island of Santa Cruz—half-crazy because it hadn’t rained. He’d be ragtag and barefoot, wearing an old striped shirt, c
hecked pants, a beard that had never known a comb. He had a wild and friendly manner. He spoke atrocious Spanish with an impossibly strong British accent. He would hang out in town for months, making friends and having a good time. Everyone in Puerto Ayora knew him.
But he suffered through each drought convinced in his bones that in one good bout of rain he could make the discovery of his career. The finch watchers posted on the other islands of the archipelago were all rooting for him.
“That’s the difference between field biology and physics,” says one of Trevor’s friends, philosophically. “You can be stuck waiting for rain. You’ve got a beautifully planned research program, and all you need is the rain.”
During Trevor’s last year, 1981, he brought a new field assistant to Daphne Major, a Turkish mathematician named Ayse Unal. She put up with him mooning around for months waiting for the rain. And when rain came at last, in March, she watched him dance in it for two solid hours praising the heavens, a dervish of tangled hair and beard and ripped clothes, hollering into the rain.
But even then it was too little too late. Not many finches bred. Trevor still thinks about that last rain in the small hours, the iguana hours, the hours of what-might-have-been. If only that bout of rain had come in February, or January. If only his watch had lasted just one more year. “It would have been an amazing thesis then.” (“It was an amazing thesis anyway,” says Peter Grant.)
But it was time for another changing of the guard. Lisle Gibbs, a Canadian graduate student of Peter Grant’s, took the next watch. He went down in December 1981 with a field assistant, to be sure to be there when it started to rain. They sat there, two men on a desert island, and waited half a year for the gray clouds to shower on them. Some rain fell—but not enough. “It was like waiting for Godot,” Gibbs says now.
The Beak of the Finch Page 12