Jonathan Weiner
The
male guppies wear black, red, blue, yellow, green, and iridescent spots in
varying sizes, shapes, hues, and combinations. In fact their spots vary so much
that they are like fingerprints: no two guppies are alike. These
spots, like the beaks of Darwin’s finches, are heritable. Although the exact
placement and arrangement of spots is unique, each guppy inherits its particular
palette of colors, and also the general size and brightness of the ensemble,
from its parents. The spots only show up on the males (they can be made to
appear on the female guppies with testosterone treatments). Like
minute variations in the beaks of finches, the spots on a guppy are the sorts of
details that one might imagine are beneath the notice of natural selection.
Nature may scrutinize the slightest variation, but there are some things even
Darwin’s process cannot see. Design could not possibly govern a thing so
small. In
the 1970s, while Peter and Rosemary Grant were watching the finches of the
Galapagos, Endler began watching the guppies of Venezuela’s Paria Peninsula,
and Trinidad’s Northern Range. There the streams run down the mountains
roughly parallel, as if in a series of vertical stripes. The streams are clear,
swift, and clean, deeply shaded by tropical evergreens and punctuated by
waterfalls. Their beds are lined with brilliant, many-colored gravel, much like
the floors of the fish tanks in the pet stores. It
is obvious to anyone who has ever tried to watch a school of these guppies
against the parti-colored sands and pebbles of a streambed that the spots are
excellent camouflage. In fact you could watch one of these clear streams for
quite a while before you noticed the guppies at all, because they tend to swim
close to the gravel while the sun is out. The
fish need this camouflage because they have seven enemies: six species of fish
and one freshwater prawn. All seven of these enemies hunt guppies from dawn till
dusk. The most dangerous is Crenicichla alta, a cichlid fish, which eats
about three guppies an hour; the least dangerous is Rivulus
hardi, which eats one guppy in about five hours. Endler
found guppies and at least a few of their enemies in almost every section of
almost every stream, from the headwaters near the summit of each mountain to the
plains and plantations below. Neither the guppies nor the guppy eaters can swim
up a waterfall, and the population of each section of stream tends to stay put.
(Sometimes a few fish get swept downstream, but none of them can get back up.) High
up near the headwaters of each stream, the only enemy the guppies have is the
comparatively mild-mannered Rivulus
hartii. But moving downstream, section by section, the population of guppies
lives and dies in the company of more and more of its enemies, until down near
the base of each mountain, the stream is loaded with all seven of the guppy
eaters. So a graph of risk and danger runs with the current. For the guppies,
the higher in the stream, the lower the risk; and the lower in the stream, the
higher the risk. In stream after stream the intensity of natural selection is
graduated in the same way: gentle pressure among the guppies at the top, violent
pressure among the guppies at the bottom. Endler
saw that the streams would make a wonderful natural laboratory for the study of
natural selection. He developed standardized methods of measuring guppy spots,
as careful and ritualized as the Grants’ methods with Darwin’s finches. He
learned to anesthetize and photograph each guppy he caught. (Like Darwin’s
finches, the guppies have met very few human beings, so they are easy to catch.)
From the photographs he recorded the color and position of each spot of each and
every male guppy, dividing each guppy into dozens of sectors to make a
standardized guppy map that is easy to read, to tally, and to enter into a
computer. 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 Galapagos.
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 farcarrying 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 out-reproduced 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 Galipagos. 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 redblind
– 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 spots, 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 bartii, 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 Galapagos
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.” |