Guppies and the Empirical Study of Adaptation

Transcription

Guppies and the Empirical Study
of Adaptation
DAVID REZNICK
T

hroughout On the Origin of Species, Charles Darwin emphasized that evolution is so slow as to be essentially invisible, unless one looks at it with the
benefit of the passage of a long interval of time. The fossil record is an excellent
place to look for evolution because the animals preserved in fossil sequences
afford images of life over vast intervals of time that far exceed our own lifespans.
In rare circumstances, the fossil record reveals fairly continuous sequences
many thousands of years long that, in turn, reveal details of change in those few
species that are often preserved as fossils. We also sometimes find the remains
of organisms that show an affinity with what are now two very different groups
of organisms, such as the early tetrapods that served to document the relationship between fish and amphibians. For Darwin, the Galápagos Islands were also
an excellent place to see evolution in action because they are of volcanic origin
and much younger than the South American continent. Those islands emerged
from the depths of the ocean as new, lifeless land, and then were colonized by
species from the mainland. The species that are now found on the Galápagos Islands and nowhere else are likely to have evolved after the islands were
formed.
We have now developed new ways in which to study evolution, and we have
found that it is far more amenable to direct observation than Darwin could
have imagined. Here I will recount my own research program, in which it has
been possible to study the process of evolution with experiments done on natural populations, to test predictions derived from evolutionary theory, and to
quantify the rate of evolution.
I study guppies (Poecilia reticulata), which are known to most of us as small,
colorful, hardy and prolific fish that are widely available in pet stores. Natural populations of guppies share all of these attributes, which makes them ideal
subjects for scientific study. They are found in northeastern South America
and on some Caribbean islands. The females are a uniform tan color, while
the males have a diversity of colorful spots and stripes. My research is divided
between studies of natural populations on the island of Trinidad and laboratory
research at the University of California, Riverside. The guppies that I study are
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r e z n i c k | Guppies and the Empirical Study of Adaptation
found in small, scattered populations living in clear mountain streams on the
island of Trinidad.
When you keep guppies in the laboratory, you can see they are a wonderful
example of what Darwin argued is a property of all living things. All organisms
have the capacity to fuel a population explosion, unless their numbers are regulated in some way. My laboratory contains 800 aquaria and thousands of guppies. Guppies live up to four years, and female guppies can produce dozens of
live-born babies every three to four weeks, so there are hundreds to thousands
of baby guppies born every day. Each female baby guppy can have babies of
her own after only 12 weeks. Because only a few fish die per day, the population could grow to many millions of guppies within a year, if only there were a
place to keep them all. Their constantly burgeoning numbers are a testament to
the way Darwin capitalized on Robert Thomas Malthus’s insight, which is that
all organisms have the capacity for exponential population growth. This capacity for rapid population growth was the source of Darwin’s preoccupation with
the “struggle for existence,” which was the title of the third chapter of On the
Origin of Species. There, Darwin argued that, even though all organisms have
the capacity to sustain explosive population growth, we rarely see this happen
because their numbers are held in check, mostly by the other organisms with
which they interact. It is these interactions with other organisms that shape how
species evolve; those few who survive the “struggle for existence” to reproduce
successfully do so because they have special attributes that they transmit to their
offspring. In fact, guppies are sometimes rare fish in their native habitat, in spite
of their rapid development and their capacity to produce many babies. In my
work, I study how predators regulate guppy populations and, in turn, how guppies have evolved in response to predation.
NATURAL SELECTION AS THE CAUSE OF
EVOLUTION
My goal at the outset of my research career in the mid-1970s was to study the
process of natural selection and to test experimentally various aspects of the
theory of evolution in a natural setting. I began at a time when there was abundant precedent for doing selection experiments in the laboratory on such model
organisms as fruit flies, but our knowledge about evolution in the natural world
relied more on indirect inferences. One such inference involved a famous species of moths (Biston betularia) that could be either black or peppered; “peppered” means that they were a patchy mix of black, gray, and white. The black
form was a rare collector’s item in the 1850s, but it became more and more
abundant over time, until nearly all that you could find in and around some cities were black moths. This change took about 80 years to complete. The history
n at u r a l s e l e c t i o n a s t h e c au s e o f e v o l u t i o n of the change could be seen in retrospect in the dated collections of thousands
of moths accumulated by moth fanciers. You might wonder that such a person
as a moth fancier could ever exist, but there were ample numbers of them in
Victorian England. They were among Charles Darwin’s audience.
This change in moth populations over time could be thought of as evolution in action because genes caused the moths to be either black or peppered.
It was a good guess that the shift from a predominance of peppered moths to a
predominance of black moths was caused by the industrialization of some parts
of England, since it was around the cities where the black moths became common. One idea was that air pollution killed the lichens that normally coat the
trunks and branches of trees, turning them from a mottled gray and black to
solid black. Moths fly at night, but they spend the day resting on tree surfaces.
Peppered moths were hard to see when they came to rest on lichens, but they
were easily seen when they came to rest on a blackened tree trunk. The reverse
was true for the black moths. Birds eat moths during the day, while they are at
rest on tree trunks and branches, so perhaps the birds were more successful in
seeing and then eating the ones that did not blend well with their background.
In cities, the moths that are easy to see are the peppered ones, since the tree
trunks are dark. In the countryside, the reverse is true. This idea was tested first
by H. Kettlewell in the 1950s. Recently, Kettlewell’s work has been the subject
of a biography that called its validity into question. Industrial melanism then
became a favorite of advocates of creation science as an example of our being
too willing to accept questionable results as evidence for evolution. What has
been missing in those counterarguments is that others have reevaluated all features of Kettlewell’s work again and again over the decades that followed. It is
certain that selective predation is at least partially responsible for the change
that occurred between 1850 and the 1920s.
The moth story is a bona fide study of evolution by natural selection. But I
was after something different. I wanted to find some modern manifestation of
evolutionary theory that made a prediction about how organisms should evolve
in response to some feature of their environment. Then I wanted to do an
experiment on a natural population that would allow me to test that prediction.
Then I wanted to sit and watch evolution happen to see if the prediction would
be fulfilled. This sort of approach had not been applied to the study of evolution
in nature because we all thought, as Darwin had originally thought and said
over and over again in the Origin, that evolution was a slow process that could
be perceived only after the passage of a long interval of time. It could be seen
only in retrospect, such as in the dated collections of moths that accumulated
over decades. Yet, in spite of its slow pace, evolution can cause big changes—so
big that it could account for the origin of all of the diversity of life forms that
we see in the world today. The catch is that the Earth is billions of years old
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and the process of evolution had this enormous interval of time to work with.
If you have the preconceived notion that evolution is too slow to see it happen
in your lifetime, then there is little incentive to look for it. Relying on studying
the changes that have already happened, as in the case of the peppered moth, is
a safer route. The difference, though, is that doing an experiment with appropriate controls is the only way to test a hypothesis formally. It also yields the
potential of defining cause-and-effect relationships more precisely than would
be possible by trying to reconstruct the history of past events. Another virtue of
doing experiments is that they provide the opportunity to measure the strength
of natural selection and the rate at which evolution occurs. I was inspired by
the fact that it had been possible to study evolution in laboratory experiments.
Those prior studies, combined with what I had learned in my course in population genetics, suggested that evolution should be readily observable in nature,
so long as selection was strong enough.
This is the logic that brought me to guppies. I rarely know where my ideas
come from for a particular research project; they are usually the product of
some slow churning of facts that metamorphoses over time into a research
plan. The origin of my guppy research was different. I can pinpoint the day and
hour when I decided on this research program.
In 1977, I had been studying a related fish, the mosquitofish (Gambusia
affinis), for two years and had been thinking about a topic called “life-history evolution,” which I define below. But driving across the Walt Whitman
Bridge from Philadelphia to New Jersey and smelling the sickening yeasty odor
from a brewery on the New Jersey side of the bridge while en route to mosquitofish habitat in Cape May County, New Jersey, did not meet my romantic
vision of fieldwork. Then I attended a lecture given by John Endler, who spoke
about guppies on the island of Trinidad, their predators, and how the predators selected for changes in the coloration of the males. What Endler described
was a perfect fit for my desire to test theories of life-history evolution in nature.
Predators could clearly select for changes in guppies. Endler’s work—even by
1977, when I saw his seminar—showed that predators could cause a big effect
in a short time. I knew that guppies were easy fish to work with because I used
to keep them as pets. They were also perfect because working on them could be
my ticket to the tropics, which was one of my ulterior motives for going into
research as opposed to going to veterinary school. I had dreamt of the tropics since I was a youngster watching National Geographic shows on television,
while ice built up on the windows outside during the northeastern winters.
Guppies could make that dream come true.
the setting
THE SETTING
The key to guppies in Trinidad and the experimental study of evolution is that
the Northern Range Mountains, which form the northern edge of the island,
are mostly uplifted limestone and soft sediments. Limestone dissolves and soft
sediments erode in the heavy tropical rainfall, forming steep, forested ravines
filled with clear running rivers that have many waterfalls. Rivers are like trees,
being large and wide at the base, then dividing into progressively smaller
branches as you move up into the headwater streams in the mountains. There
are dozens of species of fish found downstream, but each set of waterfalls is a
barrier to some of them. The headwater streams may contain only a single fish
species, or perhaps none at all.
Guppies are found in a wider range of habitats than most fish. They can be
found in the large, lowland rivers and all the way up into some of the smallest headwater streams. In the larger, lowland rivers, they live with many species of predators. Many of those predators are relatively large fish that eat large
guppies. Guppies can be rare in such big rivers. They lead a fugitive existence,
traveling in schools, being eaten quickly when they appear in open water, but
multiplying quickly when they find a refuge, such as among the submerged
branches of a fallen tree, where they are relatively safe from predators. In the
headwater streams, there is usually only one other species of fish present. This
other fish is the killifish Rivulus hartii. It is small and will eat almost anything,
including guppies. Because it is a small fish, it tends to eat small guppies.
Why are the guppies and the killifish, but not other fish, found in the headwaters? The killifish are the ecological equivalent of salamanders. On rainy
nights, they will hop out of the stream and move into the forest. Some have
argued that they can feed out of water. They penetrate aquatic habitats wherever they can be found, including water-filled tire tracks and depressions in the
forest that are not connected to any permanent water and that fill with water
only during the rainy season. Guppies are tied to water, but they are preadapted
for dispersal. A single adult female guppy can establish a new population
because she is able to store sperm cells in her body and can produce many litters
without ever again encountering another adult male guppy. Female guppies
mate promiscuously, so a single female carries the sperm of multiple males and
can initiate a new population with a modicum of genetic diversity. I have found
guppies in small pools on the margins of waterfalls, where there was a secondary channel that filled only when the river was flooding during the rainy season. Guppies can persist and reproduce in such marginal habitats, which makes
them different from any other species found below the waterfalls. I imagine that
it may be possible, on very rare occasions, for guppies to cross such barriers in
a stepping-stone fashion as they move up such side channels over the course of
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F i g u r e 1 (a) Crenicichla alta, a key guppy predator, seen here guarding its young. The female
is in the foreground and male in the background. The babies are grazing the surface of the rock
behind the female. (b)Male (upper left) and female (lower right) guppies seen in a Trinidadian
stream. (c)Tributary to the Guanapo River. (d)Waterfalls, upstream from the one pictured on
the right. These falls are actually calcium carbonate that has precipitated on underlying rocks. (e)
Waterfall on a tributary to the Turure River.
t h e t h e o ry several rainstorms during a very rainy year. Some have speculated that kingfishers may occasionally drop a guppy after flying over a barrier. However guppies
do it, they have managed to go where no fish other than the killifish Rivulus can
go. The genetic diversity of guppy populations is greatest downstream, then it
tapers off upstream and in the tributaries, which supports the idea that they
colonize from downstream to upstream.
There are many streams draining the slopes of the Northern Range Mountains. Each stream is very similar to the others in terms of the species of fish
to be found and the way the fish communities change from downstream to
upstream. Because Trinidad is an island, the diversity of species is small relative
to what is found nearby on mainland South America. While each stream tends
to be a simple replicate of the others in species composition, there is a marked
difference between the streams that drain the north slopes of the mountains
and those that drain the south slopes, as I discuss below. If one is interested in
studying how guppies adapt to the presence or absence of predators, then each
river can be thought of as an independent experiment in which guppies evolve
when they invade headwater streams and leave their predators behind.
THE THEORY
To fulfill my goal of performing experimental studies of evolution in nature,
I needed a theory that predicts how organisms would evolve in response to a
particular type of selection, and then I had to find a natural setting in which the
theory could be applied. I found this starting point by pairing the theory of lifehistory evolution with the natural history of guppies. To explain this connection, I must first define “life history” and “fitness,” then outline the structure of
life-history theory, then show how guppies can be used to test the theory.
The “life history” of a species is a composite of all of the variables that contribute to how the species reproduces itself. The variables that I am most interested in are size at birth, age and size at maturity, and reproductive effort.
Reproductive effort is a composite of all of the investments that a parent makes
in its offspring. Because baby guppies are on their own from the moment of
birth, a female guppy’s reproductive effort is a function of how many babies she
produces in each litter, how large the babies are, and how often she reproduces.
For an animal like a bird, a mammal, or any organism that provides postnatal
care for its young, reproductive effort also includes investments in the young
that are made after the young are born. These investments include lactation in
mammals, parental feeding in birds, or any effort or risk invested in protecting
and caring for the young. For animal species that provide parental care, postbirth investments can be much larger than investments that precede birth.
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Natural selection causes the mean fitness of individuals in a population to
increase. We define fitness as the relative success of an individual in contributing offspring to the next generation. A value of 1 is the average number of
surviving offspring per individual in a population. If an individual has a value
greater than 1, this means that it has contributed more offspring than average
to the next generation. A value of less than 1 means that the individual has
contributed fewer offspring to the next generation than the population average. If there are alleles of some genes that enable some individual to have a
relative fitness greater than 1, then those alleles will increase in frequency relative to others. This concept of fitness is entirely consistent with Darwin’s presentation of how evolution by natural selection works, but I will argue below
that adding life-history theory to the mix has resulted in a fundamental shift in
how we think of fitness today versus how Darwin thought of fitness when he
conceived of his theory.
I was also interested in life-history theory because there is so much diversity
among organisms in how they propagate themselves. A human will produce
and rear only a small number of offspring over a very long lifetime and will
lavish extended care on each of them. A large ocean fish, such as a cod, will produce hundreds of thousands of small eggs every year, then cast them to the fates
of ocean tides. This diversity means that this most fundamentally important
target of evolution, how organisms contribute offspring to subsequent generations, has evolved along very different pathways in different organisms. Why
does this diversity exist? What features of the environment cause organisms
to evolve such large differences in characters so intimately related to fitness?
Before addressing this question, we must first consider how the theory works.
To understand how the theory works, you need to think of your life as being
like a pie. The pie is divided into slices that represent how you allocate your
resources. One big slice is maintenance costs, or the cost of replacing all of your
parts that are constantly wearing out or in need of repair. Skin cells, blood cells,
and the cells lining your gut are some of the parts that wear out quickly and are
constantly being replaced. Another slice of the pie is fat storage. It may be hard
for you to think of fat reserves as adaptation, but that is because so many of us
make many more fat deposits than fat withdrawals. For many organisms, food
is not always abundant, so fat is a way of storing up energy in times of plenty for
use in times when food is scarce. Another slice of the pie is for growth. Finally,
there is the slice that is devoted to reproduction. The pie is finite, so increasing the size of one slice means making another slice smaller. If the slice that is
devoted to making babies is to be larger, then it must take away from growth,
maintenance, or fat storage.
Life-history theory predicts how best to divide up the pie in the face of the
day-to-day risks of dying. Natural selection can make the size of the slice that
t h e t h e o ry is devoted to reproduction bigger or smaller by changing the age at which you
begin to have babies, how often you have them, how many you have, or how
much you devote to each of them.
Theorists have argued that the risk of mortality, such as mortality from predation, is the most important factor in shaping the diversity of the life histories
that we see in nature. If the risk of being killed by a predator is high, then the
theory predicts that natural selection will favor those individuals that devote a
larger slice of the pie to reproduction by beginning to have babies when they
are younger and by making more babies. The increase in the size of the reproduction slice makes other slices smaller. A smaller slice devoted to maintenance
can mean being at greater risk of dying in the future, either because you may
become more susceptible to disease or because your body may deteriorate more
quickly. Devoting less to fat storage may put you at greater risk in the future if
food becomes scarce. Devoting less to growth can reduce the number of babies
that you can produce in the future, since so many organisms continue to grow
throughout their lives and because bigger individuals can make more babies.
But, if the odds of living from one day to the next are low because of the constant risk of being eaten by a predator, then the benefit of producing babies
early and producing more of them is predicted to outweigh those costs. If you
are not likely to live much longer, there is little use in storing fat and little to be
gained in growing. Conversely, if predators are scarce or absent and your risk
of dying is low, then your long life expectancy shifts the balance in how best to
invest your resources. The theory predicts that natural selection will favor those
individuals who devote a smaller slice of the pie to reproduction and a bigger
slice of the pie to their own maintenance. Theory also predicts that they will
produce fewer babies and will devote more resources to each of them.
Life-history theory has given us a more general concept of fitness than Darwin did in the Origin. In the Origin, Darwin argued that natural selection favors
the evolution of whatever traits make it more likely that an individual would
survive. Those who survive longer will have higher fitness because they will
have more opportunities to reproduce and will contribute more offspring to
the next generation than will those who die young. Virtually all that Darwin
says in the Origin about life-history evolution that deviates from this “naturalselection-promotes-survival” paradigm is contained in a single paragraph. In
his Chapter III, on the “Struggle for Existence” (p. 66, Origin), he saw some
role for natural selection in shaping the number of young that are produced,
because this number varies so radically (from ones to millions) among different
types of organisms. He argued that the number of young produced is perhaps a
function of their risk of dying. If the risk of dying when young is very high, then
an organism must produce more young to compensate for this loss.
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In the modern theory of life-history evolution, fitness is gauged by a composite of survival and the successful production of offspring, rather than just survival. This composite includes tradeoffs between what an organism does now
versus what it is capable of doing in the future because it involves taking a pie
of finite size, then modifying the size of the slice that is devoted to reproduction
and, as a consequence, changing the size of the remaining three slices. According to this theory, natural selection can do seemingly counterintuitive things. It
can favor the evolution of a shorter lifespan or the production of fewer young,
provided that there are appropriate tradeoffs at other stages of the life history. I
found the added complexity of this theory attractive because it seemed flexible
enough to account for the huge diversity in lifespans that we see among organisms and in the ways in which they allocate resources to reproduction. More to
the point, this theory made predictions that could be tested in nature if the right
circumstances could be found.
The connection that I made to the theory when I applied it to guppies was
to assume that predators are a major source of death in nature, but the risk of
being eaten by a predator can vary a great deal in different places. If I were to
compare guppies from localities where they co-occur with a diversity of predators (“high-predation localities”) versus localities where they co-occur with
Rivulus (“low-predation localities”), then I could predict that those from highpredation localities would attain maturity at an earlier age and would have
higher reproductive efforts than their counterparts from low-predation localities. This prediction carries the assumption that guppies in high-predation
localities really sustain higher mortality rates than those from low-predation
localities, so it was incumbent on me to find a way to evaluate this assumption.
Doing so came later in my career.
PRELIMINARY RESEARCH
My first step was to use a method championed by Darwin, which is to let nature
do the experiment for you. There are many different streams that have populations of guppies that live with the larger, more dangerous predators, and there
are other populations of guppies found in the headwaters of the same streams
that do not live with these predators. My first goal was to compare the life histories of guppies from a series of high-predation and low-predation habitats
in different streams to see if there were consistent differences in life histories
among them. John Endler had mapped out the distributions of guppies and
their predators in his work on the effects of predators on the evolution of male
coloration. We met in Trinidad in March 1978, when I began my own research.
The study sites that John recommended spanned two adjacent, high-resolution
topographic maps of the Northern Range Mountains, so he aligned the maps
p re l i m i na ry re s e a rch on the dining-room table at the research station where we were staying and laid
a piece of notebook paper on top to trace out a map of proposed study sites for
me to use as a guide in the field. I still have that map. I rented a car, then spent
10 days collecting guppies.
Does theory accurately predict differences in the life histories of guppies that live with and without predators? I was able to do enough dissections
while still in Trinidad to see that it did. Theory predicted that guppies from
the high-predation localities would be younger at maturity and would devote
more resources to reproduction than guppies from low-predation localities.
What I found was that the guppies from high-predation localities were smaller
and presumably younger when they began to reproduce. They produced many
more babies in each litter, and the individual babies were smaller. The proportion of the body weight of the gravid female guppies that consisted of developing babies was larger. This means that they displayed differences in their life
histories that were consistent among different river drainages and also consistent with predictions from life-history theory, at least to the extent that I could
test such predictions on wild-caught fish.
This was just a beginning. It was easy to show that theory accurately predicts
differences in wild-caught guppies that live with or without predators, but do
the measurements that we make on wild-caught fish really tell us what we want
to know? Consider some of the limitations of the results so far. Female guppies
from high predation localities were smaller when they began to reproduce and
produced relatively larger packages of babies with each litter, but these variables are just indices of what I really want to know. Being smaller at maturity
may mean that females from high-predation localities are younger at maturity
than their counterparts from low-predation localities, but it is not a direct estimate of age at maturity. Life-history theory predicted the evolution of age at
maturity. Devoting more resources to making one litter of babies may mean
that the slice of the pie that females from high-predation localities devote to
reproduction is bigger than what females from low-predation localities devote
to reproduction, but this is only an index of reproductive investment rather
than a complete estimate. It lacks critical information, such as how often the
fish reproduce. Futhermore, these are animals from nature and were living in
different places and possibly experiencing different environments. One type of
locality might have warmer water temperatures, more food, or some other factor that might have been the immediate cause of the patterns that I was seeing. The differences that we see among animals from different populations in
nature could reflect genetic differences, but environmental effects could also
cause them.
To discriminate among these alternatives, I performed multigenerational
laboratory experiments that showed me that what I had seen in nature did
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Riv/Cren
R-M/Eleo
B
8
North slope
7
6
5
South slope
4
3
Embryo weight (mg)
Number of offspring
A
2
1.5
1.4
1.3
1.2
1.1
1
0.9
0.8
South slope
North slope
D
18
17
16
15
14
13
12
11
10
North slope
South slope
Cren
Eleo
Riv
Riv/Macro
Mature male size (mm)
C
Reproductive allotments (%)
12
17
16
South slope
15
North slope
14
13
Cren
Eleo
Riv
Riv/Macro
F i g u r e 2 Life-history phenotypes of wild-caught guppies from the two slopes of the Northern Range Mountains (after Reznick, Rodd, and Cardenas, 1996) (means + 1 standard error). The
communities of predators are different on the two slopes, but the contrast between high and low
predation is the same. This figure shows that the differences in life histories between high- and
low-predation sites are the same as well, regardless of the species of predators. “Cren” and “Eleo”
represent the high-predation localities on both slopes, named for the key predators found at each
site (Crenicichla alta on the south slope and Eleotris pisonis on the north slope). “Riv” and “Riv/
Macro (R-M)” are the low-predation sites on the south and north slopes, respectively. “Riv” refers
to Rivulus hartii. “Macro” refers to prawns in the genus Macrobrachium, which are found in the
north slope streams. Each data point represents the mean of five to seven localities in different
drainages. (a) “Number of offspring” per female, adjusted for female size. (b) The average dry
weight of each offspring, adjusted for its stage of development. (c) Reproductive allotment, or the
percent of total dry weight that consists of developing embryos, adjusted for the stage of development. This is an estimate of the quantity of resources devoted to each reproductive event. (d) The
average size of mature males, which is an index of the size/age at maturity because males do not
grow after they attain sexual maturity and males that mature at an earlier age tend to also mature
at a smaller size. Likewise, the minimum size of pregnant females is smaller in high-predation localities (not shown).
p re l i m i na ry re s e a rch indeed have a genetic basis. The laboratory studies also enabled me to more
precisely quantify the variables of interest. The more controlled nature of the
laboratory environment meant that I could quantify features of the guppies’ life
history that were difficult or impossible to quantify in nature.
At the end of the 1978 field trip, I collected live guppies from two high-predation and two low-predation localities and brought them back to Philadelphia.
Female guppies have some handy features that make them well suited for laboratory experiments. They constantly reproduce in the field and store sperm,
so any wild-caught female can be isolated and will produce babies. I isolated
every adult female that I caught and all of them gave birth to multiple litters of
babies. The babies from each mother became a lineage that I reared separately
from the others. I reared this first laboratory-born generation to maturity, but
I separated the males and females from each litter before they matured so that
the females remained virgins. I then mated this first laboratory-born generation
to produce the fish that would be the subjects of my experiment. Each of the
wild-caught mothers contributed one male and one female offspring to these
pairings. Each of those crosses was a unique pairing of offspring from different wild-caught females. Such a design maintains as much genetic diversity as
possible from the initial sample. Avoiding the mating of brothers and sisters
prevents any artificial increase in inbreeding depression.
I kept 10 babies from each of these pairings of first-generation, laboratoryborn fish. This second generation of laboratory-born babies was reared until
they were 25 days old, by which time I could distinguish between the males and
the females. Ten is a magic number, because I did not want to keep too many
babies, but I wanted to keep enough to have a high probability of getting at least
two male and two female offspring from each litter for the experiment that followed. A sample size of 10 gave me a 95% probability of getting at least two fish
of each sex, on the assumption that each mother is equally likely to produce
male and female offspring. This expectation was fulfilled.
I wanted to rear all of the fish in a uniform environment, which meant rearing an equal number of young on the same diet in tanks of the same size. Furthermore, I did not want any microenvironmental variation in my laboratory
to become confounded with the population of origin of the fish, so I assigned
the wild-caught mothers to aquaria in what is referred to as a stratified, randomized block design, then I did the same when assigning the first-generation
babies to aquaria, then again when assigning the grandchildren to aquaria. This
means that for the wild-caught females, I divided the lab up into groups of four
aquaria, then assigned at random one female from each of the four localities to
one of those four tanks. Each “block” of four tanks was like a replicate of the
whole experiment. I performed a similar randomization for each generation.
This process of randomization means that variation in the laboratory environ-
13
14
ment, such as in light intensity or in temperature, was not associated with a
particular population of fish. An alternative would have been to rear one population on one shelf and another on a different shelf. Doing it that way would
have meant that any differences among shelves would be confounded with differences among populations.
By randomizing and maintaining uniform conditions for two generations, I
was eliminating the effects of the environment on the performance of the fish
in my experiment. Wild-caught females would certainly have experienced different environments. Those environmental effects might carry over, to some
extent, to the offspring that they produce, but those offspring were then reared
under the same, rigorously controlled conditions. It was then their offspring,
or the grandchildren of wild-caught females, that were used to estimate genetic
differences in life histories among natural populations. The first lab-born generation was thus like a filter that removed the effects of the natural environment experienced by the wild-caught mothers on the grandchildren that were
the subjects of the experiment.
The two male and two female grandchildren from each litter were reared,
one per aquarium, on controlled quantities of food. One of my most useful
tools turned out to be Hamilton micropipettes, which were invented for injecting very tiny, precise volumes of gas or liquid. I used them instead for quantifying how much food my fish got to eat: I stuffed the micropipettes with pastelike food, then gave my fish measured volumes of the food twice a day. I could
then check to see that the fish ate all that I gave them. Guppies acclimate well
to life in the laboratory, so most of the fish learned to come and eat all of the
food off of the tip of the syringe as soon as I placed it in the water. The growing females received a conjugal visit with a male from a stock tank once a week,
beginning when they were immature. Guppies are avid breeders, so a single
night will almost always result in a successful mating.
I looked at the growing males once a week, and used the metamorphosis
of their anal fins as an index of their sexual maturity. In immature fish and
females, the anal fin looks like a hand-held fan, with radial struts joined by
transparent webbing. In males, the fin undergoes a complex metamorphosis to
become the organ used to inseminate the female. It is adorned with complex
hooks, teeth, and appendages that vary among species. I discovered that the
development of these anatomical details provided a very accurate index of their
attaining sexual maturity. I was thus able to quantify precisely how old and how
large the males were when they attained maturity.
Females were different because they do not have an external anatomical feature that told me when they were mature. I instead could quantify how old and
how large the females were when they first gave birth, which was a better index
of sexual maturity than I had for wild-caught females. I could also quantify how
p re l i m i na ry re s e a rch many babies each of the females had, how large the babies were, and how often
the females reproduced. Because I knew how much food each of the females
had eaten, I could quantify the sizes of the slices of pie that defined each fish’s
life history. It turns out that average age at first reproduction of females from
a given locality was very close to the average male age at maturity plus the
average time interval between each successive litter of babies produced by the
females. This result implies that females were maturing at about the same age
as their brothers, if we assume that the interval between litters is a good estimate of the amount of time required for a fertilized egg to develop into a newly
born embryo.
I found that the high-predation guppies were indeed younger at maturity, by
around 15%. They devoted more of their available food resources to each litter
of babies. They produced litters of babies more often. Each litter of babies consisted of more and smaller offspring. It is thus clear that high-predation guppies
devote more resources to reproduction than low-predation guppies because
they start to breed when they are younger, reproduce more often, and devote
more resources to each litter of babies than their counterparts from low-predation localities. In a different kind of study, I later showed that there is genetic
variation for these traits to be found within each population of guppies. So,
while the average age at maturity is younger in guppies from a high-predation
locality, there are also genetic differences among families within each population in the age at maturity. This variation is the raw material that Darwin’s
mechanism of natural selection calls for. It means that all of these populations
have a continuing capacity to evolve, should their environments change.
All of this early work was done on populations from the south slope of the
Northern Range Mountains. I later learned that the streams that drained the
north slope of those mountains had a very different fish fauna. Those from the
south slope are typical of the fish that are found in the freshwater streams of
the Orinoco River drainage in Venezuela, including cichlids and characins. The
reason for this similarity is that Trinidad was joined to South America during
glacial periods, when water was tied up in polar ice caps and what is now a shallow sea that separates Trinidad from the mainland was then dry land. The rivers
that drain the southwest slopes of the Northern Range Mountains all drain into
the Caroni River, which was once a tributary to the Orinoco River. The rivers
on the north slope of Trinidad’s Northern Range Mountains were instead isolated from the mainland. Many of the fish found on the north slope have life
cycles that are the reverse of the life cycles of salmon. The adults occupy freshwater streams. The eggs and larvae wash out to sea, and the young then colonize
freshwater streams after metamorphosis. This kind of life cycle enables them
to colonize relatively isolated rivers, including those on islands as isolated as
Hawaii. Guppies have colonized some of the rivers on the north slope of Trini-
15
16
Riv/Cren
R-M/Eleo
A
Cren/Riv (days)
90
B
Eleo/R-M (days)
95
85
90
80
Cren/Riv (mg)
300
Eleo/R-M (mg)
150
140
250
130
85
75
70
120
200
80
Female age (days)
110
Female size (mg)
65
75
C
150
100
D
65
70
100
60
65
60
55
90
55
50
50
Male age at maturity
Male size at maturity
80
45
Riv
Riv/Macro
Eleo
Cren
45
Riv
Riv/Macro
Eleo
Cren
F i g u r e 3 Results of laboratory, common garden comparisons of the life histories of guppies
from high- and low-predation environments on the north and south slopes of the Northern Range
Mountains. Each data point represents two localities from different drainages. The abbreviations
for high- and low-predation localities are the same as in F i g u r e 2 . The data points are least
square means (+ 1 standard error). (a) Female age at first parturition. (b) Female size at first parturition. (c) Male age at maturity. (d) Male size at maturity. We also found that the guppies from
high-predation sites on both slopes produced more young in each litter but the size of each offspring was smaller. The high-predation guppies on both slopes had shorter intervals between the
birth of each litter of young. They also devoted more resources to reproduction than did their
counterparts from low-predation environments (data not shown).
Figure
01.08
File name
Losos/Brodie
In the Light of Evolutiom
Date (M/D/Y)
Final size (w x h)
0p x 0p
Author's review
the mechanism
dad as well; we think this is because they are tolerant of salt water and sometimes get washed out to sea when rivers flood during the rainy season. Some of
these waifs may survive in lenses of fresh or brackish water that eventually come
close to the outflows of isolated rivers.
The large predators found in the lower portions of the rivers that drain the
north slope of Trinidad are gobies and mullets, rather than the cichlids and
characins found on the south slope. Nevertheless, the streams of the north slope
have complex, predator-rich communities downstream and progressively simpler communities with fewer predators in the headwater streams, just as on
the south slope. I reasoned that, if it is predator-induced mortality that causes
guppy life histories to evolve, then comparisons among guppies from highpredation and low-predation environments on the north slope should yield
the same results as the earlier comparisons on the south slope. They did, both
in terms of the phenotypes of wild-caught fish and in the genetic differences
revealed by laboratory studies performed on the grandchildren of wild-caught
females (F i g u r e s 2 and 3 ).
So far, so good—but all of this is still just the preliminaries. These results
simply establish that there is a correlation between the life histories of the guppies and the predators with which they co-occur. There were two major hurdles
left to negotiate to prove the connection between predation and life-history
evolution. One was to characterize the mechanism of natural selection. The
other was to manipulate this mechanism experimentally in nature and to show
that guppies evolve as predicted by life-history theory.
THE MECHANISM
Life-history theory predicts how the risk of death alters the ways in which
organisms allocate resources to the pie of life. The theory does not address
the causes of death. The role of predators in causing death is where the natural history of guppies meets theory and where it became possible to use the
theory to make predictions that can be tested on guppies. Guppies that live in
the lower reaches of streams with many predators should suffer higher mortality rates than guppies that live in the headwater streams, where most predators
are absent. If this is true, then life-history theory predicts that, in sections of
streams with predators, natural selection will favor those individuals that attain
maturity at an earlier age and devote more of their resources to making babies.
In the headwater streams, the theory predicts that natural selection will instead
favor guppies with delayed maturity that devote less of their resources to making babies and more of their resources to their own growth and maintenance.
They gain by living longer and producing more babies during their extended
lifespans. In the first phases of my research, I showed that those predictions
17
18
were fulfilled for guppies from high-predation communities and low-predation
communities alike, and that the patterns were replicated both in north-slope
and in south-slope streams.
Is it really true that guppies that live with predators have a higher death rate?
I set out to estimate mortality rates early in my career, but it took me more
than 10 years to get an answer. You may wonder why it took so long. I originally tried to evaluate mortality rate by aging guppies, then using age structure
to make inferences about mortality schedules. I determined the ages of guppies by postmortem examination of their otoliths, which are bone like structures in the inner ear that record growth rings, like the concentric rings that
you see when you examine the stump after a tree has been cut down. The difference is that trees record annual rings, but it appears that guppy otoliths record
daily rings. If I could find the age distribution in whole-population samples of
guppies from high-predation and low-predation localities, then I could make
some inferences about mortality rates, but only if I were also able to make some
assumptions about how constant the birth and death rates of the populations
had been. As this work progressed, it became clear that those assumptions were
risky. At the same time, I developed ways of marking very small fish, down to
10 millimeters in length, because I wanted to release them in the field, then to
re-collect them to look at ring formation and to confirm that the rings that I
was counting were really daily rings. I immersed the fish in water containing
calcein before releasing them. Calcein binds to calcium-bearing tissue and it is
fluorescent when viewed under certain wavelengths of light. My goal was to recatch the fish later, to remove their otoliths, and then to count the number of
rings that had formed on the outside of the fluorescent ring. Using these and
other experiments, I found that new rings were produced daily in fish up to
around 100 days old, but that I had been systematically underestimating the
true age of older fish. It was beginning to appear that a massive amount of
work would yield only results of poor quality. Then I realized that marking and
recapturing the fish could give me much better information for evaluating mortality rates than examination of their otoliths could provide, simply because it
was so easy to re-collect marked fish. Also, spending long hours in a dark closet
staring down a microscope and counting otolith rings had begun to develop
into a dangerous obsession. I found myself going to parties and ignoring the
conversation while I attempted to determine the ages of the trees from which
my hosts’ coffee tables had been made. So, while mark–release–recapture had
begun as a means of evaluating the quality of otoliths for aging fish, it ended up
becoming a welcome and superior means for estimating mortality rates.
I worked in streams that consisted of pools of water that were bounded
upstream and downstream by riffles, where the stream is narrower and steeper
and the water flows more swiftly. Guppies like to congregate in pools, and they
the mechanism
19
are disinclined to swim the riffles to go to neighboring pools. It is possible to
collect every guppy in a pool. I can create a “guppy magnet” by sitting at the
upstream side of a pool and gently stirring up some sediment. Most species
of fish would hide in response to such a disturbance, but guppies will come to
check out the sediment to see if there is anything good to eat. By holding a butterfly net in each hand, I could chase them from one net to the other. In that
way, I could catch them all without disturbing the habitat. I measured each fish,
marked it with tiny dots of paint injected under the skin (the piscine equivalent
of a bird band), and then released it back into its home pool. I re-collected the
guppies two weeks later.
By comparing the number of marked guppies that were released with the
number that were re-caught, it was possible to estimate the number that had
died or had moved to another pool. It was also possible to see how well those
that had lived were growing, to quantify the birth of new youngsters (the small,
unmarked individuals that had accumulated between release and recapture),
and to study the movement of individual guppies from one pool to the next.
(185)
90
(132)
80
70
60
50
(278)
(143)
(127)
(127)
(165)
(424)
<12mm
12–14mm 14–18mm
>18mm
F i g u r e 4 Probability of recapture of mature females, immature males, and juveniles after an
interval of 12 days (y-axis). The blue line represents the recapture probabilities for high-predation
localities, while the red line represents recapture probabilities from the low-predation localities.
The numbers in parentheses represent the number of marked individuals that were released. The
x-axis represents four different size classes, defined by their standard length, which is measured
from the tip of the lower jaw to the outer margin of the hypleural plate, which is a cartilaginous
plate that the fin rays insert on. The smaller two size categories are immature fish and the larger
two are mature females. Mature males were analyzed separately because their bright coloration
makes them more susceptible to predation. We obtained similar results for males, which were that
males from high-predation localities have substantially higher mortality rates. These data were
derived from 14 different mark–recapture studies, seven each from high- and low-predation environments. From Reznick, Butler, Rodd, and Ross (1996).
20
I found that the death rate over a two-week period was about 15% higher
in high-predation localities. Over a seven- to eight-month period, this higher
death rate meant that a guppy that had lived in a pool without predators was 20
to 30 times more likely to have survived than one that had lived in a pool with
predators. Living with predators really does mean that guppy life expectancy is
much lower than it is when predators are absent. This result brought me one of
my proudest moments in science, which was to be featured in the supermarket tabloid National Enquirer under the headline “Uncle Sam wastes $97,000 to
learn how old guppies are when they die.” Actually, I learned a great deal more
than that from this research.
THE TEST
I wanted to do experiments to test predictions from theory. John Endler had
already shown that the distribution of guppies and their predators makes such
experiments possible because of the way in which their distribution is often
punctuated by barrier waterfalls. The first barrier waterfall often stops the large
predators but not the guppies and some other smaller fish. Each successive barrier stops more fish. Some waterfalls exclude all but guppies and Rivulus. Other
barriers exclude even guppies, so that the killifish Rivulus is the only fish present. Recall that Rivulus is able to breach barriers more effectively than other fish
because it will actually jump out of the stream on rainy nights, hop around the
forest, and invade aquatic habitats that no other fish can reach.
The discontinuities created by waterfalls make it possible to think of a stream
as being like a giant test tube. John Endler realized this when he studied the
effects of predators on the evolution of male coloration. He took guppies that
had lived with predators below a barrier waterfall and introduced them into
a previously guppy-free habitat above the waterfall. Doing so enabled him to
study how the guppies evolved when they no longer lived under the threat of
predation. Change could be perceived by comparing the descendents of the
introduced guppies with the population of guppies found below the barrier
waterfall. The introduced guppies had descended from the population found
downstream from the barrier and, at the start of the experiment, had been just
like them. This means that any differences between the introduced guppies and
their “downstream control” had evolved after the introduction.
I adopted Endler’s introduction experiment, which had been initiated in
1976, then duplicated it in 1981 in a different river, where I again transplanted
guppies from a high-predation site to a section of stream that lay above a barrier
waterfall and was occupied only by Rivulus. Life-history theory predicts that,
when guppies are transplanted from a high-predation site to a low-predation
site, natural selection should favor those individuals that devote fewer resources
the test
to reproduction. This means that, over time, the population of guppies in the
introduction site should evolve later maturity and a lower rate of investment in
reproduction relative to those from the downstream control.
I also did a different type of experiment, in which I added predators to a
stream that had previously contained guppies and Rivulus but not predators, so
that I increased, rather than decreased, guppy mortality rates. In this case, lifehistory theory predicts that an increase in mortality rate will cause the affected
guppy population to evolve earlier maturity and a higher rate of investment in
reproduction. The control was a population of guppies found above a barrier
waterfall further upstream that blocked the upstream migration of the introduced predators.
To see whether or not guppies had evolved, I collected adult females from
the experimental and control sites and transported them to my laboratory,
which was then in California. I performed a two-generation experiment, which
was identical in design to the one that I used years earlier, to show that there
was a genetic basis to the differences in life histories of guppies from high-predation and low-predation environments. The difference between the earlier
experiment and this one was that I was now comparing control and experimental populations. I knew how long ago the introductions were done, I knew
that the introduced guppies had lower mortality rates than those in the control
population, and I could quantify how the guppies in the introduction site were
different from those from the control site, who were their ancestors. Any differences between the two populations could be interpreted as being caused by the
evolution of the introduced guppies after being transplanted over the barrier
waterfall. In the first phase of my research, in which I compared guppies from
high-predation and low-predation environments, any differences that I found
were simply correlated with the presence or absence of predators. The life-history patterns that I found in that first phase of research could have been caused
by any other difference between the two types of environments.
In both types of introduction experiments, guppy life histories evolved as
predicted by theory. When guppies were transplanted from a high-predation
site to a previously guppy-free, low-predation site, they evolved a later age at
maturity and a lower rate of investment of resources into making babies, relative to the guppies from the control site found below the barrier. Likewise,
when predators were introduced, guppies evolved so that they attained maturity at an earlier age. This test goes beyond the “natural experiment” because
what we see is the product of our own manipulation, and change is judged relative to an experimental control.
This combination of comparative studies done on guppies from many rivers,
genetic studies on a subset of these populations, introduction experiments and
21
22
Table 1
Reznick and Bryga (1987)
Control
Introduction
(Crenicichla) (Rivulus)
Life history
trait
This study
Control
Introduction
(Crenicichla) (Rivulus)
Reznick (1982)
Crenicichla
Rivulus
Male age at
60.6 (1.8)
maturity (days)
72.7 (1.8)
48.5 (1.2)
58.2 (1.4)
51.8 (1.1)
58.8 (1.0)
Male size at
56.0 (1.4)
maturity
(mg-wet)
Female age at 94.1 (1.8)
first parturition
(days)
62.4 (1.4)
67.5 (1.2)
76.1 (1.9)
87.7 (2.8)
99.7 (2.5)
95.5 (1.8)(NS)
85.7 (2.2)
92.3 (2.6)
71.5 (2.0)
81.9 (1.9)
Female size at 116.5 (3.7)
first parturition
(mg-wet)
Brood size,
2.5 (0.2)
litter 1
118.9(3.7)(NS)
161.5(6.4)
185.6 (7.5)
218.0(8.4)
270.0(8.2)
3.0 (0.2)(NS)
4.5 (0.4)
3.3
(0.4)
5.2 (0.4)
3.2 (0.5)
7.0 (0.3)
8.1 (0.6)
7.5
(0.7)(NS)
10.9 (0.6)
10.2 (0.8)(NS)
11.4 (0.8)
11.5 (0.9)(NS)
16.1 (0.9)
16.0 (1.1)(NS)
(0.3)
Brood size,
litter 2
Brood size,
litter 3
6.3
Offspring size
(mg-dry),
litter 1
Offspring size,
litter 2
0.91 (0.02) 0.87 (0.02)(NS)
0.87 (0.02) 0.95 (0.02)
0.84 (0.02) 0.99 (0.03)
0.93 (0.02) 0.86 (0.02)
0.90 (0.03) 1.02 (0.04)
0.95 (0.02) 1.05 (0.03)
1.10 (0.03) 1.17 (0.04)(NS)
1.03 (0.03) 1.17 (0.04)
Offspring size,
litter 3
Interbrood
interval (days)
24.9 (0.4)
24.89(0.4)(NS)
24.5 (0.3)
25.2 (0.3)(NS)
22.8 (0.3)
25.0 (0.03)
Reproductive
effort (%)
4.0
(0.1)
3.9 (0.1)(NS)
22.0 (1.8)
18.5 (2.1)(NS)
25.1 (1.6)
19.2 (1.5)
T a b l e 1 Results of the introduction experiment initiated in 1981 after four years of selection
(left-hand columns), the results of John Endler’s 1976 introduction after 11 years of selection
(middle columns), and the results of my first comparison between guppies from high- and lowpredation environments (right-hand columns). The columns on the right represent the expected
differences in life histories for guppies from high- and low-predation environments. The results on
the left (four years of selection) show that the differences in male age and size at maturity between
the introduction site and controls were already as different as seen in the natural high- and lowpredation environments. There are no apparent differences in female life histories. The columns
in the middle (11 years of selection) show again that the differences between males from the control and introduction sites are comparable to natural high- and low-predation environments.
the test
mark-and-recapture studies argue that predators and higher mortality rates
have played an important role in shaping life-history evolution in guppies.
This was all very good, but there were still some surprises in the results. In
1979, when I described the experiments that I hoped to do, I often saw sympathetic smiles and was told that my audience hoped that I would live long
enough to see evolution happen. After all, evolution by natural selection is a
very slow process. It turns out that I did not have to wait long. Male life histories changed completely in only four years, which is a mere six to eight generations. In fact, it may have taken less than four years. I waited four years to assay
the life histories of the control and experimental populations, and I considered
it a big gamble to look for evolution so soon after the introduction. Endler had
already shown that male coloration had evolved in only two years. The females
in my experiment evolved less rapidly than males; they began to show significant change in seven years.
By the time these results began to appear, in the 1980s, others had made similar observations in other study systems (most famously, Peter and Rosemary
Grant and their colleagues on the medium ground-finch from Daphne Major
in the Galápagos Islands), so our view of the possible rate of evolution by natural selection had begun to change.
Before this research, our concept of how fast evolution can occur had been
pretty much the same as Darwin’s in the Origin. We looked at the fossil record
as the history of evolution, but also as a source of information about the process
of evolution. Many scientists had quantified how fast evolution occurs from the
rate of change in such traits as body size in fossils from successive geological
strata. Doing the same calculations for guppies showed that they had evolved
at a rate that was on the order of 10,000 to 10 million times faster than what
had been considered rapid evolution in the fossil record. It may be that guppies evolved unnaturally quickly, but I am inclined to think otherwise. Similar
high rates of evolution, such as that of the Galápagos finches, have now been
T a b l e 1 ( c o n t i n u e d ) Most female life-history traits also differ significantly between the
introduction and control sites, but the magnitude of the differences is less than seen in the natural
high- and low-predation environments. The differences that you see among these experiments in
mean values, such as for female size at first parturition, reflect differences in food availability. The
fish in the right-hand columns received more food than those in the middle columns, who in turn
received more food than those in the left-hand columns, causing a progressive decline in female
size at first parturition and male size at maturity. The key result is that the differences between
high- and low-predation guppies, or control and experimental guppies, were qualitatively the
same regardless of ration. From Reznick, Bryga, and Endler (1990).
23
24
seen in many other studies. In fact, such rapid evolution has now been documented so many times between the inception of this work (with John Endler’s
introduction in 1976) and now (2010) that the attitude of evolutionary biologists has shifted from considering such experiments to be a quixotic search for
something that cannot be seen to considering rapid evolution to be an ordinary
phenomenon.
The difference between rates estimated from fossils and rates estimated in
contemporary studies probably occurs because estimating the rate of evolution
from the fossil record seriously underestimates how fast organisms can evolve
and how strong natural selection can be. When we look at fossils it is as if we
are watching a movie but, instead of seeing the whole story unfold, we get to
see only a single frame or a short scene taken at random. Imagine seeing just a
few scenes from Gone With the Wind, with a quick succession from Rhett Butler leading his daughter on a pony ride, to the siege of a southern city during
the Civil War, to Rhett declaring, “Frankly, Scarlet, I don’t give a damn!” What
happened? We can only guess, given this paltry amount of information. Paleontologist take successive strata in the fossil record, then join them as if they
were a sequence, and as if the changes that took place between each of the sampling points were continuous and progressive. If an animal increases in size by
10% in two samples that represent a time interval of 100,000 years, then it is
implicitly assumed that its size increased at the same steady rate for that entire
time interval. In fact, its size may have increased, then decreased, then increased
again, then done nothing at all for a while before once again increasing and
decreasing. All of the changes and reversals would have been much more rapid
than the average change over the entire sequence, but all would be invisible in
the record. The record simply reveals the average change that occurred over the
entire interval.
The Grants’ research on Darwin’s finches shows that change over time is
indeed erratic. They studied the evolution of body size, among other traits, and
showed that it could alternately increase or decrease very rapidly as the finch
population tracked an environment that alternated between droughts and wet
El Niño years. If we simply looked at the finches every few decades, it might
seem that not much change had occurred. The fossil record is an irreplaceable
record of the history of life, but it has severe limitations as an accurate barometer of the process of evolution.
FURTHER RESEARCH
I have now extended my comparative studies of guppy life histories to the evolution of senescence, or the aging process, since corollaries of life-history theory
address late-life phenomena as well. My collaborators and I have also shown
further research
that life with and without predators has selected for changes in body shape and
swimming performance. Not surprisingly, guppies from high-predation environments have faster escape responses and are more likely to survive attacks by
predators. At the same time, we showed that there is a conflict between the evolution of high escape speeds and the evolution of reproductive allocation. Guppies from high-predation environments are faster, but their larger allocations
to each reproductive event slow them down. Others have shown that predators
also select for differences in various aspects of behavior. In fact, we have found
an imprint of predation on virtually every trait that we have taken the time to
study. This body of research shows how profound the effects of predators can
be on their target organisms. It also shows how great the scope of the adaptations is that are required to adapt to the presence of predators. The special
feature of guppies in Trinidad that has made these discoveries possible is the
close juxtaposition of populations (above and below waterfalls) that live with
and without serious predators, the limited rate of migration upstream, and the
repetition of this pattern in multiple river drainages.
We are currently evaluating the interaction between ecological and evolutionary processes in new introduction experiments that are similar to those
summarized above. Traditional ecology, both in practice and in theory, implicitly assumes that evolution does not occur. It makes this assumption by treating
organisms as constants or as unchanging over the course of an ecological interaction. The justification for assuming that there is no evolution is that ecology
was thought to act on such short time frames relative to evolution that the two
processes would, in effect, be independent of one another. Now we know that
significant evolutionary change can happen on a time scale that is similar to
the time scale of ecological processes. Theory and laboratory experiments have
shown that allowing evolution to occur during an ecological interaction significantly changes the predicted outcome of ecological interactions. Combining
evolution and ecology as interacting processes thus holds the promise of making both ecology and evolution more predictive sciences. The guppy system
in Trinidad offers a unique opportunity to characterize and to quantify such
interactions in a natural ecosystem. This work also reflects the growth of our
realization that evolution is much faster than previously imagined and that this
speed has consequences in many other areas; we must now incorporate change
through evolution into our day-to-day evaluation of many phenomena that
we previously thought could be explained without invoking evolution because
evolution seemed to be too slow a process.
The current work includes new introduction experiments, and we are
upgrading those introductions to take advantage of advances in research methodology. Every introduced fish is individually marked and photographed. We
remove two scales from each individual, then make a genetic fingerprint of it by
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extracting DNA from the scales and sequencing sections of DNA that are highly
variable in DNA sequence. We are making a census of each of these populations
every month, and we are photographing, individually marking, and removing scales from each new recruit. We can now use the DNA from the scales to
fingerprint the babies and then to reconstruct the entire pedigree of replicate,
evolving populations. This means that we can study evolution in the traditional
fashion, as changes in the average properties of populations over time, but also
that we can study evolution in terms of differences among individuals in reproductive success. Furthermore, there is sufficient DNA in two scales for us to
archive DNA samples from every individual in an evolving population. Our
hope is to use this archive to study the genetic basis of the evolution of all of
the traits that change in response to predation. Perhaps someday our work with
guppies will reveal the genetic basis of aging, for example, and the evolution of
extended lifespan. This work has also given us very fine resolution for seeing
how fast evolution can really happen. The last time I waited four years before
I began to look for evidence of evolutionary change. Even then, I thought that
four years was too short a time. Our perceptions of evolution are now quite
different. This time around we have monthly resolution of attributes like body
shape and male coloration and yearly resolution for life-history traits. These
experiments are only 18 months old, but we are already seeing what might be
the evolution of some important traits. Perhaps my earlier estimates of very
rapid evolution were really underestimations of how fast evolution can happen in nature. We will know for certain within the next year, since we are now
beginning our laboratory studies to get our first peek at whether the introduced
populations have indeed diverged from their control, or the high-predation
population that they were derived from.
One virtue of basic research is that its results can be applicable in other contexts. Two other applications for which the guppy research has provided a good
model for understanding how evolution can be important in our day-to-day
lives are the evolutionary consequences of man’s exploitation of natural fish
populations as a source of food or the evolutionary consequences of man’s
impact on natural communities, which often includes the removal of predators,
but now also includes the reintroduction of predators.
CONCLUSIONS
This scenario brings us back to the mechanism of natural selection and how
it works. Darwin’s first premise was that organisms produce more offspring
than are required to replace themselves in the next generation. Anyone who
has kept guppies in an aquarium knows how quickly they can multiply. A
few guppies can become many thousands within a year if all their offspring
conclusions
are well fed and protected from predation and infectious disease. When the
guppies in a high-predation locality find a refuge, such as in the submerged
branches of a fallen tree, they quickly fill it with babies. We generally see
such productivity only in these small bursts, because so few individuals survive predation. Our laboratory studies have shown that there are genetic differences between guppy populations, but also that there is genetic variation
within populations. In each population, the family averages for such traits
as the age at maturity are different, so they have the continuing capacity to
evolve if the environment changes. It is this variation and the overproduction of babies that have enabled guppy populations to evolve when their environment has been changed by their being transplanted from a high-predation site below a barrier waterfall to a low-predation site above the waterfall.
The same variation was present, and enabled the residents of low-predation
sites to adapt, when a predator was added to their community. The variation
meant that some individuals were more successful in producing offspring in
the time that was available to them. If predators were present, then life was
short, and those who matured quickly and produced many babies were more
successful. If predators were absent, then life expectancy was long, and natural selection favored those who invested more in their own maintenance and
in producing a smaller number of higher-quality young.
This story shows one view of what evolution has become since Darwin.
We have developed Darwin’s original concept of fitness into quantifiable features of organisms. We have also developed quantitative theory that can predict how organisms will evolve in response to features of their environment.
Theory has enabled us to design experiments that show that natural selection
is an observable, quantifiable, contemporary process, rather than just being
something that we can see only through the lens of history.
Guppies in Trinidad also illustrate what we need to know to understand
natural selection. We need to know about the variation that selection acts
upon, we need to know its source, we need to know how much of it is there,
and we need to know how it is transmitted from parents to offspring. We need
to know about the capacity of organisms to change from generation to generation under selection, and we need to know how much change is possible. We
need to know what in the environment controls population size and how it is
controlled. Is it predators, or other organisms that compete for resources, or
disease, or some combination of these and other factors? Whatever regulates
populations is what causes evolution by natural selection to occur and will
determine how the organism evolves in response to that regulation. Darwin
addresses all of these issues in the opening chapters of the Origin. Now we are
in a position to quantify them all in nature and to do so in the context of testing the predictions of new, quantitative versions of the theory of evolution.
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We are no longer forced to infer evolution from its historical footprints in the
fossil record or from dusty collections of moths.
RECOMMENDED READINGS
Reznick, D. N. 2009. The Origin Then and Now: An Interpretive Guide to the Origin of
Species. Princeton University Press: Princeton NJ.
Weiner, J. The Beak of the Finch. 1994. Alfred A. Knopf: New York.
This essay is modified with permission from University of Princeton Press from
chapter 7 of The Origin Then and Now: An Interpretive Guide to the Origin of
Species (2010).