INSIGHT OVERVIEW
NATURE|Vol 457|12 February 2009|doi:10.1038/nature07889
Natural selection 150 years on
Mark Pagel1,2
The theory of evolution by natural selection has prospered in its first 150 years and provides a consistent
account of species as highly adapted and rare survivors in the struggle for existence. It now faces the
challenge of finding order in the evolution of complex systems, including human society.
Happy 200th birthday to Charles Darwin, whose theory of evolution
by natural selection will be 150 later this year. Darwin had been quietly
amassing support for his ideas for nearly 20 years when in 1858 he
discovered that Alfred Russel Wallace was thinking along similar lines.
In the following year, Darwin’s 50th, he finally published the theory in
On the Origin of Species1.
It was a theory marked out for controversy from birth. Darwin’s
claim was that natural selection could explain the diversity of all life
on Earth, from bacteria to barnacles, orchids, fish, lizards, mushrooms,
pine trees, elephants, bananas, stick insects and bonobos. Provocatively,
given the religious views that prevailed at the time, it was a materialistic
account of nature. There were no guiding hands, no grand plans, no
‘great chain of being’. According to Darwin1, the varieties of forms that
are observed arose because “As many more individuals of each species
are born than can possibly survive; and as, consequently, there is a
frequently recurring struggle for existence, it follows that any being,
if it vary however slightly in any manner profitable to itself, under the
complex and sometimes varying conditions of life, will have a better
chance of surviving, and thus be naturally selected. From the strong
principle of inheritance, any selected variety will tend to propagate its
new and modified form.”
It is an idea of remarkable simplicity. Complex organisms emerge
from the gradual accumulation of successive modifications, each one
of which improves the bearer’s chance of surviving in the struggle for
existence. But Darwin would go further, yielding up what must be one
of the most daring hostages to fortune in the history of science, declaring: “if it could be demonstrated that any complex organ existed which
could not possibly have been formed by numerous, successive, slight
modifications, my theory would absolutely break down.”
Darwin has been spared the embarrassment he courted. Natural
selection is an idea that has survived and propagated in the competitive
environment of the mind. There are no serious alternative explanations
for the existence and diversity of species. Most would agree that the theory
has been immensely successful. It has been capable of explaining — as
adaptations that improve survival and reproduction — many features of
organisms: their shapes, sizes and colours; why they live so long or have
such short lives; their reproductive habits, diet and mating choices; the socalled organs of perfection, such as eyes or brains; and even social behaviours, explaining parental care, altruism, sibling rivalry and aggression. It
has been influential in understanding viral, bacterial and other microbial
evolution, and in explaining the evolutionary changes that take place at
the level of DNA itself.
The theory’s application has not been limited to biology. In the past
few decades, it has jumped to many other disciplines, with papers on
natural selection appearing in the scientific journals of, among others,
anthropologists, sociologists, philosophers, economists, mathematicians
and statisticians, demographers, physicists and even surgeons, yielding
a wide and ‘long tailed’ distribution (Fig. 1).
Given the continued success of the theory of evolution by natural
selection, it is useful to step back and take stock of what it indicates about
the nature of the biotic world. Does all life descend, as Darwin thought,
from a long unbroken line of ancestors, or have the various forms of life
evolved independently? How creative a force is natural selection? Are
all human traits adaptations? Are humans just one of many, possibly
arbitrary, outcomes of the evolutionary process, or would the same kinds
of species and adaptations arise if the tape of evolution were re-run? Is
there an unlimited variety of species?
In this Overview, I review where the theory stands on these core questions, which cut across the hundreds of specific topics of evolutionary
investigation. This list of questions is by no means comprehensive, and
many researchers will find their favourite question ignored. But the
answers that emerge here and in the articles that follow in this Insight
provide a glimpse into a process — natural selection — that is at once
conservative and severe, yet innovative and exacting, yielding organisms
that are often surprisingly well adapted from among a relatively small
number that manage to wriggle or claw their way through its sieve.
Humans are among the survivors, but the answers pondered here do far
more than tell us about ourselves. They set a benchmark for the kinds of
phenomenon that the many other disciplines that make use of Darwinian
ideas might expect to see in their observations. At the end of this Overview,
I briefly discuss how natural selection is approaching two growing areas
of research into what are becoming known as ‘complex adaptive systems’2:
one relates to the rules controlling the organization of bodies such as those
of humans; the other seeks to understand human societal evolution.
Descent with modification
Darwin used the word ‘evolve’ just once in On the Origin of Species, and
even then he waited until the final word of the book. Instead, Darwin
wrote of ‘descent with modification’. For many at the time, this meant
species descending in the ‘great chain of being’, with God at its peak.
This was a progressive view of life, in which each level was seen as more
evolved than the one below. Humans occupied the earthly pinnacle of
the chain, having supplanted the simpler monkeys.
But the only illustration that Darwin put in On the Origin of Species
shows evolution following a branching, or tree-like, process, in which
the different branches of the tree represent the separate forms of life
(Fig. 2). Successful routes through the tree reach to the present, whereas
those that fail result in extinction. This tree banished in a single stroke
the idea of progress in evolution; instead, all extant life is equally evolved.
A ‘lowly’ slime mould has been evolving as long as you have, even if you
regard yourself as more complex. Slime moulds are good at being slime
moulds, and they are better at being slime moulds than you are or than a
giraffe is. Giraffes, in turn, are good at being giraffes and better at being
them than fish or bananas are, and so on. What natural selection makes
species good at is ‘propagating’, something that is now recognized as
transmitting copies of their genes into future generations.
1
School of Biological Sciences, University of Reading, Reading RG6 6AJ, UK. 2The Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, New Mexico 87501, USA.
808
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OVERVIEW INSIGHT
NATURE|Vol 457|12 February 2009
9,000
8,000
Number of papers
7,000
6,000
5,000
4,000
3,000
2,000
1,000
Genetics and heredity
Evolutionary biology
Zoology
Ecology
Other life sciences
Molecular biology
Reproductive biology
Physiology
Behavioural sciences
Plant sciences
Anatomy and morphology
Developmental biology
Mathematics
Other science and technology
Computational biology
Immunology
Psychology
Cell biology
Nutrition and dietetics
Infectious diseases
Microbiology
Agriculture
Entomology
Neurosciences
Conservation
Marine and freshwater biology
Meteorology
Pathology
Anthropology
Parasitology
Endocrinology and metabolism
Computer science
Demography
Environmental health
Biotechnology
Sociology
Pharmacology
Philosophy of science
Social issues
Philosophy
Forestry
Engineering
Geography
Experimental medicine
Cardiology
History
Paediatrics
Haematology
Veterinary sciences
Chemistry
0
Figure 1 | The long tail of natural
selection in scholarly work. The
number of papers that include
the term ‘natural selection’ in
their title, abstract or keywords,
recorded separately for subject
areas as identified by the ISI
Web of Knowledge. Data are
derived from a search on ‘natural
selection’ in November 2008,
yielding 14,232 hits over all
years. This figure underestimates
the number of papers that
investigate topics in evolution,
being limited only to those that
include the search term. The
figure reports the top 50 subject
areas from over 140. Subject
areas are not mutually exclusive,
so the total of the quantities on
the y axis exceeds 14,232.
Subject area
Darwin concluded that humans were in the ape part of the tree, and this
led to some ribaldry among his supporters and opponents. At a debate
at the Oxford Union in 1860, the bishop of Oxford, Samuel Wilberforce,
supposedly asked Thomas Henry Huxley, a staunch supporter of Darwin, whether it was through his grandfather or his grandmother that he
claimed descent from a monkey3. Huxley’s reply can be read at leisure3.
What matters is that genetics has shown that Darwin was right. The nearest living genetic relative to humans is the chimpanzee, with the common ancestor of these species existing some 6–8 million years ago. Both
species belong to a group known as the hominids, comprising humans
and their extinct relatives, along with the great apes (chimpanzees, gorillas
and orang-utans). Its evolution has been bushy or tree-like, not a progressive line leading inevitably to us4,5. More than 20 species of hominin —
the subgroup that includes humans and the immediate fossil relatives of
humans — have been identified from fossils, including australopithecines
such as Lucy (Australopithecus afarensis) and Homo species such as Neanderthals. During part of history, up to five different hominin species have
coexisted5. Now just one survives: Homo sapiens.
Darwin’s branching idea would prove correct for more species than
just the apes. Evolutionary biologists refer to groups of species that derive
from a common ancestor not shared with any other species as ‘monophyletic’. Were species to march backwards in time6 down the branches of
Fig. 2, all of the various mammals would meet up at a common ancestor
to the exclusion of non-mammals; the birds would meet up at their own
unique common ancestor; so too would all of the vertebrates, a huge
group that includes all animals with a backbone (such as birds and mammals). On page 812 of this Insight, Graham Budd and Maximilian Telford
report on the monophyly of a different group: the arthropods. These
comprise the majority of all animal species on Earth, including insects
and crustaceans, and they all derive from a single common ancestor.
Budd and Telford place this group on the tree of life next to the worms
rather than the vertebrates (as though worms and arthropods are represented by b14 and f 14 at the top left of Fig. 2 and vertebrates are represented by a14, q14 and p14), forming a group known as Ecdysozoa7. For
years, it was thought that arthropods grouped with vertebrates. Budd
and Telford’s placement has implications for which species are the most
relevant model organisms for understanding humans: should researchers
be studying worms or fruitflies? The existence of Ecdysozoa suggests that
both are equally relevant (or irrelevant). Moving deeper in the tree of life,
past the animals, Darwin would be further vindicated by the fact that all
animals share an ancestor with the plants and fungi. And then, going back
further, all species eventually share an ancestor some 3.5 billion years ago,
somewhere among the prokaryotes (the bacteria and Archaea), from
which all life on Earth descends. No one knows if life evolved more than
once, but all extant life seems to have a single source.
Tinkerer or perfectionist
The size and details of monophyletic groups illustrate an important feature
of life. Rather than designing each species from scratch, as an engineer
might, evolution is conservative, using the same designs over and over.
Darwin recognized, as the comparative anatomist Geoffroy Saint-Hilaire
had before, that the hands of moles, horses, porpoises and bats all used the
same bones. Such traits, derived from common ancestral traits, are called
homologies. Neil Shubin, Cliff Tabin and Sean Carroll (see page 818)
trace the deep lines of conservation of many traits in ancient homologies hundreds of millions of years old. Eyes, for example, have evolved
independently perhaps dozens of times, but the gene encoding the protein
PAX6 is implicated in one way or another in nearly every known instance
of a light-sensitive organ appearing in an animal’s body. This includes the
light-sensitive tissues of some shellfish, as well as human eyes.
Pervasive monophyly and homology raises the question of whether
humans actually are adapted. Is natural selection a mere tinkerer or a
perfectionist? Arthur Cain was unequivocal in a 1964 article memorably
entitled ‘The Perfection of Animals’ 8. Although it was not one of Cain’s
examples, the sonar of insectivorous bats (acquired 70 million years
ago) has features that match those of the best sonar produced by human
engineers9. Others were less sanguine about adaptation. In 1979, Stephen
Jay Gould and Richard Lewontin attacked what they saw as an ‘adaptationist programme’ in evolutionary biology that uncritically treated all
traits as adaptations10.
Which view is correct? Not everything is an adaptation: human blood
just happens to be red, and human chins might be relics of the way the
human jaw develops. But the weight of evidence suggests that it is probably wise not to bet against natural selection. The struggle for existence
means that traits have to pay their way. The traits observed now probably
improve an animal’s chances of surviving and propagating, and those
traits that do not will tend to be lost. For example, fish that have adapted
to life in dark underwater caves lose the ability to see.
© 2009 Macmillan Publishers Limited. All rights reserved
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INSIGHT OVERVIEW
NATURE|Vol 457|12 February 2009
Figure 2 | Darwin’s tree. A reproduction of
the only figure Darwin included in On the
Origin of Species1. The diagram shows Darwin’s
conception of evolution as a branching, or treelike, process. Lines that reach to the top of the
diagram represent extant, or surviving, species.
Lines that end farther down are lineages that
have gone extinct, revealing Darwin’s hunch that
extinction rates are high. The two large groups,
or clades, of branching species issuing from
common ancestors A and I are monophyletic:
that is, each of these groups derives from a
common ancestor that is not shared with any
other species. Common ancestors within these
clades are indicated by letters with superscript
numerals where lineages converge. Lineages
associated with capital letters reach further into
the past. (Figure reproduced from ref. 1.)
One difficulty in studying evolution is that such traits tend to evolve
over vast periods of time. But there are ways of seeing evolution in action.
On page 824, Angus Buckling, R. Craig Maclean, Michael Brockhurst
and Nick Colegrave review the field of ‘experimental evolution’, in which
microorganisms are observed in test tubes over tens of thousands of
generations. Rates of evolution are high enough in these studies to test
in real time and under controlled conditions many of the basic ideas of
adaptation and natural selection.
Such studies show regular and reliable adaptation as microbial lines
diversify. They emphasize the importance of chance mutations in producing differences among individuals (Darwin’s ‘slight variations’). They also
demonstrate that the ability to adapt can itself evolve; for example, organisms can adaptively change the rate at which they produce new random
variants. More adaptive evolution is observed at the genetic level than is
expected given the redundancies in the DNA code11,12. Most evolutionary
changes are small, but they can sometimes sweep through populations
rapidly, producing sudden bursts of evolution13–15. Crucially for Darwin’s
theory, later forms can be shown to survive and reproduce better than
earlier forms when compared in the same environment.
Variation
A paradox of Darwinism is that variety is maintained among individuals
of the same species. Repeated bouts of natural selection might be expected
to use up genetic variation by selecting for the best features, making evolution grind to a halt. Many factors can contribute to variation being
maintained, but experimental evolution studies (see page 824) and the
analysis of innovations (see page 818) point to two fundamental and often
overlooked effects.
First, as organisms have increased in complexity over time, natural
selection has had more to work with. For example, it often co-opts preexisting genetic regulatory circuits, fashioning them to take on new roles
(see page 818). Second, as time passes, diversity seems to beget more diversity by creating different ways for species to make a living. For example, the
first species to appear is unlikely to be a predator, but the second might be.
This idea matches the human cultural experience of domesticating dogs.
In just a few thousand years, humans created varieties ranging from chihuahuas to Great Danes. Each new breed seems to have suggested another,
and dogs did not run out of the genetic variation that humans fancied.
Contingency
How repeatable is evolution? If the tape of evolution were replayed,
would there once again be turkeys and tomatoes, rattlesnakes, the
plague and humans? If the species observed now are the chance outcomes of many contingent historical events, there is hardly anything
810
special about any particular outcome of evolution, including humans.
Gould championed such ‘contingency’ in evolution, pointing out that
humans might not be here were it not for the fortuitous extinction of
the dinosaurs, which preceded humans on this planet16 but died out
as a result of a meteor impact. Perhaps so, but recent work17 suggests
that mammals were alive, well and vigorously diversifying before the
dinosaurs became extinct.
Studies of evolution on islands can provide direct evidence relating to
the question of contingency. In effect, the tape of evolution gets played
out independently on each island. And if the islands are similar enough,
they can be taken as replicates of each other. On page 830, Jonathan
Losos and Robert Ricklefs discuss adaptive radiations on islands, and
use as an example species of Anolis lizard on relatively isolated islands
in the Caribbean. They report that evolutionary diversification is often
similar on the different islands, yielding the same set of habitat specialists, each adapted to use a different part of the vegetation. Buckling et al.
(see page 824) report similar repeatability in independent lines of microorganisms in experimental evolution studies. Contingency does not
seem to be the pervasive force that Gould suspected. In other instances,
islands present unique opportunities for natural selection — and unique
faunas, such as those of New Zealand and Madagascar, are the result.
Speciation
Even the Pope now accepts the reality of evolution among individuals
of a single species, but he and many others with religious beliefs draw
the line at speciation. It is a clever ploy, tipping one’s hat to science by
giving evolution a minor role while reserving new species for the providence of creation. Speciation can require thousands of years, making
it difficult to observe. It does not help that Darwin said little about the
origin of species in On the Origin of Species. In addition, closely related
species are expected to be similar to each other, and yet some yawning
gaps exist. For example, the rock hyrax, a small creature, is thought to
be the closest living relative of the elephants.
Regarding these gaps, on page 837, David Reznick and Ricklefs explain
that if the rates of extinction of species are high (Fig. 2), then gaps would
be expected among the surviving species. No one knows precisely what
historical extinction rates have been, but a reasonable guess is that they
could be nearly as high as speciation rates; extant species are a rarefied
club of survivors. Many of these survivors might be responsible for the
gaps by outcompeting the similarly shaped and sized species to which
they were closely related. The hominins might be a good example: as
brain size and intelligence increased in this group, the less imaginative
species could have been driven extinct. The close human cousins the
Neanderthals might be the most recent case.
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OVERVIEW INSIGHT
NATURE|Vol 457|12 February 2009
But can speciation be observed? Yes. Field biologists have witnessed
speciation in action among several plant, amphibian, bird and fish species18. What matters for Darwin’s theory is that the process by which
populations of interbreeding individuals split into two non-interbreeding populations follows straightforward routes of natural selection. One
good example is that females of a cichlid fish species vary genetically in
their preferences for males of red and blue colours. Biologists are witnessing red males occupying the lower depths of Lake Victoria, in Africa,
and females with matching preferences are following them. These mating
preferences are causing this single species to split into two19.
Ways of life
Here is a fundamental logical challenge to the idea of adaptation. If
there were an infinite number of potential niches, or ways of life, for
organisms to fill, it would be difficult to argue that species are adapted,
because anything could do well. Darwin drew inspiration for his theory
of natural selection by observing the effects of ‘artificial selection’ by
farmers and others during the domestication of their crops and animals.
But there is nothing artificial about artificial selection. On page 843,
Michael Purugganan and Dorian Fuller show that domestication is just
another way of life, in this case a kind of plant–animal mutualism, and
their conclusions are relevant to the question of infinite niches.
Some ants can herd aphids as though they are cattle or can domesticate
fungi, and termites also practice domestication20. But humans have taken
it to new heights. There is an abundance of human-selected wheat, oilseed, barley, maize and rice genes on the planet, not to mention cows,
sheep and chickens. When humans do the domesticating, it is clear what
the ‘selector’ is hoping to achieve. Purugganan and Fuller suggest that
humans have frequently sought to improve just two characteristics —
plant germination and ease of harvesting — and they find that a relatively
small number of groups of genes lie behind most instances of successful
plant domestication.
Their conclusions invite the speculation that nature — like its human
counterpart — admits far fewer combinations of genes, and by inference
kinds of species, than are possible. There are, for example, no bananaeating snakes or flying monkeys, no species between humans and chimpanzees, nor between rock hyraxes and elephants. If the varieties of life
are severely constrained, the competition to occupy them will be fierce.
Natural selection emerges as a severe and vigilant master.
leaky: there are many different independent replicators — both biological individuals and cultural elements — each potentially with its
own strategies for survival and reproduction. Should human society be
viewed as a vehicle for the combined, cumulative effects of these replicators, rather than as a replicating system in its own right? If so, what rules
govern which vehicles are successful, and do they bear any relationship
to those for biological phenotypes?
There is a growing sense, for example, that human languages have
adapted to human minds24. Humans have domesticated languages: languages show features related to how they are used and to society15,25,26,
and this probably enhances their survival. Language might also to some
degree have domesticated humans24. It might have a regulatory role in
human society not unlike that of gene regulation27, and this may have
enhanced human survival. Much the same could be said about the interactions between humans and the varieties of religion, art and music,
topics that interested Darwin28. The ability of natural selection to keep
up with the times as more and more questions are asked shows that, far
from being old at 150, Darwin’s theory still has a spring in its step. ■
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A theory moving with the times
Some complex systems can acquire information about the environment
and respond to it, becoming ‘complex adaptive systems’2. Genomes
exhibit this behaviour on an evolutionary timescale, whereas the bodies of most organisms and human societies do so in real time. How does
this kind of adaptive complexity evolve, and is it correct to think of it as
serving the interests of a single entity?
As evolutionary studies enter the genomic era, biologists are finding out more and more about how genes combine with a surprisingly
large range of genetic regulatory mechanisms to produce the complex
systems that are the phenotypes of organisms such as ourselves21,22. The
genes of most multicellular organisms can often be counted on to ‘pull
together’ because they have the same route of reproduction and live or
die together in the same body, although there is scope for conflict23.
How natural selection favours phenotypes that are reliable and robust
to outside influences, but still able to adapt to new circumstances, will
be central to understanding development.
The question of whose interests are served is sharpened once natural
selection is allowed to venture into the realms of cultural and societal
evolution. The big complex adaptive system that is human society is
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