Re: Darwin Was Wrong (Apparently)
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- Date: Mon, 2 Feb 2009 21:06:24 -0600
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Why Darwin was wrong about the tree of life
21 January 2009 by Graham Lawton
Magazine issue 2692. Subscribe and get 4 free issues.
For similar stories, visit the Evolution Topic Guide
Read our related editorial: Uprooting Darwin's tree
IN JULY 1837, Charles Darwin had a flash of inspiration. In his study
at his house in London, he turned to a new page in his red leather
notebook and wrote, "I think". Then he drew a spindly sketch of a
tree.
As far as we know, this was the first time Darwin toyed with the
concept of a "tree of life" to explain the evolutionary relationships
between different species. It was to prove a fruitful idea: by the
time he published On The Origin of Species 22 years later, Darwin's
spindly tree had grown into a mighty oak. The book contains numerous
references to the tree and its only diagram is of a branching
structure showing how one species can evolve into many.
The affinities of all the beings of the same class have sometimes been
represented by a great tree. I believe this simile largely speaks the
truth...
The tree-of-life concept was absolutely central to Darwin's thinking,
equal in importance to natural selection, according to biologist W.
Ford Doolittle of Dalhousie University in Halifax, Nova Scotia,
Canada. Without it the theory of evolution would never have happened.
The tree also helped carry the day for evolution. Darwin argued
successfully that the tree of life was a fact of nature, plain for all
to see though in need of explanation. The explanation he came up with
was evolution by natural selection.
Ever since Darwin the tree has been the unifying principle for
understanding the history of life on Earth. At its base is LUCA, the
Last Universal Common Ancestor of all living things, and out of LUCA
grows a trunk, which splits again and again to create a vast,
bifurcating tree. Each branch represents a single species; branching
points are where one species becomes two. Most branches eventually
come to a dead end as species go extinct, but some reach right to the
top - these are living species. The tree is thus a record of how every
species that ever lived is related to all others right back to the
origin of life.
...The green and budding twigs may represent existing species, and
those produced during each former year may represent the long
succession of extinct species
For much of the past 150 years, biology has largely concerned itself
with filling in the details of the tree. "For a long time the holy
grail was to build a tree of life," says Eric Bapteste, an
evolutionary biologist at the Pierre and Marie Curie University in
Paris, France. A few years ago it looked as though the grail was
within reach. But today the project lies in tatters, torn to pieces by
an onslaught of negative evidence. Many biologists now argue that the
tree concept is obsolete and needs to be discarded. "We have no
evidence at all that the tree of life is a reality," says Bapteste.
That bombshell has even persuaded some that our fundamental view of
biology needs to change.
So what happened? In a nutshell, DNA. The discovery of the structure
of DNA in 1953 opened up new vistas for evolutionary biology. Here, at
last, was the very stuff of inheritance into which was surely written
the history of life, if only we knew how to decode it. Thus was born
the field of molecular evolution, and as techniques became available
to read DNA sequences and those of other biomolecules such as RNA and
proteins, its pioneers came to believe that it would provide proof
positive of Darwin's tree of life. The basic idea was simple: the more
closely related two species are (or the more recently their branches
on the tree split), the more alike their DNA, RNA and protein
sequences ought to be.
It started well. The first molecules to be sequenced were RNAs found
in ribosomes, the cell's protein-making machines. In the 1970s, by
comparing RNA sequences from various plants, animals and
microorganisms, molecular biologists began to sketch the outlines of a
tree. This led to, among other successes, the unexpected discovery of
a previously unknown major branch of the tree of life, the unicellular
archaea, which were previously thought to be bacteria.
By the mid-1980s there was great optimism that molecular techniques
would finally reveal the universal tree of life in all its glory.
Ironically, the opposite happened.
The problems began in the early 1990s when it became possible to
sequence actual bacterial and archaeal genes rather than just RNA.
Everybody expected these DNA sequences to confirm the RNA tree, and
sometimes they did but, crucially, sometimes they did not. RNA, for
example, might suggest that species A was more closely related to
species B than species C, but a tree made from DNA would suggest the
reverse.
Which was correct? Paradoxically, both - but only if the main premise
underpinning Darwin's tree was incorrect. Darwin assumed that descent
was exclusively "vertical", with organisms passing traits down to
their offspring. But what if species also routinely swapped genetic
material with other species, or hybridised with them? Then that neat
branching pattern would quickly degenerate into an impenetrable
thicket of interrelatedness, with species being closely related in
some respects but not others.
We now know that this is exactly what happens. As more and more genes
were sequenced, it became clear that the patterns of relatedness could
only be explained if bacteria and archaea were routinely swapping
genetic material with other species - often across huge taxonomic
distances - in a process called horizontal gene transfer (HGT).
At first HGT was assumed to be a minor player, transferring only
"optional extra" functions such as antibiotic resistance. Core
biological functions such as DNA replication and protein synthesis
were still thought to be passed on vertically. For a while, this
allowed evolutionary biologists to accept HGT without jeopardising
their precious tree of life; HGT was merely noise blurring its edges.
We now know that view is wrong. "There's promiscuous exchange of
genetic information across diverse groups," says Michael Rose, an
evolutionary biologist at the University of California, Irvine.
From tree to web
As it became clear that HGT was a major factor, biologists started to
realise the implications for the tree concept. As early as 1993, some
were proposing that for bacteria and archaea the tree of life was more
like a web. In 1999, Doolittle made the provocative claim that "the
history of life cannot properly be represented as a tree" (Science,
vol 284, p 2124). "The tree of life is not something that exists in
nature, it's a way that humans classify nature," he says.
Thus began the final battle over the tree. Many researchers stuck
resolutely to their guns, creating ever more sophisticated computer
programs to cut through the noise and recover the One True Tree.
Others argued just as forcefully that the quest was quixotic and
should be abandoned.
The battle came to a head in 2006. In an ambitious study, a team led
by Peer Bork of the European Molecular Biology Laboratory in
Heidelberg, Germany, examined 191 sequenced genomes from all three
domains of life - bacteria, archaea and eukaryotes (complex organisms
with their genetic material packaged in a nucleus) - and identified 31
genes that all the species possessed and which showed no signs of ever
having been horizontally transferred. They then generated a tree by
comparing the sequences of these "core" genes in everything from E.
coli to elephants. The result was the closest thing yet to the perfect
tree, Bork claimed (Science, vol 311, p 1283).
Other researchers begged to differ. Among them were Tal Dagan and
William Martin at the Heinrich Heine University in Düsseldorf,
Germany, who pointed out that in numerical terms a core of 31 genes is
almost insignificant, representing just 1 per cent of a typical
bacterial genome and more like 0.1 per cent of an animal's. That
hardly constitutes a mighty oak or even a feeble sapling - more like a
tiny twig completely buried by a giant web. Dagan dubbed Bork's result
"the tree of 1 per cent" and argued that the study inadvertently
provided some of the best evidence yet that the tree-of-life concept
was redundant (Genome Biology, vol 7, p 118).
The debate remains polarised today. Bork's group continue to work on
the tree of life and he continues to defend the concept. "Our point of
view is that yes, there has been lots of HGT, but the majority of
genes contain this tree signal," Bork says. The real problem is that
our techniques are not yet good enough to tease that signal out, he
says.
Meanwhile, those who would chop down the tree of life continue to make
progress. The true extent of HGT in bacteria and archaea (collectively
known as prokaryotes) has now been firmly established. Last year,
Dagan and colleagues examined more than half a million genes from 181
prokaryotes and found that 80 per cent of them showed signs of
horizontal transfer (Proceedings of the National Academy of Sciences,
vol 105, p 10039).
Surprisingly, HGT also turns out to be the rule rather than the
exception in the third great domain of life, the eukaryotes. For a
start, it is increasingly accepted that the eukaryotes originated by
the fusion of two prokaryotes, one bacterial and the other archaeal,
forming this part of the tree into a ring rather than a branch
(Nature, vol 41, p 152).
The neat picture of a branching tree is further blurred by a process
called endosymbiosis. Early on in their evolution, eukaryotes are
thought to have engulfed two free-living prokaryotes. One of these
gave rise to the cellular power generators called mitochondria while
the other was the precursor of the chloroplasts, in which
photosynthesis takes place. These "endosymbionts" later transferred
large chunks of their genomes into those of their eukaryote hosts,
creating hybrid genomes. As if that weren't complicated enough, some
early eukaryotic lineages apparently swallowed one another and
amalgamated their genomes, creating yet another layer of horizontal
transfer (Trends in Ecology and Evolution, vol, 23, p 268).
This genetic free-for-all continues to this day. The vast majority of
eukaryote species are unicellular - amoebas, algae and the rest of
what used to be known as "protists" (Journal of Systematics and
Evolution, vol 46, p263). These microscopic beasties have lifestyles
that resemble prokaryotes and, according to Jan Andersson of the
University of Uppsala in Sweden, their rates of HGT are often
comparable to those in bacteria. The more we learn about microbes, the
clearer it becomes that the history of life cannot be adequately
represented by a tree.
Hang on, you may be thinking. Microbes might be swapping genes left,
right and centre, what does that matter? Surely the stuff we care
about - animals and plants - can still be accurately represented by a
tree, so what's the problem?
Well, for a start, biology is the science of life, and to a first
approximation life is unicellular. Microbes have been living on Earth
for at least 3.8 billion years; multicellular organisms didn't appear
until about 630 million years ago. Even today bacteria, archaea and
unicellular eukaryotes make up at least 90 per cent of all known
species, and by sheer weight of numbers almost all of the living
things on Earth are microbes. It would be perverse to claim that the
evolution of life on Earth resembles a tree just because multicellular
life evolved that way. "If there is a tree of life, it's a small
anomalous structure growing out of the web of life," says John Dupré,
a philosopher of biology at the University of Exeter, UK.
More fundamentally, recent research suggests that the evolution of
animals and plants isn't exactly tree-like either. "There are problems
even in that little corner," says Dupré. Having uprooted the tree of
unicellular life, biologists are now taking their axes to the
remaining branches.
For example, hybridisation clearly plays an important role in the
evolution of plants. According to Loren Rieseberg, a botanist at the
University of British Columbia in Vancouver, Canada, around 14 per
cent of living plant species are the product of the fusion of two
separate lineages.
Hybrid humans
Some researchers are also convinced that hybridisation has been a
major driving force in animal evolution (see "Natural born chimeras",
and "Two into one"), and that the process is ongoing. "It is really
common," says James Mallet, an evolutionary biologist at University
College London. "Ten per cent of all animals regularly hybridise with
other species." This is especially true in rapidly evolving lineages
with lots of recently diverged species - including our own. There is
evidence that early modern humans hybridised with our extinct
relatives, such as Homo erectus and the Neanderthals (Philosophical
Transactions of the Royal Society B, vol 363, p 2813).
Hybridisation isn't the only force undermining the multicellular tree:
it is becoming increasingly apparent that HGT plays an unexpectedly
big role in animals too. As ever more multicellular genomes are
sequenced, ever more incongruous bits of DNA are turning up. Last
year, for example, a team at the University of Texas at Arlington
found a peculiar chunk of DNA in the genomes of eight animals - the
mouse, rat, bushbaby, little brown bat, tenrec, opossum, anole lizard
and African clawed frog - but not in 25 others, including humans,
elephants, chickens and fish. This patchy distribution suggests that
the sequence must have entered each genome independently by horizontal
transfer (Proceedings of the National Academy of Sciences, vol 105, p
17023).
Other cases of HGT in multicellular organisms are coming in thick and
fast. HGT has been documented in insects, fish and plants, and a few
years ago a piece of snake DNA was found in cows. The most likely
agents of this genetic shuffling are viruses, which constantly cut and
paste DNA from one genome into another, often across great taxonomic
distances. In fact, by some reckonings, 40 to 50 per cent of the human
genome consists of DNA imported horizontally by viruses, some of which
has taken on vital biological functions (New Scientist, 27 August
2008, p 38). The same is probably true of the genomes of other big
animals. "The number of horizontal transfers in animals is not as high
as in microbes, but it can be evolutionarily significant," says
Bapteste.
Nobody is arguing - yet - that the tree concept has outlived its
usefulness in animals and plants. While vertical descent is no longer
the only game in town, it is still the best way of explaining how
multicellular organisms are related to one another - a tree of 51 per
cent, maybe. In that respect, Darwin's vision has triumphed: he knew
nothing of micro-organisms and built his theory on the plants and
animals he could see around him.
Even so, it is clear that the Darwinian tree is no longer an adequate
description of how evolution in general works. "If you don't have a
tree of life, what does it mean for evolutionary biology?" asks
Bapteste. "At first it's very scary... but in the past couple of years
people have begun to free their minds." Both he and Doolittle are at
pains to stress that downgrading the tree of life doesn't mean that
the theory of evolution is wrong - just that evolution is not as tidy
as we would like to believe. Some evolutionary relationships are tree-
like; many others are not. "We should relax a bit on this," says
Doolittle. "We understand evolution pretty well - it's just that it is
more complex than Darwin imagined. The tree isn't the only pattern."
Others, however, don't think it is time to relax. Instead, they see
the uprooting of the tree of life as the start of something bigger.
"It's part of a revolutionary change in biology," says Dupré. "Our
standard model of evolution is under enormous pressure. We're clearly
going to see evolution as much more about mergers and collaboration
than change within isolated lineages."
Rose goes even further. "The tree of life is being politely buried, we
all know that," he says. "What's less accepted is that our whole
fundamental view of biology needs to change." Biology is vastly more
complex than we thought, he says, and facing up to this complexity
will be as scary as the conceptual upheavals physicists had to take on
board in the early 20th century.
If he is right, the tree concept could become biology's equivalent of
Newtonian mechanics: revolutionary and hugely successful in its time,
but ultimately too simplistic to deal with the messy real world. "The
tree of life was useful," says Bapteste. "It helped us to understand
that evolution was real. But now we know more about evolution, it's
time to move on."
Read our related editorial: Uprooting Darwin's tree
Two species become one
It could be time to ditch the old idea that hybrids are sterile
individuals that cannot possibly have played a role in shaping the
history of life on Earth. Hybridisation is a significant force in
animal evolution, according to retired marine biologist Donald
Williamson, formerly of the University of Liverpool, UK. His
conclusion comes from a lifetime studying marine animals such as
starfish, sea urchins and molluscs, many of which lead a strange
double life, starting out as larvae and metamorphosing into adult
forms.
The conventional explanation for metamorphosis is that it evolved
gradually, with the juvenile form becoming specialised for feeding and
the adult for mating, until they barely resembled each other.
Williamson thinks otherwise. He points out that marine larvae have
five basic forms and can be organised into a family tree based on
shared characteristics. Yet this tree bears no relationship to the
family tree of adults: near-identical larvae often give rise to adults
from different lineages, while some closely related adults have
utterly unrelated larvae.
BIOLOGICAL MASH-UP
It's as if each species was randomly assigned one of the larval forms
- which is exactly what Williamson argues happened. He believes
metamorphosis arose repeatedly during evolution by the random fusion
of two separate species, with one of the partners assuming the role of
the larva and the other that of the adult.
If that sounds unlikely, Williamson points out that many marine
species breed by casting their eggs and sperm into the sea and hoping
for the best, giving ample opportunity for cross-species
hybridisation. Normally nothing comes of this, he says, but "once in a
million years it works: the sperm of one species fertilises another
and two species become one". The most likely way for this biological
mash-up to function is if the resulting chimera expresses its two
genomes sequentially, producing a two-stage life history with
metamorphosis in the middle.
This explains many anomalies in marine biology, says Williamson. His
star witness is the starfish Luidia sarsi, which starts life as a
small larva with a tiny starfish inside. As the larva grows, the
starfish migrates to the outside and when the larva settles on the
seabed, they separate. This is perfectly normal for starfish, but in
Luidia something remarkable then happens. Instead of degenerating, the
larva swims off and lives for several months as an independent animal.
"I can't see how one animal with one genome could do that," says
Williamson. "I think the larval genome and the adult genome are
different."
Natural born chimeras
The idea that microbes regularly swap portions of genetic code with
individuals from another species doesn't seem so far-fetched (see main
story). But could the same process also have shaped the evolution of
multicellular animals? In 1985, biologist Michael Syvanen of the
University of California, Davis, predicted that it did (Journal of
Theoretical Biology, vol 112, p 333). Back then there was no way to
test that claim, but there is now.
Syvanen recently compared 2000 genes that are common to humans, frogs,
sea squirts, sea urchins, fruit flies and nematodes. In theory, he
should have been able to use the gene sequences to construct an
evolutionary tree showing the relationships between the six animals.
He failed. The problem was that different genes told contradictory
evolutionary stories. This was especially true of sea-squirt genes.
Conventionally, sea squirts - also known as tunicates - are lumped
together with frogs, humans and other vertebrates in the phylum
Chordata, but the genes were sending mixed signals. Some genes did
indeed cluster within the chordates, but others indicated that
tunicates should be placed with sea urchins, which aren't chordates.
"Roughly 50 per cent of its genes have one evolutionary history and 50
per cent another," Syvanen says.
The most likely explanation for this, he argues, is that tunicates are
chimeras, created by the fusion of an early chordate and an ancestor
of the sea urchins around 600 million years ago.
"We've just annihilated the tree of life. It's not a tree any more,
it's a different topology entirely," says Syvanen. "What would Darwin
have made of that?"
Didn't you hear?
Evolution is a bush when a tree does not fit the reasoning and it is a tree
when a bush does not fit the reasoning!
At other times evolution is just a lie.
hth.
--
It is all about the truth with:
^^^^^^^^^^^^^^^^^^^^^
·.¸Adman¸.·
^^^^^^^^^^^
.
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