Molecular Evolution: A Phylogenetic Approach

352 Pages·1998·25.505 MB·English

by  Roderick D.M. Page, Edward C. Holmes

Molecular Evolution
A Phylogenetic Approach
Roderic D .M. Page
Universityo f Glasgow
Edward C. Holmes
Universityo f Oxford
b
..
Blackwell
Science
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Molecular evolution: a phylogenetic
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First published 1998 Edward C. Holmes.
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Contents
Acknowledgements, v
1 The Archaeology of the Genome, 1
2 Trees, 11
3 Genes: Organisation, Function and Evolution, 37
4 Genes in Populations, 89
5 Measuring Genetic Change, 135
6 Inferring Molecular Phylogeny, 172
7 Models of Molecular Evolution, 228
8 Applications of Molecular Phylogenetics, 280
References and Bibliography, 315
Index, 335
iii

·A ckn.owledgements
We thank Simon Rallison for commissioning the book, and for negotiating the
contract at the same time that R.D.M.P.'s wife, Antje, was working in Blackwell's
royalties department. This, of course, was merely a fortuitous coincidence. In
any event, Antje's gentle prodding helped speed the completion of one half
of the book. Ian Sherman shepherded the book to its conclusion with great
patience in the face of our ludicrously optimistic assessments of when we would
be finished. Several anonymous referees provided very helpful comments while
Tim Anderson, John Brookfield, Mike Charleston, Nick Grassly, Rosalind
Harding, Peter Holland, Mark Ridley and Vmce Smith read chunks of the
manuscript (some very large) for which we are extremely grateful. Jake Baum's
input into part of Chapter 4 was also much appreciated. Finally we thank Paul
Harvey, Wyl Lewis, Mark Ridley at-id Rachel Urwin for encouragement and
inspiration.
Roderic D.M. Page
Glasgow
Edward C. Holmes
Oxford
V

Chapter 1
The Archaeology of the Genome
1. 1 The nature of molecular evolution
1.2 What this book will cover
1.3 Further reading
1.1 The nature of molecular evolution
Although a sometimes unpleasant occupant of our respiratory tracts, Haemophilus·
injluenzae, a small Gram-negative bacterium, was an unlikely candidate to
symbolise a revolution in molecular biology. But this is exactly what happened
in July 1995 when the entire 1830137 DNA base pairs of its genome was
published-the first of a free-living organism. A new era in biological science
had begun. Soon after Haemophilusi njluenzaec ame the first complete genome
from a eukaryote - that of the yeast Saccharomycesc erevisiae,f ollowed by
Methanococcujsa nnaschii, the first representative of the third domain of cellular
life, the Archaea. In the next few years molecular biology will claim its biggest
prize-the 3.3 billion bases that make up the genome of Homo sapiens.
DNA sequences are valuable because they provide the most detailed
anatomy possible for any organism - the instructions for how each working
part should be assembled and operate. Much of modern biology now relies
on unravelling the information stored within gene sequences and this is true
of evolutionary studies, where gene sequences are now recognised as an
invaluable document of the history of life on earth. It is the aim of this book to
show what evolutionary information is written into gene sequences and
how this information might be recovered. This is the science of molecular
evolution.
Take, for example, Haemophi[us injluenzae, Saccharomycesc erevisiae and
Methanococcujasn naschii.U ntil recently, most textbooks divided cellular organisms
into the eukaryotes, which possess a cell nucleus, and the prokaryotes, which
do not. This tidy world was upturned in the 1970s when Carl Woese and
colleagues, using the highly conserved 16S ribosomal RNA (rRNA) gene,
showed that there were in fact two very different groups of prokaryotes- the
Eubacteria like Haemophilusi njluenzae, now simply referred to as the Bacteria,
and the Archaebacteria whose members include Methanococcujsa nnaschii, now
known as the Archaea (Fig. 1.1). Until the rise of molecular biology in the
1970s, this third great branch of life was lost from us but with molecular
phylogenies we have learned that the A rrhaea are in fact probably more
1
2 CHAPTER I
Bacteria (Eubacteria) Archaea (Archaebacteria)
Green non-sulphur 1 Euryarchaeota
bacteria Halophiles
Gram-
positives
Eukarya (Eukaryotes)
Purple bacteria
Fungi
Cyanobacteria
Plants
F/avobacteria
Microsporidia
Diplomonads
Fig. 1.1 Phylogenetic relationships between members of the three domains of cellular
life--the Archaea, Bacteria and Eukarya, based on rRNA. The Archaea can be further
divided into the Crenarchaeota (also known as the eocytes) and the Euryarchaeota
(methanogens and halophiles). Although popular, this tree is by no means universally
accepted. For example, there is still some debate as to whether tbe Crenarchaeota are in
fact more closely related to the eukaryotes than they are to the other Archaea. From
Morell (1996) and originally Olsen and Woese (1993), with permission.
closely related to the eukaryotes than they are to the Bacteria, even though
they lack a cell nucleus and represent some of the most extreme forms of life
on earth. Methanococcujas nnaschii,f or example, lives on deep-sea hydrothermal
chimneys ('white smokers'), at pressures of 200 atmospheres and temperatures
of 85°C! Gene sequences dearly contain a unique and important archaeological
record of life's first tentative steps.
The importance of 16S rRNA for those interested in the early evolution of
life lies in its slow evolution, which allows the historical record preserved in its
gene sequences to be kept relatively intact. Other genes evolve a good deal
more rapidly and so allow us to reconstruct historical pathways that have
been trodden only recently. One such example of evolution in the fast lane
are the genes which make up the human immunodeficiency virus (HIV},t he
cause of the disease AIDS. HIV evolves about a million times faster than human
genes, which is why developing effective drugs and vaccines is such a problem.
This super-fast rate of evolutionary change also means that sequences from
this virus can be used to retrace its spread through populations. Studies of
this sort have had some dramatic results. For example, in 1990 the Centers
. for Disease Control (CDC) in Atlanta received reports of AIDS in a young
woman in Florida whose only risk of FIIV infection was seemingly that she
had previously been treated by a dentist suffering from AIDS. A subsequent
investigation then uncovered a number of the dentist's other former patients
THE ARCHAEOLOGY OF THE GENOME 3
who were also HIV infected. Could it be that these people were somehow
infected by their dentist? A phylogenetic tree reconstructed on part of the
envelope (env) gene of the virus revealed that those patients with no other
risk factors for HIV infection had sequences closely related to those of the
dentist, strongly suggesting that he had infected them, whilst the sequences
from two patients who could have been infected in other ways were separated
from the dentist on the tree (Fig. 1.2). The HIV genome had therefore stored
evolutionary info~ation, in the form of the mutations which had accumulated
between transmission events, which could recount the very recent history of
its spread.
Despite the attention given to it today, the ability to sequence entire genomes
is just the latest in a series of milestones which mark the development of
molecular evolution. The roots of this science were laid early in this century
by George Nuttall, a Cambridge biologist, who (along with a contemporary,
Uhlenhuth, working in Germany) mixed sera and antisera from different
species in an attempt to discover the 'blood relationship' between them. The
r---------------------------
,
Fig. 1.2 The case of the
Dentist
Florida dentist. Each branch
represents tlie sequence from
Patient C
part of the envelope (env)
gene ofHIV-1. Vrral
sequences were obtained
from the dentist and seven of
his former patients (labelled A
to G), also infected with the Patient B
virus. Five of these patients
Patient E
(A, B, C, E and G), have
sequences very closely related .._ ___ Patient A
to those of the dentist (boxed),
suggesting that he infected
------- Dentist
them. Two of his other former
patients (D and F) had other
risk factors for HIV infection
and their viruses are
separated from the dentist by
sequences taken from local
controls (LC)-HIV-infected
individuals living within a
90-mile radius of the dentist's
surgery. Because HIV-1 is so
variable, two different
sequences are included for
the dentist and patient A.
Data taken from Ou et al.
(1992j.
4 CHAPTER 1
idea was that the more closely related the species, the stronger the cross-reaction
between sera and antisera. Today we know that this depends on the extent of
genetic similarity between them. While Nuttall's techniques appear crude by
today's standards, his work establishes the most important principle in
molecular evolution-that the degree of similarity between genes reflects the
strength of the evolutionary relationship between them.
In the 50 years that followed Nuttall's work, studies of evolution at the
molecular level made little progress, largely because there was a paucity
of data to work with. This sits in stark contrast to the revolution which took
place in the theoretical wing of evolutionary biology resulting in the 'neo
Darwinian synthesis' of the 1930s. This synthesis, the basis of modem
evolutionary thought, also forms a backdrop to many of the later debates
that enveloped molecular data when it first became available. In this book
we hope to describe an even more modern synthesis-that of molecular
biology vvith phylogenetics-which enables us to explain the amazing diversity
of genomes.
The 1950s witnessed a blossoming of molecular evolution. Two events were
primarily responsible for this renaissance. The first was the discovery, by James
Watson and Francis Crick in 1953, of the molecular structure of DNA-the
double helix. This proved to be the key piece in the jigsaw that revealed DNA
as the molecule responsible for carrying between generations the instructions
for how organisms should be assembled and work correctly. At its most
fundamental level, evolution can be thought of as changes in the structure of
DNA. The second event took place in 1955 when Fred Sanger and colleagues,
also working in Cambridge, published the first comparison of amino acid
sequences {the product of DNA) from different species, in this case of the
protein insulin from cattle, pigs and sheep. Although less famous than the
breakthrough of Crick and Watson, this was the first study to reveal how species
differed at the molecular level: cattle, pigs and sheep had three amino acid
differences, indicating that their insulins had evolved along with their more
obvious anatomical features.
By the early 1960s, the amino acid sequences of a variety of proteins
had been determined. The next task was to accurately recover evolutionary
information from these sequences. This required a simple mathematical de
scription of the process of gene sequence change over time. In other words, it
was necessary to build a model of molecular evolution. Mo.dels make it easier
to reconstruct past events and make predictions about future changes, and are
an important part of molecular evolution. Although the first models were
developed ahnost 40 years ago, many of their basic elements are still relevant
today and will be encountered many times in this book. The most basic was
the assumption that evolution at the molecular level was a largely stochastic
process, dominated by chance events. It was also realised that the number of
sequence changes we observe between genes might not be the same as the
number that has actually taken place: because there are only four DNA bases