The network of life: genome beginnings and evolution. Introduction.

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The
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genomes render the tree of life only an approximation—
useful in some contexts, less so in others—or indeed
starting at least 2.4 billion years ago (reviewed by
Genomic-based rooting studies indicate that the
e the
tmos-
ryotic
proteins, as a catalyst. Progress in this field is rapid.
Just recently, ‘self-sustained’ replication of an RNA
enzyme was demonstrated (Lincoln & Joyce 2009). It
is possible that relics dating from this early world may
One contribution of 11 to a Theme Issue ‘The network of life:
genome beginnings and evolution’.genome beginnings: what preceded genomes? How were
the first genomes organized, and according to what prin-
ciples, by what mechanisms and along what paths did
they begin to diversify? Our expert contributors explore
genome diversity—among the deepest lineages, and
from the highest taxon levels to intriguing individual
groups were established. Thus, cellular life is likely to
have been present on Earth considerably earlier.
But genome beginnings extend deeper than this.
Before the cenancestor, life must have existed in forms
that are difficult, but not impossible, to study using
genomic sequences. Many scientists think that the ear-
liest life may have functioned using RNA, rather thanorigin and evolution of genomes. Key questions includehave been anticipated a dozen years ago.
papers in this theme issue of Philosophical
tions B present important perspectives on the
double-membrane prokaryotes, which includ
cyanobacteria responsible for Earth’s oxygen a
phere, originated after most of the major prokafrom the multi-genome era much more restricted in
scope, and subject to many more qualifications, than
Falkowski & Isozaki 2008, and by Fischer 2008).Introd
The network of life:
and ev
Keywords: genome origins; lateral gen
evolution of viruses; evolutio
The genome sequence is an icon of early twenty-first
century biology. Genomes of nearly 2000 cellular
organisms, and from many thousands of organelles
and viruses, are now in the public domain. For biologi-
cal research in individual species, the genome
sequence increasingly provides the common reference
for the application of polymorphism, transcriptomic,
proteomic and other genome-scale data to problems
of development or disease. More recently, through
metagenomic sequencing, the composition and func-
tion of ecosystems are being explored at the molecular
level. Genomes are now central to genetics, cell and
developmental biology, molecular and systems biology,
population biology and ecology.
At the same time, one cannot but be struck by the
diversity of genomes, both across the living world and,
in many cases, within genera or species. Whatever con-
straints may be imposed by their central role in genetics,
functional and cell biology clearly do not stand in
the way of genomes ranging in size over eight orders
of magnitude and exhibiting remarkable diversity and
variation in gene content, gene order and organization.
Perhapsmost unexpected of all is the substantial decou-
pling, now known inmost, although not all, branches of
organismal life, between the phylogenetic histories of
individual gene families and what has generally been
accepted to be the history of genomes and/or their
cellular or organismal host lineages. The tree of life
paradigm consolidated by Darwin’s Origin of Species
(1859), but itself arising from a much older tradition
of natural history, seems likely to emerge, if at all,216is the tree of life paradigm now a barrier to a richer,
more integrative understanding of life on Earth?
We have grouped these papers to reflect the chron-
ology and significant evolutionary events in the origin
and evolution of genomes. The emerging narrative is
fresh with competing concepts and theories. In other
words, in the field of genome evolution, the scientific
process is alive and healthy.
1. GENOME BEGINNINGS AND DEEP
LINEAGES
Life has existed on Earth for much of its 4þ billion
year history. Evidence in the form of microscopic fos-
sils, molecular signatures and isotopic abundances
arguably indicates that life has inhabited our planet
for considerably longer than 3 billion years. New
studies point to an increase in oxygen in the atmos-
phere, a relatively late stage in the evolution of life,ction
enome beginnings
lution
ic transfer; tree of life; network of life;
of developmental pathways
species—discussing the processes that have shaped,
and continue to shape, genomes of bacteria, archaebac-
teria and eukaryotes. A major theme is lateral (horizon-
tal) genetic transmission, some (perhaps much) of
which involves the abundant small elements that per-
vade the biosphere—viruses, plasmids, gene transfer
agents—that can not only shuttle DNA among cellular
organisms but also modify it in the process. Do the
frequency and impact of lateral transfers on (many)
Phil. Trans. R. Soc. B (2009) 364, 2169–2175
doi:10.1098/rstb.2009.00469 This journal is q 2009 The Royal Society

unequivocal evidence (e.g. from the spread of antibiotic
2170 M. A. Ragan et al. Introduction. The network of lifeexist even today in our genomes, in the distinct gene
lineages known as informational and operational
genes (Rivera et al. 1998). These gene classes are
found in all eukaryotes and prokaryotes, including
humans. Informational genes function in processes
such as protein synthesis and RNA transcription,
suggesting that they may have originated during an
RNAworld, whereas the operational genes that perform
routine cellular processes such as making cell walls and
synthesizing amino acids may have descended from
other organisms at different times. Certainly our cells
contain genes that are thought to be derived from the
RNA world, but our story here starts later, with
the last common ancestor of cellular life.
As genomes occur in organisms and every organism
contains at least one genome, we begin the story of
genome evolution with the cenancestor, or last
common ancestor of cellular life. Given the extent of
lateral gene transfer, the cenancestor was unlikely to
have been a single cell, and can better be conceptualized
as a population, or populations, containingdiverse organ-
isms. Furthermore, these organisms probably did not live
at the same time. This may sound incredible, but follows
from the way populations evolve. For example, a little
more than 15 years ago we learned from Allan Wilson
that the mother of all humans lived approximately
200 000 years ago in Africa. This Eve was first identified
by comparative sequencing of human mitochondrial
genomes, which are maternally inherited. Subsequently,
the father of us all was identified by comparative sequen-
cing of human Y chromosomes: he lived only 50 000
years ago, and even if he were Methuselah, he could
never have known mitochondrial Eve.
Because different human genes have followed
different evolutionary pathways, we must think of the
evolution of (multiple) populations. This is even more
the case among prokaryotes, whose genes continue to
evolve along different, sometimes anastomatizing,
paths. If the ‘ancestor of all cellular life’ did not live in
any one place or at any one time, there was no single
discrete ‘last universal common genome’.
Since the mid-nineteenth century, the living world
has been represented as a genealogical tree in which
some major lineages extend back in time towards the
common cellular ancestor, while others became estab-
lished only more recently. Lake, Skophammer, Herbold
and Servin emphasize the importance of ordering pre-
sent-day lineages according to time of appearance,
and identifying the deepest known lineages—i.e. rooting
the tree of life. In this way, it ‘becomes possible to
relate genetic, biochemical, ultrastructural and behav-
ioural innovations to geological, paleontological and
climatological events, thereby allowing one to trace
the interdependent histories of the Earth and its micro-
biota, and to test theories for the order of appearance
of novel biological innovations’—for example, the
order of appearance of methanogenesis, respiration
and substrate-level phosphorylation, heterotrophy
versus autotrophy, single versus double-delimiting
membranes and thermophily versus mesophily. These
advantages remain even if—as other papers in this
theme issue discuss in detail—genomic or cellular
relationships turn out to be better represented as a
ring, network or other topology.Phil. Trans. R. Soc. B (2009)resistance) that genetic information is readily transmitted
laterally within some populations, particularly but not
exclusively in strongly selective environments; some pro-
cesses are well characterized at the molecular level, and a
plenitude of potential vectors (the mobilome: Frost et al.
2005) appears to be available.
Although there is considerable consensus that these
lines of evidence point to lateral genetic transfer
(LGT) as potentially widespread and physiologically
important, many issues remain unresolved. Ragan and
Beiko organize these by Process & mechanism, Quantifi-
cation, and Impact. It is not known, for example, how
much each process (transformation, transduction,
conjugation) or each type of vector contributes to
LGT, either globally or within a species; vectors can
leave telltale clues, but in some cases interpreting
these clues has proved to be trickier than expected.
Structure is apparent in the living world, implying the
existence of constraints to exchange: are these mainly
external to organisms (lack of contact, lack of genes to
work with, selective pressure for small genome sizes),
or mainly internal (barriers to uptake and recombina-
tion, complexity of integrating new genes into the hostLake and colleagues use insertion–deletion events
(indels) in eight sets of paralogous genes to exclude the
root from many regions of the tree (or network) of life
as presently known. In this way, they localize the root
to the base of two major lineages, one consisting of
the actinobacteria and the double-membrane
(Gram-negative) prokaryotes, the other consisting of
archaebacteria and firmicutes. Their approach is pro-
gressive, in that the root (or root area) can be excluded
from additional regions as new genomic data appear
(i.e. as we realize that certain regions are not the most
ancient) without having to re-analyse everything that
has gone before. Using this approach, it can already be
concluded that double-membrane prokaryotes (includ-
ing the cyanobacteria, mentioned above) were derived
from simpler single-membrane prokaryotes, and that
members of the cenancestral population were enclosed
by ester-linked lipid membranes and surrounded by a
peptidoglycan layer. Components of the toolkit for
archaebacterial lipid biosynthesis seem also to have been
present in the common ancestral population, or at least
immediately ancestral to the bacilli and archaebacteria.
2. LATERAL GENETIC TRANSFER
Descent with modification has long been accepted
as the framework within which the transmission of
genetic determinants is best explained, at least in mor-
phologically complex eukaryotes. As for bacteria and
archaebacteria, the genomic era has thrown up data
that do not fit a straightforward vertical-descent
model. A surprising number of gene trees are, in part,
topologically discordant with each other and/or with
accepted organismal relationships. Many genes are dis-
tributed across genomes and taxa in patterns that
cannot be reconciled parsimoniously with a purely ver-
tical pattern of genetic transmission and gene loss, and
sometimes exhibit compositional features (e.g. dinucleo-
tide content) distinct from the surrounding genome and
characteristic of more-distant taxa. Further, there is

One of these has been the widespread acceptance—
Introduction. The network of life M. A. Ragan et al. 2171network)? Lateral origins have been claimed for geno-
mic regions of diverse size, from a few nucleotides to
complete chromosomes; but interestingly, domons
(exonic regions corresponding to protein domains,
hence presumably to component units of function) do
not appear to be a primary unit of LGT (Chan et al.
2009). Many genes have mixed heritage, and these
authors urge greater precision in describing them as
vertical or lateral, concordant or discordant.
Ragan and Beiko ask how we should think about
and express the extent of LGT: as the proportion of
genomes affected by LGT (close to 100%), the pro-
portion of genes with at least one lateral event in
their history (estimates in the range 25–50% or
more are not infrequent) or the proportion of internal
graph edges that are concordant with a reference tree
(perhaps 5–15% for subsets of orthologous gene
trees). More generally, is it better to count transfers,
or to model transfer? Are different evidence types—
say, gene trees and distribution data—complementary?
How much LGT is undetectable? Can the biological
sources of transfers be identified? How long do later-
ally transferred sequences persist in a genome? Can
ancient metabolisms be reconstructed? If LGT has
been frequent, then physiology (hence ecological
niche) has presumably changed repeatedly over time.
Introgressed genetic material must be connected into
the cellular networks of genetic regulation, molecular
interactions, metabolite flow and energetics. Although
the field is in its infancy, Ragan and Beiko summarize
the ‘network view’ of cell as: (i) cellular networks contain
both highly and weakly connected nodes; (ii) a species-
specific core subset of nodes is present in all strains of a
species, while other nodes may be found in some or few
strains; (iii) core nodes are chromosomal, whereas periph-
eral nodes may or may not be; (iv) core nodes typically
describe functional units, e.g. operons ormacromolecular
complexes; (v) core nodes tend to be more highly con-
nected and more highly expressed than peripheral
nodes; (vi) core-node genes accumulate point mutations
more slowly than do peripheral-node genes; (vii) periph-
eral nodes are more often implicated in functions that
are directly affected by the environment; and (viii) net-
works evolve by the addition of peripheral nodes. It
remains to be seen how general these prove to be: do all
prokaryotes have a more-or-less stable, taxon-specific
core genome? What factors determine the size and com-
position of the peripheral genome, and how large is the
pan-genome? The latter questions become important in
the arguments of Dagan and Martin, below.
At least in bacteria and archaea, LGT is often
portrayed solely as a confounding factor for genome
phylogeny: it disrupts the ‘workable alignment of phe-
netics and cladistic practices’ (Doolittle, see below). A
recurring theme within this theme issue is that this, by
itself, is too narrow a view. LGT is a central modality
of genome evolution, and treating it purely as a distrac-
tion from vertical (parent-to-offspring) transmission
hinders us from appreciating the broader fabric of
evolution, specifically the plurality of mechanism and
pattern beyond a unitary tree of life. Fournier,
Huang and Gogarten argue further that LGT events,
once properly recognized against the background
‘plurality signal’, can actually benefit phylogeneticPhil. Trans. R. Soc. B (2009)variously as metaphor, hypothesis, model or true his-
torical description—of a single unitary tree of life.
The growing appreciation that the tree of life may over-
simplify reality, or indeed be fundamentally incorrect,
necessarily bears profound implications across the
hard sciences, and well beyond.
Haggerty, Martin, Fitzpatrick and McInerney illus-
trate the extent of disjunction possible between gene
and genome histories. Working with 27 complete gen-
omes from the well-studied YESS (Yersinia, Escherichia,
Salmonella, Shigella) group of enteric bacteria, the
authors probe different subsets of the data: the entire
complement of 16S rRNA genes, three commonly ana-
lysed housekeeping genes and their concatenation, a
concatenated nucleotide alignment of all 1408 unam-
biguously orthologous genes, and a supertree of the
same 1408 genes. Within the YESS group they find
three major 16S rRNA subtrees corresponding to a
Yersinia type, a Salmonella type and an Escherichia/
Shigella type. Similar genus-level subtrees were
recovered from the other approaches; but beyond this,
agreement largely breaks down. Within-species relation-
ships are inconsistent among trees inferred from the
three individual protein-coding genes; between each of
these and the tree inferred from their concatenated
sequences; and with the rRNA and 1408-gene trees.
The two 1408-gene trees (and minimum-evolution
tree of their concatenated nucleotide data, and thereconstruction, specifically by allowing dates (relative
or absolute) to be assigned to speciation events.
Sudden radiations are unexpected under a steady-
state model of extinction and speciation, and their
presence therefore requires explanation. For example,
the radiation of major lineages deep in the bacterial
tree may have resulted from niche expansion following
a mass extinction some 3.8–4.1 Gyr ago.
Transporters originating from chlamydial endo-
symbionts may have contributed to a favourable
environment for the establishment of plastids via
cyanobacterial endosymbiosis; more broadly, novel
functions are sometimes seen to have been recruited
from multiple sources in multiple events (‘concerted
gene recruitment’: Huang & Gogarten 2008). Two
enzymes that activate acetate for input into acetoclastic
methanogenesis in Methanosarcina appear to have ori-
ginated in cellulolytic clostridia; directionality of the
transfer is clear from the phyletic distribution, and
from the adjacency of their genes in both source and
recipient genomes. Moreover, modern representatives
of the two taxa commonly co-occur in aquatic environ-
ments. Fournier et al. therefore infer thatMethanosarcina
began to contribute to acetoclastic methane production
in the environment only after cellulose (e.g. aquatic
plants) became abundant in aquatic environments, i.e.
later than 475 Myr ago.
3. THE TREE OR NETWORK OF LIFE
Darwin’s hypothesis—that all modern organisms are
historically related via genetic descent, with modifi-
cation, from one or a very small number of common
ancestors—has had the profoundest intellectual, scien-
tific and social consequences over the last 150 years.

Doolittle situates the tree of life in broader scienti-
2172 M. A. Ragan et al. Introduction. The network of lifesupertree) are topologically identical within Salmonella
and disagree only slightly within the Escherichia/Shigella
clade, but conflict seriously within Yersinia. Compared
with other taxa the YESS genomes are well sampled,
and there is no reason to believe that their genes are
particularly refractory to phylogenetic analysis; yet
within each of these three genus-level groups, different
standard samples of the YESS genomes fail to converge
on a single consistent signal, presumably due to
frequent LGT. Thus, the concept genome tree does not
appear to be helpful, or even especially meaningful, in
this important taxon.
Dagan and Martin lead us farther into the network
paradigm of genome evolution. As introduced above,
genomes of bacteria and archaea often consist of a
taxon-specific set of core genes, and a potentially
much larger set of peripheral genes associated more
transiently with, and shared among, genomes. For any
genome, the size of its peripheral gene set can vary
over time but is constrained by physical factors and
the necessity of maintaining transcriptional control
(Gagen & Mattick 2005), and except in specialized
cases of genome degeneracy (e.g. intracellular parasites:
Moran 2003) there is little reason to think that ancestral
genomes were, on average, significantly larger or smaller
than present-day examples. Any accurately inferred
gene tree can be reconciled with a discordant external
expectation (reference phylogeny) by assuming some
number of ancient gene duplications with subsequent
differential loss. But each time we assume this, we
assume that an additional gene was present in the
genome of that ancestor (Dagan & Martin 2007).
Over all such cases, this would lead to unrealistically
large ancestral genome sizes—the ‘genome of Eden’ of
Doolittle et al. (2003). By contrast, assuming LGT
reduces the inferred sizes of ancestral genomes.
To capture this broader picture of genome dynamics
(including gene loss and LGT), we need to describe
and depict phylogenetic relationships of all genes, not
only the (often relatively small) taxon-specific con-
served genomic core; and for this we require a network
perspective and tools. Dagan and Martin depict a net-
work of vertical inheritance and lateral exchange for
181 prokaryotic genomes, as well as sub-networks
within and among internal and external nodes, but
allow that it ‘will probably take some time before
LGTamong prokaryotes and the endosymbiotic origins
of chloroplasts and mitochondria can be reconstructed
at the computer in a unified framework that starts
with genome sequences and ends up with a network
that is both readily printable and readily interpretable’.
These authors extend this perspective to eukaryotes,
where the archaebacterial nature of the genetic appar-
atus does not predict the eubacterial nature of energy
metabolism. LGT is known but is much less extensive
than among prokaryotes: even in Entamoeba, which har-
bours prokaryotic endosymbionts, only 1–2% of
nuclear genes might have been acquired laterally
(Loftus et al. 2005). On the other hand, large-scale
gene transfer has occurred from endosymbionts to
host nucleus during the establishment of mitochondria
and plastids, and many more eukaryotic nuclear genes
share homologs with bacteria than with archaebacteria.
Which among these came from the proto-organelles?Phil. Trans. R. Soc. B (2009)fic, philosophical and social contexts. He argues
(following Panchen 1992 and Doolittle & Bapteste
2007) that Darwin viewed the tree as a hypothesis
about evolutionary process and the consequent pat-
terns among organismal form and function. Darwin
mobilized data on animal breeding, comparative anat-
omy and especially population dynamics, concluding
from these that selection caused descent to be with
modification and speciation, ergo tree-like. The tree
has proved to be an adequate representation of genea-
logical history within morphologically complex
eukaryotes in particular—the main focus of phyloge-
netics (and later, molecular phylogenetics) during
their formative years. Of course neither Darwin nor
his contemporaries (before 1859, at least) knew
much about microbes or microbial biodiversity. But
as knowledge grew, so did scepticism that, in view of
their morphological simplicity and physiological
flexibility, prokaryotes could ever be brought into a phy-
logenetic framework (Woese 1987). In the end,
the ‘heroic effort’ of Woese and colleagues to extend
the tree of life to bacteria and archaea was defeated
because these organisms have not, in reality, evolved
(purely) by descent with modification on a unitary tree.
Might there nonetheless be a unitary, hierarchical,
well-behaved tree of cells? Doolittle characterizes this
as a watering-down of Darwin’s theory, and an evasion
of the true aim of phylogenetics, i.e. the reconstruction
of evolutionary paths. Just as not everything in evol-
ution can be explained by natural selection (Gould’s
process pluralism), similarly not everything in phylogeny
boils down to trees (Doolittle’s pattern pluralism). The
author proposes, as a general formulation, that ‘genetic
mechanisms (broadly construed) and population and
ecological process (broadly construed) that we already
for the most part understand, operating over enormous
time, are responsible for the diversity of life we see
around us, and for the adaptedness of living things’.
We no longer have a universal hierarchical classification
or a unitary, bifurcating tree of life, but our toolkit still
contains powerful methodologies (genetics, population
biology, ecological theory) to explain the history of life
and the diversity of the natural world.
4. GENOMIC ORIGINS OF EUKARYOTES
Eukaryotes are unique in possessing a membrane-
delimited compartment, the nucleus, in which the
chromosomes are found. Eukaryotes may further
contain additional types of membrane-delimited,
genome-containing compartment, e.g. mitochondria
and plastids. Our authors argue that mitochondria are
ancestral in the eukaryotic lineage and were subsequently
lost or modified in various lineages, although alternativeThe authors argue that unlike the few ‘oddly branching
copies of highly similar genes’ currently thought to have
been transferred more recently among eukaryotes,
genes from the proto-organellar endosymbionts
contributed fundamentally new physiology, e.g. mito-
chondrial ATP synthesis and photosynthesis. In this
Dagan and Martin support the proposal of Allen
(2003) that the retention of genomes in organelles has
allowed redox-dependent regulation of gene expression.

darian and sponges, more-ancient clades that lack
Introduction. The network of life M. A. Ragan et al. 2173scenarios have been proposed. There is near-unanimity
that these two organelles, at least, have descended from
free-living bacteria that, analogously with present-day
examples, became entrapped in an endosymbiotic
relationship. However, modern free-living relatives of
the likely proto-organelles have genomes 10- to 100-fold
larger than most mitochondria and plastids. Were the
missing genes simply lost, or were they transferred to
the nuclear genome (which, to be sure, is extensively
‘prokaryotic’ as assessed by sequence similarity and
domain content); and why were specific genes, or
indeed any genes at all, retained in what is now the
organellar nucleus? Have other non-eukaryotic lineages
been merged into the eukaryotic nucleus without leaving
a telltale organellar vestige? Several papers in the earlier
sections discuss early origins of major extant lineages,
including that of the eukaryotic nucleus. Here, two
papers explicitly discuss the origin of eukaryotes and
their phylogenetic relationship to prokaryotes, and their
complex morphology.
Foster, Cox and Embley examine relationships
among the most ancient lineages; however, unlike pre-
vious authors they focus on the origin of the eukaryotic
nuclear lineage. Two hypotheses in particular have
received wide attention: the three-domain tree, in
which eukaryotes are usually presented as the sister line-
age to archaea, and the eocyte tree, in which eukaryotes
arise from within archaea as the sister lineage to cre-
narchaeotes. The application of molecular phylogenetic
approaches to such ancient events is intrinsically diffi-
cult: signal is not only weak, but potentially confounded
by the inability of evolutionary models and phylogenetic
methods to correct for site saturation, across-site and
across-tree rate variation, compositional heterogeneity
and unrecognized homoplasy. Using computational
simulations, the authors find that substitutional satur-
ation can be delayed by accounting for among-site
rate variation, potentially leaving signal in the data.
They develop a model that attempts to accommodate
among-site and across-tree compositional heterogen-
eity, and apply it in conjunction with a number of
sophisticated inference methods.
With an rRNA-sequence dataset, diverse methods
support the three-domain tree in the absence of correc-
tion for compositional heterogeneity, but support
increases for the eocyte tree using their corrective
model. A concatenated 41-protein amino acid dataset
that emphasizes core genetic machinery (slightly
expanded from Cox et al. 2008), when recoded in
order to minimize homoplasy in the analysis of deep-
level phylogenetic relationships, supports the eocyte
tree with or without their model. Four groups (bacteria,
euryarchaeotes, crenarchaeotes, eukaryotes) are indivi-
dually recovered as monophyletic in most analyses,
although interestingly, using standard amino acid
coding, amethod that is considered to be relatively resist-
ant to long-branch attraction artefacts, reconstructs
euryarchaeota as a paraphyletic group, with Pyrococcus
as the sister group of crenarchaeota and eukaryotes.
If real, this implies that crenarchaeotes (i.e. eocytes)
plus eukaryotes arose from within the euryarchaea.
Complex morphology and the complex develop-
mental pathways that bring it about are the other
eukaryotic characteristics discussed in this themePhil. Trans. R. Soc. B (2009)diverse cell types and complex morphogenesis. What
was the ancestral role of these genes, and how were
they assembled into a functional developmental
system in bilaterians?
Early bilaterians (predating the divergence of
protostomes from deuterostomes) may not have been
particularly complex, with cell-type specification and
regional patterning but not complex morphogenetic
development (Erwin & Davidson 2002). Modern bila-
terians have six major signalling pathways (Wnt,
TGF-b, Notch, Hedgehog, Jak/STAT and RT), all of
which, together with a diversity of transcription
factors, are present in cnidarians as well. Thus, the
last common ancestor of metazoa could ‘specify mul-
tiple cell types, establish body axes, array different cell
types along these axes and produce multicellular struc-
tures’ although it seems to have lacked the ‘regulatory
complexity and depth of transcription factors and
microRNAs required to produce complex gene regulat-
ory networks’ and hence complex morphologies. In this
context Erwin reminds us of the Eidacarian fauna, most
of which is believed to have predated the protostome–
deuterostome divergence; we might think of their
diverse and remarkable morphologies as outcomes of
a critical period in the evolution of regulatory networks,
as more and different types of regulatory components
were recruited into networks and different degrees
and patterns of connectivity were explored.
Even deeper in the animal tree, genomic sequencing
of the choanoflagellate Monosiga brevicollis has un-
covered a considerable diversity of cell adhesion,
extracellular matrix, signal transduction and cell
differentiation elements including 78 protein domains
shared exclusively by choanoflagellates and metazoa
(albeit often in different protein contexts, hence
presumably without the same functionality, e.g. in
cell–cell adhesion). The presence of many ‘bilaterian’
developmental tools in the morphological toolkits
available to earlier, simpler animals reinforces the
view that the original role of these genes and regulatory
networks was in the formation of specialized cell types
in specific body regions, not necessarily in producing
complex multicellular structures (Erwin & Davidson
2002). Developmental control of pattern formation
was then later intercalated into these simpler networks.
5. GENOME EVOLUTION AT THE COMMUNITY
LEVEL . . . AND BEYOND
With the role of LGT in prokaryotic evolution nowmore
fully appreciated, a new field ofmicrobiology is emerging
in which the traditionally recognized mechanisms of
genetic transfer—conjugation, transformation and bac-
teriophage transduction—are viewed from a perspective
strongly grounded in population biology, ecology andissue. Erwin focuses on the origin of the bilaterian
genomic toolkit—the transcription factors, signalling-
pathway genes and other regulatory elements once
thought to be characteristic of bilaterally symmetric
animals, and associated with their diverse cell types
and complex morphologies. Many of these genes
have now been found in genomes of non-bilaterian
animals including choanoflagellates, placozoan, cni-