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Trends in Evolutionary Biology 2012; volume 4:e6

Evolution: a view from the 21st century not static and can undergo rapid and disruptive ence of selection, is challenged not only by the
James A. Shapiro changes, mediated by mobile genetic ele- fact that cells modify or reformat (sometimes
ments. The book is stimulating and provoca- heritably) their DNA in response to external
FT Press Science, 2011 tive reading, even if all of the views and per- cues but also by the fact that changes to DNA
ISBN: 0132780933 spectives it advances are not always shared. sequences are often abrupt and substantial,
Pages: 272 The book opens with a discussion of how rather than consisting of point mutations.
Price: $23.09 cells process information, with an emphasis on Understandably, much space in the book is
the similarities (and differences) between the given over to the discussion of processes
microprocessors of computer science and through which DNA sequences undergo large
In his book, Evolution: A View from the 21st mechanisms of information processing in liv- modifications. However, this makes for less
Century, James Shapiro attacks as inadequate ing cells and organisms. Shapiro challenges a compelling reading, feeling at times like a
the 20th century idea of evolution as essential- view of cell biology that would treat DNA as an litany. For the author, these are the tools at the
ly a selection biased random walk. Several information molecule, omnisciently directing disposal of a process of natural genetic engi-
technological analogies are proposed to cellular processes from the comfort of the neering, and they include genomic freeload-
describe the required conceptual shifts includ- nucleus. An obvious example of cells acting on ers, such as DNA transposons and various
ing that genomes should be thought of, not as their DNA comes from DNA repair: cells have classes of retroelements. Some of these are
inert data storage objects, but as dynamic read- mechanisms that sense and repair DNA dam- extremely abundant, and movements of these
write devices and that evolution should be age. Shapiro interprets this as a contradiction elements have been shown to have the poten-
understood as a process through which organ- of the central dogma of molecular biology. Here tial to bring about major phenotypic changes,
isms engage in natural genetic engineering. and elsewhere in the book, the zeal of the icon- for example bringing a gene under the control
The latter idea is the most pervasive through oclast to tear down intellectual edifices, per- of different cis-regulatory elements or mod-
the book and also likely to be the most contro- haps gets the better of balance and even accu- ules. Large genetic changes can also occur
versial as it suggests and even involves an ele- racy. For instance, mRNA splicing is posed as through duplication of tracts of the genome or
ment of design and any hint of design sets off an example of information flow from proteins even complete genomes, giving rise for a peri-
alarm bells for evolutionary biologists. Aware to RNA. While it is the case that proteins pres- od following duplication, to opportunities to
of this discomfort, Shapiro is careful to put dis- ent in the cell modify the sequence informa- innovate new protein functions and even to
tance between his scientific model and anti- tion encoded in RNA molecules, it seems bring about substantial rewiring of genetic
scientific creationism although, interestingly, unlikely that Francis Crick, had he been aware networks. Shapiro discusses the evidence for
given that he views cellular processes that of alternative splicing, would have considered whole genome duplications and some well-
involve sensing and responding to the environ- this an example of the transfer of sequence known examples - the role of genome duplica-
ment as a kind of cognition and organisms and information from proteins to RNA in the same tions in vertebrate evolution and the diversifi-
cells as, in some sense, intelligent agents way that sequence information is transferred cation of flowering plants.
actively engaged in shaping their own evolu- from RNA to DNA in the process of reverse That abrupt changes make a substantial
tionary trajectories, the term intelligent natu- transcription, the discovery of which did bring contribution to genomic and sometimes even
ral genetic engineering would seem to come about revision of the central dogma in 1970. phenotypic evolution (e.g. tetraploidy), in con-
close to what he has in mind. Despite any possible disagreements over trast to Darwins gradualist view, is no longer
The intended audience is broad. Shapiro the details, most contemporary biologists controversial. Less clear cut is the extent to
sets himself the challenge of being accessible would probably share, broadly, the view of which the cells natural genetic engineering
and interesting to the non-scientist, but at the organisms and cells as complex systems, con- toolkit can be activated in response to environ-
same time provocative and yet convincing to sisting of networks of interacting components mental signals, so that in some sense, evolu-
the more specialist reader with a background that enable them to process information from tion can be seen as a process that is actively
in molecular biology and evolution. To help their environments, their own states and other managed by the cell. At least in the case of
bridge the gap and to satisfy readers with an cells - in short, a systems biology view of life, microorganisms this was demonstrated
appetite for greater detail there is a swathe of with the genome as an interactive participant. through cell stress experiments. In many such
additional material available in the form of Cells act on their genomes, maintaining and experiments cited in the book, including work
online appendices and an extensive list of sug- restructuring chromatin. For Shapiro this is by the author, the activity of mobile elements,
gested further readings, primarily directed analogous to the formatting of computer files capable of bringing about major phenotypic
towards stimulating and providing further and it is one of the reasons that genomes changes, increases in the stress condition. The
background for the interested non-scientific should properly be seen as read-write devices, genome becomes more labile precisely at a
reader. The book operates at a conceptual level, rather than, more traditionally, as a form of time when it is important for a population of
arguing the need for and describing new intel- read-only memory. Recent research has shown microorganisms to explore possible alternative
lectual frameworks for evolutionary theory. the extent to which cells are engaged in solutions in a challenging environment. But,
Throughout, Shapiros breadth of knowledge of remodelling and marking chromatin and the more importantly, not only can the cells
contemporary biology and molecular evolution importance of this for controlling many arrange it so that their genomes mutate more
are impressive, made all the more compelling processes, including mRNA expression, espe- rapidly and more aggressively under stress
by his personal perspectives and reflections on cially the large-scale and stable changes in conditions, but they can bring about directed
several of the developments of modern biology expression required as cells differentiate. genomic changes. To demonstrate this idea
that are relevant to his thesis and appear to Indeed, in some cases epigenetic changes are Shapiro points to the fascinating CRISPR
have shaped his ideas. He draws inspiration, heritable, so that life histories can influence (Clustered Regularly Interspaced Short
among other sources, from the ground-break- genetic inheritance sometimes for several Palindromic Repeats) system in prokaryotes, a
ing work of his close friend and collaborator, generations, in a throwback to the Lamarkian defence against viruses that involves incorpo-
Barbara McClintock, herself no stranger to model of evolution. ration of fragments of viruses into the prokary-
controversy, and her scientific successors who The view of evolution as a gradual, random ote genome. Such directional changes to the
were the first to demonstrate that genomes are walk in DNA sequence space, under the influ- genetic material of the cell do push evolution-

[page 32] [Trends in Evolutionary Biology 2012; 4:e6]


Book Review

ary theory towards a requirement of major con- authors case that new theoretical frameworks their environment; and that genome changes
ceptual shift. Mutations are supposed to be sto- are required is compelling. The promiscuous can be a directional, targeted result of a
chastic and not directional, but if prokaryotes uptake of genetic material by prokaryotes can process of natural genetic engineering, rather
have the means to incorporate viruses into be evolutionarily advantageous and it is not too than stochastic mistakes. The last of these is
their genomes, thus enabling them to become surprising that mechanisms exist to ensure the strongest and is probably restricted to few,
resistant to the virus, we are forced to accept that this uptake occurs, such as the CRISPR very specific examples. The first is the weakest
that heritable genomic change within a single system mentioned above, and is directional - and would not be too much of a stretch for an
individual can sometimes be a directed this does not fit neatly with a notion of discrete early 20th century evolutionary biologist to
process which occurs as a response to the species, evolving gradually through random accommodate. The incidence of the second
environment. Instead of restricting to special- mutation and selection. Researchers involved observation is difficult to quantify and the
ist examples of focussed or directional muta- in phylogenomics of prokaryotes have long had
extent to which evolutionary theory requires a
tion, often involving defence against infection, to grapple with this poor fit. It is not surprising
radical overhaul may depend on this. It is
Shapiro makes the broader claim that, truly that the parameters of the evolutionary
clearly the case that evolution colours outside
random mutation would be the exception. But, process themselves are tuned by evolution. A
the lines of evolutionary theory, but in many
this is somewhat disingenuous, given that very species that managed to evolve a perfect mech-
little in biology is truly random, and the muta- anism to replicate DNA would ultimately die and perhaps most settings it seems unlikely
tional processes described may still be largely out as it failed to adapt to the inevitable that thinking of evolution as a process of
stochastic, even if sites at which these muta- changes in its environment; an excessive directed natural genetic engineering would be
tions occur are not randomly distributed mutation rate would result in too many unfit helpful. Whether existing models and theories
through the genome. The question of whether progeny. Shapiro points to a set of observations can accommodate modifications and excep-
regulated and directed/non-random mutation that require a changed mindset in evolutionary tions to the rules, or whether the exceptions
is the exception or rule is key to the central theory: that evolution is not predominantly are the rules in some or all branches of the
thesis of the book, that evolution requires a gradual, but includes a major contribution tree of life, remains to be seen.
new conceptual framework for the 21st century. from abrupt, disruptive events; that mutation
Overall, at least for microorganisms the is regulated by cells, frequently in response to Cathal Seoighe

[Trends in Evolutionary Biology 2012; 4:e6] [page 33]

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