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The Origins of Genome Architecture

Article in Journal of Heredity · July 2007

DOI: 10.1093/jhered/esm073 · Source: OAI

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Journal of Heredity 2007:98(6):633–634
Advance Access publication August 28, 2007
Book Review
The Origins of Genome Architecture
Michael Lynch
Sinauer Associates, Inc. Publishers. Sunderland, MA. 2007.
Hardcover, 494 pp. $59.95. ISBN 978-0-87893-484-3.
In the mid-nineteenth century, Charles Darwin was the first
to identify natural selection as the mechanism of adaptive
evolution. Although his observations described how the
population evolves, there was no accurate model describing
the mechanisms responsible for the origin of variation and
its inheritance. In late 1960s and early 1970s, Kimura (1986)
proposed the neutral theory of molecular evolution that
attributed an important role to the genetic drift of neutral
mutations. The debate between 2 theories is summarized by
words of Lewin (1996):
To selectionists (natural selection) most mutations are either
beneficial or harmful; beneficial ones are retained in the
population, creating extensive variation, while harmful ones
are removed. To neutralists (neutral theory), most mutations
are adaptively neutral, and therefore become fixed in the
population because their presence posses no harm;
extensive variation is the results.
The neutral theory does not deny the role of natural
selection as Motoo Kimura stated in 1986. Michael Lynch,
in his new book, cited that
Many aspects of the evolutionary change are indeed
facilitated by natural selection, but all populations are influ-
enced by the nonadaptive forces of mutation, recombina-
tion, and random genetic drift. These additional forces are
not simple embellishments around primary axis of selection,
but are quit the opposite—they dictate what natural
selection can and cannot do.
Michael Lynch describes evolution as a population-
genetic process governed by 4 forces, where the natural
selection is the adaptive force, mutation is the ultimate
source of variation on which natural selection acts, recom-
bination assorts variation within and among chromosomes,
and genetic drift ensures that gene frequencies will deviate
a bit from generation to generation independent of other
forces (Lynch 2007). In the same article, Lynch stated that
If complexity, modularity, evolveability, and/or robustness
are entirely products of adaptive processes, then where is
the evidence? What are the expected patterns of evolution
of such properties in the absence of selection, and what
types of observations would be acceptable as a falsification
of a null, nonadaptive hypothesis?
The recent advances in genomics such as whole genome
sequencing, high throughput proteomics, and bioinfor-
matics led to a dramatic development in the molecular
evolution field. With these advances, and in an attempt to
Ó The American Genetic Association. 2007. All rights reserved.
For permissions, please email: journals.permissions@oxfordjournals.org.
answer the previous questions, this book discusses the
origin of eukaryotic gene structure and how the nonadaptive
processes initiated genome-wide repattering of eukaryotic
genes structure; these primary processes provided novel
substrates for the natural selection as secondary processes to
raise new phenotypic complexities. This hypothesis was
a topic of several articles (Lynch and Conery 2003, 2004;
Lynch 2006, 2007; Lynch et al. 2006; Paland and Lynch
2006). Lynch’s hypothesis met some opposing comments
(Daubin and Moran 2004; Vinogradov 2004). Lynch and
Conery (2003) cited that with this hypothesis, arguments
based on molecular, cellular, and/or physiological con-
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straints are insufficient to explain the disparities in gene,
genome, and phenotypic complexity between prokaryotes
and eukaryotes.
In 13 chapters, the book is expounding the hypothesis in
details. Each chapter starts with an introduction that paves
the way for the discussion. Four introductory chapters lay
the groundwork for the book’s hypothesis. The main idea
for these chapters is the emergence of eukaryotic gene
structure, which the author presented in considerable detail
in an article in Molecular Biology and Evolution (2006). In
chapter 1 the author, with help of the phylogenetic models,
tried to answer many questions such as how a DNA-based
genome evolved from an RNA world, what is the similarity
between prokaryotes and eukaryotes, and are the 2
functional groups of cellular life arise from/and share the
same ancestor. At the end of this chapter (page 26),
a 4-steps scenario summarizes the evolution during the first
2 billion years of life. Chapter 2 is devoted to explore the
relation between genome size and organism complexity. In
chapter 4, the author discusses the effect of population size
on the mutation rate and how the evolution can occur
within species depending on their population size. Based on
this concept, Lynch concluded that prokaryotes followed by
unicellular eukaryotes need bigger population sizes than
multicellular eukaryotes to evolve. The factors that control
those transitions are decreasing population size, decreasing
recombination, and increasing deleterious mutations. The
relation among genome size, complexity, and population
size met some arguments that argue the supportive exam-
ples of Lynch’s model (Daubin and Moran 2004; Vinogra-
dov 2004). In chapters 3 and 7, the author reviews the
mobile genetic element classes, their role in the genome evo-
lution, and the organization of the human genome as
examples. The example is described in detail and describes
the mobile genetic elements; but, repeating information on
mobile genetic elements in 2 chapters will not help the
reader by swing back and forward. It might have been better
to merge the human genome organization (Chapter 3) in the
mobile genetic elements (Chapter 7). Chapter 5 discusses the
importance of the noncoding futures of chromosomes and
633
 Journal of Heredity 2007:98(6)

their roles to insure probable inheritance of complete
genome from generation to generation, as well the special
mechanisms that allow them to evolve. The author con-
tinues to show how the complexity of genomes accumulates
more genetic materials by gene duplication. In chapter 8, the
author describes the duplication levels, the mechanisms to
preserve the duplicated genes, and how the multicellular
organisms retain their duplicated genes. Based on the
differences in gene structure of the prokaryotes and
eukaryotes (Chapter 9) and the gene transcripts mechanisms
(Chapter 10), the author illuminates how the multicellular
organisms have several dozens of introns, more than the
unicellular organisms, then the mechanisms of intron origin,
the transcription and translation mechanisms, and the
splicing process. In chapters 11 and 12, Lynch discusses
the effect of nonadaptive forces on noncoding DNA
(organelle genomes) and low recombination regions (sex
chromosomes), respectively. Lynch proposed that organelle
new terms in an easy and rigorous form. A comprehensive
bibliography (more than 2000 references) is provided,
followed by author and detailed subject indexes.
In summary, this is a good book on molecular evolution
and a useful addition to the evolution library. The author
has simplified the subject, so that it will be easy for the
beginners in the field of molecular evolution as well as for
experts to understand. It should be in the library of all
institutions and colleges interested in molecular evolution
and population genetics.
References
Daubin V, Moran NA. 2004. Comment on ‘‘the origins of genome
complexity’’. Science. 306:978.
Kimura M. 1986. DNA and the neutral theory. Philos Trans R Soc Lond B

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Biol Sci.. 312:343–354.
evolution is also controlled by random genetic drift and
Lewin R. 1996. Patterns in evolution: the new molecular view. New York:
mutation pressure; however, the deeper understanding of
Scientific American Library.
nucleomorph evolution will require information on aspects
Lynch M. 2006. The origins of eukaryotic gene structure. Mol Biol Evol.
of the population genetic environment associated with
23:450–468.
genomic information such as effective population size and
Lynch M. 2007. The frailty of adaptive hypotheses for the origins of
mutation pressure. In chapter 12, Lynch stated that, even
organismal complexity. Proc Natl Acad Sci USA. 104:8597–8604.
though with premature data of the sex chromosomes, the X
Lynch M, Conery JS. 2003. The origins of genome complexity. Science.
chromosome generally does not provide a suitable environ-
302:1401–1404.
ment for nonadaptive forces to evolve individual genes, in
Lynch M, Conery JS. 2004. Response to comment on ‘‘the origins of
contrast to the Y chromosome. The last chapter discusses
genome complexity. Science. 306:978.
the history of population genetics and molecular evolution.
Lynch M, Koskella B, Schaack S. 2006. Mutation pressure and the evolution
This part could well have been merged with the first chapter
of organelle genome architecture. Science. 311:1727–1730.
to give the reader the essential background on the evolution
Paland S, Lynch M. 2006. Transitions to asexuality result in excess amino-
of that branch of science.
acid substitutions. Science. 311:990–992.
The book is intended for scientists, researchers, and
Vinogradov AE. 2004. Testing genome complexity. Science. 304:389–390.
professionals with an interest in molecular evolution. Even
though the book is presented and organized in a nontext-
book style, graduate students in this discipline, with an
adequate background in genetics and molecular biology, will HUSSEIN ABDEL-HALEEM
find many chapters of this book to be a worthwhile source Center of Applied Genetic Technologies,
for studying molecular evolution. The text is good, up-to- University of Georgia,
date, and readable. Tables and figures are clear and detailed; 111 Riverbend Road,
the important points that need more explanation are Athens, GA 30605
discussed in detail in brown-shaded boxes. At the end of e-mail: hussein@uga.edu
the book, there is a glossary of terms including basic and doi:10.1093/jhered/esm073

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