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The Logic of Chance: The Nature and Origin of

Biological Evolution

Eugene V. Koonin

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ISBN-10: 0-13-254249-8ISBN-13: 978-0-13-254249-4

Library of Congress Cataloging-in-Publication DataKoonin, Eugene V.The logic of chance : the nature and origin of biological evolution / Eugene V. Koonin.—1st ed.

p. cm.Includes bibliographical references.ISBN 978-0-13-254249-4 (hardback : alk. paper)1. Evolutionary genetics. 2. Genomes. 3. Evolution (Biology) I. Title. QH390.K66 2012576.8—dc23

2011013400

To my parents

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Contents

Preface Toward a postmodern synthesis of evolutionarybiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . .vii

Chapter 1: The fundamentals of evolution: Darwin and Modern Synthesis . . . . . . . . . . . . . . . . . . . . . .1

Chapter 2: From Modern Synthesis to evolutionary genomics: Multiple processes and patterns of evolution . . . . . . . . . . . . . . . . . . . . . . . . .21

Chapter 3: Comparative genomics: Evolving genomescapes . . . . . . . . . . . . . . . . . . . . . . .49

Chapter 4: Genomics, systems biology, and universals ofevolution: Genome evolution as a phenomenon of statistical physics . . . . . . . . .81

Chapter 5: The web genomics of the prokaryotic world: Vertical and horizontal flows of genes, themobilome, and the dynamic pangenomes . . .105

Chapter 6: The phylogenetic forest and the quest for the elusive Tree of Life in the age of genomics . . . . . . . . . . . . . . . . . . . . . . . . . .145

Chapter 7: The origins of eukaryotes: Endosymbiosis,the strange story of introns, and the ultimateimportance of unique events in evolution . . .171

Chapter 8: The non-adaptive null hypothesis of genome evolution and origins of biological complexity . . . . . . . . . . . . . . . . . . . . . . . . .225

Chapter 9: The Darwinian, Lamarckian, and Wrightean modalities of evolution, robustness,evolvability, and the creative role of noise in evolution . . . . . . . . . . . . . . . . . . . . . . . . . .257

Chapter 10: The Virus World and its evolution . . . . . . . . .293

Chapter 11: The Last Universal Common Ancestor,the origin of cells, and the primordial gene pool . . . . . . . . . . . . . . . . . . . . . . . . . .329

Chapter 12: Origin of life: The emergence of translation,replication, metabolism, and membranes—the biological, geochemical, and cosmological perspectives . . . . . . . . . . . . . . . . . . . . . . . .351

Chapter 13: The postmodern state of evolutionary biology . . . . . . . . . . . . . . . . . . . . . . . . . . . .397

Appendix A: Postmodernist philosophy, metanarratives,and the nature and goals of the scientificendeavor . . . . . . . . . . . . . . . . . . . . . . . . . .421

Appendix B: Evolution of the cosmos and life: Eternal inflation, “many worlds in one,” anthropic selection, and a rough estimate of the probability of the origin of life . . . . . . . . . . . .431

References . . . . . . . . . . . . . . . . . . . . . . . . .439

Endnotes . . . . . . . . . . . . . . . . . . . . . . . . . .479

Acknowledgments . . . . . . . . . . . . . . . . . . . .495

About the author . . . . . . . . . . . . . . . . . . . . .497

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . .499

vi the logic of chance

Preface:Toward a postmodern synthesis of

evolutionary biology

The title of this work alludes to four great books: Paul Auster’s novel TheMusic of Chance (Auster, 1991); Jacques Monod’s famous treatise onmolecular biology, evolution, and philosophy, Chance and Necessity (Lehazard et la necessite) (Monod, 1972); the complementary book by Fran-cois Jacob, The Logic of Life (Jacob, 1993); and, of course, Charles Darwin’s The Origin of Species (Darwin, 1859). Each of these books, inits own way, addresses the same overarching subject: the interplay of randomness (chance) and regularity (necessity) in life and its evolution.

Only after this book was completed, at the final stage of editing, didI become aware of the fact that the phrase Logic of Chance has alreadybeen used in a book title by John Venn, an eminent Cambridge logicianand philosopher who in 1866 published The Logic of Chance: An Essayon the Foundations and Province of the Theory of Probability. This workis considered to have laid the foundation of the frequency interpretationof probability, which remains the cornerstone of probability theory andstatistics to this day (Venn, 1866). He is obviously famous for the inven-tion of the ubiquitous Venn diagrams. I am somewhat embarrassed that Iwas unaware of John Venn’s work when starting this book. On the otherhand, I can hardly think of a more worthy predecessor.

My major incentive in writing this book is my belief that, 150 yearsafter Darwin and 40 years after Monod, we now have at hand the dataand the concepts to develop a deeper, more complex, and perhaps, moresatisfactory understanding of this crucial relationship between chanceand necessity. I make the case that variously constrained randomness is at the very heart of the entire history of life.

The inspiration for this book has been manifold. The most straight-forward incentive to write about the emerging new vision of evolution isthe genomic revolution that started in the last decade of the twentiethcentury and continues to unfold. The opportunity to compare the com-plete genome sequences of thousands of organisms from all walks of lifehas qualitatively changed the landscape of evolutionary biology. Our

inferences about extinct, ancestral life forms are not anymore the wildguesses they used to be (at least, for organisms with no fossil record). Onthe contrary, comparing genomes reveals numerous genes that are con-served in major groups of living beings (in some cases, even in all or mostof them) and thus gives us a previously unimaginable wealth of informa-tion and confidence about the ancestral forms. For example, it is notmuch of an exaggeration to claim that we have an excellent idea of thecore genetic makeup of the last common ancestor of all bacteria thatprobably lived more than 3.5 billion years ago. The more ancient ances-tors are much murkier, but even for those, some features seem to bedecipherable. The genomic revolution did more than simply allow credi-ble reconstruction of the gene sets of ancestral life forms. Much moredramatically, it effectively overturned the central metaphor of evolution-ary biology (and, arguably, of all biology), the Tree of Life (TOL), byshowing that evolutionary trajectories of individual genes are irreconcil-ably different. Whether the TOL can or should be salvaged—and, if so,in what form—remains a matter of intense debate that is one of theimportant themes of this book.

Uprooting the TOL is part of what I consider to be a “meta-revolu-tion,” a major change in the entire conceptual framework of biology. Atthe distinct risk of earning the ire of many for associating with a much-maligned cultural thread, I call this major change the transition to a post-modern view of life. Essentially, this signifies the plurality of pattern andprocess in evolution; the central role of contingency in the evolution oflife forms (“evolution as tinkering”); and, more specifically, the demise of(pan)adaptationism as the paradigm of evolutionary biology. Our unfal-tering admiration for Darwin notwithstanding, we must relegate the Vic-torian worldview (including its refurbished versions that flourished in thetwentieth century) to the venerable museum halls where it belongs, andexplore the consequences of the paradigm shift.

However, this overhaul of evolutionary biology has a crucial counter-point. Comparative genomics and evolutionary systems biology (such asorganism-wide comparative study of gene expression, protein abundance,and other molecular characteristics of the phenotype) have revealed sev-eral universal patterns that are conserved across the entire span of cellu-lar life forms, from bacteria to mammals. The existence of such universalpatterns suggests that relatively simple theoretical models akin to thoseemployed in statistical physics might be able to explain important aspects

viii the logic of chance

of biological evolution; some models of this kind with considerableexplanatory power already exist. The notorious “physics envy” that seemsto afflict many biologists (myself included) might be soothed by recentand forthcoming theoretical developments. The complementary rela-tionship between the universal trends and the contingency of the specificresults of evolution appears central to biological evolution—and the cur-rent revolution in evolutionary biology—and this is another centraltheme of this book.

Another entry point into the sketch of a new evolutionary synthesisthat I am trying to develop here is more specific and, in some ways, morepersonal. I earned my undergraduate and graduate degrees fromMoscow State University (in what was then the USSR), in the field ofmolecular virology. My PhD project involved an experimental study ofthe replication of poliovirus and related viruses that have a tiny RNAmolecule for their genome. I have never been particularly good with myhands, and the time and place were not the best for experimentationbecause even simple reagents and equipment were hard to obtain. Soright after I completed my PhD project, a colleague, Alex Gorbalenya,and I started to veer into an alternative direction of research that, at thetime, looked to many like no science at all. It was “sequence gazing”—that is, attempting to decipher the functions of proteins encoded in thegenomes of small viruses (the only complete genomes available at thetime) from the sequences of their building blocks, amino acids. Nowa-days, anyone can rapidly perform such an analysis by using sleek softwaretools that are freely available on the Internet; naturally, meaningful inter-pretation of the results still requires thought and skill (that much doesnot change). Back in 1985, however, there were practically no computersand no software. Nevertheless, with our computer science colleagues, wemanaged to develop some rather handy programs (encoded at the time onpunch cards). Much of the analysis was done by hand (and eye). Againstall odds, and despite some missed opportunities and a few unfortunateerrors, our efforts over the next five years were remarkably fruitful.Indeed, we managed to transform the functional maps of those smallgenomes from mostly unchartered territory to fairly rich “genomescapes”of functional domains. Most of these predictions have been subsequentlyvalidated by experiment, and some are still in the works (bench experi-mentation is much slower than computational analysis). I believe that oursuccess was mostly due to the early realization of the strikingly simple but

preface ix

surprisingly powerful basic principle of evolutionary biology: When a dis-tinct sequence motif is conserved over a long evolutionary span, it mustbe functionally important, and the higher the degree of conservation, themore important the function. This common-sense principle that is ofcourse rooted in the theory of molecular evolution has served our pur-poses exceedingly well and, I believe, converted me into an evolutionarybiologist for the rest of my days. What I mean is not so much theoreticalknowledge, but rather an indelible feeling of the absolute centrality andessentiality of evolution in biology. I am inclined to reword the famousdictum of the great evolutionary geneticist Theodosius Dobzhansky(“Nothing in biology makes sense except in the light of evolution”)(Dobzhansky, 1973) in an even more straightforward manner: Biology isevolution.

In those early days of evolutionary genomics, Alex and I often talkedabout the possibility that our beloved small RNA viruses could be directdescendants of some of the earliest life forms. After all, they were tinyand simple genetic systems, with only one type of nucleic acid involved,and their replication was directly linked to expression through the trans-lation of the genomic RNA. Of course, this was late-night talk with nodirect relevance to our daytime effort on mapping the functionaldomains of viral proteins. However, I believe that, 25 years and hundredsof diverse viral and host genomes later, the idea that viruses (or virus-likegenetic elements) might have been central to the earliest stages of life’sevolution has grown from a fanciful speculation to a concept that is com-patible with a wealth of empirical data. In my opinion, this is the mostpromising line of thought and analysis in the study of the earliest stagesof the evolution of life.

So these are the diverse conceptual threads that, to me, unexpect-edly converge on the growing realization that our understanding of evo-lution—and, with it, the very nature of biology—have forever departedfrom the prevailing views of the twentieth century that today look bothrather naïve and somewhat dogmatic. At some point, the temptation totry my hand in tying together these different threads into a semblance ofa coherent picture became irresistible, hence this book.

Some of the inspiration came from outside of biology, from therecent astounding and enormously fascinating developments in physicalcosmology. These developments not only put cosmology researchsquarely within the physical sciences, but completely overturn our ideas

x the logic of chance

about the way the world is, particularly, the nature of randomness andnecessity. When it comes to the boundaries of biology, as in the origin oflife problem, this new worldview cannot be ignored. Increasingly, physi-cists and cosmologists pose the question “Why is there something in theworld rather than nothing?” not as a philosophical problem, but as aphysical problem, and explore possible answers in the form of concretephysical models. It is hard not to ask the same about the biological world,yet at more than one level: Why is there life at all rather than just solutions of ions and small molecules? And, closer to home, even assum-ing that there is life, why are there palms and butterflies, and cats andbats, instead of just bacteria? I believe that these questions can be givena straightforward, scientific slant, and plausible, even if tentative,answers seem to be emerging.

Recent advances in high-energy physics and cosmology inspired thisbook in more than only the direct scientific sense. Many of the leadingtheoretical physicists and cosmologists have turned out to be gifted writ-ers of popular and semipopular books (one starts to wonder whetherthere is some intrinsic link between abstract thinking at the highest leveland literary talent) that convey the excitement of their revelations aboutthe universe with admirable clarity, elegance, and panache. The modernwave of such literature that coincides with the revolution in cosmologystarted with Stephen Hawking’s 1988 classic A Brief History of Time(Hawking, 1988). Since then, dozens of fine diverse books haveappeared. The one that did the most to transform my own view of theworld is the wonderful and short Many Worlds in One, by Alex Vilenkin(Vilenkin, 2007), but equally excellent treatises by Steven Weinberg(Weinberg, 1994), Alan Guth (Guth, 1998a), Leonard Susskind(Susskind, 2006b), Sean Carroll (Carroll, 2010), and Lee Smolin (in acontroversial book on “cosmic natural selection”; Smolin, 1999) were ofmajor importance as well. These books are far more than brilliant popu-larizations: Each one strives to present a coherent, general vision of boththe fundamental nature of the world and the state of the science thatexplores it. Each of these visions is unique, but in many aspects, they arecongruent and complementary. Each is deeply rooted in hard sciencebut also contains elements of extrapolation and speculation, sweepinggeneralizations, and, certainly, controversy. The more I read these booksand pondered the implications of the emerging new worldview, the morestrongly was I tempted to try something like that in my own field of

preface xi

evolutionary biology. At one point, while reading Vilenkin’s book, itdawned on me that there might be a direct and crucial connectionbetween the new perspective on probability and chance imposed bymodern cosmology and the origin of life—or, more precisely, the originof biological evolution. The overwhelming importance of chance in theemergence of life on Earth suggested by this line of enquiry is definitelyunorthodox and is certain to make many uncomfortable, but I stronglyfelt that it could not be disregarded if I wanted to be serious about theorigin of life.

This book certainly is a personal take on the current state of evolu-tionary biology as viewed from the vantage point of comparativegenomics and evolutionary systems biology. As such, it necessarily blendsestablished facts and strongly supported theoretical models with conjec-ture and speculation. Throughout the book, I try to distinguish betweenthe two as best I can. I intended to write the book in the style of theaforementioned excellent popular books in physics, but the story took alife of its own and refused to be written that way. The result is a far morescientific, specialized text than originally intended, although still a largelynontechnical one, with only a few methods described in an oversimpli-fied manner. An important disclaimer: Although the book addressesdiverse aspects of evolution, it remains a collection of chapters onselected subjects and is by no account a comprehensive treatise. Manyimportant and popular subjects, such as the origin of multicellular organ-isms or evolution of animal development, are completely and purpose-fully ignored. As best I could, I tried to stick with the leitmotif of thebook, the interplay between chance and nonrandom processes. Anotherthorny issue has to do with citations: An attempt to be, if not comprehen-sive, then at least reasonably complete, would require thousands of ref-erences. I gave up on any such attempt from the start, so the referencelist at the end is but a small subset of the relevant citations, and the selec-tion is partly subjective. My sincere apologies to all colleagues whoseimportant work is not cited.

All these caveats and disclaimers notwithstanding, it is my hope thatthe generalizations and ideas presented here will be of interest to manyfellow scientists and students—not only biologists, but also physicists,chemists, geologists, and others interested in the evolution and origin of life.

xii the logic of chance

The fundamentals of evolution: Darwinand Modern Synthesis

In this chapter and the next, I set out to provide a brief summary ofthe state of evolutionary biology before the advent of comparativegenomics in 1995. Clearly, the task of distilling a century and a half ofevolutionary thought and research into two brief, nearly nontechnicalchapters is daunting, to put it mildly. Nevertheless, I believe that wecan start by asking ourselves a straightforward question: What is thetake-home message from all those decades of scholarship? We cangarner a concise and sensible synopsis of the pregenomic evolution-ary synthesis even while inevitably omitting most of the specifics.

I have attempted to combine history and logic in these first twochapters, but some degree of arbitrariness is unavoidable. In thischapter, I trace the conceptual development of evolutionary biologyfrom Charles Darwin’s On the Origin of Species to the consolidationof Modern Synthesis in the 1950s. Chapter 2 deals with the conceptsand discoveries that affected the understanding of evolution betweenthe completion of Modern Synthesis and the genomic revolution ofthe 1990s.

Darwin and the first evolutionary synthesis: Itsgrandeur, constraints, and difficultiesIt is rather strange to contemplate the fact that we have just cele-brated the 150th anniversary of the first publication of Darwin’s Onthe Origin of Species (Darwin, 1859) and the 200th jubilee of Darwinhimself. Considering the profound and indelible effect that Origin

1

1

2 the logic of chance

had on all of science, philosophy, and human thinking in general (farbeyond the confines of biology), 150 years feels like a very short time.

What was so dramatic and important about the change in ourworldview that Darwin prompted? Darwin did not discover evolu-tion (as sometimes claimed overtly but much more often implied,especially in popular accounts and public debates). Many scholarsbefore him, including luminaries of their day, believed that organ-isms changed over time in a nonrandom manner. Even apart fromthe great (somewhat legendary) Greek philosophers Empedokles,Parmenides, and Heraclites, and their Indian contemporaries whodiscussed eerily prescient ideas (even if, oddly for us, combinedwith mythology) on the processes of change in nature, Darwin hadmany predecessors in the eighteenth and early nineteenth cen-turies. In later editions of Origin, Darwin acknowledged their con-tributions with characteristic candor and generosity. Darwin’s owngrandfather, Erasmus, and the famous French botanist and zoolo-gist Jean-Bapteste Lamarck (Lamarck, 1809) discussed evolution inlengthy tomes.1 Lamarck even had a coherent concept of the mech-anisms that, in his view, perpetuated these changes. Moreover, Dar-win’s famed hero, teacher, and friend, the great geologist SirCharles Lyell, wrote about the “struggle for existence” in which themore fecund will always win. And, of course, it is well known thatDarwin’s younger contemporary, Alfred Russel Wallace, simultane-ously proposed essentially the same concept of evolution and itsmechanisms.

However, the achievements of all these early evolutionistsnotwithstanding, it was Darwin who laid the foundation of modernbiology and forever changed the scientific outlook of the world inOrigin. What made Darwin’s work unique and decisive? Lookingback at his feat from our 150-year distance, three breakthrough gen-eralizations seem to stand out:

1. Darwin presented his vision of evolution within a completelynaturalist and rationalist framework, without invoking any tele-ological forces or drives for perfection (or an outright creator)that theorists of his day commonly considered.

2. Darwin proposed a specific, straightforward, and readilyunderstandable mechanism of evolution that is interplay

1 • the fundamentals of evolution 3

between heritable variation and natural selection, collectivelydescribed as the survival of the fittest.

3. Darwin boldly extended the notion of evolution to the entirehistory of life, which he believed could be adequately repre-sented as a grand tree (the famous single illustration of Origin),and even postulated that all existing life forms shared a singlecommon ancestor.

Darwin’s general, powerful concept stood in stark contrast to theevolutionary ideas of his predecessors, particularly Lamarck andLyell, who contemplated mostly, if not exclusively, evolutionarychange within species. Darwin’s fourth great achievement was notpurely scientific, but rather presentational. Largely because of a well-justified feeling of urgency caused by competition with Wallace, Dar-win presented his concept in a brief and readable (even for preparedlay readers), although meticulous and carefully argued, volume.Thanks to these breakthroughs, Darwin succeeded in changing theface of science rather than just publishing another book. Immediatelyafter Origin was published, most biologists and even the general edu-cated public recognized it as a credible naturalist account of how theobserved diversity of life could have come about, and this was adynamic foundation to build upon.2

Considering Darwin’s work in a higher plane of abstraction that iscentral to this book, it is worth emphasizing that Darwin seems tohave been the first to establish the crucial interaction betweenchance and order (necessity) in evolution. Under Darwin’s concept,variation is (nearly) completely random, whereas selection introducesorder and creates complexity. In this respect, Darwin is diametricallyopposed to Lamarck, whose worldview essentially banished chance.We return to this key conflict of worldviews throughout the book.

Indeed, with all due credit given to his geologist and early evolu-tionary biologist predecessors, Darwin was arguably the first scholarto prominently bring the possibility of evolutionary change (and, byimplication, origin) of the entire universe into the realm of naturalphenomena that are subject to rational study. Put another way, Dar-win initiated the scientific study of the time arrow—that is, time-asymmetrical, irreversible processes. By doing so, he prepared theground not only for all further development of biology, but also for


the advent of modern physics. I believe that the great physicist Lud-wig Boltzmann, the founder of statistical thermodynamics and theauthor of the modern concept of entropy, had good reason to callDarwin a “great physicist,” paradoxical as this might seem, given thatDarwin knew precious little about actual physics and mathematics.Contemporary philosopher Daniel Dennett may have had a pointwhen he suggested that Darwin’s idea of natural selection might bethe single greatest idea ever proposed (Dennett, 1996).

Certainly, Darwin’s concept of evolution at the time Origin waspublished and at least through the rest of the nineteenth century facedsevere problems that greatly bothered Darwin and, at times, appearedinsurmountable to many scientists. The first substantial difficulty wasthe low estimate of the age of Earth that prevailed in Darwin’s day.Apart from any creation myth, the best estimates by nineteenth-cen-tury physicists (in particular, Lord Kelvin) were close to 100 millionyears, a time span that was deemed insufficient for the evolution of lifevia the Darwinian route of gradual accumulation of small changes.Clearly, that was a correct judgment—the 100 million years time rangeis far too short for the modern diversity of life to evolve, although noone in the nineteenth century had a quantitative estimate of the rate ofDarwinian evolution. The problem was resolved 20 years after Darwin’sdeath. In the beginning of the twentieth century, when radioactivitywas discovered, scientists calculated that cooling of the Earth from itsinitial hot state would take billions of years, just about the time Darwinthought would be required for the evolution of life by natural selection.

The second, more formidable problem has to do with the mecha-nisms of heredity and the so-called Jenkin nightmare. Because theconcept of discrete hereditary determinants did not exist in Darwin’stime (outside the obscure articles of Mendel), it was unclear how anemerging beneficial variation could survive through generations andget fixed in evolving populations without being diluted and perishing.Darwin apparently did not think of this problem at the time he wroteOrigin; an unusually incisive reader, an engineer named Jenkin,informed Darwin of this challenge to his theory. In retrospect, it isdifficult to understand how Darwin (or Jenkin or Huxley) did notthink of a Mendelian solution. Instead, Darwin came up with a moreextravagant concept of heredity, the so-called pangenesis, which evenhe himself did not seem to take quite seriously. This problem was


resolved by the (re)birth of genetics, although the initial implicationsfor Darwinism3 were unexpected (see the next section).

The third problem that Darwin fully realized and brilliantlyexamined was the evolution of complex structures (organs, in Dar-win’s terms) that require assembly of multiple parts to perform theirfunction. Such complex organs posed the classic puzzle of evolution-ary biology that, in the twentieth century, has been evocativelybranded ‘irreducible complexity.’4 Indeed, it is not immediately clearhow selection could enact the evolution of such organs under theassumption that individual parts or partial assemblies are useless.Darwin tackled this problem head-on in one of the most famous pas-sages of Origin, the scenario of evolution of the eye. His proposedsolution was logically impeccable, plausible, and ingenious: Darwinposited that complex organs do evolve through a series of intermedi-ate stages, each of which performs a partial function related to theultimate function of the evolving complex organ. Thus, the evolutionof the eye, according to Darwin, starts with a simple light-sensingpatch and proceeds through primitive eye-like structures of incremen-tally increasing utility to full-fledged, complex eyes of arthropods andvertebrates. It is worth noting that primitive light-sensing structuresresembling those Darwin postulated on general grounds have beensubsequently discovered, at least partially validating his scenario andshowing that, in this case, the irreducibility of a complex organ is illu-sory. However, all the brilliance of Darwin’s scheme notwithstanding,it should be taken for what it is: a partially supported speculative sce-nario for the evolution of one particular complex organ. Darwin’saccount shows one possible trajectory for the evolution of complexitybut does not solve this major problem in general. Evolution of com-plexity at different levels is central to understanding biology, so werevisit it on multiple occasions throughout this book.

The fourth area of difficulty for Darwinism is, perhaps, the deep-est. This major problem has to do with the title and purported mainsubject of Darwin’s book, the origin of species and, more generally,large-scale evolutionary events that are now collectively denoted asmacroevolution. In a rather striking departure from the title of thebook, all indisputable examples of evolution that Darwin presentedinvolve the emergence of new varieties within a species, not newspecies let alone higher taxa. This difficulty persisted long after


Darwin’s death and exists even now, although it was mitigated first bythe progress of paleontology, then by developments in the theory ofspeciation supported by biogeographic data, and then, most convinc-ingly, by comparative genomics (see Chapters 2 and 3). Much to hiscredit, and unlike detractors of evolution up to this day, Darwinfirmly stood his ground in the face of all difficulties, thanks to hisunflinching belief that, incomplete as his theory might be, there wasno rational alternative. The only sign of Darwin’s vulnerability was theinclusion of the implausible pangenesis model in later editions ofOrigin, as a stop-gap measure to stave off the Jenkin nightmare.

Genetics and the “black day” of DarwinismAn urban legend tells that Darwin had read Mendel’s paper butfound it uninspiring (perhaps partly because of his limited commandof German). It is difficult to tell how different the history of biologywould have been if Darwin had absorbed Mendel’s message, whichseems so elementary to us. Yet this was not to be.

Perhaps more surprisingly, Mendel himself, although obviouslywell familiar with the Origin, did not at all put his discovery into aDarwinian context. That vital connection had to await not only therediscovery of genetics at the brink of the twentieth century, but alsothe advent of population genetics in the 1920s. The rediscovery ofMendelian inheritance and the birth of genetics should have been ahuge boost to Darwinism because, by revealing the discreteness ofthe determinants of inheritance, these discoveries eliminated theJenkin nightmare. It is therefore outright paradoxical that the originalreaction of most biologists to the discovery of genes was that geneticsmade Darwin’s concept irrelevant, even though no serious scientistwould deny the reality of evolution. The main reason genetics wasdeemed incompatible with Darwinism was that the founders ofgenetics, particularly Hugo de Vries, the most productive scientistamong the three rediscoverers of Mendel laws, viewed mutations ofgenes as abrupt, saltational hereditary changes that ran counter toDarwinian gradualism. These mutations were considered to be aninalienable feature of Darwinism, in full accord with Origin. Accord-ingly, de Vries viewed his mutational theory of evolution as “anti-Darwinian.” So Darwin’s centennial jubilee and the 50th anniversary


of the Origin in 1909 were far from triumphant, even as geneticresearch surged and Wilhelm Johansson introduced the term genethat very year.

Population genetics, Fisher’s theorem, fitnesslandscapes, drift, and draftThe foundations for the critically important synthesis of Darwinismand genetics were set in the late 1920s and early 1930s by the trio ofoutstanding theoretical geneticists: Ronald Fisher, Sewall Wright,and J. B. S. Haldane. They applied rigorous mathematics and statis-tics to develop an idealized description of the evolution of biologicalpopulations. The great statistician Fisher apparently was the first tosee that, far from damning Darwinism, genetics provided a natural,solid foundation for Darwinian evolution. Fisher summarized hisconclusions in the seminal 1930 book The Genetical Theory of Nat-ural Selection (Fisher, 1930), a tome second perhaps only to Darwin’sOrigin in its importance for evolutionary biology.5 This was the begin-ning of a spectacular revival of Darwinism that later became known asModern Synthesis (a term mostly used in the United States) or neo-Darwinism (in the British and European traditions).

It is neither necessary nor practically feasible to present here thebasics of population genetics.6 However, several generalizations thatare germane to the rest of the discussion of today’s evolutionary biol-ogy can be presented succinctly. Such a summary, even if superficial,is essential here. Basically, the founders of population genetics real-ized the plain fact that evolution does not affect isolated organisms orabstract species, but rather affects concrete groups of interbreedingindividuals, termed populations. The size and structure of the evolv-ing population largely determines the trajectory and outcome of evo-lution. In particular, Fisher formulated and proved the fundamentaltheorem of natural selection (commonly known as Fisher’s theorem),which states that the intensity of selection (and, hence, the rate ofevolution due to selection) is proportional to the magnitude of thestanding genetic variation in an evolving population, which, in turn, isproportional to the effective population size.

Box 1-1 gives the basic definitions and equations that determinethe effects of mutation and selection on the elimination or fixation of


mutant alleles, depending on the effective population size. The qual-itative bottom line is that, given the same mutation rate, in a popula-tion with a large effective size, selection is intense. In this case, evenmutations with a small positive selection coefficient (“slightly” benefi-cial mutations) quickly come to fixation. On the other hand, muta-tions with even a small negative selection coefficient (slightlydeleterious mutations) are rapidly eliminated. This effect found itsrigorous realization in Fisher’s theorem.

Box 1-1: The fundamental relationships defining the rolesof selection and drift in the evolution of populations

Nearly neutral evolution dominated by drift

1/Ne >>|s|

Evolution dominated by selection

1/Ne <<|s|

Mixed regime, with both drift and selection important

1/Ne ≈|s|

Ne: effective population size (typically, substantially less than thenumber of individuals in a population because not all individualsproduce viable offspring)

s: selection coefficient or fitness effect of mutation:

s = FA – Fa

FA, Fa: fitness values of two alleles of a gene

s>0: beneficial mutation

s<0: deleterious mutation

A corollary of Fisher’s theorem is that, assuming that naturalselection drives all evolution, the mean fitness of a population cannotdecrease during evolution (if the population is to survive, that is). Thisis probably best envisaged using the imagery of a fitness landscape,which was first introduced by another founding father of populationgenetics, Sewall Wright. When asked by his mentor to present theresults of his mathematical analysis of selection in a form accessible to


A

fitne

ss

fitne

ss

B

Figure 1-1 Fitness landscapes: the Mount Fujiyama landscape with a single(global) fitness peak and a rugged fitness landscape.

biologists, Wright came up with this extremely lucky image. Theappeal and simplicity of the landscape representation of fitness evolu-tion survive to this day and have stimulated numerous subsequentstudies that have yielded much more sophisticated and less intuitivetheories and versions of fitness landscapes, including multidimen-sional ones (Gavrilets, 2004).7 According to Fisher’s theorem, a popu-lation that evolves by selection only (technically, a population of aninfinite size—infinite populations certainly do not actually exist, butthis is convenient abstraction routinely used in population genetics)can never move downhill on the fitness landscape (see Figure 1-1). Itis easy to realize that a fitness landscape, like a real one, can havemany different shapes. Under certain special circumstances, thelandscape might be extremely smooth, with a single peak correspon-ding to the global fitness maximum (sometimes this is poeticallycalled the Mount Fujiyama landscape; see Figure 1-1A). More realis-tically, however, the landscape is rugged, with multiple peaks of dif-ferent heights separated by valleys (see Figure 1-1B). As formallycaptured in Fisher’s theorem (and much in line with Darwin), a pop-ulation evolving by selection can move only uphill and so can reachonly the local peak, even if its height is much less than the height ofthe global peak (see Figure 1-1B). According to Darwin and ModernSynthesis, movement across valleys is forbidden because it wouldinvolve a downhill component. However, the development of popula-tion genetics and its implications for the evolutionary processchanged this placid picture because of genetic drift, a key concept inevolutionary biology that Wright also introduced.


As emphasized earlier, Darwin recognized a crucial role ofchance in evolution, but that role was limited to one part of the evolu-tionary process only: the emergence of changes (mutations, in themodern parlance). The rest of evolution was envisaged as a determin-istic domain of necessity, with selection fixing advantageous muta-tions and the rest of mutations being eliminated without anylong-term consequence. However, when population dynamicsentered the picture, the situation changed dramatically. The foundersof quantitative population genetics encapsulated in simple formulasthe dependence of the intensity of selection on population size andmutation rate (see Box 1-1 and Figure 1-2). In a large population witha high mutation rate, selection is effective, and even a slightly advan-tageous mutation is fixed with near certainty (in an infinite popula-tion, a mutation with an infinitesimally small positive selectioncoefficient is fixed deterministically). Wright realized that a smallpopulation, especially one with a low mutation rate, is quite different.Here random genetic drift plays a crucial role in evolution throughwhich neutral or even deleterious (but, of course, nonlethal) muta-tions are often fixed by sheer chance. Clearly, through drift, an evolv-ing population can violate the principle of upward-only movement inthe fitness landscape and might slip down (see Figure 1-2).8 Most ofthe time, this results in a downward movement and subsequentextinction, but if the valley separating the local peak from another,perhaps taller one is narrow, then crossing the valley and starting aclimb to a new, perhaps taller summit becomes possible (see Figure1-2). The introduction of the notion of drift into the evolutionary nar-rative is central to my story. Here chance enters the picture at a newlevel: Although Darwin and his immediate successors saw the role ofchance in the emergence of heritable change (mutations), drift intro-duces chance into the next phase—namely, the fixation of thesechanges—and takes away some of the responsibility from selection. Iexplore just how important the role of drift is in different situationsduring evolution throughout this book.

John Maynard Smith and, later, John Gillespie developed the the-ory and computer models to demonstrate the existence of a distinct


fitne

ss

Figure 1-2 Trajectories on a rugged fitness landscape. The dotted line is anevolutionary trajectory at a high effective population size. The solid line is anevolutionary trajectory at a low effective population size.

mode of neutral evolution that is only weakly dependent on the effec-tive population size and that is relevant even in infinite populationswith strong selection. This form of neutral fixation of mutationsbecame known as genetic draft and refers to situations in which one ormore neutral or even moderately deleterious mutations spread in apopulation and are eventually fixed because of the linkage with a bene-ficial mutation: The neutral or deleterious alleles spread by hitchhikingwith the linked advantageous allele (Barton, 2000). Some population-genetic data and models seem to suggest that genetic draft is evenmore important for the evolution in sexual populations than drift.Clearly, genetic draft is caused by combined effects of natural selec-tion and neutral variation at different genomic sites and, unlike drift,can occur even in effectively infinite populations (Gillespie, 2000).


Genetic draft may allow even large populations to fix slightly deleteri-ous mutations and, hence, provides them with the potential to crossvalleys on the fitness landscape.

Positive and purifying (negative) selection: Classifyingthe forms of selectionDarwin thought of natural selection primarily in terms of fixation ofbeneficial changes. He realized that evolution weeded out deleteri-ous changes, but he did not interpret this elimination on the sameplane with natural selection. In the course of the evolution of ModernSynthesis, the notion of selection was expanded to include “purifying”(negative) selection; in some phases of evolution, this turns out to bemore common (orders of magnitude more common, actually) than“Darwinian,” positive selection. Essentially, purifying selection is thedefault process of elimination of the unfit. Nevertheless, defining thisprocess as a special form of selection seems justified and importantbecause it emphasizes the crucial role of elimination in shaping (con-straining) biological diversity at all levels. Simply put, variation is per-mitted only if it does not confer a significant disadvantage on anysurviving variant. To what extent these constraints actually limit thespace available for evolution is an interesting and still open issue, andI touch on this later (see in particular Chapters 3, 8, and 9).

A subtle but substantial difference exists between purifying selec-tion and stabilizing selection, which is a form of selection defined byits effect on frequency distributions of trait values. These formsinclude stabilizing selection that is based primarily on purifying selec-tion, directional selection driven by positive (Darwinian) selection,and the somewhat more exotic regimes of disruptive and balancingselection that result from combinations of multiple constraints (seeFigure 1-3).

1 • the fundamentals of evolution 13fi

tnes

s

a

bd

c

Figure 1-3 Four distinct forms of selection in an evolving population: (A) Stabi-lizing selection (fitness landscape represented by solid line); (B) Directionalselection (fitness landscape represented by solid line); (C) Disruptive selection(fitness landscape represented by solid line); (D) Balancing selection (fitnesslandscape changes periodically by switching between two dotted lines).

Modern SynthesisThe unification of Darwinian evolution and genetics achieved prima-rily in the seminal studies of Fisher, Wright, and Haldane preparedthe grounds for the Modern Synthesis of evolutionary biology. Thephrase itself comes from the eponymous 1942 book by Julian Huxley(Huxley, 2010), but the conceptual framework of Modern Synthesis isconsidered to have solidified only in 1959, during the centennial cel-ebration of Origin. The new synthesis itself was the work of manyoutstanding scientists. The chief architects of Modern Synthesis werearguably experimental geneticist Theodosius Dobzhansky, zoologistErnst Mayr, and paleontologist George Gaylord Simpson. Dobzhan-sky’s experimental and field work with the fruit fly Drosophilamelanogaster provided the vital material support to the theory of pop-ulation genetics and was the first large-scale experimental validationof the concept of natural selection. Dobzhansky’s book Genetics andthe Origin of Species (Dobzhansky, 1951) is the principal manifesto ofModern Synthesis, in which he narrowly defined evolution as “changein the frequency of an allele within a gene pool.” Dobzhansky also


famously declared that nothing in biology makes sense except in thelight of evolution9 (see more about “making sense” in Appendix A).Ernst Mayr, more than any other scientist, is to be credited with anearnest and extremely influential attempt at a theoretical frameworkfor Darwin’s quest, the origin of species. Mayr formulated the so-called biological concept of species, according to which speciationoccurs when two (sexual) populations are isolated from each other fora sufficiently long time to ensure irreversible genetic incompatibility(Mayr, 1963). Simpson reconstructed the most comprehensive (in histime) picture of the evolution of life based on the fossil record (Simp-son, 1983). Strikingly, Simpson recognized the prevalence of stasis inthe evolution of most species and the abrupt replacement of domi-nant species. He also introduced the concept of quantum evolution,which presaged the punctuated equilibrium concept of Stephen JayGould and Niles Eldredge (see Chapter 2).

The consolidation of Modern Synthesis in the 1950s was a some-what strange process that included remarkable “hardening” (Gould’sword) of the principal ideas of Darwin (Gould, 2002). Thus, the doc-trine of Modern Synthesis effectively left out Wright’s concept of ran-dom genetic drift and its evolutionary importance, and remainsuncompromisingly pan-adaptationist. Rather similarly, Simpson him-self gave up the idea of quantum evolution, so gradualism remainedone of the undisputed pillars of Modern Synthesis. This “hardening”shaped Modern Synthesis as a relatively narrow, in some ways dog-matic conceptual framework.

To proceed with the further discussion of the evolution of evolu-tionary biology and its transformation in the age of genomics, it seemsnecessary to succinctly recapitulate the fundamental principles ofevolution that Darwin first formulated, the first generation of evolu-tionary biologists then amended, and Modern Synthesis finally codi-fied. We return to each of these crucial points throughout the book.

1. Undirected, random variation is the main process that providesthe material for evolution. Darwin was the first to allow chanceas a major factor into the history of life, and this was arguably oneof his greatest insights. Darwin also allowed a subsidiary role fordirected, Lamarckian-type variation, and he tended to give thesemechanisms more weight in later editions of Origin. Modern


Synthesis, however, is adamant in its insistence on random muta-tions being the only source of evolutionarily relevant variability.

2. Evolution proceeds by fixation of rare beneficial variations andelimination of deleterious variations: This is the process of nat-ural selection that, along with random variation, is the principaldriving force of evolution, according to Darwin and ModernSynthesis. Natural selection, which is obviously akin to andinspired by the “invisible hand” of the market that ruled econ-omy according to Adam Smith, was the first mechanism of evo-lution ever proposed that was simple and plausible and that didnot require any mysterious innate trends. As such, this wasDarwin’s second key insight. Sewall Wright emphasized thatchance could play a substantial role in the fixation of changesduring evolution rather than only in their emergence, viagenetic drift that entails random fixation of neutral or evenmoderately deleterious changes. Population-genetic theoryindicates that drift is particularly important in small popula-tions that go through bottlenecks. Genetic draft (hitchhiking) isanother form of stochastic fixation of nonbeneficial mutations.However, Modern Synthesis in its “hardened” form effectivelyrejected the role of stochastic processes in evolution beyond theorigin of variation and adhered to a purely adaptationist (pan-adaptationist) view of evolution. This model inevitably leads tothe concept of “progress,” gradual improvement of “organs”during evolution. Darwin endorsed this idea as a general trend,despite his clear understanding that organisms are less thanperfectly adapted, as strikingly exemplified by rudimentaryorgans, and despite his abhorrence of any semblance of aninnate strive for perfection of the Lamarckian ilk. Modern Syn-thesis shuns progress as an anthropomorphic concept but nev-ertheless maintains that evolution, in general, proceeds fromsimple to complex forms.

3. The beneficial changes that are fixed by natural selection areinfinitesimally small (in modern parlance, the evolutionarilyrelevant mutations are supposed to have infinitesimally smallfitness effects), so evolution occurs via the gradual accumula-tion of these tiny modifications. Darwin insisted on strict grad-ualism as an essential staple of his theory: “Natural selection


can act only by the preservation and accumulation of infinitesi-mally small inherited modifications, each profitable to the pre-served being. ...If it could be demonstrated that any complexorgan existed, which could not possibly have been formed bynumerous, successive, slight modifications, my theory wouldabsolutely break down.” (Origin of Species, Chapter 6). Evensome contemporaries of Darwin believed that was an unneces-sary stricture on the theory. In particular, the early objectionsof Thomas Huxley are well known: Even before the publicationof Origin, Huxley wrote to Darwin, “You have loaded yourselfwith an unnecessary difficulty in adopting Natura non facitsaltum so unreservedly” (http://aleph0.clarku.edu/huxley/).Disregarding these early warnings and even Simpson’s conceptof quantum evolution, Modern Synthesis uncompromisinglyembraced gradualism.

4. An aspect of the classic evolutionary biology that is related tobut also distinct from the principled gradualism is uniformitarianism (absorbed by Darwin from Lyell’s geology).This is the belief that the evolutionary processes have remainedessentially the same throughout the history of life.

5. This key principle is logically linked to gradualism and unifor-mitarianism: Macroevolution (the origin of species and highertaxa), is governed by the same mechanisms as microevolution(evolution within species). Dobzhansky, with his definition ofevolution as the change of allele frequencies in populations,was the chief proponent of this principle. Darwin did not usethe terms microevolution and macroevolution; nevertheless,the sufficiency of intraspecies processes to explain the origin ofspecies and, more broadly, the entire evolution of life can beconsidered the central Darwinian axiom (or perhaps a funda-mental theorem, but one for which Darwin did not have evenan inkling of the proof). It seems reasonable to speak of thisprinciple as “generalized uniformitarianism”: The processes ofevolution are the same not only throughout the history of life,but also at different levels of evolutionary transformation,including major transitions. The conundrum of microevolutionversus macroevolution is, in some ways, the fulcrum of evolu-tionary biology, so we revisit it repeatedly throughout this book.

http://aleph0.clarku.edu/huxley/


6. Evolution of life can be accurately represented by a “greattree,” as emphasized by the only illustration in Origin (inChapter 4). Darwin introduced the Tree of Life (TOL) only asa general concept and did not attempt to investigate its actualbranching order. The tree was populated with actual life forms,to the best of the knowledge at the time, by the chief Germanfollower of Darwin, Ernst Haeckel. The founders of ModernSynthesis were not particularly interested in the TOL, but theycertainly embraced it as a depiction of the evolution of animalsand plants that the fossil record amply supported in the twenti-eth century. By contrast, microbes that were increasingly rec-ognized as major ecological agents remained effectively outsidethe scope of evolutionary biology.

7. A corollary of the single TOL concept deserves the status of aseparate principle: All extant diversity of life forms evolvedfrom a single common ancestor (or very few ancestral forms,under Darwin’s cautious formula in Chapter 14 of Origin; seeDarwin, 1859). Many years later, this has been dubbed the LastUniversal Common (Cellular) Ancestor (LUCA). For thearchitects of Modern Synthesis, the existence of LUCA washardly in doubt, but they did not seem to consider elucidationof its nature a realistic or important scientific goal.

SynopsisIn his book On the Origin of Species, Charles Darwin meticulouslycollected evidence of temporal change that permeates the world ofliving beings and proposed for the first time a plausible mechanism ofevolution: natural selection. Evolution by natural selection certainly isone of the most consequential concepts ever developed by a scientistand even has been deemed the single most important idea in humanhistory (Dennett, 1996). Somewhat paradoxically, it is also oftenbranded a mere tautology, and when one thinks in terms of the sur-vival of the fittest, there seems to be some basis for this view. How-ever, considering the Darwinian scenario as a whole, it is easy to graspits decidedly nontautological and nontrivial aspect. Indeed, whatDarwin proposed is a mechanism for the transformation of random


variation into adaptations that are not random at all, including elabo-rate, complex devices that perform highly specific functions and soincrease the fitness of their carriers. Coached in physical terms andloosely following Erwin Schroedinger’s famous treatise, Darwinianevolution is a machine for the creation of negentropy—in otherwords, order from disorder. I submit that this was the single keyinsight of Darwin, the realization that a simple mechanism, devoid ofany teleological component, could plausibly account for the emer-gence, from random variation alone, of the amazing variety of lifeforms that appear to be so exquisitely adapted to their specific envi-ronments. Viewed from that perspective, the “invisible hand” of natu-ral selection appears almost miraculously powerful, and one cannothelp wondering whether it is actually sufficient to account for the his-tory of life. This question has been repeatedly used as a rhetoricdevice by all kinds of creationists, but it also has been asked in earnestby evolutionary biologists. We shall see in the rest of this book thatthe answers widely differ, both between scientists and between dif-ferent situations and stages in the evolution of life.

Of course, Darwinism in its original formulation faced problemsmore formidable and more immediate than the question of the suffi-ciency of natural selection: Darwin and his early followers had no sen-sible idea of the mechanisms of heredity and whether thesemechanisms, once discovered, would be compatible with the Darwin-ian scenario. In that sense, the entire building of Darwin’s conceptwas suspended in thin air. The rediscovery of genetics at the begin-ning of the twentieth century, followed by the development of theo-retical and experimental population genetics, provided a solidfoundation for Darwinian evolution. It was shown beyond reasonabledoubt that populations evolved through a process in which Darwiniannatural selection was a major component. The Modern Synthesis ofevolutionary biology completed the work of Darwin by almost seam-lessly unifying Darwinism with genetics. As it matured, Modern Syn-thesis notably “hardened” through indoctrinating gradualism,uniformitarianism, and, most important, the monopoly of naturalselection as the only route of evolution. In Modern Synthesis, allchanges that are fixed during evolution are considered adaptive, atleast initially. For all its fundamental merits, Modern Synthesis is arather dogmatic and woefully incomplete theory. To name three of


the most glaring problems, Modern Synthesis makes a huge leap offaith by extending the mechanisms and patterns established formicroevolution to macroevolutionary processes; it has nothing to sayabout evolution of microbes, which are the most abundant anddiverse life forms on Earth; and it does not even attempt to addressthe origin of life.

Recommended further readingFutuyma, Douglas. (2009) Evolution, 2d edition. Sunderland, MA:

Sinauer Associates.

Probably the best available undergraduate text on evolutionary biology.

Gould, Stephen Jay. (2002) The Structure of Evolutionary Theory.Cambridge, MA: Harvard University Press.

The almost 1,500-page tome obviously is not for the feeble atheart, and not many will read it in its entirety. Nevertheless, atleast the first part is valuable for its clear and witty presentation ofthe history of evolutionary biology and its pointed critique ofModern Synthesis.

Hartl, Daniel L., and Andrew G. Clark. (2006) Principles of Popula-tion Genetics, 4th edition. Sunderland, MA: Sinauer Associates.

An excellent, fairly advanced, but accessible textbook on popula-tion genetics.

Mayr, Ernst. (2002) What Evolution Is. New York: Basic Books.

A basic but clear and useful presentation of classical evolutionarybiology by one of the architects of Modern Synthesis.

Schroedinger, Erwin. (1992) What Is Life?: With “Mind and Matter”and “Autobiographical Sketches.” Cambridge, MA: CambridgeUniversity Press.

The first edition of this wonderful book was published in 1944, onthe basis of a series of lectures that Schroedinger (one of thefounders of quantum mechanics) delivered in Edinburgh, wherehe stayed during World War II. Obviously outdated, but remark-ably lucid, prescient, and still relevant in the discussion of the roleof entropy and information in biology.

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Index

499

Note: Page numbers followed by n arelocated in the endnotes.

aaaRS (aminoacyl-tRNA synthetases), 126,

355-356abbreviations, species abbreviations,

485-486nabiogenic compartmentalization, 378ACE (Anthropic Chemical Evolution),

386-391acquired characters, inheritance of.

See Lamarckian inheritanceactin, 172, 203Actinobacteria, 161Adami, Chris, 227adaptive evolvability, 284-287adaptors, 23-35Agol, Vadim, 296alpha-proteobacteria, 45, 177alternative splicing, 238-239alternative transcription, 99Altman, Sydney, 361altruism, reciprocal, 341Altstein, Anatoly, 374aminoacyl adenylate synthesis, 363aminoacyl-tRNA synthetases (aaRS),

126, 355-356Amoebozoa, 182Anfinsen cage, 279Anfinsen, Christian, 279Anthropic Chemical Evolution (ACE),

386-391anthropic principle, 384, 433-434,

437, 492nanthropic selection, 384, 433-434, 437

antibioticsantibiotic resistance, 267discovery of, 106

anticodons, 366, 369, 375antientropic devices, 414antivirus defense, 322-325antivirus immunity, CRISPR-Cas

system of, 263-265APE (Archaeal Progenitor of

Eukaryotes), 205Approximately Unbiased (AU) test, 29aptamers, 367Aquifex aeolicus, 122, 484nAquificales, 161Arabidopsis

distribution of paralogous gene family size, 92

genomescape, 63arborescence, 149archaea, 41

Caldiarchaeum subterraneum,195-196

contribution to origins of eukaryotes,189-192

expression regulation, 116-119Gene Transfer Agents (GTAs),

121, 268genome architecture, 139

conserved gene neighborhoods,113-115

gene order, 111-112genome size, 107-109operons, 112überoperons, 113wall-to-wall organization, 109

genome sequencing, 106-107genomic signatures, 135-137horizontal gene transfer (HGT) in,

119-134, 141

500 index

Ignicoccus hospitalis, 109Methanosarcina, 108, 122, 191, 205mobilome, 128-131Nanoarchaeum equitans, 108-109, 325signal transduction, 116-119Thaumarchaeota, 206Thermoplasma, 207Thermoproteales, 207

archaeal membrane phospholipids, 491nArchaeal Progenitor of Eukaryotes

(APE), 205archaeo-eukaryotic DNA primase, 309archezoa, 178, 181archezoan scenario of eukaryogenesis,

198-204Argonaute, 197artifacts of phylogenetic analysis, 30ascoviruses, 318Aspergillus fumigatus, 65ATPases, 118, 310, 335-336, 342, 349AU (Approximately Unbiased) test, 29

bBacillus subtilis, 92bacteria

Actinobacteria, 161alpha-proteobacteria, 45, 177antibiotic resistance, 267Aquifex aeolicus, 122, 484nAquificales, 161Bacillus subtilis, 92bacterial IQ, 119conjugation, 132-133contribution to origins of eukaryotes,

189-192Cyanobacteria, 161, 179Deinococcus radiodurans, 129,

136-137, 161Epulopiscium, 202Escherichia coli, 59, 120, 269, 410evolution in, 40-41expression regulation, 116-119Firmicutes, 161Fusobacteriae, 161Gene Transfer Agents (GTAs), 121, 268genome architecture, 139


gene order, 111-112genome sequencing, 106-107genomic signatures, 135-137genome size, 107-109operons, 112

überoperons, 113wall-to-wall organization, 109

giant bacteria, 202Haemophilus influenzae, 51, 65-66horizontal gene transfer (HGT) in,

119-134, 141, 266-268hyperthermophilic bacteria, 484nimportance of, 105-106mobilome, 128-131Mycobacterium leprae, 62Mycoplasma genitalium, 65-67, 483nPelagibacter ubique, 109, 246, 414Prochlorococcus, 246, 414proteobacteria, 45, 177Pseudomonas aeruginosa, 484nRickettsia, 62signal transduction, 116-119Sorangium cellulosum, 108species abbreviations, 485-486nstress-induced mutagenesis, 270Thermotoga maritima, 92, 115, 122, 161Thermus thermophilis, 129, 135

bacterial IQ, 119bacterial phospholipids, 491nbacteriophages, 120, 267, 293, 299, 305bacteriorhodopsin, 267baculoviruses, 324Bapteste, Eric, 150Baross, John, 379Bateson, William, 487nBayesian inference, 28BBB (Biological Big Bang) model,

159-160BDIM (Birth, Death, and Innovation

Model), 93-94Behe, Michael, 479nBeijerinck, Martinus, 294bidirectional best hits, 55Big Bang, 432, 436biological (evolutionary) information

density, 228-230Biological Big Bang model, 159-160biological concept of species, 14biological importance, 88-89biological information transmission,

275-281biophilic domain, 384Birth, Death, and Innovation Model

(BDIM), 93-94Blackburn, Elizabeth, 490nBohr, Niels, 427Boltzmann, Ludwig, 4, 33, 226bootstrap analysis, 29Bork, Peer, 148bricolage, 40bureaucracy ceiling hypothesis, 98-99

index 501

cc-di-GMP-dependent signal

transduction, 118c-value paradox, 35cages, 279Cairns, John, 269Caldiarchaeum subterraneum, 195-196canalization, 45capacitation, 285-286capacitors, 286capsidless genetic elements, 490ncapsids, 295Carroll, Lewis, 491nCarroll, Sean, 157Carsonella rudii, 133Cas (CRISPR-associated proteins),

263-265cas genes, 130, 263, 488-489nCas1 protein, 489ncaspase, 118catabolite repressor protein (CRP), 116Caudovirales, 305Cavalier-Smith, Tom, 183Cavalli-Sforza, Luigi-Luca, 132CC (Compressed Cladogenesis) model,

157-159CCH (coding coenzyme handles), 369Cech, Thomas, 361cell degeneration hypothesis of virus

evolution, 315-316cells, emergence of, 339-343Central Dogma of molecular biology,

259, 272, 360chance, 437chaperones, 279Chargaff, Erwin, 23, 481nChargaff rules, 23chemical frameworks for the origin of

life, 377-382chlorophyll-dependent

photosynthesis, 267chloroplasts, 44Chromalveolata, 182-183, 189chromatin, 173-175chromosomal inversions, 76circoviruses, 298Clustered Regularly Interspaced Short

Palindromic Repeats (CRISPR), 130,263-265

clustering of prokaryotes, 110Clusters of Orthologous Genes (COGs),

55-57, 124-125, 483nCMBR (cosmic microwave background

radiation), 431

CNE (constructive neutral evolution),249-250, 416

co-orthologs, 56coacervate droplets, 378coarse-grained macroscopic history,

432, 436coding coenzyme handles (CCH), 369codons, 88, 278, 366-368COGs (Clusters of Orthologous Genes),

55-57, 124-125, 483n“combinatorial scenario” for origin of

eukaryotes, 222-223comparative genomics

breakdown of genes by evolutionary age, 54

Clusters of Orthologous Genes (COGs),55-57

co-orthologs, 56elementary events of genome evolution,

75-76evolutionary relationships between

genes, 56fluidity of genomes, 59-61gene universe, 65-66

fractal structure of, 71-75minimal gene sets, 66-69non-orthologous gene displacement

(NOGD), 69-71genome architecture, 61genome diversity, 50-53genomescapes, 61-64homologs, 56minimal gene sets, 66-69multidomain proteins, 58-59non-orthologous gene displacement

(NOGD), 69-71orthologous lineages, 55-56orthologs, 56paralogs, 56sequence conservation, 54-55xenologs, 56

compartmentalization, 378complementarity principle, 366, 417-418complementation, 126complexity. See also non-adaptive theory

of genome evolutioncomplexity hypothesis, 126constructive neutral evolution (CNE),

249-250Darwinian modality of evolution, 5definition of, 227-230evolution of, 415-416exaptation, 249genomic complexity, 226as genomic syndrome, 242-245

502 index

importance of relaxed purifyingselection for evolution of complexity,237-242

“irreducible complexity,” 5, 211, 248, 479n

Kolmogorov complexity, 226-227organizational complexity, 226, 247-250paradox of biological complexity,

413-416complexity hypothesis, 126Compressed Cladogenesis model,

157-159conjugation, 132-133conserved gene neighborhoods, 113constrained trees, 29constructive neutral evolution (CNE),

249-250, 416continuum of Darwinian and Lamarckian

mechanisms of evolution, 271-274Copernicus, Nicolaus, 427core genes, 74coronaviruses, 296correlomics studies, 85cosmic microwave background radiation

(CMBR), 431cosmology

anthropic principle, 433-437Big Bang, 436coupled replication-translation systems,

434-435eternal inflation, 382-391inflation, 431-432, 436island (pocket) universes, 432, 436many worlds in one (MWO) model,

431-437multiverse, 432, 436O-regions, 432-436

coupled replication-translation systems, 434-435

Crenarchaeota, 191, 303, 318Crick, Francis, 21, 25, 35, 258, 360CRISPR (Clustered Regularly

Interspaced Short PalindromicRepeats), 130, 263-265, 489n

CRISPR-associated proteins (Cas), 263-265

crown group phylogency, 181CRP (catabolite repressor protein), 116crystallization, 332-334Cyanobacteria, 161, 179cytoskeleton, 172, 175

dd’Herelle, Felix, 315, 338Dagan, Tal, 148Danchin, Antoine, 490nDennett, Dan, 4, 406Darwin’s Black Box: The Biochemical

Challenge to Evolution (Behe), 479nDarwin, Charles, 1, 105, 257. See also

DarwinismDarwinian modality of evolution, 2-6,

14, 17-18interest in microbes, 484non evolution of organization

complexity, 248On the Origin of Species, 3, 17Tree of Life (TOL) concept, 25, 145-148

Darwin, Erasmus, 2Darwin-Eigen cycle, 353-355Darwinian modality of evolution, 2-6, 14,

17-18, 262, 271-274Darwinian threshold, 345, 349Darwinism

explained, 2, 14, 17-18, 479npostmodern assessment of, 398-399

gradualism, 402-403selection, 399-402Tree of Life (TOL), 403-404variation, 402-403

Dawkins, Richard, 35, 152, 283, 413, 481, 486n

Dayhoff, Margaret, 26defective interfering particles, 321Deinococcus radiodurans, 129,

136-137, 161Delbruck, Max, 293deletion/loss, 76Deleuze, Gilles, 422derived shared characters, 183desiccation resistance, 136determinism, 405-408dialectical materialism, 491nDicer, 197direct-RNA-templating hypothesis, 369directons, 115distance phylogenetic methods, 27diversity

of genomes, 50-53of replication-expression strategies in

viruses, 296-297DNA-dependent RNA polymerases,

277, 296DNA packaging, 121DNA polymerase, 83DNA structure, 21

index 503

DNA viruses, 304Dobzhansky, Theodosius, 13, 16, 480ndomains of life, 220, 412-413domains, evolutionary, 58Doolittle, W. Ford, 35, 147, 150Drake hypothesis, 276Drake, Jan, 276Drosophila, 13, 63, 229Drummond, Allan, 87dsDNA genomes, 296dsDNA-replicons, 312dsDNA viruses, 298-299dsRNA viruses, 312duplication, gene, 76, 91-92, 250

eE. coli, 59, 120, 269, 276, 410EAL domain, 117Echols, Harrison, 269effective population size (Ne), 101,

231-233Eigen, Manfred, 23, 353Eigen threshold, 353Einstein, Albert, 418, 428Eldredge, Niles, 14, 38, 46elementary events of genome

evolution, 75-76ELFs (Evil Little Fellows), 110emergent properties, 100Empedokles, 2empires of life, 294, 412-413endomembranes, 172, 175endosymbiosis, 44-45, 175, 179-180Engels, Friedrich, 491nentropic genomes, 229entropy, 226-230, 283, 288. See also

genome streamliningenvironmental virology, 300-301epigenetic inheritance, 288epigenetic landscape, 45epistasis, 405-406Epulopiscium, 202ERP (Error-Prone Replication) principle,

22-25, 101error catastrophe threshold, 281error threshold, 275Error-Prone Replication (EPR) principle,

22-25, 101escaped gene scenario, 315-316Escherichia coli, 59, 120, 269, 276, 410ESPs (eukaryote signature proteins), 203eternal inflation, 382-391, 432

eukaryogenesis, 172, 236, 280archael and bacterial contribution to

origin of eukaryotes, 189-192eukaryotic introns, 217-220Last Eukaryote Common Ancestor

(LECA), 185-189modeling, 198-199origin of key functional systems of

eukaryotic cell, 192-198root of eukaryotic evolutionary tree,

research into, 183-185stem phase of eukaryotic evolution,

187-189symbiogenesis versus archezoan

scenarios, 198-204symbiogenesis-triggered eukaryogenesis,

204-217Eukaryota, 41eukaryote signature proteins (ESPs), 203eukaryotes, 105

antivirus defense, 323chromatin organization, 173-175compared to prokaryotes, 171-174, 178cytoskeleton, 172, 175definition of, 171endomembranes, 172, 175endosymbiosis, 175, 179-180eukaryogenesis

archael and bacterial contributionto origin of eukaryotes, 189-192

eukaryotic introns, 217-220Last Eukaryote Common Ancestor

(LECA), 185-189modeling, 198-199origin of key functional systems of

eukaryotic cell, 192-198root of eukaryotic evolutionary

tree, research into, 183-185stem phase of eukaryotic evolution,

187-189symbiogenesis versus archezoan

scenarios, 198-204symbiogenesis-triggered

eukaryogenesis, 204-217eukaryote signature proteins

(ESPs), 203evolution of exon-intron gene structure,

234-237FECA (First Eukaryotic Common

Ancestor), 236genome architecture, 61, 412genome diversity, 53genomescapes, 63-64horizontal gene transfer (HGT), 213,

266-268

504 index

internal architecture of, 172-174intracellular trafficking, 173, 176Last Eukaryote Common Ancestor

(LECA), 187, 234-236megagroups of, 183mitochondria, 176-178mitochondria-like organelles (MLOs),

178-179nucleus, 173ratio of nonsynonymous/synonymous

substitutions, 34reverse transcription, 266RNA interference (RNAi), 265-266spliceosomes, 197, 212, 249splicing, 280supergroups of, 180-185transcription factor–binding sites, 239

Europa, potential discovery of life forms on, 390

Euryarchaeota, 191Evil Little Fellows (ELFs), 110evolution as tinkering, 40evolution of evolvability, 283-289evolution, definition of, 397evolutionary bootstrapping, 212evolutionary capacitors, 285evolutionary domains, 58evolutionary entropy, 226-230, 283, 288.

See also genome streamliningevolutionary extrapolation, 284evolutionary foresight, 283-289evolutionary genomics, birth of, 43-44evolutionary information density, 228-230evolvablity, evolution of, 283-289exaptation, 39, 249, 368, 370Excavates, 183, 186exon-intron gene structure, 234-237exon theory of genes, 217exosome, 280experimental evolution, 410-411expression regulation in bacteria and

archaea, 116-119extinction, 10eye, evolution of, 5, 248

fF-ATPases, 342false (high-energy) vacuum, 432FECA (First Eukaryotic Common

Ancestor), 236Feynman, Richard, 427Firmicutes, 161

First Eukaryotic Common Ancestor(FECA), 236

Fisher’s theorem, 7-9, 480nFisher, Ronald, 7, 21, 480-481nFitch (least squares) method, 27Fitch, Walter, 37fitness, 8, 89fitness landscapes, 480n

explained, 8Mount Fujiyama landscape, 9

flagella, 180Forest of Life (FOL), 165-166

Biological Big Bang model, 159-160Compressed Cladogenesis model,

157-159definition of, 152horizontal gene transfer (HGT),

164-165Inconsistency Score, 158Nearly Universal Trees (NUTs), 153-156web-like signals, 160-163

“A Formal Test of the Theory ofUniversal Common Ancestry”(Theobald), 491n

Forterre, Patrick, 295, 339Foster, Patricia, 269Fowles, John, 479nFox, George, 41fractal gene space-time, 110-111fractal organization of gene universe,

71-75Franklin, Rosalind, 21Freeland, Stephen, 367The French Lieutenant’s Woman

(Fowles), 479nfrozen accident, 366FtsK family, 310FtsK/HerA, 310functional space, 135-137fundamental units of evolution, 151-153fungal prion proteins, 286fungi, Aspergillus fumigatus, 65Fusobacteriae, 161

gGell-Mann, Murray, 486ngene duplication, 36-37, 76, 91-92, 250gene homology, 37gene jumping, 268gene knockout, phenotypic effects of,

88-89gene neighborhood networks, 113-115

index 505

“Gene Order Is Not Conserved inBacterial Evolution” (Mushegian andKoonin), 483n

gene orthology, 55gene replication, tree-like nature of, 149gene sharing, 113gene status, 86-87gene transfer, 416Gene Transfer Agents (GTAs), 121,

268, 301gene universe, 65-66

elementary events of genome evolution,75-76

fractal structure of, 71-75minimal gene sets, 66-69non-orthologous gene displacement

(NOGD), 69-71generalized uniformitarianism, 16genes in pieces, 217genetic draft, 11, 15genetic drift, 9, 15, 415The Genetical Theory of Natural

Selection (Fisher), 7genetics

birth of, 6-7population genetics, 7-12

Fisher’s theorem, 7-8fitness landscapes, 8-9genetic draft, 11, 15genetic drift, 9-10, 15

Genetics and the Origin of Species(Dobzhansky), 13

genome streamlining, 242-245, 252, 414genome-to-phenotype mapping, 409-410genomes

architecture, 61breakdown of genes by evolutionary

age, 54definition of, 50diversity, 50-53entropic genomes, 229fluidity of, 59-61genome evolution, non-adaptive theory

of, 250-253gene architecture in eukaryotes,

234-237genome streamlining, 242-245importance of relaxed purifying

selection for evolution ofcomplexity, 237-242

population bottlenecks, 232population genetics, 231-233,

245-247genome streamlining, 242-245, 252, 414

genome-to-phenotype mapping, 409-410

genomescapes, 61-64identifying in selfish elements, 490ninformational genomes, 229orthologous lineages, 55-56sequence conservation, 54-55

genomescapes, 61-64genomic complexity, 226genomic hitchhiking, 113genomic parasites, 324genomic signatures, 135-137genomic syndrome, 399geochemical frameworks for the origin of

life, 377-382GGDEF domain, 117giant bacteria, 202giant viruses, 293Gibbs, Josiah Willard, 33Gilbert, Walter, 217, 361Gillespie, John, 10GINS subunits, 203giruses, 293Global Ocean Survey, 301Gogarten, J. Peter, 147Gould, Stephen Jay, 14, 38, 249, 406gradualism, 15, 38-40, 402-403. See also

punctuated equilibriumThe Grand Design (Hawking and

Mlodinov), 493nGray, Michael, 249Greider, Carol, 490nGros, Olivier, 206Group II self-splicing introns, 209-210Group selection, 341GTAs (Gene Transfer Agents), 121,

268, 301GTPases, 118, 356Guattari, Felix, 422Guth, Alan, 431

hH+(Na+)-ATPase/ATP synthase, 342Haeckel, Ernst, 17, 40, 105, 146Haemophilus influenzae, 51, 65-66Haldane, J. B. S., 7, 315, 338, 377,

481-482nhallmark genes, 305-314halobacteria, 122Hawking, Stephen, 427, 493nHeat Shock Protein (HSP), 285Heisenberg principle, 432

506 index

helicases, 197helix-turn-helix (domain), 117herA-nurA operon, 129Heraclites, 2heredity. See inheritanceheterokonts, 183HGT (horizontal gene transfer), 147-148,

164-165, 266-268, 336, 403HGT optimization hypothesis, 132-133in eukaryotes, 213-214in prokaryotes, 119-134, 141

‘highly conserved’ genes, 55highly resolved tree of life, 148hitchhiking, 11, 15HIV, 275Hodgkinia cicadicola, 107, 133holographic bound, 432At Home in the Universe: The Search for

the Laws of Self-Organization andComplexity (Kauffman), 486n

Homo sapiens, 92homologous genes, 37homologous recombination, 150-151homologs, 56homoplasy, 30horizontal gene transfer. See HGTHSP (Heat Shock Protein), 285Hurst, Lawrence, 367Huxley, Julian, 13Huxley, Thomas Henry, 16, 479nHydrogen Hypothesis, 207hydrogenosomes, 178hydrothermal vents, 337, 379, 381hyperthermophiles, 135hyperthermophilic bacteria, 135, 484n

iicosahedral (spherical) capsids, 342icosahedral viruses, 308ID (intelligent design), 479nIgnicoccus hospitalis, 109illegitimate recombination, 150immunoglobulin gene clusters, 323in paralogs, 56Inconsistency Score, 158Inconstancy of the Genome

(Khesin), 481ninfectious proteins, 489ninflating bureaucracy, 98inflation, 431-432, 436inflationary cosmology

anthropic principle, 433-434, 437Big Bang, 436

coupled replication-translation systems,434-435

island (pocket) universes, 432, 436many worlds in one (MWO) model,

431-437multiverse, 432O-regions, 432-436

influenza viruses, 275information theory, 275information transmission, 275-281informational genomes, 229inheritance

epigenetic inheritance, 288Lamarckian inheritance, 487n

compared to Darwinian modalityof evolution, 262

compared to Wrightian modality ofevolution, 262

continuum of Darwinian andLamarckian mechanisms ofevolution, 271-274

CRISPR-Cas system of antivirusimmunity in prokaryotes, 263-265

eukaryotic RNA interference(RNAi), 265-266

explained, 257-259horizontal gene transfer (HGT),

266-268Lamarckian-type epigenetic

inheritance, 266piRNAs, 266principles of, 259-261stress-induced mutagenesis,

268-271Mendelian inheritance, 6

inorganic catalysts, 417insertion, 76intelligent design (ID), 479ninterferon system, 323intergenic regions, 139intracellular trafficking, 173, 176intron excision, 200introns

eukaryotic introns, 217-220evolution of exon-intron gene structure,

234-237intron excision, 200“introns early” hypothesis, 217self-splicing introns, 200, 209-210

“introns early” hypothesis, 217iron sulfide, 337“irreducible complexity,” 5, 211,

248, 479nirremediable complexity, 250

index 507

irreversible gene loss, 416island (pocket) universes, 383, 432, 436Ivanovsky, Dmitri, 294

jJacob, Francois, 39, 112, 406jelly roll capsid protein (JRC), 307-308Jenkin, Henry Charles Fleeming, 4Johansson, Wilhelm, 7JRC (jelly roll capsid protein), 308“jumping genes” (mobile elements), 36junk DNA, 35-36, 239-241junk recruitment, 239-241, 252Just So Stories (Kipling), 482n

kKammerer, Paul, 258, 487-488nKauffman, Stuart, 486nKelvin, Lord William Thomson, 4Kepler, Johannes, 427Khesin, Roman, 481nKimura, Motoo, 31Kipling, Rudyard, 482nKishino-Hasegawa test, 29Knight, Rob, 369knockout, phenotypic effects of, 88-89Kol’tzov, Nikolai, 481nKolmogorov complexity, 226-227, 486nKuhn, Thomas, 422

lLa Philosophie Zoologique

(Lamarck), 479nlac operon, 269, 409lac-repressor, 116lactobacilli, 247Lamarck, Jean-Bapteste, 2-3, 257, 479nLamarckian evolution, 3, 403. See also

Lamarckian inheritanceLamarckian inheritance, 257, 487n

compared to Darwinian modality ofevolution, 262

compared to Wrightian modality ofevolution, 262

continuum of Darwinian andLamarckian mechanisms of evolution,271-274

CRISPR-Cas system of antivirusimmunity in prokaryotes, 263-265

eukaryotic RNA interference (RNAi),265-266

explained, 257-259horizontal gene transfer (HGT),

266-268Lamarckian-type epigenetic

inheritance, 266piRNAs, 266principles of, 259-261stress-induced mutagenesis, 268-271

Lamarckian-type epigenetic inheritance, 266

Lamarckism, 3, 257-259. See alsoLamarckian inheritance

lambda phage, 299Landweber, Laura, 369Lane, Nick, 201Last Ancestral Universal Common State

(LUCAS), 332-333, 346-347Last Eukaryote Common Ancestor

(LECA), 185-189, 234-236Last Universal Common (Cellular)

Ancestor (LUCA), 17, 329, 491nlipid vesicle model of precellular

evolution, 340LUCAS (Last Ancestral Universal

Common State), 332primordial Virus World model of

precellular evolution, 337-340, 343, 346

progenotes, 334reconstructing gene repertoire of,

330-337Last Universal Common Ancestor of

Viruses (LUCAV), 313-314lateral genomics, 165Lawrence, Jeffrey, 115, 127LBA (long branch attraction), 26, 30least squares (Fitch) method, 27LECA (Last Eukaryote Common

Ancestor), 185-189, 234-236Lederberg, Joshua, 132Lenski, Richard, 276, 410Lewontin, Richard, 38, 249LexA, 116life, definition of, 352life, origin of, 351-353

Anthropic Chemical Evolution (ACE),386-391

chemical frameworks, 377-382codon assignments, 366-368eternal inflation, 382391geochemical frameworks, 377-382

508 index

primordial broth scenario, 377RNA World hypothesis

problems with, 375-377protein domain evolution, 355-360ribozymes, 360-366

translation, 368-375lipid vesicle model, 340lipid vesicles, 341Lobkovsky, Alexander, 88log-normal distribution, 84long branch attraction (LBA), 26, 30look-ahead effect, 282Lost City, 380LUCA (Last Universal Common

(Cellular) Ancestor), 17, 329, 491nlipid vesicle model of precellular

evolution, 340LUCAS (Last Ancestral Universal

Common State), 332primordial Virus World model of

precellular evolution, 337-340, 343, 346

progenotes, 334reconstructing gene repertoire of,

330-337LUCAS (Last Ancestral Universal

Common State), 332-333, 346-347LUCAV (Last Universal Common

Ancestor of Viruses), 313-314Lyell, Charles, 2-3Lynch, Michael, 131, 230, 250, 276, 400Lyotard, Jean-Francois, 421Lysenko, Trofim, 488nLysenkoist pseudoscience, 258

mM-theory, 493nmacroevolution, 5, 16macroscopic (coarse-grained) history,

432, 436Major Histocompatibility Complex, 323many worlds in one (MWO) model,

384-386, 431-437mapping genomes to phenotype, 409-410Margulis, Lynn, 44, 180Mars, potential discovery of life

forms on, 390Martin, William, 148, 201, 207, 216Maslov, Sergei, 98master universe, 436maturases, 364maximum likelihood (ML), 28

maximum parsimony (MP), 26-27Mayr, Ernst, 13-14, 25, 54mbp (mega basepairs), 52McClintock, Barbara, 36, 268McDonald-Kreitman test, 35mega basepairs (mbp), 52megagroups (of eukaryotes), 183megaplasmids, 129megaverse, 436meiosis, 214Mendel, Gregor, 4-7Mendelian inheritance, 6Mereschkowsky, Konstantin, 44, 482nmesophiles, 136mesophilic archaea, 205metabolomes, 82metagenomics, 293, 300-302metanarratives

construction of, 424trust in, 421-425

metaphors in biology, 481nmetaphysical implications, 426Methanocaldococcus jannaschii, 65, 69Methanosarcina, 122, 191, 205Methanosarcina barkeri, 108Methanosarcinales, 118microbes

Darwin’s interest in, 484nevolution in, 40-42

microcompartments, networks of, 337microevolution, 16microRNAs, 238microspheres, 378mimivirus, 293, 298minimal gene sets, 66-69misfolding, 87-91, 279-280mitochondria, 176-178mitochondria-like organelles (MLOs),

178-179mitosomes, 178ML (maximum likelihood), 28Mlodinow, Leonard, 427, 493nMLOs (mitochondria-like organelles),

178-179mobile elements, 36mobilome, 128-131model-dependent realism, 427-430Modern Synthesis, 7

fundamental principles of, 14-17origins of, 13-14postmodern assessment of, 398-399

gradualism, 402-403selection, 399-402Tree of Life (TOL), 403-404variation, 402-403

problems with, 18-19

index 509

molecular clock, 26molecular evolution

birth of, 25-26gene duplication, 36junk DNA, 35mobile elements, 36molecular clock, 26neutral theory, 31-32orthologs, 37paralogs, 37selfish genes, 35

molecular phenomic variables,correlations with evolutionary rates, 83-89

molecular phylogenetics. See phylogenetics

Monera, 105. See also prokaryotesMonod, Jacques, 112, 423monophyly, 302-305Mount Fujiyama landscape, 9MP (maximum parsimony), 26-27mRNAs, 296Mulkidjanian, Armen, 381Müller’s ratchet, 131Müller, Miklos, 131, 207multidomain proteins, 58-59multiverses, 384, 432, 436Mushegian, Arcady, 67, 483nmutagenesis, stress-induced,

268-271, 403mutations, 402

mutation rates, 275-277mutational meltdown, 131, 275, 280phenotypic mutations, 277-283stress-induced mutagenesis, 268-271de Vries mutational theory of

evolution, 6MWO (many worlds in one) model,

384-386, 431-437Mycobacteria, 247Mycobacterium leprae, 62Mycoplasma genitalium, 65-67, 483n

nNaegleria gruberi, 186Nanoarchaeum equitans, 108, 247, 325natural selection, 3-4

bricolage concept, 40explained, 15Fisher’s theorem, 7-9in generative models for the

genome-wide universals, 100group selection, 341

measuring by sequence comparison, 32-35

population genetics theory, 231-233positive selection, 34purifying (negative) selection, 12, 34-35role and status of, 399-402stabilizing selection, 12-13

NCLDV (Nucleo-Cytoplasmic LargeDNA Viruses), 302, 305, 307

nearly neutral networks, 90-91Nearly Universal Trees (NUTs), 153-156negative selection, 12, 34-35

and evolution of complexity, 237-242population genetics theory, 231-233

negative-strand RNA viruses, 312negentropy, 18neighbor-joining (NJ) method, 27nematodes, 300neo-Darwinism, 7neofunctionalization, 35nested genes, 218net of life, 147, 165networks, 94, 483n

of microcompartments, 337nearly neutral networks, 90-91node degree distribution, 94scale-free networks, 95-96universal scaling laws, 97-99

neutral theory, 31-32, 252The New Foundations of Evolution: On

the Tree of Life (Sapp), 485nNewton, Isaac, 427-428Nidovirales, 298NJ (neighbor-joining) method, 27NMD (Nonsense-Mediated Decay),

211, 280node degree distribution, 94NOGD (non-orthologous gene

displacement), 69-71, 126, 140noise, 277-283non-adaptive theory of genome evolution,

250-253, 415-416case study: gene architecture in

eukaryotes, 234-237genome streamlining, 242-245importance of relaxed purifying

selection for evolution of complexity,237-242

population bottlenecks, 232population genetics, 231-233, 245-247

non-orthologous gene displacement(NOGD), 69-71, 126, 140

non-sequence-based genome trees, 30nonhomologous (illegitimate)

recombination, 150

510 index

Nonsense-Mediated Decay (NMD), 211, 280

nonsynonymous positions, 33nonsynonymous substitutions, 32-35NTP (nucleoside triphosphates), 356NTPase, 310nuclear envelope, 211nuclear pore complexes, 211Nucleo-Cytoplasmic Large DNA Viruses

(NCLDV), 302, 305-307nucleomorph, 179nucleoside triphosphates (NTP), 356nucleus, 173nudiviruses, 318NUTs (Nearly Universal Trees), 153-156

oO-regions, 432-436observable regions of the universe

(O-regions), 432-436off-lattice models (of protein folding), 88Ohno, Susumu, 36Ohta, Tomoko, 32oligonucleotides, 367-369oligophyly, 325one-component systems, 117Oparin, Alexander Ivanovich, 377, 492noperonization, 115operons, 112, 139

herA-nurA operon, 129lac operon, 269operonization, 115selfish operon hypothesis, 115selfish operons, 127, 139überoperons, 113

Opisthokonts, 182ORFans, 110-111, 128, 306organization of bacterial and archaeal

genomes, 109organizational complexity, 226, 247-250organs, use and disuse of, 260Orgel, Leslie, 35, 361origin of life, 351-353, 416-417

Anthropic Chemical Evolution (ACE),386-391

chemical frameworks, 377-382codon assignments, 366-368eternal inflation, 382-391geochemical frameworks, 377-382primordial broth scenario, 377

RNA World hypothesisproblems with, 375-377protein domain evolution, 355-360ribozymes, 360-366

translation, 368-375On the Origin of Species (Darwin), 3, 17,

145-146, 258orthologous lineages, 55-56orthologs, 37, 55-56out paralogs, 56

pP-loop, 356, 359, 492npackaging ATPase, 310Paleoproterozoic era, 204Paley, William, 486nPalm-domains, 312pangenesis, 4pangenomes, 107, 110Panglossian paradigm, 38papilloma viruses, 311papovaviruses, 309paradigms, 25, 32, 35-36paralogs, 37, 56, 92-93parasites

emergence of, 345inevitability of, 320-321Red Queen hypothesis, 322-325

Parmenides, 2Pasteur, Louis, 377pathogenicity islands, 59, 120Pauling, Linus, 25, 146PCD (programmed cell death), 118, 323Pelagibacter ubique, 109, 246, 414Penny, David, 353peptidyltransferase ribozymes, 363Phage Group, 293phagocytosis, 202phenomic variables, correlations with

evolutionary rates, 83-89phenotypes, 401

genome-to-phenotype mapping, 409-410

phenotypic mutations, 277-283Philosophie Zoologique (Lamarck), 257phospholipids, 491nphotosynthesis, 267phyletic pattern, 30phylogenetics, 26, 146

artifacts of, 30Bayesian inference, 28

index 511

bootstrap analysis, 29least squares (Fitch) method, 27maximum likelihood (ML), 28maximum parsimony (MP), 27neighbor-joining (NJ) method, 27non-sequence-based genome trees, 30sequence-based methods, 27shared derived characters, 30simulated trees, 29statistical tests (tree topology), 29ultrametric (simple hierarchical

clustering) methods, 27physics. See statistical physicspiRNAs, 266PIWI-interacting (pi)RNA, 265-266Planctomycetes, 216Plantae, 182-183, 189, 219plasmids, 128, 304, 324plasmodesmata, 299plastids, 179polydnaviruses, 318polyoma viruses, 311polyphyly, 302-305Poole, Anthony, 274, 374Popper, Karl Raymund, 429-430population bottlenecks, 208, 232population dynamics, 400population genetics, 7-12, 231-233,

245-247, 281Fisher’s theorem, 7-8fitness landscapes

explained, 8genetic draft, 11, 15genetic drift, 9-10, 15Mount Fujiyama landscape, 9

founders of, 481npositive selection, 34, 231-233positive-strand RNA viruses, 304Postmodern Synthesis, 417-421postmodernism, 397-398, 421-424

complementarity principle, 417-418determinism, 405-408empires and domains of life, 412-413enigma of origin of life, 416-417experimental evolution, 410-411genome-to-phenotype mapping,

409-410paradox of biological complexity,

413-416postmodern reassessment of Darwin

and Modern Synthesis, 398-399gradualism, 402-403selection, 399-402Tree of Life (TOL), 403-404variation, 402-403

Postmodern Synthesis, 417-419statistical physics, 404-405stochasticity, 405-408viruses and prokaryotes, 411

postmodernist philosophy, 421-424power law 92-96poxviruses, 308, 324pre-cellular compartmentalization, 378preferential attachment, 95-96primordial broth, 337, 377primordial Virus World model of

precellular evolution, 315-317, 337-340,343, 346

prions, 489nprion-mediated potentiation of

evolvability, 286self-propagating prions, 491n

probability, 437Prochlorococcus, 246, 414progenotes, 334programmed cell death (PCD), 118, 323progress, 253, 260, 486nprokaryotes, 105. See also

archaea; bacteriaantivirus defense, 323chromatin organization, 175clustering of, 110compared to eukaryotes, 171-174, 178conjugation, 132-133CRISPR-Cas system of antivirus

immunity, 263-265difficulty in defining, 138-139evolution in, 40expression regulation, 116-119fluidity of genes, 59fractal gene space-time, 110-111Gene Transfer Agents (GTAs), 121, 268genome architecture, 61, 139


gene order, 111-112genome size, 107-109operons, 112überoperons, 113wall-to-wall organization, 109

genome diversity, 53genomescapes, 61genomic signatures, 135-137HGT (horizontal gene transfer),

119-134, 141, 147, 266-268mobilome, 128-131ORFans, 110-111pangenomes, 110ratio of nonsynonymous/synonymous

substitutions, 34

512 index

signal transduction, 116-119signals of tree-like and web-like

evolution, 160-163transcription-translation coupling,

173, 176proofreading, 277properties, emergent, 100protease, 118proteasome, 194, 280protein between

misfolding, 87off-lattice folding model, 88

Protein Breakthrough, 366, 374protein-coding sequences, 34-35proteinoids, 378proteins

archaeo-eukaryotic DNA primase, 309Argonaute, 197ATPase subunit of terminase, 310Cas (CRISPR-associated proteins),

263-265Cas1, 489nchaperones, 279Dicer, 197eukaryote signature proteins

(ESPs), 203fungal prion proteins, 286Heat Shock Protein (HSP), 280, 285infectious proteins, 489njelly roll capsid protein (JRC), 307-308multidomain proteins, 58-59packaging ATPase, 310Protein Breakthrough, 366, 374protein domain evolution, 355-360protein evolution

model of misfolding-driven proteinevolution, 90-91

robustness to misfolding, 87, 90-91,279-280

protein foldingmisfolding, 87, 90-91, 279-280models of, 483n

protein sequence conservation, 26reverse transcriptase (RT), 298, 311RNA-binding proteins, 287RNA-dependent RNA polymerase

(RdRp), 298, 311rolling circle replication initiation

endonuclease (RCRE), 309-311security proteins, 324Sm proteins, 197Superfamily 3 helicase (S3H), 307-308ubiquitin, 195-196UL9-like superfamily 2 helicase, 309

proteobacteria, 177proteomes, 82

Protista, 105. See also eukaryotesproto-ribosome, 374Prusiner, Stanley, 489npseudo-paralogs, 94pseudogenes, 62Pseudomonas aeruginosa, 484nPuigbo, Pere, 152punctuated equilibrium, 37-38purifying (negative) selection, 12, 34-35

and evolution of complexity, 237-242population genetics theory, 231-233

q-rThe Quark and the Jaguar: Adventures

in the Simple and the Complex(Gell-Mann), 486n

radioresistance, 136-137Radman, Miroslav, 269random genetic drift, 263random variation, 3, 14randomness, 437Raoult, Didier, 295, 422, 493nrare genomic changes (RGCs), 30, 183ratchet of constructive neutral

evolution, 416ratchet of gene transfer, 208, 416ratchet of irreversible gene loss, 416RCRE (rolling circle replication initiation

endonuclease), 309, 311RdRp (RNA-dependent RNA

polymerase), 298, 311realism, model-dependent, 427-430reciprocal altruism, 341Reclinomonas americana, 176, 184recombination, 76

homologous recombination, 150-151nonhomologous (illegitimate)

recombination, 150tree-like nature of, 150-151

reconstructed gene repertoire of LUCA(Last Universal Common (Cellular)Ancestor), 330-337

Red Queen hypothesis, 322-325regulators, 116, 286regulons, 116relaxed purifying selection and evolution

of complexity, 237-242replication

Darwin-Eigen cycle, 353-355Eigen threshold, 353error rates, 275-277

index 513

Error-Prone Replication (EPR)principle, 22-25

replication-expression strategies inviruses, 296-297

tree-like nature of, 149replicators, 320-321. See also origin of lifereplicon fusion, 129restriction enzymes, 130restriction-modification (RM), 128retro-transcribing elements, 296-298,

304, 312reverse gyrase, 135reverse transcriptase (RT), 210, 296,

298, 311reverse transcription, 266RGCs (rare genomic changes), 30, 183Rhizaria, 183rhizome of life, 404, 422rhizomes, 493nribbon-helix-helix (domain), 117ribosomal (r)RNA, 176ribosomal peptidyltransferase, 363ribosomal superoperon, 113ribozymes, 209, 360-362, 365-366Rickettsia, 62, 177, 247RM (restriction-modification), 128RNA 3’-aminoacylation, 363RNA-binding proteins, 287RNA demethylases, 276RNA endonuclease toxins, 130RNA interference (RNAi), 265-266, 345RNA ligase, 363RNA polymerase, 363RNA recognition motif (RRM), 312RNA viruses. See also viruses

negative-strand RNA viruses, 312positive-strand RNA viruses, 296

RNA World hypothesis, 312problems with, 375-377protein domain evolution, 355-360ribozymes, 360-362, 365-366

RNA-dependent RNA polymerase(RdRp), 298, 311

RNAi (RNA interference), 265-266, 345RNAse P, 364RNome, 238robustness, 45, 87-91robustness of biological systems, 283-287robustness to misfolding, 279-280Rogozin, Igor, 184rolling circle replication initiation

endonuclease (RCRE), 309-311Rossmann fold, 355Rous Sarcoma Virus, 293RpoS, 269

RRM (RNA recognition motif), 312rRNA, 41, 176, 364RT (reverse transcriptase), 210,

296-298, 311Russell, Michael, 337, 379

sS3H (Superfamily 3 helicase), 307-308Saccharomyces cerevisiae, 65, 89, 92Sagan, Dorion, 180Sagan, Lynn (Margulis), 44Sapienza, Carmen, 35Sapp, Jan, 485nscale-free networks, 95-96scaling

scale-free networks, 95-96universal scaling laws, 97-99

Schroedinger, Erwin, 18, 481nsea anemone, 65security proteins, 324selection

group selection, 341population genetics theory, 231-233purifying (negative) selection, 12, 34-35

and evolution of complexity, 237-242

population genetics theory, 231-233

role and status of, 399-402selection amplification (SELEX), 367

SELEX (selection amplification), 367self-aminoacylation, 363self-propagating prions, 491nself-splicing introns, 200, 209-210, 249selfish cooperators, 341-342, 346The Selfish Gene (Dawkins), 481nselfish genes, 35, 152, 413selfish operons, 115, 127, 139semi-adaptive hypothesis on evolution of

mutation rates, 276sequence analysis of protein-coding

sequences, 34-35sequence-based phylogenetic

methods, 27sequence comparison, 32-35sequence conservation, 54-55serine-threonine protein kinases, 118Shannon formula for entropy, 226Shannon, Claude, 275, 480nshared derived characters, 30signal recognition particle (SRP), 336signal transduction, 116-119

514 index

simple hierarchical clustering(ultrametric) methods, 27

Simpson, George Gaylord, 13-14, 38simulated trees, 29singularity, 432siRNA system, 265size of genomes

in viruses, 298in bacteria and archaea, 107-109

Sm proteins, 197, 249small nuclear (sn)RNAs, 249, 364Smith, Adam, 15Smith, Hamilton, 51Smith, John Maynard, 10snRNAs, 249Sorangium cellulosum, 108SOS (stress response) regulator, 116SOS repair, 269, 284spandrels, 38-40“Spandrels of San Marco” (Gould and

Lewontin), 38species abbreviations, 485-486nspecies tree, 146, 159Spiegelman, Sol, 245, 410spliceosomes, 197, 212, 249splicing, 209-210, 237-239, 280, 364sponges, 65SRP (signal recognition particle), 336ssDNA, 296ssDNA-replicons, 311stabilizing selection, 12-13Stanier, Roger, 106Stanley, Wendell, 295statistical physics, 81, 101, 404-405.

See also systems biologystatistical tests (tree topology), 29stem phase of eukaryotic evolution,

187-189stereochemical hypothesis, 367stochasticity, 99-101, 405-408Stoltzfus, Arlin, 249streamlined genomes, 414streamlining, 217, 242-245, 252stress response (SOS) regulator, 116stress-induced mutagenesis, 268-271, 403strict gradualism, 15string theory landscape, 432“strong” anthropic principle, 433, 492nStructure of Scientific Revolutions

(Kuhn), 422struggle for existence, 2subfunctionalization, 370-372substitution, 76Superfamily 3 helicase (S3H), 307-308

supergroups (of eukaryotes), 180-185supernetwork, 157superoperon, 341supplying devices, 414survival of the fittest, 3, 287survival of the flattest, 287Susskind, Leonard, 432symbiogenesis-triggered eukaryogenesis,

198-217“symbiosis islands,” 120synapomorphies, 30, 183synonymous substitutions, 32-35systems biology, 82

Birth, Death, and Innovation Model(BDIM), 93-94

bureaucracy ceiling hypothesis, 98-99correlations between evolutionary and

phenomic variables, 83-89emergent properties, 100gene duplication, 91-92gene status, 86-87networks

nearly neutral networks, 90-91node degree distribution, 94preferential attachment, 95-96scale-free networks, 95-96universal scaling laws, 97-99

stochasticity, 99-101universal distribution of paralogous

family sizes, 92-93Szathmary, Eors, 341, 365Szostak, Jack, 340, 490n

tTA (toxin-antitoxin) systems, 128-130tailed bacteriophages, 305Taq polymerase, 136telomerase, 213, 299, 312, 490ntemperate bacteriophages, 299terminase, ATPase subunit of, 310testing performance of phylogenetic

methods, 29Tetrahymena, 361Thaumarchaeota, 191, 206Theobald, Douglas, 491nthermophiles, 136thermophilic phenotype, 135Thermoplasma, 207Thermoproteales, 207Thermotoga maritima, 92, 115, 122Thermotogae, 161Thermus thermophilis, 129

index 515

Theseus ship metaphor, 490nThomson, William (Lord Kelvin), 4Thousand Plateaus: Capitalism and

Schizophrenia (Deleuze and Guattari), 493n

three-domain Tree of Life, 41-43Through the Looking Glass and What

Alice Found There (Lewis), 491ntime arrow, 3Timofeev-Resovski, Nikolai, 481ntinkering, evolution as, 40TOL. See Tree of Lifetoxin-antitoxin (TA) systems, 128-130, 324trans-translation, 280transcription, 238

error rates, 277transcription factor–binding sites,

239-241transcription factors, 241-242

transcription factor–binding sites, 239-241

transcription factors, 241-242transcription-translation coupling,

173, 176, 199, 216transcriptomes, 82transitional epochs

Biological Big Bang model, 159-160Compressed Cladogenesis model,

157-159transformation, 38, 45translation

error rates, 277origin of, 368-375

TRAPP complex, 203Tree of Life (TOL), 17, 25, 165, 403-404,

485n. See also Forest of Life (FOL)arborescence, 149controversy over, 147-148“highly resolved tree of life,” 148history of, 145-147intrinsic tree-like nature of fundamental

units of evolution, 149-150, 153three-domain Tree of Life, 41-43

tree topology, 29Trichoplax, 65triplicase, 375tRNAs, 176, 359, 364, 369-373tubulin, 172, 203two-component systems, 117

uUb (ubiquitin), 195-196Ub ligase, 196überoperons, 113ubiquitin, 195-196, 203ubiquitin ligase, 196ubiquity of viruses, 300-301UL9-like superfamily 2 helicase, 309ultrametric (simple hierarchical

clustering) methods, 27uniformitarianism, 16, 398Unikonts, 182-183Universal Common Ancestry

hypothesis, 146universal distribution of paralogous

family sizes, 92-93universal scaling laws, 97-99universes

island (pocket) universes, 383, 432, 436master universes, 436

untranslated regions (UTRs), 86use and disuse of organs, 260UTRs (untranslated regions), 86

vV-ATPases, 343Van Niel, Cornelius, 106Van Nimwegen, Eric, 97, 484nVan Valen, Leigh, 491nvariation, 402-403Venter, J. Craig, 51, 301Vilenkin, Alexander, 383viral domains, 413viral hallmark genes, 305-314viral packaging, 342Virchow, Rudolf, 318virions, 295, 342viroids, 295, 298viromes, 300-301virus defense islands, 322Virus World, 294, 314-319, 325-326,

335-346, 411, 490nviruses, 411-413, 482n

antivirus defense, 322-325bacteriophages, 293, 299, 305baculoviruses, 324and birth of evolutionary genomics,

43-44circoviruses, 298classes of viral genes, 303

516 index

Crenarchaeota, 303, 318definition of, 294-295DNA viruses, 304dsDNA viruses, 298-299dsRNA viruses, 312environmental virology, 300-301functional content, 298-299Gene Transfer Agents (GTAs), 301genome architecture, 298-300, 490ngenome diversity, 53genome sizes, 298genomescapes, 61giant viruses, 293HIV, 275icosahedral viruses, 308influenza viruses, 275Last Universal Common Ancestor of

Viruses (LUCAV), 313-314metagenomics of, 300-302mimivirus, 293, 298negative-strand RNA viruses, 312Nucleo-Cytoplasmic Large DNA

Viruses (NCLDV), 302, 305-307origin and evolution, 314

cell degeneration scenario, 315-316escaped gene scenario, 315-316“primordial” hypothesis, 315-317

papovaviruses, 309polyphyly versus monophyly, 302-305positive-strand RNA viruses, 296, 304poxviruses, 308, 324replication-expression strategies,

296-297retro-transcribing elements, 296-298,

304, 312Rous Sarcoma Virus, 293ubiquity of, 300-301viral domains, 413viral genes, 306-307viral hallmark genes, 305-314viroids, 295, 298viromes, 300-301virus defense islands, 322Virus World, 294, 314-319, 325-326,

335-346, 411, 490nvon Neumann, John, 481nde Vries, Hugo, 6

wWachtershauser, Günter, 379Waddington, Conrad, 45Walker A motif, 356Walker, John, 492nwall-to-wall genomes, 109Wallace, Alfred Russel, 2Watson, James, 21“weak” anthropic principle, 384,

433, 492nWeb of Life, 404Web-like signals, 160-163Weismann, August, 258, 487nWGD (whole genome duplication), 36whole genome duplication (WGD), 36Wilke, Claus, 87Wilson, Allan, 83Winkler, Hans, 483nWoese, Carl, 41, 106, 220, 332, 336,

360, 412Wolbachia, 177, 247Wolf, Yuri, 88, 152, 369Wollman, Elie, 132Wright, Sewall, 7-10, 15, 262Wrightian evolution, 262, 403

x-y-zxenologs, 56, 126

Yarus, Michael, 369yeasts, Saccharomyces cerevisiae, 65,

89, 92

Zhang, Jianzhi, 89zinc sulfide mounds, 381Zn-ribbon, 117Zuckerkandl, Emile, 25, 146

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