Chapter 55

Darwin in the Twenty-First Century:Natural Selection, Molecular Biology,and Species Concepts1

Francisco J. Ayala

55.1 CHARLES DARWIN

Charles Darwin was born in 1809, 70 years beforeEinstein, and published The Origin of Species in 1859.The year 2009 marked the 200th anniversary of Darwin’sbirth and the sesquicentennial of The Origin of Species’publication. Scientists, universities, natural history muse-ums, and other sorts of people and institutions throughoutthe world celebrated these anniversaries with scientificlectures, symposia, exhibitions, and otherwise. Einsteinpublished his special theory of relativity in 1905 andthe general theory of relativity in 1916. The theoryof relativity is too abstruse to be taught in detail toelementary school children, but its physical implicationsconcerning mass and energy are part of the curriculumin higher school grades and are held without objection orcontempt by the general public. Yet, in the United States,the theory of evolution is not taught in some schools, andonly begrudgingly in others. The general public has heardof evolution and of the claim that humans have evolvedfrom nonhuman ancestors. However, a large numberof people, perhaps a majority, do not consider that the

1In this chapter I have made extensive use of previous publicationsof mine: One hundred fifty years without Darwin are enough! GenomeRes . 19:693–699, 2009; Where is Darwin two hundred years later?J. Genet . 87:321–325, 2008; Evolution in the 21st Century.Co-editors: Daniel Kleinman, Jason Delborne, Karen Cloud-Hansen,and Jo Handelsman, Controversies in Science & Technology , thirdVolume. Mary Ann Liebert, Inc., New Rochelle, NY, 2010; and thebook, Darwin’s Gift to Science and Religion , F. J. Ayala. JosephHenry Press, Washington, DC, 2007.

Handbook of Molecular Microbial Ecology, Volume II: Metagenomics in Different Habitats, First Edition. Edited by Frans J. de Bruijn.© 2011 Wiley-Blackwell. Published 2011 by John Wiley & Sons, Inc.

claims of biological evolution have been demonstrated,or simply reject them as false.

Consider the following: According to a Gallup poll of1016 U.S. adults, taken in November 2004, 45% of thosesurveyed favored the statement that “God created humanbeings in their present form within the last 10,000 years”(38% favored that “man developed over millions of years,but God guided the process,” and 13% favored that “mandeveloped over millions of years from less advanced lifeforms”). The public attitude about the teaching of the the-ory of evolution is no less scary. In a CNN/USA TodayGallup poll of 1001 adults conducted in March 2005, 76%would not “be upset if public schools in (their) communitytaught creationism,” but only 63% would not “be upset ifthe schools taught evolution.” Only 22% would be upsetif creationism would be taught, while 34% would be upsetif evolution would be taught. Other polls yield similarstatistics. There can be no doubt that a crucial link ismissing in the U.S. educational system. Moreover, thepress, television, and other mass communication mediaare failing in any role one might want to allocate to themin informing and educating the citizenry. Many newspa-pers dedicate a much larger amount of print copy to thehoroscope than to science.

55.2 DARWIN AND THE HISTORYOF IDEAS

Darwin occupies an exalted place in the history of West-ern thought, deservedly receiving credit for the theory of

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evolution. In The Origin of Species , published in 1859,he laid out the evidence demonstrating the evolutionof organisms. Darwin did not use the term “evolution,”which did not then have its current meaning, but referredto the evolution of organisms by the phrase “commondescent with modification” and similar expressions.However, Darwin accomplished something much moreimportant for intellectual history than demonstratingevolution. Indeed, accumulating evidence for commondescent with diversification may very well have been asubsidiary objective of Darwin’s masterpiece. Darwin’sThe Origin of Species is, first and foremost, a sustainedeffort to solve the problem of how to account scientificallyfor the adaptations or “design” of organisms. Darwinsought to explain the design of organisms, as well astheir complexity, diversity, and marvelous contrivances,as a result of natural processes. Darwin brought aboutthe evidence for evolution, because evolution was anecessary consequence of his theory of design.

There is a priggish version of the history of the ideasthat sees a parallel between Copernicus’ and Darwin’smonumental intellectual contributions, which are said tohave eventuated two revolutions. According to this ver-sion, the Copernican Revolution consisted in displacingthe Earth from its previously accepted locus as the cen-ter of the universe, moving it to a subordinate place asone more planet revolving around the sun. In congruousmanner, this version affirms that the Darwinian Revolu-tion consisted in displacing humans from their position asthe center of life on Earth, with all the other species cre-ated for the purpose of humankind, and placing humansinstead as one species among many in the living world,so that humans are related to chimpanzees, gorillas, andother species by shared common ancestry. Copernicus hadaccomplished his revolution with the heliocentric theoryof the solar system; Darwin’s achievement emerged fromhis theory of organic evolution.

I propose that this version of the two revolutions isinadequate: What it says is true, but it misses what is mostimportant about these two intellectual revolutions, namelythat they ushered in the beginning of science in the mod-ern sense of the word. These two revolutions may jointlybe seen as the one scientific revolution, with two stages,the Copernican and the Darwinian. Darwin is deservedlygiven credit for the theory of biological evolution, becausehe accumulated evidence demonstrating that organismsevolve and discovered the process, natural selection, bywhich they evolve their functional organization. But TheOrigin of Species is most important because it completedthe Copernican Revolution, initiated three centuries ear-lier, and thereby radically changed our conception of theuniverse and the place of mankind in it.

The Copernican Revolution was launched with thepublication in 1543, the year of Nicolaus Copernicus’

death, of his De Revolutionibus Orbium Celestium (On theRevolutions of the Celestial Spheres), and bloomed withthe publication in 1687 of Isaac Newton’s PhilosophiaeNaturalis Principia Mathematica . The discoveries ofCopernicus, Kepler, Galileo, Newton, and others, inthe sixteenth and seventeenth centuries, had graduallyushered in a conception of the universe as matter inmotion governed by natural laws. It was shown thatthe Earth is not the center of the universe, but a smallplanet rotating around an average star; that the universeis immense in space and in time; and that the motionsof the planets around the sun can be explained bythe same simple laws that account for the motion ofphysical objects on our planet (laws such as f = m × a ,force = mass × acceleration, or the inverse-square lawof attraction, f = g(m1 × m2)/γ2). These and otherdiscoveries greatly expanded human knowledge, butthe conceptual revolution they brought about was morefundamental yet: a commitment to the postulate thatthe universe obeys immanent laws that account fornatural phenomena. The workings of the universe werebrought into the realm of science: explanation throughnatural laws. Physical phenomena could be accounted forwhenever the causes were adequately known.

Darwin completed the Copernican Revolution bydrawing out for biology the ultimate conclusion of thenotion of nature as a lawful system of matter in motion.The adaptations and diversity of organisms, the originof novel and highly organized forms, and the origin ofmankind itself could now be explained by an orderlyprocess of change governed by natural laws.

55.3 FROM NATURAL THEOLOGYTO NATURAL SELECTION

The advances of physical science had driven mankind’sconception of the universe to a sort of intellectualschizophrenia, which persisted well into the mid-nineteenth century. Scientific explanations, derived fromnatural laws, dominated the world of nonliving matter,on the Earth as well as in the heavens. However, super-natural explanations, depending on the unfathomabledeeds of the Creator, were accepted in order to accountfor the origin and configuration of living creatures—themost diversified, complex, and interesting realities of theworld. It was Darwin’s genius that resolved this intel-lectual inconsistency. Darwin completed the CopernicanRevolution by bringing the design of organisms into therealm of science, as an outcome of natural processesgoverned by natural laws.

The conundrum faced by Darwin can hardly be over-estimated. The strength of the “argument from design” todemonstrate the role of the Creator had been forcefully

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set forth by the English clergyman and author WilliamPaley in his Natural Theology; or, Evidences of the Exis-tence and Attributes of the Deity , published in 1802, abook that had greatly impressed Darwin, while he was astudent at Cambridge University. Natural Theology is asustained argument-from-design claiming that the livingworld provides compelling evidence of being designed byan omniscient and omnipotent Creator. Paley’s keystoneclaim is that, “There cannot be design without a designer;contrivance, without a contriver; order, without choice;means suitable to an end, and executing their office inaccomplishing that end, without the end ever having beencontemplated” [Paley, 1802, pp. 15–16].

The argument-from-design to demonstrate the exis-tence of God had been put forward by theologians andother authors over the centuries. But Paley elaboratedthe argument-from-design with greater cogency and moreextensive knowledge of biological detail than has everbeen done by any other author, before or since. Paleybrings in all sorts of biological knowledge, ranging fromthe geographic distribution of species to the interactionsbetween predators and their prey, the interactions betweenthe sexes, the camel’s stomach and the woodpecker’stongue, the compound eyes of insects, and the spider’sweb. Natural theology has chapters dedicated to (a) thecomplex design of the human eye, (b) the human frame,which displays a precise mechanical arrangement ofbones, cartilage, and joints, (c) the circulation of the bloodand the disposition of blood vessels, (d) the comparativeanatomy of humans and animals, (e) the digestive system,kidneys, urethras, and bladder, (f) the wings of birds andthe fins of fish, and (g) much more. After detailing theprecise organization and exquisite functionality of eachbiological object or process, Paley draws again and againthe same conclusion, that only an omniscient and omnipo-tent deity could account for these marvels of mechanicalperfection, purpose, and functionality, as well as for theenormous diversity of inventions that they entail.

Darwin’s greatest accomplishment, and his main con-tribution to the history of ideas, was to show that thecomplex organization and functionality of living beingscan be explained as the result of a natural process, naturalselection, without any need to resort to a Creator or otherexternal agent. The origin and adaptation of organisms intheir profusion and wondrous variations were thus broughtinto the realm of science.

55.4 NATURAL SELECTIONVERSUS EVOLUTION

Important as the evidence for evolution was, Darwin con-sidered the discovery of natural selection to be his mostimportant scientific achievement, as becomes apparent

from consideration of his life and works. In his diariesand correspondence, Darwin referred to natural selectionas “my theory,” a designation he never used whenreferring to the evolution of organisms. The discoveryof natural selection, Darwin’s awareness that it was agreatly significant discovery because it was science’sanswer to Paley’s argument from design, and Darwin’sdesignation of natural selection as “my theory” can betraced in Darwin’s “Red Notebook” and “TransmutationNotebooks B to E,” which he started in March 1837,not long after returning (on 2 October 1836) from hisfive-year voyage on the Beagle, and completed in late1839 (see Eldredge [2005, pp. 71–138]).

The evolution of organisms was commonly acceptedby naturalists in the middle decades of the nineteenth cen-tury. The distribution of exotic species in South America,in the Galapagos Islands, and elsewhere, along with thediscovery of fossil remains of long-extinguished animals,confirmed the reality of evolution in Darwin’s mind. Theintellectual challenge was to explain the origin of dis-tinct species of organisms and how new ones are adaptedto their environments, that “mystery of mysteries,” as ithad been labeled by Darwin’s older contemporary, theprominent scientist and philosopher Sir John Herschel(1792–1871).

Early in the Notebooks of 1837 to 1839, Darwin reg-istered his discovery of natural selection and repeatedlyreferred to it as “my theory.” From then until his death in1882, Darwin’s life would be dedicated to substantiatingnatural selection and its companion postulates, mainly thepervasiveness of hereditary variation and the enormousfertility of organisms, which much surpassed the capacityof available resources. Natural selection became for Dar-win “a theory by which to work.” He relentlessly pursuedobservations and performed experiments in order to testthe theory and resolve presumptive objections.

As I read it, Darwin’s focus in The Origin of Specieswas the explanation of design, with evolution playing thesubsidiary role of supporting evidence. The Introductionand Chapters I through VIII of The Origin of Speciesexplain how natural selection accounts for the adaptationsand behaviors of organisms, their “design.” The extendedargument starts in Chapter I, where Darwin describes thesuccessful selection of domestic plants and animals and,with considerable detail, the success of pigeon fanciersseeking exotic “sports.” The success of plant and animalbreeders manifests how much selection can accomplishby taking advantage of spontaneous variations that occurin organisms but happen to fit the breeders’ objectives. Asport (mutation) that first appears in an individual can bemultiplied by selective breeding, so that after a few gen-erations that sport becomes fixed in a breed, or race. Thefamiliar breeds of dogs, cattle, chickens, and food plants

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have been obtained by this process of selection practicedby people with particular objectives.

The ensuing chapters (II–VIII) of The Origin ofSpecies extend the argument to variations propagatedby natural selection for the benefit of the organismsthemselves, rather than by artificial selection of traitsdesired by humans. As a consequence of natural selection,organisms exhibit design—that is, exhibit adaptive organsand functions. The design of organisms as they exist innature, however, is not “intelligent design” imposed byGod as a “Supreme Engineer” or by humans; rather, itis the result of a natural process of selection, promotingthe adaptation of organisms to their environments. Thisis how natural selection works: Individuals that havebeneficial variations—that is, variations that improvetheir probability of survival and reproduction—leavemore descendants than individuals of the same speciesthat have less beneficial variations. The beneficialvariations will consequently increase in frequency overthe generations; less beneficial or harmful variationswill be eliminated from the species. Eventually, all ormost individuals of the species will have the beneficialfeatures; new features will arise over eons of time.

From Darwin’s explanation of adaptation, it followsthat evolution must necessarily occur as a consequenceof the following: Organisms become adapted to (a)different environments in different localities and (b)the ever-changing conditions of the environment overtime; and as hereditary variations become available at aparticular time that improve, in that place and at that time,the organisms’ chances of survival and reproduction.The Origin of Species’ evidence for biological evolutionis central to Darwin’s explanation of design, becausethis explanation implies that biological evolution occurs,which Darwin therefore seeks to demonstrate in mostof the remainder of the book [Darwin, 1859, ChaptersIX–XIII]. In the 6th edition of The Origin of Species ,these are Chapters X–XIV, and the concluding chapteris XV, because Darwin added one earlier chapter aboutobjections raised against his theory.).

In the concluding chapter (XIV) of The Origin ofSpecies , Darwin returns to the dominant theme of adap-tation and design. In an eloquent final paragraph, Darwinasserts the “grandeur” of his vision:

It is interesting to contemplate an entangled bank,clothed with many plants of many kinds, with birdssinging on the bushes, with various insects flitting about,and with worms crawling through the damp earth, and toreflect that these elaborately constructed forms, sodifferent from each other, and dependent on each other inso complex a manner, have all been produced by lawsacting around us. . .. Thus, from the war of nature, fromfamine and death, the most exalted object which we arecapable of conceiving, namely, the production of the

higher animals, directly follows. There is grandeur in thisview of life, with its several powers, having beenoriginally breathed into a few forms or into one; and that,while this planet has gone cycling on according to thefixed law of gravity, from so simple a beginning-endlessforms most beautiful and most wonderful have been, andare being, evolved.

[Darwin 1859, pp. 489–490]:

55.5 EVIDENCE FOR EVOLUTION:THE FOSSIL RECORD

Darwin and other nineteenth-century biologists foundcompelling evidence for biological evolution in thecomparative study of living organisms, in their geo-graphic distribution, and in the fossil remains of extinctorganisms. Since Darwin’s time, the evidence fromthese sources has become stronger and more compre-hensive, while biological disciplines that have emergedrecently—genetics, biochemistry, ecology, animal behav-ior (ethology), neurobiology, and especially molecularbiology—have supplied powerful additional evidenceand detailed confirmation. Accordingly, evolutionistsare no longer concerned with obtaining evidence tosupport the fact of evolution, but rather are concernedwith finding out additional information of the historicalprocess in cases of particular interest. Moreover andmost importantly, evolutionists nowadays are interestedin understanding further and further how the process ofevolution occurs.

Nevertheless, important discoveries continue, evenin traditional disciplines, such as paleontology. Skepticalcontemporaries of Darwin asked about the “missinglinks,” particularly between apes and humans, but alsobetween major groups of organisms, such as betweenfish and terrestrial tetrapods or between reptiles andbirds. Evolutionists can now affirm that these missinglinks are no longer missing. The known fossil recordhas made great strides over the last century and a half.Many fossils intermediate between diverse organismshave been discovered over the years. Two examples areArchaeopteryx , an animal intermediate between reptilesand birds, and Tiktaalik , intermediate between fishes andtetrapods.

The first Archaeopteryx was discovered in Bavariain 1861, two years after the publication of Darwin’sThe Origin of Species , a discovery that was notedby Darwin in the last two editions of The Origin ofSpecies . Other Archaeopteryx specimens have beendiscovered in the past 100 years. The most recent,the tenth specimen so far recovered, was described inDecember 2005. Archaeopteryx lived during the LateJurassic period, about 60 million years ago, and exhibited

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a mixture of both avian and reptilian traits. All knownspecimens are small, about the size of a crow, andshare many anatomical characteristics with some of thesmaller bipedal dinosaurs. Its skeleton is reptile-like,but Archaeopteryx had feathers, clearly shown in thefossils, with a skull and a beak like those of a bird.Archaeopteryx is now considered an early bird. Therecently described Haplocheirus sollers , 15 million yearsolder than Archaeopteryx , is more nearly intermediatebetween dinosaurs and birds [Stone, 2010; Choiniereet al., 2010].

Paleontologists have known for more than a centurythat tetrapods (amphibians, reptiles, birds, and mammals)evolved from a particular group of fishes called lobe-finned. Until recently, Panderichthys was the known fossilfish closest to the tetrapods. Panderichthys was some-what crocodile-shaped and had a pectoral fin skeleton andshoulder girdle intermediate in shape between those oftypical lobe-finned fishes and those of tetrapods, whichallowed it to “walk” in shallow waters, but probably noton land. In most features, however, Panderichthys wasmore like a fish than like an amphibious tetrapod. Pan-derichthys is known from Latvia, where it lived some 385million years ago (the mid-Devonian period).

Until very recently, the earliest tetrapod fossils thatare more nearly fishlike were also from the Devonian,about 376 million years old. They have been found inScotland and Latvia. Ichthyostega and Acanthostega fromGreenland, which lived more recently, about 365 millionyears ago, are unambiguous walking tetrapods, with limbsthat bear digits, although they retain from their fish ances-tors such characteristics as true fish tails with fin rays.Thus, the time gap between the most tetrapodlike fish andthe most fishlike tetrapods was nearly 10 million years,between 385 and 376 million years ago.

Recently, several specimens have been discovered ofa fossil that has been named Tiktaalik , which goes a longway toward breaching this gap; it is the most nearly inter-mediate between fishes and tetrapods yet known. Severalspecimens have been found in Late Devonian river sed-iments, dated about 380 million years ago, on EllesmereIsland in Nunavut, Artic Canada. Tiktaalik displays anarray of features that are just about as precisely interme-diate between fish and tetrapods as one could imagineand exactly fits the time gap as well (see Daeschler et al.[2006] and Shubin et al. [2006]).

The missing link between apes and humans is nolonger missing. The fossils that belong to the human lin-eage after its separation from the ape lineages are calledhominids (or hominins, in most recent use). Hundreds offossil remains from hundreds of individual hominids havebeen discovered since Darwin’s time and continue to bediscovered at an accelerated rate. The oldest known fossilhominids are 6–7 million years old, come from Africa,

and are known as Sahelanthropus and Orrorin . Theseancestors were predominantly bipedal when on the groundand had very small brains. Ardipithecus lived about 4.4million years ago, also in Africa. Numerous fossil remainsfrom diverse African origins are known of Australopithe-cus , a hominid that appeared between 3 and 4 millionyears ago. Australopithecus had an upright human stancebut a cranial capacity of less than 500 cc, comparable tothat of a gorilla or chimpanzee. The skull of Australopithe-cus displayed a mixture of ape and human characteristics.Other early hominids partly contemporaneous with Aus-tralopithecus include Kenyanthropus and Paranthropus;both had comparatively small brains. Paranthropus rep-resents a side branch of the hominid lineage that becameextinct.

Along with increased cranial capacity, other humancharacteristics have been found in Homo habilis , whichlived between about 2 and 1.5 million years ago inAfrica and had a cranial capacity of more than 600 cc,and in Homo erectus , which evolved in Africa sometimebefore 1.8 million years ago and had a cranial capacityof 800–1100 cc. Shortly after its emergence in Africa,H. erectus spread to Europe and Asia, even as far asthe Indonesian archipelago and northern China. Homoerectus fossils from Java have been dated at 1.81 and1.66 million years ago, with those from Georgia datedbetween 1.6 and 1.8 million years ago.

The transition from H. erectus to H. sapiens may havestarted around 400,000 years ago. Some fossils of thattime appear to be “archaic” forms of H. sapiens . Thespecies Homo neanderthalensis appeared in Europe morethan 200,000 years ago and persisted until 30,000 yearsago. The Neandertals have been thought to be ancestral toanatomically modern humans, but comparisons of DNAfrom Neandertal fossils with living humans indicate thatH. neanderthalensis may have been a separate species thatbecame extinct.

55.6 MOLECULAR EVOLUTION

Molecular biology, a discipline that emerged in the sec-ond half of the twentieth century, nearly 100 years afterthe publication of The Origin of Species , has providedthe strongest evidence yet of the evolution of organisms.Molecular biology proves the fact of evolution in twoways: first, by showing the unity of life in the natureof DNA and the workings of organisms at the level ofenzymes and other protein molecules; second, and mostimportant in practice for evolutionists, by making it possi-ble to (a) reconstruct evolutionary relationships that werepreviously unknown and (b) confirm, refine, and timeall evolutionary relationships from the universal commonancestor up to all living organisms. The precision with

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which these events can be reconstructed is one reasonwhy the evidence from molecular biology is so useful toevolutionists and so compelling.

The molecular components of organisms are remark-ably uniform—in the kinds of molecules that are present,as well as in the ways in which these molecules are assem-bled and used. In all microorganisms, plants, animals, andhumans, the instructions that guide the development andfunctioning of organisms are encased in the same hered-itary material, DNA, which provides the instructions forthe synthesis of proteins. The thousands of enormouslydiverse proteins that exist in organisms are synthesizedfrom different linear combinations, in sequences of vari-able length, of 20 amino acids, the same 20 in all proteinsand in all organisms. Yet several hundred other aminoacids exist, such as are found in a variety of plants, anda virtually infinite number of them could be synthesized.Moreover, the genetic code, by which the informationcontained in the DNA of the cell nucleus is passedon to proteins, is virtually the same in all organisms.Similar metabolic pathways—sequences of biochemicalreactions—are used by the most diverse organisms toproduce energy and to make up the cell components.

The unity of life reveals the genetic continuity andcommon ancestry of all organisms. There is no other ratio-nal way to account for their molecular uniformity, giventhat numerous alternative structures and fundamental pro-cesses are in principle equally likely.

DNA and proteins have been called “informationalmacromolecules” because they are long linear moleculesmade up of sequences of smaller units—nucleotides in thecase of DNA, amino acids in the case of proteins—thatembody evolutionary information in their particularsequence, similarly as particular sequences of lettersand words convey semantic information. Comparingthe sequence of the components in two macromoleculesestablishes how many units are different. Becauseevolution usually occurs by changing one unit at a time,the sequence differences between two organisms are anindication of their recency of common ancestry. Thus,the inferences from paleontology, comparative anatomy,and other disciplines that study evolutionary history canbe tested in molecular studies of DNA and proteins byexamining the sequences of nucleotides and amino acids.The authority of this kind of test is overwhelming: Eachof the thousands of genes and thousands of proteinscontained in an organism provides an independent test ofthat organism’s evolutionary history.

Molecular evolutionary studies have three notableadvantages over comparative anatomy and the other clas-sical disciplines: precision, universality, and multiplicity.First, precision because molecular information is readilyquantifiable. The number of units that are different iseasily established when the sequence of units is known

for a given macromolecule in different organisms. It issimply a matter of aligning the units (nucleotides oramino acids) between two or more species and countingthe differences. The second advantage is universality :Comparisons can be made between very different sorts oforganisms. There is very little that comparative anatomycan say when, for example, organisms as diverse asyeasts, pine trees, and human beings are compared, butthere are numerous DNA and protein sequences thatcan be compared in all three. The third advantage ismultiplicity . Each organism possesses thousands of genesand proteins, every one of which reflects the same evolu-tionary history. If the investigation of one particular geneor protein does not satisfactorily resolve the evolutionaryrelationship of a set of species, additional genes andproteins can be investigated until the matter has beensettled.

The resourcefulness of molecular biology to studyevolution can be noted in other ways as well. The widelydifferent rates of evolution of different sets of genes opensup the opportunity for investigating different genes inorder to achieve different degrees of resolution in thetree of evolution. Evolutionists rely on slowly evolvinggenes for reconstructing remote evolutionary events, butincreasingly faster evolving genes for reconstructing theevolutionary history of more recently diverged organisms.

Genes that encode ribosomal RNA molecules areamong the slowest-evolving genes. They have beenused to reconstruct the evolutionary relationships amonggroups of organisms that diverged very long ago: forexample, among bacteria, archaea, and eukaryotes(the three major divisions of the living world), whichdiverged more than 2 billion years ago, or among theprotozoa compared with plants and with animals, groupsof organisms that diverged about 1 billion years ago.Cytochrome c evolves slowly, but not as slowly as theribosomal RNA genes. Thus, it is used to decipher therelationships within large groups of organisms, suchas among humans, fishes, and insects. Fast-evolvingmolecules, such as the fibrinopeptides involved in bloodclotting, are appropriate for investigating the evolutionof closely related animals—the primates, for example,macaques, chimps, and humans.

It is now possible to make an assertion that wouldhave delighted Darwin and would surely shock creation-ists and other antievolutionists, and perhaps startle manyscientists and most of the general public: Gaps of knowl-edge in the evolutionary history of living organisms nolonger need to exist. Molecular biology has made it possi-ble to reconstruct the “universal tree of life,” the continuityof succession from the original forms of life, ancestral toall living organisms, to every species now living on Earth.The main branches of the tree of life have been recon-structed on the whole and in great detail. More details

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about more and more branches of the universal tree oflife are published in scores of scientific articles everymonth. The virtually unlimited evolutionary informationencoded in the DNA sequence of living organisms allowsevolutionists to reconstruct all evolutionary relationshipsleading to present-day organisms, with as much detail aswanted. Invest the necessary resources (time and labora-tory expenses) and you can have the answer to any query,with as much precision as you want.

Molecular investigations of evolutionary processesand evolutionary history recently have enormouslyexpanded precisely because of the mechanistic as well asphylogenetic insights that they provide. There are nowjournals dedicated to molecular evolutionary studies,such as the Journal of Molecular Evolution, MolecularBiology and Evolution , and Molecular Phylogenetics andEvolution . Thousands of articles are published every yearin these and numerous other less specialized journals. Ihave just received the most recent issue of MolecularPhylogenetics and Evolution , Vol. 54, issue 2, February2010. It includes 35 research articles, accounting for 355pages. The January 2010 issue of Infection, Genetics andEvolution (Vol. 10, issue 1) contains 15 articles (158pages), all of which but one are molecular evolutioninvestigations.

55.7 SPECIES CONCEPTS

It is apparent that there are distinguishable kinds inthe world of life. We easily distinguish plants fromanimals and, among the animals, there are worms,insects, mollusks, fishes, lizards, birds, and mammals.We can, also easily, achieve greater resolution withinany of these kinds: we distinguish among the mammalscats, dogs, elephants, monkeys, and many more. Sincetime immemorial and in different cultures, people haveachieved the lowest level of resolution of kinds oforganisms, called species. An important landmark forbiologists was C. Linnaeus’ Systema Naturae [10thedition, 1758]: species are identified by two names, genusand species, and are considered distinctive entities atthe lowest level of taxonomic differentiation. There is adiversity of individuals within a species, and there mayalso be distinctive varieties or races within a species, butthese do not have well-defined boundaries and are notstable over time.

Linnaeus’ concept of species is “phenotypic,” by-and-large characterized by the appearance or phenotype. Twoother species concepts are the “biological” or reproduc-tive species concepts and the “phylogenetic” or lineage-based species concept. Distinctions can be made withineach one of these three concepts and additional consider-ations brought to bear [Mayr, 1963; Coyne and Orr, 2004].

Mayden [1997] has catalogued 22 species concepts cur-rently in use to a greater or lesser extent.

The biological species concept (BSC) was first artic-ulated by Theodosius Dobzhansky, who proposed that “aspecies is a group of individuals fully fertile inter se, butbarred from interbreeding with other similar groups by itsphysiological properties (producing either incompatibilityof parents, or sterility of hybrids, or both)” [Dobzhan-sky, 1935]. This species concept is also known as the“reproductive isolation species concept.” Dobzhanskywent on to characterize the isolating “mechanisms” orbarriers that impede the exchange of genes betweendifferent species, including sexual isolation, ecologicalisolation, hybrid sterility, and others [Dobzhansky, 1937,1951]. The biological species concept was expanded atlarge by Ernst Mayr [1963] and elsewhere), whose namehas, indeed, become antonomastically associated withit. The BSC accounts for the morphological distinctnessof species in nature. They remain differentiated becauseindividuals from different species cannot exchange genes;that is, they cannot interbreed.

It soon became apparent that there are “sibling”species, reproductively isolated species that are notmorphologically distinguishable. Sibling species becameknown in breeding experiments, showing the inabilityto interbreed between sets of individuals with seeminglyidentical (or, at least, indistinguishable) phenotypes. Sib-ling species were first identified among Drosophila fliesand a few other kinds of organisms that could be manip-ulated experimentally in the laboratory, the greenhouse,or the field. The existence of sibling species in all sortsof organisms became increasingly apparent by meansof molecular biology. F. J. Ayala and J. R. Powell firstpointed out that simple allozyme methods could serve as“diagnostic characters of sibling species in Drosophila”[Ayala and Powell, 1972]. Allozyme and other molecularmethods were soon extended to all sorts of animals andplants, and even microorganisms (e.g., Tibayrenc et al.[1990] and Tibayrenc and Ayala [1991, 2002]).

The phylogenetic species concept identifies speciesin terms of their evolutionary history, which seeks touncover evolutionary relatedness among individuals andpopulations. This lineage-based species concept acquiredconsiderable currency first when techniques became avail-able to obtain the amino acid sequence of proteins and,later, with the development of DNA sequencing methods.DNA sequencing methods by now have become simplerand much less expensive to use. There is, moreover, morephylogenetic information in the DNA than in the encodedamino acids. In addition, much of eukaryotic DNA doesnot encode amino acids, but has phylogenetic information.Care must be taken, however, to distinguish organismicphylogeny from DNA that comes about by duplication andother processes such as horizontal DNA transfer between

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species, as well as plasmid and viral DNA incorporation,and the multitude of alu sequences, LINEs (long inter-spersed elements), SINEs (short interspersed elements),LTRs (long terminal repeat elements), and other DNAcomponents that are incorporated in the genome withoutstrict association with phylogenetic history.

Species should ideally be identified using all three cri-teria: phenotypic, reproductive, and phylogenetic. But inpractice this is not often feasible. As a matter of fact, thereconstruction of phylogeny by means of DNA sequenceshas become a cottage industry pervading not only jour-nals primarily dedicated to molecular evolution, but manyothers as well. Molecular phylogeny research has surelycontributed to describe numerous cases of cryptic (sib-ling) species, as well as species complexes and groups oforganisms that are morphologically indistinguishable, yetexhibit considerable genetic differentiation and are repro-ductively isolated as well (e.g., Tibayrenc [2006], Prug-nolle et al. [2010], and Perkins [2010]). The phylogeneticspecies concept overwhelmingly prevails in the case ofprokaryotes, where reproductive isolation is not relevant(because their reproduction is clonal, rather than sexual)and morphological criteria are of limited use as well.

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