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In the Light of Evolution III: Two Centuries of Darwin

In the Light of Evolution III: Two Centuries of Darwin

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In the light of III: Two centuries of Darwin

John C. Avise1 and Francisco J. Ayala1 Department of and , University of California, Irvine, CA 92697

harles Darwin’s enthusiasm autobiography (13) that Paley’s logic able to itself, under the complex and and expertise in natural history ‘‘gave me as much delight as did Euclid’’ sometimes varying conditions of life, contributed hugely to his eluci- and that it was the ‘‘part of the Aca- will have a better chance of surviving, dation of evolution by natural demical Course [at the University of and thus be naturally selected. From the selection,C which stands as one of the Cambridge] which...wasthemost use strong principle of inheritance, any se- grandest intellectual achievements in the to me in the education of my mind.’’ lected variety will tend to propagate its history of science. Darwin was a lifelong Darwin was still a natural theologian new and modified form.’’ Darwin’s clear observer of nature, stating in correspon- when he boarded the Beagle in 1831 on elucidation of launched dence that some of his happiest times in what would become a fateful voyage, for a revolutionary new paradigm in biology youth were spent fishing on rainy days Darwin and for humanity, into un- wherein organismal traits could be stud- and ‘‘entomologizing’’ when England’s charted philosophical (as well as scien- ied and interpreted as products of natu- weather was nice. At the age of 22, he tific) waters. ral (rather than supernatural) forces boarded the HSM Beagle for a 5-year In the articles of this Colloquium, amenable to rational scientific inquiry. stint as Captain Fitzroy’s traveling com- leading evolutionary biologists and sci- Scientific studies of natural selection are panion and the ship’s naturalist, an ence historians reflect on and commem- now more popular and powerful than appointment that introduced him to bio- orate the Darwinian Revolution. The ever, and they have revealed the evolu- diversity on a global geographic scale. authors of these Proceedings canvass tionary origins and trajectories of nu- Darwin’s breadth and depth of natural- modern research approaches and cur- merous biological features and taxa. history experience would later be on full rent scientific thought on each of the A major limitation in Darwin’s char- display in his most defining scientific 3 main categories of selection (natural, acterization of evolution concerned he- works (3–5) in his detailed treatises on artificial, and sexual) that Darwin ad- reditary mechanisms, a difficulty that orchids, insectivorous plants, coral reefs, dressed during his career. Although his the field began to rectify early in the barnacles, and earthworms (6–10). legacy is associated primarily with the 20th century by incorporating Mende- The year 2009 marks the 200th anni- illumination of natural selection in The lian genetics and versary of ’s birth and Origin, Darwin also contemplated and into the emerging evolutionary synthesis the 150th anniversary of his most influ- wrote extensively about what we would (14). Today, in the genomics era, scien- ential publication (3). Darwin trans- now term artificial selection and sexual tists routinely extend studies of natural formed the biological sciences in much selection, as reflected for example in selection and trait evolution to the level the same way that Nicolaus Copernicus, two books titled, respectively, The Varia- of DNA itself, as several papers in these Galileo Galilei, and Isaac Newton, cen- tion of Animals and Plants Under Domes- Proceedings will attest. Genomic dissec- turies earlier, transformed the physical tication (1869) and The Descent of Man tions are also providing fresh insights sciences—by demonstrating that the uni- and Selection in Relation to Sex (1871). into the ancient mystery alluded to in verse operates according to natural laws In a concluding section of these Pro- the title of Darwin’s seminal work: how that fall within the purview of rational originate. Ironically, The Origin scientific inquiry. In 1543, Copernicus ceedings, several science historians com- published De revolutionibus orbium ment on Darwin’s seminal contributions. says relatively little about the evolution celestium (‘‘On the Revolutions of the Thus, these Proceedings are organized of reproductive isolating barriers, which Celestial Spheres’’) that challenged con- in 4 parts: Natural Selection, or Adapta- under the modern biological species ventional wisdom that the Earth was the tion to Nature; Artificial Selection, or concept are key to understanding clado- center of Creation, and instead pro- to Demands; Sexual genetic (speciational) processes. moted the idea that natural laws govern Selection, or Adaptation to Mating De- In the opening presentation of these the motion of physical objects in the mands; and The Darwinian Legacy, 150 Proceedings, Via (15) takes a fresh per- universe. In 1859, in On the Origin of Years Later. spective by char- Species, Darwin developed the equally acterizing genomic regions that appear Natural Selection, or Adaptation to revolutionary concept that a natural but to be diverging early in a pro- Nature nonrandom process—natural selection— yields biological that other- The concept of natural selection—as the unconscious broker of adaptive evolu- This paper serves as an introduction to this PNAS supple- wise can give the superficial impression ment, which resulted from the Arthur M. Sackler Collo- of direct intelligent craftsmanship. tion—is Darwin’s seminal contribution. quium of the National Academy of Sciences, ‘‘In the Light of Darwin’s impacts have been felt far It provided a materialistic account of Evolution III: Two Centuries of Darwin,’’ held January 16– beyond science. Before Darwin, most nature’s operations that contrasted 17, 2009, at the Arnold and Mabel Beckman Center of the sharply with the traditional invocations National Academies of Sciences and Engineering in Irvine, scientists and theologians accepted what CA. It is the third in a series of colloquia under the general seemed obvious: that divine intervention of supernatural causation that predomi- title ‘‘In the Light of Evolution’’ (ILE; and see Box 1). The must have underlain nature’s design. nated before The Origin. The basic logic complete program and audio files of most presentations of natural selection is astonishingly sim- are available on the NAS web site at www.nasonline.org/ The traditional ‘‘argument from design’’ ࿝ ple. As phrased by Darwin in The Ori- Sackler Darwin. Papers from the first two colloquia in the traces back at least to the classical ILE series, titled ‘‘Adaptation and Complex Design’’ and Greek philosopher Socrates in the 5th gin, ‘‘As many more individuals of each ‘‘ and ,’’ appeared in refs. 1 and 2, century B.C. (see ref. 11), and it was species are born than can possibly sur- respectively. expressed again in a thoughtful and ele- vive; and as, consequently, there is a Author contributions: J.C.A. and F.J.A. wrote the paper. gant treatise (Natural Theology) pub- frequently recurring struggle for exis- The authors declare no conflict of interest. lished in 1802 by the Reverend William tence, it follows that any being, if it vary 1To whom correspondence may be addressed. E-mail: Paley (12). Darwin later recalls in his however slightly in any manner profit- [email protected] or [email protected].

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0903381106 PNAS ͉ June 16, 2009 ͉ vol. 106 ͉ suppl. 1 ͉ 9933–9938 Downloaded by guest on October 5, 2021 cess. She calls this the ‘‘magnifying and prezygotic isolation under gene and species in nature. In chapter 1 of glass’’ approach for speciation in action, flow, and the role of standing genetic The Origin, Darwin discussed several and contrasts it with the more tradi- variation in the process) and specifically domesticated plant and animal species, tional ‘‘spyglass’’ approach in which each (with reference to speciation in stickle- ranging from beans, melons, and plums completed speciation is characterized back fishes). For the sticklebacks, they to dogs, cattle, and horses. He devoted a retrospectively by scrutinizing genetic develop an interesting ‘‘transporter long section to how differences between established sister model’’ of in which had altered the domestic pigeon, fancy taxa. Via develops and presents genetic ecological selection pressures in fresh- varieties of which were widely prized in evidence for a model in which incipient water streams consistently select for al- the Victorian era. Ten years later, he species become, in effect, genealogical leles different from those normally would expand greatly on these themes in mosaics in which ecologically important present in marine populations. However, The Variation of Animals and Plants Un- genomic regions (i.e., those under diver- occasional hybridization between fresh- der Domestication. gent ecological selection, sometimes water and marine forms ensures a con- In chapter 1 of The Origin, Darwin even in sympatry) become resistant to tinual supply of freshwater alleles in the lamented that ‘‘We hardly know any- genetic exchange, whereas sea, at low frequency and disassembled thing about the origin or history of our remains possible over most of the ge- by genetic recombination. When marine domestic breeds’’; and ‘‘The origin of nome. The key genomic regions under fish colonize a newly opened stream, most of our domestic animals will prob- divergent selection become focal points natural selection can act on this stand- ably for ever remain vague.’’ Darwin for ‘‘divergence hitchhiking’’ by linked ing pool of to reconsti- would therefore be both pleased and loci, because they reduce the porosity of tute the freshwater genotype. The anal- surprised by recent scientific progress in the emerging species boundary to gene ogy in the title of their model is to a deciphering the evolutionary origins of exchange. Under this scenario, Via fictional process in the movie Star Trek, many domesticated plant and animal views divergent selection as the motiva- wherein an organic body placed in the species. Much of this evidence has tor of genealogical differences (in these transporter is disintegrated only to be re- come from molecular genetic and phylo- particular genomic regions) that later assembled at a future time in a distant genetic analyses of domesticated breeds will crystallize into the branching pat- location. vis-a`-vis their wild ancestors. Driscoll, tern in the species phylogeny. Eventu- The vast majority of phylogenetic di- Macdonald, and O’Brien (19) tabulate ally, in responses to selection, genetic versity in is to be found not some of this evidence for various do- drift, and , gene genealogies in in the lineages of multicellular plants mestic animals, and then provide a de- the remainder of the genome will come and animals, but rather in unicellular tailed case-in-point by describing the into topological concordance with the microbes (protists). Perhaps it is not phylogenetic and biological history of species phylogeny, but these additional surprising, therefore, that these microeu- the domestic cat. The cat appears to be genetic differences will have been the karyotes provide a wealth of opportuni- nearly unique among animal domesti- effect of speciation rather than its cause. ties (heretofore relatively untapped) for cates (including dogs) in the sense that Some of the richest biological quarries scientific investigations into natural se- it was initially self-selected for tolerance for extracting information about natural lection and evolutionary operations. to , rather than actively selected selection and speciation involve clades Lukesˇ, Leander, and Keeling exemplify by humans for tameness or for desired (monophyletic groups) that have arisen the utility of protists for providing evo- services such as companionship, hunting via rapid adaptive radiations. Darwin lutionary insights by summarizing nu- or guard duties, or food. According to presaged such evolutionary analyses in merous phenotypic and genomic the authors’ reconstruction, cat domesti- his considerations of different forms of features in representatives of two huge cation probably began near some of the mockingbirds in the Galapagos Islands, protistan phylads: Alveolata and earliest agricultural settlements of the and in the various finch species he col- Euglenozoa. They underscore the mind- Neolithic, in the Fertile Crescent region lected there that now bear Darwin’s boggling diversity in protists of molecu- of the Near East, as wildcats became name (but whose evolutionary appraisal lar genetic and phenotypic features, accustomed to feeding on rodents and mostly awaited later researchers). ranging from cellular ultrastructures to refuse near human towns. If so, their Hodges and Derieg (16) take a modern mechanisms of mRNA processing and evolution to companion animals, and approach to speciation analysis by inte- the organization of organellar genomes. their ecological isolation from wildcats, grating observations from field studies The picture that emerges is one of were initially a response to natural with molecular and phylogenetic dissec- extraordinary evolutionary experimenta- selection more so than to conscious arti- tions of genes for traits (especially tion in these protists, sometimes chan- ficial selection. flower color) that probably played key neled into convergent outcomes by Apart from appraising the phyloge- cladogenetic roles in a spectacular evo- natural selection, sometimes constrained netic histories of domestic organisms, lutionary radiation of Aquilegia (colum- by the idiosyncrasies of phylogeny, but the field of molecular genetics is also bine) plants. The authors describe how always tinkered endlessly by various uncovering the genes responsible for key molecular investigations of genomes can mixes of both chance and necessity. phenotypes that have emerged from complement traditional approaches and artificial selection. Tian, Stevens, and contribute to a better mechanistic un- Artificial Selection, or Adaptation to Buckler (20) provide cases-in-point in- derstanding of how new species arise. Human Demands volving domestic corn (maize), the Schluter and Conte (17) emphasize a Darwin titled the first chapter in The ancestors of which are wild teosinte theme—ecological speciation—that Origin of Species‘‘variation under domes- grasses native to Mexico. The evolution- would please Darwin. Under ecological tication,’’ probably because he felt that ary transformation from teosinte to speciation, reproductive isolation be- developing a case for the effectiveness maize ranks among the most impressive tween populations emerges from the of human-mediated selection in generat- of all feats of artificial selection. For effects of ecology-based divergent natu- ing new domestic varieties would facili- example, teosinte lacks a cob-like inflo- ral selection. The authors address this tate his efforts in later chapters to rescence and instead produces only 6–12 speciation mode generally (with respect communicate the concept of how natu- kernels in 2 rows protected by a hard to the genetics of postzygotic isolation ral selection can generate new varieties covering, whereas each cob of modern

9934 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0903381106 Avise and Ayala Downloaded by guest on October 5, 2021 maize consists of Ϸ20 rows with numer- new proteins for medicine and pharma- into various aspects of ous exposed kernels; and teosinte has cology. Directed protein evolution has both in theory and empirically. The au- long lateral branches terminated by also yielded new insights into the funda- thors close by suggesting several lines of male tassels, whereas modern maize has mental nature of evolutionary processes. future research on sexual selection. short lateral branches tipped by female The authors emphasize 3 major conclu- Shuster (24) provides a comprehen- ears. The authors review current knowl- sions from directed evolution experiments: sive overview (and contrast) of how sex- edge about the genetic loci responsible (i) most desirable protein properties can ual selection has been measured and for these and other such morphological be incrementally improved through suc- studied in plant systems versus animal transitions. Several genes with major cessions of single mutation steps; (ii) systems. One general theme that he em- effect can be specified, and many others much of the epistatic coupling between phasizes is the need to reconcile Dar- are implicated, including a newly discov- is due to protein stability and win’s idea that sexual selection tends to ered region on 10 that its influence on mutational robustness be less rigorous than natural selection spans Ͼ1,000,000 base pairs and retains and protein evolvability; and (iii) adap- with the observation that sexual selec- the molecular footprints of strong artifi- tive protein evolution is heavily reliant tion would seem to be responsible for cial selection during the domestication on the prevalence of promiscuous pro- many if not most differences between process. tein functions (initial traces of activity the two genders (in features other than Allendorf and Hard (21) describe an- that proteins routinely display on for- the primary sex organs). In The Origin, other form of human-induced selection eign substrates) that in turn are rou- Darwin wrote that sexual selection ‘‘de- that they term unnatural selection. tinely influenced by neutral mutations. pends, not on the struggle for existence, When breeders artificially select domes- Directed protein evolution goes far be- but on a struggle between males for tic animals for food or companionship, yond the wildest imaginings of Darwin, possession of the females; the result is they purposefully try to propagate traits who would doubtless be impressed that not of the unsuccessful competi- that people deem desirable. However, the general principles of selection he tor, but few or no offspring. Sexual se- hunting and fishing (especially for tro- illuminated would prove to be so lection is, therefore, less rigorous than phies) routinely violate such ground universal. natural selection.’’ Shuster, by contrast, rules by culling rather than propagating views sexual selection as being ‘‘among the animals that humans prize most. In Sexual Selection, or Adaptation to the most powerful of evolutionary other words, unnatural selection via Mating Demands forces.’’ The author proposes to recon- hunting, unlike artificial selection by In The Descent of Man, and Selection in cile these two stances in evolutionary people (or natural selection by nature), Relation to Sex, Darwin defined sexual models that combine quantitative differ- often eventuates biotic outcomes that selection as the ‘‘advantage which cer- ences in the fitness variances between run counter to what humans (or nature) tain individuals have over other individ- the sexes (an approach traditionally otherwise would strive to achieve. For uals of the same sex and species, in applied to animal systems) with pheno- example, the evolutionary responses to exclusive relation to reproduction.’’ typic and genotypic correlations underly- the continued selective removal of Darwin appreciated that sexual selection ing reproductive traits among breeding larger or healthier animals from a popu- could be mediated by intrasexual com- pairs (an approach often taken in plant lation of deer or fish could include, in bat (e.g., between males) or by intersex- systems). The net result, he claims, will principle, earlier sexual maturation and ual preferences (e.g., female choice of be the ability to predict the magnitudes smaller adult body sizes. The authors attractive mates). He also appreciated of and classify mat- review arguments and empirical evi- that sexual selection could be in opposi- ing systems using existing genetic and dence for unnatural selection imposed tion to natural selection with respect to life history data. by human harvests of wild animal popu- particular phenotypic traits (such as a Gowaty and Hubbell (25) offer a lations, and they discuss the manage- peacock’s tail), but he generally viewed unique perspective on what underlies ment problems generated by such sexual selection as less effective than the individual decision-making process selective mortality. Darwin mostly over- natural selection. that in turn underlies patterns of mate looked this important topic, which con- After discussing Darwin’s original choice and sexual selection in various tinues to be neglected by many wildlife ideas about sexual selection (especially species. Their central thesis is that even and fisheries agencies today. This article as presented in The Descent of Man), stochastic variation in various parame- may help to rectify that situation by Jones and Ratterman (23) identify 3 ters that predict the time available for bringing to broader attention the impor- modern triumphs in sexual selection re- mating might promote considerable flex- tant contrasts between standard hunting search: the introduction and widespread ibility in individual decision-making with and fishing practices (unnatural selec- use of molecular markers to assess ge- regard to mate choice; and that even tion) on the one hand and standard ag- netic parentage (the key to describing consistent sex differences in these mat- ricultural and aquacultural practices actual mating systems in nature) un- ing proclivities might therefore, in at (artificial selection) on the other. equivocally; a better conceptual under- least some cases, reflect ecological con- Artificial selection traditionally refers standing (at least in formal models) of straints (habits-of-life considerations) to human-mediated differential propaga- the mechanisms and consequences of rather than behavioral differences that tion of plants or animals with desirable mate choice by females (or by males in might otherwise be genetically hard- hereditary traits. In the modern biotech- role-reversed taxa); and a better appre- wired between the sexes. The parame- nology era, an entirely different form of ciation of why differences exist among ters that might impact available time genetic engineering is possible in which lineages in the intensity of various forms for mating include the probabilities of particular proteins are subjected to of sexual selection. For the latter two encountering mates, individual survivor- repeated rounds of mutation and selec- topics, the histories of ideas on sexual ships, mating latencies (times-out tion, in laboratory test tubes, for im- selection—beginning with Darwin—are between mating events), and fitness dis- proved stability or biochemical function. interwoven with how those notions laid tributions, all of which are likely to vary Bloom and Arnold (22) review this form the foundation for categorizing various as functions of the natural histories and of directed evolution, which is becoming forms of sexual selection, and for ex- the evolutionary histories of species. a powerful approach to the design of tending and expanding modern research Such considerations lead the authors to

Avise and Ayala PNAS ͉ June 16, 2009 ͉ vol. 106 ͉ suppl. 1 ͉ 9935 Downloaded by guest on October 5, 2021 their switch point theorem, which in The actual methods of Darwin, Ayala no longer accept the old picture of hu- principle can quantitatively evaluate contends, were far different from this mans as somehow the miraculous prod- what proportion of potential mates in a depiction, falling instead squarely within ucts of special creation. In other words, population a focal individual should find a hypothetico-deductive framework. The the revolution challenged us to rethink acceptable as mating partners if it is to latter scientific method has 2 steps: the dramatically—both emotionally and maximize its relative lifetime fitness. formulation of one or more conjectures intellectually—what it means to be hu- In an uncharacteristic conceptual or hypotheses about the natural world man. The second resounding yes comes lapse, Darwin failed to appreciate that and the design and implementation of from the evidence that it was Darwin, sexual selection (including both male- critical empirical tests of whether deduc- rather that his predecessors or contem- male competition and female choice) tions derived from each hypothesis are poraries, who was primarily responsible can continue even after copulation has consistent with real-world observations. for the scientific and the metaphysical begun. The intrasexual (male-male) In support of his contention that shifts that society entailed in coming to component can happen via sperm com- Darwin consistently used the hypo- terms with natural selection’s role in the petition for the fertilization of ova, and thetico-deductive method, Ayala cites evolutionary process. The qualified yes the intersexual component can occur via examples from Darwin’s work and even comes from the realization that the cryptic female choice of alternative uses some of Darwin’s own words, such third question is somewhat philosophi- sperm, all within the female’s reproduc- as ‘‘How odd it is that anyone should cal; the answer depends in part on tive tract. Eberhard (26) reviews the not see that all observation must be for whether to interpret major transforma- history of ideas for these underappreci- or against some view if it is to be of any tions of thought as continuous and grad- ated but nevertheless intense forms of service.’’ Ayala speculates on why Dar- ual, or discontinuous and abrupt. Ruse postcopulatory sexual selection. The win sometimes pretended to be a Baco- discusses philosophical nuances of his miniature worlds of gametic competition nian inductivist when in fact he mostly own position on these issues. and gametic choice have proven to be practiced what today would be consid- Natural selection is the key Darwinian every bit as fascinating and compelling ered modern hypothesis-driven deduc- concept, and the evolutionary force as the macroscopic worlds of mating tive science. given top billing in The Origin. However, competition and mate choice that have In considering Darwin’s legacy from common ancestry is a key concept too, a been the traditional foci of sexual selec- the current vantage, Ruse (30) asks 3 costar (albeit not originating strictly tion studies. Eberhard brings this minia- related questions: Was there a Darwin- with Darwin) of the evolutionary the- ture Kama Sutra realm to light by ian revolution? Was there a Darwinian atre. Sober (31) considers how natural detailing fascinating examples of sexual revolution? And was there a Darwinian selection and common ancestry are re- selection in the time interval (which is revolution? Ruse’s answers to these lated under Darwin’s worldview, and he often but not invariably brief) between questions are two resounding yesses and argues that the latter has a sort of logi- the onset of copulation and the comple- a qualified yes, respectively. The first cal (as well as historical) priority over tion of fertilization. resounding yes comes from the fact that the former. This is because, under after Darwin, rational observers could Darwinian logic, arguments about natu- The Darwinian Legacy, 150 Years Later Beyond his numerous books and autobi- ography (27), Darwin left a wealth of personal correspondence (28) and addi- Box 1. In the Light of Evolution. In 1973, A grasp of evolutionary principles and tional written material that science his- Theodosius Dobzhansky penned a processes is important in other societal torians can now sift through to better short commentary titled ‘‘Nothing in arenas as well, such as education, med- understand Darwin’s developing ideas at biology makes sense except in the light icine, sociology, and other applied different stages of his life. Prominent of evolution’’ (35). Most scientists fields including agriculture, pharmacol- among these were notebooks that agree that evolution provides the uni- ogy, and biotechnology. The ramifica- Darwin wrote during the voyage of the fying framework for interpreting bio- tions of evolutionary thought extend into Beagle, and a lettered series of Transmu- logical phenomena that otherwise can learned realms traditionally reserved for tation Notebooks that he wrote in the often seem unrelated and perhaps un- philosophy and religion. The central goal 2 years after his return. Several authors intelligible. Given the central position of the In the Light of Evolution series will in this concluding part of the In the of evolutionary thought in biology, it is be to promote the evolutionary sciences Light of Evolution III Proceedings scru- sadly ironic that evolutionary perspec- through state-of-the-art colloquia and tinize these writings to illuminate tives outside the sciences have often their published proceedings. Each in- Darwin’s thought processes and thereby been neglected, misunderstood, or pur- stallment will explore evolutionary per- better appreciate and contextualize his posefully misrepresented. Biodiver- spectives on a particular biological topic scientific legacy. sity—the genetic variety of life—is an that is scientifically intriguing but also Ayala (29) describes a fundamental exuberant product of the evolutionary has special relevance to contemporary discrepancy between Darwin’s scientific past, a vast human-supportive resource societal issues or challenges. Individually methodology and how Darwin portrayed (aesthetic, intellectual, and material) and collectively, the In the Light of Evo- his methods to the general public. The of the present, and a rich legacy to lution series will aim to interpret phe- version for public consumption empha- cherish and preserve for the future. nomena in various areas of biology sized how Darwin proceeded on the Two challenges, and opportunities, for through the lens of evolution, address principles of Baconian induction, which 21st-century science are to gain deeper some of the most intellectually engaging at that time were favored by British phi- insights into the evolutionary processes and pragmatically important societal is- losophers such as John Stuart Mill. Un- that foster biotic diversity and to trans- sues of our times, and foster a greater der this approach, facts are collected late that understanding into workable appreciation of evolutionary biology as wholesale—presumably without the bias solutions for the regional and global a consolidating foundation for the life of preconceived notions—and broader crises that biodiversity currently faces. sciences. biological principles eventually emerge.

9936 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0903381106 Avise and Ayala Downloaded by guest on October 5, 2021 ral selection often require the supposi- pose and biological progress. It will be than a vast, complex and evolving sub- tion or backdrop of common ancestry interesting to monitor the responses of ject to which many other great figures (i.e., genealogy and heredity), whereas other evolutionary historians to this pro- have contributed. . . . Obsessively focus- the logical defense of common ancestry vocative suggestion. ing on Darwin, perpetually asking does not require natural selection. In The title of Dennett’s essay (33)— whether he was right about this or that, this epistemological sense, Darwin or- ‘‘Darwin’s strange inversion of reason- implies that the discovery of something dered things backwards, Sober argues, ing’’—refers to a quote from one of he did not think of or know about when he presented natural selection, Darwin’s critics who in 1868 wrote that somehow undermines or threatens the rather than common ancestry, first and Darwin, ‘‘by a strange inversion of rea- whole enterprise of evolutionary biology foremost in The Origin. Rather than soning, seems to think Absolute Igno- today.’’ The term also ‘‘sug- ‘‘evolution by natural selection,’’ rance [natural selection; editors’ gests that Darwin was the beginning and Darwin’s theory might better be de- addition] fully qualified to take the the end, the alpha and the omega, of scribed as ‘‘common ancestry plus natu- place of Absolute Wisdom [God] in all evolutionary biology, and that the sub- ral selection.’’ of the achievements of creative skill.’’ ject has not changed much in the 150 Richards (32) presents a revisionary Dennett likens Darwin’s strange inver- years since the publication of the Ori- argument that seems likely to be highly sion of reasoning to another such pro- gin.’’ Judson went on to suggest that controversial. Using excerpts from Dar- found inversion of reasoning, this time constantly, using terms such as Darwin- win’s writings, Richards makes a case by Alan Turing in the physical sciences. ism and Darwinian is rather like calling that ‘‘Darwin’s theory originally rein- In the 1930s, Turing argued that it all of modern aeronautical engineering fused nature with moral purpose and would be possible to design exquisite ‘‘Wrightism’’ after the Wright brothers, used teleological means of doing so,’’ calculating machines [such as modern or referring to all fixed-wing aircraft as and that ‘‘Darwinian evolution had the computers] that were absolutely igno- ‘‘Wrightian’’ planes. Similar sentiments goal of reaching a fixed end, namely rant yet fully capable of performing were expressed by another well-known man as a moral creature.’’ These conclu- highly complex mathematical tasks. biologist, Carl Safina, in a N.Y. Times sions fly in the face of conventional Whereas the truth of Turing’s strange article (Feb. 10, 2009), entitled ‘‘Dar- wisdom, which holds that Darwin’s inversion in physics is universally ac- winism must die so that evolution may elucidation of natural selection was knowledged today, many people live.’’ philosophically and scientifically revolu- (namely, creationists) still cannot abide Our intent in this Sackler Collo- tionary precisely because it banished the Darwin’s strange inversion in biology. quium has not been to idolize Charles necessity for invoking ultimate purpose Dennett explores the philosophical rami- Darwin, but rather to celebrate the or goal-directedness in biological evolu- fications for Darwin’s inversion of rea- field of evolutionary biology that he tion. Nevertheless, Richards contends soning, and finds them to be truly played such an important role in devel- that many of Darwin’s writings are in- profound. oping nearly 2 centuries ago. We sub- fused with teleological statements, and A recent article in the New York mit that if Darwin were alive today, he that to dismiss these, or to rationalize Times (July 15, 2008) was entitled ‘‘Let’s would be satisfied with his own pio- them as rhetorical devices (for example, get rid of Darwinism.’’ It was written by neering efforts, but also completely whether Darwin was trying to assuage Olivia Judson, an evolutionary biologist astonished at the breadth, depth, and Victorian readers) is unwarranted. and the author of a best-selling evolu- vibrancy of the modern field. Richards bolsters this argument by trac- tionary book (34). In that article, Judson ACKNOWLEDGMENTS. The organizers and ing various of Darwin’s ideas to his wrote, ‘‘I’d like to abolish the insidious founding editors of this effort (J.C.A. and F.J.A.) early life, and how these concepts even- terms Darwinism, Darwinist, and Dar- are the academic grandson and son, respectively, tually played into the construction of winian. They suggest a false narrowness of Theodosius Dobzhansky, to whose fond mem- Darwin’s theory. Thus, Richards inter- to the field of modern evolutionary biol- ory this In the Light of Evolution series is dedi- cated. May Dobzhansky’s words and insights con- prets many of Darwin’s writings as con- ogy, as although it was the brainchild of tinue to inspire rational scientific inquiry into sistent with notions of evolutionary pur- a single person 150 years ago, rather nature’s marvelous operations.

1. Avise JC, Ayala FJ, eds (2007) In the Light of Evolution I: 11. Sedley D (2008) Creationism and Its Critics in Antiquity prints of maize domestication and evidence for a mas- Adaptation and Complex Design. Proc Natl Acad Sci (University of California Press, Berkeley). sive selective sweep on chromosome 10. Proc Natl Acad USA 104 (Suppl):8563–8676. 12. Paley W (1802) Natural Theology (American Tract So- Sci USA 106(Suppl):9979–9986. 2. Avise JC, Hubbell SP, Ayala FJ, eds (2008) In the Light of ciety, New York). 21. Allendorf FW, Hard, JJ (2009) Human-induced evolu- Evolution II: Biodiversity and Extinction. Proc Natl Acad 13. Darwin F, ed (1887) Charles Darwin’s Autobiography tion caused by unnatural selection through harvest of Sci USA 105 (Suppl):11453–11586. (Basic Books, New York), 1959 Ed. wild animals. Proc Natl Acad Sci USA 106(Suppl):9987– 3. Darwin CD (1859) On the Origin of Species by Means of 14. Dobzhansky T (1937) Genetics and the Origin of Spe- 9994. Natural Selection (Murray, London). cies (Columbia Univ Press, New York). 22. Bloom JD, Arnold, FH (2009) In the light of directed 4. Darwin CD (1868) The Variations of Animals and Plants 15. Via S (2009) Natural selection in action during specia- evolution: Pathways of adaptive protein evolution. Under Domestication (Murray, London). Proc Natl Acad Sci USA 106(Suppl):9995–10000. tion. Proc Natl Acad Sci USA 106(Suppl):9939–9946. 5. Darwin CD (1871) The Descent of Man and Selection in 23. Jones AG, Ratterman NL (2009) Mate choice and sexual 16. Hodges SA, Derieg NJ (2009) Adaptive radiations: From Relation to Sex (Random House, Modern Library, New selection: What have we learned since Darwin? Proc field to genomic studies. Proc Natl Acad Sci USA York). Natl Acad Sci USA 106(Suppl):10001–10008. 106(Suppl):9947–9954. 6. Darwin CD (1842) The Structure and Distribution of 24. Shuster S (2009) Sexual selection and mating systems. 17. Schluter D, Conte G (2009) Genetics and ecological Coral Reefs (Smith, Elder & Co, London). Proc Natl Acad Sci USA 106(Suppl):10009–10016. speciation. Proc Natl Acad Sci USA 106(Suppl):9955– 7. Darwin CD (1851) A Monograph on the Sub-Class Cir- 25. Gowaty PA, Hubbell SP (2009) Reproductive decisions 9962. ripedia, with Figures of All the Species (The Ray Society, under ecological constraints. Its about time. Proc Natl London). 18. Lukesˇ J, Leander BS, Keeling PJ (2009) Cascades of Acad Sci USA 106(Suppl):10017–10024. 8. Darwin CD (1875) Insectivorous Plants (Murray, : The corresponding evolutionary 26. Eberhard WG (2009) Post-copulatory sexual selection: London). histories of euglenozoans and dinoglagellates. Proc Darwin’s omission and its consequences. Proc Natl Acad 9. Darwin CD (1877) The Various Contrivances by Which Natl Acad Sci USA 106(Suppl):9963–9970. Sci USA 106(Suppl):10025–10032. Orchids Are Fertilized by Insects (Murray, London). 19. Driscoll CA, Macdonald DW, O’Brien SJ (2009) From wild 27. Barlow N (1958) The Autobiography of Charles Darwin 10. Darwin CD (1881) The Formation of Vegetable Moulds animals to domestic pets, an evolutionary view of domes- (Collins, London). through the Action of Worms, with Observations on tication. Proc Natl Acad Sci USA 106(Suppl):9971–9978. 28. Darwin F, ed (1887) The Life and Letters of Charles Their Habits (Murray, London). 20. Tian F, Stevens NM, Buckler ES, IV (2009) Tracking foot- Darwin (Murray, London), Vols 1–3.

Avise and Ayala PNAS ͉ June 16, 2009 ͉ vol. 106 ͉ suppl. 1 ͉ 9937 Downloaded by guest on October 5, 2021 29. Ayala FJ (2009) Darwin and the scientific method. Proc Proc Natl Acad Sci USA 106(Suppl):10048–10055. 34. Judson O (2002) Dr. Tatiana’s Sex Advice to All Cre- Natl Acad Sci USA 106(Suppl):10033–10039. 32. Richards RJ (2009) Darwin’s place in the history of ation: The Definitive Guide to the Evolutionary Biology 30. Ruse M (2009) The Darwinian revolution: Rethinking its thought: A reevaluation. Proc Natl Acad Sci USA of Sex (Henry Holt and Co, New York). meaning and significance. Proc Natl Acad Sci USA 106(Suppl):10056–10060. 35. Dobzhanksy T (1973) Nothing in biology makes sense 106(Suppl):10040–10047. 33. Dennett D (2009) Darwin’s ‘‘strange inversion of reason- except in the light of evolution. Amer Biol Teacher 31. Sober E (2009) Did Darwin write the Origin backwards? ing.’’ Proc Natl Acad Sci USA 106(Suppl):10061–10065. 35:125–129.

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