RMTEAAEY OLQIMPERSPECTIVE COLLOQUIUM ACADEMY: THE FROM

In the light of I: and complex design

John C. Avise* and Francisco J. Ayala* Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697

arwin’s elucidation of natural proves that....Totell them that it In the first article of this Colloquium, selection as a creative evolu- made it self, or sprung up by chance, Francisco Ayala (1) develops the thesis tionary force was one of the would be as ridiculous as to tell the that the Darwinian revolution in effect monumental intellectual greatest Philosopher so. completed the Copernican revolution by achievementsD in the history of science, The Wisdom of God Manifested in extending from physics to biology a no- not only revolutionizing thought across the Works of Creation tion that the universe operates by natu- the biological sciences but also funda- ral laws that fall within the purview When Darwin boarded the HMS Bea- mentally impacting much discourse in of rational scientific inquiry. In 1543, gle in 1831, he had no inkling that his the social sciences, philosophy, and reli- Nicolaus Copernicus published De revo- voyage of discovery would eventually gion. No longer were explanations for lutionibus orbium celestium (On the Rev- lead him to a revolutionary concept: the origin and marvelous of olutions of the Celestial Spheres), which that a purely natural process—natural organisms necessarily to be sought solely introduced the idea that the earth is not selection—can yield biological outcomes in the context of supernatural causation. at the center of Creation and that natu- Instead, biological outcomes could now that otherwise seem to have the ear- marks of intelligent craftsmanship. Nat- ral laws govern the motion of structures be interpreted within the critical scien- in the physical universe. This thesis was tific framework of natural processes gov- ural selection is an inevitable process of nature whenever organisms show herita- bolstered and elaborated by the scien- erned by natural processes and laws. tific discoveries of Galileo, Kepler, New- As a young man, (like ble variation in their capacity to survive and reproduce in particular environ- ton, and others during the 16th and 17th most biologists of his era and before) centuries, but it was left to Darwin in was a natural theologian steeped in the ments, but the operation has no more consciousness or intelligence than do the 19th century to discover that natural notion that an attentive study of organ- laws and processes also govern the isms in nature would ineluctably serve natural physical forces such as gravity or weather. Thus, Darwin’s key legacy is emergence of apparent design in biolog- to document and further glorify the infi- ical systems. nite creative powers of the Almighty. not the mere demonstration that evolu- tion occurs (several of Darwin’s prede- Most of the remaining articles in the Darwin read and greatly admired Wil- Colloquium fall under three themes: liam Paley’s 1802 Natural Theology, cessors were aware that species evolve), but rather the stunning revelation that a Epistemological Approaches to Biocom- which eloquently developed the ‘‘argu- plexity Assessment, From Ontogeny to ment from design’’ that biological com- natural rather than a supernatural direc- Symbiosis (A Hierarchy of Complexity), plexity was prima facie evidence for an tive agent can orchestrate the evolution- and Dissecting Complex Phenotypes (Case intelligent engineer. This age-old idea ary emergence of biological adaptations. Studies). had an illustrious intellectual pedigree. Nevertheless, 150 years after Darwin the challenge of understanding nature’s For example, it had been one of the Epistemological Approaches to complexity remains in many regards in ‘‘Five Ways’’ that St. Thomas Aquinas Biocomplexity Assessment (an influential Dominican scholar of the its infancy. Only recently has science The sphere of biological phenomena 13th century) purported to prove God’s developed the necessary laboratory tools interpretable in the light of evolution is existence. In 1779, the Scottish philoso- for delving deep within the molecular vast, so perhaps it is not surprising that pher David Hume again encapsulated structure and function of genes that un- researchers from many different scien- conventional wisdom when he wrote derlie particular complex adaptations (such as the eye or the body plans of tific backgrounds and orientations have the curious adapting of means to vertebrate animals). Only recently has it weighed in on how best to approach the ends, throughout all of nature, re- become possible to conduct genomic study of complex adaptations. The arti- sembles exactly, although it much analyses in ways that permit the discov- cles under this heading will illustrate exceeds, the productions of human ery of heretofore unspecified structural some of this diversity. contrivance, of human design, and regulatory genes that contribute to Robert Hazen et al. (2) raise two im- thought, wisdom, and intelligence.... the molecular assembly of complex or- portant related questions: What actually By this argument a posteriori, and by ganismal phenotypes. Only recently have is meant by biological ‘‘complexity’’ and this argument alone, do we perceive phylogenetic methods progressed to the how might complexity be quantified? at once the existence of a Deity, and point where the histories of complex his similarity to human mind and in- phenotypes can be reliably elucidated. telligence. Scientific progress is occurring on many This paper serves as an introduction to this PNAS supple- Dialogues Concerning Natural Religion ment, which resulted from the Arthur M. Sackler Collo- related fronts as well. For example, re- quium of the National Academy of Sciences, ‘‘In the Light of The link between adaptation, biological cent developments in evolutionary ge- Evolution I: Adaptation and Complex Design,’’ held Decem- ber 1–2, 2006, at the Arnold and Mabel Beckman Center of complexity, and omnipotent design was netic theory have opened exciting new avenues for exploring the geneses and the National Academies of Sciences and Engineering in apparent not only to philosophers and Irvine, CA. It is the first in a planned series of colloquia under theologians. As phrased in the 1600s by maintenance of biological complexity at the umbrella title ‘‘In the Light of Evolution’’ (see Box 1). the Christian scholar and scientist John Ray, the levels of genetic and metabolic path- The complete program is available on the NAS web site at ways. The articles in this Colloquium www.nasonline.org/adaptation࿝and࿝complex࿝design. You may hear illiterate persons of illustrate a wide variety of current scien- Author contributions: J.C.A. and F.J.A. wrote the paper. the lowest Rank of the Commonality tific perspectives and methodological The authors declare no conflict of interest. affirming, that they need no Proof of approaches directed toward understand- *To whom correspondence may be addressed. E-mail: the being of God, for that every Pile ing the origin and maintenance of com- [email protected] or [email protected]. of Grass, or Ear of Corn, sufficiently plex biological adaptations. © 2007 by The National Academy of Sciences of the USA

www.pnas.org͞cgi͞doi͞10.1073͞pnas.0702066104 PNAS ͉ May 15, 2007 ͉ vol. 104 ͉ suppl. 1 ͉ 8563–8566 Downloaded by guest on September 30, 2021 The authors suggest that a hallmark of Michael Lynch (7) reminds us that and cellular operations within an organ- any complex system (physical or biologi- mechanistic explanations of phenotypic ism to species’ interactions in ecological cal) is its potential to perform a quanti- evolution that emerge from the fields of communities. At any level, biological fiable operation. Starting with that and molecular entities are enmeshed in interactive net- premise, they formally define a metric— genetics cannot violate the fundamental works that typically involve potential functional information—that basically dynamics of the evolutionary process as conflicts as well as collaborations. For describes the fraction of all possible elucidated by a century of work in theo- example, a multicellular organism can configurations of the system that possess retical population genetics. Regardless be viewed as a social collective of cells a specified degree of function. Although of which genes underlie complex or whose genes must not only collaborate this metric may be difficult to apply in other phenotypes, their microevolution- to generate a viable individual but also the real world (because it requires ary dynamics remain governed by the compete for inclusion in gametes that knowledge of all possible configurations forces of , gene flow, natural will form the next generation. Articles in and the degree of function of each), it selection, recombination, and random this section deal with some of the complex nonetheless may have heuristic merit for genetic drift. The point, however, is not interactions that characterize biological studying the properties of complex to claim priority for one discipline over systems at the levels of ontogeny, multicel- systems. The authors illustrate this ap- another, but rather to emphasize that lularity, eusociality, and symbiosis. proach using a virtual world of com- any evolutionary model that disregards During ontogeny, suites of genes (and puter programs that self-replicate, population genetic reality does so at its the RNA and protein molecules they mutate, and adapt by natural selection. peril. To illustrate his argument, Lynch encode) direct the molecular dances of In 1975, Mary-Claire King and Allan examines the ineluctable consequences development that produce a functional Wilson (3) popularized an earlier idea of genetic drift, especially in small popu- multicellular organism. The ontogenetic by Roy Britten and Eric Davidson (4) lations, and he highlights a wide assort- choreographies themselves evolve, as that evolutionary changes in gene regu- evidenced by the great diversity of body lation, rather than DNA sequence muta- ment of genic and genomic phenomena tions in protein-coding exons per se, that make sense only after accounting for plans and other phenotypes in different were largely responsible for phenotypic variation among taxa in the relative power organismal lineages. What kinds of ge- evolution and the emergence of complex of nonadaptive evolutionary forces. netic mechanisms underlie ontogenetic adaptations. This sentiment has since shifts and the emergence of novel mor- From Ontogeny to Symbiosis become mainstream, as reflected in sev- phologies? Most researchers suspect that (A Hierarchy of Complexity) eral articles in this Colloquium. John evolutionary changes in gene regulation Gerhart and (5) accept Biological complexity is displayed at are especially important and that such the notion that regulatory changes are many hierarchical levels, from molecular alterations often involve the cooption of of central importance, and indeed they argue that most key phenotypic evolu- tion over the past 600 million years has resulted from altered usage patterns in a Box 1. In the Light of Evolution. In ture, pharmacology, and biotechnology. large set of otherwise conserved core 1973, Theodosius Dobzhansky penned a The ramifications of evolutionary genetic components that direct organis- short commentary titled ‘‘Nothing in Bi- thought extend into learned realms tra- mal development and physiology. In the ology Makes Sense Except in the Light of ditionally reserved for philosophy and ‘‘theory of facilitated variation’’ formu- Evolution’’ (24). Most scientists agree religion. The central goal of the In the lated by Gerhart and Kirschner (5), sev- that evolution provides the unifying Light of Evolution series will be to pro- eral regulatory features of the genome framework for interpreting biological mote the evolutionary sciences through collude to foster more phenotypic evolu- phenomena that otherwise can often state-of-the-art colloquia and their pub- tion with less genetic change than would seem unrelated and perhaps unintelligi- lished proceedings. Each installment will otherwise have been possible. ble. Given the central position of evolu- explore evolutionary perspectives on a Adam Wilkins (6) then examines the tionary thought in biology, it is sadly particular biological topic that is scien- converse of evolutionary plasticity: phe- ironic that evolutionary perspectives out- tifically intriguing but also has special notypic constraint. It has long been side the sciences have often been ne- relevance to contemporary societal is- evident that phylogenetic legacies and glected, misunderstood, or purposely sues or challenges. Individually and col- developmental contingencies restrict misrepresented. Biodiversity—the ge- lectively, the In the Light of Evolution (albeit to a debatable degree) the suite netic variety of life—is an exuberant series will aim to interpret phenomena in of evolutionary pathways potentially product of the evolutionary past, a vast various areas of biology through the lens available to any species. Wilkins pro- human-supportive resource (aesthetic, of evolution, address some of the most poses that, in addition to these conven- intellectual, and material) of the present, intellectually engaging as well as prag- tionally recognized inhibitors of pheno- and a rich legacy to cherish and preserve matically important societal issues of our typic evolution, inherent constraints also for the future. Two challenges, as well as times, and foster a greater appreciation operate at the levels of interacting genes opportunities, for 21st-century science of evolutionary biology as a consolidat- and complex genetic networks. If molec- are to gain deeper insights into the evo- ing foundation for the life sciences. ular biologists can illuminate the genetic lutionary processes that foster biotic The organizers and founding editors biases that constrain as well as promote diversity and to translate that under- of this effort (J.C.A. and F.J.A.) are the the evolution of particular phenotypes, standing into workable solutions for the academic grandson and son, respectively, it might become possible, Wilkins ar- regional and global crises that biodiver- of Theodosius Dobzhansky, to whose gues, to specify the relative probabilities sity currently faces. A grasp of evolution- fond memory this In the Light of Evolu- of alternative evolutionary trajectories ary principles and processes is important tion series is dedicated. May Dobzhan- (at least over the short term) for partic- in other societal arenas as well, such as sky’s words and insights continue to in- ular lineages. Traditionally, this kind of education, medicine, sociology, and spire rational scientific inquiry into predictability about evolutionary futures other applied fields including agricul- nature’s marvelous operations. had been regarded as essentially impossible.

8564 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0702066104 Avise and Ayala Downloaded by guest on September 30, 2021 preexisting genes and proteins into new behavioral phenomena in eusocial colo- primates and butterflies. The research functions. Benjamin Prud’homme et al. nies, nicely exemplifies the power of summarized by these authors demon- (8) illustrate how such cooptions can scientific explanation for complex bio- strates some remarkable parallels in how occur via shifts in the deployment of logical phenomena. particular amino acid sites in photopig- cis-regulatory elements and their associ- Genomic evolution was traditionally ments can be involved in color percep- ated transcription factors. They argue thought to proceed independently in tion in both insects and mammals. that this specific kind of architectural different lineages, but a growing body of Darwin was interested in the close change in regulatory networks offers a literature has revealed numerous excep- parallels between natural selection and key to understanding how morphological tions. For example, horizontal gene artificial selection, and in 1868 he evolution is linked to molecular ontoge- transfer events have proved to be rather published a book on the topic of pheno- netic processes. common in various prokaryotic groups, types in domesticated plants and ani- Multicellularity itself is a complex sometimes affording the recipient with mals (16). Jeffrey Ross-Ibara et al. (17) trait, yet the phenomenon has arisen novel metabolic capabilities. Another illustrate modern genetic approaches to independently on numerous occasions. evolutionary route by which lineages dissecting important phenotypes that Each evolutionary transition from uni- may acquire functional innovations in- have evolved under human influence, cellularity to multicellularity likely pro- volves the establishment of stable (and with special reference to domestic corn. ceeds through a succession of stages: sometimes heritable) symbiotic associa- They distinguish top-down genetic ap- initial aggregation of cells, increased tions. Nancy Moran (13) interprets vari- proaches (such as QTL mapping) from cooperation within the group, the evolu- ous symbioses among microorganisms, bottom-up approaches (such as candi- tion of policing mechanisms against and between microorganisms and their date gene assays) and conclude that the cheater cells, increases in group size, multicellular hosts, as important (and latter method, despite some pitfalls, gen- and the spatial and functional specializa- previously underappreciated) evolution- erally holds greater promise for reveal- tion of cell types. The process is remark- ary sources of phenotypic novelty. Using ing how key phenotypes in crop plants able because it entails, in effect, the compelling examples from insects and have evolved under domestication from emergence of reproductive altruism, other organisms, Moran shows how obli- their ancestral wild states. wherein most cells forego personal re- gate symbiosis can yield complex evolu- Al Bennett and Richard Lenski (18) production in favor of working on the tionary outcomes, ranging from the address a longstanding question: Is there colony’s behalf, a situation that un- emergence of specialized cell types and a necessary cost to adaptation? In other doubtedly necessitates high within- organs to various developmental mecha- words, does the evolution of a pheno- colony kinship (9). Rick Michod (10) nisms that regulate the intergenerational type that is adaptive to a particular en- discusses these topics with special refer- continuance of the symbiotic association. vironment necessitate deterioration in ence to living volvocine green algae, other traits? If so, what natural selection which collectively display several stages Dissecting Complex Phenotypes can achieve via the adaptive process along the unicellularity to multicellular- (Case Studies) would inevitably be constrained by such ity continuum. Michod contends that The articles under this heading provide fitness “tradeoffs.” To examine this issue multicellularity is not ‘‘irreducibly com- examples of how scientists are tackling empirically, the authors monitored mul- plex’’ in an evolutionary sense, but rather the empirical challenge of dissecting tigeneration selection responses of bac- can be understood in terms of evolution- complex phenotypes. In The Origin of teria to altered temperature regimes. ary tradeoffs and fitness advantages that Species (14), Darwin deemed the eye to After 2,000 generations of thermal se- can attend various intermediate stages in be an organ of ‘‘extreme perfection and lection, most colonies that showed im- the evolutionary transitions between one complication.’’ He also wrote, ‘‘To sup- proved fitness at low temperatures also kind of individual and another. pose that the eye with all its inimitable showed fitness declines at high tempera- Eusociality is perhaps the epitome of contrivances for adjusting the focus to tures, but this was not invariably the complex social behavior and apparent different distances, for admitting dif- case. The fact that exceptions exist indi- reproductive selflessness. In eusocial ferent amounts of light, and for the cates that fitness tradeoffs are not an colonies, such as those of many hyme- correction of spherical and chromatic inevitable component of the adaptive nopteran insects, individuals show strik- aberration, could have been formed by evolutionary process. ing reproductive divisions of labor, with natural selection, seems, I freely confess, Bacteria such as Escherichia coli are sterile workers striving to maintain and absurd in the highest degree.’’ Nonethe- model experimental organisms because defend a colony whose offspring are less, ‘‘reason tells me, that if numerous they have short generation lengths and produced by the reproductive elites. Eu- gradations from a simple and imperfect are easy to manipulate, but they also sociality has long intrigued biologists. A eye to one complex and perfect can be have relatively simple phenotypes. Near key insight came from William Hamilton shown to exist, each grade being useful the other end of the continuum is Homo (11), who proposed that the evolution of to its possessor, ....then the difficulty sapiens, which has many complex pheno- extreme reproductive altruism by work- of believing that a perfect and complex types of special interest but is far less ers was facilitated by the altered genetic eye could be formed by natural selec- tractable to experimental manipulation. relationships among various colony tion, although insuperable to our Cynthia Beall (19) describes the adapta- members stemming from haplodiploid imagination, should not be considered tions to high-altitude hypoxia (oxygen sex determination. Joan Strassman and subversive of the theory.’’ Ayala’s open- shortage) displayed by humans indige- David Queller (12) review current ing article of this Colloquium (1) ad- nous to the Andean and Tibetan Pla- thought about the evolution of eusocial- dresses how light-sensing organs in teaus. Remarkably, the physiological and ity, including the important point that mollusks vary from the simple to the molecular adaptations to hypoxia differ kin selection predicts a degree of cross- highly complex, each type nonetheless of dramatically between these two popula- purpose and conflict (as well as exten- utility to its bearers. Francesca Frentiu tions, suggesting different evolutionary sive cooperation and common purpose) et al. (15) delve deeper into the molecu- pathways to the same functional out- in eusocial insect colonies. They con- lar basis of vision by discussing the com- come. Beall describes how scientists are clude that kin-selection theory, by mak- parative evolution of genes and proteins currently dissecting the evolutionary ge- ing specific testable predictions about underlying color-vision phenotypes in netic responses to oxygen deprivation

Avise and Ayala PNAS ͉ May 15, 2007 ͉ vol. 104 ͉ suppl. 1 ͉ 8565 Downloaded by guest on September 30, 2021 displayed by these two populations, and pleasure as collecting beetles’’ (21). complexity can only be the product of a in so doing reveals some of the special Douglas Emlen et al. (22) describe mod- supreme intelligence (i.e., God). In the challenges of working with a nonmodel ern research on the molecular genetics, closing article of this Colloquium, Eug- experimental species. ontogeny, and phylogenetics of beetle enie Scott and Nicholas Matzke (23) Beetles (Coleoptera) have long in- horns. These authors advance fascinat- examine the history of the ID move- trigued biologists. The British geneticist ing mechanistic scenarios for the evolu- ment, and they conclude that although and evolutionist J. B. S. Haldane fa- tionary origins of these peculiar devices without scientific merit, the crusade it- mously remarked that the Creator must and for subsequent evolutionary alter- self is of consequence to broader society have had an inordinate fondness for ations in horn shapes, allometries, body because it represents a serious assault beetles because he made so many spe- locations, and patterns of sexual dimorphism. on the integrity of science education. Perhaps there is a middle ground for cies of them (at least half a million). A Overall, the collection of ideas and scientific and theological interpretations of century earlier, Darwin had speculated data in this Colloquium is highly eclectic complex biological design. In his 1973 that the oft-ornate horns that many bee- but nonetheless broadly illustrative of commentary titled ‘‘Nothing in Biology tles carry on their heads or thorax were modern scientific attempts to under- Makes Sense Except in the Light of Evo- favored by sexual selection as weapons, stand the evolution of complex adapta- lution’’ (24), Theodosius Dobzhansky fa- used in jousts between males over mat- tions. These scientific endeavors are mously proclaimed ‘‘I am a creationist and ing access to females (20). Darwin’s fas- coming at a time of resurgent societal an evolutionist. Evolution is God’s, or Na- cination with beetles began in childhood interest in supernatural explanations for ture’s method of creation.’’ Regardless of and grew in his college years, as indi- biological complexity. Especially in the what our personal philosophical persua- cated in his autobiography: ‘‘no pursuit United States, proponents of intelligent sion may be, let us rejoice in biotic com- at Cambridge was followed with nearly design (ID)—the latest reincarnation of plexity and in the scientific efforts to so much eagerness or gave me so much religious —argue that biotic understand its geneses.

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