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In the Light of Evolution


Volume I: Adaptation and Complex Design



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John C. Avise and FrAnCisCo J. AyAlA, Editors THE NATIONAL ACADEMIES PRESS Washington, D.C. www.nap.edu

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THE NATIONAL ACADEMIES PRESS 500 Fifth Street., N.W. Washington, DC 20001 This volume is based on the Arthur M. sackler Colloquium of the national Academy of sci- ences, “in the light of evolution i: Adaptation and Complex Design,” held December 1-2, 2006, at the Arnold and Mabel Beckman Center of the national Academies of sciences and engineering in irvine, California. The articles appearing in these pages were contributed by speakers at the colloquium and have been anonymously reviewed. Any opinions, findings, conclusions, or recommendations expressed in this volume are those of the authors and do not necessarily reflect the views of the national Academy of sciences. Library of Congress Cataloging-in-Publication Data in the light of evolution / John C. Avise and Francisco J. Ayala, editors. p. cm. vol. i based on a colloquium of the national Academy of sciences, held December 1–2, 2006, in irvine, California. includes bibliographical references. isBn-13: 978-0-309-10405-0 (hardcover) isBn-10: 0-309-10405-X (hardcover) isBn-13: 978-0-309-66786-9 (pdf) isBn-10: 0-309-66786-0 (pdf) 1. evolution (Biology)—Congresses. i. Avise, John C, 1948-. ii. Ayala, Francisco José, 1934- iii. national Academy of sciences (U.s.) Qh359.i55 2007 576.8--dc22 2007032455 Additional copies of this book are available from the national Academies Press, 500 Fifth st., n.W., lockbox 285, Washington, DC 10055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); internet, http://www.nap.edu. Cover image: Aboriginal art (acrylic on canvas), Arnhem land, northwest Territories, Australia. Left: “saltwater Crocodile” by neil Manyita. Right: “Mimi spirit with Dillybag and stone Axe” by Abraham Dakgalawuy. These images evoke an impression of biotic complexity. images courtesy of John C. Avise. Copyright 2007 by the national Academies of sciences. All rights reserved. Printed in the United states of America

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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal govern- ment on scientific and technical matters. Dr. ralph J. Cicerone is president of the national Academy of sciences. The National Academy of Engineering was established in 1964, under the charter of the national Academy of sciences, as a parallel organization of outstanding engineers. it is autonomous in its administration and in the selection of its mem - bers, sharing with the national Academy of sciences the responsibility for advis- ing the federal government. The national Academy of engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. vest is president of the national Academy of engineering. The Institute of Medicine was established in 1970 by the national Academy of sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The insti- tute acts under the responsibility given to the national Academy of sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. harvey v. Fineberg is president of the institute of Medicine. The National Research Council was organized by the national Academy of sciences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the national Academy of sciences and the national Academy of engineering in pro- viding services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the institute of Medicine. Dr. ralph J. Cicerone and Dr. Charles M. vest are chair and vice chair, respectively, of the national research Council. www.national-academies.org

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Arthur M. Sackler, M.D. 1913-1987 Born in Brooklyn, new york, Arthur M. sackler was educated in the arts, sciences, and humanities at new york University. These interests remained the focus of his life, as he became widely known as a scientist, art collector, and philanthropist, endowing institutions of learning and culture throughout the world. he felt that his fundamental role was as a doctor, a vocation he decided upon at the age of four. After completing his internship and service as house physician at lincoln hospital in new york City, he became a resident in psychiatry at Creedmoor state hospital. There, in the 1940s, he started research that resulted in more than 150 papers in neuroendocri - nology, psychiatry, and experimental medicine. he considered his scien- tific research in the metabolic basis of schizophrenia his most significant contribution to science and served as editor of the Journal of Clinical and Experimental Psychobiology from 1950 to 1962. in 1960 he started publica- tion of Medical Tribune, a weekly medical newspaper that reached over one million readers in 20 countries. he established the laboratories for Therapeutic research in 1938, a facility in new york for basic research that he directed until 1983. As a generous benefactor to the causes of medicine and basic science, Arthur sackler built and contributed to a wide range of scientific insti- tutions: the sackler school of Medicine established in 1972 at Tel Aviv University, Tel Aviv, israel; the sackler institute of Graduate Biomedical science at new york University, founded in 1980; the Arthur M. sackler science Center dedicated in 1985 at Clark University, Worcester, Massachu- setts; and the sackler school of Graduate Biomedical sciences, established in 1980, and the Arthur M. sackler Center for health Communications, established in 1986, both at Tufts University, Boston, Massachusetts. his pre-eminence in the art world is already legendary. According to his wife Jillian, one of his favorite relaxations was to visit museums and art galleries and pick out great pieces others had overlooked. his interest in art is reflected in his philanthropy; he endowed galleries at the Metro- politan Museum of Art and Princeton University, a museum at harvard vii

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University, and the Arthur M. sackler Gallery of Asian Art in Washing- ton, D.C. True to his oft-stated determination to create bridges between peoples, he offered to build a teaching museum in China, which Jillian made possible after his death, and in 1993 opened the Arthur M. sackler Museum of Art and Archaeology at Peking University in Beijing. in a world that often sees science and art as two separate cultures, Arthur sackler saw them as inextricably related. in a speech given at the state University of new york at stony Brook, Some reflections on the arts, sciences and humanities, a year before his death, he observed: ‘‘Commu- nication is, for me, the primum movens of all culture. in the arts. . . i find the emotional component most moving. in science, it is the intellectual content. Both are deeply interlinked in the humanities.’’ The Arthur M. sackler Colloquia at the national Academy of sciences pay tribute to this faith in communication as the prime mover of knowledge and culture. viii

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Contents Arthur M. sackler Biography vii Preface to the In the Light of Evolution series xiii Preface to In the Light of Evoluion I: Adaptation and Complex Design xv PART I INTRODUCTORY ESSAY 1 1 Darwin’s Greatest Discovery: Design Without Designer 3 Francisco J. Ayala PART II EPISTEMOLOGICAL APPROACHES TO BIOCOMPLEXITY ASSESSMENT 23 2 Functional information and the emergence of Biocomplexity 25 Robert M. Hazen, Patrick L. Griffin, James M. Carothers, and Jack W. Szostak 3 The Theory of Facilitated variation 45 John Gerhart and Marc Kirschner ix

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x / Contents 4 Between “Design” and “Bricolage”: Genetic networks, levels of selection, and Adaptive evolution 65 Adam S. Wilkins 5 The Frailty of Adaptive hypotheses for the origins of organismal Complexity 83 Michael Lynch PART III FROM INDIVIDUAL ONTOGENY TO SYMBIOSIS: A HIERARCHY OF COMPLEXITY 105 6 emerging Principles of regulatory evolution 109 Benjamin Prud’homme, Nicolas Gompel, and Sean B. Carroll 7 evolution of individuality During the Transition from Unicellular to Multicellular life 129 Richard E. Michod 8 insect societies as Divided organisms: The Complexities of Purpose and Cross-Purpose 145 Joan E. Strassmann and David C. Queller 9 symbiosis as an Adaptive Process and source of Phenotypic Complexity 165 Nancy A. Moran PART IV CASE STUDIES: DISSECTING COMPLEX PHENOTYPES 183 10 Adaptive evolution of Color vision as seen Through the eyes of Butterflies 187 Francesca D. Frentiu, Gary D. Bernard, Cristina I. Cuevas, Marilou P. Sison-Mangus, Kathleen L. Prudic, and Adriana D. Briscoe 11 Plant Domestication, a Unique opportunity to identify the Genetic Basis of Adaptation 205 Jeffrey Ross-Ibarra, Peter L. Morrell, and Brandon S. Gaut

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Contents / xi 12 An experimental Test of evolutionary Trade-offs During Temperature Adaptation 225 Albert F. Bennett and Richard E. Lenski 13 Two routes to Functional Adaptation: Tibetan and Andean high-Altitude natives 239 Cynthia M. Beall 14 on the origin and evolutionary Diversification of Beetle horns 257 Douglas J. Emlen, Laura Corley Lavine, and Ben Ewen-Campen PART V CONCLUDING ESSAY 283 15 Biological Design in science Classrooms 285 Eugenie C. Scott and Nicholas J. Matzke references 305 index 345

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Preface to the In the Light of Evolution Series B iodiversity—the genetic variety of life—is an exuberant product of the evolutionary past, a vast human-supportive resource (aesthetic, intellectual, and material) of the present, and a rich legacy to cherish and preserve for the future. Two urgent challenges, and opportunities, for 21st-century science are to gain deeper insights into the evolutionary pro - cesses that foster biotic diversity, and to translate that understanding into workable solutions for the regional and global crises that biodiversity cur- rently faces. A grasp of evolutionary principles and processes is important in other societal arenas as well, such as education, medicine, sociology, and other applied fields including agriculture, pharmacology, and bio- technology. The ramifications of evolutionary thought also extend into learned realms traditionally reserved for philosophy and religion. in 1973, Theodosius Dobzhansky penned a short commentary entitled “nothing in biology makes sense except in the light of evolution.” Most scientists agree that evolution provides the unifying framework for inter- preting biological phenomena that otherwise can often seem unrelated and perhaps unintelligible. Given the central position of evolutionary thought in biology, it is sadly ironic that evolutionary perspectives outside the sciences have often been neglected, misunderstood, or purposefully misrepresented. The central goal of the ILE series will be to promote the evolutionary sciences through state-of-the-art colloquia—in the series of Arthur M. sackler colloquia sponsored by the national Academy of sciences—and their published proceedings. each installment will explore evolutionary xiii

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xiv / Preface to the in the light of evolution Series perspectives on a particular biological topic that is scientifically intriguing but also has special relevance to contemporary societal issues or chal - lenges. individually and collectively, the ILE series will aim to interpret phenomena in various areas of biology through the lens of evolution, address some of the most intellectually engaging as well as pragmatically important societal issues of our times, and foster a greater appreciation of evolutionary biology as a consolidating foundation for the life sciences. The organizers and founding editors of this effort (Avise and Ayala) are the academic grandson and son, respectively, of Theodosius Dobzhansky, to whose fond memory this ILE series is dedicated. May Doby’s words and insights continue to inspire rational scientific inquiry into nature’s marvelous operations. John C. Avise and Francisco J. Ayala Department of ecology and evolutionary Biology, University of California, irvine

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Preface to In the Light of Evolution, Volume I: Adaptation and Complex Design D arwin’s elucidation of natural selection as a creative evolutionary force was one of the monumental intellectual achievements in the history of science, revolutionizing thought not only across the biological sciences but also fundamentally impacting much discourse in the social sciences, philosophy, and religion. no longer were explanations for the origin and marvelous adaptations of organisms necessarily to be sought solely in the context of supernatural causation. instead, biological outcomes could now be interpreted within the critical scientific framework of natural processes governed by natural laws. As a young man, Charles Darwin (like most biologists of his era, and before) was a natural theologian steeped in the notion that an atten - tive study of organisms in nature would ineluctably serve to document and further glorify the infinite creative powers of the Almighty. Darwin read and greatly admired William Paley’s 1802 Natural Theology, which eloquently developed the “argument from design” that biological com- plexity was prima facie evidence for an intelligent engineer. This age-old idea had an illustrious intellectual pedigree. For example, it had been one of the “Five Ways” that st. Thomas Aquinas (an influential Dominican scholar of the 13th century) purported to prove God’s existence. in 1779, the scottish philosopher David hume again encapsulated conventional wisdom when he wrote: the curious adapting of means to ends, throughout all of nature, resem - bles exactly, though it much exceeds, the productions of human contriv- xv

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xvi / Preface to in the light of evolution, volume i ance, of human design, thought, wisdom, and intelligence. . . . By this argument a posteriori, and by this argument alone, do we perceive at once the existence of a Deity, and his similarity to human mind and intelligence (Dialogues Concerning Natural Religion). The link between adaptation, biological complexity, and omnipotent design was apparent not only to philosophers and theologians. As phrased in the 1600s by the Christian scholar and scientist John ray: you may hear illiterate persons of the lowest rank of the Commonality affirming, that they need no Proof of the being of God, for that every Pile of Grass, or ear of Corn, sufficiently proves that. . . . To tell them that it made it self, or sprung up by chance, would be as ridiculous as to tell the greatest Philosopher so (The Wisdom of God Manifested in the Works of Creation). When Darwin boarded the HMS Beagle in 1831, he had no inkling that his voyage of discovery would eventually lead him to a revolution - ary concept: that a purely natural process—natural selection—can yield biological outcomes that otherwise seem to have the earmarks of intel - ligent craftsmanship. natural selection is an inevitable process of nature whenever organisms show heritable variation in their capacity to survive and reproduce in particular environments, but the operation has no more consciousness or intelligence than do natural physical forces such as gravity or weather. Thus, Darwin’s key legacy is not the mere demonstra - tion that evolution occurs (several of Darwin’s predecessors were aware that species evolve), but rather the stunning revelation that a natural rather than a supernatural directive agent can orchestrate the evolutionary emergence of biological adaptations. nevertheless, 150 years after Darwin the challenge of understanding nature’s complexity remains in many regards in its infancy. only recently has science developed the necessary laboratory tools for delving deep within the molecular structure and function of genes that underlie particu- lar complex adaptations (such as the eye, or the body plans of vertebrate animals). only recently has it become possible to conduct genomic analy- ses in ways that permit the discovery of heretofore unspecified structural and regulatory genes that contribute to the molecular assembly of com- plex organismal phenotypes. only recently have phylogenetic methods progressed to the point where the histories of complex phenotypes can be reliably elucidated. scientific progress is occurring on many related fronts as well. For example, recent developments in evolutionary genetic theory (such as formal network analysis) have opened exciting new avenues for exploring the geneses and maintenance of biological complexity at the levels of genetic and metabolic pathways.

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Preface to in the light of evolution, volume 1 / xvii This book is the outgrowth of the Arthur M. sackler colloquium on “Adaptation and Complex Design,” which was sponsored by the national Academy of sciences on December 1–2, 2006, at the Academy’s Arnold and Mabel Beckman Center in irvine, California. it is the first in a proposed series of sackler colloquia under the umbrella title “in the light of evolu- tion.” The chapters that follow illustrate a wide variety of current scientific perspectives and methodological approaches directed toward understand- ing the origin and maintenance of complex biological adaptations. in the opening chapter of this volume, Francisco Ayala develops the thesis that the Darwinian revolution in effect completed the Copernican revolution by extending from physics to biology a notion that the universe operates by natural laws that fall within the purview of rational scientific inquiry. in 1543, nicolaus Copernicus published De revolutionibus orbium celestium (on the revolutions of the Celestial spheres), which introduced the idea that the earth is not at the center of creation and that natural laws govern the motion of structures in the physical universe. This thesis was bolstered and elaborated by the scientific discoveries of Galileo, Kepler, newton, and others during the 16th and 17th centuries, but it was left to Darwin in the 19th century to discover that natural laws and processes also govern the emergence of apparent design in biological systems. subsequent chapters in this volume then illustrate the wide variety of current scientific avenues for exploring the nature of complex adapta - tions. Chapters are arranged into three parts, each immediately preceded by a brief editorial introduction. Authors in Part ii set a conceptual stage by addressing epistemological issues related to biotic complexity from several disparate scientific perspectives including population genetics, information theory, and systems biology. in Part iii, authors address the evolution of biotic complexity in a hierarchy of contexts, from the onto - genetic programs underlying particular phenotypes to the cooperation and conflicts often associated with multicellularity, social behaviors, and symbiotic associations. Chapters in Part iv provide additional case studies of how genetic, developmental, ecological, and other biological phenom- ena are now being dissected for complex phenotypes ranging from beetle horns to human adaptations for high-altitude hypoxia. overall, the col- lection of ideas and data in this volume is highly eclectic but nonetheless broadly illustrative of modern scientific attempts to understand the evolu- tion of complex adaptations. These scientific endeavors are coming at a time of resurgent societal interest in supernatural explanations for biological complexity. especially in the United states, proponents of intelligent design (iD)—the latest reincarnation of religious creationism—argue that biotic complexity can only be the product of a supreme intelligence (i.e., God). in the closing chapter of this volume, eugenie scott and nicholas Matzke examine the

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xviii / Preface to in the light of evolution, volume i history of the iD movement and they conclude that although its scientific merit is nil, the crusade itself is of consequence to broader society because it represents a serious assault on the integrity of science education. Perhaps there is a middle ground for scientific and theological inter- pretations of complex biological design. in his 1973 commentary entitled “nothing in Biology Makes sense except in the light of evolution,” Theodosius Dobzhansky famously proclaimed “i am a creationist and an evolutionist. evolution is God’s, or nature’s method of creation.” regard- less of what our personal philosophical persuasion may be, let us rejoice in biotic complexity and in the scientific efforts to understand its geneses.