FROM THE ACADEMY: COLLOQUIUM PERSPECTIVE In the light of evolution I: Adaptation 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 Dachievements 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 adaptations 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, Charles Darwin (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 developmental biology 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 mutation, 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