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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

arwins elucidation of natural proves that. . . . To tell 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
achievements 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
mentally impacting much discourse in When Darwin boarded the HMS Bea-
of rational scientific inquiry. In 1543,
the social sciences, philosophy, and reli- gle in 1831, he had no inkling that his
Nicolaus Copernicus published De revo-
gion. No longer were explanations for voyage of discovery would eventually
lutionibus orbium celestium (On the Rev-
the origin and marvelous adaptations of lead him to a revolutionary concept:
olutions of the Celestial Spheres), which
organisms necessarily to be sought solely that a purely natural processnatural
introduced the idea that the earth is not
in the context of supernatural causation. selectioncan yield biological outcomes
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, Darwins 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 Darwins prede- Most of the remaining articles in the
Darwin read and greatly admired Wil- Colloquium fall under three themes:
liam Paleys 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-
tive agent can orchestrate the evolution- Symbiosis (A Hierarchy of Complexity),
plexity was prima facie evidence for an
ary emergence of biological adaptations. and Dissecting Complex Phenotypes (Case
intelligent engineer. This age-old idea
Nevertheless, 150 years after Darwin Studies).
had an illustrious intellectual pedigree.
For example, it had been one of the the challenge of understanding natures
Epistemological Approaches to
Five Ways that St. Thomas Aquinas complexity remains in many regards in
Biocomplexity Assessment
(an influential Dominican scholar of the its infancy. Only recently has science
developed the necessary laboratory tools The sphere of biological phenomena
13th century) purported to prove Gods
for delving deep within the molecular interpretable in the light of evolution is
existence. In 1779, the Scottish philoso-
structure and function of genes that un- vast, so perhaps it is not surprising that
pher David Hume again encapsulated
derlie particular complex adaptations researchers from many different scien-
conventional wisdom when he wrote
(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-
ment, which resulted from the Arthur M. Sackler Collo-
Dialogues Concerning Natural Religion 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-

complexity, and omnipotent design was netic theory have opened exciting new ber 12, 2006, at the Arnold and Mabel Beckman Center of
the National Academies of Sciences and Engineering in
apparent not only to philosophers and avenues for exploring the geneses 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
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- or
of Grass, or Ear of Corn, sufficiently plex biological adaptations. 2007 by The National Academy of Sciences of the USA

www.pnas.orgcgidoi10.1073pnas.0702066104 PNAS May 15, 2007 vol. 104 suppl. 1 8563 8566
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 informationthat 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 they
mutate, and adapt by natural selection. encode) direct the molecular dances of
peril. To illustrate his argument, Lynch
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-
ment of genic and genomic phenomena evidenced by the great diversity of body
lation, rather than DNA sequence muta-
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 phologies? Most researchers suspect that
become mainstream, as reflected in sev-
(A Hierarchy of Complexity) evolutionary changes in gene regulation
eral articles in this Colloquium. John
Gerhart and Marc Kirschner (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. Biodiversitythe ge- lectively, the In the Light of Evolution
(albeit to a debatable degree) the suite netic variety of lifeis 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 skys 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- natures marvelous operations.
had been regarded as essentially impossible.

8564 www.pnas.orgcgidoi10.1073pnas.0702066104 Avise and Ayala

preexisting genes and proteins into new behavioral phenomena in eusocial colo- primates and butterflies. The research
functions. Benjamin Prudhomme 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
colonys 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. Ayalas 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
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). Darwins fas- coming at a time of resurgent societal an evolutionist. Evolution is Gods, or Na-
cination with beetles began in childhood interest in supernatural explanations for tures 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 creationismargue that biotic understand its geneses.

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8566 www.pnas.orgcgidoi10.1073pnas.0702066104 Avise and Ayala