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In the Light of Evolution
Volume VI: Brain and Behavior
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In the Light of Evolution
Volume VI: Brain and Behavior
GEORG F. STRIEDTER, 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, NW 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 VI: Brain and Behavior,” held January 20-21, 2012, 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 view of
the National Academy of Sciences.
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: 978-0-309-26175-3
ISBN-10: 0-309-26175-9
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., NW, Keck 360, Washington, DC 20001; (800) 624-6242 or (202) 334-3313; http://www.
nap.edu.
Cover image: Pictured is a diffusion MRI image of a human brain, viewed from above, with
the back of the head at the bottom of the image. Each line represents thousands of axons,
traveling as a group along a particular axis (green: front to back; red: left to right; blue: top to
bottom). This technique represents one of numerous methods used to infer the evolutionary
processes that shaped the brain and behavior. Articles in this Arthur M. Sackler Colloquium,
“In the Light of Evolution VI: Brain and Behavior,” explore research on how and why com-
plex nervous systems evolved, showing the progress that has been made since the dawn of
evolutionary neuroscience 150 years ago. Image courtesy of Patric Hagmann (Department
of Radiology, University Hospital Center, University of Lausanne, Switzerland).
Copyright 2013 by the National Academy 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 cademy has a mandate that requires it to advise the federal govern-
A
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 philanhropist,
t
endowing institutions of learning and culture
through ut the world.
o
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 Metropolitan Museum of Art and Princeton University, a museum at
vii
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Harvard University, and the Arthur M. Sackler Gallery of Asian Art in
Washington, 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: ‘‘Communi-
cation 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 Evolution VI: Brain and Behavior xv
PART I EVOLUTIONARY ORIGINS OF NEURONS AND
NERVOUS SYSTEMS 1
1 Functionalization of a Protosynaptic Gene Expression Network 3
Cecilia Conaco, Danielle S. Bassett, Hongjun Zhou, Mary Luz Arcila,
Sandie M. Degnan, Bernard M. Degnan, and Kenneth S. Kosik
2 Adaptive Evolution of Voltage-Gated Sodium Channels:
The First 800 Million Years 21
Harold H. Zakon
3 Evolution of Centralized Nervous Systems: Two Schools of
Evolutionary Thought 37
R. Glenn Northcutt
ix
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x / Contents
PART II DEVELOPMENTAL AND ADULT VARIATION
IN NEURAL ORGANIZATION 57
4 Evolving Specialization of the Arthropod Nervous System 61
Erin Jarvis, Heather S. Bruce, and Nipam H. Patel
5 Expansion, Folding, and Abnormal Lamination of the Chick
Optic Tectum After Intraventricular Injections of FGF2 75
Luke D. McGowan, Roula A. Alaama, Amanda C. Freise,
Johnny C. Huang, Christine J. Charvet, and Georg F. Striedter
6 Cortical Evolution in Mammals: The Bane and Beauty of
Phenotypic Variability 91
Leah A. Krubitzer and Adele M. H. Seelke
7 Evolution of Columns, Modules, and Domains in the
Neocortex of Primates 113
H. Kaas
Jon
8 The Remarkable, Yet Not Extraordinary, Human Brain as a
Scaled-Up Primate Brain and Its Associated Cost 127
Suzana Herculano-Houzel
PART III FROM NEURAL CIRCUIT EVOLUTION TO
ADAPTIVE BEHAVIOR 149
9 Homology and Homoplasy of Swimming Behaviors and
Neural Circuits in the Nudipleura (Mollusca, Gastropoda,
Opisthobranchia) 153
James M. Newcomb, Akira Sakurai, Joshua L. Lillvis,
Charuni A. Gunaratne, and Paul S. Katz
10
Shared Developmental and Evolutionary Origins for
Neural Basis of Vocal–Acoustic and Pectoral–Gestural
Signaling 175
Andrew H. Bass and Boris P. Chagnaud
11 Flock or Fight: Neurochemical Signatures of Divergent
To
Life Histories in Sparrows 193
James L. Goodson, Leah C. Wilson, and Sara E. Schrock
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Contents / xi
12
From Chemotaxis to the Cognitive Map: The Function
of Olfaction 211
Lucia F. Jacobs
13
Evolution of Brains and Behavior for Optimal Foraging:
A Tale of Two Predators 229
Kenneth C. Catania
PART IV PHYLOGENY OF HUMAN BRAINS AND
HUMAN MINDS 251
14
Human Brain Evolution: From Gene Discovery to
Phenotype Discovery 253
Todd M. Preuss
15
Integration of Faces and Vocalizations in Ventral Prefrontal
Cortex: Implications for the Evolution of Audiovisual Speech 273
Lizabeth M. Romanski
16
Math, Monkeys, and the Developing Brain 293
Jessica F. Cantlon
17 Hierarchical Model of the Evolution of Human Brain
A
Specializations 313
H. Clark Barrett
Epilogue 335
References 337
Index 397
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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 cher-
ish and preserve for the future. Two urgent challenges, and opportunities,
for 21st-century science are to gain deeper insights into the evolutionary
processes that foster biotic diversity, and to translate that understanding
into workable solutions for the regional and global crises that biodiver-
sity currently 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 biotechnology. 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 In the Light of Evolution (ILE) series is to pro-
mote 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 explores
xiii
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xiv / Preface to the In the Light of Evolution Series
evolutionary perspectives on a particular biological topic that is scientifi-
cally intriguing but also has special relevance to contemporary societal
issues or challenges. Individually and collectively, the ILE series aims
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 Dobzhansky’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 (January 2007)
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Preface to
In the Light of Evolution, Volume VI:
Brain and Behavior
T
his book is the outgrowth of the Arthur M. Sackler Colloquium
“Brain and Behavior,” which was sponsored by the National Acad-
emy of Sciences on January 20–21, 2012, at the Academy’s Arnold
and Mabel Beckman Center in Irvine, CA. It is the sixth in a series of
Colloquia under the general title “In the Light of Evolution.” The first five
books in this series were titled Adaptation and Complex Design (Avise and
Ayala, 2007), Biodiversity and Extinction (Avise et al., 2008), Two Centuries
of Darwin (Avise and Ayala, 2009), The Human Condition (Avise and Ayala,
2010), and Cooperation and Conflict (Strassmann et al., 2011).
In On the Origin of Species by Means of Natural Selection, Darwin (1859)
barely mentioned the brain. Only in The Descent of Man, and Selection in
Relation to Sex, published in 1871, did Darwin emphasize that the human
nervous system, like any other organ system, must have evolved. Even so,
Darwin himself wrote little on the brain. Instead, Darwin asked his good
friend T. H. Huxley to write a chapter for the second edition of The Descent
of Man, and Selection in Relation to Sex that dealt specifically with human
brain evolution. In this chapter, Huxley laid to rest Richard Owen’s ear-
lier argument that human brains are outliers among mammalian brains.
Instead, Huxley argued that our brains resemble the brains of other apes
in all fundamental respects. He even downplayed the greater size of
human brains, noting that brain size is quite variable among humans.
Importantly, Huxley did not deny that our brains must somehow differ
from the brains of other apes, for he could see no other way to explain
our unique cognitive capacities, most notably language. However, Huxley
xv
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xvi / Preface to In the Light of Evolution, Volume VI
(1863b) postulated that the differences that set our brains apart are not
apparent in gross dissections (Cosans, 1994; Desmond, 1994; Gross, 1998;
Striedter, 2005).
Of course, in the days of Darwin and Huxley, the only methods avail-
able for studying large brains were gross dissections or, for functional
analyses, gross brain lesions. It was only in the late 1880s that Ramón y
Cajal focused neuroanatomy onto structural details by applying Golgi’s
famous staining method to the nervous systems of various species (De
Carlos and Borrell, 2007). Similarly, techniques for electrical recording of
neural activity and brain stimulation were just starting to be developed
in the 1870s by Richard Canton, Eduard Hitzig, and many other pioneers
(Ferrier, 1886; Young, 1970; Niedermeyer, 2005). Aside from these techni-
cal constraints, neurobiological knowledge was limited in Darwin’s day
to relatively few species. In particular, ape brains were rare in England at
the time, because they could only be obtained through research expedi-
tions to Africa. Gorillas, for example, were not even discovered by Western
scientists until Richard Owen (1859) described them and their brains in
the late 1850s.
Since that dawn of evolutionary neuroscience, the arsenal of meth-
ods and panoply of data relevant to brain evolution have expanded tre-
mendously. Intracellular and extracellular chronic recording techniques,
immunohistochemistry, axon tracing, and excitotoxic brain lesions are
just a few of the many methods that revolutionized our understanding of
brain structure and function. Obviously, neuroscience has also been trans-
formed by molecular methods that Darwin could not have envisioned.
Researchers can now compare gene sequences and gene expression pat-
terns across species. They can also test causal hypotheses about how genes
control neural development, brain function, and, ultimately, behavior.
Collectively, these methods make it possible to compare across species not
just individual structures, such as genes or brain regions, but molecular
interactions, developmental processes, and intriguing behaviors. Finally,
the range of species studied by comparative neurobiologists now includes
not just a few model species but a broad assemblage of vertebrates and,
increasingly, invertebrates (Strausfeld, 2012).
These methodological advances have unleashed a flood of data rel-
evant to brain evolution. Fortunately, conceptual advances in data analysis
kept pace. Particularly important have been breakthroughs in phyloge-
netic systematics, which have yielded more elaborate and detailed phy-
logenetic trees, or cladograms, and sophisticated statistical methods for
evaluating phylogenetic correlations between various traits (Nunn, 2011).
Cladists have also developed a rigorous methodology for distinguishing
similarities caused by homology from those similarities that resulted
from independent evolution (Northcutt, 1984; Nieuwenhuys, 1994a; Pritz,
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Preface to In the Light of Evolution, Volume VI / xvii
2005). With these methodologies, comparative biologists can begin to infer
the evolutionary processes that created the complex tapestry of neurologi-
cal systems in extant species.
Because the field of evolutionary neuroscience now includes a vast
array of different approaches, data types, and species, how can one select
from this diversity a set of 17 chapters that represent the field adequately?
The task seems Herculean, if not Sisyphean. Confronted with this chal-
lenge, we opted for an eclectic approach. Thus, we here gather 17 chapters
that represent a broad assortment of contemporary research in evolution-
ary neurobiology.
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