Table Of ContentFOREWORD
It is amazing to what great extent variation in natural populations has been
neglected in the study of evolution. Amazing because natural selection would be
meaningless without variation. This conclusion gave me the idea to consider the
production of variation as a step in the process of natural selection. Periods of high
phenotypic variation (as in the Pre-Cambrian, Cambrian) have alternated at other
geological periods with periods of relative stasis. As natural selection is active at all
periods, it would seem that evolutionary change depends more on the availability
of variation than that of selection.
The discovery by Monod and Jacob that there are regulatory genes in addition
to the structural genes has shed important light on the activity of genes. What, in
turn, regulates the regulatory genes? What environmental conditions favor high
variability? What others favor stability? Why has no geological period in the last
400 million years been able to produce such a reckless invention of new structural
types as the Pre-Cambrian, Cambrian times? Can high variability by itself be favored
by selection because it increases the probability of the production of unusual charac-
tercombinations? Why are alterations of rapid and stagnant evolution (punctuated
equilibria) so frequent in many phyletic lineages? Only the study of variation will
enable us to explain why there are so many extraordinary productions like the
peacock tail or certain Pre-Cambrian genes, which on first sight, would seem
difficult to explain as the product of natural selection.
In short, variation is an endless source of challenging questions.
Ernst Mayr
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CONTRIBUTORS
ALEXANDER V. BADYAEV, Department of Ecology and Evolutionary Biology,
University of Arizona, Tucson, Arizona, USA
AARON M. BAUER, Department of Biology, Villanova University, Villanova,
Pennsylvania, USA
PETER J. BOWLER, School of Anthropological Studies, Queen’s University,
Belfast, Northern Ireland, United Kingdom
JEVON JAMES YARDLEY BROWN, Joint Injury and Arthritis Group, University of
Calgary, Calgary, Alberta, Canada
THEODORE M. COLE III, Department of Basic Medical Science, School of
Medicine, University of Missouri-Kansas City, Kansas City, Missouri, USA
IAN DWORKIN, Department of Genetics, North Carolina State University,
Raleigh, North Carolina, USA
REBECCA Z. GERMAN, Department of Physical Medicine and Rehabilitation,
Johns Hopkins Hospital, Baltimore, Maryland, USA
BRIAN K. HALL, Department of Biology, Dalhousie University, Halifax, Nova
Scotia, Canada
BENEDIKT HALLGRÍMSSON, Department of Cell Biology and Anatomy, Joint
Injury and Arthritis Research Group, The Bone and Joint Institute, University of
Calgary,Calgary, Alberta, Canada
ARY A. HOFFMANN, Centre for Environmental Stress and Adaptation Research,
Department of Genetics, University of Melbourne, Parkville, Victoria, Australia
DONNA CARLSON JONES, Department of Physical Medicine and Rehabilitation,
Johns Hopkins Hospital, Baltimore, Maryland, USA
xix
xx
Contributors
CHRISTIAN PETER KLINGENBERG, Faculty of Life Sciences, The University of
Manchester, Manchester, United Kingdom
ELLEN LARSEN, Department of Zoology, University of Toronto, Toronto, Ontario,
Canada
SUBHASH R. LELE, Department of Mathematical and Statistical Science,
University of Alberta, Edmonton, Alberta, Canada
JOHN A. MCKENZIE, Centre for Environmental Stress and Adaptation Research,
Department of Genetics, University of Melbourne, Parkville, Victoria, Australia
DANIEL W. MCSHEA, Biology Department, Duke University, Durham, North
Carolina, USA
LAUREN ANCEL MEYERS, Section of Integrative Biology, University of Texas at
Austin, Austin, Texas, USA
A. RICHARD PALMER, Systematics and Evolution Group, Department of
Biological Sciences, University of Alberta, Edmonton, Alberta, Canada; Bamfield
Marine Sciences Centre, Bamfield, British Columbia, Canada
DAVID M. PARICHY, Department of Biology, University of Washington, Seattle,
Washington, USA
JOAN T. RICHTSMEIER, Department of Anthropology, The Pennsylvania State
University, University Park, Pennsylvania, USA; Center for Craniofacial Development
and Disorders, The Johns Hopkins University, Baltimore, Maryland, USA
DEREK A. ROFF, Department of Biology, University of California, Riverside,
California, USA
V. LOUISE ROTH, Biology Department, Duke University, Durham, North
Carolina, USA
ANTHONY P. RUSSELL, Department of Biological Sciences, University of Calgary,
Calgary, Alberta, Canada
SONIA E. SULTAN, Biology Department, Wesleyan University, Middletown,
Connecticut, USA
SAMUEL SHOLTIS, Department of Anthropology, Pennsylvania State University,
University Park, Pennsylvania, USA
STEPHEN C. STEARNS, Department of Ecology and Evolutionary Biology, Yale
University, New Haven, Connecticut, USA
LEIGH VAN VALEN, Department of Ecology and Evolution, University of Chicago,
Chicago, Illinois, USA
xxi
Contributors
KENNETH M. WEISS, Department of Anthropology, Pennsylvania State
University, University Park, Pennsylvania, USA
KATHERINE E. WILLMORE, Department of Medical Sciences, University of
Calgary, Health Sciences Centre, Calgary, Alberta, Canada
MIRIAM LEAH ZELDITCH, Museum of Paleontology, University of Michigan,
Ann Arbor, Michigan, USA
ACKNOWLEDGMENTS
This book represents the collaborative effort of many people. The editors would
like to thank the contributors for accepting the invitation to contribute this volume
and for the work and intellectual effort that went into writing each contribution.
We appreciate that the time spent on these chapters is time not spent on some-
thing else and we hope that the final product has made that investment worth-
while. We would also like to thank Chuck Crumly for soliciting the original book
proposal from us and for his role in the early stages of this book. We are grateful
to Suzanne Harrison for kindly giving us permission to publish her father’s fore-
word to our book, which he so generously wrote, as it turned out, only shortly
before his death. We thank Kelly Sonnack, Lisa Royse, and Nancy Maragioglio for
all of their hard work and professionalism and for keeping the production on track.
We are grateful for the excellent assistance provided by Courtney Rippin, Wendy
Swales, and Mitzi Murray at different times during this process.
Finally, we would both like to thank our spouses Leigh (BH) and June (BKH)
for their support and encouragement and for patiently tolerating all of the imposi-
tions and inconveniences of academic life and thus allowing us to collaborate on
projects such as this.
Benedikt Hallgrímsson
Brian K. Hall
1
CHAPTER
Variation and Variability:
Central Concepts in Biology
BENEDIKT HALLGRÍMSSON∗ AND BRIAN K. HALL†
∗
Department of Cell Biology and Anatomy, Joint Injury and Arthritis Research Group,
University of Calgary, Calgary, Alberta, Canada
†Department of Biology, Dalhousie University, Halifax, Nova Scotia, Canada
Phenotypic variation is the raw material for natural selection, yet
a century after Darwin, it is an almost unknown subject.
Leigh Van Valen, 1974
Van Valen’s assessment of our understanding and appreciation of phenotypic varia-
tion is only slightly less true today than it was 30 years ago. Yet, variation is a central
topic, both conceptually and historically in evolutionary biology. Phenotypic varia-
tion was Darwin’s fundamental observation. Indeed, the first two chapters of On the
Origin of Species deal explicitly with variation. Variation within and among species
has certainly been as central to the thinking of Ernst Mayr (1963) as it was to the
thinking of Sewall Wright (1968), two of the fathers of the modern synthesis.
However, the study of variability or the propensity to vary, with few exceptions
(Bateson, 1894; Schmalhausen, 1949; Waddington, 1957), has remained peripheral
to study of the mechanisms of evolutionary change at any level of the biological hier-
archy. Although implicit in virtually all research in the biological sciences, whether
one is seeking understanding at the genetic, developmental, organismal, species,
population, or ecologic/community levels, variation is seldom treated as a subject in
and of itself. The perception of this major gap prompted the present volume.
Variation is an extremely broad topic, and a modern treatment of this subject is
not possible without a thematic focus. In this volume, we focus on the determinants
and constraints on the generation of variation. We address this theme through
both a hierarchical treatment and integrative approaches that point toward new
directions of research.
Although it is not overtly noted, the book is organized thematically, beginning with
Peter Bowler’s overview of the historical and conceptual foundations of the topic.
Variation
Copyright 2005, Elsevier Inc. All rights reserved. 1
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Benedikt Hallgrímsson and Brian K. Hall
We chose to solicit an historical perspective for this chapter because of the deep
roots of the conceptualization of variation, many of which precede Darwin’s
synthesis. Bowler also deals with alternate theories of variation, thus providing a
broader historical perspective against which later studies can be viewed.
The second section (Chapters 3–5) deals with the analysis of variation. The ana-
lytical issues deal with ways to compare and separate size and shape in biological
structures. The field is surprisingly complex, and there are several methodologic
approaches. Leigh Van Valen’s treatment of approaches to variation is a classic that
must be read by all serious investigators in this area (Van Valen, 1978). Current
approaches include the geometric morphometric school as well as Euclidean
distance matrix analysis. The methodologic debates are well beyond the scope of
this volume, but readers interested in exploring these issues will find pertinent
chapters in a forthcoming volume by Slice (2005).
The chapter by Joan Richtsmeier et al. lays out a recently developed and parti-
cularly useful approach for the analysis of variation. Their approach has been
successfully used for the analysis of variability in dysmorphology in both mice and
humans (Richtsmeier et al.,2000). The contribution by Jones and German deals with
the conceptual and methodologic issues that relate to the ontogenetic analysis of bio-
logical variation. Important aspects of variation can only be seen through ontogenetic
analyses, and this is often overlooked. Jones and German deal with issues such as
appropriate units of analysis and the levels at which variation can be measured.
The third section (Chapters 6–12) deals with the genetic and developmental
determinants of the propensity to vary. The chapter by Lauren Myers deals with con-
straints on the propensity to vary at the molecular and genomic level, particularly in
RNA. Her treatment includes mutational constraints and their evolution, the evolu-
tion of epistatic constraints, and modularity at the molecular level. A particular focus
of her approach is the interaction of constraint and modularity in limiting and
enabling the generation of molecular level variation.
Ellen Larsen’s chapter focuses on the role of intrinsic developmental variation,
by which she means variation that originates inherently in developmental processes
and translates to heritable phenotypic variation. Her chapter essentially takes a
broad view of the origin and role of variation that arises from emergent properties
of complex developmental systems.
Chapter 8 by Dworkin focuses on canalization and the limitation of variation by
development. Dworkin outlines different frameworks for the study of canalization.
He relates canalization to reaction norms, and he devotes considerable thought
and insight to the issue of how canalizing mechanisms influence the translation of
genetic into phenotypic variation.
Ary Hoffman and John McKenzie take a genetic approach to the analysis of
canalization. They discuss the evidence for the existence of specific genetic factors,
such as heat shock proteins, which modulate variability in phenotypic traits in
natural populations. Their work adds another layer to the hierarchy, that of
interaction between genetic and environmental factors.
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Chapter 1 Variation and Variability: Central Concepts in Biology
In the tenth chapter, Willmore and Hallgrímsson review the developmental
basis for phenotypic variation that derives from developmental instability. This
chapter takes a hierarchical and integrative approach to the developmental mech-
anisms from which developmental instability may arise. In particular, this chapter
devotes thought to the issue of specific mechanisms versus diffuse emergent prop-
erties as the basis for variation in developmental stability, a theme that emerges in
several other chapters such as that of Sultan and Stearns.
Chris Klingenberg continues the developmental and integrative theme from the
previous chapter with a discussion of modularity and evolvability and develop-
mental constraints. His conceptual work builds on the foundation laid by Wagner
and others (Wagner and Altenberg, 1996). He presents methods for discriminating
modularity caused by direct and indirect developmental and genetic interaction
and discusses the implications of the finding based on these methods for evolv-
ability of developmental systems.
The final chapter in this section, by Miriam Zelditch, takes an epigenetic view of
the developmental regulation of variability. Focusing on the role of the mechanicalenvi-
ronment and particularly muscle–bone interactions, Zelditch uses morphometric
techniques to test hypotheses about the mechanisms responsible for the ontoge-
netic patterning of phenotypic variation. Although morphometri-cally based, her
perspective is overtly developmental in that the focus is on the developmental
mechanisms that generate or remove variance throughout ontogeny.
Following our hierarchical theme, the fourth section (Chapters 13–15) deals
with environmental determinants of variation as well as genotype–environment
interactions. The theoretical thrust of this section is to place the generation of vari-
ation into ecologic contexts. Alex Badayev’s chapter deals with the relationship
between stress, developmental integration, and both phenotypic and genetic vari-
ability. Two major themes of his contribution are that stress-induced increases in
variation are structured by developmental systems and that the resulting pattern
can have evolutionary consequences.
In the next chapter, Sonia Sultan and Steve Stearns review the vast area of
phenotypic plasticity and the norm of reaction and lay out new directions of
research in this vibrant area. The norm of reaction concept is central to the under-
standing of the interaction of genetic and environmental factors in the generation
of phenotypic variation. This is true both historically, through Schmalhausen’s
work, and conceptually in current work in the area. Despite the large amount of
work in this area, the relationship between norms of reaction and canalization is
underappreciated, a point that is developed in this chapter.
The discussion of phenotypic plasticity is further elaborated in the context
of life history by the following chapter by Roff. This chapter emphasizes the role
of predictable versus stochastic environments in affecting patterns of phenotypic
plasticity over life history using a population-genetic framework. Roff reviews the
current population genetic concepts related to the central issues of the mainte-
nance and reduction of genetic variance and relates these to life-history evolution.
4
Benedikt Hallgrímsson and Brian K. Hall
The fifth section (Chapters 16–19) deals with comparative and phylogenetic
approaches to the study of variation. Obviously, this is a vast field encompassing
many areas of study and perspectives. The chapters solicited address four impor-
tant topics within this vast area. These are variation in relation to organismal sym-
metry, structure and function, the evolution of developmental and morphologic
complexity, and macroevolution. This selection of topics is not intended to be
comprehensive or exhaustive. Rather, these are areas of important intersection
between the study of the processes that underlie variation and large-scale evolu-
tionary patterns.
Rich Palmer’s chapter entitled “Antisymmetry” deals with variation across
planes of symmetry and evolution of asymmetric phenotypes. This is an interest-
ing area because the evolution of directional asymmetry such as that seen in floun-
der heads or in the human heart involves the evolution of heritable variation
across planes of symmetry from developmental systems in which, presumably,
such variation does not exist. Palmer’s argument, supported by hundreds of
examples, is that antisymmetry, or the tendency for negative covariation across
planes of symmetry, is a critical intermediary step in the evolution of asymmetry
phenotypes.
Tony Russell and Aaron Bauer tackle the ambitious topic of how variation in
structure relates to variation in function. They review different approaches to this
issue, including the advantages and limitations of natural (in situ) versus laboratory
(ex situ) studies. They advocate an approach that combines these two kinds of
studies and point out that the degree to which structure–function relationships
can ever be worked out depends critically on the level of detail specified by the
theoretical model.
Dan McShea tackles the issue of how long-term evolutionary trends in devel-
opmental complexity, developmental buffering, and the generation of variability
interact. He discusses the selective forces and trade-offs that may determine the
overall evolutionary trend and argues that there is a long-term increase in internal
variance that goes along with a tendency for complexity to increase. This chapter
builds on his extensive work on complexity and evolution (McShea, 1996), adding
an explicit consideration of the role of variability.
Having begun with a historical perspective and an analysis of current concepts,
the sixth section (Chapters 20–22) looks to the future in dealing with new direc-
tions of research relating to variation and variability. This section explores impor-
tant intersections and integrations between disciplines, principally evo-devo,
phenogenetics, and evolutionary theory.
In the first chapter of this section, David Parichy argues that, despite the strong
history of population thinking in evolutionary biology since Darwin, developmental
biology has remained essentially typologic in approach. He argues that this will
finally change in coming years as developmental biologists are forced to turn their
attention to issues of variability by addressing the remaining large issues that face
5
Chapter 1 Variation and Variability: Central Concepts in Biology
that field. This includes understanding the developmental genetic basis for variation
among evolutionary lineages, among closely related species, and phenotypic
variation within species. The latter topic, he argues, important for both evolutionary
and biomedical research, will focus on how developmental systems translate
genetic to phenotypic variation. In this area, canalization is a central concern.
In the second chapter, Sholtis and Wiess lay out the theoretical perspective of
phenogenetics. Their perspective focuses on the complexities of the genotype to
phenotype relationship. Arguing, like Minelli (2003) and others, that modern
developmental biology is overly “gene centric,” they point out that the compli-
cations introduced by gene regulation, epigenetic factors, and the environmental
context of development create a many-to-many relationship between genotype and
phenotype. The relationship is further complicated by the fact that the genetic
basis for development can and does evolve without phenotypic change and by
developmental stability. None of this is individually contentious or novel, but their
overall perspective is in that they argue that the implications of these compli-
cations are that the gene-driven paradigm of modern developmental genetics is
fundamentally flawed. They argue for a more phenotype-focused approach and
explicit consideration of these complications in experimental investigation of the
developmental basis for evolutionary change and the developmental-genetics of
human disease.
A theme that emerges from the approaches that authors have taken is the
distinction between variation and variability and an emphasis on the latter. Günter
Wagner et al.(1997) have made this distinction explicitly, defining variation as the
set of observed differences and variability as the tendency of a system to generate
differences. The distinction, therefore, is one of pattern versus process. Although
they were not explicitly asked to do so, the authors in this volume by and large
chose to focus on process and, therefore, on variability. Current questions about
variability deal with factors that enhance or limit the tendency for biological
systems to exhibit variation at the different levels of the biological hierarchy.
A common theme that emerges through the chapters by Larsen, Roth, McShea,
and Russell and Bauer is the phylogenetic diversity in the processes that influence
variability from variation in molecular, developmental, and functional constraints.
Canalization is another central theme that emerges through many of the chapters.
As a conceptual framework for understanding variability, Waddington’s concept of
canalization is clearly pivotal. Nearly all of the chapters touch on canalization in
one form or another. In particular, the chapters by Larsen, Dworkin, Hoffman and
McKenzie, Willmore, and Parichy as well as our own chapter deal explicitly with
canalization, and this arose without instruction or encouragement from the editors
despite our own obvious interest in the subject. In the final chapter, we attempt to
pull together some of these themes to define a theoretical framework for the study
of phenotypic variability at the level of the organismal phenotype. Understanding
the mechanisms by which developmental systems buffer, augment, or structure
