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Variation and Variability
CHAPTER
1
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 variation 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 variation 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 hierarchy. 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
2
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 analytical 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 particularly 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 biological 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 constraints on the propensity to vary at the molecular and genomic level, particularly in RNA. Her treatment includes mutational constraints and their evolution, the evolution 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.
Chapter 1 Variation and Variability: Central Concepts in Biology
3
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 mechanisms from which developmental instability may arise. In particular, this chapter devotes thought to the issue of specific mechanisms versus diffuse emergent properties 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 developmental 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 evolvability 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 mechanical environment and particularly muscle–bone interactions, Zelditch uses morphometric techniques to test hypotheses about the mechanisms responsible for the ontogenetic 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 variation into ecologic contexts. Alex Badayev’s chapter deals with the relationship between stress, developmental integration, and both phenotypic and genetic variability. 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 understanding 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 maintenance 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 important topics within this vast area. These are variation in relation to organismal symmetry, 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 evolutionary patterns. Rich Palmer’s chapter entitled “Antisymmetry” deals with variation across planes of symmetry and evolution of asymmetric phenotypes. This is an interesting area because the evolution of directional asymmetry such as that seen in flounder 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 developmental 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 directions of research relating to variation and variability. This section explores important 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
Chapter 1 Variation and Variability: Central Concepts in Biology
5
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 complications 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 complications 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
6
Benedikt Hallgrímsson and Brian K. Hall
phenotypic variation is central to understanding the relationship between genetic and phenotypic variation. The complexities of that relationship, after all, are principally what make the study of development so relevant to understanding evolutionary processes. A central motivation behind much of the work in this book is the need for a coherent theory of phenotypic variation. The most fundamental task is a coherent framework for relating genetic to phenotypic variation. This would be a trivial task if genetic variation mapped directly onto phenotypic variation as is often assumed in population genetic models. We argue that developmental processes are the level at which one can understand how genetic variation is translated to phenotypic variation within and among species. Experimental developmental biology, complex systems modeling, and bioinformatics all have important roles to play for the theory. Morphometrics also have an important role by providing methods to quantify phenotypic variation in shape and size. A theory of phenotypic variation must also be firmly grounded in population genetics and must be able to relate selection, gene flow patterns, population structure and size, geographic range, and spatiotemporal environmental variation to the developmentally based expression of phenotypic variation. Finally, a theory of phenotypic variation must draw on both developmental biology and population genetics to provide a framework to understand how developmental systems influence the dynamics of macroevolutionary change. These tasks situate variation centrally within the evolutionary developmental biological paradigm and thus return the concept to the forefront of evolutionary thought. This volume appears at a time when the synthesis of developmental and evolutionary biology (evo-devo) is reaching a mature phase. Indeed, the prospect for a new synthesis bridging genetics, development, ecologic, and evolutionary biology now seems more likely than at any time in the past. Understanding the significance of both variation and variability will be crucial to this emerging synthesis. One trend that may contribute to increased understanding and appreciation of variation and variability is the increased focus on systems (as opposed to gene or developmental process) level understanding of development, which is enabled by the ongoing growth and maturation of bioinformatics and computational biology. Recent work by Siegal and Bergman is an example of early contributions to this emerging area (Siegal and Bergman, 2002; Bergman and Siegal, 2003). This area is only tangentially treated here because the subject of modeling biological systems to understand the origins of variation would require a separate volume. The goal here is to bring together a diversity of treatments of variation and variability at multiple levels and thus situate the role of variability within this broad emerging synthesis. Only three other volumes have attempted a broad treatment of phenotypic variation since Darwin: William Bateson’s Materials for the Study of Variation (Bateson, 1894), Sewall Wright’s Variability Within and Among Natural Populations (1984), and Yablokov’s Variability in Mammals (1966). This volume aims to
Chapter 1 Variation and Variability: Central Concepts in Biology
7
examine the concept of variation through the lenses created by different levels and areas of research. The processes related to phenotypic variation emerge from the complexities of interaction among and within different levels of organization. For this reason, a hierarchical approach is critical. We believe that the resulting treatment is unique in juxtaposing a series of perspectives with a transdisciplinary approach that seeks to contextualize variation as a foundational concept in biology.
REFERENCES Bateson, W. (1894). Materials for the Study of Variation Treated with Especial Regard to Discontinuity in the Origin of Species (reprinted in 1992). Baltimore and London: Johns Hopkins University Press. Bergman, A., and Siegal, M. L. (2003). Evolutionary capacitance as a general feature of complex gene networks. Nature 424(6948), 549–552. Mayr, E. (1963). Animal Species and Evolution. Cambridge, MA: Belknap Press. McShea, D. W. (1996). Metazoan complexity and evolution: Is there a trend? Evolution 477–492. Minelli, A. (2003). The Development of Animal Form: Ontogeny, Morphology, and Evolution. Cambridge, England: Cambridge University Press. Richtsmeier, J. T., Baxter, L. L., and Reeves, R. H. (2000). Parallels of craniofacial maldevelopment in Down syndrome and Ts65Dn mice. Development Dynamics 217(2), 137–145. Schmalhausen, I. I. (1949). Factors of Evolution. Chicago: University of Chicago Press. Siegal, M. L., and Bergman, A. (2002). Waddington’s canalization revisited: Developmental stability and evolution. Proceedings of the National Academy of Science USA 99(16), 10528–10532. Slice, D. E., ed. (2005). Modern Morphometrics in Physical Anthropology. New York: Kluwer. Van Valen, L. M. (1978). The statistics of variation. Evolutionary Theory 433–443. Waddington, C. H. (1957). The Strategy of the Genes. New York: MacMillan Company. Wagner, G. P., and Altenberg, L. (1996). Complex adaptations and the evolution of evolvability. Evolution 50, 967–976. Wagner, G. P., Booth, G., and Bagheri-Chaichian, H. (1997). A population genetic theory of canalization. Evolution 51(2), 329–347. Wright, S. (1968). Evolution and the Genetics of Populations: A Treatise. Chicago: University of Chicago Press. Vol. 4. Wright, S. (1984). Evolution and the Genetics of Populations, Volume 4: Variability within and among Natural Populations. Chicago: University of Chicago Press. Yablokov, A. V. (1966). Variability of Mammals. New Delhi, India: Amerind.
1
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 variation 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 variation 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 hierarchy. 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
2
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 analytical 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 particularly 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 biological 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 constraints on the propensity to vary at the molecular and genomic level, particularly in RNA. Her treatment includes mutational constraints and their evolution, the evolution 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.
Chapter 1 Variation and Variability: Central Concepts in Biology
3
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 mechanisms from which developmental instability may arise. In particular, this chapter devotes thought to the issue of specific mechanisms versus diffuse emergent properties 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 developmental 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 evolvability 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 mechanical environment and particularly muscle–bone interactions, Zelditch uses morphometric techniques to test hypotheses about the mechanisms responsible for the ontogenetic 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 variation into ecologic contexts. Alex Badayev’s chapter deals with the relationship between stress, developmental integration, and both phenotypic and genetic variability. 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 understanding 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 maintenance 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 important topics within this vast area. These are variation in relation to organismal symmetry, 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 evolutionary patterns. Rich Palmer’s chapter entitled “Antisymmetry” deals with variation across planes of symmetry and evolution of asymmetric phenotypes. This is an interesting area because the evolution of directional asymmetry such as that seen in flounder 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 developmental 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 directions of research relating to variation and variability. This section explores important 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
Chapter 1 Variation and Variability: Central Concepts in Biology
5
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 complications 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 complications 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
6
Benedikt Hallgrímsson and Brian K. Hall
phenotypic variation is central to understanding the relationship between genetic and phenotypic variation. The complexities of that relationship, after all, are principally what make the study of development so relevant to understanding evolutionary processes. A central motivation behind much of the work in this book is the need for a coherent theory of phenotypic variation. The most fundamental task is a coherent framework for relating genetic to phenotypic variation. This would be a trivial task if genetic variation mapped directly onto phenotypic variation as is often assumed in population genetic models. We argue that developmental processes are the level at which one can understand how genetic variation is translated to phenotypic variation within and among species. Experimental developmental biology, complex systems modeling, and bioinformatics all have important roles to play for the theory. Morphometrics also have an important role by providing methods to quantify phenotypic variation in shape and size. A theory of phenotypic variation must also be firmly grounded in population genetics and must be able to relate selection, gene flow patterns, population structure and size, geographic range, and spatiotemporal environmental variation to the developmentally based expression of phenotypic variation. Finally, a theory of phenotypic variation must draw on both developmental biology and population genetics to provide a framework to understand how developmental systems influence the dynamics of macroevolutionary change. These tasks situate variation centrally within the evolutionary developmental biological paradigm and thus return the concept to the forefront of evolutionary thought. This volume appears at a time when the synthesis of developmental and evolutionary biology (evo-devo) is reaching a mature phase. Indeed, the prospect for a new synthesis bridging genetics, development, ecologic, and evolutionary biology now seems more likely than at any time in the past. Understanding the significance of both variation and variability will be crucial to this emerging synthesis. One trend that may contribute to increased understanding and appreciation of variation and variability is the increased focus on systems (as opposed to gene or developmental process) level understanding of development, which is enabled by the ongoing growth and maturation of bioinformatics and computational biology. Recent work by Siegal and Bergman is an example of early contributions to this emerging area (Siegal and Bergman, 2002; Bergman and Siegal, 2003). This area is only tangentially treated here because the subject of modeling biological systems to understand the origins of variation would require a separate volume. The goal here is to bring together a diversity of treatments of variation and variability at multiple levels and thus situate the role of variability within this broad emerging synthesis. Only three other volumes have attempted a broad treatment of phenotypic variation since Darwin: William Bateson’s Materials for the Study of Variation (Bateson, 1894), Sewall Wright’s Variability Within and Among Natural Populations (1984), and Yablokov’s Variability in Mammals (1966). This volume aims to
Chapter 1 Variation and Variability: Central Concepts in Biology
7
examine the concept of variation through the lenses created by different levels and areas of research. The processes related to phenotypic variation emerge from the complexities of interaction among and within different levels of organization. For this reason, a hierarchical approach is critical. We believe that the resulting treatment is unique in juxtaposing a series of perspectives with a transdisciplinary approach that seeks to contextualize variation as a foundational concept in biology.
REFERENCES Bateson, W. (1894). Materials for the Study of Variation Treated with Especial Regard to Discontinuity in the Origin of Species (reprinted in 1992). Baltimore and London: Johns Hopkins University Press. Bergman, A., and Siegal, M. L. (2003). Evolutionary capacitance as a general feature of complex gene networks. Nature 424(6948), 549–552. Mayr, E. (1963). Animal Species and Evolution. Cambridge, MA: Belknap Press. McShea, D. W. (1996). Metazoan complexity and evolution: Is there a trend? Evolution 477–492. Minelli, A. (2003). The Development of Animal Form: Ontogeny, Morphology, and Evolution. Cambridge, England: Cambridge University Press. Richtsmeier, J. T., Baxter, L. L., and Reeves, R. H. (2000). Parallels of craniofacial maldevelopment in Down syndrome and Ts65Dn mice. Development Dynamics 217(2), 137–145. Schmalhausen, I. I. (1949). Factors of Evolution. Chicago: University of Chicago Press. Siegal, M. L., and Bergman, A. (2002). Waddington’s canalization revisited: Developmental stability and evolution. Proceedings of the National Academy of Science USA 99(16), 10528–10532. Slice, D. E., ed. (2005). Modern Morphometrics in Physical Anthropology. New York: Kluwer. Van Valen, L. M. (1978). The statistics of variation. Evolutionary Theory 433–443. Waddington, C. H. (1957). The Strategy of the Genes. New York: MacMillan Company. Wagner, G. P., and Altenberg, L. (1996). Complex adaptations and the evolution of evolvability. Evolution 50, 967–976. Wagner, G. P., Booth, G., and Bagheri-Chaichian, H. (1997). A population genetic theory of canalization. Evolution 51(2), 329–347. Wright, S. (1968). Evolution and the Genetics of Populations: A Treatise. Chicago: University of Chicago Press. Vol. 4. Wright, S. (1984). Evolution and the Genetics of Populations, Volume 4: Variability within and among Natural Populations. Chicago: University of Chicago Press. Yablokov, A. V. (1966). Variability of Mammals. New Delhi, India: Amerind.