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Developmental constraints and patterns: some pertinent distinctions
J. theor. Biol. (1995) 173, 231–240
Developmental Constraints and Patterns: Some Pertinent Distinctions D R Department of Philosophy, University of Wyoming, Laramie, WY 82071-3392, U.S.A. (Received on 2 December 1993, Accepted in revised form on 29 November 1994)
This paper remedies some of the conceptual ambiguity in the union of evolution and development by explicating two key concepts in this disciplinary integration: that of a developmental constraint on evolution and of a developmental pattern or form. The phrases ‘‘developmental pattern’’ and ‘‘developmental constraint’’ often mean quite different things to different people in different theoretical contexts. It is intended that this paper will help clarify thinking about evolution and development by distinguishing between historical/ahistorical, local/universal and passive/active senses of these terms and by suggesting some expressions to help stabilize and clarify usage.
such as Maynard Smith et al. (1986), Mayo (1983) and Thomson (1988), attempt to unify development and evolution without challenging the neo-Darwinian paradigm; others, such as Kauffman (1993), Buss (1987) and Gould (1977), see shortcomings with neo-Darwinism but still operate within a neoDarwinian framework; while others still, such as Goodwin (1984), Salthe (1993) and Wolpert (1983) envisage a union of development and evolution that overthrows many neo-Darwinian assumptions. These different perspectives on development and evolution, in turn, have generated very different interpretations of some key concepts in the union of development and evolution. As a result, those people who employ these concepts may be ‘‘talking past’’ each other since they may have very different interpretations of the same terms and ideas. This paper attempts to remedy some of this ambiguity by explicating two key concepts in this new union: that of a developmental constraint on evolution (Kauffman,1983; Mayo, 1983; Wolpert, 1983; Maynard Smith et al., 1986; Thomson, 1988) and that of a developmental pattern (Gould & Lewtonin, 1979; Holder, 1983; Buss, 1987; Arthur, 1988; Atkinson, 1992; Salthe 1993). Although many biologists employ these concepts in their work, not all biologists understand these concepts in the same way: the phrases ‘‘developmental pattern’’ and ‘‘developmental
1. Introduction In the last two decades developmental biologists, evolutionary biologists and some philosophers of biology have sought to resolve some of the outstanding problems in development and evolution by forging a ‘‘new’’† union between the study of development and the study of evolution (Gould, 1977; Alberch, 1982; Bonner, 1982; Mayo, 1983; Wolpert, 1983; Ho & Saunders, 1984; Burian, 1986; Maynard Smith et al., 1986; Wimsatt, 1986; Buss, 1987; Raff & Raff, 1987; Arthur, 1988; Thomson, 1988; Atkinson, 1991; Smith, 1992a, 1992b; Kaufmann, 1993; Salthe, 1993). In this union, evolutionary biologists look to development for important insights into evolution, and developmental biologists look to evolution for important insights into developmental processes and mechanisms. Those who attempt to forge connections between development and evolution often have very different perspectives on biology, and hence very different ideas about the shape this new union should take. Some, † There was an old union between development and evolution founded on Haeckel’s biogenic law, ‘‘ontogeny recapitulates phylogeny’’ (Gould, 1977). According to this view, the developmental patterns of species indicated their phylogenetic relationships in that evolutionary history repeats itself in development. On this old union, developmental biology offered crucial insights into evolution. For more on the fall of the biogenic law and the separation of evolution and development, see Gould (1977). 0022–5193/95/070231+10 $08.00/0
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constraint’’ often mean quite different things to different people in different theoretical contexts. This essay will remedy this problem by distinguishing between the historical/ahistorical, local/universal and passive/ active senses of these terms. In addition, I shall suggest some terminology that may be useful in clarifying and stabilizing usage. Although this analysis is not designed to settle any substantive, empirical questions in development and evolution, I hope it aids the study of development and evolution by helping to clarify the conceptual framework for thinking about the relationship between development and evolution. 2. Development vs. Evolution Most biologists recognize that development and evolution are different processes (Gould, 1977; Gilbert, 1985; Patterson, 1983; Thomson, 1988). If there were no difference, then debates about the union of development and evolution would be misguided, since there would not be two different things to unite. Although this point seems quite trivial and obvious, it is still important. Indeed, most biologists did not distinguish between development and evolution until the 1840s, when they began to appreciate von Baer’s distinction between ontogeny and phylogeny (Patterson, 1983). Although few biologists would dispute the assumption that evolution and development are different processes, not all biologists would agree on how one should characterize this difference. Indeed, one’s perspective on the difference between development and evolution will inevitably be infused with various (often controversial) assumptions about these processes (Patterson, 1983; Salthe, 1993). Nevertheless, for the purposes of this essay I shall offer a fairly standard interpretation of the differences between development and evolution. In noting these differences, I do not intend to point out anything that is not obvious to most biologists, but it is still worth having these points before us. In order to understand the differences, I shall first note some important similarities. First, development and evolution both involve changes over time (Salthe, 1993). In development, immature organisms become adult organisms through differentiation, growth, and learning. In evolution, species (or populations) transform over time, adapt to their environments, or become extinct. Of course, evolution (usually) takes more time than development and evolution and development act on different entities, but both development and evolution bring about changes over time. Second, development
and evolution both produce changes by means of interactions between the genome and the environment. In development, the genome and environment interact to produce an adult organism (Gilbert, 1985); in evolution the interactions between the genome and environment produce changes in gene frequencies through natural selection, random drift or other evolutionary mechanisms (Lewontin, 1974). The differences between development and evolution, then, involve the types of changes that occur, what undergoes change and the ways that changes are produced. Some of the differences between development and evolution are as follows: (i) Developmental changes occur within individual organisms; evolutionary changes occur within or between populations of organisms (Lewontin, 1974; Maynard Smith, 1983; Gilbert, 1985; Thomson, 1988; Salthe, 1993). In development, organisms grow, differentiate, learn and age over time; in evolution the genetic and phenotypic properties of populations, relative abundances and distributions of populations, gene flow between populations and so forth change over time. (ii) Developmental changes occur in one generation; evolutionary changes occur over many generations (Lewontin, 1974; Endler, 1984; Gilbert, 1985). (iii) Evolutionary changes must involve changes in gene distributions in populations; developmental changes need not involve changes in gene distributions (Lewontin, 1974; Endler, 1984; Gilbert 1985). (iv) Development exhibits a high degree of stability despite external and internal disturbances (Waddington, 1957, 1975; Gilbert, 1985; Kauffman, 1993); evolution does not exhibit this same degree of stability. There may of course be some other differences between development and evolution than these, but certainly these four differences need to be mentioned. Given these differences, one may naturally ask how these two processes causally influence each other. From an evolutionary perspective, one might ask how development influences evolution. Ever since Darwin, evolutionary biologists have been aware that development plays an important role in evolution. We find this recognition in Darwin (1859) as well as in the work of Russell (1916), Huxley and de Beer (1934), Morgan (1932), Waddington (1940), Schmaulhausen (1949), Bonner (1958), Rensch (1960) and Monod (1971), among many others. Biologists working within the neo-Darwinian tradition have
employed many concepts to understand development’s role in evolution, including the concept of an epigenetic landscape (Waddington, 1940), the concept of developmental constraints (Maynard Smith et al., 1986) and the concept of phenotypic plasticity (Dobzhansky, 1970). Although these concepts differ considerably in their theoretical context, the basic idea behind these three important concepts is that development can in some way constrain or influence evolution. From a developmental perspective, one may ask how the developmental systems of various species have been shaped by evolution. This study, dubbed ‘‘the evolution of development’’, is unlike most experimentally oriented embryology because it must be comparative and historical in its orientation (Atkinson, 1991). In studying the evolution of development, scientists attempt to understand the evolutionary basis of similarities (i.e. homologies and analogies) and differences among developmental systems (Buss, 1987; Atkinson, 1991). Scientists can also discover whether developmental mechanisms and processes are adaptations to various environmental demands. This type of study also has a long tradition (Gould, 1977; Churchill, 1991). We find a concern for the evolution of development in the work of Darwin (1859), Muller (1864), Haeckel (1866), Conklin (1915), Waddington (1940), Bonner (1958), among many others. Since the study of the evolution of development is comparative in its approach, many different concepts originally employed by comparative embryologists have proven useful in this inquiry. These concepts include the notion of notion of an archetype (Kauffman, 1993), the concept of a morphogenic field (Goodwin & Trainor, 1983) and the concept of a developmental pattern or form (Gould & Lewontin, 1979; Buss, 1987; Atkinson, 1991; Churchill, 1991). Although biologists have used these concepts in many different ways, the main idea behind each of them is that some common patterns manifest themselves in various developmental systems. A rat and a horse are phenotypically and genotypically quite different, but we still can learn that their developmental systems exhibit similar mechanisms and processes.
3. Differences of Interpretation Thus, two of the most crucial concepts in the union of development and evolution are the concepts † Obviously, the existence of developmental patterns is important to the study of development regardless of its evolutionary implications, but in this paper I am only focusing on the bearing such patterns have for the union of evolution and development.
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‘‘developmental constraint’’ and ‘‘developmental pattern’’. The notion of a developmental constraint is important in understanding how development influences evolution; the notion of a developmental pattern is important in understanding the evolution of development.† Having located these key concepts, we also find that different writers give them vastly different interpretations, and that these different interpretations reflect different approaches to the study of evolution and development. For instance, neo-Darwinians tend to view developmental constraints as nothing more than evolution’s constraint on itself (Jacob, 1982). Developmental systems are themselves products of evolution and they are therefore historical accidents: if evolution had taken a different course, then we would find different developmental constraints on evolution. Other writers, however, hold that developmental constraints are largely independent of evolution. Although developmental systems are produced by evolution, there are some aspects of development that are not historical and that would still obtain even if evolution had taken a different course (Goodwin, 1984; Kauffman, 1993). One also finds different interpretations of the notion of a developmental pattern (or form). Again, the standard, neo-Darwinian interpretation of developmental patterns is to view them as similar to other patterns one finds in evolution: developmental patterns are historical and contingent (Buss, 1987). If evolution had taken a different course, then we would find different patterns in development. Other writers, however, view developmental patterns as ahistorical and non-contingent; some patterns would still obtain even if evolution had taken a different course (Goodwin, 1984; Kauffman, 1993). But the different interpretations of these key concepts do not stop here. In addition to historical/ ahistorical interpretations, we also find Maynard Smith et al. (1986) offering local/universal interpretations: local constraints and patterns are taxonspecific while universal constraints and patterns apply to all (or perhaps nearly all) organisms. Some writers emphasize local constraints and patterns (e.g. French, 1983) while others emphasize universal constraints and patterns (e.g. Kauffman, 1993). One final difference of interpretation found in the literature concerns the causal power of constraints and patterns: some writers, for example Goodwin (1984) and Ho & Saunders (1984), hold that development is itself a positive (or active) force in evolution and that developmental patterns act as causal agents in ontogeny. Other writers who work
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within neo-Darwinian and gene-centric† traditions hold that development is not an independent, evolutionary mechanism and that developmental patterns are mere causal epiphenoma with no important influence on evolution itself (Maynard Smith et al., 1986; Gilbert, 1985). It should be clear that different writers employ the terms ‘‘developmental constraint’’ and ‘‘developmental pattern’’ in different ways. A survey of the historical record also indicates that biologists have used these terms (or ones like them) in different ways at different times (Sapp, 1991). Although scientists should be free to use language in a creative and idiosyncratic fashion, considerable confusion can result when people use the same words in different ways or apply the same concepts in different ways. In order to avoid ambiguity, it is useful to distinguish between various senses of the same terms and concepts and to specify one’s intended sense when employing them. To this end, I suggest we distinguish between local/universal, historical/ahistorical and active/passive senses of these terms.
4. Local vs. Universal Maynard Smith et al. (1986) distinguish between universal and local constraints: a universal constraint holds for all populations, and all organisms are bound by this constraint. Local constraints are taxon-specific in that they hold only for certain populations, and only organisms within these taxa are bound by these constraints. For example, the laws of physics pose universal constraints on all organized systems, be they biological systems or physical systems; principles of aerodynamics essential for flying only impose constraints on systems that fly, be they organisms or airplanes; the possible ways of making a three-rayed flower only impose constraints on monocotyledonous plants. However, Maynard Smith et al. (1986) recognize that this distinction is not entirely clear or rigid, since universality and ‘‘bindingness’’ come in degrees. For instance, some constraints, such as meiosis, range over many taxa, while other constraints, such as courtship behavior, range over fewer species. Even constraints that range over all species are not as ‘‘universal’’ as they might appear. For instance, in all species, all amino acids made into proteins are L-isomers rather than D-isomers. But this constraint † Some readers may wonder what I mean by the phrase ‘‘gene-centric’’. Gene-centrism is the commitment to explaining ontogeny, morphology, physiology, behavior and other biological processes in terms of genetic regulation and control. Salient examples of gene-centric research Dobzhansky’s (1970) approach to evolution and Dawkins’s (1982) sociobiology. See Ho & Saunders (1984) for critiques of gene-centric views.
might not hold if the early history of life had taken a different course, i.e. if early organisms had made proteins out of D-isomer amino acids. While it is important to recognize the bindingness comes in degrees, one might well ask whether some classes of constraints are more binding than others and why. The only obvious answer here is that universal constraints are more binding than local ones. Among the most binding constraints we might include constraints imposed by biochemistry, chemistry, biophysics and physics. Within the domain of local constraints, temporal priority might provide a rough guideline for distinguishing between degrees of bindingness: those constraints that occur earlier in the history of evolution are (in general) more binding than those that occur later in evolution. For instance, some of the earliest constraints concern cellular structure, function, metabolism and so forth. One might argue that these older constraints are more binding than more recent innovations, such as meiosis or four-leggedness, since it is more difficult for evolution to produce species that have radically different cell structures, metabolisms and so forth. ‘‘Difficulty’’ in this context refers to the number of changes and the number of generations it takes to bring them about. I suspect it would not require many changes or much time (on a geological scale) for us to evolve an extra finger on each hand, but it would take many changes and a great deal of time for us to develop the capacity to photosynthesize. Of course, there are bound to be some exceptions to this generalization, and it should only be viewed as a suggestion to guide further research. We can also apply the local/universal distinction to developmental patterns: a local pattern in development is taxon-specific, while a universal pattern holds for all organisms. For instance, language-learning is a developmental pattern that is, as far as we know, limited to homo sapiens; while blastulation is a pattern that we find in all metazoan species (Buss, 1987). Growth and reproduction are patterns we are likely to find in nearly all biological organisms. In considering such patterns, it is important to distinguish between two senses of the word ‘‘pattern’’: as a process and as an object. In addition, the sense of pattern as object has two distinct senses, as a program or blueprint, and as the product or result of a process. Thought of as a process, a pattern is a sequence of causal events over time, such as a volcanic eruption, the change of seasons, blastulation or meiosis. The ‘‘pattern’’ in such a process refers to the order, timing, unfolding and inter-relatedness of different events in the process. Viewed as an object, a pattern implies a particular (static) structure or form, such as
a helium atom, the human genome, a continental plate, a cell membrane or a notochord. An object can be thought of as either providing a blueprint or plan for a process, such as the nineteenth century German usuage of the word bauplan in biology. Alternatively, an object can be simply the product of a process: for example, two cells are the product of the process of cell division. Many biologists do not carefully distinguish between these different senses of the word ‘‘pattern’’ when talking about patterns, and we can find evidence of the three senses of this word in the biological literature (Goodwin 1984; Buss, 1987; Thomson, 1988; Atkinson, 1992). For the purposes of this paper, I shall simply note these possible senses of this ‘‘pattern’’ and I shall use the word in the process or product senses, as indicated by context. 5. Historical vs. Ahistorical Although the universal vs. local distinction is useful, many of the controversies in the union of development and evolution also concern the historical or contingent nature of constraints and patterns. Thus, I propose that it is also useful to distinguish between historical and ahistorical constraints and patterns. An historical constraint is one which is the product of evolution; it is a constraint that would not obtain if evolution had taken a different direction. An historical constraint is nothing more than evolution’s constraint on itself. For instance, insect segmentation patterns could be viewed as historical constraints on insect evolution since if the earliest insects had different segmentation patterns, then later ones would have had different patterns (French, 1983). An ahistorical constraint, on the other hand, is one that will hold no matter what direction evolution takes; it is one which is not historically contingent and is based on ahistorical laws of nature, such as the laws of physics or chemistry. For example, Kauffman (1993) argues that all complex systems, including biological systems, have some inescapable self-organizing properties. If Kauffman’s ideas can be verified, they would constitute ahistorical constraints on evolution (and development). To use an analogy, the use of an internal combustion engine is an historical constraint on automobile production since automobiles might not have been made with internal combustion engines. The laws of aerodynamics, chemistry, and mechanics are ahistorical constraints since all automobiles would be constrained by these laws even if automobile production had taken a different course. We can distinguish between degrees of generality among historical constraints: some constraints are very local and specific, others are less local and
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more general. For instance, the L-isomer constraint on proteins mentioned above, though quite general, is still historical. Constraints on neural integration are less general, and constraints on biped locomotion are even less general. We can say that the generality of an historical constraint depends on its place in the evolutionary tree; the oldest modifications are usually (though not always) the most general and more recent ones are usually (though not always) less general. Labeling a constraint as historical need not imply that it is insignificant, since historical constraints can exhibit a very powerful influence over evolution (Gould, 1977; Buss, 1987; Thompson, 1988). For instance, the vertebrate skeleton is an historical constraint that has limited vertebrate evolution in many ways. We can also think of developmental patterns as historical or as ahistorical. An historical pattern is one which is the product of evolution; while an ahistorical pattern is one that would obtain even if evolution had taken a different course. For instance, one might argue that multicellularity is an historical (though very general) pattern (Buss, 1978; Maynard Smith, 1978) because if evolution had taken a different course, multicellular organisms might not have emerged. One might also argue that some patterns are ahistorical in the sense that they would still obtain (on this planet at least) no matter what course evolution had taken (Kauffman, 1993). For example, all life on this planet is carbon-based. Given the facts of carbon chemistry and the earth’s conditions (atmosphere, climate etc.), one might argue that no other type of life (e.g. silicon-based) is possible on this planet. 6. Passive vs. Active Having taken care of two fairly straightforward distinctions, I now turn to a more difficult one. As I noted earlier, some writers have challenged the traditional, neo-Darwinian framework by maintaining that development can itself be an independent, evolutionary mechanism, while other writers resist this view. Some writers have also challenged traditional, gene-centric approaches to development by holding that developmental patterns, not just genes, can regulate development (Goodwin, 1986; Kauffman, 1993). This dispute suggests a third distinction, a distinction between active and passive constraints and patterns. How might we make sense of this distinction? To shed some light on this distinction, we need to think a bit more about our concept of causation. For any event, we can distinguish between the causal agent(s) bringing about the event and the background conditions for the event (Mackie, 1974). Whether we
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cite a particular agent or set of conditions as the cause of an event depends on what we want to know about the event and what we already know, i.e. our interests and background knowledge (Scriven, 1975). For instance, if I want to know the causes of a forest fire, I might cite some initial background conditions, for example the forest was very dry, the weather was hot and windy and so on, or I could cite a causal agent or mechanism, for example someone left a campfire burning, the fire spread from the campsite etc. Both the conditions and the agent(s) or mechanism(s) could be viewed as causes of the fire, depending on what we want to know about the forest fire or what we already know. However, even if we recognize both the agents/mechanisms and the conditions as causes of the fire, we could still maintain that the campfire is a more active cause than the conditions in the sense that it is a causal agent or mechanism. Though the conditions were an important part of the causal nexus, they functioned merely as a passive background for changes initiated by the campfire. Thus, we can think of causal agents or mechanisms as active causes and causal conditions as passive causes. We should also note that some events and properties are not properly regarded as causes at all: they are viewed as epiphenomena (Mackie, 1974). Such properties and events are effects that are not themselves causes, given our interests and background knowledge. For instance, the shadow made by a moving vehicle might be regarded as a causal epiphenomenon from the point of view of automotive engineering. The shadow does not affect the vehicle’s aerodynamics or fuel economy. The shadow, given this context, is causally inert. It is an effect but not a cause. Consider an avalanche—suppose that after the rocks have fallen, we discover that they spell out the word ‘‘HELP’’. Most people would hold that this abstract pattern, the word ‘‘HELP’’, played no role in this avalanche. It was an effect but not a cause. Bringing this general discussion back to biology, consider the development of an individual rat’s skeleton. According to standard genetic approaches to development, the rat’s genome regulates this development by providing information for the manufacture of proteins which regulate growth and differentiation via interactions with the rat’s environment. The genome and the environment function as causal agents or mechanisms, and the laws of biochemistry and the materials used for growth and † One might argue that the word ‘‘selection’’ does not refer to one, active cause but is a shorthand for the result of many different active causes (Byerly & Michod, 1991). Although I think it is useful to use ‘‘selection’’ to refer to a single, active cause, I recognize the importance of this other view.
differentiation (e.g. proteins, lipids, minerals) function as background conditions. But what about the overall pattern we see, viz. its skeleton? According to a gene-centric view, this pattern itself plays no active role in the rat’s development. The pattern is either a background condition for changes brought about by the genome and the environment, i.e. a passive cause, or it is a mere effect that results from genetic regulation, environmental input and other lower level processes that does not cause anything at all, i.e. a causal epiphenomenon. The rat’s developmental patterns are, on this view, causal conditions of its development or mere causal epiphenomena, but they are not causal agents. Thus, developmental mechanisms are mere passive causes at best; at worst they are causal epiphenomena. Genes and the environment are the active causes of development. Consider the evolution of a population of rats. On a standard (rather simplistic), neo-Darwinian view, evolution is understood as a change in gene frequencies in this rat population. Gene frequency changes can result from natural selection or random drift. Development plays a role in the evolution of this population by limiting or biasing phenotypic variation in various ways. It helps provide the material (phenotypic variation) that natural selection acts upon. Selection and drift are the active causes in evolution; development is, at best, a causal condition or passive cause in evolution.† How might developmental patterns and constraints come to be regarded as active causes as opposed to passive causes or causal epiphenomena? Consider the development of a rat again. Developmental patterns could be viewed as active causes if we abandon the standard, gene-centric approach to development and adopt a more holistic, process-oriented approach (Kauffman, 1993). The standard approach views genomes as having a privileged causal role in development, but an alternative approach would view genomes not as controllers or regulators of ontogeny but merely as important players in complex, developmental processes. In these processes, genes interact with RNA, proteins and other macromolecules in such a way that different molecules in this developmental system regulate each other (Kauffman, 1993). Ontogeny, on this view, is not simply the unfolding of some genetic program (Mayr, 1961), but it is a complex process with its own patterns and momentum (Goodwin, 1984; Kauffman, 1993). If we adopt this view of development, then developmental patterns could function as active causes of development. They would be analogous to patterns that govern the formation of thunderstorms; patterns are not mere causal epiphenoma or background
conditions, but they play an active role in thunderstorm formation. But what about evolution? How could developmental constraints function as causal agents in evolution? Two major assumptions of the neo-Darwinian paradigm stand in the way of viewing development as an independent, evolutionary mechanism, the genetic approach to evolution and Weissman’s doctrine. The genetic approach to evolution is simply the idea that evolution is defined as a change in the gene distributions of populations (Lewontin, 1974). The main reason for defining evolution in this way is that evolution is equated with long-term changes to a population, and most biologists believe that only genetic changes can result in long-term changes. A population of rats may grow larger than its ancestors due to better nutrition, but if this increase in growth has no genetic basis, then it does not produce a long-term change in the rat population: the next generation of rats, if they have poorer nutrition, will not be as large. Weissman’s doctrine is the assertion that acquired characteristics are not inherited—it is one of the main assumptions of Darwinian evolution (Maynard Smith, 1983; Saunders, 1985). Weissman’s doctrine, in its recent form, is based on our understanding of the mechanisms of inheritance (in animals).† For most animals, changes in an organism do not affect its germ cells and information flows from genotype to phenotype but not vice versa. Weissman’s doctrine also supports measuring evolution in genetic terms, since most biologists believe that evolution should be equated with long-term changes. If developmental changes do not affect the genome, and only changes in the genome can bring about long-term changes, then developmental changes do not result in evolutionary ones. If we accept these two assumptions, then there can be no independent, developmental causes of (animal) evolution, since developmental changes and processes do not result in long-term changes. Development plays an important role in the expression of genotypes, but since it does not cause changes in genotypes, and since evolutionary changes must be based on genetic
† Weissman’s doctrine does not apply to plants, since plants do not segregate their germ-lines. Thus, many of the points relating to Weissman’s doctrine only apply to the evolution of animals. ‡ Although I think it makes sense to think of natural selection as an active cause in evolution, we need not think of selection as a force or an agent. It is a causal mechanism analagous to weathering, but not a force. This same point applies to development’s role in evolution: we might think of development as an active cause without holding that it is a force or causal agent. See Endler (1986).
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changes, development can only play a role in evolution by limiting and biasing phenotypic variation. Developmental biologists who want to posit an active role for developmental constraints in evolution must either show that (a) we should not define evolution solely as changes in gene distributions; and/or (b) Weissman’s doctrine is false. Concerning (a), there are some compelling reasons for thinking that evolution should not be measured solely in genetic terms since we have evidence that many elements of the somatic environment are inherited, such as microtubles and mitochondria, and that these non-genetic forms of inheritance can result in long-term changes (Margulis, 1981; Buss, 1987; Smith, 1992a). Concerning (b), there are some well-known exceptions to Weissman’s doctrine that occur in many unicellular species and in some multicellular ones (Nieuwkoop & Sutasurya, 1983; Saunders, 1985; Buss, 1987), but we have evidence that the doctrine generally holds for most animals (Thomson, 1988). Nevertheless, it may be useful to think of Weissman’s doctrine as a rough generalization resulting from certain evolutionary processes (Maynard Smith, 1983; Buss, 1987), i.e. an historical constraint on animal evolution. Given these considerations, there are no a priori reasons why development could not function as an independent, evolutionary mechanism, although we may be able to produce some empirical evidence demonstrating that it usually does not do so. Developmental processes could play an active role in evolution by either causing changes in the genome or by allowing for non-genetic modes of inheritance. Clearly, more empirical work needs to be done here. To bring the discussion back to the active/passive distinction, developmental constraints could be viewed as active provided that we have some evidence that they function as independent, causal mechanisms in evolution.‡ An active constraint on evolution would be one that functions as an independent, evolutionary mechanism; a passive constraint would be one that merely operates via natural selection by restricting or biasing phenotypic variation. Likewise, an active pattern in development would be a pattern that functions as a causal agent in development by regulating or guiding developmental processes, whereas a passive pattern would be one that is a mere background condition or a causally inert by-product of genetic regulation and control. How might biologists go about settling questions concerning the activity or passivity of developmental patterns and constraints? Since we have very strong experimental evidence that most developmental patterns are not active (Gilbert, 1985), we can assume passivity as a null hypothesis. The experimental burden
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would then fall on those who wish to prove that a pattern is active. In order to show that a pattern is itself an active cause (as opposed to a background condition or causal epiphenomon), one needs to show that the genome or environment do not act as the primary causal agents for a given effect. Classic ‘‘knockout’’ experiments in molecular genetics might be useful in this regard: if a developmental pattern persists despite damage to parts of the genome thought to be vital in development, it would be strong evidence that the pattern is itself a cause of development. One might also show that a pattern is active through experiments related to phenocopies, i.e. environmental mimics of genetic mutations. If an environmental stimulus produces the same phenotypic effect as a genetic mutation, this would constitute strong evidence for viewing the phenotypic effect as a developmental system’s stereotypic response to genetic or environmental inputs (Goodwin, 1984). I think we can also assume the passivity of developmental constraints as a null hypothesis in evolutionary biology, since we have strong evidence for the neo-Darwinian approach to developmental constraints (Thomson, 1988). Once again, the burden of proof should fall on those people who would try to show that developmental constraints are active causes in evolution (as opposed to background conditions or causal ephinomena). In order to show that development plays an active role in evolution, one would need to show that (i) developmental systems have some nongenetic components that are heritable, such as materials in the cytoplasm, the centromeres, RNA, and so forth (Smith, 1992a); and/or that (ii) there are some exceptions to Weissman’s doctrine that have important effects relating to evolution. In order to demonstrate (i) or (ii) it will be necessary to obtain experimental evidence from molecular biology, biochemistry cytology, and from ecology, population biology and paleontology. One needs evidence from the first three in order to show that it is at least possible for development to play an active role in evolution; one needs evidence from ecology, population biology and ecology in order to show that development does actually play an active role in evolution. Clearly, biologists need to do a great deal more empirical work before they can determine whether there are (or can be) active developmental patterns and/or constraints. At this point we can only suggest some guidelines for further research.
7. Conclusion In this paper I have attempted to clarify some of the conceptual issues surrounding the new union of development and evolution. To this end, I have distinguished between several different senses of two key concepts in this new synthesis: the concept of a developmental constraint on evolution and that of a developmental pattern or form. I think we can see from this brief discussion that there are several very different senses of these concepts and that these different senses reflect entirely different approaches to evolution and development. Since these are significant distinctions, it would be useful for biologists to pay more careful attention to their usage of the terms ‘‘developmental pattern’’ and ‘‘developmental constraint’’ in order to avoid ambiguity and confusion. Accordingly, I suggest the following terminology which help clarify thinking about development and evolution: / (i) Historical: ‘‘evolutionary trends’’ (constraints or patterns) (ii) Ahistorical: ‘‘physical necessities’’ (constraints or patterns) (iii) Passive: ‘‘existing limits on variation’’ (constraints) ‘‘the developmental map’’ (pattern) (iv) Active: ‘‘ontogenetic, evolutionary mechanism’’ (constraints) ‘‘structural causes in development’’ (patterns) (v) Local: ‘‘taxon-specific’’ (constraints or patterns) (vi) Universal: ‘‘taxon-neutral’’ (constraints or patterns) In addition, I suggest the following terminology to clarify talk that employs expressions like ‘‘developmental pattern’’, ‘‘developmental form’’ and so forth: Patterns in development: (i) Sequences of events: ‘‘developmental processes’’ or ‘‘mechanisms’’ (ii) Objects or properties: ‘‘developmental products’’ or ‘‘structures’’ (iii) Designs: ‘‘Developmental blueprints,’’ ‘‘programs’’ or ‘‘bauplans’’. Of course, these expressions are only suggestions and any words that preserve the distinctions made in this paper would be acceptable, Once the fundamental distinctions are grasped, word-choice can be largely a matter of convenience.
Given the distinctions used in the paper, it is fair to say that the neo-Darwinian paradigm recognizes historical, local, universal and passive developmental constraints, but it opposes active constraints. Although neo-Darwinians can recognize ahistorical constraints on evolution, they are not inclined to search for these constraints, given their historical orientation. It is also fair to say that the standard, gene-centric paradigm of development recognizes historical, local, universal and passive patterns, but that it opposes any active patterns. The gene-centric view also can recognize ahistorical developmental patterns, although gene-centrists have been disinclined to search for them, given the dominance of neo-Darwinism. Given the dominance of neo-Darwinian and gene-centric thinking, the notions of active and ahistorical constraints and patterns will prove to be most controversial, since the existence of such constraints and patterns would challenge standard views about the nature of inheritance, evolution, ontogeny and genetic regulation. Whether there are any active and/or ahistorical constraints or patterns is an empirical issue whose outcome depends on further experimental investigation into developmental mechanisms, processes, and on further research on the history of life on Earth.
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Developmental Constraints and Patterns: Some Pertinent Distinctions D R Department of Philosophy, University of Wyoming, Laramie, WY 82071-3392, U.S.A. (Received on 2 December 1993, Accepted in revised form on 29 November 1994)
This paper remedies some of the conceptual ambiguity in the union of evolution and development by explicating two key concepts in this disciplinary integration: that of a developmental constraint on evolution and of a developmental pattern or form. The phrases ‘‘developmental pattern’’ and ‘‘developmental constraint’’ often mean quite different things to different people in different theoretical contexts. It is intended that this paper will help clarify thinking about evolution and development by distinguishing between historical/ahistorical, local/universal and passive/active senses of these terms and by suggesting some expressions to help stabilize and clarify usage.
such as Maynard Smith et al. (1986), Mayo (1983) and Thomson (1988), attempt to unify development and evolution without challenging the neo-Darwinian paradigm; others, such as Kauffman (1993), Buss (1987) and Gould (1977), see shortcomings with neo-Darwinism but still operate within a neoDarwinian framework; while others still, such as Goodwin (1984), Salthe (1993) and Wolpert (1983) envisage a union of development and evolution that overthrows many neo-Darwinian assumptions. These different perspectives on development and evolution, in turn, have generated very different interpretations of some key concepts in the union of development and evolution. As a result, those people who employ these concepts may be ‘‘talking past’’ each other since they may have very different interpretations of the same terms and ideas. This paper attempts to remedy some of this ambiguity by explicating two key concepts in this new union: that of a developmental constraint on evolution (Kauffman,1983; Mayo, 1983; Wolpert, 1983; Maynard Smith et al., 1986; Thomson, 1988) and that of a developmental pattern (Gould & Lewtonin, 1979; Holder, 1983; Buss, 1987; Arthur, 1988; Atkinson, 1992; Salthe 1993). Although many biologists employ these concepts in their work, not all biologists understand these concepts in the same way: the phrases ‘‘developmental pattern’’ and ‘‘developmental
1. Introduction In the last two decades developmental biologists, evolutionary biologists and some philosophers of biology have sought to resolve some of the outstanding problems in development and evolution by forging a ‘‘new’’† union between the study of development and the study of evolution (Gould, 1977; Alberch, 1982; Bonner, 1982; Mayo, 1983; Wolpert, 1983; Ho & Saunders, 1984; Burian, 1986; Maynard Smith et al., 1986; Wimsatt, 1986; Buss, 1987; Raff & Raff, 1987; Arthur, 1988; Thomson, 1988; Atkinson, 1991; Smith, 1992a, 1992b; Kaufmann, 1993; Salthe, 1993). In this union, evolutionary biologists look to development for important insights into evolution, and developmental biologists look to evolution for important insights into developmental processes and mechanisms. Those who attempt to forge connections between development and evolution often have very different perspectives on biology, and hence very different ideas about the shape this new union should take. Some, † There was an old union between development and evolution founded on Haeckel’s biogenic law, ‘‘ontogeny recapitulates phylogeny’’ (Gould, 1977). According to this view, the developmental patterns of species indicated their phylogenetic relationships in that evolutionary history repeats itself in development. On this old union, developmental biology offered crucial insights into evolution. For more on the fall of the biogenic law and the separation of evolution and development, see Gould (1977). 0022–5193/95/070231+10 $08.00/0
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constraint’’ often mean quite different things to different people in different theoretical contexts. This essay will remedy this problem by distinguishing between the historical/ahistorical, local/universal and passive/ active senses of these terms. In addition, I shall suggest some terminology that may be useful in clarifying and stabilizing usage. Although this analysis is not designed to settle any substantive, empirical questions in development and evolution, I hope it aids the study of development and evolution by helping to clarify the conceptual framework for thinking about the relationship between development and evolution. 2. Development vs. Evolution Most biologists recognize that development and evolution are different processes (Gould, 1977; Gilbert, 1985; Patterson, 1983; Thomson, 1988). If there were no difference, then debates about the union of development and evolution would be misguided, since there would not be two different things to unite. Although this point seems quite trivial and obvious, it is still important. Indeed, most biologists did not distinguish between development and evolution until the 1840s, when they began to appreciate von Baer’s distinction between ontogeny and phylogeny (Patterson, 1983). Although few biologists would dispute the assumption that evolution and development are different processes, not all biologists would agree on how one should characterize this difference. Indeed, one’s perspective on the difference between development and evolution will inevitably be infused with various (often controversial) assumptions about these processes (Patterson, 1983; Salthe, 1993). Nevertheless, for the purposes of this essay I shall offer a fairly standard interpretation of the differences between development and evolution. In noting these differences, I do not intend to point out anything that is not obvious to most biologists, but it is still worth having these points before us. In order to understand the differences, I shall first note some important similarities. First, development and evolution both involve changes over time (Salthe, 1993). In development, immature organisms become adult organisms through differentiation, growth, and learning. In evolution, species (or populations) transform over time, adapt to their environments, or become extinct. Of course, evolution (usually) takes more time than development and evolution and development act on different entities, but both development and evolution bring about changes over time. Second, development
and evolution both produce changes by means of interactions between the genome and the environment. In development, the genome and environment interact to produce an adult organism (Gilbert, 1985); in evolution the interactions between the genome and environment produce changes in gene frequencies through natural selection, random drift or other evolutionary mechanisms (Lewontin, 1974). The differences between development and evolution, then, involve the types of changes that occur, what undergoes change and the ways that changes are produced. Some of the differences between development and evolution are as follows: (i) Developmental changes occur within individual organisms; evolutionary changes occur within or between populations of organisms (Lewontin, 1974; Maynard Smith, 1983; Gilbert, 1985; Thomson, 1988; Salthe, 1993). In development, organisms grow, differentiate, learn and age over time; in evolution the genetic and phenotypic properties of populations, relative abundances and distributions of populations, gene flow between populations and so forth change over time. (ii) Developmental changes occur in one generation; evolutionary changes occur over many generations (Lewontin, 1974; Endler, 1984; Gilbert, 1985). (iii) Evolutionary changes must involve changes in gene distributions in populations; developmental changes need not involve changes in gene distributions (Lewontin, 1974; Endler, 1984; Gilbert 1985). (iv) Development exhibits a high degree of stability despite external and internal disturbances (Waddington, 1957, 1975; Gilbert, 1985; Kauffman, 1993); evolution does not exhibit this same degree of stability. There may of course be some other differences between development and evolution than these, but certainly these four differences need to be mentioned. Given these differences, one may naturally ask how these two processes causally influence each other. From an evolutionary perspective, one might ask how development influences evolution. Ever since Darwin, evolutionary biologists have been aware that development plays an important role in evolution. We find this recognition in Darwin (1859) as well as in the work of Russell (1916), Huxley and de Beer (1934), Morgan (1932), Waddington (1940), Schmaulhausen (1949), Bonner (1958), Rensch (1960) and Monod (1971), among many others. Biologists working within the neo-Darwinian tradition have
employed many concepts to understand development’s role in evolution, including the concept of an epigenetic landscape (Waddington, 1940), the concept of developmental constraints (Maynard Smith et al., 1986) and the concept of phenotypic plasticity (Dobzhansky, 1970). Although these concepts differ considerably in their theoretical context, the basic idea behind these three important concepts is that development can in some way constrain or influence evolution. From a developmental perspective, one may ask how the developmental systems of various species have been shaped by evolution. This study, dubbed ‘‘the evolution of development’’, is unlike most experimentally oriented embryology because it must be comparative and historical in its orientation (Atkinson, 1991). In studying the evolution of development, scientists attempt to understand the evolutionary basis of similarities (i.e. homologies and analogies) and differences among developmental systems (Buss, 1987; Atkinson, 1991). Scientists can also discover whether developmental mechanisms and processes are adaptations to various environmental demands. This type of study also has a long tradition (Gould, 1977; Churchill, 1991). We find a concern for the evolution of development in the work of Darwin (1859), Muller (1864), Haeckel (1866), Conklin (1915), Waddington (1940), Bonner (1958), among many others. Since the study of the evolution of development is comparative in its approach, many different concepts originally employed by comparative embryologists have proven useful in this inquiry. These concepts include the notion of notion of an archetype (Kauffman, 1993), the concept of a morphogenic field (Goodwin & Trainor, 1983) and the concept of a developmental pattern or form (Gould & Lewontin, 1979; Buss, 1987; Atkinson, 1991; Churchill, 1991). Although biologists have used these concepts in many different ways, the main idea behind each of them is that some common patterns manifest themselves in various developmental systems. A rat and a horse are phenotypically and genotypically quite different, but we still can learn that their developmental systems exhibit similar mechanisms and processes.
3. Differences of Interpretation Thus, two of the most crucial concepts in the union of development and evolution are the concepts † Obviously, the existence of developmental patterns is important to the study of development regardless of its evolutionary implications, but in this paper I am only focusing on the bearing such patterns have for the union of evolution and development.
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‘‘developmental constraint’’ and ‘‘developmental pattern’’. The notion of a developmental constraint is important in understanding how development influences evolution; the notion of a developmental pattern is important in understanding the evolution of development.† Having located these key concepts, we also find that different writers give them vastly different interpretations, and that these different interpretations reflect different approaches to the study of evolution and development. For instance, neo-Darwinians tend to view developmental constraints as nothing more than evolution’s constraint on itself (Jacob, 1982). Developmental systems are themselves products of evolution and they are therefore historical accidents: if evolution had taken a different course, then we would find different developmental constraints on evolution. Other writers, however, hold that developmental constraints are largely independent of evolution. Although developmental systems are produced by evolution, there are some aspects of development that are not historical and that would still obtain even if evolution had taken a different course (Goodwin, 1984; Kauffman, 1993). One also finds different interpretations of the notion of a developmental pattern (or form). Again, the standard, neo-Darwinian interpretation of developmental patterns is to view them as similar to other patterns one finds in evolution: developmental patterns are historical and contingent (Buss, 1987). If evolution had taken a different course, then we would find different patterns in development. Other writers, however, view developmental patterns as ahistorical and non-contingent; some patterns would still obtain even if evolution had taken a different course (Goodwin, 1984; Kauffman, 1993). But the different interpretations of these key concepts do not stop here. In addition to historical/ ahistorical interpretations, we also find Maynard Smith et al. (1986) offering local/universal interpretations: local constraints and patterns are taxonspecific while universal constraints and patterns apply to all (or perhaps nearly all) organisms. Some writers emphasize local constraints and patterns (e.g. French, 1983) while others emphasize universal constraints and patterns (e.g. Kauffman, 1993). One final difference of interpretation found in the literature concerns the causal power of constraints and patterns: some writers, for example Goodwin (1984) and Ho & Saunders (1984), hold that development is itself a positive (or active) force in evolution and that developmental patterns act as causal agents in ontogeny. Other writers who work
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within neo-Darwinian and gene-centric† traditions hold that development is not an independent, evolutionary mechanism and that developmental patterns are mere causal epiphenoma with no important influence on evolution itself (Maynard Smith et al., 1986; Gilbert, 1985). It should be clear that different writers employ the terms ‘‘developmental constraint’’ and ‘‘developmental pattern’’ in different ways. A survey of the historical record also indicates that biologists have used these terms (or ones like them) in different ways at different times (Sapp, 1991). Although scientists should be free to use language in a creative and idiosyncratic fashion, considerable confusion can result when people use the same words in different ways or apply the same concepts in different ways. In order to avoid ambiguity, it is useful to distinguish between various senses of the same terms and concepts and to specify one’s intended sense when employing them. To this end, I suggest we distinguish between local/universal, historical/ahistorical and active/passive senses of these terms.
4. Local vs. Universal Maynard Smith et al. (1986) distinguish between universal and local constraints: a universal constraint holds for all populations, and all organisms are bound by this constraint. Local constraints are taxon-specific in that they hold only for certain populations, and only organisms within these taxa are bound by these constraints. For example, the laws of physics pose universal constraints on all organized systems, be they biological systems or physical systems; principles of aerodynamics essential for flying only impose constraints on systems that fly, be they organisms or airplanes; the possible ways of making a three-rayed flower only impose constraints on monocotyledonous plants. However, Maynard Smith et al. (1986) recognize that this distinction is not entirely clear or rigid, since universality and ‘‘bindingness’’ come in degrees. For instance, some constraints, such as meiosis, range over many taxa, while other constraints, such as courtship behavior, range over fewer species. Even constraints that range over all species are not as ‘‘universal’’ as they might appear. For instance, in all species, all amino acids made into proteins are L-isomers rather than D-isomers. But this constraint † Some readers may wonder what I mean by the phrase ‘‘gene-centric’’. Gene-centrism is the commitment to explaining ontogeny, morphology, physiology, behavior and other biological processes in terms of genetic regulation and control. Salient examples of gene-centric research Dobzhansky’s (1970) approach to evolution and Dawkins’s (1982) sociobiology. See Ho & Saunders (1984) for critiques of gene-centric views.
might not hold if the early history of life had taken a different course, i.e. if early organisms had made proteins out of D-isomer amino acids. While it is important to recognize the bindingness comes in degrees, one might well ask whether some classes of constraints are more binding than others and why. The only obvious answer here is that universal constraints are more binding than local ones. Among the most binding constraints we might include constraints imposed by biochemistry, chemistry, biophysics and physics. Within the domain of local constraints, temporal priority might provide a rough guideline for distinguishing between degrees of bindingness: those constraints that occur earlier in the history of evolution are (in general) more binding than those that occur later in evolution. For instance, some of the earliest constraints concern cellular structure, function, metabolism and so forth. One might argue that these older constraints are more binding than more recent innovations, such as meiosis or four-leggedness, since it is more difficult for evolution to produce species that have radically different cell structures, metabolisms and so forth. ‘‘Difficulty’’ in this context refers to the number of changes and the number of generations it takes to bring them about. I suspect it would not require many changes or much time (on a geological scale) for us to evolve an extra finger on each hand, but it would take many changes and a great deal of time for us to develop the capacity to photosynthesize. Of course, there are bound to be some exceptions to this generalization, and it should only be viewed as a suggestion to guide further research. We can also apply the local/universal distinction to developmental patterns: a local pattern in development is taxon-specific, while a universal pattern holds for all organisms. For instance, language-learning is a developmental pattern that is, as far as we know, limited to homo sapiens; while blastulation is a pattern that we find in all metazoan species (Buss, 1987). Growth and reproduction are patterns we are likely to find in nearly all biological organisms. In considering such patterns, it is important to distinguish between two senses of the word ‘‘pattern’’: as a process and as an object. In addition, the sense of pattern as object has two distinct senses, as a program or blueprint, and as the product or result of a process. Thought of as a process, a pattern is a sequence of causal events over time, such as a volcanic eruption, the change of seasons, blastulation or meiosis. The ‘‘pattern’’ in such a process refers to the order, timing, unfolding and inter-relatedness of different events in the process. Viewed as an object, a pattern implies a particular (static) structure or form, such as
a helium atom, the human genome, a continental plate, a cell membrane or a notochord. An object can be thought of as either providing a blueprint or plan for a process, such as the nineteenth century German usuage of the word bauplan in biology. Alternatively, an object can be simply the product of a process: for example, two cells are the product of the process of cell division. Many biologists do not carefully distinguish between these different senses of the word ‘‘pattern’’ when talking about patterns, and we can find evidence of the three senses of this word in the biological literature (Goodwin 1984; Buss, 1987; Thomson, 1988; Atkinson, 1992). For the purposes of this paper, I shall simply note these possible senses of this ‘‘pattern’’ and I shall use the word in the process or product senses, as indicated by context. 5. Historical vs. Ahistorical Although the universal vs. local distinction is useful, many of the controversies in the union of development and evolution also concern the historical or contingent nature of constraints and patterns. Thus, I propose that it is also useful to distinguish between historical and ahistorical constraints and patterns. An historical constraint is one which is the product of evolution; it is a constraint that would not obtain if evolution had taken a different direction. An historical constraint is nothing more than evolution’s constraint on itself. For instance, insect segmentation patterns could be viewed as historical constraints on insect evolution since if the earliest insects had different segmentation patterns, then later ones would have had different patterns (French, 1983). An ahistorical constraint, on the other hand, is one that will hold no matter what direction evolution takes; it is one which is not historically contingent and is based on ahistorical laws of nature, such as the laws of physics or chemistry. For example, Kauffman (1993) argues that all complex systems, including biological systems, have some inescapable self-organizing properties. If Kauffman’s ideas can be verified, they would constitute ahistorical constraints on evolution (and development). To use an analogy, the use of an internal combustion engine is an historical constraint on automobile production since automobiles might not have been made with internal combustion engines. The laws of aerodynamics, chemistry, and mechanics are ahistorical constraints since all automobiles would be constrained by these laws even if automobile production had taken a different course. We can distinguish between degrees of generality among historical constraints: some constraints are very local and specific, others are less local and
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more general. For instance, the L-isomer constraint on proteins mentioned above, though quite general, is still historical. Constraints on neural integration are less general, and constraints on biped locomotion are even less general. We can say that the generality of an historical constraint depends on its place in the evolutionary tree; the oldest modifications are usually (though not always) the most general and more recent ones are usually (though not always) less general. Labeling a constraint as historical need not imply that it is insignificant, since historical constraints can exhibit a very powerful influence over evolution (Gould, 1977; Buss, 1987; Thompson, 1988). For instance, the vertebrate skeleton is an historical constraint that has limited vertebrate evolution in many ways. We can also think of developmental patterns as historical or as ahistorical. An historical pattern is one which is the product of evolution; while an ahistorical pattern is one that would obtain even if evolution had taken a different course. For instance, one might argue that multicellularity is an historical (though very general) pattern (Buss, 1978; Maynard Smith, 1978) because if evolution had taken a different course, multicellular organisms might not have emerged. One might also argue that some patterns are ahistorical in the sense that they would still obtain (on this planet at least) no matter what course evolution had taken (Kauffman, 1993). For example, all life on this planet is carbon-based. Given the facts of carbon chemistry and the earth’s conditions (atmosphere, climate etc.), one might argue that no other type of life (e.g. silicon-based) is possible on this planet. 6. Passive vs. Active Having taken care of two fairly straightforward distinctions, I now turn to a more difficult one. As I noted earlier, some writers have challenged the traditional, neo-Darwinian framework by maintaining that development can itself be an independent, evolutionary mechanism, while other writers resist this view. Some writers have also challenged traditional, gene-centric approaches to development by holding that developmental patterns, not just genes, can regulate development (Goodwin, 1986; Kauffman, 1993). This dispute suggests a third distinction, a distinction between active and passive constraints and patterns. How might we make sense of this distinction? To shed some light on this distinction, we need to think a bit more about our concept of causation. For any event, we can distinguish between the causal agent(s) bringing about the event and the background conditions for the event (Mackie, 1974). Whether we
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cite a particular agent or set of conditions as the cause of an event depends on what we want to know about the event and what we already know, i.e. our interests and background knowledge (Scriven, 1975). For instance, if I want to know the causes of a forest fire, I might cite some initial background conditions, for example the forest was very dry, the weather was hot and windy and so on, or I could cite a causal agent or mechanism, for example someone left a campfire burning, the fire spread from the campsite etc. Both the conditions and the agent(s) or mechanism(s) could be viewed as causes of the fire, depending on what we want to know about the forest fire or what we already know. However, even if we recognize both the agents/mechanisms and the conditions as causes of the fire, we could still maintain that the campfire is a more active cause than the conditions in the sense that it is a causal agent or mechanism. Though the conditions were an important part of the causal nexus, they functioned merely as a passive background for changes initiated by the campfire. Thus, we can think of causal agents or mechanisms as active causes and causal conditions as passive causes. We should also note that some events and properties are not properly regarded as causes at all: they are viewed as epiphenomena (Mackie, 1974). Such properties and events are effects that are not themselves causes, given our interests and background knowledge. For instance, the shadow made by a moving vehicle might be regarded as a causal epiphenomenon from the point of view of automotive engineering. The shadow does not affect the vehicle’s aerodynamics or fuel economy. The shadow, given this context, is causally inert. It is an effect but not a cause. Consider an avalanche—suppose that after the rocks have fallen, we discover that they spell out the word ‘‘HELP’’. Most people would hold that this abstract pattern, the word ‘‘HELP’’, played no role in this avalanche. It was an effect but not a cause. Bringing this general discussion back to biology, consider the development of an individual rat’s skeleton. According to standard genetic approaches to development, the rat’s genome regulates this development by providing information for the manufacture of proteins which regulate growth and differentiation via interactions with the rat’s environment. The genome and the environment function as causal agents or mechanisms, and the laws of biochemistry and the materials used for growth and † One might argue that the word ‘‘selection’’ does not refer to one, active cause but is a shorthand for the result of many different active causes (Byerly & Michod, 1991). Although I think it is useful to use ‘‘selection’’ to refer to a single, active cause, I recognize the importance of this other view.
differentiation (e.g. proteins, lipids, minerals) function as background conditions. But what about the overall pattern we see, viz. its skeleton? According to a gene-centric view, this pattern itself plays no active role in the rat’s development. The pattern is either a background condition for changes brought about by the genome and the environment, i.e. a passive cause, or it is a mere effect that results from genetic regulation, environmental input and other lower level processes that does not cause anything at all, i.e. a causal epiphenomenon. The rat’s developmental patterns are, on this view, causal conditions of its development or mere causal epiphenomena, but they are not causal agents. Thus, developmental mechanisms are mere passive causes at best; at worst they are causal epiphenomena. Genes and the environment are the active causes of development. Consider the evolution of a population of rats. On a standard (rather simplistic), neo-Darwinian view, evolution is understood as a change in gene frequencies in this rat population. Gene frequency changes can result from natural selection or random drift. Development plays a role in the evolution of this population by limiting or biasing phenotypic variation in various ways. It helps provide the material (phenotypic variation) that natural selection acts upon. Selection and drift are the active causes in evolution; development is, at best, a causal condition or passive cause in evolution.† How might developmental patterns and constraints come to be regarded as active causes as opposed to passive causes or causal epiphenomena? Consider the development of a rat again. Developmental patterns could be viewed as active causes if we abandon the standard, gene-centric approach to development and adopt a more holistic, process-oriented approach (Kauffman, 1993). The standard approach views genomes as having a privileged causal role in development, but an alternative approach would view genomes not as controllers or regulators of ontogeny but merely as important players in complex, developmental processes. In these processes, genes interact with RNA, proteins and other macromolecules in such a way that different molecules in this developmental system regulate each other (Kauffman, 1993). Ontogeny, on this view, is not simply the unfolding of some genetic program (Mayr, 1961), but it is a complex process with its own patterns and momentum (Goodwin, 1984; Kauffman, 1993). If we adopt this view of development, then developmental patterns could function as active causes of development. They would be analogous to patterns that govern the formation of thunderstorms; patterns are not mere causal epiphenoma or background
conditions, but they play an active role in thunderstorm formation. But what about evolution? How could developmental constraints function as causal agents in evolution? Two major assumptions of the neo-Darwinian paradigm stand in the way of viewing development as an independent, evolutionary mechanism, the genetic approach to evolution and Weissman’s doctrine. The genetic approach to evolution is simply the idea that evolution is defined as a change in the gene distributions of populations (Lewontin, 1974). The main reason for defining evolution in this way is that evolution is equated with long-term changes to a population, and most biologists believe that only genetic changes can result in long-term changes. A population of rats may grow larger than its ancestors due to better nutrition, but if this increase in growth has no genetic basis, then it does not produce a long-term change in the rat population: the next generation of rats, if they have poorer nutrition, will not be as large. Weissman’s doctrine is the assertion that acquired characteristics are not inherited—it is one of the main assumptions of Darwinian evolution (Maynard Smith, 1983; Saunders, 1985). Weissman’s doctrine, in its recent form, is based on our understanding of the mechanisms of inheritance (in animals).† For most animals, changes in an organism do not affect its germ cells and information flows from genotype to phenotype but not vice versa. Weissman’s doctrine also supports measuring evolution in genetic terms, since most biologists believe that evolution should be equated with long-term changes. If developmental changes do not affect the genome, and only changes in the genome can bring about long-term changes, then developmental changes do not result in evolutionary ones. If we accept these two assumptions, then there can be no independent, developmental causes of (animal) evolution, since developmental changes and processes do not result in long-term changes. Development plays an important role in the expression of genotypes, but since it does not cause changes in genotypes, and since evolutionary changes must be based on genetic
† Weissman’s doctrine does not apply to plants, since plants do not segregate their germ-lines. Thus, many of the points relating to Weissman’s doctrine only apply to the evolution of animals. ‡ Although I think it makes sense to think of natural selection as an active cause in evolution, we need not think of selection as a force or an agent. It is a causal mechanism analagous to weathering, but not a force. This same point applies to development’s role in evolution: we might think of development as an active cause without holding that it is a force or causal agent. See Endler (1986).
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changes, development can only play a role in evolution by limiting and biasing phenotypic variation. Developmental biologists who want to posit an active role for developmental constraints in evolution must either show that (a) we should not define evolution solely as changes in gene distributions; and/or (b) Weissman’s doctrine is false. Concerning (a), there are some compelling reasons for thinking that evolution should not be measured solely in genetic terms since we have evidence that many elements of the somatic environment are inherited, such as microtubles and mitochondria, and that these non-genetic forms of inheritance can result in long-term changes (Margulis, 1981; Buss, 1987; Smith, 1992a). Concerning (b), there are some well-known exceptions to Weissman’s doctrine that occur in many unicellular species and in some multicellular ones (Nieuwkoop & Sutasurya, 1983; Saunders, 1985; Buss, 1987), but we have evidence that the doctrine generally holds for most animals (Thomson, 1988). Nevertheless, it may be useful to think of Weissman’s doctrine as a rough generalization resulting from certain evolutionary processes (Maynard Smith, 1983; Buss, 1987), i.e. an historical constraint on animal evolution. Given these considerations, there are no a priori reasons why development could not function as an independent, evolutionary mechanism, although we may be able to produce some empirical evidence demonstrating that it usually does not do so. Developmental processes could play an active role in evolution by either causing changes in the genome or by allowing for non-genetic modes of inheritance. Clearly, more empirical work needs to be done here. To bring the discussion back to the active/passive distinction, developmental constraints could be viewed as active provided that we have some evidence that they function as independent, causal mechanisms in evolution.‡ An active constraint on evolution would be one that functions as an independent, evolutionary mechanism; a passive constraint would be one that merely operates via natural selection by restricting or biasing phenotypic variation. Likewise, an active pattern in development would be a pattern that functions as a causal agent in development by regulating or guiding developmental processes, whereas a passive pattern would be one that is a mere background condition or a causally inert by-product of genetic regulation and control. How might biologists go about settling questions concerning the activity or passivity of developmental patterns and constraints? Since we have very strong experimental evidence that most developmental patterns are not active (Gilbert, 1985), we can assume passivity as a null hypothesis. The experimental burden
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would then fall on those who wish to prove that a pattern is active. In order to show that a pattern is itself an active cause (as opposed to a background condition or causal epiphenomon), one needs to show that the genome or environment do not act as the primary causal agents for a given effect. Classic ‘‘knockout’’ experiments in molecular genetics might be useful in this regard: if a developmental pattern persists despite damage to parts of the genome thought to be vital in development, it would be strong evidence that the pattern is itself a cause of development. One might also show that a pattern is active through experiments related to phenocopies, i.e. environmental mimics of genetic mutations. If an environmental stimulus produces the same phenotypic effect as a genetic mutation, this would constitute strong evidence for viewing the phenotypic effect as a developmental system’s stereotypic response to genetic or environmental inputs (Goodwin, 1984). I think we can also assume the passivity of developmental constraints as a null hypothesis in evolutionary biology, since we have strong evidence for the neo-Darwinian approach to developmental constraints (Thomson, 1988). Once again, the burden of proof should fall on those people who would try to show that developmental constraints are active causes in evolution (as opposed to background conditions or causal ephinomena). In order to show that development plays an active role in evolution, one would need to show that (i) developmental systems have some nongenetic components that are heritable, such as materials in the cytoplasm, the centromeres, RNA, and so forth (Smith, 1992a); and/or that (ii) there are some exceptions to Weissman’s doctrine that have important effects relating to evolution. In order to demonstrate (i) or (ii) it will be necessary to obtain experimental evidence from molecular biology, biochemistry cytology, and from ecology, population biology and paleontology. One needs evidence from the first three in order to show that it is at least possible for development to play an active role in evolution; one needs evidence from ecology, population biology and ecology in order to show that development does actually play an active role in evolution. Clearly, biologists need to do a great deal more empirical work before they can determine whether there are (or can be) active developmental patterns and/or constraints. At this point we can only suggest some guidelines for further research.
7. Conclusion In this paper I have attempted to clarify some of the conceptual issues surrounding the new union of development and evolution. To this end, I have distinguished between several different senses of two key concepts in this new synthesis: the concept of a developmental constraint on evolution and that of a developmental pattern or form. I think we can see from this brief discussion that there are several very different senses of these concepts and that these different senses reflect entirely different approaches to evolution and development. Since these are significant distinctions, it would be useful for biologists to pay more careful attention to their usage of the terms ‘‘developmental pattern’’ and ‘‘developmental constraint’’ in order to avoid ambiguity and confusion. Accordingly, I suggest the following terminology which help clarify thinking about development and evolution: / (i) Historical: ‘‘evolutionary trends’’ (constraints or patterns) (ii) Ahistorical: ‘‘physical necessities’’ (constraints or patterns) (iii) Passive: ‘‘existing limits on variation’’ (constraints) ‘‘the developmental map’’ (pattern) (iv) Active: ‘‘ontogenetic, evolutionary mechanism’’ (constraints) ‘‘structural causes in development’’ (patterns) (v) Local: ‘‘taxon-specific’’ (constraints or patterns) (vi) Universal: ‘‘taxon-neutral’’ (constraints or patterns) In addition, I suggest the following terminology to clarify talk that employs expressions like ‘‘developmental pattern’’, ‘‘developmental form’’ and so forth: Patterns in development: (i) Sequences of events: ‘‘developmental processes’’ or ‘‘mechanisms’’ (ii) Objects or properties: ‘‘developmental products’’ or ‘‘structures’’ (iii) Designs: ‘‘Developmental blueprints,’’ ‘‘programs’’ or ‘‘bauplans’’. Of course, these expressions are only suggestions and any words that preserve the distinctions made in this paper would be acceptable, Once the fundamental distinctions are grasped, word-choice can be largely a matter of convenience.
Given the distinctions used in the paper, it is fair to say that the neo-Darwinian paradigm recognizes historical, local, universal and passive developmental constraints, but it opposes active constraints. Although neo-Darwinians can recognize ahistorical constraints on evolution, they are not inclined to search for these constraints, given their historical orientation. It is also fair to say that the standard, gene-centric paradigm of development recognizes historical, local, universal and passive patterns, but that it opposes any active patterns. The gene-centric view also can recognize ahistorical developmental patterns, although gene-centrists have been disinclined to search for them, given the dominance of neo-Darwinism. Given the dominance of neo-Darwinian and gene-centric thinking, the notions of active and ahistorical constraints and patterns will prove to be most controversial, since the existence of such constraints and patterns would challenge standard views about the nature of inheritance, evolution, ontogeny and genetic regulation. Whether there are any active and/or ahistorical constraints or patterns is an empirical issue whose outcome depends on further experimental investigation into developmental mechanisms, processes, and on further research on the history of life on Earth.
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