Science Developmental 10:1 (2007), pp 30 34
DOI: 10.1111/j.1467-7687.2007.00560.x
Blackwell Publishing Ltd
Endless minds most beautiful
Barbara L. Finlay
Department of Psychology, Cornell University, USA
Abstract
The marriage of evolution and development to produce the new discipline evo-devo in biology is situated in the general history of evolutionary biology, and its signicance for developmental cognitive science is discussed. The discovery and description of the highly conserved, robust and evolvable mechanisms that organize the vertebrate body plan and fundamental physiology have direct implications for what we should investigate in the evolution of behavior and cognition.
There is a grandeur in this view of life . . . from so simple a beginning, endless forms most beautiful and most wonderful have been, and are being, evolved. (Charles Darwin, The origin of species, 1859)
Evolution itself evolves, as evolving organisms come to carry the history of successful solutions to the recurring challenges of life on earth in their genomes and in their epigenetic expectations of the structures the environment will support and inform. Our understanding of evolution has also evolved, very rapidly of late. The title of this essay is a double-reference, not only to the often-quoted last sentence of The origin of species but also to Carrols recent book Endless forms most beautiful: the new science of evo devo (2005), one exemplar of a current outpouring of both scholarly and popular works on the unexpected wealth of understanding that has arisen about the current structure of organisms, their development, and their evolution when the three domains are closely compared (just a few: Wilkins, 2001; Gould, 2002; West-Eberhard, 2003; Kirschner & Gerhart, 2005). Evo-devo as a discipline so far has primarily concerned itself with the evolution of fundamental body form, physiological processes and their genomic specication in basic vertebrate and invertebrate radiations, with some consideration as to types of mechanisms that emerge when nervous systems elaborate themselves. This essay will have two parts, the rst a bit of didactic scolding about the necessity for developmental scientists to keep themselves informed of progress in evolutionary biology, including a brief outline of the history of evolutionary biology. The second part is an exhortation to begin including this new view of evolution into developmental science, with some specic suggestions. I will contend
that a good majority of psychologists, cognitive scientists, biomedical researchers, and even biologists do not understand the implications of current work in the evolution of development and employ instead an outmoded gene/ environment conceptual scheme that ill suits what we now know is out there. I will borrow from Gerhart and Kirschners several expositions of the kinds of organization in organisms that are evolvable (1997, 2005) and suggest how their concepts might be imported into developmental science.
A very brief history of evolution
Darwins Origin of species and subsequent works concerned themselves with the historical relationships of current species, with the insight of natural selection and sexual selection: that natural variations in organisms ability to survive, nd mates and reproduce, if heritable, inevitably produce evolution in the traits animals possessed. This argument was based on the reasonable assumption of selection on a distribution of small random variations, accumulating over long evolutionary time, which could produce anything from quantitative variation in morphology for example, beak length to a novel complex organ for example, an eye. Darwin knew little of the quantitative aspects of heritability and nothing about the actual genetic mechanisms that preserve information about a particular organisms attributes over generations. The Modern Synthesis, germinating with Mendel, to Watson and Crick, to the current vast number of individuals working on transcribing the genome, synthesizes the Darwinian view of adaptation, selection and evolution with its mechanism the particular features that DNA
Address for correspondence: Barbara L. Finlay, Department of Psychology, Cornell University, Ithaca, NY 14853, USA; e-mail: [e-mail] 2007 The Author. Journal compilation 2007 Blackwell Publishing Ltd, 9600 Garsington Road, Oxford OX4 2DQ, UK and 350 Main Street, Malden, MA 02148, USA.
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as a molecule confers on the process of evolutionary change. Just how genes replicate, the kinds of errors made in this process, how genes are transcribed to proteins, and how proteins typically build cells confers an enormous amount of structure onto the kinds of organisms that are possible, and changes permissible. Within this context, variations observed are assumed to be essentially random. In the modern synthesis, as described most eloquently by Dawkins (1976), the fundamental component of evolution becomes the gene, the digitally self-replicating unit that clothes itself in a phenotype and whose success is measured in its replications. The unit of evolution is not the individual organism and most assuredly not the species. At a mechanistic level, the operation done by a gene was thought to be explicit: each gene codes a protein (but see Pearson, 2006). These proteins in turn may have diverse functions: they could control what other parts of the genome are expressed and how long by altering the packaging and transcription of the DNA molecule; as enzymes or components of enzymes they could chaperone the construction of diverse types of structural or signaling molecules; or they could become parts of the organisms signaling or structural components directly, for example, as a neurotransmitter or a component of muscle. Dawkins particularly has been at pains to defend the essential tenet of gradualism in Darwins view: that any structure, no matter how complex and precise, can be built up in small increments by selection from random variation, with each new stage adaptive compared to its predecessor. For structures built de novo this must certainly be true, and the modeling of these processes is quite persuasive. The eye, an organ Darwin was puzzled to explain, can be built in enumerated steps, each a little better than the one before, i.e. an eyespot to register light; protection of the eyespot; several units amid the spot to confer directionality and so forth. In fact, across phyla every diverse kind of intermediate eye can be found, though of course the point is that no particular eye in an existing animal is on its way toward a goal of greater complexity or better design and each eye is satisfactory for its particular niche (Land & Nilsson, 2001; Fernald, 2004). The rst mechanistic account of how genes work, necessarily oversimplied in its beginnings, coupled with the idea that every component of an organism is adaptive with respect to its immediate, or immediately historical, environment produced gigantic research initiatives, which have produced both remarkable successes and remarkable failures. The rst enterprise is to locate the gene for X where X might be a single structural or signaling protein, like an opsin, or a membrane receptor (or their disorders, color blindness or muscular dystrophy, for example), or a trait of extreme complexity with
2007 The Author. Journal compilation 2007 Blackwell Publishing Ltd.
respect to a single protein, like reading or intelligence (or their disorders, dyslexia or retardation). Of course, no sensible researcher would presume a single gene for every nameable trait, and the rapid invention of technology of immense complexity for identifying multiple genes that contribute to smaller and smaller amounts of the variation in complex traits is surely one of the major achievements of current genomic work. However, even for simple traits, considering that genes are duplicated and redundantly represented in multiple body components, often with radically different functional roles in their separate sites, and that the effect of a gene may be the control of the duration or amount of expression of another gene at a particular point in development, that expression dependent on the immediate environmental context (these features of the genome to be discussed more later), it is remarkable that this approach ever works. Keller and Miller (2006) have an excellent review of the conceptual and empirical literature of the genetics of mental disorders that illuminate the implicit models we bring to the genetics of complex traits. A second enterprise related to the explicit gene mechanism/ universal adaptation view is the current reincarnation of the just-so story in the eld of evolutionary psychology (Barkow, Toobey & Cosmides, 1995). Some just-so stories are in fact just-so, and the attempt to nd the evolutionary roots of human behavior is entirely laudable, though the Pleistocene may not be far enough to excavate. However, there are some odd mistakes in logic that crop up repeatedly in explanation of human behavior, which I will expand on a bit before returning to the present stage in the account of the evolution of evolution.
Sources of predictability and universality
One maddening habit of the popular press, many introductory textbooks, and a large percentage of social scientists at any university is to contrast biological and cultural, where biological implies predictable, universal, rule-based and genetic, and cultural variable, undened and plastic. In fact, universality is often taken as explicit evidence of the genetic determination of some behavior or cultural pattern (for example, Buss & Schmitt, 1993). The secondary assignment of a political stance to preference for one or the other class of explanation is more maddening still. It just isnt so. The reader is referred to Jablonka and Lambs Evolution in four dimensions (2005), an entertaining account of how genetic, epigenetic, behavioral and cultural transmission of information can each produce complete predictability or variability in simple or complex traits of interest, from which these examples are generally drawn. For example, all the cells in any individuals liver
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are genetically identical to the cells in the same individuals brain, yet in each organ its stem cells reliably produce only cells of the appropriate type, this controlled by epigenetic factors (of either ultimate environmental or genetic origin) which control which genes will be expressed and what environmental information sampled. In the behavioral realm, consider the identical genomes of queen, worker and nurse bees, induced by each individuals environmental history to produce diverse behavioral capacities. Jablonka and Lamb describe and populate an alternative planet with as diverse species as earths, whose genomes are identical to each other and whose diversity is produced entirely by known epigenetic mechanisms, and is heritable i.e. transferred from one generation to the next, but with the same underlying DNA. In contrast to the usual argument, the environment can be an extreme source of stability for nervous systems and behavior. For all of the history of life on earth, the sun has risen and set each day, and the genome takes in this information to set its internal clocks (Fernald, 2004). The stability of the statistics of the visual world and what sort of data reduction best expresses its structure in combination build visual systems of completely interleaved genetic and learned structure (Field, 1994). The more so when animals must inhabit a particular kind of niche if it is required that you have parents to survive, only crude mechanisms need orient you to the parent, and general learning mechanisms can take it from there, building species-specic preferences for free (Johnson & Morton, 1991). Basic statistical learning can extract from the necessary parental environment basic regularities of language; operant learning the sexiest way to sing or talk (Goldstein, King & West, 2003). Cultures learn what food supports you and what poisons you, and what a group ingests may stay stable for centuries without any individual ever exploring the limits of the edible in their environment. There is a lot of hard work to be done tracing the sources of stable information structures through the genome, and through epigenesis, individual and cultural learning. Understanding of language, emotional communication, the elaboration of the concept of agency and theory of mind, the development of behavioral control are all current topics that would benet from the evo-devo frameworks to be described. Finally, it would also do well to remember that there is nothing particularly liberal about the environment that contrasts with the conservatism of the genome.
Unexpected developmental structure in evolution
My colleagues and I have extended this account in several earlier papers (Finlay, 2005; Finlay, Cheung &
2007 The Author. Journal compilation 2007 Blackwell Publishing Ltd.
Darlington, 2005). This section is a prcis of the empirical and interpretational changes that began in the early 1990s when it became possible to identify regulatory genes and the proteins that are expressed in early development across phyla. The attention-getting demonstration for many was the experiment that a regulatory gene, Pax-6, which in a mouse or human directs the organization of an eye in its domain of expression, if inserted into a Drosophila embryo, directs expression the of a Drosophilaspecic compound eye where it is placed (Callaerts, Halder & Gehring, 1997). Subsequently, extensive conservation of the regulatory genes that direct the polarity and segmental organization of the vertebrate and invertebrate body plan was demonstrated, as well as the conservation of particular developmental mechanisms in the case of the brain, for example, the molecules directing axon extension and halting, or synaptic stabilization through calcium signaling. This conservation of developmental mechanisms served to back-illuminate the conservation of a wide number of fundamental cellular processes. Because it is commonplace to do so, for example, researchers dont often view it as a remarkable fact that it is possible to use the marine mollusk Aplysia, pigeons and rats all as animal models for learning, both at the level of cellular mechanisms and at the level of their organismal responses to various classes of reward regimes (Greenough & Bailey, 1988). Why this conservation? The general answer is that while evolution can t each creature into an adaptive niche by successive small steps, all life on earth has also been repeatedly ltered through local and global catastrophes for those developmental and physiological mechanisms that are robust and stable to environmental challenges, that are by denition evolvable. A version of the modern synthesis, integrating the properties of DNA itself into evolutionary history, comes in as well: the propensity of the genome to evolve by the general tactic of duplicating (or multiplying) itself at the level of the single gene, chunks of genes or the whole genome. This tactic has the advantage of conserving basic organismal mechanisms while allowing local temporal or spatial variations in the duplicated gene, and allows access to old adaptations in a way a single, constantly overwritten set of genes could not. Gerhart and Kirschner, in their two books Cells, embryos and evolution (1997) and The plausibility of life: Resolving Darwins dilemma (2005), have begun to analyze the organizational properties of conserved and evolvable developmental systems. To conclude, I will briey recount the properties they have proposed and argue that we should export them wholesale as a way of examining brain structure and cognition, because the requirements of appreciating and moving in the environment, predicting the future, nding mates and raising
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young are fully as ancient as the body plan, and should benet from the same explanatory scheme.
Four properties of evolved and evolvable systems
The features Gerhart and Kirschner observe are the following. First, fundamental physiological processes are conserved. In the case of cell biology, they are referring to such processes as oxidative metabolism, the transcription of genes and construction of proteins, and basic signaling systems between extracellular and intracellular space. I have already mentioned the associative learning demonstrated by Aplysia, rats and humans as one example of a conserved physiological mechanism shown by (arguably) all nervous systems we have investigated. We should attempt to expand this category to look for similar basic solutions to data reduction and representation systems, motor control systems and homeostasis. In addition, it is quite possible that any nervous system needs a fundamental repertoire of distinct learning mechanisms. To list a few candidates for such a list, consider these processes characterizing large mammalian brain systems: associative learning with different time constants; errordriven learning, as in the cerebellum; learning by reinforcement (Atallah, Frank & OReilly, 2004), and learning through prediction (Elman, 1990). It would be interesting to re-examine development with an eye to how fundamental operations like these are rst deployed and integrated. Second, they argue for modularization of function, as is seen so repeatedly in the segmentation of the body plan and also in the nervous system. It is important to note here that the word module is used in a different way in biology than it is in cognitive science. Segmentation is a common embryological feature that is closely related to the duplicate and vary genomic strategy previously described, and allows initially identical structures to diverge in function, for example, as in spinal cord segments innervating the leg versus the body wall. Since the same genes are being deployed in each segment, in order to produce variation, local modications of genetic cascades must be protected from constraining effects of pleiotropy. To take a familiar example to cognitive scientists, while the gene Fox P2 may be linked in several taxa to improvements in rapid vocal behavior (Teramitsu, Kudo, London, Geschwind & White, 2004), but is expressed widely in the developing organism, and to change the amount of its expression in every location it is expressed could not possibly be a benet. The brain presents us with a diversity of potential modular structures in this sense, from the segments of the spinal cord, the rhombomeres and prosomeres that are the initial
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segments of the brain, the cerebellum and the repeating columns of all the cortical structures of the forebrain, hippocampus, neocortex and olfactory cortex. Of course, one of the most central and persistent arguments in cognitive science is whether there is modularity in language at the functional level and whether this modularity has a direct mapping onto brain parts. I would suggest that we have become mired in the discussion of this particular case, and should step back and return to the biological theme and variation version of modularity and whether it might have application to cognition more generally. For example, some region of the cortex might become specialized in membrane receptors optimal for rapid temporal processing useful for speech, and retain other areas better for processing with a larger time window (also useful for speech). If these areas were modularized genetically this means only that genetic variation could proceed independently in these areas, but it does not mean that the areas, in maturity, might not directly commingle their physiological and functional processing, for a representation of speech that integrates the entire spectrum of time windows the language faculty is not identical with the area with the receptor tweak. A third property observed in evolving systems is weak linkage between modules allowing for recombination. The G-protein signaling system is an example of this, where different extracellular signals may become attached to this common system linking the environment to fundamental cellular processes, allowing for recombination and integration of external signals to activate intracellular mechanisms. This is an interesting way of considering brain circuitry, both in the specic case of what is connected to what across species, and at the metaphorical level of function. Space precludes development of this idea, in this essay, but note the similarity of this concept to the idea of cognitive penetrability that has produced a massive literature in diverse elds of psychology. Finally, evolved cellular systems show exploratory behavior, particularly in development expressing a wider variety of metabolic and signaling possibilities than mature cells do. This is obviously a feature of organisms in which nervous systems must play a central role, and is one of the central areas of study in cognitive science. Exploratory behavior is rarely considered systematically as an evolutionary phenomenon in cognitive science, however, with a few tantalizing exceptions: for example, modeling of the Baldwin effect in language evolution. Burghardts The Genesis of Animal Play (2005) is a beautiful example of a systematic cataloging of the causes and possible functions of a particular type of exploratory behavior both in phylogeny and ontogeny. All of these properties in concert produce facilitated variation, evolvability, organisms...