Evolutionary Developmental Biology

[Rob]

The fact about science is that everyone who had made a serious contribution to it is aware, or very strongly suspects, that the world is not only queerer than anyone has imagined, but queerer than any one can imagine. This is a most disturbing thought, and one flees from it by stating the exact opposite. (Clark R. 1968, citing a letter from J.B.S. Haldane to Robert Gaves.)

-- Reid, Robert G. B. (1985) Evolutionary Theory: The Unfinished Synthesis. New York: Cornell Univesity Press. p. 117.

The key to development, form, and function in multicellular organisms is differential gene expression, and the most intimate knowledge of the genetic code reveals nothing about the implementation of its information in space and time.

-- Reid, Robert G. B. (1985) Evolutionary Theory: The Unfinished Synthesis. New York: Cornell Univesity Press. p. 46.

A little over 25 years later our "intimate knowledge" has grown significantly, providing insights which have yet to be fully intergrated into evolutionary theory:

Animal body plans, their structures and the functions with which their morphology endows them, are the integrals over time and space of their successive developmental processes.... At the outside, development is mediated by the spatial and temporal regulation of expression of thousands of genes that encode the diverse proteins of the organism, and that catalyze the creation of its nonprotein constituents. Deeper in is a dynamic progression of regulatory states, defined by the presence and state of activity in the cell nuclei of particular sets of DNA-recognizing regulatory proteins (transcription factors), which determine gene expression. At the core is the genomic apparatus that encodes the interpretation of these regulatory states. Physically, the core apparatus consists of the sum of the modular DNA sequence elements that interact with transcription factors. These regulatory sequences "read" the information conveyed by the regulatory state of the cell, "process" that information, and enable it to be transduced into instructions that can be utilized by the biochemical machines for expressing genes that all cells possess. The sequence content, arrangement, and other aspects of the organization of these modular control elements are the heritage of each species. They contain the sequence-specific code for development; and they determine the particular outcome of developmental processes, and thus the form of the animal produced by every embryo. In evolution, the alteration of body plans is caused by changes in the organization of this core genomic code for developmental gene regulation. (Davidson 2006: 1-2)

... [T]he system level organization of the core genomic regulatory apparatus, and how this is the locus of causality underlying the twin phenomena of animal development and animal evolution. Because the sequence of the DNA regulatory elements is the same in every cell of each organism, the regulatory genome can be thought of as hardwired, and genomic sequence may be the only thing in the cell that is. Indeed that is a required property of gene regulatory elements, for they must endow each gene with the information-receiving capacity that enables it to respond properly to every conditional regulatory state to which it might be exposed during all phases of the life cycle, and in all cell types. For development, and therefore for major aspects of evolution, the most important part of the core control system is that which determines the spatial and temporal expression of regulatory genes. As used here, "regulatory genes" are those encoding the transcription factors that interact with the specific DNA sequence elements of the genomic control apparatus. The reason that the regulation of genes encoding transcription factors is central to the whole core system is, of course that these genes generate the determinant regulatory states of development. (Davidson 2006: 2)

There follow several important and general principles of organization of the developmental regulatory apparatus, that is, of the control machinery directing expression of the regulatory genes themselves. First, signaling affects regulatory gene expression: The intercellular signals upon which spatial patterning of gene expression commonly depends in development must affect transcription of regulatory genes, or else they could not affect regulatory state. Therefore, the transcriptional termini of the intracellular signal transduction pathways required in development are located in the genomic regulatory elements that determine expression of genes encoding transcription factors. Second, developmental control systems have the form of gene regulatory networks: Since when they are expressed given transcription factors always affect multiple target genes, and since the control elements of each regulatory gene respond to multiple kinds of incident regulatory factor, the core system has the form of a gene regulatory network. That is, each regulatory gene has both multiple inputs (from other regulatory genes) and multiple outputs (to other regulatory genes), so each can be conceived as a node of the network. Third, the nodes of these genes regulatory networks are unique: Though it is not a priori obvious, each network node performs a unique job in contributing to overall regulatory state, in that its inputs are a distinct set, just as the factor it produces has a distinct set of target genes. Fourth, regulatory genes perform multiple roles in development: The repertoire of regulatory genes is evolutionarily limited, and all animals use more or less the same assemblage of DNA binding domains, which define the classes of transcription factor. However, given factors are frequently required for different processes in different forms of development, and they are often used for multiple unrelated purposes within the life cycle. Thus, both within and among animal species, many regulatory genes must be able to respond to diverse regulatory inputs that are presented in various space/time places in the developing organism. (Davidson 2006: 2-3)

A general character of genomic programs for development is that they progressively regulate their own readout, in contrast, for example, to the way architects' programs (blueprints) are used in constructing buildings. All of the structural characters of an edifice, from its overall form to local aspects such as placement of wiring and windows, are prespecified in an architectural blueprint. At first glance the blueprints for a complex building might seem to provide a good metaphoric image for the developmental regulatory program that is encoded in the DNA. Just as in considering organismal diversity, it can be said that all the specificity is in the blueprints: A railway station and a cathedral can be built of the same stone, and what makes the difference in form is the architectural plan. Furthermore, in bilaterian development, as in an architectural blueprint, the outcome is hardwired, as each kind of organism generates only its own exactly predictable, species-specific body plan. But the metaphor is basically misleading, in the way the regulatory program is used in development, compared to how the blueprint is used in construction. In development it is as if the wall, once erected, must turn around and talk to the ceiling in order to place the windows in the right positions, and the ceiling must use the joint with the wall to decide where its wires will go, etc. The acts of development cannot all be prespecified at once, because animals are multicellular, and different cells do different things with the same encoded program, that is, the DNA regulatory genome. In development, it is only the potentialities for cis-regulatory information processing that are hardwired in the DNA sequence. These are utilized, conditionally, to respond in different ways to the diverse regulatory states encountered (in our metaphor that is actually the role of the human contractor, who uses something outside of the blueprint, his brain, to select the relevant subprogram at each step). The key, very unusual feature of the genomic regulatory program for development is that the inputs it specifies in the cis-regulatory sequences of its own regulatory and signaling genes suffice to determine the creation of new regulatory states. Throughout, the process of development is animated by internally generated inputs. “Internal” here means not only nonenvironmentali.e., from within the animal rather than external to it but also, that the input must operate in the intranuclear compartments as a component of regulatory state, or else it will be irrelevant to the process of development. (Davidson 2006: 16-17)

-- Davidson, Eric H. (2006) The Regulatory Genome. Amsterdam: Academic Press.

SUPERGENES ARE IN COMMAND

We have just seen that the cells of a pluricellular organism all have the some genes. If they differentiate into distinct cell types, it is because they do not express the totality of their genes but practice a selection that varies according to cell type. Otherwise, all the cells of an organism would be identical. Cells thus contain "genetic switches," systems that switch on or off the expression of certain genes. This control is carried out by proteins, called transcription factors, that either stimulate or repress the transcription of the genes involved. These proteins being themselves the products of genes, which are subject in turn to a similar regulation, genomes house a whole complex and hierarchical network of regulatory genes--the term "supergene" is sometimes used--next to those that code for "housekeeping," that is, for enzymes, structural proteins, etc. (de Duve 2002: 155)

Regulatory genes are known in bacteria, in which they are involved, among other things, in the adaptation of metabolism to different nutrients. A historic example, which made the fame of the French investigators Fançois Jacob and Jacques Monod, concerns the manner in which bacteria transferred to a medium containing milk sugar (lactose) as sole food supply switch on the genes coding for enzymes specifically needed to use this sugar. Regulatory genes are, however, much more numerous in eukaryotes, and their number increases with the complexity of the body plan of the species. Such is not the case for housekeeping genes, for which there is hardly any difference among species. Or when there is a difference, impoverishments rather than enrichments most often go together with increasing complexity. Witness the many vitamins we are unable to make, whereas humble bacteria do so without difficulty.... In spite of the advances of biotechnologies, we are still far from mastering evolution. (de Duve 2002: 155-156)

The discovery of regulatory genes has allowed us to discern, at least in principle, the mechanisms that direct and control development. Once fertilized, the egg cell divides into two cells, which similarly divide to produce four, which divide into eight, and so forth. Soon, in the course of this process, the cells cease to be identical. Depending on their location in the ensemble, they start expressing or stifling certain regulatory genes, with the consequence that the proteins translated from those genes create concentration gradients between the areas where they are produced and those where they are not. These gradients influence in unequal fashion the expression of other genes, which in turn influence others, in a cascade whose complexity soon exceeds the limits of our imagination and even anything that can be simulated by the most powerful computer programs. At the end of the game, there is an oak plantule, a jellyfish larva, or a newborn baby, depending on the program written into the genome. (de Duve 2002: 156)

Such a mechanism has long been suspected. Already, in the early part of the twentieth century, the German embryologist Hans Spemann demonstrated, by means of remarkably skillful and ingenious experiments, the existence of what he called morphogenetic--shape creating--gradients in embryos. Modern biology is beginning to flesh out those gradients in terms of genes and their protein products. Particularly important has been the discovery of so-called homeogenes, whose control is so wide-ranging that a single mutation of such a gene may cause a fruitfly to grow an extra pair of wings or to sprout additional antennae on its head. Homeogenes have been recognized throughout the pluricellular world, from simple fungi to the most complex animals. (de Duve 2002: 156)

EVOLUTION OCCURS BY WAY OF DEVELOPMENTAL PROGRAMS

With these elementary notions we may now address the problem of evolution, which is conditioned, as we have seen, by changes in the developmental program of organisms. This fact implies almost necessarily that the underlying genetic changes have as targets regulatory genes. But all depends on the cell type to which the modified gene belongs. Thus, a mutation in a skin, stomach, or brain cell may start a new cell line, for example, a cancerous one. But the individuals concerned do not, if they reproduce, give birth to descendants afflicted with cancer of the skin, stomach, or brain. Only genetic modifications of a germ cell that will eventually be involved in the generation of a new individual can be of significance for evolution. [See Epigenetics] Such modifications are the only ones that can influence the development of the fertilized egg. They are also the only ones that can be hereditarily transmitted, as they affect all the cells of the organism, including those that will become germ cells in turn and will give rise to the next generation. (de Duve 2002: 156-157)

-- de Duve, Christian Nobel Laureate. Life Evolving: Molecules, Mind, and Meaning. Oxford: Oxford University Press; 2002: 155-157.

Chapter 4: Development and Evolution

Constraint and Saltation

Developmental biology has long been a focus for evolutionary theory (Bonner 1982; de Beer 1958; Garstang 1922; Goldschmidt 1938; Gould 1977; Haeckel 1866; Raff 1996; Raff and Kaufman 1983; Waddington 1940). Evolution can be seen as a change in developmental programs that elaborate the phenotype. The effects of genes and the range of genetic variation would best be investigated on a mechanistic basis, yet until the 1990s, we had only a very small window on this enormously important developmental landscape.

Once we can understand the nature of development and how it constructs the phenotype, we confront anew some of the age-old questions of evolutionary biology. Development is legendary for its organization, sometimes appearing to be remarkably automatic and even self-organizing. The strong integration of the developmental process might not easily be breached by a mutant, which would disrupt fundamental and tightly integrated cellular and molecular processes. This would suggest a force for conservatism in evolution. On the other hand, the tremendous organization of developmental processes suggest to many that simple genetic changes might beget enormous salutatory evolutionary change.

The Janus-headed coin of development is illustrated well by the evolutionary change of the tail in ascidian tadpole larva, which has been lost in evolution several times independently (Jeffery 1997). (....) This major switch in morphology is associated with a mundane larval adaptation for reduced dispersal by the tail-less form. (Tadpole larvae are not brilliant dispersers, either.) Tail-less development results from the abbreviation of developmental programs owing to maternal message and gene regulation in the zygote. The zinc-finger gene Manx is expressed in tailed species but is downregulated in tail-less species, which suggests a simple mechanism for a momentous developmental reorganization, dropping some of the lynchpins of the chordate anatomical plan (Swalla and Jeffery 1996).

The message told by the Manx gene is not clear, despite teh elegant experimental results. On the one hand, it tells us that it is rather easy to lose the tail and a host of associated developmental trajectories (e.g., notochord, tail, otolith, and muscle cells). (....) If it is that easy, why is it so uncommon? Again, we face teh two faces of constraint and possibility for major change.

Time and again, the concepts of constraint and saltation have been formulated in terms of development. Developmental constraints are nonrandom channelizations of evolutionary direction due to limitations imposed by complex interactions of gene expression and epigentic interactions, such as tissue inductions, in the developing organism. The disruption of such interactions may strongly influence fitness and therefore restrict evolutionary change. In the context of development, saltations are rapid evolutionary fixations of phenotypic discontinuities guided by developmental controls, which do not permit continuity of form in polymorphic populations.

The Holy Grail: Connecting an Understanding of Genes and Development

(....) We are now at the threshold of a completely new period, in which development and genetics are being connected in great detail. At first, this became apparent from the emerging understanding of a widespread homeobox sequence that united all of the triploblastic animals at least. Now, modern methods of gene sequencing, manipulation of gene expression, and tracing of spatial patterns of gene expression have resulted in an explosion of information that is not leading, as yet, to many useful evolutionary rules. So far, we are seeing the same errors promulgated in lionizing past laws of ontongeny and phylogeny. Beliefs in major genetic revolutions, master switch genes, and other universals are beginning to form a modern version of the ontogentic laws of old, with little consideration for the possibilities of convergence in developmental gene function. Nevertheless, the new tools allow us to better peak through the curtains, and the early flush of enthusiasm will likely be followed by substantial advances in development evolution.

Phylogeneticists and Developmentalists

(….) The developmentalists claim that “the diversity of structures that have been formed through the process of evolution is constrained by the rules which govern pattern formation during development” (Stock and Bryant 1981, p. 432). As such, evolutionary change of necessity is the evolution of developmental sequences. The individual, therefore, is treated in terms of its entire ontogeny, and development is therefore both the constraint and target of selection. There is a developmental toolbox, and certain tools may be used in many contexts, but this does impose a possibly limited set of alternative developmental pathways.

(….) [M]orphological structures often come as complete structures or not at all. Of equal interest is the importance of localization in development. Embryos develop only as the result of a complex series of timing events that bring different cells into contact or place cells or molecules of restricted developmental potency in a proper environment for induction. The spatial position of cell groups seems crucial in the generation of morphological patterns, owing to

· Localized intercellular movement and regional movement of dissolved substances that often set gene expression in motion (Garcia-Bellido, Rippoil, and Morata 1973; Summerbell 1981; Turing 1952; Wolpert 1969)
· Transcellular electric fields (Jaffe and Stern 1979; Nuccitelli 1983)
· Mechanochemical interactions (e.g., Odell, Oster, Alberch, and Burnside 1981; Oster, Murray, and Harris 1983)
· Specialized cell adhesion molecules (Edelman 1986)

Must these not influence the direction of evolution? These two phenomena integrity of structure and topological restriction of development suggest that an embryo can be transformed in only limited number of directions during the process of development and evolution. That is the fundamental message about form that Richard Goldschmidt’s pioneering book Physiological Genetics (1938), derived from Spémann (1938), underscored so well.

Some examples of developmental mutants show the discontinuous and often spectacular nature of possible structural change. Consider the cyclops mutant (Bowen, Hanson, Dowling, and Poon 1966) of brine shrimp males. After the fourth instar, the lateral eyes move forward and fuse together, forming a single large compound eye by the ninth instar. During this fusion, the ganglia and nerves of the two optic stalks fuse; the resultant eye resembles the normal medial eye of the cladoceran Leptodora. Thus, a quirk of development has caused a structure to change from that characteristic of one taxonomic order to another! The development of the vertebrate limb shows similar quantum steps.



(….) A developmental notion of macromutation springs from the nature of development described above. If a simple transplant places toes on wings or replaces scales with feathers, why couldn’t evolution occur in major steps? Some have seen such discontinuities in development as a vehicle for major evolutionary jumps (Goldschmidt 1940; Gould 1980a; Lovtrup 1974; Maderson et al. 1982; Schinderwolf 1936, 1950), or at least see them as possible stuff of major saltations (Alberch, Gould, Oster, and Wake 1979; Frazzetta 1970)

-- Levinton, Jeffrey S. Genetics, Paleontology, and Macroevolution. Cambridge: Cambridge University Press; 2001; pp. 157-162.

[Rob]

Does evolutionary change often proceed by saltation down channels of historical constraint?

Internally channeled evolution (orthogenesis) has been intimately linked with discontinuous change (saltationism) in the history of structuralist thought (with the model of “Galton’s polyhedron” serving as the classical image for the connection). The linkage isn’t physically necessary or logically impelled, for some orthogeneticists have favored gradualism (C. O. Whitman, pp. 383-395), whereas some saltationists have rejected internal directionality (Hugo de Vries, pp. 415-451). But in expanding the causes of evolutionary change beyond the incremental gradualism of externally directed Darwinian selection, and in regarding internal channels of developmental constraint as important mediators of phyletic trending, most advocates of formalist or stucturalist explanation (Bateson, D’Arcy Thompson, and Goldschmidt, for example) have supported some linkage of channeled directionality with at least the possibility of saltational movement down the channels -- of only because the potential phyletic analog of such ontogenetic phenomena as metamorphosis seems intriguing and worth exploration. (Gould 2002: 1142)

Thus, with the reintroduction of internal channeling by historical constraint (based on genetic homology) into our explanatory schemes, we must ask whether saltational themes (that had been even more firmly rejected by the Darwinian Synthesis) can also advance a strong case for a rehearing. My own conclusions are primarily negative (hence my parsing of this theme as a scherzo, and as the shortest movement of my analysis), but the subject clearly merits some airing (and undoubtedly holds limited validity), if only as a sign of respect for the intuition of so many fine evolutionists, throughout the history of our subject, that structural channeling -- now clearly affirmed as a theme of central importance -- implies a serious consideration of saltational mechanics. (Gould 2002: 1142)

… In the context of debate over punctuated equilibrium, notions of “rapidity” depend strongly upon the time scales of their context. Invocations of suddenness raise quite different evolutionary issues at each level of consideration. In this section, I shall discuss true saltation (discontinuous changes, potentially across a single generation, and usually mediated by small genetic alterations with major developmental effects), and not punctuational patterns at larger scales of time (continuous changes that would be regarded as slow and gradual across human lifetimes, but that appear instantaneous when scaled against the millions of years in stasis for a resulting species or developmental Bauplan). (Gould 2002: 1142)

Nevertheless, I note … the relevance of developmental themes to punctuational patterns at these larger, and very different, scales of explanation. For example, several authors have argued that our emerging concepts of deep homology might help to elucidate such marcroevolutionary “classics” of large-scale rapidity as the Cambrian explosion. Under Lewis’ (1978) original model of evolution from ancestral homonomy (multiple, identical segments by accretion of duplicated Hox genes to achieve differentiation of specialized parts along the body axis, the Baupläne of the major animal phyla must originate separately and gradually [same claim was made about evolution of eyes, hearts, etc.], as each added developmental component permits further differentiation. How, then, could so many basic designs make such a coordinated first appearance in five to ten million years, unless some genetic glitch or unknown environmental trigger initiated a rampant episode of duplication in many lineages simultaneously, or unless the pattern only represents an artifact of preservation, rather than the actual macroevolutionary event? (Gould 2002: 1142-1143)

But the first fruits of evo-devo … have reversed this scenario by documenting a full complement of Hox genes in the most homonomously segmented invertebrate bilaterian phyla, thus suggesting the opposite process of loss and divergence for the differentiation of numerous complex and specialized patterns from initial homonomy (De Rosa et al. 1999). The puntuational character of the Cambrian explosion seems far easier to understand if the basic regulatory structure already existed in ancestral homonomous taxa, and the subsequent diversification of Baupläne therefore marks the specialization and regionalization of potentials already present, rather than a dedicated and individualized addition for each major novelty of each new Bauplan. The Cambrian explosion still requires a trigger (see Knoll and Caroll, 1999, for a discussion of possible environmental mediators, including the classical idea of an achieved threshold in atmospheric oxygen), but our understanding of the geological rapidity of this most puzzling and portentous event in the evolution of animals will certainly be facilitated if the developmental prerequisites already existed in an ancestral taxon. (Gould 2002: 1143)

Knoll and Carroll (1999, p. 2134) stress this point in a section of their article entitled “Cambrian diversification: So many arthropods, so little time.” The add …:

The entire onychophoran-anthropod clade possesses essentially the same set of Hox genes that pattern the main body axis. Thus, Cambrian and recent diversity evolved around an ancient and conserved set of Hox genes …. Most body plan evolution arose in the context of very similar sets of Hox genes, and thus was not driven by Hox gene duplication … Bilaterian body plan diversification has occurred primarily through changes in developmental regulatory networks rather than the genes themselves, which evolved much earlier.

… [T]he possibility and meaning of evolutionary saltation at the organismic level of discontinuity across generations we may at least assert a case for plausibility, so that, at the very least, this perennially contentious subject will not be dismissed a priori. First of all, we cannot deny either the existence of such large and discontinuous phenotypic shifts in mutant organisms, or the conventional basis assigned to them: small genetic alterations with major developmental consequences. For example, a single base substitution in bicoid, the maternal gene product that sets the AP axis by supplying positional information within the Drosophila larva, can reverse the axes of symmetry (Frohnhofer and Nusslein-Volhard, 1986; Struhl et al., 1989). Of this and other cases, Akam et al., in the introduction to their 1994 book on The Evolution of Developmental Mechanics write (1994, p. ii): “It is commonplace of developmental genetics that minimal genetic change can lead to the most dramatic morphological effect.” (Gould 2002: 1143-1144)

(....) Of this interesting correlation between constraint and saltation, Fitch concludes (1997, pp. 166-167): “Because single genetic changes can be postulated for some of the evolutionary change in the male tail, I predict that many evolutionary changes in morphology will have resulted mainly from changes in single loci … Because the power of selection is limited by variation, such developmental constraints could cause significant bias [directionality] in the evolution of form.” (Gould 2002: 1147)

-- Gould, Stephen J. The Structure of Evolutionary Theory. Cambridge: Harvard University Press; 2002; pp. 1142-1144.

Gould goes on to caution that it is to early to tell what role such "saltationary" mutations may play in evolution, (see p. 1144 for valid reasons to be cautious), saying

In any case, and however important such saltational changes may be in establishing fundamental evolutionary novelties (my own betting money goes on a minor and infrequent role), phyletic discontinuity at lower taxonomic levels, based on small genetic changes with large regulatory effects, has been documented in several cases. (Gould 2002: 1146)

My bet is that it plays a larger role than just "minor and infrequent" gradualist assumptions would lead us to believe, but with Gould caution against jumping to a priori conclusions this early in the process of uncovering and understanding these new mechanisms of evolution.

The main focus of Gould’s work, as exemplified by his Scientific American article[5] “The Evolution of Life on Earth” …, has been to curtail the thought that there is anything “progressive” about the evolutionary process.[6] In Gould’s worldview, random (contingent) events control evolution and render the process unpredictable. If one could rewind the tape of life and play it over again, says Gould, nothing like human life (or even intelligent life) would have much chance of evolving a second time. Gould has defined intelligent life as a life form capable of understanding its own evolutionary history, a definition with which I would agree. (McMenamin 1998: 239-240)

Gould’s view on contingency is a minority one, however, and others have spoken out against this rendering of life’s history. Simon Conway Morris, in his typically colorful language, argued that similar environmental conditions often cause unrelated organisms “to find the same biological solutions” because there are a limited number of ways that things can be done.[7] If the tape of life were to be rewound, the probability that any one of us would be here today is “infinitesimally small. But I’d say that the odds of an upright, two-legged, introspective organism are rather high.” (McMenamin 1998: 240)

Could such a scenario occur? To gain a fuller understanding of this question, I must first sketch out the background of evolutionary thought on the origins of animals. Yet again, we must turn to the scientific thought of German scientists. Otto Heinrich Schindewolf, in his 1950 book Der Zeitfactor in Geologie und Palaontologie (The Time Factor in Geology and Paleontology), spoke of how there were no forerunners of the Cambrian animals, but that they suddenly appeared as a result of Grossmutation, or rapid macroevolutionary change.[8] Seilacher in 1956 agreed with Schindewolf’s assessment of the evolution of the Cambrian fauna (not surprising, because Seilarcher was Schindewolf’s student), but Seilarcher went further, noting that the trace fossil makers of the Lipalian suddenly and simultaneously changed their behaviors and activities.[9] The petrogaeicum gives way to the Biogaeicum. (McMenamin 1998: 240)

Daniel I. Axelrod attacked the Schindewolf-Seilarcher rendering of the Cambrian lower boundry, saying that their ideas were not “acceptable because they do not conform to our present understanding of the evolutionary process.”[10] Here Axelrod was defending what is called the “modern synthesis” of neo-darwinian evolutionary thought. (McMenamin 1998: 240)

Neo-darwinian thought not only is at odds with the abruptness of the Cambrian evolutionary event, but also “excludes symbiogenesis except as an oddity of limited interest, mainly to cell biologists and biochemists.”[11] Now, thanks to our progress in understanding the Ediacarans, we can navigate past the Scylla of scerotic neo-darwinian thought and the Charybdis of denial of progressive evolutionary change.[12] (McMenamin 1998: 240)

[The phrase between Scylla and Charybdis has come to mean being in a state where one is between two dangers and moving away from one will cause you to be in danger of the other. Between Scylla and Charybdis is the origin of the phrase "between the rock and the whirlpool" (the rock upon which Scylla dwelt and the whirlpool of Charybdis) and may be the genesis of the phrase "between a rock and a hard place".]


[5] S. J. Gould, “The Evolution of Life on Earth,” Scientific American 271 (1997):84-91.
[6] cf. Francisco J. Ayala, “Ascent by Natural Selection,” Science 275 (1997):495-496.
[7] See p. 125 in R. Gore, “The Cambrian Period Explosion of Life,” National Geographic 184, no. 4 (1993):120-135; S. Conway Morris, “Rerunning the Tape,” Times Literary Supplement, December 12, 1991:6.
[8] O. H. Schindewolf, Der Zeitfactor in Geologie und Palaontologie (Stuttgart: E. Schweizerbart, 1950).
[9] A. Seilarcher, “Der Beginn des Kambriums als biologische Wende,” Neues Jahrbuch fur Geologie und Palaontologie, Abhandlungen 108 (1956):155-180.
[10] Page 7 in D. I. Axelrod, “Early Cambrian Marine Fauna,” Science 128 (1958):7-9.
[11] See pp. xxii-xxiii in L. N. Khakhina, Concepts of Symbiogenesis: A Historical and Critical Study of the Research of Russian Botanists, edited by Lynn Margulis and Mark McMenamin (New Haven: Yale University Press, 1992).
[12] “Progressive evolutionary change” is used here in the sense of complexification and encephalization.

-- McMenamin, Mark A. S. Discovering the First Complex Life: The Garden of Ediacara. New York: Cambridge University Press; 1998; c1998 pp. 239-240.

[Rob]

Charles Darwin always thought of embryology as one of the really important parts of his theory, and he took great pride in the way that evolution explained the similarities among embryos of different species. Natural selection in particular threw light on the nature of embryological development, in Darwin's view. At the turn of the nineteenth century, during evolution's long non-Darwinian phase, embryology continued to absorb the energies of evolutionists, although (as with everything else) phylogeny--the change of species into other species over time--was their main focus. In the 1940s, when the synthetic theory (as it was called in America; in England, it was better known as neo-Darwinism) came into being, precisely because embryology was a major part of what the synthesis's architects were rejecting, the development of individual organisms from embryos to adults was ignored. In recent years, this has changed completely, and evolutionary development (evo-devo) has become the hottest part of the discipline. Much molecular-informed activity is being directed toward an understanding of development and the ways in which it can affect the course of evolution.[3]

The most dramatic discoveries in evo-devo have been quite unexpected DNA homologies. It turns out that organisms as different as fruit flies and humans share considerable amounts of practically unaltered DNA, especially those stretches that are involved in development itself--ordering the rates and ways in which the parts of the body are formed (heads before legs and so forth). The jury is still out on the precise significance of all of this. Some seem to think that selection will now have to take a back seat in evolution: “The homologies of process within morphogenetic fields provide some of the best evidence for evolution just as skeletal and organ homologies did earlier. Thus, the evidence for evolution is better than ever. The role of natural selection in evolution, however, is seen to play less an important role. It is merely a filter for unsuccessful morphologies generated by development. Population genetics is destined to change if it is not to become as irrelevant to evolution as Newtonian mechanics is to contemporary physics.”[4]

Others find these new discoveries less threatening to the established order. Darwin himself would probably not have been particularly fazed. In his little book on orchids, written just after the Origin, he stressed how organisms use and reuse different body parts, and how things change only with good reason. Hence, the molecular homologies like all cases of phylogenetic inertia might simply reflect the fact that they do the job well in all organisms, fruit flies and humans. By analogy, “the fact that tires are round more likely means that round wheels are optimally functional than that tire companies are somehow constrained by the round shape of their existing molds. Thus phylogenetic inertia is not an alternative to natural selection as a mechanism of persistence, and evidence of the former is not evidence against the latter.”[5]

-- Ruse, Michael. The Evolution-Creation Struggle. Cambridge: Harvard University Press; 2005; p. 193.

Notes:

[3] Bowler 1996. Carrol, Grenier, and Weatherbee 2001; Raff 1996.
[4] Gilbert, Opitz, and Raff 1996, 368.
[5] Reeve and Sherman 1993, 18. Se also Darwin 1862.

-- Bowler, P. 1996. Life's Splendid Drama. Chicago: University of Chicago Press.

-- Carroll, S. B., J. K. Grenier, and S. D. Weatherbee. 2001. From DNA to diversity: Molecular Genetics and the Evolution of Animal Design. Oxford: Blackwell.

-- Raff, R. 1996. The Shape of Life: Genes, Development, and the Evolution of Animal Form. Chicago: University of Chicago Press.

-- Gilbert, S. F., J. M. Opitz, and R. A. Raff. 1996. Resynthesizing evolutionary and developmental biology. Developmental Biology 173: 357-372.

-- Reeve, H. K., and P. W. Sherman. 1993. Adaptation and the goals of evolutionary research. Quaterly Review of Biology 68: 1-32.

[Rob]

There is a quite but very important scientific revolution taking place today in our understanding of the actual paths and mechanisms of evolution. It has been going on for many years, ever since the beginning, under the name of "embryology," but lacked the technology to make the advances that molecular biology has brought within its grasp today. Its new name is Evolutionary Developmental Biology (evo-devo for short), and is revealing astonishing new facts about the paths and mechanisms of evoution that have yet to be fully understood or intergrated into existing evolutionary theory.

For example, it is still often repeated by many that:

Only three of the 11 major phyla of animals have developed well-formed, image-resolving eyes; the arthropods (insects, crabs, spiders), mollusks (octopus, squid) and vertebrates. These three types of eye are entirely independent developments. There is no connection among them, anatomical, embryological or evolutionary. This is an important realization, for it means that three times, in complete independence of one another, animals on this planet have developed image-forming eyes. It is all the more remarkable for this reason that in all three types of eye the chemistry of the visual process is very nearly the same. In all cases the pigments which absorb the light with stimulates vision is made of vitamin A. (....) How does it happen that whenever vision has developed on our planet it has come to the same group of molecules, the A vitamins, to make it light-sensistive pigments?

-- Wald, George. Radiant Energy and the Origin of Life. In The Molecular Basis of Life: An Instroduction to Molecular Biology. (Readings From Scientific American, ed.).: Freeman; 1968; pp. 302-303.

But today, with the aid of molecular biology and evo-devo, the following is now known:

Natural selection has not forged many eyes completely from scratch; there is a common genetic ingredient [Pax-6] to making each eye type, as well as to the many types of appendages, hearts, etc. These common genetic ingredients must date back deep in time, before there were vertebrates or arthropods, to animals that may have first used these genes to build structures with which to see, sense, eat, or move.

-- Carroll, Sean B. Endless Forms Most Beautiful. New York: Norton & Company; 2005; p. 72.

One particularly interesting area of research has to do with understanding the evolution and developmental biology (embryology) of organisms, a new field referred to as “evo-devo.”

“Evo-devo.” Advances in molecular biology have permitted developmental biologists to study the genetics behind the early stages of embryological development in many groups of animals. What they are discovering is astounding. It is apparent that very small changes in genes affecting early, basic structural development can cause major changes in body plans. For example, there is a group of genes operating very early in animal development that is responsible for determining the basic front-to-back, top-to-bottom, and side-to-side orientations of the body. Other early-acting genes also control such bodily components as segments and their number, and the production of structures such as legs, antennae, and wings. Major changes in body plan can come about through rather small changes in these early-acting genes. What is perhaps the most intriguing result of this research is the discovery of identical or virtually identical early genes in groups as different as insects, worms, and vertebrates. Could some of the body plan differences of invertebrate groups be the result of changes in genes that act early in embryological development?

-- Scott, Eugenie C., ed. Evolution vs. Creationism: And Introdution. California: University of California Press; 2004; pp. 30-31.

The classic microevolutionary porcesses are natural selection, mutation, migration, and genetic drift, though some scientists would also include isolating mechanisms and other factors involved in speciation. These are genetically based mechanisms that affect gene pools of species, and that result in change (adaptation) or stasis. Microevolutionary processes operate at the level of the species or population. (Scott 2004: 183)

(....) Evolutionary biologists use the term "macroevolution" to refer to the topics relevant to understanding the distribution of patterns that emerge as species and lineages branche through time. Some of these are the rate of evolutionary change (rapid or slow), the pace of evolutionary change (gradual or jerky), adaptive rediation, morphological trends in lineages (e.g., whether body size gets smaller or larger), extinction or branching of a lineage, concepts ... such as species sorting, and the emergence of major new morphological features (such as segmentation, or shells, or the fusion or loss of bones). Scientists sometimes colloquially refer to macroevolution as "evolution above the species level," but this term does not do justice to the complexity of topics included within the concept. (Scott 2004: 183)

Micro- and macroevolution are thus different levels of analysis of the same phenomenon: evolution. Macroevolution cannot solely be reduced to microevolution because it encompasses so many other phenomena: adaptive radiation, for example, cannot reduce only to natural selection, though natural selection helps bring it about. (Scott 2004: 183)

(....) There is a robust argument among evolutionary biologists over how new body plans or major new morphological features arose. No one disputes the importance of natural selection: it affects the genetic variation in populations, which may be the basis for a new species (in conjunction with isolating mechanisms). All parties likewise recognize the possibility or even likelihood of other biological mechanisms affecting morphological features that distinguish major groups of organisms. The issue in evolutionary biology is how and how much natural selection and other microevolutionary processes are supplemented by other mechanisms (such as regulatory genes operating early in embryological development). (Scott 2004: 184)

-- Scott, Eugenie C., ed. Evolution vs. Creationism: And Introdution. California: University of California Press; 2004; p. 183; 184.

[Rob]

[W]hat is macro-evolution? How would you recognize it if it occured? How would you meassure it? And what is it that stops what you call "micro-evolution" from turning into "macro-evolution" over time?

These are the very questions that are now once again being asked based upon the new scientific findings of evolutionary developmental biology. The evidence that we have been able to gain via molecular biology is uncovering the actual mechanisms of macromutations that are saltational, and very well may turn out to the be mechanisms upon which macroevolution is based. It is simply to early to tell how these newly emerging mechanisms (which were proposed by scientists long ago, but rejected with the rise of the neo-Darwinian Synthesis) will mesh with natural selection (which was extrapolated as the cause of novelty and phylogentic change of form, i.e., the creative force for change) and whether they will turn out to be the real mechanisms behind the creative force for change in evolution.

The following is taken from a study I am currently engaged in and might add some interesting information to the mix:

The following article proposes that some other "macroevolutionary" (body plan) differences may be produced by genetic factors operating during embyological growth and development. The new field of "evo-devo" ... explores these and other subjects. The the review article by Hughes and Kaufman introduces some of these ideas as applied to the anthropod body plan....

Hox Genes and Evolution of the Anthropod Body Plan

Introduction

The evolution of different animal body plans is one of the great mysteries of biology. The phylum Anthropoda, for instance, includes millions of extinct and extant species with diverse morphology, including ticks and trilobites, crabs and centipedes, spiders, shrimps, and spittlebugs. From basic organization consisting of a series of segments encased in an exoskeleton, the various anthropod groups have developed a multitude of specialized forms. Such morphological diversity begs the question of how it arose. To answer this question in invoking natural selection is correct--but insufficient. The fangs of a centipede, the sucking proboscis of a bug, and the claws of a lobster indisputably accord these organisms a fitness advantage. However, the crux of the mystery is this: From what developmental genetic changes did these novelties arise in the first place? To begin to address this question, researchers have turned to the Hox genes. (Scott 2004: 191)

The Hox genes are a set of related genes encoding homeodain transcription factors. The genes are important developmental regulators, acting together to determine the identity of segments along the anterior-posterior axis of the embryo. Each Hox gene is thought to control the expression of a variety of target genes, which may number into the hundreds. Thus the activity of a single Hox gene can be sufficient to induce an entire “developmental module” of target genes, which act in concert to confer a particular identity upon a developing segment. Express a Hox gene in the wrong place, and a completely different kind of appendage will develop. For example, gain-of-function mutations in antennapedia cause legs instead of antennae to grow out of the head of the fruit fly. Because of their important role in determining segment identity, the Hox genes are closely associated with development of the regionalization of the body plan. (Scott 2004: 191)

In fact, it seems to be the expression profile of the Hox genes and their activity that are largely responsible for determining the body patterning of a species. Therefore, evolutionary changes in the expression of Hox genes or their activity might have caused evolutionary changes in body patterning. Why does the lobster have two pairs of specialized front legs (maxillipeds), whereas brine shrimp have none? It seems to be correlated with a shift in Hox gene expression. Why do insects have a thorax and abdomen, whereas centipedes have just one long homonomous trunk? Again, the difference may be due to the different expression of Hox genes. (Scott 2004: 191)

The Hox genes are typically found together in a single complex on the chromosome. The genes promote the identity of segments along the anterior-posterior axis of the embryo in the same order in which they lie on the chromosome…. In addition to conferring identity to segment(s) via target genes, most Hox genes interact with each other to maintain proper expression domain boundaries by both positive and negative regulation. For instance, in general a more posterior gene will suppress the expression or the function of the more anterior Hox gene, phenomena known as posterior prevalence, posterior dominance, or phenotypic suppression. Thus, Hox genes are not merely located together on the chromosome, but they also interact together in complex ways to collectively define segment identity along the anterior-posterior axis of the embryo…. (Scott 2004: 191-192)

Our goal in this review is to introduce the reader to the role of the Hox genes in the evolution of the anthropods. The cast of characters includes some genes that have changed their developmental roles wildly, some genes that have merely tweaked their expression patterns in different species, and some that have stubbornly remained expressed in a nearly invariant pattern. (Scott 2004: 192)

… Because of the high conservation of the Hox genes and their important role in specifying segment identity, they have been studied in many anthropod species. Unfortunately, this wealth of information is scattered among dozens of original data articles and thus is not easily compared. (Scott 2004: 192)

… After all, in general researchers are not obsessed with studying, say, a particular species of centipede purely for its own sake. Rather, each seemingly arcane study is meant to provide some enlightenment into general principles of evolution that may apply to all animal life. But have we actually achieved this quixotic goal? To some degree the answer is yes. In fact, the study of changes in anthropod Hox genes might well be called one of the first success stories of the nascent field of evo-devo. In addition to a greater understanding of the development of particular anthropod species, emerging themes have led to some provocative general models for how Hox genes may have been involved in evolution…. The comparative work in anthropod hox genes has been truly revolutionary because it has succeeded in providing some of the first concrete models of the mechanistic basis of morphological evolution (pp. 459-462). (Scott 2004: 192)

… Although our understanding of genetic events that occurred million of years ago can never be totally conclusive, the ability to simulate evolutionary events in the laboratory environment by manipulation of a critical gene would be convincing evidence to support a theoretical model. With the increased power of expanding functional techniques, the field of anthropod evo-devo is coming to the stage of its development in which some of the beautiful theories described here are bound to be shattered by some ugly facts. But as developmental biologists know, although the coming-of-age process may be awkward at times, it is a necessary step to full maturity. Finally, in further studies we must avoid Hox snobbery. Although Hox genes are important developmental regulatory genes and have been extremely practical to begin studying the evolution of the anthropod, analysis of the Drosophilia genome suggests that there are approximately 13,590 other genes in the genome, which we have barely begun to explore in other species (p. 494). (Scott 2004: 192)

[References omitted.]

Selection excerpted from:

Hughes, Cynthia L., and Thomas G. Kaufman. 2002. Hox Genes and the Evolution of the Anthropod Body Plan. Evolution and Development 4 (6): 459-499.

-- Scott, Eugenie C., ed. Evolution vs. Creationism: And Introdution. California: University of California Press; 2004; pp. 191-192.

Paleontologists have never regarded the Cambrian explosion as a genealogical event -- that is, as the actual time of initial splitting for bilaterian phyla from a single common ancestor that, so to speak, crawled across the Precambrian-Cambrian boundary all by its lonesome. The Cambrian explosion, as paleontologists propose and understand the concept, marks an anatomical transition in the overt phenotypes of bilaterian organisms -- that is, a geologically abrubt origin of the major Baupläne of bilaterian phyla and classes -- not a claim about times of initial phyletic branching. The facts of the Cambrian explosion remain quite agnostic with respect to the two views about branching times now contending in the literature.... Similarly, the facts of the Cambrian explosion cannot distinguish whether ... one tiny worm, or ten tiny worms, crawled across the Cambrian boundary as bilaterian precursors.... [T]he factuality of the Cambrian explosion as an anatomical episode in the differentiation of Baupläne remains equally comfortable with either genealogical alternative. The question of one vs. ten does, however, bear strongly upon the important question of internal vs. external triggers for the explosion. If only on lineage generated all Cambrian diversity, then an internal trigger based upon some genetic or developmental "invention" becomes plausible.... Thus, given the Cambrian explosion was a real event, and that the basic homologies and developmental rules of bilaterian design (particularly as manifested in the spatial and temporal colinearity of [Hox genes]) had already been established in the ancestors of the explosion (those one to ten tiny worms, if you will), then we may infer that bilaterian diversity unfoled along channels of developmental patterns held in common from the beginning of this holophyletic clade. Bilaterian diversity, in other words, represents an extensive set of modifications and tinkerings upon a basic pattern set by history at the outset and then adumbrated in one geologically brief episode to establish all fundamental building plans. Forever after, for more than half a billion years, the subsequent evolution of complex animals -- that is, all bilaterian history since the Cambrian explosion -- has been restricted to much more limited permutation within the confines of these early, congealed designs.

-- Gould, Stephen J. The Structure of Evolutionary Theory. Cambridge: Harvard University Press; 2002; pp. 1156-1159.

Metazoan Origins and the Beginnings of Complex Animal Evolution

The emergence of [the] Metazoa remains the salient mystery in the history of life.

-- P. W. Signor and J. H. Lipps (1992)

Amazing as it might have seemed only 10 or 15 years ago, the great problem of animal origins has become both the source and the object of experimental enquiry. This is a consequence of the realization that the fundamental mechanism underlying the evolution of metazoan morphologies was change in the genomic regulatory programs that control development; and of the accessibility of these programs to experimental investigation.

-- Kevin J. Peterson et al. (2000)

(....) At the outset, it has to be said that the riddle of metazoan origins presents some formidable difficulties. Neither of the two normal data sources for EDB [Evolutionary Developmental Biology], fossil evidence ... and comparative molecular studies ..., seems adequate to the task. The paleontological problem is a general absence of relevant data; there is simply no long fossil series of "pre-animal" forms (of whatever conceivable form) that antedate fossils of unambiguous animal kinds. Instead of a long, detailed, and informative history of animal evolution starting with simple forms, there is a fairly abrupt appearance in the startigraphic record of the fist fossil forms that can definitely be related to contemporary metazoan phyletic groups. A few recognizable metazoan groups (as well as some very unusual forms) appear in the final phase of the Neoproterozoic -- namely, the Vendian period -- but most of the first fossil animals that can be related to contemporary forms occur in the next stratigraphic unit, that of the Cambrian period. The suddenness of their appearance is denoted by the term "the Cambrian explosion." (Wilkens 2002: 468)

(....) This puzzle is beginning to acquire the aura of one that will, eventually, prove solvable. In particular, comparative molecular and developmental analyses of living forms have provided some hints about the genetic composition of the ancestors of the bilaterian metazoan phyla, which comprise the majority of, and all of the more complex, forms of animal life. In addition, and unexpectedly, new fossil finds may be opening a window into the late Precambrian period. Furthermore, several ideas that may help to propel thinking in new directions have been proposed or elaborated in recent years. Not least, molecular phylogenetic analysis has permitted the earliest events of metazoan evolution to be dissected into a series of stages. Finally, as we come to understand more about the processes of gene recruitment in well-established metazoan lineages, such knowledge may prove useful in thinking about the events in metazoan evolution. (Wilkens 2002: 469)

(....) What changes in genetic architecture within the early metazoan lineage accompanied and facilitated the process of metazoan diversification? This question was first raised explicitly a quarter century ago (Valentine and Campbell, 1975; Valentine 1977) and remains as pertinent today as it was then. It is clear that something novel -- and quite possibly many new things -- in the genetic machinery of the organisms at the starting point of the metazoan lineage must have accompanied, and made possible, the first events of animal evolution. Identifying those elements, however, is quite a challenge. Did the beginnings of metazoan life require the creation of new genes, or even new forms of regulatory mechanisms? Or was the key change a restructuring of pathways and networks? Alternatively, was the origin of diverse animal forms near the end of the Neoproterzoic and the beginning of the Cambrian part of an ongoing process of complexity increase (Valentine et al., 1991; Vanentine 1994)? In such a sequence, the attainment of a certain threshold of genetic complexity, in combination with external factors, might, in principle, have led to an explosive diversification of organisms. Were such the case, there could well have been a long history of animal evolution prior to the Cambrian, but one that apparently was not captured in the fossil record. (Wilkens 2002: 469)

That possibility becomes even more interesting when its larger implications are considered. If we are to understand the true nature of the events in early animal origins and diversification, we need an accurate picture of the temporal sequence of those events. The temporal sequence provides hints about both the pattern of events and the processes involved in generating that pattern. Or, to use the words employed by G.G. Simpson (1944), the tempo of events can provide clues to their mode. If, on the one hand, the traditional picture, drawn from the fossil evidence, is correct, the argument that these events were driven by qualitative novelties in genetic machinery is strengthened. Conversely, an extended period of animal evolution, in which the explosion of fossilizable forms in the Cambrian was but one event, would make that hypothesis less necessary. Recent findings, and some new ideas, have indeed sharpened debate about these questions concerning rates and duration, which might seem ancillary to the main question of what happened but, in reality, will be vital to its solution. (Wilkens 2002: 469-470)

-- Wilkins, Adam S. The Evolution of Developmental Pathways. Massachusetts: Sinaur Associates; 2002; pp. 467-470.

[Rob]

One view, Darwin's, captivates us all: natural selection and the great branching tree of life, spreading from the major phyla to the minor genera and species, to terminal twigs, to curious humans seeking their place. Darwin and evolutionism stand astride us, whatever the mutterings of creation scientists. But is the view right? Better, is it adequate? I believe not. It is not that Darwin is wrong, but that he got hold of only part of the truth. For Darwin's answer to the sources of the order we see all around us is overwhelmingly an appeal to a single singular force: natural selection. [Not exactly true; Darwin did appeal to natual selection in his theory solely as the mechanims, but for practical reasons; it was the only one within his reach given knowledge at that time. Darwin openly admitted there may be other possible mechanims.] It is this single-force view which I believe to be inadequate, for it fails to notice, fails to stress, fails to incorporate the possibility that simple and complex systems exhibit order spontaneously. That spontaneous order exists, however, is hardly mysterious. The nonbiological world is replete with examples, and no one would doubt that similar sources of order are available to living things. What is mysterious is the extent of such spontaneous order in life and how such self-ordering may mingle with Darwin's mechanism of evolution--natural selection--to permit or, better, to produce what we see. (Kauffman 1993: xiii)

Biologists have not entirely ignored the spontaneous emergence of order, the occurrence of self-organization. We all know that oil droplets in water manage to be spherical without the benefit of natural selection and that snowflakes assume their evanescent sixfold symmetry for spare physiochemical reasons. But the sheer imponderable complexity of organisms overwhelms us as surely as it did Darwin in his time. We customarily turn to natural selection to render sensible the order we see, but I think the answer to our questions about the origins of order is broader. We already have some inkling of the kinds of spontaneous order which may bear on biological evolution, and I believe we must make the most profound assessment of such self-organization. We must look in any direction that seems profitable because whatever spontaneous order may abound is available for evolution’s continuing uses. (Kauffman 1993: xiii-xiv)

What makes the present stage of biological science so extraordinary is that molecular biology is driving us to the innermost reaches of the cell’s ultimate mechanisms, complexity, and capacity to evolve. At the very same time, work in mathematics, physics, chemistry, and biology is revealing how far-reaching the powers of self-organization can be. These advances hold implications for the origin of life itself and for the origins of order in the ontogeny of each organism. One major theme of this book is an effort to link recent work in molecular biology with these new insights into spontaneous order in complex systems. Union of the two streams of insight promises to transform our understanding. The order inherent in the busy complexity within the cell may be largely self-organized and spontaneous rather than the consequence of natural selection alone. (Kauffman 1993: xiv)

(….) While these points hardly seem contentious, it is no secret that we have, as yet, no theory which embodies them. Physics has its examples of remarkable order, but no use for natural selection. Biologists are secretly aware that selection must be working on systems which to one degree or another exhibit order by themselves. D’Arcy Thompson (1942) told us so with eloquence years ago, but we have not troubled to think through the implications. (Kauffman 1993: xiv)

(….) [W]e have been persuaded by Monod’s (1971) evocative phrase, “Evolution is chance caught on the wing.” And we are equally persuaded by Jacob’s (1983) view that evolution “tinkers together contraptions.” Here broods our sense of organisms as ultimately accidental and evolution as an essentially historical science. In this view, the order in organisms results from selection sifting unexpected useful accidents and marshaling them into improbable forms. In this view, the great universals of biology -- the genetic code, the structure of metabolism, and others are to be seen as frozen accidents, present in all organisms only by virtue of shared descent. The quiet sense that spontaneous order is everywhere present is itself not central to this view. Hence it is not stressed, not investigated, not integrated. (Kauffman 1993: xv)

(….) None can doubt Darwin’s main idea. If we are to consider the implications of spontaneous order, we must certainly do so in the context of natural selection, since biology without it is unthinkable. Therefore, we must understand how selection interacts with systems which have their own spontaneously ordered properties. At a minimum, we must wonder whether selection [is] sufficiently powerful to obviate any inherent order in life’s building blocks. (….) We shall in fact find critical limits to the power of selection: As entities under selection become progressively more complex, selection becomes less able to avoid the typical features of those systems. Consequently, should such complex systems exhibit spontaneous order, that order can shine through not because of selection, but despite it. Some of the order in organisms may reflect not selections success, but its failure. (Kauffman 1993: xv)

-- Kauffman, S. A. The Origins of Order: Organization and Selection in Evolution. New York: Oxford University Press; 1993; p. xiii-xv.

[Rob]

We now need to confront the question of whether the biological community -- or at least the large proportion of it -- has come to accept a theory of evolution that is based on a broadly parallel error. Our case studies on the action of natural selection all involve microevolutionary changes occurring within particular lineages hundreds of millions of years after the origin of the major body plans of which the species concerned represent variations. Many of these case-studies are well known, especially the evolution of industrial melanism in Biston (Bishop and Cook 1980), the evolution of pigmentation patterns in Cepaea (Jones,Leith and Rawlings 1977) and the evolution of Batesian mimicry in several lepidopterans (Turner 1977). Many paleontological case studies are also restricted to particular lineages, with studies on the horse (Simpson 1951; MacFadden 1992) and the mollusks of Lake Turkana (Williamson 1981) being among the best known. While such studies are usually transspecific, and therefore in the realm of 'macroevolution', they are only a very short distance in that direction from an origin-of-body-plans perspective. (Simpson (1944) used the term 'mega-evolution' for the biggest-scale evolutionary events such as body plan origins, but this term has not become widely adopted.)

So, this book is starting with an exhortation to the reader to believe that current evolutionary theory, based on natural selection and adaptation in present-day lineages is, at the very least, incomplete; and this exhortation is based on the drawing of a parallel between the processes of development and evolution. (Arthur 1997: 2-3)

(….) [O]ur current (neo-Darwinian) theory of evolution is incomplete.... In fact, neo-Darwinian theory is incomplete even when assessed against its own criteria. The essence of the neo-Darwinian view is that the evolutionary process is of a two-fold nature, involving the production of organismic novelties (of whatever sort) ultimately by mutation and the sieving of these by natural selection. (Arthur 1997: 9)

(....) The main problem with neo-Darwinism in its current form is that its theoretical structure is extremely lopsided. There has been sustained development of quantitative models of the action of selection, from the pioneering work of Fisher (1930), Haldane (1932) and Wright (1931) up to recent work such as that of Charlesworth (1994); while the mutational and developmental production of the variants being sieved by selection has continued to be treated by too many evolutionists as a 'black box', despite the numerous advances that have been made in developmental genetics in recent years. Essentially, the individual and population levels have been treated as quasi-independent. The fitness of mutant genotypes have been considered to be crucially important in models of selection, while the ways in which fitness effects are produced ... have been largely disregarded. (Arthur 1997: 9-10)

This situation should of course be considered undesirable by all evolutionary biologists, including the strictest of neo-Darwinians, but how serious a problem the lack of a mutational/developmental component of evolutionary theory is perceived to be depends on the extent to which the 'perceiver' is a gradualist. If, despite the views put forward herein, all evolution proceeds through the accumulation of very minor variations -- an extreme view popularized by Dawkins (1986) -- then it may not be too much of a deficiency in the theory to simply assume that mutation perpetually generates morphologies that are slight variants on the existing form. But to anyone proposing the existence of one or more radical morphogenetic phases in evolution, the need for an adequate picture of the genetic architecture of development and of the ways in which this is altered by mutation becomes compelling. Hence the feelings of dissatisfaction that many evolutionary developmental biologists have with neo-Darwinism. There is nothing wrong with elaborate models of selection, but a detailed quantitative statement of how existing types are sorted and selectively eliminated (or held in a state of stable equilibrium) cannot pretend to be a complete theory. (Arthur 1997: 10)

Ironically, most of the alternative approaches to evolution that have proliferated in the last few decades have allowed the focus on destructive rather than creative forces to persist. The neutral theory of molecular evolution (Kimura 1983) -- arguably within a broad neo-Darwinian world view -- concentrates on the stochastic loss of neutral and nearly neutral alleles produced in an unspecified way by mutation. Punctuated equilibrium (Eldredge and Gould 1972) is a pattern, not a process, and may simply be a geological reflection of the standard neo-Darwinian mechanism of allopatric speciation, although some authors (e.g. Williamson 1981) have suggested otherwise…. (Arthur 1997: 10)

(….) The only approach [as of 1997, at the time of this writing] to evolution that has attempted to focus on creative forces has been that of Evolutionary Developmental Biology. I use this label (... Hall 1992) to cover the work of a heterogeneous group of biologists including, among others, von Baer (1828), Thompson (1917), de Beer (1930), Goldschmidt (1940), Waddington (1957), Gould (1977b [2002]), Raff and Kaufman (1983), Buss (1987), Arthur (1988), Thomson (1988) and Raff (1996). (Arthur 1997: 11)

-- Arthur, Wallace. The Origin of Animal Body Plans: A Study in Evolutionary Developmental Biology. Cambridge: Cambridge University Press; 1997; pp. 2-11.

"We have seen that the members of the same class, independently of their habits of life, resemble each other in the general plan of their organisation. This resemblance is often expressed b the term 'unity of type'; or by saying that the several parts and organs in the different species of the class are homologous. The whole subject is included under the general name Morphology. This is the most interesting department of natural history, and may be said to be its very soul." (Charles Darwin, 1859, p. 435)

The body of evolutionary theory that currently occupies a dominant position in biological thought is neo-Darwinism. While this theory has considerable explanatory power, it is widely recognized as being incomplete in that it lacks a component dealing with individual development, or ontogeny. This lack is particularly conspicuous in relation to attempts to explain the evolutionary origin of the 35 or so animal body plans, and the developmental trajectories that generate them.

-- Arthur, Wallace. The Origin of Animal Body Plans: A Study in Evolutionary Developmental Biology. Cambridge: Cambridge University Press; 1997; p. Front Inner Cover.

Wallace Arthur is Professor of Evolutionary Biology at the University of Sunderland, UK.

[Rob]

In The Shape of Life, Raff analyzes the rise of evolutionary developmental biology and proposes new research questions, hypotheses, and approaches to guide the growth of this recently founded discipline. Drawing on a number of key discoveries from the past decades, Raff explains how research in diverse disciplines has forged closer links between developmental and evolutionary biology. For instance, the discovery that both insects and vertebrates use homologous homeobox-containing genes in the development of their body plans has revealed that fundamental genetic relationships underly the development of animals in disparate phyla.

Raff uses the evolution of animal body plans to exemplify the interplay between developmental mechanisms and evolutionary patterns. Basic animal body plans emerged over 530 million years ago during the Cambrian radiation, and the subsequent evolution of developmental processes acting on these plans has resulted in the tremendous diversity of living animal forms. The evolution of animal body plans shows the internal architecture of the genome and of developmental processes and their controls constrain the course of evolution.

Updating the proposal he first advanced with Thomas Kaufmann in their 1983 book Embryos, Genes, and Evolution, Raff argues in The Shape of Life for an integrated approach to the study of the intertwined roles of development and evolution involving phylogenetic, comparative, and functional biology. This new synthesis will interest not only scientists working in these areas, but also paleontologists, zoologists, morphologists, molecular biologists, and geneticists.

-- Raff, Rudolf A. The Shape of Life: Genes, Development, and the Evolution of Animal Form. Chicago: University of Chicago Press; 1996; p. Backcover.

In Rudolf A. Raff's book "The Shape of Life," he states the following conclusion regarding the scientific findings of Evolutionary Devlelopmental Biology and the findings of 530 million year old genetic architectures and developmental pathways shared by diverse phyla:

I present the mechanistic issues posed by the hypothesis that the internal architecture of the genome and of developmental processes and their controls constrains the course of evolution. This issue is a central one in the study of development and evolution. If externally applied natural selection is the only force required to produce evolutionary change, then developmental processes don't matter except as features upon which selection can act. If internal organization and processes govern modes of change, then development must be incorporated into any complete theory of evolution. I propose that internal organization and a set of distinct evolutionary processes acting to sort internal variation produce nonrandom morphological variation in evolution.

-- Raff, Rudolf A. The Shape of Life: Genes, Development, and the Evolution of Animal Form. Chicago: University of Chicago Press; 1996; p. xviii.

Rudolf A. Raff is professor of biology at Indiana University and director for the Institute for Molecular and Cellular Biology. He goes on to state:

To those of us attempting to unravel the mechanisms by which animals change form in evolution, the issues emerge in the guise of the tension between the demands of natural selection and the internal rules that govern the expression of genes and the development of embryos. The nature of the existing developmental system somehow constrains or channels acceptable change, so that selection is limited in what it can achieve given some starting anatomy.

(....) Current evolutionary biology holds that natural selection acting on randomly generated variation produces the biological order we see around us. Natural selection operates externally to the organism [upon the phenotype], and in principle, it should not matter what particular internal rules of gene organization or developmental machinery are in place. Population genetics, which has dominated evolutionary theory for the past few decades, has operated with this scenario as its worldview.

(....) There is no doubt that existing order constrains the variation available, but a purely selectionist approach (probably not supported by many) would nevertheless consider that such apparent constraint is merely a matter of historical accident and probability. Some variations are more likely to occur than others in any particular genome. However, nothing would be really forbidden, and given enough time, sufficient variation could arise for selection to transform a horsefly into a horese.

This hypothetical conception of the freedom of selection to shape the evolution of development has been opposed by the hypothesis that internal organization constrains evolutionary possibilities in a systematic way.

-- Raff, Rudolf A. The Shape of Life: Genes, Development, and the Evolution of Animal Form. Chicago: University of Chicago Press; 1996; p. 296.

There have been some slippery phenomena and hypothesis in science, and their continued investigation has led to rather diverse and even strange outcomes. The notorious N-rays (hyperimagination in dark rooms), polywater (human sweat in small glass capillaries), and cold fusion (critical thinking eclipsed by hopes of striking it rich) proved ignominious for their “discoverers.” On the other hand, other improbable phenomena, such as reports of stones and even chunks of iron falling from the sky, and outlandish concepts, such as continents drifting apart, bore up under ridicule and were ultimately validated as major discoveries about nature. What do we make of the hypothesis of developmental constraints?

There have been some slippery phenomena and hypothesis in science, and their continued investigation has led to rather diverse and even strange outcomes. The notorious N-rays (hyperimagination in dark rooms), polywater (human sweat in small glass capillaries), and cold fusion (critical thinking eclipsed by hopes of striking it rich) proved ignominious for their “discoverers.” On the other hand, other improbable phenomena, such as reports of stones and even chunks of iron falling from the sky, and outlandish concepts, such as continents drifting apart, bore up under ridicule and were ultimately validated as major discoveries about nature. What do we make of the hypothesis of developmental constraints?

If constraints exist, they can come from only three sources. Identifying these formal sources doesn’t explain how constraints operate, but should allow a more precise way of defining them. The first kind of constraint that we will consider arises from the rules of physics operating on organisms. Such physical limits form the subject matter of biomechanics. Effects of gravity on large organisms, effects of hydrodynamic properties on small ones, strengths of materials, geometrical constraints on surface-to-volume ration, and efficiency of energy conservation all affect how organisms are constructed. In development, the physical constraints that are likely to be interesting are those that affect morphogenetic processes. There may be only a few ways of stretching a cell sheet or forming a tube. Quite aside from the particulars of gene regulation and cell biology, such physical limits, if they exist, could bound the universe of morphogenetic possibilities, and thus the diversity of phylotypic stages….

A second source of constraints may lie in the organization of animal genomes. Genetic constraints may be consequences of genome size. Numbers of genes are not the issue, as even the smallest animal genomes contain enough DNA to encode as many expressed genes as larger genomes. However, … genome size affects properties such as cell size and division rate.... The existence of ...

-- Raff, Rudolf A. The Shape of Life: Genes, Development, and the Evolution of Animal Form. Chicago: University of Chicago Press; 1996; p. 299-300.

Another group of scientists have now proposed a new evolutionary theory which incorporates the findings of evo-devo into standard evolutionary theory, which they call "Facilitated Variation" and which is based on the premise that variation is nonrandom and "facilitated," a theory they claim is supported by the evidence of deeply conserved core processes and developmental pathways, for over half a billion years of evolution, which they refer to as a "secret architiecture" of form. The title is "The Plausibility of Life: Resolving Darwin's Dilemma," by Marc W. Kirschner, John C. Gerhart, and John Norton.

[Rob]

Waddington and Schmalhausen, two of the few biologists actually interested in connecting development and evolution during the height of influence of the modern synthesis, introduced the first phenomenon, what Waddington (1942) termed “canalization.” (….) The evolution of discrete traits has been a problem in evolutionary theory since its inception, especially because these traits often have a complex genetic architecture so that single mutations are unlikely to produce the necessary change (but see the next section for a situation in which this could occur). Goldschmidt’s notion of “hopeful monsters” has been universally panned, but several lines of recent evidence suggest that saltational change may have played a role in evolution (Dietrich, 2003). Probably most important for reviving at least some acceptability for the notion of sudden change was the discovery of the genetic basis of change in the numbers or arrangements of segmental or meristic traits. The classic instance was the finding that Hox gene mutation could produce extra wings or leg-antennal substitutions I flies, examples of traits considered long ago in this context by William Bateson (Bateson, 1894). Change in segment number can be brought about by mutation in a single gene. Though the change is often not completely viable or competitively “fit,” it shows that small genetic change can lead to organized morphological change, and some of this resembles evolutionary changes in body plan (Carroll et al., 2001)

-- Hallgrimsson, Benedikt and Hall Brian. Variation: A Central Concept in Biology. Amsterdam: Elsevier Academic Press; 2005; p. 511.

[Rob]

[T]he phenomenon of gene recruitment can explain evolutionary increases in the complexity of pathways and networks. The process is intrinsically involves the insertion or addition of a "new" gene to a preexisting pathway, either upstream or downsteam. The "new" gene, of course, is one that was already employed in another pathway for function. Gene recruitment is inherently a saltatory process -- a genetic jump, as it were -- rather than a simple modification of a preexisting structure. With gene recruitment, new pathways and new linkages between pathways come into being, and do so suddenly. While the spread and fixation of any such genetic change will be contingent upon the forces of selection and genetic drift, as occurs in standard neo-Darwinian evolution, the initial event is novel in character. Furthermore, gene recruitment events are more likely to produce a discernable change in phenotype than a conventional neo-Darwinian, quantitative trait change. In the earlier terminology of evolutionary genetics, gene recruitment events are more likely to be "macromutations" (mutations creating an obvious phenotypic change) than "micromutations" (mutations of individually tiny effect). [emphasis added]

-- Adam S. Wilkins (2002) The Evolution of Developmental Pathways. Sinauer Press. p. 310.

Chapter 12 Speciation and Developmental Evolution

The Genetic Basis of Species versus Larger Taxonomic Differences

It is the first issue -- the nature of the genetic differences that lead to speciation -- that has received the most attention and that has been the subject of the most controversy. The focus here is not on the genetic differences that lead to reproductive isolation, which may involve artifactual epistatic interactions, but on those genetic differences that lead to differential adaptation on the road to the formation of different species.

The starting point of most discussions is Fisher's argument that adaptive evolution is driven by mutations of individually minute effect (Fisher, 1930) -- "micromutations," to use the term from the older literature. To the extent that species formation is accompanied by or driven by such adaptive evolution, developmental evolution in species formation would also consist of changes of individually tiny effect. This view, however, has always seemed deeply implausible to numerous developmental biologists (e.g., Goldschmidt, 1940; Gilbert et al., 1996) and patently untrue to the majority of paleontologists, based on their study of the fossil record (Valentine and Erwin, 1987; Gould, 1994; Erwin, 1999). To many members of these groups, an important role for mutations of large, or at least visible, phenotypic effect -- so-called "macromutations" -- has seemed far more probable than not.

Nevertheless, the gulf between evolutionary geneticists on the one hand and developmental biologists and paleontologists on the other has narrowed in recent years, with a shift toward the position of the latter group. The new consensus is that some mutations of large phenotypic effect can and do play a part in speciation.

[Note: Gould after reviewing the new evidence of evo-devo, modified his previous views somewhat, making room for the "plausibility" of such macromutations (saltations), which were not part of his theory of punctuated equilibria, and which relied solely on allopatric speciation as the mechanism of his punctuations occuring over periods of 10 to 40 thousand years, which he termed a "geological moment." The truth -- fact -- is that a bedding plane which represents a "geological moment" is only resolvable to 10,000 to 40,000 years, and Gould used statistical methods to determine changes in morphology over time which he associated with punctuational events. He admits in his book The Structure of Evolutionary Theory that one could not differentiate between a sudden saltation and accelerated allopatric speciation, since both events would leave the same data signature in the bedding plane. In other words, it is an assumption that the process of speciation in punctuated equilibria is due to allopatric speciation, although at an accelerated rate, after a period of stasis. It is also a fact that the fossil record does not contain the level of detailed data required to distinquish between these two events; hence, at the time Gould developed his theory one was left in the position of having to choose between one of two assumptions; allopatric speciation at an accelerated rate, or sudden saltation. The recorded data in the fossil record would be exactly the same, and one could not distinguish empirically between the two. The new evidence of molecular biology, developmental genetics, and evolutionary developmental biology (evo-devo) are adding to the plausibility of sudden saltations, a point which Gould himself (2002: 1143-1144) argues based upon this new evidence, can no longer be dismissed a priori. Jeffrey Schwartz has now written a book Called "Sudden Origins" which makes this very argument.]

-- Wilkins, Adam S. The Evolution of Developmental Pathways. Massachusetts: Sinaur Associates; 2002; p. 462.

Regulation by Way of Genes

Occupying an even higher level in the hierarchy of biological control are the various factors that determine which parts of the genome are expressed at any moment, and in what amounts. Cells hardly ever express all the information contained in their DNA. Those of multicellular organisms usually express only a small fraction of this information. Whatever fraction they do express is what determines the cell's specificity, as a muscle cell, a nerve cell, or any other cell type. The expression of genes is controlled at the transcriptional, at the maturational (in the case of split genes), or at the translational level, sometimes also posttranslationally, by factors that are still poorly understood but are obviously of central importance. Such factors participate in metablic regulation and adaptation and, especially, in differentiation and development. The way in which they bind to specific DNA (or RNA) sequences represents yet another set of lock-and-key phenomena (for a survey, see Reference 424).

Crowning it all is the sort of stupendously complex script that unfolds in space and time in the sheltered environment of a germinating seed, of an incubating egg, or of the womb, faultlessly leading from the single fertilized egg cell to the multicellular miracle that is an emerging sapling, a freshly hatched chick, or a newborn baby. It all works through the opening and closing of genetic switches controlled by the products of previously expressed genes, by the products of these products, and so on ..., in a fantastic network--as yet almost totally unraveled--of interactive influences. (36)

424. Struhl, K. Helix-turn-helix, zinc-finger, and leucine-zipper motifs for eukarytic transcriptional regulatory proteins. Trends Biochem. Sci. 14:137-140; 1989.

-- -- de Duve, Christian (Nobel Laureate) Blueprint for a Cell: The Nature and Origin of Life. Neil Patterson Publishers. 1991.