Good Vibrations: the Silent Symphony of Life

176 Evolutionary Anthropology

CROTCHETS & QUIDDITIES

Good Vibrations: The Silent Symphony of Life

KENNETH WEISS

A century ago a leading biologist suggested that repetitively structured biolog- evolve incrementally. What is actually ical traits resembled interference patterns used in tuning violin plates. Are such inherited? A different gene for each ideas in tune with modern biology? hair or vertebra? That made no sense to him, and it may have been a reason for the non-specific suggestion a cen- Look at the life around you. Every- of the first prominent biologists to as- tury later that evolution was a “punc- tuated” process. where, you are confronted with mod- semble objections was St George 1 ularity and repetition, from the leaves Jackson Mivart (1870), previously re- One of his ideas about this is strik- and branches on plants, to your hair spected by and on good terms with ingly modern in concept. The sugges- and the skeletal and other structures Darwin, Huxley, and the rest of the tion drew biological parallels with concepts of fields and vibrations or within you. Modularity, segmenta- biological “in” crowd. The main issue oscillations borrowed from physics. tion, and repetition are, like measures was whether adaptive natural selec- As we’ll see, Bateson used a musical and tones in music, the way in which tion could explain species variation analogy that makes some evolution- the living opus has been assembled by and evolution. Mivart so irritated Dar- ary genetic points easy to understand. the composing processes of evolution. win that he responded at great length th There were then no actual genes In his elegant book Evolution Emerg- in the 6 edition of Origin. Some of known and his views were ignored or ing, W.K. Gregory (1951) likened Mivart’s objections involved the na- even ostracized during the decades of modular (“polyisomeric”) organiza- ture of inheritance and homology in ascendance of the neodarwinian syn- tion to “the notes in an octave...evo- regard to discontinuous variation, thesis. But the basic ideas are enjoy- lution emerging has involved an infi- such as repetitive, serially homolo- ing a justified revival in a profound nite number and variety of natural gous structures. Mivart became a beˆte advance in our understanding of the polyisomeres in both space and time.” noir who was ostracized by the Dar- role of genes in the evolution and gen- This has long been known, but little winian community then becoming the eration of complex morphologies. We analyzed, in modern evolutionary mainline of biology. Mivart also tried can trace these ideas, at least fanci- terms until very recently. To continue to reconcile evolution and Catholi- fully, back to the famous Geoffroy- the musical analogy, we can view pat- cism, and was excommunicated from Cuvier debates in 1830 on the nature terned structures as a harmony of that church, too, poor fellow. But his of animal form itself, and perhaps organization, with many parts inte- theme was picked up by W.K. Brooks even push the musical analogy back to grated to form an organism, the way in the US who credited Mivart and that time as well. the violins, horns, flutes, and so on, then by William Bateson (1892, 1894, form an orchestra. In fact, old ideas 1913, see Webster, in Bateson, 1894; and new facts suggest that musical Webster and Goodwin, 1996). A FEW BASIC QUESTIONS similes are relevant to the symphony Bateson coined the term “genetics” How Fundamental Is Modular of life. and was a strong promoter of Mende- Patterning? Soon after Darwin published his Or- lian genetics, but he did not think that igin of Species, opponents of his views the darwinian evolution by gradual It’s worth stressing how very modu- began marshaling their evidence. One natural selection could generate spe- lar structure is in the construction of cies or their diversity (e.g., Bateson, life. If the canonical essence of evo- 1913). He pointed out problems in in- lution is descent with modification terpreting modular (repetitive, seri- among individuals across genera- ally homologous, or meristic) struc- tions, to me an equally important Ken Weiss is Evan Pugh Professor of An- tures: “Segmentation ...is almost principle is duplication with variation thropology and Genetics at Penn Univer- sity. universally present...greater or less within the individual. From DNA to repetition of various structures is one proteins to morphology, among plants of the chief factors in the composition and animals (even bacterial colony Evolutionary Anthropology 11:176–182 (2002) of animal forms.” (Quoted in Web- 1 DOI 10.1002/evan.10034 Bateson’s reference to Chladni figures was made Published online in Wiley InterScience ster’s preface to Bateson, 1894). But most clearly in a letter to his sister (see B. Bateson, (www.interscience.wiley.com). discrete segment numbers cannot 1928). CROTCHETS & QUIDDITIES Evolutionary Anthropology 177

a way to make the vibrations caused by sound waves visible. He covered glass, metal, and wooden plates with sand and ran a violin bow against them. The vibrations moved the sand into patterns that are known today as “Chladni’s figures.” The vibration jos- tles the powder to areas or nodes of the plate in which vibration waves cancel each other out and there’sno net motion. The idea of using a tuning fork as a source of oscillating energy suggested an interesting way to illus- trate the phenomenon. A physician named Fe´lix Savart was interested in applying Chladni’s notions to this problem, by dusting the plate with black powder, applying a tone to the plate and observing the interference waves or nodes, as shown in Figure 3. Plates of great violins have consistent patterns within, and consistent differences between them. Makers of great violins “tune” the top and back plates by shaving small amounts of Figure 1. William Bateson in youth A; and his wood here and there until appropri- interests, B. Supernumerary premolar in ate frequencies generate the stan- upper but not lower jaw of Ateles mon- dard “modes.” An important point to key. (sources: (A) http://post.queensu.ca/ ϳforsdyke/bateson1.htm# with permission note is that the same plate has dif- of Donald R. Forsdyke; (B) from Bateson, ferent patterns if the energy, loca- 1894). tion, or frequency of the source is changed. In 1952, Alan Turing (known for de- formation), from cells to ants in a col- bers to explain comparable structures ciphering the Nazi cryptographic sys- ony, there is modular organization ev- within an organism and for repeated tem during World War II and ideas on erywhere. This is built by gene dupli- regulatory sequences around genes designing programmable computers) cation to form the genome, protein expressed in similar cellular contexts. suggested that two interacting sub- polymerization or multimerization to Wavelike patterning mechanisms stances diffusing through a uniform form functional biochemical units, have been a widely observed phenom- fluid could generate wavelike interfer- and at the morphological level, begin- enon in development. ence patterns. One substance is ning with cells themselves. known as an activator, and diffuses Across the plant and animal world, from some source, inducing its own if you look at structures, organs, or How Does Modular Structure activity as well as that of the second substance, known as an inhibitor. In organ systems you will see how com- Relate to Genes? such a “reaction-diffusion” process, monly they are built of repeated Bateson’s “vibratory” theory of pat- the inhibitor reduces the level of the subunits (themselves sometimes terning was that repeated structures activator. Depending on the produc- hierarchically modified). To make were manifestations of sympathetic tion and diffusion levels of the two this happen, sets of differently pro- vibration or similar interference substances, and their interaction dy- grammed cells are produced in peri- phenomena. His imagery was that of namics, an initially uniform area or odic or episodic fashion, and become Chladni figures. These are the wave- “field” will generate wavelike patterns the precursors of each unit within the like interference patterns that form of high and low levels of the activator. structure. In this way, duplication when a source of oscillating energy with variation has allowed life to be- diffuses through a material of some come complex, and organisms to sort (Waller, 1961). The pattern is a achieve larger size and functional spe- function of the location, frequency, cialization. and energy level of the source of vi- Recognition of modularity is thor- bration. Ernst Chladni was a Leipzig (Virtual) Figure 2. Modular structure in life: oughly built into modern biology. We lawyer, musician, and amateur scien- left-right symmetry, hair, pores, teeth, cusps, routinely search for gene family mem- tist. As early as 1787, he had reported papillae on the tongue,... 178 Evolutionary Anthropology CROTCHETS & QUIDDITIES

cascades occurs when activator levels cross some threshold, with the valleys the structure-free inhibition zones. In recent years, the ability to detect cell-specific levels of expression of specific gene products (proteins or mRNA) has put these ideas to direct tests. Embryonic tissue is tested for spatiotemproal distribution of signaling factor molecules diffusing from cells of origin across the tissue. Ini- tially broad patterns narrow to stripes and then periodic spots surrounded by expression of diffusible inhibitors. For example, hair and feathers develop in zones expressing the Fgf and Wnt signaling factors, but are inhib- ited in areas where Bmp factors are found. These gene products have patchy distribution that presages the location and spacing of future feathers, sometimes appearing first as an initial line of expressing cells (e.g., the dental lamina), that resolves into spots, and then spreads laterally to form other spots. Short distance spacing among adjacent cells may be patterned by additional activator-inhibitor interactions (e.g., the Notch-Delta system). These are highly conserved processes; for example, the same Notch-Delta signaling helps pattern the ommatidia in insect eyes, teeth, and feathers. These patterning systems then activate “selector” genes that initiate cascades of gene expression that lead to organ formation (see Gilbert and Gerhart references). In addition to direct molecular examples, activation-inhibition processes have been shown by computer simulation to apply in varying ways to coloration in mammals, fish, sea- shells, butterfly wings, the location of mammary glands, feathers, scales, and digits in animals and flower parts. This is probably just the first peek at Figure 3. A: Chladni’s figures shown here are 12 engravings of these acoustically produced patterns (Source: Chladni, 1787, copied from http://www.sil.si.edu/Exhibitions/Science-and- the wide distribution of such pattern- the-Artists-Book/phys.htm). B: Cross section of vibrating plate to show nodes (N) of no ing mechanisms in nature. motion. C: Chladni figures of the 7 classical “modes” of a handmade violin (tonal frequen- The concepts are highly relevant to cies 91, 138, 196, 231, 306, 312, 392 Hz, respectively). (Source: J. Wolfe, http://www.phys. anthropology. My own interest is in unsw.edu.au/ϳjw/chladni.html) dental patterning, in which it seems likely that the number, location, and differential morphology of teeth along Turing did not acknowledge that the nodes and internodes as “the seat the jaws are due to such mechanisms. Bateson had thought of this in regard of appropriate and distinct chemical Indeed, the same genes demonstrably to biology, but several biologists no- processes leading to the differentia- expressed in this way in feather ticed the relevance of Turing’s ideas to tion of the parts” of organisms. Struc- and other vertebrate patterning pro- diverse repetitive or wavelike biologi- tures can develop at the peaks, for ex- cesses are expressed in teeth in ways cal traits. Bateson (1913) referred to ample, if expression of developmental consistent with activation-inhibition CROTCHETS & QUIDDITIES Evolutionary Anthropology 179

ing Darwin’s solution to the species question. In the 20th century, Richard Goldschmidt (1940) suggested that mutational hopeful monsters may from time to time be produced that have new structures or traits. On rare occasions, these might pass the selective screen as adaptations to a new form of life. Sal- tational evolution was and is generally held to be a serious kind of heresy (or madness). Nobody thinks wings can evolve suddenly from legs, but patterned organ systems do normally vary in their number and morphology of elements (teeth, cusps, feathers, limb- bones, regions of the gut, etc., Figure 1B). This could address Bateson’s ob- jection that neither darwinian gradualism nor simple mendelian segregation were consistent with the evolution of meristic traits. As Bateson (1928) said, an eight-petal form is to a four-petal Figure 4. Peaks erupting from a simple reaction-diffusion process. Wire-screen is concentra- form as one octave is to another. A mu- tion of activator (this could be proportional to growth, for example), grey-scale of inhibitor tationally derived shift in the dynamics (courtesy Brian Lambert). of an interaction process can bring about such differences, and there are many examples. patterning. (Jervall and Jung, 2000; sulting intermediate states with the in- Recognition of dynamic patterning Weiss et al., 1998). In elegant experi- termediate states of real tooth germs processes has a second important im- ments that I wish I had done rather that are closely imitated by the dy- plication for evolutionary thinking. As than they, Jukka Jernvall, Soile Ker- namic process simulation (J. Jernvall, Bateson (1894) said, “Of course, he- anen, and others in Irma Thesleff’s lab personal communication). As far as redity becomes quite a simple phe- in Helsinki have shown that gene ex- the morphed intermediates go, art nomenon in light of this.” There is no pression and expression-manipula- does not imitate life. Only the dy- single gene “for” a specific feather or tion are consistent with this general namic patterning process resembled tooth or intestinal villus or nephron. type of patterning process. Zones the real thing. All the elements in each system ex- known as enamel knots expressing Fgf Bateson could only speculate about press essentially the same genes. In and other growth factors appear along such matters, but a century later we principle, all that need differ along the the dental lamina; cusps form when have at least some examples vindicat- jaw would be the position of the peaks this induces down-growth in sur- ing the idea at the molecular level. of expression of say odontogenic rounding tissue, while the knots them- Dynamic patterning mechanisms like genes. Not only need there not be sep- this seem to a ubiquitous means by selves are self-inhibiting (Fig. 5B). In- arate genes for each iteration of a which complex animals and plants are deed, an earlier round of patterned structure, but what may differ be- produced from single fertilized egg expression of similar genes appears to tween the dentitions of carnivores and cells. Of course, to credit Bateson for be involved in the serially patterned herbivores may mainly, or only, in- his prescience does not mean that we location of tooth germs. volve the interaction dynamics— would expect to see his—or Turing’s, Salazar-Ciudad and Jernvall have things like diffusion rates, activation or anyone’s—ideas fulfilled exactly, subsequently shown by computer or inhibition efficiencies—of the same and repetitive patterning is brought patterning genes. simulation that activation-inhibition about in many ways. processes modeling the behavior of enamel knots can generate strikingly What About Homology? How Does Modular Structure realistic molariform cusplike crown All of this affects notions of homol- Evolve? patterns (Salazar-Ciudad and Jern- ogy (see Abouheif, 1997; Hall, 1999). vall, 2002; Fig. 5). In an important A long-standing question of the “tem- It may be evolutionary non-questions test, the authors tried the darwinian po and mode” of evolution has been the to ask whether the diastema in a gradualism experiment of simply way complex traits evolve. Arguments mouse jaw represents “missing” teeth, computer “morphing” a tooth from its about this pitted darwinian gradualism or what the homologous digits are in a initial to its final states (both of which versus saltational evolution. As noted bird and mammal. Homology may re- matched between program and actual earlier, this problem bothered Bateson ally lie in the patterning process it- tooth embryos), and compared the re- and others and kept them from adopt- self—a common generative mecha- 180 Evolutionary Anthropology CROTCHETS & QUIDDITIES

mals—including humans (Figure 6).2 Hair form is regionally differentiated and individual hairs can themselves be striped. Thus, hair is patterned by several simultaneously occurring wave-generating processes. Murray (1993) provides a Chladni-like simulation of haircolor patterning in just that way. Similarly nested patterning is seen along the mammalian dentition, in feathers, intestinal epithelial structure, tongue, limb, and vertebral patterning, bristles in various parts of a ﬂy, and many others. As in tooth development, the same activation-inhibition process may be involved in multiple traits at different times or places in the same organism.

THE MUSIC OF EVOLUTION Chemical “vibration” is harmonious to the organism and has properties similar to those of music. Ideas about this relate to age-old debates in biology. These ideas were applied to pale- ontological, comparative, and embry- ological data, and they may even have been relevant to early 19th century dis- cussions of animal form. In 1830, Georges Cuvier and Etienne Geoffroy St. Hilaire held famous debates in Figure 5. Simulation of tooth crown shape by a class of reaction-diffusion-like mechanism. A: Paris (Appel, 1987). Cuvier believed Basic model of simulated spatial units showing activator (A) and inhibitor (I) relative to enamel knot (dark) and differential cell growth. B: Predicted (simulated) and observed that complex animal form was due to mouse (left) and vole (right) first molar crown surfaces (with permission from Salazar-Ciudad independent adaptation (at that time, and Jernvall, 2002). in the functional, not darwinian, sense of the term) of different body structures, such as limbs, claws, teeth, and so on. Geoffroy held that varia- nism, in Bateson’s terms. The pattern- have the same problem assigning ho- tions among animals reflected under- ing process and genes may be shared, mology to members of gene families lying body plans that could be dis- and the patterning genes may be the that have undergone repeated dupli- torted and modified but represented same, but there may be no specific cation, such as globin or photore- functional wholes. gene or gene combination that is a ceptor genes between birds and These were bitter and celebrated de- particular member and can form the mammals. Should we call teeth and bates. A new edition of Chladni ap- basis of taxonomic homologies. An ex- feathers or insect eyes homologous peared in 1830, and I have speculated ample may be the transitory dental because at some point in their devel- (Weiss et al., 1998) that Fe´lix Savart, rudiments that appear in the (upper opment the same patterning circuitry as a member of the Paris intellectual but not lower) diastema region of an is used? set, may have attended the debates. embryonic mouse jaw (Keranen et al., Might he have seen the similarities 1999), but are not obviously identical between biological patterning and the to the teeth absent in the mouse. way Chladni figures demonstrate vari- The Hairs on Your Head May It seems likely that one problem ation on an underlying plan (the basic that taxonomy has is its tacit reliance Be Numbered, But What structure of a violin plate), and sided with Geoffroy? on a gene-for notion of the relation- About the Wave? Ideas about serial homology were ship between genes and traits. Such Dynamic patterning processes are around for most of the 20th century, assignments may not explain dynam- typically nested. For example, hairs ically patterned serially homologous are individually periodic structures, 2I can personally attest that in their younger years, traits, of which there are so many. We but pelage is also striped in mam- these stripes were clearer. CROTCHETS & QUIDDITIES Evolutionary Anthropology 181

Figure 6. Variably striped humans.2 A: George Milner, archeologist. B: James Wood, demographer. C: Andrew Clark, geneticist.

though suggestions as to cause did not the implication of these generalities. cell to become a harmonious com- get very far, and were often deni- Similar genes are used in diverse plex organism, with tones and over- grated as untestable, or unscientific. traits, but this does not mean that the tones. This is a developmental or- But that was then and this is now. same genes will be used in any partic- chestra that all organisms can play, 3 Dynamic patterning processes are a ular trait, or even in the same trait but none can hear. We are probably fundamental part of the developmen- among different species. Two logically just beginning to discover the degree tal toolkit, that are used and re-used, similar patterning mechanisms can to which we owe our nature to the and deeply conserved phylogeneti- involve different, perhaps entirely un- good vibrations of this silent sym- cally. But it is tempting to over-extend related sets of genes. For example, phony of life. similar periodic patterning processes are involved in plants, but not with NOTES animal signaling factors. Interestingly, a recent paper has ex- I welcome any comments on this amined various patterning differences column: [email protected]. I maintain a between teosinte and maize (Lauter CrotchetyComments page at www. and Doebley, 2002). A long-standing anthro.psu.edu/rsrch/weiss_lab. question is how these traits, that are I thank Anne Buchanan and Jukka invariant within each species, could Jernvall for helpful comments. have evolved. Did it involve a Gold- schmidt leap? We can’t say, but Lau- TO READ ter and Doebley have shown by clever cross-breeding experiments that there Most things discussed here can be is variation within teosinte that does profitably explored by web searching. not lead to trait variation, but that could be the latent source of rapid Abouheif E. 1997. Developmental genetics and evolution of the trait. A small amount homology: a hierarchical approach. Trends Ecol of mutational change might have suf- Evol 12:405–408. ficed to reconfigure this silent back- Appel T. 1987. The Cuvier-Geoffroy debate. New ground variation to jump teosinte to York: Oxford Press. Bateson B. 1928. William Bateson, F.R.S. natu- maize form, creating this most impor- ralist. Cambridge: Cambridge University Press. tant cultivar—just as a Chladni figure Bharathan G, Goliber T, Moore C, Kessler S, can jump when the sound frequency Pham T, Sinha N. 2002. Homologies in leaf form changes. The developmental timing of inferred from KNOXI gene expression during development. Science 296:1858–1860. a single gene can change the shape of Bateson W. 1894. Materials for the study of vari- Figure 7. Pattern variants in teosinte and a leaf from simple to complex maize that are phenotypically invariant (Bharatham et al., 2002). 3DNA sequences can be made into much more within strain but with underlying variation re- The musical analogy is probably than a 4-tone exercise in minimalism, but transla- vealed by gene mapping in crosses. Are not a bad one. Throughout an em- tions to date are more aesthetic than biological. these differences due to genes for dy- CDs and software are available; for example http:// namic-patterning mechanisms rather than bryo as it develops, a highly orches- algoart.com/dnamusic/ or http://education.llnl. for specific traits? (from Lauter and Doeb- trated program of “vibrational” pat- gov/msds/music/midi-dna.html or http://www. ley, 2002, courtesy John Doebley). terning mechanisms enables a single dnamusiccentral.com/. 182 Evolutionary Anthropology CROTCHETS & QUIDDITIES

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