Darwin's Doubt

by Stephen C. Meyer

  Yet MAPs, and indeed many other necessary proteins, are only part of the story. The locations of specified target sites on the interior of the cell membrane also help to determine the shape of the cytoskeleton. And, as noted, the gene products out of which these targets are made do not determine the location of these targets. Similarly, the position and structure of the centrosome—the microtubule-organizing center—also influences the structure of the cytoskeleton. Although centrosomes are made of proteins, the proteins that form these structures do not entirely determine their location and form. As Mark McNiven, a molecular biologist at the Mayo Clinic, and cell biologist Keith Porter, formerly of the University of Colorado, have shown, centrosome structure and membrane patterns as a whole convey three-dimensional structural information that helps determine the structure of the cytoskeleton and the location of its subunits.32 Moreover, as several other biologists have shown, the centrioles that compose the centrosomes replicate independently of DNA replication: daughter centrioles receive their form from the overall structure of the mother centriole, not from the individual gene products that constitute them.33

  Additional evidence of this kind comes from ciliates, large single-celled eukaryotic organisms. Biologists have shown that microsurgery on the cell membranes of ciliates can produce heritable changes in membrane patterns without altering the DNA.34 This suggests that membrane patterns (as opposed to membrane constituents) are impressed directly on daughter cells. In both cases—in membrane patterns and centrosomes—form is transmitted from parent three-dimensional structures to daughter three-dimensional structures directly. It is not entirely contained in DNA sequences or the proteins for which these sequences code.35

  Instead, in each new generation, the form and structure of the cell arises as the result of both gene products and the preexisting three-dimensional structure and organization inherent in cells, cell membranes, and cytoskeletons. Many cellular structures are built from proteins, but proteins find their way to correct locations in part because of preexisting three-dimensional patterns and organization inherent in cellular structures. Neither structural proteins nor the genes that code for them can alone determine the three-dimensional shape and structure of the entities they build. Gene products provide necessary, but not sufficient, conditions for the development of three-dimensional structure within cells, organs, and body plans.36 If this is so, then natural selection acting on genetic variation and mutations alone cannot produce the new forms that arise in the history of life.

  Epigenetic Mutations

  When I explain this in public talks, I can count on getting the same question. Someone in the audience will ask whether mutations could alter the structures in which epigenetic information resides. The questioner wonders if changes in epigenetic information could supply the variation and innovation that natural selection needs to generate new form, in much the same way that neo-Darwinists envision genetic mutations doing so. It’s a reasonable thing to ask, but it turns out that mutating epigenetic information doesn’t offer a realistic way of generating new forms of life.

  First, the structures in which epigenetic information inheres—cytoskeletal arrays and membrane patterns, for example—are much larger than individual nucleotide bases or even stretches of DNA. For this reason, these structures are not vulnerable to alteration by many of the typical sources of mutation that affect genes such as radiation and chemical agent.

  Second, to the extent that cell structures can be altered, these alterations are overwhelmingly likely to have harmful or catastrophic consequences. The original Spemann and Mangold experiment did, of course, involve forcibly altering an important repository of epigenetic information in a developing embryo. Yet the resulting embryo, though interesting and illustrative of the importance of epigenetic information, did not stand a chance of surviving in the wild, let alone reproducing.

  Altering the cell structures in which epigenetic information inheres will likely result in embryo death or sterile offspring—for much the same reason that mutating regulatory genes or developmental gene regulatory networks also produces evolutionary dead ends. The epigenetic information provided by various cell structures is critical to bodyplan development, and many aspects of embryological development depend upon the precise three-dimensional placement and location of these information-rich cell structures. For example, the specific function of morphogenetic proteins, the regulatory proteins produced by master regulatory (Hox) genes, and developmental gene regulatory networks (dGRNs) all depend upon the location of specific, information-rich, and preexisting cell structures. For this reason, altering these cell structures will in all likelihood damage something else crucial during the developmental trajectory of the organism. Too many different entities involved in development depend for their proper function upon epigenetic information for such changes to have a beneficial or even neutral effect.

  In Chapter 16 I will examine several new theories of evolution, including one known as “epigenetic inheritance.” We’ll see that there are some additional difficulties associated with the idea that mutations in epigenetic structures can produce significant evolutionary innovation.

  Darwin’s Growing Anomaly

  With the publication of On the Origin of Species in 1859, Darwin advanced, first and foremost, an explanation for the origin of biological form. At the time, he acknowledged that the pattern of appearance of the Cambrian animals did not conform to his gradualist picture of the history of life. Thus, he regarded the Cambrian explosion as primarily a problem of incompleteness in the fossil record.

  In Chapters 2, 3, and 4, I explained why the problem of fossil discontinuity exemplified by the Cambrian forms has, since Darwin’s time, only intensified. Yet clearly a more fundamental problem now afflicts the whole edifice of modern neo-Darwinian theory. The neo-Darwinian mechanism does not account for either the origin of the genetic or the epigenetic information necessary to produce new forms of life. Consequently, the problems posed to the theory by the Cambrian explosion remain unsolved. But further, the central problem that Darwin set out to answer in 1859, namely the origin of animal form in general, remains unanswered—as Müller and Newman in particular have noted.37

  Contemporary critics of neo-Darwinism acknowledge, of course, that preexisting forms of life can diversify under the twin influences of natural selection and genetic mutation. Known microevolutionary processes can account for small changes in the coloring of peppered moths, the acquisition of antibiotic resistance in different strains of bacteria, and cyclical variations in the size of Galápagos finch beaks. Nevertheless, many biologists now argue that neo-Darwinian theory does not provide an adequate explanation for the origin of new body plans or events such as the Cambrian explosion.

  For example, evolutionary biologist Keith Stewart Thomson, formerly of Yale University, has expressed doubt that large-scale morphological changes could accumulate by minor changes at the genetic level.38 Geneticist George Miklos, of the Australian National University, has argued that neo-Darwinism fails to provide a mechanism that can produce large-scale innovations in form and structure.39 Biologists Scott Gilbert, John Opitz, and Rudolf Raff have attempted to develop a new theory of evolution to supplement classical neo-Darwinism, which, they argue, cannot adequately explain large-scale macroevolutionary change. As they note:

  Starting in the 1970s, many biologists began questioning its [neo-Darwinism’s] adequacy in explaining evolution. Genetics might be adequate for explaining microevolution, but microevolutionary changes in gene frequency were not seen as able to turn a reptile into a mammal or to convert a fish into an amphibian. Microevolution looks at adaptations that concern the survival of the fittest, not the arrival of the fittest. As Goodwin (1995) points out, “the origin of species—Darwin’s problem—remains unsolved.”40

  Gilbert and his colleagues have tried to solve the problem of the origin of form by invoking mutations in genes called Hox genes, which regulate the expression of other genes involved in animal development�
��an approach that I will examine in Chapter 16.41 Notwithstanding, many leading biologists and paleontologists—Gerry Webster and Brian Goodwin, Günter Theissen, Marc Kirschner, and John Gerhart, Jeffrey Schwartz, Douglas Erwin, Eric Davidson, Eugene Koonin, Simon Conway Morris, Robert Carroll, Gunter Wagner, Heinz-Albert Becker and Wolf-Eckhart Lönnig, Stuart Newman and Gerd Müller, Stuart Kauffman, Peter Stadler, Heinz Saedler, James Valentine, Giuseppe Sermonti, James Shapiro and Michael Lynch, to name several—have raised questions about the adequacy of the standard neo-Darwinian mechanism, and/or the problem of evolutionary novelty in particular.42 For this reason, the Cambrian explosion now looks less like the minor anomaly that Darwin perceived it to be, and more like a profound enigma, one that exemplifies a fundamental and as yet unsolved problem—the origination of animal form.

  Part Three

  After Darwin, What?

  15

  The Post-Darwinian World and Self-Organization

  The year 2009 marked the 150th anniversary of the publication of The Origin of Species. In that year, the renowned Cambrian paleontologist Simon Conway Morris published an essay in the journal Current Biology titled “Walcott, the Burgess Shale and rumours of a post-Darwinian world,” assessing the current state of evolutionary biology. “Everywhere elsewhere in the Origin the arguments slide one by one skillfully into place, the towering edifice rises, and the creationists are left permanently in its shadow,” he wrote. “But not when it comes to the seemingly abrupt appearance of animal fossils.”1 Instead, unresolved problems exposed by the Cambrian explosion have, in Conway Morris’s view, “opened the way to a post-Darwinian world.”2 The evidence we reviewed in the previous sections of the book—evidence for a real, rather than merely apparent, explosion of animal form in the fossil record, and against the neo-Darwinian mechanism as an explanation for the origin of form and information—may help to explain why biology has begun to enter such a world.

  Moreover, any doubts that at least some biologists have begun to embrace a post-Darwinian perspective should have been laid to rest in the summer of 2008, when sixteen influential evolutionary biologists met for a private conference at the Konrad Lorenz Institute in Altenberg, Austria. The scientists, whom the science media later dubbed the “Altenberg 16,”3 met to explore the future of evolutionary theory. These biologists had many different, and sometimes conflicting, ideas about how new forms of life might have evolved. But all were united by the conviction that the neo-Darwinian synthesis had run its course and that new evolutionary mechanisms were needed to explain the origin of biological form. As paleontologist Graham Budd, who was in attendance, explained, “When the public thinks about evolution, they think about [things like] the origin of wings… . But these are things that evolutionary theory has told us little about.”4

  Of course, explaining the origin of form is precisely what has made the Cambrian explosion so mysterious. In Chapter 7, in discussing the idea of punctuated equilibrium, I quoted Cambrian paleontologists James Valentine and Douglas Erwin, who concluded exactly that. They argued that neither punctuated equilibrium nor neo-Darwinism has accounted for the origin of new body plans and that, consequently, biology needs a new theory to explain “the evolution of novelty.”5

  The Altenberg 16 sought to address this challenge. Since the conference, and for nearly two decades preceding it, many evolutionary biologists have been working to formulate new theories of evolution, or at least new ideas about evolutionary mechanisms with more creative power than mutation and natural selection alone. Each of these new theories attempts to answer the increasingly urgent question: After Darwin—or neo-Darwinism—what?

  The Neo-Darwinian Triad

  The neo-Darwinian mechanism rests on three core claims: first, that evolutionary change occurs as the result of random, minute variations (or mutations); second, that the process of natural selection sifts among those variations and mutations, such that some organisms leave more offspring than others (differential reproduction) based on the presence or absence of certain variations; and third, favored variations must be inherited faithfully in subsequent generations of organisms, thus causing the population in which they reside to change or evolve over time.6 Biologists Marc Kirschner and John Gerhart call these three elements—variation, natural selection, and heritability—the “three pillars” of neo-Darwinian evolution.7

  Those evolutionary biologists who now doubt orthodox neo-Darwinian theory typically question or reject one or more of the elements of this neo-Darwinian triad (see Fig. 16.1). Eldredge and Gould questioned Darwinian gradualism, which led them to reject the idea that mutational change occurs in minute increments (i.e., the first element of the neo-Darwinian triad just mentioned). Other evolutionary biologists have since rejected other core elements of the neo-Darwinian mechanism and sought to replace them with other mechanisms or processes. This chapter will examine a new class of post-neo-Darwinian evolutionary models that attempt to explain the origin of biological form by deemphasizing the role of random mutations. These models instead emphasize the importance of “self-organizational” laws or processes to the evolution of biological form.

  Self-Organizational Models

  Well before the Altenberg 16 convened, a significant number of evolutionary theorists had already begun to explore alternatives to the neo-Darwinian synthesis. Punctuated equilibrium was one such alternative. But as scientific criticisms of that theory began to mount during the 1980s and 1990s, a group of scientists associated with a think tank in New Mexico, the Santa Fe Institute, developed a new theoretical approach. They called it “self-organization.”

  Whereas neo-Darwinism explains the origin of biological form and structure as the consequence of natural selection acting on random mutations, self-organizational theorists suggest that biological form often arises (or “self-organizes”) spontaneously as a consequence of the laws of nature (or “laws of form”). Natural selection, they theorize, acts to preserve this spontaneously arising order. They think spontaneous self-organizing order, not random genetic mutations, typically provides the ultimate source of new biological form. Thus, they deemphasize two of the three parts of the classical neo-Darwinian triad: random mutations and, to a lesser extent, natural selection.

  In 1993, the most prominent scientist associated with the Santa Fe Institute, former University of Pennsylvania biochemist Stuart Kauffman (see Fig. 15.1), released an eagerly awaited treatise, The Origins of Order: Self-Organization and Selection in Evolution.8 Kauffman articulated a trenchant critique of the creative power of the mutation and selection mechanism, emphasizing some of the criticisms described here in previous chapters. Kauffman advanced a comprehensive alternative theory to account for the emergence of new form. In addition, he advanced a specific proposal for explaining the Cambrian explosion.9

  FIGURE 15.1

  Stuart Kauffman. Courtesy Wikimedia Commons, user Teemu Rajala.

  Kauffman notes that the development of animal body plans involves two phases: cell differentiation and bodyplan morphogenesis (cell organization). He explores the possibility that self-organizational processes at work today—specifically in cell differentiation and bodyplan formation—might help explain how new animal forms originated in the past.

  Kauffman proposes, first, that gene regulatory networks in animal cells—genes that regulate other genes—influence cell differentiation. They do this by generating predictable “pathways of differentiation,”10 patterns by which one type of cell will emerge from another over the course of embryological development as cells divide. For example, early in embryological development, one type of cell (call it cell type “A”) will divide and give rise to two other types of cells (call them types “B” and “C”), which will eventually generate cell types “D” and “E,” and “F and G,” respectively, and many other cell types as the process continues. Kauffman suggests that these pathways of differentiation “may reflect self-organizing features of complex genomic regulatory networks.”11 In other words, networks of regulat
ory genes in embryonic cells determine the pathways by which cells divide and differentiate. Since these patterns of cell differentiation may be determined by regulatory genes, Kauffman regards them as the inevitable byproducts of self-organizational processes. Moreover, since “pathways of cell differentiation [have been] present in all multicellular organisms presumably since the Precambrian,”12 he suggests that self-ordering properties “inherent in a wide class of genomic regulatory networks”13 played a significant role in the origin of the animal forms.

  Kauffman makes a similar case for the importance of self-organizational processes during bodyplan morphogenesis, the second phase of animal development. This phase involves not so much the differentiation of one cell type from another, but the arrangement and organization of different cell types into the distinct tissues and organs that jointly constitute various animal body plans.

  Kauffman again points to known processes of bodyplan development and suggests that they could have played an important role in the formation of the first animal body plans. He cites the importance of the structural or “positional”14 information in cells and cell membranes as the crucial determinants of how different cell types are organized into different animal forms. I discussed the importance of such “epigenetic” information to animal development in Chapter 14 and explained why it poses a problem for neo-Darwinian theory. By recognizing the importance of such information, Kauffman also rejects the neo-Darwinian assumption that a “genetic program” entirely determines animal development. He further regards the patterns of development that result from this positional information as evidence of self-ordering tendencies in matter and the existence of laws of biological form.

  Do these self-ordering tendencies or laws of form, if they exist, explain the origin of animal body plans and the information necessary to build them? They don’t.