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Suggested Readings on the Problem of Animal Macroevolution

Purple sea urchins.jpg

An email correspondent asks:

Given the saltations seen in the fossil record (as well as molecular data), it seems that the gradual ratcheting of "point mutation by point mutation" evolution has little efficacy in explaining the diversity of life. Doug Axe has done work on this. Are there other clear demonstrations of the improbability of getting from one adaptive peak to another via this model?

Yes, an enormous literature exists within evolutionary biology about the implausibility of point-mutation-by-point-mutation transitions between adaptive peaks. The following list, which focuses only on animal macroevolution, runs only to 2011. Many more recent papers have been published.

These papers represent a sample of biological thinking about the problem of animal macroevolution, or macroevolution generally, over the past three decades. The authors agree that some amendment, perhaps radical, is needed to fix "textbook" (standard) neo-Darwinian theory, in order to solve the open question of how animal form and complexity arose via an undirected evolutionary process.

They do not, however, agree on the solution, and may disagree strongly among themselves, for instance, on the question of whether animal embryos will tolerate deep changes to their essential developmental control networks. The authors come from a range of disciplinary backgrounds, such as genetics, developmental biology, paleontology, and comparative anatomy. None is an advocate of intelligent design, and none would see his ideas as supporting intelligent design.

A recommendation: While all the articles are thoughtful, if the reader is pressed for time, Thomson's 1992 article is the shortest and most accessible, while Miklos's 1993 article, although the longest, is the most wide-reaching and vigorously argued.

1. John F. McDonald, "The Molecular Basis of Adaptation: A Critical Review of Relevant Ideas and Observations," Annual Review of Ecology and Systematics 14 (1983):77-102.

In 1983, geneticist John McDonald (at the time, at the University of Georgia) surveyed the evidence bearing on the role of genetic variation in macroevolutionary change. He argued that "naturally segregating" variation -- that is, of the character or magnitude normally seen in animal populations -- appeared to play a limited role, if any, in "macroevolutionary events" (p. 92). So striking was this pattern that McDonald dubbed it "a great Darwinian paradox" (p. 93), placing the following points in italics for emphasis:

Those loci that are obviously variable within natural populations do not seem to lie at the basis of many major adaptive changes, while those loci that seemingly do constitute the foundation of many, if not most, major adaptive changes apparently are not variable within natural populations. [p. 93]

2. Keith Stewart Thomson, "Macroevolution: The Morphological Problem," American Zoologist 32 (1992):106-112.

Keith Thomson is a vertebrate paleontologist and anatomist who taught at Yale and Oxford; at the time this paper was published, he was president of the Academy of Natural Sciences in Philadelphia. Throughout his career, Thomson has been concerned with the explanatory adequacy of neo-Darwinism. "The basic article of faith of a gradualist [neo-Darwinian] approach," he writes in this paper,

is that major morphological innovations can be produced without some sort of saltation. But the dilemma of the New Synthesis [textbook theory] is that no one has satisfactorily demonstrated a mechanism at the population genetic level by which innumerable very small phenotypic changes could accumulate rapidly to produce large changes: a process for the origin of the magnificently improbable from the ineffably trivial.

3. George L.G. Miklos, "Emergence of organizational complexities during metazoan evolution: perspectives from molecular biology, palaeontology, and neo-Darwinism." Memoirs of the Association of Australasian Palaeontologists 15 (1993):7-41.

George Miklos is an Australian geneticist (who, when this paper was published, worked at the Australian National University in Canberra). His 1993 paper, the longest in this collection of articles, is an often vehement manifesto attacking the explanatory claims of neo-Darwinian theory, largely on the grounds that textbook theory completely ignores the relevant level of mechanistic detail where macroevolutionary change is concerned. From the Abstract:

The popular theory of evolution is the modern synthesis (neo-Darwinism) based on changes in populations underpinned by the mathematics of allelic variation and driven by natural selection. It accounts more for adaptive changes in the colouration of moths, than in explaining why there are moths at all. This theory does not predict why there were only 50 or so modal body plans, nor does provide a basis for rapid, large-scale innovations. It lacks significant connection with embryogenesis and hence there is no nexus to the evolution of form. It fails to address the question of why the anatomical gaps between phyla are no wider today than they were at their Cambrian appearance....I believe that the search for the Holy Grail (evolution of complex morphologies and nervous systems) has been conducted in the wrong place and at the wrong levels by evolutionary biologists. [p. 7]

4. Robert L. Carroll, "Toward a new evolutionary synthesis," Trends in Ecology and Evolution 15 (2000):27-32.

Robert Carroll is a vertebrate paleontologist and professor emeritus at McGill University in Montreal. In this article, he argues:

Research in many disciplines over the past 40 years has demonstrated that the patterns, processes and forces of evolution are far more diverse than hypothesized by Darwin and the framers of the evolutionary synthesis...Increasing knowledge of the fossil record and the capacity for accurate geological dating demonstrate that large-scale patterns and rates of evolution are not comparable with those hypothesized by Darwin on the basis of extrapolation from modern populations and species. [p. 27]

5. Scott F. Gilbert, John M. Opitz, and Rudolf A. Raff, "Resynthizing Evolutionary and Developmental Biology," Developmental Biology 173 (1996):357-72.

The authors are developmental biologists (Gilbert at Swarthmore College and Raff at Indiana University) and a medical geneticist specializing in developmental anomalies (Opitz at the University of Utah). In this paper, published during a period of rapid growth for the young field of "evo-devo" (evolutionary developmental biology), the authors argue that, despite its merits with smaller-scale phenomena, "the Modern Synthesis" (textbook neo-Darwinism) fails to explain macroevolution. They write:

Starting in the 1970s, many biologists began questioning its 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 only 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."

6. Douglas Erwin, "Evolutionary uniformitarianism," Developmental Biology 357 (2011):27-34.

Douglas Erwin is an invertebrate paleontologist at the Smithsonian's National Museum of Natural History and a leading expert on the origin of animal body plans. He collaborates frequently with developmental biologist Eric Davidson (see reading 7, below) on macroevolutionary questions. In this paper, Erwin argues that the manifold discontinuities among the animal groups -- what he calls "the clumpy distribution of morphologies" (p. 27) -- is not an artifact of sampling, but the real signal of history. Neo-Darwinism, he continues, "attempted to rescue [its] uniformitarian explanations by 'explaining away' this empirical pattern as a result of various biases" (p. 33). In Erwin's view, however, the processes of evolution have changed fundamentally over time, and evolutionary events possible in the Cambrian, such as the origin of the animal phyla, were unique occurrences.

7. Eric Davidson, "Evolutionary biology as regulatory systems biology," Developmental Biology 357 (2011):35-40.

Eric Davidson was a developmental biologist at Caltech who pioneered the study of the purple sea urchin (Strongylocentrotus purpuratus) as a model system. In his books and articles, he strongly attacked the explanatory shortcomings of neo-Darwinism, arguing that the theory focuses attention at the wrong level (small-scale variation), neglecting the genuine mechanisms of body plan construction. This paper gives a good overview of Davidson's recent thinking, starting with his critique of neo-Darwinian theory:

Of [neo-Darwinism], I shall have nothing to say, as mechanistic developmental biology has shown that its fundamental concepts are largely irrelevant to the process by which the body plan is formed in ontogeny. In addition it gives rise to lethal errors in respect to evolutionary process. Neo-Darwinian evolution is uniformitarian in that it assumes that all process works the same way, so that evolution of enzymes or flower colors can be used as current proxies for study of evolution of the body plan. It erroneously assumes that change in protein coding sequence is the basic cause of change in developmental program; and it erroneously assumes that evolutionary change in body plan morphology occurs by a continuous process. All of these assumptions are basically counterfactual. This cannot be surprising, since the neo-Darwinian synthesis from which these ideas stem was a pre-molecular biology concoction focused on population genetics and adaptation natural history, neither of which have any direct mechanistic import for the genomic regulatory systems that drive embryonic development of the body plan. [pp. 35-36]

8. Andreas Wagner, "The molecular origins of evolutionary innovations," Trends in Genetics 27 (2011):397-410.

Andreas Wagner is a theoretical biologist at the Institute of Evolutionary Biology, University of Zurich. His research focuses on how complex systems function, respond to perturbation, and are modified by evolutionary processes. Recently, he has been addressing the problem of innovation, or the origin of complex novelties in organisms, the sine qua non of any evolutionary theory: How did new structures -- body plans, organ systems, etc. -- come to be, where they did not exist before? In this paper, Wagner begins by expressing his dissatisfaction with standard (neo-Darwinian) theory:

We know many examples of innovations, each a fascinating piece of natural history. However, we know few of the principles that explain the ability of living things to innovate through a combination of natural selection and random genetic change. Random change by itself is not sufficient, because it does not necessarily bring forth beneficial phenotypes. For example, random change might not be suitable to improve most man-made, technological systems. Similarly, natural selection alone is not sufficient: As the geneticist Hugo de Vries already noted in 1905, "natural selection may explain the survival of the fittest, but it cannot explain the arrival of the fittest." Any principle of innovation needs to explain how novel, beneficial phenotypes can originate. [p. 397]

These brief summaries are intended to orient the reader who may be unfamiliar with the authors or the disputes, but cannot substitute for a careful reading of the papers themselves. These papers are only a tiny sample, of course, of a very much larger scientific literature addressing the problem of macroevolution.

Image: Purple sea urchins, by Gregory "Slobirdr" Smith [CC BY-SA 2.0], via Wikimedia Commons.