Developmental Plasticity and Organismal Ingenuity Challenge Darwin's Theory

At a time when endorsement of Darwinism is reflexively identified with belief in evolution, it may come as a surprise that alternative accounts are gaining acceptance. Scientists studying the history of life on Earth are increasingly moving beyond the nineteenth-century theory, and concepts and insights that were unknown to the founding figures are now on the table. A recent commentary section in that most mainstream of scientific journals, Nature, titled "Does evolutionary theory need a re-think," pitted researchers who answered, "No, all is well," against ones asserting, "Yes, urgently." Denis Noble, a senior figure in British physiology, has recruited a group of investigators from multiple evolution-related disciplines to describe their work on a website that advances the proposition that mechanisms other than natural selection "would better explain evolution processes." None of these critics of Darwinism is a creationist.

Darwin's theory did not simply consist of the observation that plants and animals (including humans) generally breed true but can nonetheless spawn new variants. People had understood this for thousands of years. It also advanced a new model for how large-scale differences between types of organisms (e.g., oysters vs. porcupines) emerge. This was the hypothesis that repeated selection of barely distinguishable variants is the only directional cause of evolutionary modification. According to Darwin there was no other mechanism for the diversification of organisms.

With our current knowledge of embryonic development, however, we have numerous examples of body and organ morphology changing abruptly (though often predictably) as a multicellular animal or plant takes form. This happens when the tissue layers of an early embryo become distinct, when body cavities and segments appear, and when the bones of the limbs of tetrapods, like ourselves, individuate. In many cases we also know just why these sudden changes take place during development. Embryonic tissues are subject to physical effects like phase separation (think oil and water) and nonlinear oscillations based on feedback (similar to noise-reduction circuits in electronic devices). For these phenomena, small changes in the system components or inputs can lead to large changes in outputs. Precipitating events can include mutations in certain "toolkit" genes. But alterations in external conditions can also do the same thing. Phenotypic modification due to the latter is known as "developmental plasticity."

Charles Darwin 1809 - 1882

Could developmental phenomena of this sort drive evolutionary change? Darwin's theory says absolutely not. While Darwin and Carl Linnaeus (the founder of modern biological classification) before him were well aware that novel organisms could appear suddenly (Darwin and his English contemporaries called them "sports"), these were considered "one-offs," akin to miracles. The scientific-technological mindset in Darwin's time instead was Newtonian gradualism ("an object in motion remains in motion unless acted upon by an external force"), and the trial-and-error optimization characteristic of nascent industrialism. Although some scientists ("mutationists") thought that sudden changes in biological properties ("saltations") were a factor in evolution, they lacked the later knowledge of developmental mechanisms that would have explained why only some mutations were of "large effect" (also called "macromutations"). Most scientists who carried on Darwin's ideas simply ignored development, assuming that only mutations of small effect contributed to evolutionary change.

Carl Linnaeus 1707 - 1778

The dismissal of macromutations was in accord with the Malthusian assumption of Darwinism that all members of a given population compete for the same resources. The supposed need to "get with the program" and do the same thing as well as your relatives and neighbors, or even better, if you are to push evolution forward is the essence of natural selection. Darwin appropriated Thomas Malthus' notion that population growth tends to outstrip growth of food availability, adding that if there was variability among individuals, those who survived would be better suited ("fitter") for the task of acquiring the commonly desired resources. These sought-after resources came to include such things as preferred mates or, in the case of flowers, pollinators.

Thomas Robert Malthus 1766 - 1834

Any heritable variant that promoted fitness (called an "adaptation") would be more prominently represented in the following generation. Without developmental plasticity or macromutations, any distinctive adaptations ("novelties": the flowers of plants, the hands and feet of tetrapods) would have to emerge bit by bit. In the words of the arch-Darwinist Richard Dawkins, evolution "must be gradual when it is being used to explain the coming into existence of complicated, apparently designed objects.... Without gradualness in these cases, we are back to miracle, which is simply a synonym for the total absence of explanation."

But novel structures, which can arise suddenly by developmental reorganization, need only emerge gradually in a population if all its members are trying to do the same thing. It would be exceedingly unlikely for a macromutation or environmentally induced plastic response to make an individual better at doing exactly what other members of its population already do. But is the Malthusian assumption necessary? Human ingenuity has generally thwarted overpopulational catastrophe; whatever the ultimate carrying capacity of the Earth may be, the trajectory of human evolution up till now is not explained by Malthus' model. Darwinists still adhere to the doctrine of scarcity when it comes to nonhuman evolution, however. The notion that an animal or plant very different in form or functional capability from a typical member of its founding population could utilize the new property in a creative fashion, to inhabit a new ecological niche and live off different resources, is alien to the Darwinian way of thinking. If "hopeful monsters" (a term coined by the mid-twentieth-century geneticist Richard Goldschmidt to describe the results of macromutations), could establish new categories of organisms, the role of natural selection would be greatly diminished.

This happens all the time, however:

• Invasive species are organisms introduced into places where their ancestors never lived. It would be difficult to argue that they come equipped with adaptations refined by Darwinian selection suitable to their new habitats. They are strangers in a strange land yet figure out how to make their way and often prosper.

• A macromutation that radically changed the orientation of head feathers appeared in the distant past in a subspecies of pigeon and caused its carriers to have a prominent head crest. The crest came to be used for display and mate selection. A confirmed Darwinist might argue that this was one of the extremely rare cases where a suddenly appearing novelty happened to insinuate itself into a preexisting, evolutionarily refined behavioral complex. But this is contradicted by the fact that the original macromutation spread by breeding into a wide range of ecologically and behaviorally disparate pigeon varieties.

• Plants can hybridize and form fertile progeny more readily than animals. In certain cases, by a process of "transgressive segregation," the hybrid progeny will exhibit extreme phenotypes compared with the parental lines. These phenotypically novel forms can then become founding members of new species, inhabiting environmental niches very different from those in which they originated. It is entirely untenable to maintain that the latent novel traits originated by past rounds of gradual natural selection that specifically adapted them to the prospective novel niches.

The question of how the novelties exhibited by hopeful monsters could be passed on to their offspring has been something of a puzzle in the past. This is because phenotypic plasticity does not depend on genetic change, and macromutations typically occur in a single individual that would lack mating partners. But the more we learn about the dynamics of development, the more it becomes clear that the abrupt transitions in form or function due to plasticity and macromutations are complementary effects of the workings of the same underlying "physico-genetic" systems.

A novelty due to perturbation of the developmental system by factors in a new environment can be maintained over generations without genetic change. It can become independent of its environment when genetic change after the fact stabilizes it, its production thereby becoming "assimilated" to the genome. A novelty associated with a macromutation tips the balance of a developmental system in a similar fashion. Since the gene itself is not the "cause" of the complex novelty (the full developmental system is), it can be transferred by mating to offspring with a similar developmental system and (as seen with the pigeon head crest gene), precipitate the same transformation. Contrary to Linnaeus, Darwin and Dawkins, there is nothing miraculous about this.

All of this has been seriously contemplated by the most insightful evolutionary theorists of the past century, despite the domination of the narrative by more hide-bound Darwinians. William Bateson, before the age of molecular biology, understood that forms are generated by genes only with the participation of physics, which makes development sensitive to the environment, and evolutionary change often discontinuous. John Maynard Smith declared himself "open-minded about the possibility that development may impose discontinuous constraints on the pattern of phenotypic variation," concluding that "[i]f so, mutations of large phenotypic effect may sometimes initiate new evolutionary departures." W. D. Hamilton, like Maynard Smith, an icon of the Darwinian synthesis, writing with colleagues on evolution in flooded forests, asserted, "Genetically assimilable plasticity often precedes radical novelty." More recently, Richard Lewontin's recognition that organisms invent their own ways of life, rather than passively fitting into preexisting niches, laid the foundation for modern niche construction theory.

To be sure, the extent to which these non-Darwinian mechanisms may have contributed to evolutionary change was difficult to ascertain in the absence of an understanding of the developmental relationship between genes and form. Now that this is coming into clearer view and more phenomena are yielding to these new modes of explanation, only the most obdurate keepers of Darwin's flame remain in denial of the extent to which the old theory is being sidelined.

Stuart A. Newman is professor of cell biology and anatomy at New York Medical College, where he directs a research program in developmental biology. He has contributed to several scientific fields, including the theory of biochemical networks and cell pattern formation, protein folding and assembly, and mechanisms of morphological evolution. He also writes on the social and cultural dimensions of biology and biotechnology, and was a co-founder of the Council for Responsible Genetics, Cambridge, MA. He is co-editor (with Gerd B. Müller) of: "Origination of Organismal Form: Beyond the Gene in Developmental and Evolutionary Biologyand co-author (with Gabor Forgacs) of Biological Physics of the Developing Embryo".

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