966. Where Do Complex Organisms Come From?

Stuart A. Newman

By Stuart A. Newman, Huffington Post, December 4, 2012

Although evidence is all around us of a deep geological past, and of multifarious genealogical relationships among ourselves and the organisms we currently share the planet with, scientists still have only sketchy ideas about how complex living forms arose in the course of evolution. As James Shapiro described in a recent Huffington Post blog entry, there has been good progress in understanding how complex cells arose from simpler ones by cell mergers, or "symbiogenesis." But even "simple" cells are quite complex, and the origins of cellular life (aka "chemical evolution"; read more here), are far from settled.

What about the complex bodies and organs of animals and plants? This is what primarily concerned the nineteenth century naturalists Alfred Russel Wallace and Charles Darwin (neither of whom knew anything about the internal intricacies of cells, including the nature of their genes), as they pondered the transformations of life throughout its history. Their solution was "natural selection," the acquisition of new forms and functions in populations of organisms by small increments, over long times, with each gradual change being subject to the sieve of "adaptation." Was each heritable variation better suited to some pre-existing task? If so, its exemplars increased and multiplied. If not, their kind faded away.

While it may be an adequate scenario for the refinement of some already-existing characters -- the beaks of finches, color intensity of moths -- the "microevolutionary" process envisioned by Darwin and his successors does not account in any plausible way for "macroevolutionary" patterns such as the differences between oysters and grasshoppers, fish and birds. In fact, adaptationist gradualism, though still popular in some scientific circles, is increasingly questioned and found wanting by evolutionary biologists working in an expanded set of disciplines.

By incorporating embryonic development and its underlying physico-genetic processes into evolutionary theory, investigators are learning that abrupt alterations in body plan and other aspects of organismal form can occur in response to environmental change or gene mutation in ways that affect multiple members of a population and exhibit consistent patterns of inheritance. Furthermore, there is increasing emphasis on the resourcefulness of organisms and their ability to construct their own niches. Having a "phenotype" (the outward manifestation of biological identity), very different from that of one's progenitors is no longer considered disqualifying for survival.

Although the writings of Wallace and Darwin's predecessor Jean-Baptiste Lamarck anticipated some current ideas about the morphologically prolific processes of embryo generation ("Le pouvoir de la vie") and the active strivings of organisms for survival in their environmental settings ("L'influence des circonstances"), Darwin's less speculative approach encouraged readier acceptance of his ideas by other scientists and the educated public. (The playwright George Bernard Shaw, in the preface to Back to Methuselah, put it more sharply as "Why Darwin converted the crowd.") By specifying that the variations in organismal form and function sorted out by natural selection were entirely incremental, Darwin's theory could side-step any questions about how the altered forms actually arose. It also created an incentive to deny the relevance of the more profound changes (Darwin called them "sports") that were well known to arise in natural populations. This may have been the best that could be done circa 1850, but its retention in the so-called modern evolutionary synthesis a century later was a scandalous legacy of the banishment of developmental biology (embryology) from the synthesis, and the indifferent attitude of biological education regarding the physical sciences.

The physical science of Darwin's time, which provided a backdrop to his thinking, was dominated by Newton's concept that material bodies only change course in proportion to external forces that act on them. It also included the often more pertinent notion (e.g., for the molding of pliable materials) from Aristotle of matter changing position or shape only to the extent that it continues to be pushed. These ideas, however, did not pretend to account for the sudden reorganizational changes (freezing, melting, phase separation, compositional change) seen in complex chemically and mechanically active materials. We now recognize that the tissues of a developing embryo are indeed such non-Newtonian, non-Aristotelian materials. By the end of Darwin's life new physical theories were being put forward to explain abrupt and large-scale changes in such materials, and by extension, the character and transformations of organisms and their organs.

Here is a partial list of late nineteenth and early twentieth-century physical concepts that have proved relevant to developmental processes (with the phenomenon they explain, at least partly, in parentheses): dynamical systems (ability of cells having the same genome to switch between different "types"), phase separation of liquids (capacity of embryonic tissues to form several non-mixing layers), chemical oscillations (propensity of embryonic tissues to organize into tandem segments), "Turing-type" reaction-diffusion systems (the formation in tissues of regularly spaced structures like feather and hair buds, pigment stripes, or the bones of the limb skeleton). All or most of these processes (termed "mesoscale," being most relevant to objects the size and texture of cell clusters), along with several others, are harnessed and mobilized by the secreted products of specific genes during embryogenesis in every one of the animal phyla (e.g., arthropods, mollusks, nematodes, chordates and so forth).

What can the existence and action of such protean generative processes tell us about the origin of organismal complexity? First, let's look at some of the expectations of the natural selection-based modern synthesis: (i) the largest differences within given categories of multicellular organisms, the animals or plants, for example, should have appeared gradually, only after exceptionally long periods of evolution; (ii) the extensive genetic changes required to generate such large differences over such vast times would have virtually erased any similarity between the sets of genes coordinating development in the different types of organism; and (iii) evolution of body types and organs should continue indefinitely. Since genetic mutation never ceases, novel organismal forms should constantly be appearing.

All these predictions of the standard model have proved to be incorrect. The actual state of affairs however, are expected outcomes of the "physico-genetic" picture outlined above. Briefly, we now know that complex multicellular organisms appeared rapidly (on a geological time scale, i.e., two episodes of no more than 10-20 million years each), employing for developmental patterning not newly evolved genes, but genes that had evolved for entirely different functions in single-celled ancestors. Generation of novel complex forms was able to happen so rapidly because the genetic ingredients were already at hand, but in addition because the mesoscale physical processes described above also did not require an incremental sequence of steps to come into existence. Everything was in place for an organismal "big bang" once simple multicellular clusters had appeared.

Unlike the presumption of the standard model, however, the physico-genetic scenario for the origination of complex multicellular forms is not open-ended and limitless. As with any material organizational process (think waves and eddies in liquid water), the relevant physics can only elicit those structural motifs inherent to the material in question. Thus we should not expect to see, and indeed don't, the "endless forms" that Darwin invoked in The Origin of Species.

With a 19th century notion of incremental material transformations no longer relevant to comprehending the range of organismal variation that has appeared throughout the history of life on Earth, the other pillar of the standard model can be discarded along with it. Specifically, if, as affirmed by niche construction theory, phenotypically novel animals or plants can invent new modes of existence in novel settings, rather than succumbing to a struggle for survival in the niches of their origin, there is no need for cycles of selection for marginal adaptive advantage to be the default explanation for macroevolutionary change.

Additional reading

Newman, S.A. (2012). Physico-genetic determinants in the evolution of development. Science 338, 217-219.

Müller, G.B. (2007). Evo-devo: extending the evolutionary synthesis. Nature Reviews Genetic 8, 943-949.

Forgacs, G., and Newman, S.A. (2005). Biological physics of the developing embryo (Cambridge, Cambridge Univ. Press).

Odling-Smee, F.J., Laland, K.N., and Feldman, M.W. (2003). Niche construction: the neglected process in evolution (Princeton, N.J., Princeton University Press).

Stuart A. Newman is Professor of Cell Biology and Anatomy at New York Medical College.