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