Suggested Readings on the Problem of Animal Macroevolution
Evolution News & Views February 25, 2016 3:47 AM
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.