On punctuated equilibria: Reply to Eldredge and Gould
by Jerry A. Coyne and Brian Charlesworth
n the past 25 years, Eldredge and Gould have proposed so many
different versions of their theory that it is difficult to describe it with any
accuracy. Initially, punctuated equilibrium theory described an ubiquitous
pattern of morphological stasis in fossil lineages, interrupted by rare but
rapid bursts of change that accompanied the splitting of lineages (speciation).
These rapid changes were also said to be random with respect to long-term
evolutionary trends, which were caused by the differential persistence of
species having different traits (1).
Our concern as evolutionary geneticists (2) has been with Eldredge and Gould's
repeated revisions of the mechanisms proposed for stasis and rapid evolution.
Punctuated equilibrium originally attracted great attention because it invoked
distinctly non-Darwinian mechanisms for stasis and change (3). These mechanisms
were said to decouple macroevolution from microevolution, leading to Gould's
pronouncement that "if Mayr's characterization of the synthetic theory [of
evolution] is accurate, then that theory, as a general proposition, is
effectively dead, despite its persistence as textbook orthodoxy" (4, p. 120).
Yet many evolutionists saw no obvious contradiction between punctuated pattern
and Darwinian process: Stasis can result from stabilizing selection (for
example, long periods of environmental stability); rapid evolution can result
from selection-driven responses to sudden environmental change or invasion of
new habitats; and the association of morphological change with speciation can
result from the fact that both are promoted by adaptation to new environments
Eldredge and Gould originally ascribed stasis to developmental constraints:
Organisms could not respond to selection because their developmental programs
were inherently resistant to change (1, (3, (4, (6). This non-Darwinian
explanation, which was severely criticized (5), was supplanted by the notion
(7). that species show morphological stasis because their constituent
populations adapt to diverse local habitats, resulting in no net change in the
"average" phenotype of the species. This idea is inconsistent with their view
that developmental constraints often prevent adaptive change.
Gould and Eldredge now suggest that stasis may be caused by species tracking
their habitats as the environment changes [an idea proposed earlier by Maynard
Smith (8)], which is a form of stabilizing selection. They also appeal to
Sewall Wright's shifting balance theory of evolution, suggesting that a species
composed of partially isolated populations cannot evolve as a unit. This
suggestion appears to be a misinterpretation of Wright's theory, which he
consistently presented as a mechanism for adaptive transformation of an entire
species (9). Partial isolation of populations resulting from spatial separation
does not preclude favorable or neutral mutations from spreading through an
entire species (10). The suggestion by Eldredge and Gould that "[g]enetic
theory should have explicitly predicted stasis in numerically rich species"
contradicts theoretical arguments showing that natural selection is most
effective in large populations (11) and does not account for abundant evidence
from artificial selection experiments confirming this prediction (12).
Eldredge and Gould have proposed an equally diverse array of explanations for
rapid "punctuated" evolution. It was initially ascribed to the breakdown of
developmental constraints in small, speciating populations (a non-Darwinian
process) (1) and later to the occurrence of single mutations with large effects
(including homeotic mutations) or to chromosome rearrangements affecting gene
expression (3, (4, (6). Gould, for example, asserted (4), p. 127)
I envisage a potential saltational origin for
the essential features of key adaptations. Why may we not imagine that gill
arch bones of an ancestral agnathan moved forward in one step to surround
the mouth and form proto-jaws?
But Gould and Eldredge later said (13), p. 226; see also(10), p. 66) that
"Opponents now accept that punctuated equilibrium was never meant as a
saltational theory... ." Yet even this statement was later qualified.
Commenting on the experiments of Elena et al. in E. coli (14), which showed
punctuated change in cell size resulting from sporadic mutations of large
effect, Gould noted that these results are "deeply similar to [punctuated
equilibrium]. There is an underlying commonality in the style of change" (14),.
Eldredge and Gould now appear to see no connection between punctuated
equilibrium and the results of Elena et al.
Eldredge and Gould's disclaimer about the role of species selection in
punctuated equilibrium theory (our attribution of this idea to Elena et al. was
a typographical error) is not consistent with their numerous published
statements that species selection is a major engine of macroevolution (4); p.
119; see also (3, 6).
If a scientific theory is to be of any value as a tool for exploring the real
world, it must have some stability as a set of propositions open to empirical
test. Punctuated equilibrium has undergone so many transformations that it is
hard to distinguish its core of truth from the "statement that morphological
evolution sometimes occurs episodically."
Jerry A. Coyne
Department of Ecology and Evolution,
University of Chicago,
1101 East 57 Street,
Chicago, IL 60637, USA
- N. Eldredge and S. J. Gould, in Models
in Paleobiology, T. J. M. Schopf, Ed.
(Freeman, Cooper, San Francisco, 1973), pp. 82-115.
- J. A. Coyne and B. Charlesworth, Science 274, 1748 (1996) .
- S. J. Gould and N. Eldredge, Paleobiology 3, 115 (1977).
- S. J. Gould, ibid. 6, 119 (1980).
- R. Lande, ibid., p. 233; B. Charlesworth, M. Slatkin, R. Lande, Evolution 36,
474 (1982); J. S. Levinton, Genetics, Paleontology and Macroevolution
(Cambridge Univ. Press, Cambridge, 1988); B. Charlesworth in Paleobiology: A
Synthesis, D. E. G. Briggs and P. R. Crowther, Eds. (Blackwell, Oxford, 1990),
- S. J. Gould, Science 216, 380 (1982) .
- N. Eldredge, Macroevolutionary Dynamics (McGraw-Hill, New York, 1989).
- J. Maynard Smith, Ann. Rev. Genet. 17, 11 (1983).
- S. Wright, Proc. 6th Int. Congr. Genet. 1, 356 (1932).
- R. A. Fisher, Ann. Eugen. 7, 355 (1937).
- , The Genetical
Theory of Natural Selection (Oxford Univ. Press, Oxford, 1930).
- K. E. Weber, Genetics 144, 205 (1996) .
- S. J. Gould and N. Eldredge, Nature 366, 226 (1993) .
- S. J. Gould, New York Times, 25 June 1996, p. B5.
[ Jerry A. Coyne, Brian Charlesworth, "On punctuated equilibria. Reply to
Eldredge and Gould [letter]." Science 1997, 276 (5311): 337-341. ]
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