On Punctuated Equilibria

by Niles Eldredge, Stephen Jay Gould and Jerry A. Coyne, Brian Charlesworth

On punctuated equilibria

by Niles Eldredge and Stephen Jay Gould

n their technical comment of 6 December (21 June 1996, p. 1748) on a report of punctuated patterns of evolutionary change in a laboratory culture of Escherichia coli, Jerry A. Coyne and Brian Charlesworth perpetuate several incorrect perceptions of the original notion, and subsequent discussions, of punctuated equilibria (1).

They are correct that punctuated equilibria apply to sexually reproducing organisms and that morphological evolutionary change is regarded as largely (if not exclusively) correlated with speciation events. However, they err in suggesting that we attribute stasis strictly to "developmental constraints," which represent only one of a set of possible mechanisms that we have suggested for the causes of stasis. Others include habitat tracking and the internal structure of species themselves [for example, (2)].

Habitat tracking [as when the distributions of Pleistocene species oscillate on a north-south gradient in concert with global temperature fluctuations (3)] demonstrates the stability of species morphologies in the face of environmental change as long as suitable habitat can be found and occupied. Although habitat tracking does not rule out developmental homeostasis, it suggests that stabilizing selection, rather than directional selection, will be the rule as long as species can continue to "recognize" and occupy suitable habitat elsewhere under a regime of environmental change.

Moreover, the very structure of species, broken up into semi-isolated populations each integrated into different ecosystems, should for the most part preclude the possibility of any widespread species evolving as an entirety in any one particular direction (4). Genetic theory should have explicitly predicted stasis in numerically rich species. B. S. Lieberman et al. (5) present empirical data suggesting that stasis in two species lineages of Devonian brachiopods was governed more by such constraints of species organizational structure than by habitat tracking.

Coyne and Charlesworth further state that "the punctuated changes in the fossil record are said to occur via 'species selection,' in which descendant species rapidly supplant their ancestors"—a statement they attribute to Santiago F. Elena et al. (Reports, 21 June 1996, p. 1802). Species selection is one of a set of models proposed to explain evolutionary trends in the fossil record—given the absence of strong evidence that long-term trends are merely the accumulated outcome of within-species gradual directional evolution (1, 2, 6). Replacements of ancestral species by presumed descendants (which usually appear "punctuational" in the fossil record) are generally interpreted as ecological or biogeographic replacement events [for example, (2, 7)] and not as the result of differential species births, direct competition, or any other phenomenon that might be considered "species selection."

Coyne and Charlesworth conclude with a critique of punctuated equilibria—asserting that when one excises the "novel and non-Darwinian" mechanisms of punctuated equilibria, "the theory reduces to the noncontroversial statement that morphological evolution sometimes occurs episodically." The documentation that (i) morphological stasis is the overwhelming rule in the fossil record of metazoan species and that (ii) morphological change does indeed seem to be correlated to a strong and unexpected degree with true speciation constitutes a two-pronged empirical pattern that requires careful analysis. To so mischaracterize punctuated equilibria not only impugns the significance of our model, it misstates the dominant empirical evolutionary pattern of the history of life itself.

Niles Eldredge
Department of Invertebrates,
American Museum of Natural History,
New York, NY 10024, USA

Stephen Jay Gould
Museum of Comparative Zoology,
Harvard University,
Cambridge, MA 02138, USA

References

1. N. Eldredge and S. J. Gould, in Models in Paleobiology, T. J. M. Schopf, Ed.
(Freeman, Cooper, San Francisco, 1972), pp. 82-115; S. J. Gould and N. Eldredge, Paleobiology 3, 115 (1977); Nature 332, 211 (1988); ibid. 334, 19 (1988); ibid. 366, 223 (1993).
2. N. Eldredge, Macroevolutionary Dynamics (McGraw-Hill, New York, 1989); in New Approaches to Speciation in the Fossil Record, D. Erwin and R. Anstey, Eds. (Columbia Univ. Press, New York, 1995), p. 39; Reinventing Darwin (Wiley, New York, 1995), p. 57.
3. G. R. Coope, Ann. Rev. Ecol. Syst. 10, 247 (1979).
4. S. Wright, Proc. Sixth Int. Congr. Genet. 1, 356 (1932).
5. B. S. Lieberman, C. E. Brett, N. Eldredge, Paleobiology 21, 15 (1995).
6. E. S. Vrba, S. Afr. J. Sci. 76, 61 (1980); Syst. Zool. 33, 318 (1984).
7. C. E. Brett and G. C. Baird, in New Approaches to Speciation in the Fossil Record, D. Erwin and R. Anstey, Eds. (Columbia Univ. Press, New York, 1995), p. 285; E. S. Vrba, S. Afr. J. Sci. 81, 229 (1985).

[ Niles Eldredge, Stephen Jay Gould, "On punctuated equilibria [letter]." Science 1997, 276 (5311): 337-341. ]

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 (5).

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
Brian Charlesworth
Department of Ecology and Evolution,
University of Chicago,
1101 East 57 Street,
Chicago, IL 60637, USA

References

1. N. Eldredge and S. J. Gould, in Models in Paleobiology, T. J. M. Schopf, Ed. (Freeman, Cooper, San Francisco, 1973), pp. 82-115.
2. J. A. Coyne and B. Charlesworth, Science 274, 1748 (1996) .
3. S. J. Gould and N. Eldredge, Paleobiology 3, 115 (1977).
4. S. J. Gould, ibid. 6, 119 (1980).
5. 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), pp. 100-106.
6. S. J. Gould, Science 216, 380 (1982) .
7. N. Eldredge, Macroevolutionary Dynamics (McGraw-Hill, New York, 1989).
8. J. Maynard Smith, Ann. Rev. Genet. 17, 11 (1983).
9. S. Wright, Proc. 6th Int. Congr. Genet. 1, 356 (1932).
10. R. A. Fisher, Ann. Eugen. 7, 355 (1937).
11. ———, The Genetical Theory of Natural Selection (Oxford Univ. Press, Oxford, 1930).
12. K. E. Weber, Genetics 144, 205 (1996) .
13. S. J. Gould and N. Eldredge, Nature 366, 226 (1993) .
14. 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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