Gould & Eldredge, Punctuated equilibrium comes of age


transition from Mesohippus to Miohippus68, conforms to punctuated equilibrium, with stasis in all species of both lines, transition by rapid branching rather than phyletic transformation, and stratigraphic overlap of both genera (one set of beds in Wyoming has yielded three species of Mesohippus and two of Miohippus, all contemporaries). Prothero and Shubin conclude: "This is contrary to the widely-held myth about horse species as gradualistically-varying parts of a continuum, with no real distinctions between species. Throughout the history of horses, the species are well-marked and static over millions of years. At high resolution, the gradualistic picture of horse evolution becomes a complex bush of overlapping, closely related species."

* Relative frequencies.
Elegant cases don't make punctuated equilibrium any more than a swallow makes a summer, but there are a growing number of reports documenting an overwhelming relative frequency (often an exclusivity) for punctuated equilibrium in entire groups or faunas. Consider the lifetime testimonies of taxonomic experts on microfossils69, on brachiopods70,71 and on beetles72. Fortey73 has concluded for trilobites and graptolites "that the gradualistic mode does occur especially in pelagic or planktic forms, but accounts for 100% or less of observations of phyletic change, and is relatively slow".

Other studies access all available lineages in entire faunas and assert the dominance of punctuated equilibrium. Stanley and Yang26 found no gradualism at all in the classic Tertiary molluscan sequences of the Gulf and Atlantic Coasts, With the exception of Gryphma, Hallam23 detected no phyletic change in shape (but only for body size) in any Jurassic bivalve in Europe. Kelley24,25 documented the prevalence of punctuation for molluscs in the famous Maryland Miocene sequence, and Vrba74 has done the same for African bovids. Even compilations from the literature, so strongly biased by previous traditions for ignoring stasis as non-data and only documenting putative gradualism, grant a majority to punctuated equilibrium, as in Barnovsky's75 compendium for Quaternary mammals, with punctuated equilibrium "supported twice as often as phyletic gradualism . . . the majority of species considered exhibit most of their morphological change near a speciation event, and most species seem to be discrete entities". When controlled studies are done by one team in the field, punctuated equilibrium almost always seems to predominate. Prothero76 "examined all the mammals with a reasonably complete record from the Eocene-Oligocene beds of the Big Badlands of South Dakota and related areas in Wyoming and Nebraska . . . With one exception (gradual dwarfing in the oreodont Miniochoerus), we found that all of the Badlands mammals were static through millions of years, or speciated abruptly (if they changed at all)."

* Inductive patterns.
Even more general inductive patterns should be explored as criteria. Stanley38,77 has proposed a series of tests, all carried out to punctuated equilibrium's advantage. Others suggest that certain environments and ecologies should be conducive to one preferred mode along the continuum of possibilities. "Johnson78,79 suggests that punctuated equilibrium should dominate in the benthic environments that yield most of our fossil record, while gradualism might prevail in pelagic realms. Sheldon80 proposes the counter-intuitive but not unreasonable idea that punctuated equilibrium may prevail in unstable environments, gradualism in stable regimes.

* Tests from living organisms.
Distinct evolutionary modes yield disparate patterns as results; punctuated equilibrium might therefore be tested by studying the morphological and taxonomic distributions of organisms, including living faunas. (Several of Stanley's tests38 use modern organisms, and other criteria from fossils should be explored—especially the biometric discordance or orthogonality, favourable to punctuated equilibrium and actually found where investigated25,81, of within and between species trends.)

Cladistic patterns should provide a good proving ground. Avise82 performed an interesting and much quoted test, favourable to gradualism, by comparing genetic and morphological differences in two fish clades of apparently equal age and markedly different speciation frequencies. But as Mayden83 argued, this test was wrong in its particular case, and non-optimal as a general procedure; a better method would compare cladistic sister groups, guaranteed by this status to be equal in age. Mindel et al.84,85 have now performed such a test on the reptilian genus Sceloporus and on allozymic data in general, and have validated punctuated equilibrium's key claim for positive correlation of evolutionary distance and speciation frequency. Lemen and Freeman's86 interesting proposal for additional cladistic tests cannot be sustained because they must assume that unbranched arms of their cladograms truly feature no speciation events along their routes, whereas numerous transient and extinct species must populate most of these pathways. Wagner87 has developed a way of estimating rapidly branching speciation versus gradual speciation or transformation from cladograms, and his initial results favour predominant rapid branching in Palaeozoic gastropods.

Difficulties and prospects
Many semantic and terminological muddles that once impeded resolution of this debate have been clarified. Opponents now accept that punctuated equilibrium was never meant as a saltational theory, and that stasis does not signify rock-hard immobility, but fluctuation of little or no accumulated consequence, and temporal spread within the range of geographic variability among contemporary populations—by Stanley's proper criterion, so strikingly validated in his classic study26. We trust that everyone now grasps the centrality of relative frequency as a key criterion (and will allow, we may hope, that enough evidence has now accumulated to make a case, if not fully prove the point).

Evolutionary biologists have also raised a number of theoretical issues from their domain of microevolution. Some, like the frequency of sibling speciation, seem to us either irrelevant or untroublsome as a bias against, rather than for, our view (as we then underestimate the amount of true speciation from palaeontologically defined morphospecies, and such an under-estimate works against punctuated equilibrium). Others, like the potential lack of correspondence between biospecies and palaeontological morphospecies, might be worrisome, but available studies, done to assess the problem in the light of punctuated equilibrium, affirm the identity of palaeontological taxa with true biospecies (see Jackson and Cheetham88 on bryozoan species, and Michaux27 on palaeontological stasis in gastropod morphospecies that persist as good genetic biospecies).

But continuing unhappiness, justified this time, focuses upon claims that speciation causes significant morphological change, for no validation of such a position has emerged (while the frequency and efficacy of our original supporting notion. Mayr's genetic revolution" in peripheral isolates, has been questioned). Moreover, reasonable arguments for potential change throughout the history of lineages have been advanced6.34, although the empirics of stasis throws the efficacy of such processes into doubt. The pattern of punctuated equilibrium exists (at predominant relative frequency, we would argue) and is robust. Eppur non si muove; but why then? For the association of morphological change with speciation remains as a major pattern in the fossil record.

We believe that the solution to this dilemma may be provided in a brilliant but neglected suggestion of Futuyma89. He holds that morphological change may accumulate anywhere along the geological trajectory of a species. But unless that change be "locked up" by acquisition of reproductive isolation (that is, speciation), it cannot persist or accumulate and must be washed out during the complexity of interdigitation through time among varying populations of a species. Thus, species are not special because their origin permits a unique moment for instigating change, but because they provide the only mechanism for protecting change. Futuyma writes: "In the absence of reproductive

226 NATURE - VOL 366 - 18 NOVEMBER 1993