Gould & Eldredge, Punctuated equilibrium comes of age


theorists, while not accepting our preference for viewing stasis in the context or habitat tracking 17 or developmental constraint 33,34, have been persuaded by punctuated equilibrium that maintenance of stability within species must be considered as a major evolutionary problem.

Macroevolution as a problem in species sorting. If punctuated equilibrium has provoked a shift in paradigms for macroevolutionary theory (see ref. 35 for a defence of this view), the main insight for revision holds that all substantial evolutionary change must be reconceived as higher-level sorting based on differential success of certain kinds of stable species, rather than as progressive transformation within lineages (see Eldredge 36 on taxic versus transformational views of evolution; Simpson 37, however, in the canonical paleontological statement of the generation before punctuated equilibrium, had attributed 90% of macroevolution to the transformational mode, and only 10%. to speciation). Figure 1, our original diagram of punctuated equilibrium, shows how a trend may be produced by differential success of certain species without directional change in any species following its origin.

Darwin's theory of natural selection locates the causality of evolutionary change at one domain on one level: natural selection operating by struggle among individual organisms for reproductive success. Given Darwin's crucial reliance upon lyellian uniformity for extrapolating this mode of change to encompass all magnitudes through all times, the interposition of a level for sorting among stable species breaks this causal reduction and truly, in Stanley's felicitous term 38, "decouples" macro- from microevolution. Decoupling is not a claim for the falseness or irrelevancy of microevolutionary mechanisms, especially natural selection, but a recognition that Darwinian extrapolation cannot fully explain large-scale change in the history of life.

The main point may be summarized as follows. Most macro-evolution must be rendered by asking what kinds of species within a clade did better than others (speciated more frequently, survived longer), or what biases in direction of speciation prevailed among species within a clade. Such questions enjoin a very different programme of research from the traditional how did natural selection within a lineage build substantial adaptation during long stretches of time?' The new questions require a direct study of species and their differential success, older queries focused downward upon processes within populations and their extrapolation through time. Darwin's location of causality in organisms must be superseded by a hierarchical model of selection, with simultaneous and important action at genie, organismal and taxic levels 39,40. Williams 34, who so stoutly defended classical Darwinism against older, invalid, and very different forms of group selection 41, now acknowledges the importance of such clade selection in macroevolution. Punctuated equilibrium has been used as a central concept in the development of hierarchy theory in evolutionary biology.

Implications. Any theory with a claim to novelty in broad perspective must enlighten old problems and suggest extensions. The speciational view of macroevolution, which does not strictly require punctuated equilibrium, but which was nurtured and has thrived in its context, requires a reformulation of nearly all macroevolutionary questions. For example, so-called living fossils, once treated as lineages rendered static by optimal adaptation, unusually Stable environment, or lack of genetic variation, should be reconceptualized as members of groups with unusually low speciation rates, and therefore little opportunity to accumulate change 42, (We have no evidence that the species of 'living fossil' groups are particularly old. For example, the western Atlantic horseshoe crab, Limulus polyphemus--the 'type example' of the phenomenon--has no fossil record at all, whereas the genus can only be traced to the Miocene.)

Going further, the entire tradition of expressing evolutionary change in darwin units (where 1 darwin equals character change by a factor of e in 1 million years) 43 makes no sense in a speciational context. (If a lineage goes from species A to D in 10 million years through three episodes of rapid change with intervening stasis, a cited rate of so many millidarwins becomes a meaningless average,) We learn as a received truth of evolution, for example, that human brain size increased at an extra-ordinary (many say unprecedented) rate during later stages of our lineage. But this entrenched belief may be a chimaera born of an error in averaging rates over both punctuations and subsequent periods of stasis. Homo sapiens is a young species, perhaps no more than 200,000 years old. If most of our increment accrued quickly at our origin, but we then express this entirety from our origin to the present time as a darwin rate, we calculate a high value because our subsequent time of stasis has been so short. But if the same speciation event, with the same increment in the same time, had occurred two million years ago (with subsequent stasis), the darwin rate for the identical event would be much lower.

Cope's rule, the tendency for phyletic increase in body size, had generally been attributed to selective value of large size within anagenetic lineages, but is probably better interpreted 44,45 as greater propensity for speciation in smaller species, for whom increasing size is the only 'open' pathway (see Martin 46 on the negative correlation of generic species richness and body size). Raup and Sepkoski 47 proposed a conventional explanation for decreasing rate of background extinction through geological time: generally better adaptation of later species. But Valentine 48 and Gilinsky (personal communication) offer an interesting speciational alternative: if extinction intensities were constant through time, groups with equally high speciation and extinction

FIG. 1 Three-dimensional sketch contrasting a pattern of relative stability (A) with a trend (B), where speciation (dashed lines) is occurring in both major lineages. Morphological change is depicted here along the horizontal axes, while the vertical axis is time. Though a retrospective pattern of directional selection might be fitted as a straight line in (B), the actual pattern is stasis within species, and differential success of species exhibiting morphological change in a particular direction. For further explanation, see ref. 1.

224 NATURE - VOL 366 - 18 NOVEMBER 1993