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Evolutionary Stability PAUL J Proc. Natl. Acad. Sci. USA Vol. 92, pp. 11269-11273, November 1995 Evolution The challenge of paleoecological stasis: Reassessing sources of evolutionary stability PAUL J. MORRIS*t, LINDA C. IVANYt, KENNETH M. SCHOPFi, AND CARLTON E. BRETT§ *Paleontological Research Institution, Ithaca, NY 14850-1398; tDepartment of Earth and Planetary Sciences, Harvard University, Cambridge, MA 02138; and §Department of Geological Sciences, University of Rochester, Rochester, NY 14627 Communicated by Stephen Jay Gould, Harvard University, Cambridge, MA, August 7, 1995 ABSTRACT The paleontological record of the lower and principle of evolutionary stability that results from constraints middle Paleozoic Appalachian foreland basin demonstrates imposed by ecology. an unprecedented level of ecological and morphological sta- bility on geological time scales. Some 70-80%o of fossil mor- "Coordinated Stasis" phospecies within assemblages persist in similar relative abundances in coordinated packages lasting as long as -7 Data from the Hamilton Group of New York State provide million years despite evidence for environmental change and the best documented example of long-term faunal stability biotic disturbances. These intervals of stability are separated in the marine fossil record at the species level (Fig. 1). Within by much shorter periods of ecological and evolutionary the Hamilton Group, Brett and Baird (8, 9) recognize and change. This pattern appears widespread in the fossil record. describe some 20 recurring fossil assemblages, each charac- Existing concepts of the evolutionary process are unable to terized by a consistent, statistically recognizable taxonomic explain this uniquely paleontological observation of fauna- composition. These broadly defined biofacies are stable and wide coordinated stasis. A principle of evolutionary stability statistically recognizable, and many workers have identified the same sets of taxa independently (14-19). When examined that arises from the ecosystem is explored here. We propose on both a spatial and temporal basis, biofacies are seen to be that hierarchical ecosystem theory, when extended to geolog- distributed across depth and turbidity gradients (3, 18, 20), and ical time scales, can explain long-term paleoecological stabil- each shows faunal, taphonomic, and sedimentological evi- ity as the result of ecosystem organization in response to dence for a narrow range of environmental conditions. Within high-frequency disturbance. The accompanying stability of a given biofacies, species persist stratigraphically from bottom fossil morphologies results from "ecological locking," in to top essentially unchanged morphologically, a characteristic which selection is seen as a high-rate response of populations noted as long ago as 1842 (14, 21) and verified more recently for that is hierarchically constrained by lower-rate ecological several species with morphological analyses (22, 23). Some 80% processes. When disturbance exceeds the capacity of the of the species found at the bottom of the unit are still present in system, ecological crashes remove these higher-level con- similar rank order at the top of the Hamilton Group, some 6 straints, and evolution is free to proceed at high rates of million years later (8, 9). However, very few (9-10% of 335 directional selection during the organization of a new stable Hamilton species; refs. 8 and 9) occur in units below or above ecological hierarchy. (Fig. 1). More extensive documentation of coordinated stasis in the Hamilton Group can be found in Brett and Baird (9). Paleontologists have long recognized that the fossil record seems to consist of packages of ecological and evolutionary stability Evidence for Disturbance bounded by episodes ofrelatively rapid change (e.g., refs. 1-5; see particularly refs. 6 and 7). Data recently presented from the Faunal stability in the Hamilton Group persisted in the face of Silurian and Devonian Periods of the Appalachian Basin, in both physical (abiotic) and biotic disturbances. Physical dis- particular the Middle Devonian Hamilton Group (8, 9), provide turbances are evident in the Hamilton Group on many time the first rigorous documentation of long-term faunal stability at scales, ranging from individual storm beds to episodes of the species level and show that it is possible to identify packages basin-wide mass mortality to widespread, lithologically distinct of rock, bounded in space and time, that contain coherent species horizons indicating changes in oxygenation or supply of clastic assemblages that persist for millions ofyears in the face ofphysical material on a time scale of 102 to 104 years. "Faunal tracking" and biotic These and (3) reflects biogeographic change associated with migration of disruptions. assemblages change rapidly various depth-parallel environments up to 200 km perpendic- synchronously to a new stable composition over comparatively ular to shoreline in response to relative sea-level fluctuations. shorter periods of time. Brett and Baird (8, 9) have called this Widespread biotic disturbances include ecological and incur- pattem oflinked stability and linked change "coordinated stasis." sion epiboles, stratigraphic horizons characterized by the Existing explanations for widespread evolutionary stasis have proliferation and transient dominance of (respectively) rare tended to invoke either developmental constraints that limit taxa or taxa not otherwise present in the basin (Fig. 1). The change within individual lineages (10) or stabilizing selection reverse pattern, "outages" of otherwise characteristic mem- derived from the absence of environmental change (physical or bers of the fauna, is also observed (see closed and open circles biotic) that could induce speciation in multiple lineages (refs. 2 in Fig. 1). Epiboles and outages both occur within stratigraphic and 7; other explanations have been proposed for stasis in intervals on the order of decimeters and thus represent short particular cases-e.g., see refs. 11 and 12). A fossil record but ecologically significant periods of time (8, 9). After these characterized by coordinated ecological and evolutionary stabil- events, the original assemblage returns unaffected. ity, despite evidence for repeated disturbance, is incompatible Evidence for disturbances of different types on such a wide with these explanations. This pattern implies the need for a range of scales suggests that frequent opportunities for spe- The publication costs of this article were defrayed in part by page charge tTo whom reprint requests should be addressed at the present address: payment. This article must therefore be hereby marked "advertisement" in Organismic and Evolutionary Biology Program, Morrill Science accordance with 18 U.S.C. §1734 solely to indicate this fact. Center, University of Massachusetts, Amherst, MA 01003. 11269 Downloaded by guest on September 29, 2021 11270 Evolution: Morris et al.11270 Evolution: Morris et al. ~~~~~Proc. Nati. Acad. Sci. USA 92 (1995) FSU-SEA LEVEL BA 4-5 BA 3-4. cN uN~rrs BENT'HIC ASSEM. DYSAEROBICFULAEOI/VRS 5 ASSEMBLAGE ASSEMBLAGE- 375 I Ma z hxi .. ........... .cu. ....v. .. F U.VI.... .. ......6..... ... ......B i ..jjjjj iiiiiiiiiiiiiii 0~ ~ ~~~~~~~~. ......p..:.i..... ..I... ....... .... UM... ...... EIXO T-i...-B -~~~~~.. .1 ...L m .... ...0.. ..... !..D 39 FO SSILTA.............XA.-...................G .. .... .. ... ... ...... J Ma W~~~~~~~~~ W.. .. .. .. .. ..... ... ... .... ... .. .. .. ... S - - -~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~C FIG. 1. Stratigraphic ranges of Middle to earliest Late Devonian fossil species of two broadly defined biofacies in the Hamilton Group of west-central New York (Cayuga to Owasco Lake outcrops). Symbols for range lines: thick line, species common to dominant; thin line, species present; arcuate curves to left/right, species migrated temporarily downslope (south)/upslope (north) from study area tracking favored environment; *, incursion epibole; 0, outage (see text). These data encompass a small subset of available Hamilton Group taxonomic ranges and are presented from a limited geographic perspective so as to illustrate faunal tracking. Note that most Hamilton-Tully species are first recorded at the base of subunit X, track their preferred environment in unison, maintain similar relative abundances throughout, and disappear in concert at the top of the interval. EE subunits are ecological-evolutionary "faunas" defined by Brett and Baird (8, 9); IX, Onondaga fauna; IXA, modified Onondaga assemblage plus unique elements of the Stony Hollow fauna; X, Hamilton-Tully fauna; XI, Genesee fauna. Adjoining portions of subunits IX and XI are included only for comparison. Relative sea-level curve is calibrated by fossil benthic assemblages (BA) as defined by Boucot (13); note that only the deeper end of this scale is shown; BA 3.5, diverse coral-rich offshore communities; BA 4, diverse brachiopod communities; BA 4.5, ambocoeliid communities; and BA 5, high-dominance leiorhynchid communities typical of dark-gray to black shale. Fossil species are subdivided roughly by biofacies into two groups: (i) those that characterize deeper water, dysaerobic areas typified by small ambocoeliid, chonetid, and leiorhynchid brachiopods (BA 4-5); (ii) those that typify diverse brachiopod biofacies of shallower, oxic, calcareous gray mudstones or argillaceous limestones (BA 3-4). Abbreviations for biostratigraphic zones, major shallowing pulses, and species are as in ref. 71. ciation occurred throughout the duration
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