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Colloquium Lessons from the past: Evolutionary impacts of mass extinctions David Jablonski* Department of Geophysical Sciences, University of Chicago, 5734 South Ellis Avenue, Chicago, IL 60637 Mass extinctions have played many evolutionary roles, involving differential survivorship or selectivity of taxa and traits, the dis- ruption or preservation of evolutionary trends and ecosystem organization, and the promotion of taxonomic and morphological diversifications often along unexpected trajectories after the destruction or marginalization of once-dominant clades. The fossil record suggests that survivorship during mass extinctions is not strictly random, but it often fails to coincide with factors promoting survival during times of low extinction intensity. Although of very serious concern, present-day extinctions have not yet achieved the intensities seen in the Big Five mass extinctions of the geologic past, which each removed 50% of the subset of relatively abundant marine invertebrate genera. The best comparisons for predictive purposes therefore will involve factors such as differ- ential extinction intensities among regions, clades, and functional groups, rules governing postextinction biotic interchanges and evolutionary dynamics, and analyses of the factors that cause taxa and evolutionary trends to continue unabated, to suffer setbacks but resume along the same trajectory, to survive only to fall into a marginal role or disappear ("dead clade walking"), or to undergo a burst of diversification. These issues need to be addressed in a spatially explicit framework, because the fossil record suggests regional differences in postextinction diversification dynamics and biotic interchanges. Postextinction diversifications lag far behind the initial taxonomic and morphological impoverishment and ho- mogenization; they do not simply reoccupy vacated adaptive peaks, but explore opportunities as opened and constrained by intrinsic biotic factors and the ecological and evolutionary context of the radiation. To the conservation biologist, there is little positive to be said about extinction. From an evolutionary perspective, how- ever, extinction is a double-edged sword. By definition, extinc- tion terminates lineages and thus removes unique genetic vari- ation and adaptations. But over geological time scales, it can reshape the evolutionary landscape in more creative ways, via the differential survivorship of lineages and the evolutionary op- portunities afforded by the demise of dominant groups and the postextinction sorting of survivors. The interplay between the destructive and generative aspects of extinction, and the very different time scales over which they appear to operate, remains a crucial but poorly understood component of the evolutionary process. The fossil record is rich in extinction events at all intensities and spatial scales, and thus provides the essential raw material for an extremely important research objective: the comparative calibration of evolutionary responses, both positive and negative, to perturbation. Despite limits on direct comparisons to present- day and future events, discussed below, paleontological data afford the opportunity to test the evolutionary impact of such factors as the initial state of the system, the nature, duration, and magnitude of the perturbation, and postextinction physical and biotic conditions. Comparative analysis of the Big Five mass extinctions (1, 2) is just beginning, as is work on the myriad www.pnas.org/cgi/doi/10. 1 073/pnas. 101092598 smaller and sometimes more localized events manifest in the geologic record, and so this paper is as much a research agenda as a review. One approach to the problem is through the related issues of extinction selectivity and evolutionary continuity across mass extinction events in the geologic past. Recent work on the geographic fabric of extinction events and their aftermath sug- gests that the spatial dimension of diversity dynamics also will be an important component of a rigorous theory of extinction and its evolutionary consequences, and so although data are sparse I will raise some of these issues as well. Selectivity and Loss Mass extinctions would be important evolutionary agents even if they simply intensified variations in clade survivorship seen in times of low extinction rates. For example, if mass extinctions primarily removed lineages in decline or in the early stages of diversification, truncating the time span available to those and other clades for the acquisition of evolutionary novelties, then they would significantly reinforce the stability of the status quo. The fossil record shows, however, that the major extinction events of the geologic past have played a larger and more complex role, by removing not just marginal players but also dominant incumbents, owing at least in part to extinction selectivities that are partly independent of those seen under "normal" extinction regimes. For example, factors such as local abundance, species richness, and species-level geographic ranges, all apparently significant during times of low extinction intensities (3), played little role in the survival of marine invertebrate clades during the end-Cretaceous (K-T) mass ex- tinction, where the data are most extensive (2, 4, 5, l), and have been unimportant in at least some of the other mass extinction events as well (2, 6~. At the same time, broad geographic distribution at the clade level, regardless of species-level ranges, significantly enhanced survivorship at all of the major extinction events (2, 4, 7) (note that this discordance across hierarchical levels means that surviving clades need not consist of generalized or opportunistic species, contrary to some oversimplifications of these results). These analyses suggest that clades or adaptations may be lost not because they are poorly adapted to the pre~or post) disturbance settings, but because they lack the broad geographic deployment or other traits that favor survival during the extinction bottlenecka pattern of "nonconstructive selec- tivity" (8) that yields differential survival among clades without promoting the long-term adaptation of the biota (2, 6, 9~. This is not to say that traits favored under low extinction intensities were never advantageous during mass extinctions: resting stages in phytoplankton, occupation of unperturbed This paper was presented at the Nationai Academy of Sciences coiloqulum, "The Future of Evolution," held March 16-20, 2000, at the Arnoid and Mabei Beckman Center in Irvine, CA. Abbreviation: K-T, end-Cretaceous. *E-mail: djablons~midway.uchicago.edu. ~Lockwood, R. (1997) Geo/. Soc. Am. Abstr. Programs 29, A-404. PNAS 1 May 8, 2001 1 vol. 98 1 no. 10 1 5393-5398
5394 1 www.pnas.org/cgi/doi/10.1073/pnas.101092598 regions, clades and functional groups; long-term effects of geographic variation not only in extinction but also in postex- tinction biotic interchanges and evolutionary dynamics; patterns of biotic continuity, lag times, and innovation as reflected in postextinction evolutionary rates and patterns. Also important, of course, are the looming questions of what causes the transition to selectivities seen under paleontological mass-extinction re- gimes, and whether that threshold can be avoided in the near future. Still unknown, for example, is whether that threshold is simply a function of the spatial scale and intensity of the forcing perturbation, of the quality of the perturbation See, for example, the apparently more severe biotic effects of increased seasonality as opposed to simple changes in mean annual temperature (20~] or whether feedbacks involving, for example, the compounding of perturbations (21), or the disruption of biotic interactions or community structures come into play. In principle, threshold effects should be detectable in time series around mass extinction events, and this would be especially valuable in light of the cumulative extinction processes operating today. The demonstrable selectivity of extinctions raises the issue of weakening vs. hardening of the biota if unfavorable conditions are imposed over a protracted interval: as the most vulnerable taxa such as endemic species are lost, under what circumstances will the extinction-resistant residue withstand further stresses, and when will they give way to the mass-extinction regime? A hardening process may underlie the pulse of extinction near the onset of Pleistocene glaciation and the dearth of extinction thereafter (22) (the end-Pleistocene megafaunal extinction is probably a different issue), and we need a better understanding of exactly what separates such events from the major mass extinctions, and to what extent such hardening processes under- mine linear projections of present-day extinction estimates to future losses. We can simply appeal again to the spatial scale, intensity, or quality of the perturbation, or to the quality of the perturbation, but this leads us back to the uncertain nature of the threshold, whether it is graded or a step-function, and its potential variation among taxa, communities, and regions. Spatial Patterns Most paleontological analyses of mass extinctions have neglected the spatial dimension, tending to focus instead either on single stratigraphic sections or regions, or on synoptic global databases. Both scales have been extremely productive, but the global biota is spatially complex, with diversity gradients and hotspots (e.g., refs. 23-26) and concomitant variation in the generation and persistence of evolutionary novelties and higher taxa (27) tal- though the relation to species-level evolutionary dynamics is still unclear (28, 29~. Paleontological analyses that contain a spatial component, for example regarding regional extinction events at all scales (30) or the biogeographic fabric of postextinction evolutionary patterns, therefore would be especially valuable with reference to present-day and future processes. Biotic in- terchanges in the paleontological record, such as the late Ce- nozoic responses to the joining of North and South America after the final uplift of the Panama Isthmus, or the opening of transpolar interchange between Pacific and Atlantic, clearly document asymmetries in biotic interchanges that correspond to regional differences in extinction intensities (31, 32~. These paleontological findings that regions suffering greater losses were more heavily invaded is an important verification and extension into deep time of observations made in modern communities (33~. Geographical analyses of mass extinctions and their after- math. however. show that more complex dynamics may some- times operate. For example, although K-T extinction intensities were statistically homogeneous for marine mollusks on a global scale (except perhaps for shallow, clear-water tropical plat- forms), the evolutionary and biogeographic response was decid- Jabionski
edly inhomogeneous. Of the four regions analyzed as time series (34), only the North American Gulf and Atlantic Coastal Plain showed a prolific but short-lived burst of diversification by several clades ttermed "bloom taxa" (35~] that were quiescent elsewhere and was significantly more subject to postextinction biotic invasions. Although further analyses are desirable, partic- ularly from a phylogenetic standpoint, these patterns are likely to be robust: they hold whether the bloom taxa are treated as a proportion of the biota or as raw species numbers when the K-T bottleneck is taken into account (34~. Furthermore, neither burst nor excess invasion appears in an extensive new analysis of an important fauna in the earliest Tertiary of northern Europe (36), which is the region most likely to conform to North America by reason of proximity and climatic similarity. Understanding these paleontological patterns is particularly pressing in light of the massive biotic interchanges that are currently being directly or indirectly mediated by human activ- ities. Why was North America subject to more intense invasion after the K-T event despite its unexceptional (if severe) extinc- tion intensities? This response implies a nonlinear between extinction and invasion intensities, or perhaps simply a threshold above which the relation breaks down. Another possibility is that when losses approach paleontological mass-extinction levels (that is, 50% of the relatively abundant and widespread genera) or are globally both severe and homogeneous, qualitative as well as quantitative losses determine the probability of the evolu- tionary excursions and invasions seen in North America: the identity of the victims and not just their numbers becomes particularly important. The functional role of taxa lost from each of the regional biotas will be difficult to assess rigorously, but divergent regional responses to homogeneous extinction inten- sities provide a natural experiment sufficiently rich in potential insights to demand further investigation. Lockwood's analyses) showing no relation between abundance and survivorship in this fauna undermines one of the simplest hypotheses: that prefer- ential removal of abundant and thus dominant taxa was masked by a strictly taxonomic approach (although a detailed parallel analysis of other regions is required for a definitive test, of course). The evolutionary effects of biotic homogenization may de- pend in part on how it is achieved. Homogenization via elimi- nation of endemics will leave a residue of already widespread taxa that may be relatively resistant to geographic isolation and rapid diversification, whereas homogenization via range expan- sion may more readily promote the origin and diversification of new endemic taxa. Invaders are not drawn randomly from the source biota, however (34, 37), and this bias could itself channel subsequent evolution into narrower pathways among regions than would otherwise be expected. Spatial effects may be important in finer scales as well. For example, in North America within-habitat molluscan diversity appears to recover within a few million years after the K-T extinction (38), but total regional diversity evidently does not reach preextinction levels until roughly 10 million years after the event (34, 35~. Although this result needs to be verified else- where, and tested more rigorously for sampling artifacts, it suggests that beta diversity, the differentiation of local faunas among habitats and along environmental gradients, takes longer to recover than alpha, i.e., local, diversity. Continuity and Creativity Mass extinctions have never entirely reset the evolutionary clock: even the huge losses at the end of the Permian, which appear to have permanently restructured marine and terrestrial commu- nities, left enough taxa and functional groups standing to seed the recovery process without the origin of new phyla (39~. One key to understanding the past and future evolutionary role of extinctions will involve the factors that permit the persistence of Jablonsky certain biological trends or patterns e.g., net expansion or contraction of clades or directional shifts in morphology" in the face of extensive taxonomic loss and ecological disruption. Besides extinction, at least four evolutionary patterns can be seen in the fossil record. These are: (i) unbroken continuity, (~ii) continuity with setbacks, (,~iii) survival without recovery ("dead clade walking"), and (v) unbridled diversification. Unbroken Continuity. Some large-scale patterns withstood one or more of the Big Five extinctions with little disruption. These include the continued dominance of reefs by rugose and tabulate corals and stromatoporoid sponges across the Ordovician- Silurian boundary (40, 41), the escalation of morphological responses seen in molluscan shells to increased predation inten- sity across the K-T boundary (42), the prolonged Paleozoic decline of trilobites (43), and the onshore-offshore expansions and retreats of a number of post-Paleozoic marine orders (44~. Continuity with Setbacks. Other trends suffer setbacks- presumably owing to the contrast between mass extinction and "normal" selectivities but then resume their long-term trajec- tories. These include rising cheilostome bryozoan dominance relative to cyclostomes (45), the ecological expansion of angio- sperms (46, 47) although this may be more an ecological than an evolutionary setback, and the spread to greater burrowing depths by veneroid bivalves,¢ all at the K-T boundary, the early Paleozoic spread of suspension-feeding bivalves to offshore shelf environments (48), and the overall Paleozoic increase in suture complexity in ammonoids (49~. An important open question amenable to direct testing and simulation is whether such setbacks are generally a simple byproduct of high extinction intensities (if the extremes of the morphospace volume are sparsely occupied, for example, then random extinction could clear those portions), or represent selection against the traits being maximized under low extinction intensities. Dead Clade Walking. Clade survival is no guarantee that preex- tinction trends will persist or be reasserted in the postextinction setting. Each extinction has examples of clades that survived the extinction event only to fall into a marginal role or eventually disappear (dead clade walking). These include bellerophontid snails (7) and prolecanitid ammonoids at the Permo-Triassic boundary (50), the brachiopod order Spiriferoida after the end-Triassic extinction (51), and the planktic foraminiferal Zeauvigerina lineage after the K-T event (524. Such lingering demises need to be tested against stochastic attrition, of course (43~. My preliminary, unpublished analysis suggests that the intervals after mass extinctions tend to be significantly enriched in taxa that failed to cross the next stage boundary, relative to other intervals before the extinction event; in other words more clades that survived a mass extinction tend to dwindle or disappear shortly after the event than would be expected by chance. Also intriguing is the geographic variation in the pro- portion of dead clade walking taxa across the K-T boundary, with values highest not in North America (which makes an interesting statement on the impact of the greater influx of invaders therethey followed extinctions but did not drive them), but in the tropical Indian Ocean. These diverse postextinction trajectories again demonstrate that analysis of the evolutionary role of extinctions must include much more than taxonomic survivorship at the event itself. We need to understand why some clades, and some polyphyletic trends such as escalation of antipredatory defenses, persist uninterrupted across the extinction event, why others stumble but recover their preextinction trajectory, and still others survive tLockwoocl, R. (1998) Geo/. Soc. Am. Abstr. Programs 30, A-286. PNAS | May 8, 2001 | vol. 98 | no. 10 | 5395
but never recover. All of the patterns discussed so far strongly attest that postextinction evolutionary processes involve not simply unbridled radiation (see below), but a sorting of survivors in the postextinction world. At this early stage, many alternative hypotheses are feasible and the relative power of the alternatives may vary among different situations. The most obvious is the taxonomic breadth of the trend: all else being equal, any evolutionary trend that advances along a broad ecological or taxonomic front is less likely to be halted by extinction. Although this is surely a factor, it is unlikely to be sufficient in all cases, because many trends are fairly circumscribed phylogenetically, as in the bryozoan and veneroid examples given above. Given the discordance in selectivity between times of high and low extinction intensities, another factor in the persistence of trends is likely to be the strength of association between traits involved in trends and those related to survivorship. The role of this macroevolutionary linkage in promoting the long-term persistence of trends is virtually unexplored. A final potential explanation is even more context-specific, that the differential persistence of trends depends less on the intrinsic traits of clades than on the strong variation recorded in postextinction recovery (i) among ecosystems, e.g., the more rapid recovery of diversity in oceanic plankton vs. marine benthos (53, 54) (with potentially important implications for the relative persistence of mineral and nutrient cycles); (ii) across ecological scales, e.g., discor- dances in the time to recovery of local vs. global diversity (as mentioned above, with potentially important implications for the accumulation of biological diversity and the development of spatial structure); and (iii) among regions in clade dynamics and biotic interchanges, e.g., the concentration of bloom taxa and postextinction invasions in particular areas (with potentially important implications for the persistence and recovery of local biotas and intrerregional source-sink dynamics). Unbridled Diversification. The most dramatic and creative evolu- tionary role of mass extinctions is the promotion of postextinc- tion diversifications, typified most vividly by the exuberant radiation of the mammals after the demise of the dinosaurs and other reptilian clades at or near the K-T boundary. Postextinc- tion bursts of diversification have been extensively discussed and documented for many extinction events, both morphologically and at several taxonomic levels (6, 39, 41, 55-58~. Therefore, before returning to the need for further analysis of geographic variation in evolutionary dynamics, I will make only two further points, on predictability and time scales. Predictability. Although the evolutionary response to mass ex- tinction has sometimes been depicted simply in terms of the reoccupation of preextinction adaptive peaks ("reinventing the ecological wheel," ref. 59), evolution is both too opportunistic and too constrained by inherited body plans for this to be wholly true. Striking convergences in form and habit are, of course, a major theme in evolution, but postextinction dynamics are complicated by near-simultaneous radiation of multiple clades With the powerful incumbency advantage at stake (32~], the distinct ecological context of each postextinction interval, and the raw material provided by surviving lineages. These effects can be seen in the incomplete congruence of successive occu- pations of morphospace after extinction events (60, 61~. To drive home these important but somewhat abstract points on the long-term prospects for evolutionary replacements, con- sider the Cenozoic history of birds. The large, flightless pho- rusrhacid and diatrymid birds, probably the top carnivores of early Cenozoic terrestrial communities (62, 63), interfered with the triumphant mammalian ascent to center stage in the post- dinosaurian world, and probably were not replaced by an exact mammalian analog once they disappeared. Note also that these carnivorous birds opportunistically converged on theropod di- 5396 1 www.pnas.org/cgi/doi/10. 1 073/pnas. 101092598 nosaurs rather than adhering to the pterosaur models that might have been the most likely targets for convergence given a flying avian starting point (62~. Over the course of Cenozoic diversi- fication, other birds did assume modes of life similar to those vacated by pterosaurs: skimmers may roughly correspond to Tropeognathus with its keeled jaws, swallows and swifts to Pterodactylus with its similar size and wing proportions, flamin- gos to Pterodaustro with its bristling array of fringe-like teeth, and perhaps even condors to the enormous Quetzlcoatlus (64, 65~. This does not mean, however, that birdsor even birds plus bats managed to occupy the full range of pterosaur habits (66~. Equally important, the granivorous habit so important in mod- ern birds evidently represents a novel expansion of bird ecospace relative to their supposed pterosaur models (see ref. 66 on the avian trophic diversification). There may be good functional or ecological reasons for this (e.g., was the Mesozoic seed bank as rich and dependable a resource as in the angiosperm-dominated Cenozoic?), just as there seems to have been for the absence of baleen-like filter-feeding in Mesozoic marine reptiles (67), but such constraints and contingencies are precisely the factors that prevent a given set of clades at a given time from fully overlap- ping the evolutionary pathways of their predecessors. Attempts to predict evolutionary behavior after major extinction events can only operate in broad generalities, and always with the caveat, "expect the unexpected." Time Scales. The fossil record shows that destructive and gener- ative aspects of extinction generally operate in different time frames, as many authors have pointed out (2, 41, 68~. The biotic impoverishment and homogenization necessarily precedes the evolutionary response, and there is surprisingly little hard evi- dence for major evolutionary innovations within a major extinc- tion episode. Even for apparently protracted or multistep ex- tinctions that see origination within the extinction interval, such as the end-Ordovician or end-Permian episodes, "little biolog- ical innovation is apparent" (41~. Recoveries of different biomes, clades, or communities may have different postextinction lag times; for example, broadly defined "reef" systems lag behind oceanic plankton systems (see ref. 2 for discussion). Whether these lags reflect a general property of large-scale diversity dynamics (13, 69), sampling and other biases (6, 70), the duration or intensity of environmental stresses (71), a protracted process of assembling new ecological communities (2, 72), or evolutionary waiting times set by intrinsic diversification rates (73) awaits further comparative analysis. Geography. The spatial dimension is important not only to extinction selectivity and postextinction interchange, but to long-term evolutionary dynamics in a postextinction world. Certain habitats and regions, such as onshore marine settings (44), and the tropics in both marine (27) and terrestrial (74-76) settings, appear to be important sources of postextinction evo- lutionary novelty, but the implications of this nonrandom cre- ativity have only begun to be explored. On finer geographic scales, a systematic search for diversity hotspots in the geologic record to test for their long-term persistence and evolutionary significance would be valuable. For example, is the end- Ordovician extinction of brachiopods and other benthic taxa in North America a potential case study in the destruction and later refurbishment of a diversity hotspot? North America straddled the equator and harbored a rich biota of endemic taxa in the epicontinental sea that occupied the center of the continent. Oscillating climates and fluctuating sea levels virtually elimi- nated this and other interior seaways and their biotas, and the postextinction interval saw an invasion pulse as taxa from outside the region expanded to occupy the returning favorable habitats (77, 78~. Tracking such hotspots and other crucibles of biotic novelty Jab~onski
over evolutionary time might help to prioritize targets for both research and conservation efforts in the near future. Do rela- tively localized hotspots primarily contribute taxonomic richness to the global biotic inventory, or are they also important reservoirs of biodisparity, that is morphological richness? The evolutionary importance of the answer will depend in part on the mean lifetime of such hotspots, and the extent to which novelties that arise in hotspots tend to spread elsewhere, as has been documented for novelties that originated in onshore environ- ments or within tropical latitudes (27, 44, 74-76~. For these and many other questions, paleontology can be a rich source of natural experiments in macroevolutionary dynamics before, during, and after perturbations of widely varying intensities and durations. Conclusion I would not go far wrong in saying that the most dramatic evolutionary effects of mass extinctions can be epitomized in just four words: they remove successful incumbents. But going beyond what amounts to a concession to contingency, what are the lessons of the past that transcend the specific mechanisms, intensities, and participants of earlier events? (i) Mass extinctions happen. The fossil record provides ample evidence that even the more widespread and species-rich Glades, ecosystems, and biogeographic provinces are not infinitely re- silient. Biogeochemical and other data are accumulating on the concomitant breakdown of nutrient cycling and other ecosystem- level processes (53), and the links among the collapse and 1. Sepkoski, J. J., Jr. (1993) Paleobiology 19, 43-51. 2. Jablonski, D. (1995) in Extinction Rates, eds. May, R. M. & Lawton, J. H. (Oxford Univ. Press, Oxford), pp. 25-44. 3. McKinney, M. L. (1997) Annul Rev. Ecol. Syst. 28, 495-516. 4. 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An understanding of the evolutionary role of mass extinctions requires continued analysis of why well- established incumbents are lost, surely at least in part a function of the spatial scale of perturbations, and the long-term conse- quences of such losses. (iii) Extinction itself promotes biotic interchange. Asymme- tries in ancient biotic interchange generally appear to reflect geographic differences in extinction intensity. The K-T extinc- tion shows, however, that although biotic interchanges pervade the postextinction world, simple linear relationships can break down to produce unexpected source-sink patterns. (iv) The evolutionary response to mass extinction is slow on human time scales, difficult to predict owing to the contingencies of postextinction conditions including the identity and evolu- tionary dynamics of the survivors, and geographically heteroge- neous. 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