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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 bottleneck—a 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
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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
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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
there—they 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
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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 birds—or 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
OCR for page 9
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
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Jablonski
Representative terms from entire chapter:
extinction events
