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13
The interplay of physical and
biotic factors in macroevolution
David Jablonski
ABSTRACT
Large-scale evolutionary patterns are shaped by the interplay of physical and biotic processes. We
have a new appreciation of the role of physical constraints and perturbations in evolution, and the
challenge is to evaluate the roles of physical, intrinsic biotic and extrinsic biotic factors in specific
situations. Intrinsic biotic factors such as dispersal ability and environmental tolerance, or at the
species or lineage levels geographic range or species richness, clearly influence the origination and
extinction rates that underlie the dynamics of evolution above the species level (macroevolution). Such
biotic factors determine the differential response of taxa to a physical perturbation, but can be overwhelmed if the perturbation is sufficiently severe or extensive (which helps to explain why mass
extinction events can play an important evolutionary role while accounting for only a small fraction
of the total extinction in the history of life).
Extrinsic biotic factors such as predation and competition are more difficult to quantify paleontologically, but some long-term changes in the morphology and composition of the biota appear to be
driven by such interactions, perhaps mediated locally by physical perturbations. Pervasive incumbency effects at all scales, where established taxa exclude potential rivals, demonstrate both the
importance of extrinsic biotic factors and the role of physical factors in opening opportunities for
new or marginalized taxa to diversify: the long Mesozoic history of the mammals and their exuberant
diversification after the demise of the dinosaurs is only the most famous example, and similar
dynamics may occur on local and regional scales as well.
Physical, intrinsic biotic and extrinsic factors have each been afforded a role in many of the largescale patterns of the fossil record, including: (i) the Cambrian explosion of complex metazoan life, (ii)
the ‘reef gap’, in which the reassembly of diverse benthic communities in clear, shallow tropical waters
lags 5–10 million years behind major extinction events, and (iii) the biogeographic pattern of recoveries
from mass extinctions, in which regional biotas do not exhibit simultaneous or coordinated re-diversifications following global extinction events.
13.1 Introduction
The study of macroevolution, here defined
simply as evolution above the species level,
has seen a growing appreciation of the role of
physical factors in shaping large-scale evolutionary patterns. Many of the major biotic turnovers, extinctions, and radiations that had once
been attributed to direct competitive replace-
ments or adaptive breakthroughs are now
seen as physically mediated. Asteroid impacts,
abrupt changes in ocean circulation and atmospheric chemistry, and a host of other physical
perturbations and secular trends have been
emerging as plausible hypotheses for major
biotic patterns in the history of life.
Now that the range of potential hypotheses
has expanded more fully into the physical
Evolution Planet Earth
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Evolution on Planet Earth
realm, the next challenge lies in critically evaluating the relative roles of biotic and physical
factors, and their interaction, in a given
macroevolutionary situation. (This challenge
has arisen repeatedly in evolutionary paleontology, see discussions in Gould, 1977; Allmon
and Ross, 1990; Skelton, 1991; Van Valen,
1994.) In this chapter, I review some of the
paleontological evidence for the effects of
both intrinsic and extrinsic biotic factors, and
discuss how the interplay and feedbacks
among these biotic and physical factors
shape large-scale evolutionary patterns. At
the very least, biotic factors can determine
the contrasting responses of different taxa to
the same physical factor, or the contrasting
responses of the same taxon to different physical factors. I conclude by discussing some
major evolutionary events where the relative
roles of the different factors are controversial,
with at least some evidence not only for physical drivers but for either (or both) intrinsic
and extrinsic biotic factors. I cannot provide
final answers for these problems, but I can
lay out some alternatives that underscore the
need for interdisciplinary approaches, and
comment on some strengths and weaknesses
of alternatives.
This chapter will necessarily address both
origination and extinction: these are the fundamental terms of the macroevolutionary
equation. Large-scale evolutionary patterns
are molded by differential birth and death –
and their higher-level analogs origination and
extinction – and so extinction data are as
necessary for macroevolutionary analysis as
are data on individual survivorship for a
microevolutionary analysis. As discussed
below, sometimes extinction directly shapes
the direction and fate of a particular lineage,
whereas at other times the extinction of cooccurring taxa plays the overriding role.
Theoretically, trends at any level might be driven entirely by differential birth/origination,
but this is a hypothesis to be tested and not
a starting assumption. In any event, the relation between extinction and origination needs
to be explored when attempting to understand
the interplay of the physical and biotic environment in driving evolution.
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13.2 Intrinsic and extrinsic biotic factors
and their interaction with abiotic
factors
As mentioned above, biotic factors can be partitioned into intrinsic and extrinsic categories.
Physical factors can also be divided this way,
and intrinsic physical factors are certainly
important in evolution, for example as biomechanics affect embryonic development (e.g.
Gilbert, 1997; Wolpert et al., 1998) and organismal function (e.g. Schmidt-Kittler and Vogel,
1991; Rayner and Wootton, 1991; Alexander,
1998; and references therein), but here I will
focus on the physical factors external to the
organism. Extrinsic physical factors can also
be subdivided, of course, for example according to rate or spatial scale. These can range
from the slow drifting of continents as driven
by seafloor spreading (which averages about
5 cm a year, approximately the pace of fingernail growth), to the sudden violence of an
asteroid impact; they can be as localized as
the shift of a riverbed or the suppression of
an oceanic upwelling cell, or as pervasive as a
change in the CO2 content of the atmosphere.
For this discussion, intrinsic biotic factors
are aspects of an organism, or of a unit at any
other focal level within the biological hierarchy, that affect its probability of becoming
extinct or producing descendants. (Besides
these aspects of evolutionary tempo, intrinsic
factors can also affect evolutionary mode, for
example branching vs phyletic evolution, e.g.
Jablonski, 1986a.) Extrinsic biotic factors
involve the impact of one biological entity
upon another, for example via competition or
predation. Because life is organized hierarchically, intrinsic and extrinsic status can shift
according to focal level; the other members of
a breeding population are extrinsic factors for
an individual organism, but together may help
to determine the intrinsic response of a species
to climate change.
13.2.1
Intrinsic biotic factors
A huge array of intrinsic biotic factors have
been implicated in differential extinction and
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speciation probabilities (e.g. Jablonski 1986b,
1995; Pimm et al., 1988; McKinney 1997).
Traits that clearly reside at the organismal
level include body size, mobility, metabolic
rate, physiological tolerance limits, and feeding
type (e.g. herbivore, carnivore, parasite). The
variation of these factors even among closely
related species helps explain why higher taxa
such as families, orders and classes are generally poor analytical units for studying evolutionary rate differences, even for groups
noted for their high average rates. For example,
genus-level origination and extinction rates can
vary by an order of magnitude among ammonite superfamilies, and by a factor of four
among trilobite orders (Gilinsky, 1994).
Dispersal ability is an interesting intrinsic
factor because it often plays a role in determining rates and patterns of gene flow, and geographic ranges, which are aspects of species
that are not simply aggregate characteristics
of individual bodies. These intrinsic biotic features at the species level can in turn affect speciation and extinction probabilities, just as
species richness is a clade-level trait that can
influence extinction (and perhaps origination)
probabilities (e.g. Jablonski, 1986a, 1987, 1995,
2000; Williams 1992; Grantham, 1995). Views
differ on how larval dispersal operates within
a hierarchical framework. This is unimportant
for the present discussion, so I will simply note
that marine species achieve broad geographic
ranges and high rates of gene flow by several
mechanisms besides larval dispersal (e.g. rafting of bryozoans, Watts et al, 1998); those species-level properties, however achieved, are
subject to higher-level selection processes,
which can oppose or reinforce processes operating on individual-level traits.
Hierarchy arguments aside, fossil larval
shells can be used to infer modes of development and are good predictors of evolutionary
rates in marine gastropods, where the data are
most plentiful. Although there are of course
exceptions, species with high-dispersal, planktotrophic larvae tend to be widespread and
geologically long-lived, and to speciate infrequently, whereas those with low-dispersal,
non-planktotrophic larvae tend to be more narrowly distributed and more extinction-prone,
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and to have higher speciation rates, as tested
in Cretaceous, Paleogene, and Neogene settings (Scheltema, 1977, 1989; Hansen, 1978,
1980; Jablonski, 1986a, 1995; Gili and
Martinell, 1994). For each of these analyses,
the species are drawn from a single regional
pool, within a single biogeographic province
at continental shelf depths within a discrete
time frame. Therefore the paleontological data
show, at least in part, how taxa with different
intrinsic biotic features respond to the same
environmental parameters at a particular time.
This differential response, along with a number of others, evidently did not operate during
the end-Cretaceous extinction (Jablonski, 1986a,
b; Valentine and Jablonski, 1986), although as
noted above, it returned in the early Cenozoic.
Smith and Jeffery (1998) also found no significant difference in survivorship of echinoids
across the Cretaceous–Tertiary boundary
according to larval type, although with a pvalue of 0.11 they considered this a ‘weak correlation’. McGhee (1996: 129) argued for a similar lack of selectivity according to
developmental type in the late Devonian mass
extinction, although this requires inference of
brachiopod developmental types from present-day relatives, which may not be reliable
(see Valentine and Jablonski, 1983).
Kammer et al. (1998) found in Paleozoic crinoids that habitat generalists had significantly
greater species longevities than habitat specialists, at least during times of ‘normal’ extinction
intensities. This is by far the most rigorous test
of this intuitively appealing relationship (for
earlier observations on mollusks, see
Jablonski, 1980; Erwin, 1989; Stanley, 1990;
and references therein), and as with molluscan
larval modes we are seeing the differential
response of taxa within a single region to the
challenges of temporal and spatial environmental variation. However, this intrinsic biotic attribute did not confer extinction-resistance upon
molluscan genera during the end-Cretaceous
extinction (Jablonski and Raup, 1995).
Kammer et al. (1998) note that greater species longevity does not necessarily scale up to
greater clade longevity: for their crinoids the
specialist clades attained higher species
richness and became dominant in the late
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Paleozoic. Although species-rich clades often
tend to be extinction-resistant (an intrinsic biotic feature at the clade level), this effect is not
seen for molluscan or echinoid genera at the
end-Cretaceous mass extinction (Jablonski,
1986b; Smith and Jeffery, 1998). The benefit of
species richness is lost for a number of major
clades across mass-extinction boundaries, from
end-Ordovician bryozoans to end-Permian brachiopods (Table 2.2 of Jablonski, 1995; Erwin’s
(1989) gastropods appear to be an exception).
These analyses exemplify two general
points: first, that co-occuring taxa can differ
in extinction and origination rates in ways
that can be related to intrinsic biotic factors,
and second, that such differences can be overwhelmed by physical factors when perturbations become sufficiently severe or extensive
(see also Jablonski, 1995, 1996; McKinney,
1997; Smith and Jeffrey, 1998). This does not
mean that all intrinsic factors are ineffective
during mass extinction events, however. For
example, the presence of a resting cyst in certain phytoplankton life cycles may have promoted diatom and dinoflagellate survival
across the K–T boundary (Kitchell et al., 1986;
Brinkhuis et al., 1998); this is a nice example of
an individual feature molded by natural selection under ‘normal’ extinction that is also effective under the mass extinction regime.
At least one clade-level feature generally
appears to enhance survivorship during
mass extinction: geographic range. In endCretaceous bivalves, for example, clades (in
this case genera) restricted to only one or
two biogeographic provinces suffered about
65% extinction, whereas the few clades spread
over six or seven provinces showed about
35–45% extinction (Figure 13.1). This largescale biogeographic effect can be seen for
many groups at many extinctions, from endOrdovician brachiopods, trilobites, bivalves
and bryozoans to Permian gastropods to
end-Triassic bivalves (Table 2.3 of Jablonski,
1995); Smith and Jeffrey’s (1998) analysis of
K–T echinoids is one of the very few studies
that have failed to detect such an effect.
McGhee (1996) finds no overall geographic
effect in the late Devonian mass extinction,
although clades with broad latitudinal ranges
survive preferentially to those with broad
longitudinal ranges, a pattern perhaps related
to tropical perturbations and needing fuller
quantitative analysis. Overall, intrinsic biotic
factors of different kinds, and at different
levels, help to determine survivorship at all
spatial scales, from within-province processes
to global patterns during the five major mass
extinctions that punctuated the Phanerozoic
history of life.
Figure 13.1 Broad geographic range – measured here in terms of biogeographic provinces – significantly
enhanced survival of bivalve genera during the end-Cretaceous mass extinction (Kendall’s rank test,
p < 0.05). The plot shows the structure of the data but is inappropriate for regression analysis because
error terms increase with the number of provinces (more genera are restricted than widespread); from
Jablonski and Raup (1995).
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13.2.2 Extrinsic biotic factors
Extrinsic biotic factors are more difficult to
quantify in the fossil record, because they
involve biotic interactions like predation, competition, and even more elusive indirect effects.
We can find fossil evidence for momentary,
individual interactions, such as drillholes or
bitemarks on shells, insect damage on leaves,
or overgrowths among competing colonies of
corals or bryozoans, but the question is how to
scale up such short-term, small-scale encounters to the macroevolutionary arena?
In a series of important contributions,
Vermeij (1977, 1987, 1994) argued that evolutionary changes in the effectiveness of shellpenetrating predators drove a change in the
structure of marine communities, and in the
range of morphologies present in bivalves, gastropods and other marine prey. The biotic interactions engendered by this ‘Mesozoic Marine
Revolution’ are evident, for example, in an
increase in the proportion of taxa bearing
defensive adaptations such as narrow and reinforced apertures. Some smooth, small, openaperture forms have persisted (although species with open coiling, in which successive
shell whorls are not in contact, have almost vanished), but few observers would confuse an
assemblage of shallow-water Carboniferous
shells (age c. 300 Ma) with one from equivalent,
more ‘escalated’ habitats of Eocene age (age c.
50 Ma).
The kinds of morphological changes seen
during the Mesozoic Marine Revolution, and
their timing relative to the diversification of
predators, from bony fish to crabs to carnivorous snails, build a powerful case for an escalation process driven by extrinsic biotic factors.
The interactions may have been quite diffuse –
large, heterogeneous sets of species impinging
on other large, heterogeneous sets of species,
rather than the tight, reciprocal predator/prey
interactions usually studied by ecologists – but
their net effect is quite apparent. Although
more work would be welcome, a variety of
experimental data corroborate the view that
molluscan shells of modern aspect are more
resistant to predation than certain shell types
more commonly found in Paleozoic assem-
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blages (e.g. Palmer, 1979; Vermeij, 1982;
Harper, 1991; Harper and Skelton, 1993;
Miller and LaBarbera, 1995). Still open for testing is exactly how these extrinsic factors interacted with intrinsic ones. The waxing and
waning of individual clades, partly a function
of intrinsic factors such as those discussed
above, might have helped to determine how
many species of, say, muricine gastropods,
and thus how many species with those extravagant spines, were present at any one time
and place.
Not all hypothesized evolutionary responses
to predators have been verified, and sometimes
further testing may implicate physical factors
instead. In Cenozoic terrestrial faunas, for
example, Janis and Wilhelm (1993) found that
fast-running long-legged ungulates evolved at
least 20 million years before the pursuit carnivores that were supposed to drive a coevolutionary process of escalation (e.g. Bakker,
1983). Instead, high-mobility herbivores more
likely evolved in response to climatic changes
that led to increasingly open grassland habitats.
Even for the Mesozoic Marine Revolution,
where the basic faunal changes do appear to
be driven by extrinsic biotic factors, physical
factors may also have played an important
role. First, there is the question of the initiation
and expansion of the escalation process. A
strictly biotic mechanism might rest entirely
on a coevolutionary arms race launched by
one or a few shell-penetrating innovations
among early Mesozoic predators. An alternative (which of course need not be completely
exclusive of the first) is that pulses or long-term
trends in nutrient input might have promoted
these intensified biotic interactions by fueling
more active predators and prey, and perhaps a
larger (or more rapidly turning over) prey
resource base (e.g. Vermeij, 1995, and this
volume, Chapter 12; Bambach, 1993, 1999).
Testing these alternatives, or perhaps attempting to quantify their relative contributions, will
require multidisciplinary approaches in which
independent proxies for nutrient levels are
tested against realistic models of biotically driven escalation, in an explicit geographic and
temporal framework.
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Physical factors might have played a role at
the local and regional scale as well. As Miller
(1998) notes, few instances of gradual escalation have been documented in a single basin
or biogeographic region (Kelley’s work (1989,
1991) is an exception, but her studies were in
the Miocene, well after the major faunal
changes of the Mesozoic and early Cenozoic).
Instead, species are largely morphologically
static, so that escalation appears to proceed
mainly by episodic, local or regional replacements. The argument is largely inferential,
based on what we don’t see, but Roy (1996)
provides a concrete example in the geographic
variation in the timing and pattern of the replacement of aporrhaid gastropods by their arguably more escalated relatives, the strombids.
Their contrasting regional patterns suggest
that environmental changes in factors such as
climate or productivity can mediate the regional expression of a biotically driven, essentially
global macroevolutionary change (Roy, 1996).
Thus, even the large-scale biotic changes of the
Mesozoic Revolution may require local perturbations to open opportunities for the establishment of more derived taxa. The derived taxa
may be better equipped to cope with more
escalated predators, but at the local scale
incumbents must be removed or reduced
before the more effective taxa can become
established in a given region. The fossil record
is rich in such incumbency effects.
13.2.3 Incumbency
Incumbency effects beautifully exemplify the
interplay between biotic and physical factors.
On the one hand, it is often physical perturbations that break incumbencies, removing dominant forms and opening opportunities for
previously minor groups. The spectacular
diversification of mammals after the extinction
of the dinosaurs is just the most familiar example. The establishment of dinosaurs in the early
Mesozoic, and of advanced mammalian carnivores in the mid-Cenozoic also represent biotic
replacements and diversifications once thought
to be competitively driven but that now appear
to have been mediated by extinction of incumbents (see Benton, 1987, 1996; Jablonski 1986b;
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Rosenzweig and McCord, 1991; Jablonski and
Sepkoski, 1996; McKinney, 1998; Van
Valkenburgh, 1999; Sereno, 1999). This is one
reason for the evolutionary importance of mass
extinctions (cf. MacLeod, this volume, Chapter
14): they account for just a small fraction of the
total species extinction over the past 600 Ma
(e.g. Raup, 1991), but by removing incumbents
– perhaps owing to changes in the effectiveness
of intrinsic biotic factors, as discussed above –
they open up evolutionary opportunities for
other groups that had been minor players.
On the other hand, the limited ecological
role and morphological diversity of mammals
for the first two thirds of their history, and
more generally the very importance of incumbency-breaking events, attest to the importance
of extrinsic biotic factors, such as competition,
in damping or channeling evolutionary
change. Even groups that appear to have
enjoyed unimpeded diversification, and thus
might seem to have been free of extrinsic biotic
effects, show a different story on close examination. For example, marine bivalves (Figure
13.2) diversify exponentially throughout most
of their history, suggesting a process driven
mostly by intrinsic biotic factors, interrupted
by a few sudden downdrops that show the
intrusion of physical factors, mass extinction
events, into the system. But what about the
dynamics immediately after the mass extinctions? The rate of recovery is significantly
greater – for a short time – than the general
pace of bivalve diversification, and Miller and
Sepkoski (1988) argue that these ‘hyperexponential’ episodes represent the true rate of
unimpeded diversification for the clade. The
general exponential rate must be a damped
one, presumably by biotic interactions so diffuse and pervasive that we can only study their
effects via perturbations to the system. Such a
pattern might also be generated as an artifact of
taxonomy, sampling or preservation around
extinction boundaries, but the true termination
of many bivalve taxa at or around major extinction horizons (e.g. MacLeod et al., 1997: 278),
along with a vacating and rapid refilling of a
morphospace defined quantitatively without
reference to individual taxa (Lockwood, 1998),
suggest that the pattern is real in the bivalves
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223
Figure 13.2 Diversity of bivalve genera from the Ordovician to the Recent. Both (a) arithmetic and (a)
logarithmic plots illustrate the approximately exponential nature of bivalve diversification after their initial
Ordovician radiation. However, recoveries from end-Permian and end-Cretaceous mass extinctions occur at
substantially greater rates than the group’s basic exponential rate, suggesting that the basic rate is damped
by biotic interactions that are reduced during the post-extinction rebounds. Vertical tick marks represent the
Big Five mass extinction events. After Sepkoski and Miller (1988).
(see also Patzkowsky’s 1995 reanalysis). Most
intriguing is that the interactions are not
imposing a ceiling on a clade’s diversity, but
instead are evidently slowing the pace of
ongoing diversification in a successful clade.
Sepkoski (1996) modeled these more complex
dynamics in some detail, providing a more realistic set of expectations at this scale.
13.3 Some large-scale patterns
The preceding sections discuss how intrinsic
biotic factors can affect rates and patterns of
extinction and origination; how extrinsic biotic
factors can both promote and inhibit evolutionary change; and how physical factors can play
a pivotal role in when and how the biotic factors operate. For a number of the most important episodes in the history of life, however, the
relative contributions of these factors remain
controversial. Although I cannot resolve these
controversies, it may be useful to discuss them
in terms of competing and complementary
hypotheses on causal mechanisms.
13.3.1 The Cambrian explosion
Regardless of exactly when the major metazoan
lineages actually diverged, the Cambrian
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explosion represents a uniquely rich and temporally discrete episode of morphological evolution (for recent reviews see Conway Morris,
1998a; Valentine et al., 1999; Knoll and Carroll,
1999). Almost all of the skeletonized metazoan
phyla appear within an interval of perhaps
10 My, and the accompanying diversification
of microplankton, of forms having agglutinated skeletons (i.e. pieced-together sand
grains or skeletal debris), and of behavioral
traces all suggest that this is a real evolutionary
event and not simply a change in the preservation potential of an already diverse biota.
Decisive tests have been elusive for the
many hypotheses put forward for the onset
and, equally important, the termination, of
the Cambrian explosion. A physical trigger is
often invoked. For example, Kirschvink et al.
(1997) used paleomagnetic data to argue for a
10–15 My episode of rapid plate-tectonic reorganization of early Cambrian continents and
suggested that these geographic changes,
including attendant shifts in climate and
ocean circulation, would have greatly accelerated biological evolution; as the geographic
changes slowed, so would evolution.
Hoffman et al. (1998) revived an old idea relating metazoan diversification to Proterozoic glacial ages, this time presenting evidence for a
‘snowball Earth’ (that is, a truly global glacia-
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tion), and, in a breathtaking extrapolation from
Hawaiian Drosophila populations, suggested
that this would bottleneck metazoan lineages
and yield an episode of explosive evolution
once conditions relaxed.
The principal candidate for a physical trigger is the crossing of a threshold in atmospheric oxygen, usually set at 10% present
atmospheric level (PAL) by analogy to the
drop in metazoan diversity when oxygen tension falls below this level in modern seas.
However, as discussed by Lenton (this volume,
Chapter 3), some evidence suggests that the
threshold was crossed too early for oxygen to
have been the primary trigger for the explosion
itself. Canfield and Teske (1996), for example,
estimate 10% PAL at 650 Ma, nearly 100 My too
early (see also Knoll, 1996; and Rye and
Holland, 1998, who suggest that 10% PAL
was reached by 2 billion years ago). Oxygen
availability may have been a critical prerequisite for the evolution of large, complex metazoans (Lenton, this volume, Chapter 3; but see
Conway Morris, 1998a: 898), but it may not
have been the proximate trigger.
In theory, the major biotic hypotheses contrast starkly. Hypotheses based on intrinsic
biotic factors, which might be termed the
‘loose genes’ or genomic hypotheses, postulate
the crossing of a threshold in the complexity of
developmental systems that allowed organisms to generate more elaborate forms, and in
an especially prolific fashion, because those
developmental systems were relatively unconstrained (see Valentine and Erwin, 1987; Erwin,
1994, 1999; Arthur 1997). The later damping of
the explosion, then, would have occurred as
genomes became increasingly burdened by
interdependencies among genes and signaling
pathways.
The extrinsic biotic hypotheses, which might
be called the ‘loose niches’ or ecological
hypotheses, postulate ecological feedbacks
both to trigger and to damp the explosion.
The evolution of predation and its consequences for driving an evolutionary arms race
and for mediating coexistence among competitors represent a potential trigger mechanism
(e.g. Stanley, 1976; Bengtson, 1994). The explosion would slow down as the ecological barrel
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became full and opportunities became more
limited for new biological designs. Thus, the
loose-genes hypothesis involves an intrinsic
slowing of the generation of evolutionary
novelty, independent of ecological changes,
whereas the loose-niches hypothesis involves
a steady production of evolutionary novelty,
but declining success of novel forms owing to
extrinsic factors. Despite this clear-cut conceptual distinction, the two hypotheses make very
similar predictions in terms of paleontological
patterns (Jablonski and Bottjer, 1990; Valentine,
1995).
At the moment, the loose-niches view probably has the edge. Although far more work is
needed, present knowledge of molecular developmental biology, combined with phylogenetic
data on the relationships of living phyla, suggests that a number of the important developmental pathways that built the organisms of
the Cambrian explosion were in place well
before the event itself (like oxygen, perhaps,
necessary but not sufficient) (see Valentine,
1995; Erwin et al., 1997). However, this view
may be premature. We still understand only
a fraction of the developmental machinery
required to build metazoans, and one inescapable message of the recent work on developmental pathways is that the molecular pathways that generate morphology have evolved
in as complex and quirky a fashion as the morphology itself. Early establishment of basic signaling pathways does not necessarily exclude
later accumulation of multiple roles for individual genes, for example. One approach to testing genomic vs ecologic hypotheses might be to
take a closer look at the kinds of novelties
established at different points in a clade’s history, eventually with reference to the developmental basis for those novelties (see Jacobs,
1990; Wagner, 1995; Foote, 1999, all three of
whom conclude that their evidence supports
a genomic hypothesis). For example, Foote
(1999) found that post-Paleozoic crinoid diversification was functionally and ecologically
prolific but morphologically much more stereotyped than the initial Paleozoic radiation of the
group, and concluded that this pattern was
more consistent with a genomic hypothesis.
Clearly, without a time machine to perform
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reciprocal transplants between Cambrian and
modern seas (to test whether early Paleozoic
organisms would be as prolific in their novel
morphologies in a more crowded world, or
whether modern organisms would spill forth
a host of novel forms in the ostensibly more
permissive Cambrian seas), a new round of
multidisciplinary work will be needed to tackle
this fascinating problem.
13.3.2 The ‘reef gap’
Following mass-extinction events, the reassembly of complex communities found in clear,
shallow, tropical waters often involves a distinct lag time, loosely termed the reef gap
(e.g. Hallam and Wignall, 1997) (Figure 13.3).
‘Reef’ is not being applied in the strict sense of
a demonstrably wave-resistant framework, but
simply as a general term for the diverse benthic
225
communities characteristic of tropical onshore
habitats over most of geologic time, except for
the 5–10–My after major extinction events (e.g.
Copper 1988, 1994a, b; Stanley, 1992; Jablonski,
1995; see Webb, 1996, for a somewhat different,
microbial perspective; and Wood, 1998, for difficulties of applying strict definitions to ancient
associations). Thus, the bizarre rudist bivalves
that dominated late Cretaceous tropical
onshore settings did not make reefs in the strict
sense, but they generated massive, extensive
skeletal accumulations in clear-water tropical
settings (e.g. Gili et al., 1995). With the demise
of the rudists at or near the K–T boundary,
diverse and extensive metazoan carbonates
were scarce or absent until assemblages dominated by colonial corals began to appear with
increasing frequency in the late Paleocene,
8–10 My into the Cenozoic. Coral build-ups
are clearly not close analogs of rudist commu-
Figure 13.3 Episodes in the history of ‘reefs’ and other tropical build-ups through geologic time. Arrows
represent the major extinctions (those in parentheses are less well documented than the Big Five); asterisks
mark small events. Superimposed on the global diversity curve for marine families are vertical black bars
representing intervals that lack major reef development. The icehouse/greenhouse curve gives a rough
assessment of the global climatic state. As noted in the text, the ability of Cretaceous rudists to build
large frameworks is hotly debated. Modified from Stanley (1992).
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nities, but the temporal gap is still striking, and
similar gaps appear after the other mass extinctions as well.
The reef gap might be the result of physical
factors, so that the development of diverse tropical carbonate communities was impeded by
the persistence of the physical perturbations
that had triggered the extinction itself (e.g.
Stanley, 1988; Stanley, 1992). However, isotopic
and other time series, along with modeling of,
for example, the effects of asteroid impacts and
massive volcanic eruptions, suggest that the
reef gap persists far longer than the climatic
and other disruptions (e.g. for the K–T event,
D’Hondt et al., 1996, 1998; Conway Morris
1998a, b; Erwin, 1998: 345). Clearly more
work is needed to track the return of physical
environmental parameters to their old, or a
new, steady state. With improved geochronological methods the necessary data are sure to
become available.
Alternatively, the reef gap might be imposed
by intrinsic biotic factors. Perhaps the assembly
of these tropical communities is determined by
the intrinsic diversification rates of their major
constituents. This ‘waiting time’ hypothesis
seems weakened, first by the general acceleration of evolutionary rates after mass extinction
events discussed above, and second by
Kirchner and Weil’s (2000) finding that recoveries tend to have a characteristic (c. 10 My) lag
until peak origination rates are reached,
regardless of the geologic age or magnitude
of the event (see also Sepkoski, 1998); but the
hypothesis has yet to be tested by detailed
comparisons of evolutionary rates in the appropriate taxa before and after extinction events.
Extrinsic biotic effects are also a possibility.
Perhaps the reef gap is a problem in ecological
assembly, with lags set by the time required
for complex ecosystems to attain a coherent
structure (Talent, 1988; Conway Morris,
1998b). Here, the limiting step is not taxonomic origination, but the reassembly of a
complex, stable ecosystem (see also D’Hondt
et al., 1998, who suggest that plankton production recovered shortly after the K–T event,
while ecosystem structure lagged by almost
3 My). Paleontological testing of this hypothesis will be difficult, but comparative analysis
[10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d]
of the details of reassembly among recovery
intervals should help. Analyses might include:
detailed time-series for temperature and other
environmental parameters (to test the role of
physical factors as controls), data on the
occurrence and phylogenetic relationships of
important taxa in the interval before the community takes on its distinctive flavor (to test
for evolutionary lags), and testing whether the
duration of the recovery lag is positively
related to the complexity of the new system
(for which there is some evidence, at least
regarding ‘reef’ vs level-bottom assemblages,
Erwin, 1998).
More subtle lags in biotic recovery may
occur in level-bottom habitats. For example,
after the K–T mass extinction, extratropical,
within-habitat molluscan diversity appears
to recover within a few million years (see
Hansen et al., 1993). But regional diversity,
the number of taxa in an entire biogeographic
province, evidently does not reach Cretaceous
levels until the late Paleocene or early Eocene,
on the order of 10 My after the extinction
(Hansen, 1988; Jablonski, 1998). This might
mean that beta diversity, the differentiation of
local faunas among habitats and along environmental gradients, takes longer to recover than
alpha, or local diversity. These possibilities
need to be tested more rigorously for sampling
artifacts, but should be pursued.
Extrinsic biotic factors have been invoked to
explain a lag in the occurrence of maximum
diversification rates after extinction events
(Sepkoski, 1998, Kirchner and Weil, 2000).
Diversification itself creates niches, the argument goes, so that the evolution of parasites,
predators, and other clades taking advantage
of enlarged biotic opportunities will accelerate,
leading to higher per-taxon origination rates as
the recovery proceeds. Alternatively, however,
the lag could result from strong intrinsic differences in diversification rates among clades (see
Sepkoski, 1998): given unimpeded post-extinction diversification, the global per-taxon rate
will be increasingly dominated by the most
rapidly evolving groups, leading to an increase
in the overall rate until another extinction, or
diversity-dependent feedback, damps the rise
of the high-rate taxa. It would be interesting to
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The interplay of physical and biotic factors in macroevolution
determine whether this intrinsic biotic factor
also plays a role in the recovery of beta and
regional diversity, which occurs on a similar
timescale, for example by testing whether
increases in beta diversity are set by the highorigination taxa.
If either type of biotic factor can be verified
for the ‘reef gap’, or for other lags in the recovery of ecological structure (such as the ‘coal
gap’ after the end-Permian extinction, Faure
et al., 1996; Retallack et al., 1996), this would
have sobering implications for the restoration
ecology of modern ecosystems. It would provide concrete evidence that the recovery of a
system that has been degraded below some
threshold will lag far behind the removal of
the immediate extinction driver. The fossil
record presents real opportunities for exploring the magnitudes and types of losses that
might impose such recovery lags.
13.3.3 The biogeographic fabric of recoveries
Because the major mass extinctions are global
events, presumably driven by physical perturbations at that scale, the general assumption
has been that the subsequent recoveries
would be global as well. But the molluscan
recovery from the end-Cretaceous mass extinction is geographically heterogeneous. Despite
indistinguishable extinction intensities at the
K–T boundary, faunal dynamics for two tropical regions (North Africa, and the northern
margin of the Indian plate including Pakistan)
and two temperate regions (the North
American Gulf and Atlantic Coastal Plain,
and northern Europe) show significant differences, with North America being the odd man
out. The evolutionary burst and decline of
‘bloom taxa’ in the North American early
Paleocene documented by Hansen (1988),
with other taxa in the region showing slower,
steadier diversification, is not seen in the other
three regions (Figure 13.4). This pattern holds
whether the bloom taxa are treated as a proportion of the biota, or, once the phylogenetic bottleneck is taken into account by estimating
minimum surviving lineages at the boundary,
as raw species numbers (Jablonski, 1998). It is
also unlikely to be an artifact of regional differ-
[10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d]
227
Figure 13.4 Geographic variation in the molluscan
recovery from the end-Cretaceous mass extinction.
The same ‘bloom taxa’ that burst and decline immediately after the extinction in North America show
significantly less volatile evolutionary behavior in
three other regions, as a proportion of species in
each fauna as shown here, in raw numbers (as
shown by Jablonski, 1998). The reasons for this difference are debated. For details and statistical confidence limits, see Jablonski (1998).
ences in sampling resolution, because in northern Europe at least, the region most likely to
conform to North America by reason of proximity and climatic similarity, an earliest
Paleocene fauna (the Cerithium Limestone,
nannofossil zone NP1) has been well studied
by Claus Heinberg (1999), and clearly lacks
the expected pulse of bloom taxa. A further
contrast among faunas is the source of new
taxa: the North American fauna is significantly
more subject to invasion from outside the
region, whereas the other three faunas accumulate more of their post-extinction diversity by
diversification within the region (Jablonski,
1998).
The most obvious physical explanation for
this surprising geographic variation in the
Paleocene recovery is that North America
was nearest to the K–T impact near
Chicxulub on the Yucutan Peninsula (which
might even have been oblique, with its greatest effects to the northwest, Schultz and
D’Hondt, 1996). It might therefore have suffered the greatest perturbation and conse-
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Evolution on Planet Earth
quently would have been subject to a most
complicated recovery. However, this explanation is undercut by the similarities in extinction intensities among the four regions (Raup
and Jablonski, 1993). An alternative might lie
in potential geographic differences in the
Paleocene recovery environment. By some
models, North American forests would have
ignited at the time of impact (Toon et al.,
1997). Weathering, erosion and transport of
the incinerated organic material to the continental shelf might have created a very different nutrient regime around southeastern
North America relative to regions whose
neighboring lands had not been subject to
conflagration. The million-year timescale
seems long for this effect, but geochemical
analyses aimed at isotopes and biomarkers
should permit testing of this hypothesis.
Intrinsic biotic factors might have played a
role in the interregional differences in recovery
dynamics. For example, the differences might
have arisen if the North American set of survivors had features such as low-dispersal larvae
that would have promoted rapid speciation
and high extinction rates, relative to related
taxa in other regions. Both phylogenetic analysis, to confirm the monophyly of the North
American bursts of bloom taxa, and a quantitative assessment of the interregional distribution of appropriate character states, are needed
here. So far I have seen no evidence suggesting
that North America’s bloom taxa (turritellid
gastropods, and carditid, ostreid, and cucullaeid bivalves) were richer in speciation-promoting intrinsic features such as lowdispersal larvae compared to relatives elsewhere, but comparisons among subclades
would certainly be worth pursuing.
Finally, extrinsic biotic factors might have
been involved. Similar extinction intensities
might yield different long-term consequences
among regions according to the ecological
roles of the victims or the invaders. For the
K–T mollusks, for example, perhaps the
North American victims were drawn from the
more abundant taxa, or included more keystone species (that is, species whose activities
help to structure communities), so that their
disappearance was especially disruptive of
[10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d]
competitive or predator/prey relationships
and thus enhanced the volatility and invasibility of that region relative to the others.
Lockwood (1997) found no correlation between
abundance and extinction in North American
mollusks, which undermines the simplest version of the extrinsic hypothesis, but more rigorous comparative analyses are needed to rule
it out (perhaps, for example, the victims in the
other regions are drawn from rare taxa rather
than at random – unlikely, given my qualitative observations, but in need of testing).
Keystone species are understood in only a
few present-day situations, and their loss will
be exceedingly difficult to detect in the fossil
record, particularly in light of our growing
appreciation of the role of indirect effects in
structuring communities (e.g. Wootton, 1994).
Nevertheless, a more detailed and standardized analysis of the ecological roles of victims,
survivors, and invaders in different regions
would be extremely valuable. The finding
that invaders were not randomly drawn from
the pool of survivors, but were significantly
more widespread prior to the K–T extinction
(Jablonski, 1998), suggests that biotic factors
will prove to be important in determining the
intensity and asymmetry of post-extinction
interchanges. More generally, it suggests a
line of research that would contribute to a
more complete, general theory of donor/recipient dynamics for biotic invasions in the geologic past and in the accelerating humanmediated invasions of the present day.
The realization that recoveries do not necessarily unfold simultaneously and in a coordinated fashion among regions is mirrored by
recent analyses of the geographic fabric of the
Ordovician radiations of marine life – a profuse
set of variations on the themes initiated during
the Cambrian explosion. After correcting for
sampling, Miller (1997a, b) found that some
regions follow a nearly monotonic diversity
increase through the Ordovician, while others
peak early and then decline. Thus, like the
replacement of aporrhaid gastropods by the
strombids, and the region-specific K–T recovery patterns, the global history of the
Ordovician diversification is an aggregate of
rather disparate patterns on the different con-
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The interplay of physical and biotic factors in macroevolution
229
tinents. Miller (1997a, b; Miller and Mao, 1995)
found that the regional diversity trends appear
to correlate with the extent or intensity of
mountain-building activity, an intriguing physical factor that has been invoked before, but
never with such a rich and detailed database
(e.g. Lull, 1918; Grabau, 1940; Umbgrove, 1947;
Henbest, 1952). Clearly, decomposing global
diversity patterns into regional components
will be a major area of paleontological research.
13.4 Conclusion
Macroevolutionary patterns are shaped by
both physical and biotic factors, and the rich
feedbacks between them. The very healthy
surge in our interest in, and our ability to quantify rate and magnitude of, physical environmental change has helped to redress a
conceptual imbalance that had tended to overemphasize biotic interactions. The growing
geologic database on physical factors will provide important opportunities to calibrate magnitudes of perturbations with magnitude and
type of biotic response – a long-sought goal
anticipated by Raup’s (1991, 1992) pioneering
‘kill curve’ for asteroid impact events. The geologic database also provides a much wider
range of parameter values, from temperatures
to atmospheric compositions to asteroid
impacts, than are available today or in the
immediate geologic past, and this expanded
range is crucial for a more rigorous understanding of the operation of the Earth/life system (Figure 13.5).
It would be a mistake, however, to allow the
pendulum to swing too far in the direction of
physical effects or to allow false dichotomies,
e.g. that the existence of physical forcing
mechanisms or geographic variation in biotic
transitions somehow negates the importance
of intrinsic biotic factors. Instead, we need to
develop protocols for exploring the tension
between physical and biotic factors in shaping
large-scale evolutionary patterns. These are
complementary components of macroevolutionary processes, operating in tandem or in
sequence (see also Lister and Rawson, this
[10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d]
Figure 13.5 The importance of data from the geologic record. The recent and immediate geologic past
encompasses a relatively narrow range of situations,
leading to potentially faulty extrapolations of biotic
responses to physical variables (broken line). With
the enlarged range of conditions and biotic
responses provided by the geologic record, we can
better understand – and perhaps predict – the behavior of the Earth/life system.
volume, Chapter 16), and as discussed above
their relative strengths will vary with the situation. Sometimes physical factors will be the
ultimate causes of disruptions mediated by
proximate biotic causes, as probably seen at
the K–T boundary. However, for several reasons it would be an oversimplification to
assume that life goes about its business until
a rock falls out of the sky, metaphorically or
literally, and that physical factors completely
reset or even reverse the accumulated biotically
driven changes.
First, intrinsic biotic factors apparently
determine how co-occurring clades respond
to a perturbation, an effect especially strong
away from the Big Five mass extinctions, but
detectable even at the times of the most
extreme global events.
Second, perturbations come at all scales, and
they mediate biotic transitions at all scales. A
stream bisecting a field means very different
things to a mouse and an elephant. But the
importance of those perturbations is attributable to their disruption of the incumbent advantage. Incumbency, an extrinsic biotic factor that
slows or blocks invasion or diversification, may
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Evolution on Planet Earth
be such an important component of the macroevolutionary process that local perturbation
may be crucial to the establishment of global
trends (Miller, 1998). Positive biotic feedbacks
may also play a role in diversification rates, as
suggested by Sepkoski (1998) and Kirchner and
Weil (2000), among others.
Third, major biotic trends can transcend perturbations, even the Big Five mass extinctions.
Those trends may suffer momentary setbacks,
or at least pauses, but the basic trajectory is
recovered. Consider, just for the K–T extinction, the persistence of: the Mesozoic Marine
Revolution, discussed above; the onshore/offshore shift or expansion of most post-Paleozoic
orders (Jablonski and Bottjer 1990, 1991); the
increasing taxonomic and ecological dominance of cheilostome bryozoans relative to
cyclostomes (Lidgard et al., 1993; McKinney et
al., 1998); and the rise of flowering plants
(Niklas, 1997; Boulter et al. (1998; Lupia, 1999;
Magallon et al., 1999). One of the challenges
ahead is to understand why such trends persist
in the face of major and minor extinction
pulses, while others do not. Whatever the ultimate answer, it is clear that physical and biotic
factors cannot be reduced to simple, antagonistic alternatives in the explanation of macroevolutionary patterns.
13.5 Acknowledgments
I thank the editors for inviting me to participate
in this stimulating symposium, and am grateful to Susan M. Kidwell, Mike Foote, Adrian
Lister, and Michael J. Benton for valuable
reviews. Supported by the National Science
Foundation, grants EAR93-17114 and EAR9903030.
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