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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 ISBN 0-00-000000-X [10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] Copyright # 2002 Academic Press Limited All rights of reproduction in any form reserved Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 217 1-403 218 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. [10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] 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 Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 218 1-403 The interplay of physical and biotic factors in macroevolution 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, [10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] 219 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 Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 219 1-403 220 Evolution on Planet Earth 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). [10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 220 1-403 The interplay of physical and biotic factors in macroevolution 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- [10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] 221 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. Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 221 1-403 222 Evolution on Planet Earth 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; [10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] 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 Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 222 1-403 The interplay of physical and biotic factors in macroevolution 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 [10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] 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- Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 223 1-403 224 Evolution on Planet Earth 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 [10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] 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 Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 224 1-403 The interplay of physical and biotic factors in macroevolution 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). [10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 225 1-403 226 Evolution on Planet Earth 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 Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 226 1-403 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- Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 227 1-403 228 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- Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 228 1-403 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 Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 229 1-403 230 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. 13.6 References Alexander, R.McN. (1998). All-time giants: the largest animals and their problems. Palaeontology, 41: 1231–1245. Allmon, W.A. and Ross, R.M. (1990). Specifying causal factors in evolution: the paleontological con- [10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] tribution. In: RT.M. Ross and W.A. Allmon (eds) Causes of Evolution: A Paleontological Perspective. Chicago: University of Chicago Press, pp. 1–17. Arthur, W. (1997). The Origin of Animal Body Plans. Cambridge: Cambridge University Press. Bakker, R.T. (1983). The deer flees, the wolf pursues: incongruencies in predator–prey coevolution. In: D.J. Futuyma and M. Slatkin (eds) Coevolution. Sunderland, Mass.: Sinauer, pp. 350–382. Bambach, R.K. (1993). Seafood through time: changes in biomass, energetics, and productivity in the marine ecosystem. Paleobiology, 19: 372–397. Bambach, R.K. (1999). Energetics in the global marine fauna: a connection between terrestrial diversification and change in the marine biosphere. Geobios, 32: 131–144. Bengtson, S. (1994). The advent of animal skeletons. In: S. Bengtson (ed.) Early Life on Earth. New York: Columbia University Press, pp. 412–425. Benton, M.J. (1987). Progress and competition in macroevolution. Biological Reviews, 62: 305–338. Benton, M.J. (1996). On the nonprevalence of competitive replacement in the evolution of tetrapods. In: D. Jablonski, D.H. Erwin and J.H. Lipps (eds) Evolutionary Paleobiology. Chicago: University of Chicago Press, pp. 185–210. Boulter, M.C., Gee, D. and Fisher, H.C. (1998). Angiosperm radiations at the Cenomanian/ Turonian and Cretaceous/Tertiary boundaries. Cret. Res., 19: 107–112. Brinkhuis, H., Bujak, J.P., Smit, J. et al. (1998). Dinoflagellate-based sea surface temperature reconstructions across the Cretaceous–Tertiary boundary. Palaeogeogr., Palaeoclimatol., Palaeoecol., 141: 67–83. Canfield, D.E. and Teske, A. (1996). Late Proterozoic rise in atmospheric oxygen concentration inferred from phylogenetic and sulphur-isotope studies. Nature, 382: 127–132. Conway Morris, S. (1998a). Palaeontology: grasping the opportunities in the science of the twenty-first century. Geobios, 30: 895–904. Conway Morris, S. (1998b). The evolution of diversity in ancient ecosystems: a review. Phil. Trans. Roy. Soc. London B, 353: 327–345. Copper, P. (1988). Ecological succession in Phanerozoic reef ecosystems: is it real? Palaios, 3: 136–152. Copper, P. (1994a). Ancient reef ecosystem expansion and collapse. Coral Reefs, 13: 3–11. Copper, P. (1994b). Reefs under stress: the fossil record. Cour. Forsch.-Inst. Senckenberg, 192: 87–94. D’Hondt, S., King, J. and Gibson, C. (1996). Oscillatory marine response to the Cretaceous–Tertiary impact. Geology, 24: 611–614. Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 230 1-403 The interplay of physical and biotic factors in macroevolution D’Hondt, S., Donaghay, P., Zachos, J.C. et al. (1998). Organic carbon fluxes and ecological recovery from the Cretaceous–Tertiary mass extinction. Science, 282: 276–279. Erwin, D.H. (1989). Regional paleoecology of Permian gastropod genera, southwestern United States and the end-Permian mass extinction. Palaios, 4: 424–438. Erwin, D.H. (1994). Early introduction of major morphological innovations. Acta Palaeont. Polonica, 38: 281–294. Erwin, D.H. (1998). The end and the beginning: recoveries from mass extinctions. Trends Ecol. Evol., 13: 344–349. Erwin, D.H. (1999). The origin of bodyplans. Am. Zool., 39: 617–629. Erwin, D.H., Valentine, J.W. and Jablonski, D. (1997). The origin of animal body plans. Am. Sci., 85: 126–137. Faure, K., de Wit, M.J. and Willis, J.P. (1996). Late Permian global coal discontinuity and Permian–Triassic boundary ‘events’. In: Nine Gondwana. Rotterdam: Balkema, pp. 1075–1089. Foote, M. (1999). Morphological diversity in the evolutionary radiation of Paleozoic and postPaleozoic crinoids. Paleobiology, 25 (Supplement to No. 2): 115pp. Gilbert, S.F. (1997). Developmental Biology. 5th edition. Sunderland, Mass.: Sinauer, 918pp. Gili, C. and Martinell, J. (1994). Relationship between species longevity and larval ecology of nassariid gastropods. Lethaia, 27: 291–299. Gili, E., Masse, J.-P. and Skelton, P.W. (1995). Rudists as gregarious sediment-dwellers, not reefbuilders, on Cretaceous carbonate platforms. Palaeogeogr., Palaeoclimatol., Palaeoecol., 118: 245–267. Gilinsky, N.L. (1994). Volatility and the Phanerozoic decline of background extinction intensity. Paleobiology, 20: 445–458. Gould, S.J. (1977). Eternal metaphors of paleontology. In: A. Hallam (ed.) Patterns of Evolution. Amsterdam: Elsevier, pp. 1–26. Grabau, A.W. (1940). The Rhythm of the Ages. Peking: Henri Vetch, 561pp. Grantham, T.A. (1995). Hierarchical approaches to macroevolution: recent work on species selection and the ‘effect hypothesis’. Ann. Rev. Ecol. Syst., 26: 301–322. Hallam, A. and Wignall, P.B. (1997). Mass Extinctions and their Aftermath. Oxford: Oxford University Press, 320pp. Hansen, T.A. (1978). Larval dispersal and species longevity in Lower Tertiary gastropods. Science, 199: 885–887. [10:54 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] 231 Hansen, T.A. (1980). Influence of larval dispersal and geographic distribution on species longevity in neogastropods. Paleobiology, 6: 193–207. Hansen, T.A. (1988). Early Tertiary radiation of molluscs and the long-term effects of the Cretaceous–Tertiary extinction. Paleobiology, 14: 37–51. Hansen, T.A., Farrell, B.R. and Upshaw, B. III. (1993). The first 2 million years after the Cretaceous–Tertiary boundary in east Texas: rate and paleoecology of the molluscan recovery. Paleobiology, 19: 251–265. Harper, E.M. (1991). The role of predation in the evolution of cementation in bivalves. Palaeontology, 34: 455–460. Harper, E.M. and Skelton, P.W. (1993). The Mesozoic Marine Revolution and epifaunal bivalves. Scripta Geol. Special Issue, 2: 127–153. Heinberg, C. (1999). Lower Danian bivalves, Stevns Klint, Denmark: continuity across the K/T boundary. Palaeogeogr., Palaeoclimatol., Palaeoecol., 154: 87–106. Henbest, L.G. (1952). Significance of evolutionary explosions for diastrophic division of Earth history – introduction to the symposium. J. Paleontol., 26: 299–318. Hoffman, P.F., Kaufman, A.J., Halverson, G.P. and Schrag, D.P. (1998). A Neoproterozoic snowball Earth. Science, 281: 1342–1346. Jablonski, D. (1980). Apparent versus real biotic effects of transgression and regression. Paleobiology, 6: 397–407. Jablonski, D. (1986). Larval ecology and macroevolution of marine invertebrates. Bull. Mar. Sci., 39: 565–587. Jablonski, D. (1986b). Background and mass extinctions: the alternation of macroevolutionary regimes. Science, 231: 129–133. Jablonski, D. (1987). Heritability at the species level: analysis of geographic ranges of Cretaceous mollusks. Science, 238: 360–363. Jablonski, D. (1995). Extinction in the fossil record. In: R.M. May and J.H. Lawton (eds) Extinction Rates. Oxford: Oxford University Press, pp. 25–44. Jablonski, D. (1996). Mass extinctions: persistent problems and new directions. Geol. Soc. Am. Spec. Paper, 307: 1–11. Jablonski, D. (1998). Geographic variation in the molluscan recovery from the end-Cretaceous extinction. Science, 279: 1327–1330. Jablonski, D. (2000). Micro- and macroevolution: the infusion of scale and hierarchy into evolutionary biology. Paleobiology, ???? Jablonski, D. and Bottjer, D.J. (1990). The ecology of Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 231 1-403 232 Evolution on Planet Earth evolutionary innovations: the fossil record. In: M.H. Nitecki (ed.) Evolutionary Innovations. Chicago: University of Chicago Press, pp. 253–288. Jablonski, D. and Bottjer, D.J. (1991). Environmental patterns in the origins of higher taxa: the postPaleozoic fossil record. Science, 252: 1831–1833. Jablonski, D. and Raup, D.M. (1995). Selectivity of end-Cretaceous marine bivalve extinctions. Science, 268: 389–391. Jablonski, D. and Sepkoski, J.J. Jr. (1996). Paleobiology, community ecology, and scales of ecological pattern. Ecology, 77: 1367–1378. Jacobs, D.K. (1990). Selector genes and the Cambrian radiation of Bilateria. Proc. Natl. Acad. Sci. USA, 87: 4406–4410. Janis, C.M. and Wilhelm, P.B. (1993). Were there mammalian pursuit predators in the Tertiary? Dances with wolf avatars. J. Mammalian Evol., 1: 103–125. Kammer, T.W., Baumiller, T.K. and Ausich, W.I. (1998). Evolutionary significance of differential species longevity in Osagean–Meramecian (Mississippian) crinoid clades. Paleobiology, 24: 155–176. Kelley, P.H. (1989). Evolutionary trends within bivalve prey of Chesapeake Group naticid gastropods. Hist. Biol., 2: 139–156. Kelley, P.H. (1991). The effect of predation intensity on rate of evolution of five Miocene bivalves. Hist. Biol., 5: 65–78. Kirchner, J.W. and Weil, A. (2000). Delayed biological recovery from extinctions throughout the fossil record. Nature, 404: 177–180. Kirschvink, J.L., Ripperdan, R.L. and Evans, D.A. (1997). Evidence for a large-scale reorganization of Early Cambrian continental masses by inertial interchange true polar wander. Science, 277: 541–545. Kitchell, J.A., Clark, D.L. and Gombos, A.M. Jr. (1986). Biological selectivity of extinction: a link between background and mass extinction. Palaios, 1: 504–511. Knoll, A.H. (1996). Breathing room for early animals. Nature, 382: 111–112. Knoll, A.H. and Carroll, S.B. (1999). Early animal evolution: emerging views from comparative biology and geology. Science, 284: 2129–2137. Lidgard, S., McKinney, F.K. and Taylor, P.D. (1993). Competition, clade replacement, and a history of cyclostome and cheilostome bryozoan diversity. Paleobiology, 19: 352–371. Lockwood, R. (1997). Abundance and survivorship: K–T extinction patterns in North American [10:55 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] bivalves (Abstract). Geol. Soc. Am. Abstr. Programs, 29: A-404. Lockwood, R. (1998). K–T extinction and recovery: taxonomic versus morphological patterns in veneroid bivalves (Abstract). Geol. Soc. Am. Abstr. Programs, 30: A-286. Lull, R.S. (1918). The pulse of life. In: J. Barrell, C. Schuchert, L.L. Woodruff, R.S. Lull and E. Huntington (eds) The Evolution of the Earth and its Inhabitants. New Haven: Yale University Press, pp. 109–146. Lupia, R. (1999). Discordant morphological disparity and taxonomic diversity during the Cretaceous angiosperm radiation: North American pollen record. Paleobiology, 25: 1–28. MacLeod, N. et al. (1997). The Cretaceous–Tertiary biotic transition. J. Geol. Soc. London, 154: 265–292. Magallon, S., Crane, P.R. and Herendeen, P.S. (1999). Phylogenetic pattern, diversity, and diversification of dicots. Ann. Missouri Bot. Garden, 86: 297–372. McGhee, G.R. Jr. (1996). The Late Devonian Mass Extinction. New York: Columbia University Press, 303pp. McKinney, F.K., Lidgard, S., Sepkoski, J.J. Jr. and Taylor, P.D. (1998). Decoupled temporal patterns of evolution and ecology in two post-Paleozoic clades. Science, 281: 807–809. McKinney, M.L. (1997). Extinction vulnerability and selectivity: combining ecological and paleontological views. Annu. Rev. Ecol. Syst., 28: 495–516. McKinney, M.L. (1998). Biodiversity dynamics: niche preemption and saturation in diversity equilibria. In: M.L. McKinney and J.A. Drake (eds) Biodiversity Dynamics. New York: Columbia University Press, pp. 1–16. Miller, D.J., LaBarbera, M. (1995). Effects of foliaceous varices on the mechanical properties of Chicoreus dilectus (Gastropoda, Muricidae). J. Zool., 236: 151–160. Miller, A.I. (1997a). Comparative diversification dynamics among palaeocontinents during the Ordovician radiation. Geobios Mém. Spec., 20: 397–406. Miller, A.I. (1997b). Dissecting global diversity patterns: examples from the Ordovician Radiation. Annu. Rev. Ecol. Syst., 28: 85–104. Miller, A.I. (1998). Biotic transitions in global marine diversity. Science, 281: 1157–1160. Miller, A.I. and Mao, S. (1995). Association of orogenic activity with the Ordovician radiation of marine life. Geology, 23: 305–308. Miller, A.I. and Sepkoski, J.J. Jr. (1988). Modeling bivalve diversification: the effect of interaction Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 232 1-403 The interplay of physical and biotic factors in macroevolution on a macroevolutionary system. Paleobiology, 14: 364–369. Niklas, K.J. (1997). The Evolutionary Biology of Plants. Chicago: University of Chicago Press, 449pp. Palmer, A.R. (1979). Fish predation and the evolution of gastropod shell sculpture: experimental and geographic evidence. Evolution, 33: 697–713. Patzkowsky, M.E. (1995). A hierarchical branching model of evolutionary radiations. Paleobiology, 21: 440–460. Pimm, S.L., Jones, H.L. and Diamond, J. (1988). On the risk of extinction. Am. Nat., 132: 757–785. Raup, D.M. (1991). A kill curve for Phanerozoic marine species. Paleobiology, 17: 37–48. Raup, D.M. (1992). Large-body impact and extinction in the Phanerozoic. Paleobiology, 18: 80–88. Raup, D.M. and Jablonski, D. (1993). Geography of end-Cretaceous marine bivalve extinctions. Science, 260: 971–973. Rayner, J.M.V. and Wootton, R.J. (eds) (1991). Biomechanics in Evolution. Cambridge: Cambridge University Press. Retellack, G.J., Veevers, J.J. and Morante, R. (1996). Global coal gap between Permian–Triassic extinction and Middle Triassic recovery of peat-forming plants. Geol. Soc. Am. Bull., 108: 195–207. Rosenzweig, M.L. and McCord, R.D. (1991). Incumbent replacement: evidence for long-term evolutionary progress. Paleobiology, 17: 202–213. Roy, K. (1996). The roles of mass extinction and biotic interaction in large-scale replacements: a reexamination using the fossil record of stromboidean gastropods. Paleobiology, 22: 436–452. Rye, R., Holland, H.D. (1998). Paleosols and the evolution of atmospheric oxygen: a critical review. Am. J. Sci., 298: 621–672. Scheltema, R.S. (1977). Dispersal of marine organisms: paleobiogeographic and biostratigraphic implications. In: E.G. Kauffman and J.E. Hazel (eds) Concepts and Methods of Biostratigraphy. Stroudsburg, PA: Dowden, Hutchinson & Ross, pp. 83–108. Scheltema, R.S. (1989). Planktonic and non-planktonic development among prosobranch gastropods and its relationship to the geographic range of species. In: J.S. Ryland and P.A. Tyler (eds) Reproduction, Genetics and Distributions of Marine Organisms. Fredensborg, Denmark: Olsen & Olsen, pp. 183–188. Schmidt-Kittler, N., Vogel, K. (eds) (1991). Constructional Morphology and Evolution. Berlin: Springer, 409pp. Schultz, P.H. and D’Hondt, S. (1996). Cretaceous–Tertiary (Chicxulub) impact angle and its consequences. Geology, 24: 963–967. [10:55 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] 233 Sepkoski, J.J. Jr. (1996). Competition in macroevolution: the double wedge revisited. In: D. Jablonski, D.H. Erwin and J.H. Lipps (eds) Evolutionary Paleobiology. Chicago: University of Chicago Press, pp. 211–255. Sepkoski, J.J. Jr. (1998). Rates of speciation in the fossil record. Phil. Trans. Roy. Soc. London B, 353: 315–326. Sereno, P.C. (1999). The evolution of dinosaurs. Science, 284: 2137–2147. Skelton, P.W. (1991). Morphogenetic versus environmental cues for adaptive radiations. In: N. Schmidt-Kittler and K. Vogel (eds) Constructional Morphology and Evolution. Berlin: Springer-Verlag, pp. 375–388. Smith, A.B. and Jeffery, C.H. (1998). Selectivity of extinction among sea urchins at the end of the Cretaceous period. Nature, 392: 69–71. Stanley, G.D. Jr. (1992). Tropical reef ecosystems and their evolution. In: W.A. Nierenberg (ed.) Encyclopedia of Earth System Science, Volume 4. San Diego: Academic Press, pp. 375–388. Stanley, S.M. (1976). Fossil data and the Precambrian–Cambrian evolutionary transition. Am. J. Sci., 276: 56–76. Stanley, S.M. (1988). Paleozoic mass extinctions: shared patterns suggest global cooling as a common cause. Am. J. Sci., 334–352. Stanley, S.M. (1990). The general correlation between rate of speciation and rate of extinction: fortuitous causal linkages. In: R.M. Ross and W.A. Allmon (eds) Causes of Evolution: A Paleontological Perspective. Chicago: University of Chicago Press, pp. 103–127. Stone, M.H.I. (1998). On predator deterrence by pronounced shell ornament in epifaunal bivalves. Palaeontology, 41: 1051–1068. Talent, J.A. (1988). Organic reef-building: episodes of extinction and symbiosis? Senckenbergiana Lethaea, 69: 315–368. Toon, O.B., Zahnle, K., Morrison, D. et al. (1997). Environmental perturbations caused by the impacts of asteroids and comets. Rev. Geophys., 35: 41–78. Umbgrove, J.H.F. (1947). The Pulse of the Earth. 2nd edition. The Hague, Netherlands: Martin Nijhoff, 358pp. Valentine, J.W. (1995). Why no new phyla after the Cambrian? Genome and ecospace hypotheses revisited. Palaios, 10: 190–194. Valentine, J.W. and Erwin, D.H. (1987). Interpreting great developmental experiments: the fossil record. In: R.A. Raff and E.C. Raff (eds) Development as an Evolutionary Process. New York: Liss, pp. 71–107. Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 233 1-403 234 Evolution on Planet Earth Valentine, J.W. and Jablonski, D. (1983). Larval adaptations and patterns of brachiopod diversity in space and time. Evolution, 37: 1052–1061. Valentine, J.W. and Jablonski, D. (1986). Mass extinctions: sensitivity of marine larval types. Proc. Natl. Acad. Sci. USA, 83: 6912–6914. Valentine, J.W., Jablonski, D. and Erwin, D.H. (1999). Fossils, molecules and embryos: new perspectives on the Cambrian explosion. Development, 126: 851–859. Van Valen, L.M. (1994). Concepts and the nature of selection by extinction: is generalization possible? In: W. Glen (ed.) Mass Extinction Debates: How Science Works in a Crisis. Stanford, CA: Stanford University Press, pp. 200–216. Van Valkenburgh, B. (1999). Major patterns in the history of carnivorous mammals. Ann. Rev. Earth Planet. Sci., 27: 463–493. Vermeij, G.J. (1977). The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology, 3: 245–258. Vermeij, G.J. (1982). Gastropod shell form, breakage, and repair in relation to predation by the crab Calappa. Malacologia, 23: 1–12. Vermeij, G.J. (1987). Evolution and Escalation. Princeton, New Jersey: Princeton University Press, 527pp. Vermeij, G.J. (1994). The evolutionary interaction [10:55 21/1/03 N:/3981 ROTHSCHILD.751/3891-book.3d] among species: selection, interaction, and coevolution. Ann. Rev. Ecol. Syst., 25: 219–236. Vermeij, G.J. (1995). Economics, volcanos, and Phanerozoic revolutions. Paleobiology, 21: 125–152. Wagner, P.J. (1995). Testing evolutionary constraint hypotheses with Early Paleozoic gastropods. Paleobiology, 21: 248–272. Watts, P.C., Thorpe, J.P. and Taylor, P.D. (1998). Natural and anthropogenic dispersal mechanisms in the marine environment: a study using cheilostome Bryozoa. Phil. Trans. Roy. Soc. London B, 353: 453–464. Webb, G.E. (1996). Was Phanerozoic reef history controlled by the distribution of non-enzymatically secreted reef carbonates (microbial carbonate and biologically induced cement)? Sedimentology, 43: 947–971. Williams, G.C. (1992). Natural Selection. Oxford: Oxford University Press, 208pp. Wolpert, L., Beddington, R., Brockes, J. , et al. (1998). Principles of Development. Oxford: Oxford University Press, 484pp. Wood, R. (1998). The ecological evolution of reefs. Annu. Rev. Ecol. Syst., 29: 179–206. Wootton, J.T. (1994). The nature and consequences of indirect effects in ecological communities. Annu. Rev. Ecol. Syst., 25: 443–466. Ref: 3981 Auth: ROTHSCHILD Title: Evolution Planet Earth Sample Page: 234 1-403