© 2003 by The Society for Integrative and Comparative Biology
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Taking the Pulse of the Cambrian Radiation1
1 Department of Geology and Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas 66045
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The Cambrian radiation is that key episode in the history of life when a large number of animal phyla appeared in the fossil record over a geologically short period of time. Over the last 20 years, scientific understanding of this radiation has increased significantly. Still, fundamental questions remain about the timing of the radiation and also the tempo of evolution. Trilobites are an excellent group to address these questions because of their rich abundance and diversity. Moreover, their complex morphology makes them readily amenable to phylogenetic analysis, and deducing the nature of macroevolutionary processes during the Cambrian radiation requires an understanding of evolutionary patterns. Phylogenetic biogeographic analysis of Early Cambrian olenellid trilobites, based on a modified version of Brooks Parsimony Analysis, revealed the signature of the breakup of Pannotia, a tectonic event that most evidence suggests is constrained to the interval 600 to 550 Ma. As trilobites are derived metazoans, this suggests the phylogenetic proliferation associated with the Cambrian radiation was underway tens of millions of years before the Early Cambrian, although not hundreds of millions of years as some have argued.
Phylogenetic information from Early Cambrian olenellid trilobites was also used in a stochastic approach based on two continuous time models to test the hypothesis that rates of speciation were unusually high during the Cambrian radiation. No statistical evidence was found to support this hypothesis. Instead, rates of evolution during the Cambrian radiation, at least those pertaining to speciation, were comparable to those that have occurred during other times of adaptive or taxic radiation throughout the history of life.
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INTRODUCTION |
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The Cambrian radiation is a key episode in the history of life that involves the apparent proliferation of many but not all bilaterian metazoan taxa in the fossil record (Conway Morris, 1993
, 2000; Fortey et al., 1996; Budd and Jensen, 2000). The study of this radiation has received rich attention for more than 100 years, and the last 20 years have witnessed particular progress. Still, several questions remain unanswered about the nature of that radiation. Among these questions, two of the important ones concern timing and tempo. Data from such areas as molecular biology and developmental biology have partly helped elucidate questions about the timing and tempo of the Cambrian radiation in an important way (e.g., Davidson et al., 1995; Wray et al., 1996; Ayala et al., 1998; Bromham et al., 1998), but the fossil record remains an important place to test hypotheses about that radiation (Valentine, 1994; Fortey et al., 1996; Conway Morris, 2000; Budd and Jensen, 2000). This paper will focus on how the analysis of trilobites using a phylogenetic framework has enhanced what we know about whether there was an early, hidden radiation preceding the apparent Cambrian radiation in the fossil record and also whether the rate of evolution was unusually high at this time.
Trilobites are among the best organisms to test hypotheses about the Cambrian radiation because of their rich abundance and diversity in Cambrian strata and also because they are perhaps the only diverse Cambrian metazoan group with a complex anatomy easily amenable to phylogenetic analysis. Moreover, phylogenetic methods are central to addressing any questions about the rate of evolution and the timing of evolutionary events because calculation of an evolutionary rate presumes some knowledge about evolutionary relationships (Brooks and McLennan, 1991; Sanderson and Donoghue, 1996). Phylogenetic information, in conjunction with information from stratigraphy, can also help constrain the timing of speciation events (Novacek and Norell, 1982; Edgecombe, 1992).
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The debate about the timing of the Cambrian radiation has a significant pedigree, and two primary viewpoints exist. Some have argued that the appearance of metazoan taxa in the Early Cambrian corresponds closely or directly to the evolutionary origin of these taxa (e.g., Gould, 1989
). In contrast, others have argued that the Metazoa must have originated much earlier (e.g., Darwin, 1859, 1872; Runnegar, 1982; Davidson et al., 1995; Fortey et al., 1996; Wray et al., 1996; Ayala et al., 1998; Bromham et al., 1998; Xiao et al., 1998). These two viewpoints have been referred to, respectively, as the Simpsonian and Darwinian viewpoints by Lieberman (1999a). The former view treats the fossil record as a real evolutionary document (a view akin to G. G. Simpson's thoughts on evolution and the fossil record), while the latter view treats the fossil record as either fundamentally flawed, biased, or inaccurate (a view akin to C. Darwin's thoughts on evolution and the fossil record).
Information from trilobites can contribute in an important way to our understanding of the Cambrian radiation. Ostensibly, trilobites diversified during the Early Cambrian, and in fact roughly the first 10 to 15 million years of the Cambrian are devoid of trilobites. Therefore, they might initially be treated as excellent candidates for the Simpsonian view of the Cambrian radiation. Fortey et al. (1996), however, have argued that there may be a signature of diversification events preserved in patterns of trilobite biogeography that actually indicates a much earlier origin and proliferation of the trilobites, supporting the Darwinian view of the radiation. A reconsideration of Fortey et al.'s (1996) study is now possible using a phylogenetic biogeographic approach.
Phylogenetic biogeography is a powerful research tool because it considers patterns of geographic change in the context of evolutionary events and because it is based on a rigorous, repeatable analytical method (Brooks, 1985; Wiley, 1988; Brooks and McLennan, 1991; Lieberman, 2000). It also can be used to identify both episodes of vicariance and congruent range expansion (geo-dispersal) that allow biogeographic patterns to be considered in the context of tectonic and climatic change. This enhances the value of biogeographic patterns because if the timing of tectonic events is known and if biogeographic patterns in a group resemble what is predicted to arise from a specific tectonic event, then the pattern can be treated as a temporal constraint on the origin and evolution of that group.
Fortey et al.'s (1996) study was pioneering, but it could not be based on the analysis of detailed phylogenetic biogeographic patterns since many studies of Early Cambrian trilobite phylogeny (e.g., Lieberman, 1998, 1999b, 2001a, 2002) post dated their study. These phylogenetic data, when analyzed using techniques from phylogenetic biogeography, can be used to consider the tectonic signature preserved in patterns of trilobite biogeography and thus can be used to consider which viewpoint, the Simpsonian or the Darwinian, best describes the Cambrian radiation.
Key tectonic events
Three major tectonic events in the late Neoproterozoic and Early Cambrian might have influenced patterns of trilobite biogeography and evolution. Although the nature of these events and their timing are not ironclad, consensus seems to be emerging indicating this sequence: 1) breakup of the supercontinent Rodinia, occurring around 750 Ma and involving separation of western North America (Laurentia) and eastern Gondwana (East Antarctica, Australia, and possibly South China) (Hoffman, 1991; Moyes et al., 1993; Powell et al., 1993; Li et al., 1996; Torsvik et al., 1996; Dalziel, 1997; Scotese, 1997; Unrug, 1997; Wingate et al., 1998; Karlstrom et al., 1999); 2) ephemeral assembly and then breakup of the supercontinent Pannotia, occurring from 600 to 550 Ma and involving collision and later separation of Laurentia from western Gondwana (including northern Africa and the Amazon region of South America) and some smaller terranes marginal to Gondwana (Dalziel, 1992, 1997; Aleinikoff et al., 1995; Powell, 1995; Faill, 1997; Scotese, 1997; Unrug, 1997; Scotese et al., 1999) that included Avalonia (roughly southern Great Britain, eastern Newfoundland, and northern France) and also southern Europe; and 3) a potential episode of True Polar Wander involving large-scale rapid movement of most of the Earth's cratons in the Early Cambrian (Kirschvink et al., 1997). A possible Early Cambrian paleogeography is shown in Figure 1. Major dissensions from this general sequence have been put forward by Bond et al. (1984) and Veevers et al. (1997), who argued that the breakup of Rodinia occurred around the earliest Cambrian at about 540 Ma. Although these authors did not consider the events related to the breakup and assembly of Pannotia, that event either would not have occurred or it would have been telescoped into the Early Cambrian. Other studies arguing against the general view put forward involve divergences at a smaller temporal scale and include the work of Prave (1999), who suggested that Rodinia split apart slightly later than 750 Ma and instead between 600 Ma and 700 Ma.
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Methods
The phylogenies of Lieberman (1998
, 1999b, 2001a, 2002) allowed approximately 120 species of olenellid trilobites to be considered in phylogenetic biogeographic analysis. These species belong to the Olenelloidea, Nevadioidea, Judomioidea, and "Fallotaspidoidea," and are basal trilobite lineages according to phylogenetic topologies of the Trilobita given by Fortey (1990) and Fortey and Owens (1997).
The biogeographic method used is a modified version of Brooks Parsimony Analysis (BPA) described in detail by Lieberman and Eldredge (1996) and Lieberman (1997, 2000). Because this method has been described already and for the purposes of brevity and clarity, it is not discussed at great length here. The interested reader, however, should see the references listed above for more elaboration and also Brooks (1985), Wiley (1988), and Brooks and McLennan (1991) for discussions of BPA in general. The outputs of the biogeographic analysis are trees showing the relationships of different regions or areas. These depict the best supported patterns of vicariance and geo-dispersal. The more closely biogeographic areas are related on the trees, the more recently they shared a common biogeographic history.
Both vicariance and geo-dispersal trees provide information about the relative timing of tectonic events and climate changes that influenced biogeographic patterns. The vicariance tree provides information about the fragmentation of areas leading to geographic differentiation and speciation (vicariance); the geo-dispersal tree provides information about the joining of areas that leads to congruent range expansion (geo-dispersal). The vicariance tree will be the focus of this study because the tectonic signatures for which I am searching primarily involve continental fragmentation. Geological processes that produce vicariance in such marine invertebrates as trilobites include continental fragmentation and also sea-level fall. The vicariance data matrix is given in Table 1; it is an analytical distillation of the available phylogenies and associated distributional data from the olenellid trilobites. All autapomorphic characters were deleted and all multi-state characters were treated as ordered (see discussion by Lieberman [2000]). A hypothetical ancestor or outgroup, treated as primitively absent from all regions, was used to polarize character states in the data matrix. The matrix was then analyzed using the exhaustive search option of PAUP 4.08b (Swofford, 2001).
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Results
The best-supported phylogenetic pattern of vicariance is shown in Figure 2. Laurentia, although a single craton, is a polyphyletic biogeographic region. There is close area relationship between parts of Laurentia and western Gondwana (northern Africa, southern Europe, and Avalonia) and also between Laurentia, Siberia, and Baltica. East Antarctica and Australia also have a close biogeographic area relationship. The tree-length skewness distribution test of (Hillis, 1991
) and the cladistic permutation tail probability (PTP) test (Faith, 1991) both revealed strong biogeographic signal in the data. Moreover, Bremer (1994) branch support analysis, bootstrap analysis, and jack-knife analysis all revealed moderate to strong support for the various nodes in Figure 2. These tests suggest a good deal of support for the biogeographic patterns presented herein. This biogeographic signature is most compatible with an original distribution of basal trilobite taxa across the supercontinent Pannotia that subsequently became fragmented and vicariated as this continent split apart. As the bulk of the tectonic evidence suggests that assembly and breakup of Pannotia is constrained to 550 to 600 Ma, this result suggests trilobites likely had evolved and begun to diversify minimally by between 550 to 600 Ma. This is a significant period before the trilobites appeared in the fossil record (around 525 to 530 Ma). Of course, if consensus on the timing of the assembly and breakup of Pannotia were to change to encompass a later or earlier date, then my conclusions regarding the timing of the origin and diversification of trilobites would change accordingly.
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Discussion
Because biogeographic patterns in Early Cambrian trilobites are most compatible with tectonic events that appear to date back to the late Neoproterozoic between 550 to 600 Ma it suggests this group had begun to diversify well before the Cambrian radiation's manifestation in the rock record. (The radiation is traditionally held to have begun approximately 543 Ma and ended around 515 to 520 Ma.) This result is given further significance when we consider the phylogenetic position of the trilobites within the Bilateria and the Metazoa. Recent phylogenetic topologies of the Arthropoda (e.g., Briggs and Fortey, 1989
; Wills et al., 1998) suggest that trilobites are euarthropods, and these are in turn derived Bilateria and Metazoa. The result from biogeographic patterns thus suggests that numerous fundamental episodes of metazoan and bilaterian cladogenesis preceded the interval 550 to 600 Ma and thus the Cambrian radiation. Moreover, it points out that there is a disjunction between the phylogenetic events we associate with the Cambrian radiation and the ecological and paleontological emergence of these taxa. This disjunction between evolutionary origin and ecological emergence is potentially a more general pattern in the history of life that deserves more scrutiny. For example, it has already been documented for various orders of Bryozoa (McKinney et al., 1998), for Ordovician trilobites (Droser et al., 1996) at smaller scales such as the radiation of trilobite clades like the Devonian calmoniids (Lieberman, 1993), and also in the sense that authors have argued for a pre-Cenozoic diversification of mammals at the superordinal level (e.g., Archibald et al., 2001).
The use of biogeographic patterns to constrain the timing of the Cambrian radiation is analogous to the use of biogeographic patterns by Murphy et al. (2001) to constrain the mammalian radiation in the Cretaceous. Moreover, these estimates on divergence times of the Bilateria and Metazoa are roughly in line with the predictions from the recent molecular clock analysis of Peterson and Takacs (2002). In spite of the fact that these results support an early, hidden Cambrian radiation, biogeographic patterns from trilobites do not, however, support a diversification of the bilaterian metazoans far back into the Proterozoic that has been predicted by some authors (e.g., Wray et al., 1996). The history of bilaterian metazoan cladogenesis may extend that far back, but there is no evidence to that effect from such derived bilaterians as the trilobites. Furthermore, the fact that well-resolved biogeographic patterns were retrieved in these basal Early Cambrian trilobites and the fact that these patterns were congruent with a major tectonic event suggests that earth history events had a fundamental influence on the topology and perhaps the timing of the Cambrian radiation.
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RATES OF EVOLUTION DURING THE CAMBRIAN RADIATION |
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Introduction
Determining the relative tempo of evolution during the Cambrian radiation is important because it helps elucidate the nature of macroevolutionary processes and how they may vary through time. Truly dramatic tempos of evolution during the Cambrian radiation would point to the uniqueness of this time period in the history of life. Tempos of evolution comparable to other time periods, by contrast, would de-emphasize the uniqueness of the Cambrian radiation, at least in terms of its relevance to our understanding of macroevolutionary processes.
There are two aspects of evolutionary rates. One involves the pace of cladogenesis or speciation. This is based on the recognition that some of the primary data bearing on rates of evolution are rates of speciation (Eldredge, 1979; Stanley, 1979; Vrba, 1980). Another aspect of the rate of evolution involves the amount of morphological change that occurs at speciation or cladogenetic events. This involves the topic of disparity, which has figured prominently in discussions about the nature of the Cambrian radiation. Some (e.g., Gould, 1989, 1991; Hughes, 1991) have argued that the Cambrian radiation marks an interval of unusual evolutionary flexibility relative to subsequent times, such that the disparity of Cambrian faunas equals or exceeds modern faunas. Others have suggested that there is nothing unusual about Cambrian faunas in terms of their flexibility or disparity (e.g., Briggs et al., 1992; Wills et al., 1994; Fortey et al., 1996; Hughes et al., 1999; Smith and Lieberman, 1999; Conway Morris, 2000).
The issue of disparity and the Cambrian radiation is still a topic that is being intensely debated by paleontologists and evolutionary biologists but will not be the focus of this analysis. Instead, here the focus will only be on the question of how, if at all, rates of speciation during the Cambrian radiation differed from rates of speciation documented at other time periods. Very high speciation rates at this time might suggest either that speciation per se occurred more easily in the Early Cambrian or that there were more opportunities for speciation, perhaps due to lower levels of competition in the Early Cambrian (Conway Morris, 2000, 2002) or tectonic processes that facilitated vicariant differentiation and speciation (see Lieberman, 1997). This analysis will rely on the phylogenetic database of trilobites used in the previous part of this paper but will focus on trilobites of the Olenelloidea, the most diverse and abundant clade of olenellids and also the clade containing those species with the most well-characterized stratigraphic ranges (Lieberman, 1998). Lieberman (2001b) discussed why a stochastic approach is the best way to test whether speciation rates were unusually high during the Cambrian radiation. The null hypothesis tested in such an approach is whether rates of speciation documented at other times in the history of life could produce the diversity change seen in Early Cambrian trilobites.
Materials and methods
Four items, all in place, are required to pursue this analysis. 1) Phylogenetic patterns are needed for without knowledge of lineage relationships the calculation of speciation rates is tenuous (Lieberman, 2001c). Phylogenies can be combined with information from stratigraphy to constrain the time when lineages diversified in the manner described by Novacek and Norell (1982) and Edgecombe (1992). Here the phylogenetic framework described above and based on the work of Lieberman (1998, 1999b) was used. 2) A chronology for the interval being studied is needed because calculating rates of speciation requires dates. Although stratigraphic correlation in the Cambrian interval is not without controversy (Landing, 1996; but see Knoll, 1996), the publication of several new radiometric dates for the Early Cambrian (Bowring et al., 1993; Isachsen et al., 1994; Landing et al., 1998) as well as several chemostratigraphic (Kirschvink et al., 1991; Brasier et al., 1996; Kaufman et al., 1996) and biostratigraphic studies (Qian and Bengston, 1989; Ahlberg, 1991; Rozanov, 1992; Vidal and Moczydlowska-Vidal, 1997) now make it possible to constrain with some degree of confidence the duration of the entire Cambrian radiation and even the duration of some of the sub-intervals within that time span. 3) Knowledge of speciation rates from other time periods is needed. This involved collecting a database using results from Walker and Valentine (1984), Vrba (1987), Hulbert (1993), and Lieberman (1999c). These studies were chosen because they focused on species-level fossil taxa for which the phylogenetic context was at least roughly known and because they concentrated on a time interval roughly comparable to those considered for the Early Cambrian trilobites. Moderately high rates of speciation (75th and 90th percentile) were used in the test because past authors have suggested that rates of speciation were extremely high during the Cambrian radiation; low to moderate rates of extinction were used because it has never been argued that the Cambrian radiation was a time of unusual extinction. Furthermore, using high extinction rates could make it artificially difficult or even impossible to reject the null hypothesis. 4) Some model of the evolutionary process is needed. Lieberman (2001b, c) considered different models that have been used to evaluate speciation rates and concluded that the Yule or pure-birth process and the birth and death process were the most robust continuous time models, following the recommendations of Sanderson and Donoghue (1996).
Results
When the test of the null hypothesis was implemented with all of the four items described above in place, the null hypothesis could not be rejected; in short, speciation rates among olenellid trilobites in the Cambrian radiation were not unusually high (Lieberman, 2001b). Speciation rates were somewhat elevated during the Cambrian radiation, relative to the Phanerozoic average, but they have been elevated at other times in the history of life too. In fact, a much greater diversity change would have to have occurred for the null hypothesis to be rejected. These results were also resilient to substantial changes in phylogenetic topology and Early Cambrian chronostratigraphy (Lieberman, 2001b).
Discussion
If the results from trilobites can be extended to other groups, they suggest no need to invoke special rules of evolution, at least those pertaining to rates of speciation, to explain that radiation. Instead, the Cambrian radiation is perhaps best viewed as a time of taxic radiation equivalent to radiations at other major era boundaries, for example, those known to have occurred at the start of the Mesozoic and the start of the Cenozoic. Thus, if there is anything unique about the macroevolutionary processes operating during the Cambrian radiation, it must involve the issue of disparity discussed by Gould (1989, 1991), Briggs and Fortey (1989), Briggs et al. (1992), Conway Morris (1993, 2000), Foote (1995), Wills et al. (1994), Fortey et al. (1996), and Smith and Lieberman (1999).
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A clearer picture of the Cambrian radiation is beginning to emerge. Although high rates of evolution may have prevailed during the Cambrian radiation, they were not phenomenally high nor high enough to merit the formulation of new rules of evolution relating to the tempo of speciation. Furthermore, some period of cryptic diversification must be acknowledged to have occurred prior to the appearance of Early Cambrian organisms in their eponymous stratigraphic sections. Evidence suggests derived bilaterian metazoans such as trilobites had already begun to diversify anywhere from 20 to 70 million years before their appearance in the fossil record, if support for the timing of key tectonic events used as calibration points remains strong. This estimate is comparable to estimates for the diversification of crown group Metazoa derived from the recent molecular clock analysis of Peterson and Takacs (2002)
. This recognition may at first appear troubling to paleontologists because it implies some inadequacy in the fossil record between the transition from evolutionary origin to either ecological dominance or paleontological emergence of the Metazoa; however, this need not be the sole interpretation. First of all, it is comforting that even though the actual late Neoproterozoic diversification of trilobite taxa is not preserved in the fossil record, the evolutionary signature of these events is retained in the history of life preserved in phylogenetic trees.
In addition, the inferred gap between evolutionary origin and paleontological appearance is relatively small compared to the inferred total duration of the derived Metazoa (on the order of ten percent or less). This type of postulated small discrepancy between macroevolution and the fossil record at the grand scale of life may be analogous to the discrepancy at smaller scales such as the divergence of species argued to occur under the punctuated equilibria hypothesis of Eldredge and Gould (1972). The punctuated equilibria hypothesis predicts that speciation events comprise about ten percent of a species' total duration. Further, it posits that very rarely can paleontologists observe speciation in the fossil record; instead, the appearance of a new species in the fossil record represents a migration of that species from other regions where they originated as small, environmentally marginal populations that are unlikely to be preserved in the fossil record. In fact, it was a species' restriction to small population sizes in marginal environments that made them more likely to differentiate and also less likely to be preserved as fossils (Eldredge and Gould, 1972). At the grand scale of initial metazoan cladogenesis this may also have been true, with species restricted to small population sizes in narrow, marginal environments. Again, by analogy, this may have masked their paleontological presence while facilitating their evolutionary diversification.
Finally, the data from trilobites and also other studies (e.g., Budd, 2002) suggest that the gap in timing between the visible manifestation of the Cambrian radiation and the evolutionary diversification of its component fauna, at least for such derived metazoans as the trilobites, is not as profound as some earlier studies had argued. In fact, Budd (2002) argues that the gap is even smaller than the one favored here. For example, Runnegar (1982), Wray et al. (1996), and Ayala et al. (1998) suggested that divergence events we associate with the Cambrian radiation happened back between 670 to 1,200 Ma. Even Darwin (1859, 1872) suggested the diversification seen in the Cambrian radiation should have required a period of time equal to the length of the entire Phanerozoic, which would actually make his estimate for metazoan origins similar to that of Wray et al. (1996). Although these interpretations are still possible, they are not initially supported by the data presented herein or even from other studies deriving from the reanalysis of molecular clock data (e.g., Peterson and Takacs, 2002). Thus, of the two competing legacies of the Cambrian radiation both appear to be vindicated. Data presented here suggest there likely is a gap in the fossil record between the evolutionary origin of Early Cambrian faunas and their appearance in the fossil record, according well with the Darwinian view. An important record of this early Cambrian radiation, however, is preserved in the fossil record, especially in phylogenetic and biogeographic patterns; this accords well with the Simpsonian view. In addition, the implied gap in the quality of the fossil record is not so profound as to obviate the value of the fossil record for addressing macroevolutionary questions in general.
In the end, what will become important to know about the Cambrian radiation and indeed other major evolutionary radiations in the fossil record is why there appears to be a lag between evolutionary origin and paleontological manifestation. It is possible that this lag represents a basic flaw in the fossil record, but it may represent something more significant. For example, in the case of the Cambrian radiation, some have argued that the delay represents the origin of skeletons or some biomineralization event (Kazmierczak et al., 1985), although Bengston (2002) has presented cogent arguments against this. Moreover, the trace fossil record also does not support this interpretation (Crimes, 1992; Fedonkin, 2002; Jensen, 2002). (Note though, this explanation could not in any event apply to other radiations preserved in the fossil record.) It is possible that the Cambrian radiation represents the origins of large size in several metazoan lineages as Davidson et al. (1995) argued. Finally, this apparent discrepancy between evolutionary origin and paleontological emergence may have something to do with the interplay of diversity dynamics. Perhaps a group's probability of becoming visible in the fossil record depends on its attaining a level of diversity; especially when speciation rates are low for whatever reason or speciation and extinction rates are nearly identical at low diversity levels, groups will not reach sufficient levels of diversity to be seen typically in the fossil record. Instead, maybe events like the Cambrian radiation or even the Cenozoic radiation of mammals represent times when speciation rates quite suddenly outstripped extinction rates. At least in the case of the Cambrian radiation, this may have been caused by geological changes including continental rifting leading to multiple episodes of vicariance (Lieberman, 1997) or ecological opportunities (Conway Morris, 1993, 2000, 2002). These processes, acting alone or in concert, may have allowed diversity levels to rise and groups to reach levels where they became in a sense paleontologically emergent. In any event, it is clear that the analysis of the fossil record will continue to yield insight into the nature of the Cambrian radiation and evolutionary radiations in general.
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ACKNOWLEDGMENTS |
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I thank G. Budd and K. Peterson for inviting me to participate in the 2002 SICB symposium on the Cambrian explosion. Thanks to N. Hughes, R. Kaesler, R. Robison, A. Rowell, and an anonymous reviewer for comments on earlier versions of this paper. This research was supported by NSF OPP-9909302, EAR-0106885, and a Self Faculty Fellowship.
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FOOTNOTES |
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1 From the Symposium The Cambrian Explosion: Putting the Pieces Together presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 2–6 January 2002, at Anaheim, California.
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