Micro- and Macroevolution: Scale and Hierarchy in Evolutionary Biology and Paleobiology Author(S): David Jablonski Source: Paleobiology, Vol

Paleontological Society

Micro- and Macroevolution: Scale and Hierarchy in Evolutionary Biology and Paleobiology Author(s): David Jablonski Source: Paleobiology, Vol. 26, No. 4, Supplement (Autumn, 2000), pp. 15-52 Published by: Paleontological Society Stable URL: http://www.jstor.org/stable/1571652 Accessed: 28/10/2008 17:29

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Micro- and macroevolution: scale and hierarchy in evolutionary biology and paleobiology

David Jablonski

Abstract. -The study of evolution has increasingly incorporated considerations of history, scale, and hierarchy, in terms of both the origin of variation and the sorting of that variation. Although the macroevolutionary exploration of developmental genetics has just begun, considerable progress has been made in understanding the origin of evolutionary novelty in terms of the potential for coordinated morphological change and the potential for imposing uneven probabilities on different evolutionary directions. Global or whole-organism heterochrony, local heterochrony (affecting single structures, regions, or organ systems) and heterotopies (changes in the location of developmental events), and epigenetic mechanisms (which help to integrate the developing parts of an organism into a functional whole) together contribute to profound nonlinearities between genetic and morphologic change, by permitting the generation and accommodation of evolutionary novelties without pervasive, coordinated genetic changes; the limits of these developmental processes are poorly understood, however. The discordance across hierarchical levels in the production of evolutionary novelties through time, and among latitudes and environments, is an intriguing paleontological pattern whose explanation is controversial, in part because separating effects of genetics and ecology has proven difficult. At finer scales, species in the fossil record tend to be static over geologic time, although this stasis-to which there are gradualistic exceptions-generally appears to be underlain by extensive, nondirectional change rather than absolute invariance. Only a few studies have met the necessary protocols for the analysis of evolutionary tempo and mode at the species level, and so the distribution of evolutionary patterns among clades, environments, and modes of life remains poorly understood. Sorting among taxa is widely accepted in principle as an evolutionary mechanism, but detailed analyses are scarce; if geographic range or population density can be treated as traits above the organismic level, then the paleontological and maCroecol- ogical literature abounds in potential raw material for such analyses. Even if taxon sorting operates on traits that are not emergent at the species level, the differential speciation and extinction rates can shape large-scale evolutionary patterns in ways that are not simple extrapolations from short- term evolution at the organismal level. Changes in origination and extinction rates can evidently be mediated by interactions with other clades, although such interactions need to be studied in a geographically explicit fashion before the relative roles of biotic and physical factors can be assessed. Incumbency effects are important at many scales, with the most dramatic manifestation being the postextinction diversifications that follow the removal of incumbents. However, mass extinctions are evolutionarily important not only for the removal of dominant taxa, which can occur according to rules that differ from those operating during times of lower extinction intensity, but also for the dramatic diversifications that follow upon the removal or depletion of incumbents. Mass extinctions do not entirely reset the evolutionary clock, so survivors can exhibit unbroken evolutionary continuity, trends that suffer setbacks but then resume, or failure to participate in the recovery.

David Jablonski. Department of Geophysical Sciences, University of Chicago, 5734 South Ellis Avenue, Chicago, Illinois 60637. E-mail: [email protected]

Accepted: 18 July 2000

Introduction heralds a more profound integration of evolutionary biology, paleobiology, systematics, The landscape of evolutionary biology has ecology, and developmental biology. What- changed significantly over the past quarter- ever the intellectual forebears of these ideas century. Evolutionary and ecological studies (and some of their roots are very deep), the now regularly incorporate serious consider- growing number and diversity of studies that ations of history, scale, and hierarchy. This ex- directly address such factors as intrinsic con- pansion of the working toolkit of the disci- straints, phylogenetic effects, differential orig- pline-the near-routine application of ideas ination and extinction rates, and local vs. re- that were once barely developed, highly ab- gional effects represent a true operational ex- stract, or in some circles outright anathema- pansion of evolutionary theory. As a window

? 2000 The Paleontological Society. All rights reserved. 0094-8373 / 00/ 2604-0002 / $1.00 16 DAVID JABLONSKI onto a wide range of spatial and temporal awareness has been somewhat lost in the em- scales, including extreme events not accessible pirical evidence from quantitative genetics to neontological study, paleontology is play- that many traits are underlain by a large num- ing a vital role in this expansion and will cer- ber of genes of small and mainly additive ef- tainly continue that role in the coming de- fect. However, intensive study of developmen- cades. tal processes in multicellular organisms has This is by no means to declare the demise led to a new appreciation of how modest ge- of the highly successful microevolutionary netic changes can be amplified and channeled paradigm, which is alive and well, but rather developmentally to yield significant variations to say that the study of evolution continues to in the magnitude and direction of phenotypic evolve and expand conceptually, and increas- change. We are only beginning to understand ingly incorporates approaches that explicitly how and when to apply this expanding set of emphasize scale and hierarchy. These ap- approaches to the origin of novel morpholo- proaches, even those that can be traced back gies (and the absence or rarity of certain to Darwin, were barely visible when Tom forms), but few would deny the potential to Schopf and Ralph Johnson were mustering both illuminate and be illuminated by the fos- support for a new journal to be titled Paleobi- sil record of morphological evolution-not ology. Paleontology was one of the fields that least because, as discussed below, that record provided a phenomenology, a conceptual exhibits nonrandom patterns in space and base, and a battery of new quantitative meth- time. ods, that fostered the expansion of evolution- Genetic Control and Networks ary theory in the first quarter-century of this Pathways journal. At one extreme in the nonlinearities be- One way to survey the infusion of hierarchy tween genotypic and phenotypic change are and scale into evolutionary biology is through the high-level regulatory genes now under in- the classic darwinian two-step process: the or- tense study by molecular developmental bi- igin and the sorting of variation. Other ologists. Some of these genes, such as the Hox schemes are possible, of course, from the in- clusters that help to pattern the body axis and trinsic/extrinsic dichotomy of causal mecha- appendages across the entire breadth of meta- nisms (e.g., Gould 1977a; Jablonski 2000a) to a zoan diversity, specify positional information nested set of temporal and spatial scales (e.g., and thereby regulate the transcription of a Gould 1985; Bennett 1997), and those elements large number of downstream genes. Others sit will inevitably appear here as well. near the top of a regulatory cascade, or perhaps more commonly within a regulatory net- of Variation Origin work, that determines a specific tissue or The origin of heritable variation, the raw structure. For example, perhaps 2500 genes material of the evolutionary process, is by def- are involved in building and maintaining the inition a matter of genetics. One major issue Drosophila eye (Halder et al. 1995; 18% of the in bridging scales and hierarchical levels, fly's genome by Adams et al.'s [2000] count, al- however, has been the correspondence be- though of course many are also used else- tween genotypic changes and the magnitude where), but experimental manipulation of a and direction of phenotypic transformation. A single gene-most famously eyeless, but also reasonable assumption underlying most mod- eyes absent, dachshund, and others-can yield els of evolution has been that the probability well-formed eyes in the middle of wings and of a phenotypic change is inversely related to other improbable sites (see reviews by Gehr- the complexity or magnitude of the genetic ing and Ikeo 1999 and Hodin 2000; and see change required to generate it (among other Chow et al. 1999 for similar results in the frog factors, of course). Geneticists have long rec- Xenopus). Such high-level regulatory genes ognized that mutations of equal magnitude and even entire signaling pathways have been can have strikingly different phenotypic con- recruited as modular units ("cassettes") in the sequences depending on context, but this service of novel morphologies. Thus, the MICRO- AND MACROEVOLUTION 17 hedgehog pathway that underlies the genera- Shubin et al. 1997; Weatherbee et al. 1999), tion of limbs also participates in the produc- morphological transitions of vertebrae along tion of eyespot patterns on butterfly wings the spinal column (Burke et al. 1995; Belting et (Keys et al. 1999); the Toll pathway has been al. 1998), the origin and diversification of tet- recruited to the development of chick limbs, rapod limbs (Shubin et al. 1997; Coates and the operation of the vertebrate immune sys- Cohn 1998), and the suppression of those tem, and the development of ventral structure limbs and the homogenization of vertebral in Drosophila (Gonzalez-Crespo and Levine morphology along the body axis of snakes 1994; Ghosh et al. 1998), and even the "master (Cohn and Tickle 1999; Greene and Cundall control gene" for eyes, Pax-6, plays multiple 2000). Vertebral identity and digit size and roles (e.g., Quinn et al. 1996; Duboule and Wil- number appear to be dose-dependent func- kins 1998; Hodin 2000; and see Heanue et al. tions of Hox gene products (Zakany et al. 1999 and Relaix and Buckingham 1999 for an 1997), providing a mechanism for selection on analogous situation involving Pax-3). high-level regulatory factors within popula- Many of the major molecular components of tions, and thus a pathway for coordinated metazoan development appear to have arisen change effected by major genes but in a poly- very early and been retained across taxa with morphic population rather than a strictly ty- very different bodyplans of varying complex- pological context. Similar situations, again ity (reviews in Finnerty and Martindale 1998; underlain by polymorphisms in regulatory Erwin 1999; Valentine et al. 1999; Holland genes, have been recognized by plants as well 1999; Knoll and Carroll 1999, among others); (e.g., Purugganan 1998, 2000; Lawton-Rauh et although data are sketchier, the same appears al. 2000). to hold for plants (Purugganan 1998; Lawton- These are very early days in the macroevo- Rauh et al. 2000; Theissen et al. 2000). The ex- lutionary exploration of developmental genet- traordinary conservation (albeit in a highly ics. Careful study is needed in the inference of dynamic fashion involving gene loss, gain, causal, evolutionary relationships between and duplication) and the multiple expression variations in Hox expression and morpholog- events and sites of these genes strongly sug- ical differences among taxa (e.g., Rogers et al. gests that the evolutionary action at this level 1997). And the next step, taking insights de- is in the enhancer regions that govern the tim- rived from laboratory populations into natu- ing and intensity of gene expression (see Ar- ral evolutionary processes, has just begun. none and Davidson 1997 for an excellent re- Gibson et al. (1999) found that crossing mu- view). The evolutionary impact of changes in tants of the Hox genes Ubx and Antp into nat- the major regulatory genes will therefore be ural populations of Drosophila could evoke a more complex than the extreme binary effects wide range of extreme phenotypes whose ex- suggested by the homeotic mutants that pression depended on the overall genetic con- abruptly transform segment identities. In- text of the mutation, again showing how stead, that impact should probably be visual- large-effect genes might impinge on morpho- ized in terms of finer modulations in the ex- logical variation generated in the wild. More pression of major regulatory genes, and there- speculatively, DeSalle and Carew (1992) attri- fore should include evolutionary changes that bute some of the morphological extremes seen do not depend on the viability of extreme sal- in Hawaiian drosophilid species, such as gro- tations and lone individuals (Gellon and tesquely reshaped heads and bizarre mouth- McGinnis 1998; Akam 1998; Duboule and Wil- part appendages, to mutations in Hox genes kins 1998; Purugganan 1998, 2000; Gibson because of their resemblance to Antp mutants 1999; Li and McGinnis 1999; Ludwig et al. in laboratory D. melanogaster-an attractive 2000). Possible examples of striking morpho- hypothesis that invites direct molecular study. logical changes that may have involved rela- Nevo et al. (1992) reported apparent Hox gene tively subtle shifts in Hox expression patterns polymorphisms that significantly correlated include the evolutionary differentiation of ar- with a wide array of morphological variables thropod appendages (Averof and Patel 1997; in the mole rat Spalax ehrenbergi,an early, pro- 18 DAVID JABLONSKI vocative result that needs further work. On ing polygenic changes (e.g., McKenzie and the other hand, Ahn and Gibson (1999a,b) Batterham 1994). The growing weight of evi- found intraspecific variation in expression do- dence suggests that genetic differences even mains of Hox genes along the body axis of the among closely related taxa often involve genes three-spined stickleback, but this variation did of large effect that in the few cases of func- not correlate with phenotypic variation. Fi- tional analysis are involved in regulating de- nally, considerable within-species variation velopment (e.g., Doebley and Lukens 1998); has been recorded for a number of major de- corroboration for this view has been found in velopmental genes in natural and domesticat- a number of "candidate loci" identified ed plant populations, and several dramatic in- through mutations that are then mapped to traspecific variants have proven to be under- QTLs accounting for natural variation in pop- lain by high-level developmental genes (for ulations (e.g., Long et al. 1996; Mackay 1996; overview see Lawton-Rauh et al. 2000). Nuzhdin et al. 1999). This calls for a more Evolution via changes in Hox-gene expres- complex treatment of the raw material for evo- sion is hardly a prerequisite for a strong non- lutionary change, and for new models of how linearity between genetic and phenotypic this raw material can influence the direction or change, of course, and both theory and evi- pace of evolution, in concert with more tra- dence are accumulating that genes of large ef- ditional parameters like population size or fect-many of them presumably involved in structure-models that can be applied, tested, regulating development-do play a role in the and refined paleontologically in many in- origin of adaptations and the divergence of stances. One potential avenue might be to use species (e.g., Gottlieb 1984; Orr and Coyne neontological data on a well-fossilized group 1992; Palopoli and Patel 1996; Orr 1998). Much to pinpoint some of the phenotypic changes empirical work is still needed, of course, but most likely to be underlain by large-effect an absolutely micromutational view of evolu- genes, and then to test whether those changes tionary change in natural populations seems can predict the evolutionary trajectories of increasingly untenable even for quantitative clades in the fossil record. The interplay of traits that are often seen as the bastion of the evolutionary factors mentioned above might "many genes of equal and infinitesimal ef- be assessed in a comparative framework in fect" approach championed by R. A. Fisher. which several related clades are targeted that One recent surprise, for example, has been the differ in such features as genetic population number of studies reporting quantitative trait structure (see below for paleontological ap- loci (QTLs) of large phenotypic effect in both proaches to this parameter). laboratory and natural populations (Orr 1998: and p. 936; see also Paterson et al. 1997; Voss and Heterochrony Heterotopy Shaffer 1997; Doebley and Wang 1997; Brad- Heterochrony, a change in the rate or timing shaw et al. 1998; Schemske and Bradshaw of developmental events, has received much 1999; Goffinet and Gerber 2000). QTL analy- attention as a potential avenue to dramatic ses have their limitations, of course: they are morphological evolution. As Klingenberg only feasible among species or morphs that (1998) points out, the pervasiveness of heter- can be hybridized, they may not permit an ab- ochrony hinges on its definition. Developmen- solute determination of the numbers of genes tal biologists restrict heterochrony to changes involved in important traits because minor in the relative timing of developmental events, factors may not be detected, and they can even emphasizing the dissociation between devel- be biased toward artificially inflating the ef- opmental units (e.g., Raff and Wray 1989; Raff fects of single QTLs or underestimating the 1996; Hall 1999), while evolutionary biologists number of genes involved in complex traits and paleontologists have used a broader def- (Routman and Cheverud 1997; Lynch and inition that also includes changes in the rela- Walsh 1998: p. 474-476; Via and Hawthorne tive rates of developmental processes even 1998). On the other hand, laboratory selection when the order of events is unchanged (e.g., experiments can be biased toward document- Gould 1977b; Alberch et al. 1979; McKinney MICRO- AND MACROEVOLUTION 19 and McNamara 1991). Further difficulties are stay in their aquatic neighborhoods, yielding imposed by the hierarchy of biological orga- lower rates of gene flow, and thus potentially nization: changes in timing at the molecular or higher speciation rates compared with meta- cellular level need not produce heterochronic morphosing relatives free to travel among patterns at the whole-organism level, and the ponds. Similarly, selection for small body size heterochrony at the organismal level need not per se, energy economy, or short generation involve changes in the timing of molecular time in benthic invertebrates can evidently events (e.g., some salamanders owe their pae- give rise to paedomorphs that are so small domorphosis simply to the disabling of the that they must evolve a low-dispersal, non- production or reception of the hormone thy- planktotrophic mode of development due to roxin, which is closer to a binary switch than fecundity constraints (see Jablonski and Lutz a change in timing). 1983; Lindberg 1988); such a change in devel- Global or systemic heterochrony-in which opmental mode would in turn be likely to re- the entire phenotype is shifted relative to the sult in high speciation and high extinction ancestral ontogeny-has the greatest evolu- rates at the clade level, as discussed below tionary potential, and is most readily detect- (and see experiments showing that selection ed, in species that undergo substantial phe- on egg size can in turn alter other aspects of notypic changes during ontogeny. Both con- larval biology, such as those of Sinervo and tinuous but nonlinear changes such as onto- McEdward [1988] and Emlet and Hoegh- genetic allometry and saltational changes such Guldberg [1997]). Again, this intriguing inter- as metamorphosis (as in the classic example of section of micro- and macroevolution, where neotenic salamanders that mature in the life-history theory meets heterochrony (an im- aquatic larval state) provide ample raw mate- portant but neglected insight in Gould 1977b; rial for dramatic evolutionary events. This im- see also McKinney and McNamara 1991; Mc- plies a little-explored predictive approach to Kinney and Gittleman 1995), would produce differences in morphological diversification dramatic shifts not only in morphology but in among clades, based on the nature of ancestral evolutionary dynamics. ontogenies. This might involve, for example, Although global or systemic heterochrony testing how well the ontogeny of individual has enjoyed the most attention, local or spe- organisms can predict the extent of morpho- cific heterochrony has been much more com- logical diversification of their descendant mon (e.g., McKinney and McNamara 1991). clades, a macroevolutionary equivalent of Such changes in the rate or timing of devel- Wayne's (1986) classic conclusion that the opment of particular structures within an or- great array of morphologically extreme dog ganism can break allometric relationships and breeds relative to cats is a consequence of their generate new and coordinated morphologies, contrasting ontogenetic allometries (see also again by drawing on established developmen- Wayne and Ostrander 1999). tal interactions but this time within a localized The preceding example represents just one region or developmental field. For example, way in which the evolution of development at the most successful crinoids in modern the individual level might indirectly shape oceans, the stemless, mobile comatulids, were large-scale patterns. Selection on life-history derived from the stemmed crinoid order Iso- traits over ecological timescales, which as crinida; intermediates such as Eocomatulaand Gould (1977b) notes can often result in het- Paracomatulasuggest progressively earlier off- erochrony, can also have far-reaching, indirect set of stem formation, with the substratum- macroevolutionary effects, for example via gripping cirri, which adorn the long stem in changes in genetic population structures. For the isocrinids, finally arising from a single example, populations of obligate paedomor- centro-dorsal ossicle on the base (Simms phic ambystomatid salamanders are geneti- 1988a,b, 1994; Hagdorn and Campbell 1993). cally more distinct from one another than are In mammals, the ossification of facial bones is metamorphosing populations (Shaffer 1984). accelerated relative to the central nervous sys- Presumably the obligate paedomorphs tend to tem in marsupials compared with both mono- 20 DAVID JABLONSKI tremes and placentals, correlated with the an expanded definition that may include vir- particular demands of neonate survival, in- tually every developmental change that is not cluding head movements during migration to narrow-definition heterochrony (see Klingen- the pouch, attachment to the teat, and suckling berg 1998: p. 83), spatial changes in develop- (Smith 1996, 1997; Nunn and Smith 1998). mental events can certainly give rise to novel Such localized developmental changes, from morphologies, as in the shifting of the scapula the elongation of pterosaur digits to support a from outside to inside the ribcage in turtles wing to the elongation of echinoid plates to (Burke 1989, 1991). Hall (1999: p. 388) goes so create a protruding rostrum, represent coor- far as to say, "heterochrony tinkers, but het- dinated changes in suites of complex tissues. erotopy creates" and to anticipate that "het- Such dissociation and reintegration among lo- erotopy may be about to come into its own as cal growth fields is still poorly understood but heterochrony wanes and our knowledge of de- permits an enormous range of morphologies velopmental mechanisms increases." This to be tapped by alterations of local growth may be selling heterochrony a bit short (Hall fields. This does not mean that phenotypes are goes on to note the intimate connections be- infinitely malleable, but that the scope for evo- tween heterochrony and heterotopy), but the lution via heterochronies of existing morphol- recognition that the evolution of development ogies is far wider than implied by global het- involves more than just heterochrony-also erochrony alone. being driven home by molecular work on gene Calibration of ontogenetic trajectories regulation-is welcome. And, continuing one against better metrics than the convenient but of the themes of this section, heterotopy is an unreliable size criterion will be important for effective evolutionary mechanism because, rigorous analysis of local and global heteroch- like heterochrony, it draws on preexisting de- rony, particularly if life-history parameters velopmental pathways and components: the are potential targets or by-products of selec- spatial reordering of the turtle skeleton is tion. Fortunately, this can be achieved in pa- striking by any measure, but the turtle tucks leontological material where accretionary its scapula, identifiable as such during mor- growth leaves internal growth lines and a sta- phogenesis, under its ribcage rather than ble isotope record that can be calibrated at the evolving a novel structure. level of monthly, seasonal, and annual peri- odicities (e.g., Jones 1988, 1998). In some taxa Epigenetics these can be tied to onset and perhaps fre- Local heterochronies and heterotopies are quency of reproduction, because reproductive effective evolutionary agents because of an- growth interruptions can often be distin- other aspect of developmental systems that guished from disturbance checks (Kennish contributes to the nonlinearities between ge- 1980; Harrington 1987; Sato 1995, 1999). Such netic change and morphological effect: epi- skeletal chronometers have been used exten- genetics in the classical sense, i.e., the local cell sively in ecological studies of bivalves, but and tissue interactions that help to integrate will be extremely valuable in evolutionary ap- the developing parts of an organism into a plications (for an exemplary study, see Jones functional whole (for example the induction of and Gould 1999). vertebral cartilage formation by contact with A final mechanism for coordinated mor- the spinal cord [Hall 1983] or the growth re- phological change is heterotopy, or alteration sponse of both embryonic and postnatal bone in the location of a developmental event. Het- to mechanical loading [Carter et al. 1998]). By erotopy has received much less attention than drawing on a set of preprogrammed respons- heterochrony, but some authors have argued es to local signals, such interactions allow the that spatial changes in development may developing embryo to accommodate evolu- prove to have greater evolutionary impact tionary changes in particular morphological than temporal ones (e.g., Raff 1996; Zelditch elements without a host of independent but and Fink 1996; Hall 1999). Although this per- mutually beneficial mutations. We have little ceived frequency is in part a consequence of detailed knowledge of mechanisms, but strik- MICRO- AND MACROEVOLUTION 21 ing epigenetic responses to experimental al- lular, and tissue levels. The challenge is to take terations in morphology have been described these new insights from the organismal level by many workers, and their evolutionary im- to the population, species, and clade level to plications abundantly discussed (reviews in- forge a better understanding of the links and clude Rachootin and Thomson 1981; Raff and discontinuities among those levels. Kaufman 1983; Thomson 1988; Atchley and A synthesis of developmental and popula- Hall 1991; McKinney and McNamara 1991; tion genetics will not be easy, as R. A. Fisher Hall 1999). Those experiments show that evo- himself recognized ("I can no longer calculate lutionary changes in, for example, eye size it," he said when confronted with early evi- need not be accompanied by independent mu- dence for nonadditive genetic variation [Mayr tations in genes governing bones, nerves, mus- 1992]). A general mathematical theory may cles, or blood vessels in the skull (see Twitty's not much resemble our textbook versions of famous transplant experiments reviewed by microevolutionary population genetics or Muiiller 1990), and changes in vertebral pos- quantitative genetics but will contain elements ture need not involve independent mutations of both. Various, rather disparate, pioneering in genes that collectively control thoracic attempts suggest some potential components cross-sectional shape or the sites of muscle in- of such a program (e.g., Arthur 1988, 1997; sertions on limb bones (see Slijper's bipedal Atchley and Hall 1991; Atchley et al. 1994; goat, reviewed by Rachootin and Thomson Schluter 1996; Nijhout and Paulsen 1997; Wag- 1981), because epigenetic interactions yield ac- ner et al. 1997; Orr 1998; Rice 1998). Given that commodations to those morphological chang- our knowledge of the genotype-phenotype es. relation is still heavily biased toward labora- The epigenetic interactions that help gen- tory strains of a few model organisms, far erate complex forms do have limits to the more extensive analysis of natural popula- changes they can accommodate, as attested by tions will be a critical step whose early phases many "failed" embryological manipulations were noted in the section on genetic hierar- or the more bizarre gene regulation experi- chies and networks, above. ments that haunt the pages of Nature, Cell, and A discouraging possibility is that so much similar journals. The macroevolutionarily im- taxon-specific information will be required portant questions revolve around where those that quantitative models, or even qualitative limits lie for particular clades or particular predictions, at the macroevolutionary scale kinds of changes, and how evenly the poten- will have little power. However, the strong tial directions of permissible change are dis- commonalities among phyla in basic devel- tributed in morphospace. An approach along opmental genetics hold out some hope, and those lines will help to illuminate how two of certain differences among clades suggest the seemingly conflicting themes of develop- some simple hypotheses that might be ex- ment, modularity, and integration-at several plored. For example, protostomes have hierarchical levels within the organism from evolved the genetic machinery for generating molecular pathways to tissue inductions- complex morphologies by keeping genomes conspire to produce evolutionary novelty. relatively small and increasing the number of times a gene is used during development, Wanted: An Genetics Integrated whereas deuterostomes have enlarged the ge- All of these aspects of genetics strongly un- nome by two rounds of duplication so that derscore the nonrandom and nonlinear nature multiple copies of a given gene are available of variation that is the raw material for evo- to diverge functionally (Akam 1998; Holland lution. Any probability distribution of poten- 1999; Valentine 2000; among many others). Do tial changes around a genotype (phenotype) these differences in genetic architecture im- will inevitably be inhomogeneous, reflecting pinge on phenotypic evolution to produce dif- evolutionary lines of least resistance that are ferences in evolutionary style between the two conditioned by the underlying structure of de- main metazoan branches (e.g., in dissociabil- velopmental pathways at the molecular, cel- ity of structures-that is, the relative degree of 22 DAVID JABLONSKI developmental independence of structures or Temporal and Spatial Variation in the Origin organs within bodies, styles of heterochrony of Novelties or The two architectures heterotopy, etc.)? Given the in which to be from many ways develop- may prove functionally equivalent mental can a but demon- changes generate evolutionary macroevolutionary perspective, novelties, the that as macroevolutionary expectation strating they generate qualitatively be that novelties arise ac- well as similar variation would might stochastically quantitatively to and be Whether cording clade-specific pressures op- equally interesting. phenotypic The nonrandom first evolution is or discontinuous when portunities. highly ap- gradual of novelties in the fossil record thus rise to mor- pearances regulatory changes give major an de- novelties is still present intriguing challenge. Although phological utterly uncertain, bate continues on the mechanisms behind and on the of char- probably depends types these and more work is acters involved. Reasonable are patterns, empirical arguments needed, these in available for either and sorely large-scale patterns evolutionary dynamic time and hint at the potential so data rather than will be to space paleon- theory required tological contributions to a of evolu- determine relative theory frequencies. tionary novelty. the and Bridging empirical conceptual gap TemporalPatterns.-The most striking burst between and macro- developmental biology of evolutionary creativity in the animal fossil evolution remains a and fos- challenge. Living record comes early in the Phanerozoic, with sil are all the of organisms products develop- the Cambrian explosion of metazoan body- mental that themselves had to sequences plans. This extraordinary interval, which saw evolve to the diverse forms of and yield past the first appearance of all but one of the pre- taxa, but on the nature present hypotheses sent-day skeletonized phyla (along with an ar- and of those evolutionary impact develop- ray of less familiar forms) in an interval of less mental are difficult to test, and infer- changes than 15 m.y., has received considerable atten- ences on in extinct developmental changes tion recently from both geological and devel- clades can be our rarely precise. Using grow- opmental perspectives. The standing of the of events ing knowledge gene-expression two major explanatory models, one involving for a or crustacean within, example, Drosophila intrinsic, developmental or genomic controls as a basis for the mor- embryo understanding and the other involving extrinsic, environ- diversification of the phological arthropod mental or ecological controls, has varied over a clade (and vice-versa) represents truly the past decade, but resolution has been dif- daunting shift in spatial and temporal scale. ficult (see Erwin et al. 1987; Jablonski and Bo- But here as elsewhere, paleontology has much ttjer 1990a; Valentine 1995; Conway Morris to gain and much to offer. For example, pale- 1998; Erwin 1999, 2000a; Knoll and Carroll ontological comparisons across clades, habi- 1999; Valentine et al. 1999; Jablonski 2000a). tats, or time intervals of the density distribu- The rival hypotheses need not be mutually ex- tions and sequences of novel morphologies clusive, of course, for as Erwin (2000a) notes, around their ancestral starting points can "successful innovations require ecological op- make substantial contributions to under- portunity, developmental possibility and an standing the large-scale consequences of the appropriate environmental setting." The organization of developmental systems. This problem therefore becomes a matter of assess- work will of course be most powerful if done ing which of Erwin's triad of requirements- in concert with actual developmental infor- for example, open ecospace as set by the biota, mation from the clade in question, but pale- intrinsic morphogenetic potential, or by favor- ontology's spectacular array of morphologies able oxygen levels or other physical limiting viewed in historical perspective can lead the factors-was the immediate trigger of the ex- way for a host of new questions and help to plosion. An equally intriguing and no less elu- target organisms for developmental analyses sive problem is to determine which of them likely to yield macroevolutionary insights. damped the production of bodyplan after- MICRO- AND MACROEVOLUTION 23 wards, without actually damping diversifica- noids, although representing a rapid increase tion at lower levels-including further devel- in morphological disparity, yielded a narrow- opmental modifications-so that the produc- er set of architectural novelties than those es- tion of phyla ceased but lower-level taxonomic tablished in their initial, early Paleozoic radi- diversity soared to new heights during the Or- ation. He took this as evidence for less con- dovician, and again in the post-Paleozoic. strained developmental inputs to the Cambri- And of course the trigger might have been dif- an explosion than in later times. Wagner ferent from the damper. (1995) also argued for the lability of different Secondary pulses of evolutionary innova- kinds of traits during the initial and later tion occur in the wake of mass extinctions, phases of Paleozoic gastropod diversification. adding further temporal structure to the ori- These are intriguing results that appear to gin of novelties. These repeated pulses, mea- support a genomic component to the Cambri- sured either as the first appearances of high- an explosion, but they are just a first step, in ranking taxa or increases in morphological part because they lack an explicitly generative disparity, strongly suggest a role for ecologi- or developmental component. For example, a cal opportunity in the origin of novelties (see developmentally based partitioning of traits also below). But is this sufficient to account for to compare the long-term behavior of those the Cambrian explosion, or were genomic fac- that might have been more subject to initial tors also involved? Erwin et al. (1987) rea- freedom and later limitation, relative to those soned that taxonomic diversity but not geno- that might have been subject to earlier en- mic flexibility should have approached Cam- trenchment (as attempted by Jacobs 1990) brian levels after the Permo-Triassic extinc- would be valuable. Pinpointing appropriate tion, allowing a test of the genomic and characters for comparative analysis may not ecological hypotheses. However, they found be straightforward, however. For example, that even the end-Permian debacle, although Hughes et al.'s (1999) finding that the vari- cutting deep into taxonomic diversity, failed ability of thoracic segment number in trilo- to remove major functional groups from the bites depends on the number of segments in a marine biosphere and thus did not sufficiently given species rather than its phylogenetic po- mimic the ecological character of Cambrian sition or geologic age undermines a particular seas for a definitive test. argument (McNamara 1983) but cannot fully Another approach is to sidestep taxonomic address the kinds of regulatory networks that rank and examine the evolution of morphol- were involved in the radiation of arthropod ogy more directly. The rapid filling of a quan- and related clades in the Early Cambrian. titatively defined morphospace has been doc- Instead of focusing on particular characters, umented for a number of clades originating in the role of genomic changes in the damping of the early Paleozoic (see Foote's 1997 review). the Cambrian explosion might be tested by More daunting is the task of quantifying larg- tracking levels of morphological integration er and more heterogeneous groups such as the through the early Paleozoic (Erwin 1994)- deuterostomes or the bilaterians for the pur- that is, the morphometric correlation patterns pose of gaining an overall picture of the de- within an organism (e.g., Olson and Miller ployment of morphological diversity through 1958; Cheverud 1996). This may require a bet- time-but see Thomas et al.'s (2000) analysis ter understanding of developmental mecha- showing that 80% of the theoretical skeleton nisms than presently available, because phe- designs available to living and extinct meta- notypic integration can be stable even when zoans were occupied by the Middle Cambri- genotypic covariances are not (e.g., Turelli an. 1988; Shaw et al. 1995; Schlichting and Pig- Comparative approaches to morphospace liucci 1998). However, Nemeschkal's (1999) occupation can be used to address the rival finding that avian morphometric correlation hypotheses for temporal trends in the origin patterns correspond to the expression do- of novelties. For example, Foote (1999) found mains of Hox and other developmental con- that the post-Paleozoic rediversification of cri- trol genes is encouraging in its implication 24 DAVID JABLONSKI that morphometric matrices can reflect devel- cordance between the diversity dynamics of opmental architecture (see also Leamy et al. marine taxa ranked as phyla and classes rel- 1999). Operational questions aside, the evolu- ative to the very different dynamics of those tionary role of morphological integration ranked as families and genera (see also Erwin needs further theoretical and empirical study: et al. 1987). Such discordances are not simply maximal evolutionary lability may come at an an artifact of the greater inclusiveness of high- intermediate level of integration, where the er taxa (as suggested by Smith [1994], among body is composed of locally integrated units others), because similar patterns emerge from that can behave as modules, as discussed taxon-free analyses of multivariate morpho- above (e.g., G. P. Wagner 1996; Kirschner and logic data (Foote 1993, 1996a, 1997, 1999; and Gerhart 1997). G. P. Wagner (1996) argues that see Lupia 1999 on an early burst of disparity the origin of multicellularity led to an de- followed by stability in angiosperm pollen, crease in integration as regional specialization discordant with species-level diversity). Raup of morphology led to differential gene expres- (1983) essentially recognized this as well by sion, but developmental "burden" is held to noting that the requirements of tree topology increase through time as developmental inter- alone could not account for morphological di- dependencies accumulate (e.g., Riedl 1978; vergences like the Cambrian explosion (that Donoghue 1989). The two perspectives are of is, the topology of the tree cannot account for course potentially compatible, as they may the autapomorphies on each branch). represent very different scales (multicellular- The dynamics of novelty production at low- ity vs. the developmental genetics of a single er levels can be quite unexpected when ex- feature), but they do suggest that this issue amined in detail. For example, Jablonski et al. would be worth exploring in greater depth. (1997) found the production of morphological Although direct comparisons are difficult, a novelties within the bryozoan orders Cyclo- major burst of novel plant architectures is as- stomata and Cheilostomata to be opposite in sociated with the invasion of land (e.g., Niklas timing to that expected from the ecological- 1997; Bateman et al. 1998). We need to develop opportunity hypothesis that is the chief con- criteria to determine whether the establish- tender for explaining high-level originations. ment of the major land plant designs was as Cyclostomes generated novelties in a steady profound an evolutionary event as the Cam- trickle despite their occurrence in the relative- brian explosion, as sometimes suggested. If ly low-diversity early Mesozoic world, where- so, we will probably need to confront the in- as the cheilostomes produced novelties in a trinsic/extrinsic debate here as well: were burst despite being embedded in the presum- plant developmental systems more labile as ably more crowded, predator- and competi- late as the Devonian (in contrast to animal sys- tor-rich mid-Cretaceous environment. In this tems), or is the ecological opportunity afford- comparative study, ecological context mat- ed by the assembly of traits permitting terres- tered less than the relative speciation rates trial existence a sufficient explanation? Recent (and competitive abilities?) of the respective work suggests that the MADS-box genetic ar- clades. chitecture that orchestrates plant development Spatial Patterns.-Evolutionary novelties in ways reminiscent of Hox and other high- also show spatial patterns in their first ap- level regulatory genes in animals were in pearance in the fossil record. Like the major place early in land plant evolution (Theissen temporal patterns, onshore-offshore patterns et al. 2000). show discordances between the first appear- Evolutionary novelties at lower levels exhib- ances of higher taxa and patterns of origina- it very different temporal patterns from major tion, extinction, and diversity accumulation at novelties, and may depend on different vari- lower taxonomic levels: benthic marine orders ables. As made clear by Valentine's (1969, tend to originate in onshore, disturbed habi- 1973, 1980, 1990) seminal work on evolution- tats, regardless of the diversity dynamics of ary and ecological hierarchies in the fossil rec- their constituent species, genera, and families ord, this is immediately evident from the dis- (Jablonski and Bottjer 1990a,b, 1991; Droser et MICRO- AND MACROEVOLUTION 25 al. 1993; Jablonski et al. 1997). Although much et al. 1994], terrestrial plants [Wen 1999]). The more work is needed, this pattern can also be relative fraction of high-latitude origination at seen in terms of derived characters (Jablonski low taxonomic levels has not been sufficiently and Bottjer 1990b is only a crude beginning) quantified to compare with the preferential and in the morphological divergence of the low-latitude appearance of the much smaller founding species for two echinoid orders rel- number of higher taxa, however. Plotting the ative to the disparity among species in the an- mean or median geologic age, or alternatively cestral group, showing how the onshore ini- the estimated net diversification rates, of ex- tiators of these orders "broke away from the tant lower taxa against latitude has given ap- bounds of [their ancestor's] morphospace parently conflicting results (e.g., for marine from the very start" (Eble 2000: p. 68). In ap- taxa [Wei and Kennett 1986; Flessa and Jablon- parent agreement with these patterns, major ski 1996 and references therein; Crame and land plant originations also appear to be con- Clarke 1997], terrestrial birds [Gaston and centrated in disturbed habitats, in both Paleo- Blackburn 1996], birds and butterflies [Car- zoic and Mesozoic settings (e.g., DiMichele dillo 1999]). Violation of assumed time-ho- and Aronson 1992 and Wing and Boucher mogeneous dynamics may be one source of 1998, respectively), although the botanical the conflict, but this entire area deserves more data have not been analyzed for the marine extensive study. discordance across hierarchical levels. Potential mechanisms for spatial biases in The geography of first occurrences of major evolutionary innovation are plentiful but dif- groups is particularly subject to sampling ficult to test, and as with the temporal bias the bias, but an attempt to take these into account jury is still out on whether this is a genetic or found disproportionate appearances of ma- an environmental problem, or even whether rine invertebrate orders in tropical latitudes the pattern is underlain by differential pro- (Jablonski 1993). Similarly, phylogenetic anal- duction or differential persistence of evolu- ysis suggests that major plant lineages tend to tionary novelties (or both). Environmental originate in the Tropics and spread poleward, possibilities include high rates of local extinc- in that primitive members of clades tend to be tion and invasion and thus local opportunity tropical and derived taxa tend to be restricted for innovation, more variable and/or intense to or best developed in the temperate zones selection pressures, or the potential extinc- (e.g., Judd et al. 1994, and in a very different tion-resistance of novelty-bearing species, in tradition, Meyen 1992), although of course dif- more disturbed habitats relative to more sta- ferent dynamics could underlie this pattern ble ones (e.g., Jablonski and Bottjer 1983, (but see also Askin and Spicer 1995 on pale- 1990b; Hoffmann and Parsons 1997). Latitu- ontological data). More work is needed, how- dinal patterns might simply represent diver- ever, to test whether the latitudinal trend in sity-dependent novelty production at this spa- higher-level originations significantly exceeds tial scale, or more complex combinations of the probabilistic, per-taxon expectation, given novelty production and survival to produce that the latitudinal trend in species richness the net effect recorded paleontologically (Ja- appears to have been present over most of the blonski 1993). Phanerozoic, albeit with varying slope and Genetic explanations for these patterns in- subject to considerable sampling and preser- clude the greater potential of small peripheral vation bias (e.g., Stehli et al. 1969; Humphre- isolates-which would arguably be more fre- ville and Bambach 1979; Kelley et al. 1990; quently formed in disturbed, heterogeneous Crame 1996; Walsh 1996). habitats-to have lower developmental stabil- Species and genera show less striking lati- ity or to break developmental canalization tudinal origination patterns, and many clearly (Levin 1970; Jablonski and Bottjer 1983; Clarke started in high latitudes (e.g., macroinverte- 1993; Hoffmann and Parsons 1997). Most re- brates [Feldmann et al. 1993; Crame 1997], cently, Rice's (1998) model suggests that can- Neogene Foraminifera [Buzas and Culver alization might most readily be broken by 1986; Wei and Kennett 1986; Spencer-Cervato strong truncation selection, when significantly 26 DAVID JABLONSKI less than 50% of a population is selected to ski 2000a). These aspects of the evolutionary produce the next generation, a situation that process can also be seen in the sorting of var- might obtain most often with the enormous iation. mortality of propagules in shallow-marine Sorting of Variation benthos (although the selective basis of that Stasis and mortality and its overall impact relative to Species-Level Change mortality in other populations is poorly un- Stasis and Its Causes.-As many authors have derstood [e.g., Rumrill 1990; Pechenik 1999]). pointed out, microevolution can occur as rap- The potential role of highly variable environ- idly as needed to account for virtually any ments in fostering evolutionary innovation speed observed in the fossil record (e.g., Char- (e.g., Parsons 1993, 1994; Hoffmann and Par- lesworth et al. 1982; Gingerich 1993; Kirkpa- sons 1997; Hoffmann and Hercus 2000) has trick 1996; Hendry and Kinnison 1999; and gained a new developmental wrinkle with the many others). This has been abundantly dem- finding that some regulatory molecules that onstrated not only in the laboratory but in nat- suppress phenotypic variation can be disabled ural populations from Galapagos finches not only by mutation but by environmental ex- (Grant 1986; Grant and Grant 1995) to Baham- tremes such as high temperatures (Rutherford ian anoles (Losos et al. 1997) to mosquitoes in and Lindquist 1998; Wagner et al. 1999). the London Underground (Byrne and Nichols The connection between any of these mech- 1999), although as discussed above simple ex- anisms and the empirical macroevolutionary trapolations of these changes may not provide patterns remains highly speculative. However, the best model for all of the inhomogeneities they do suggest testable ways of making in the origins of major novelties. The more mechanistic sense of evolutionary patterns challenging question then becomes, why are that are not smooth extrapolations up the tax- evolutionary rates generally so slow in the fos- onomic hierarchy. Comparative analyses of sil record? This question pertains both to the morphological divergences within and among species level, which is the domain of punctu- clades, structured along environmental gra- ated equilibrium and its alternatives (Gould dients, would be a valuable-and tractable- 1982; Gould and Eldredge 1993), and to the step in this area, particularly because the first clade level, where large-scale evolutionary appearances of most orders are not as diver- trends often unfold with excruciating slow- gent from likely ancestors as are the phyla of ness when viewed on microevolutionary time- the Cambrian explosion. Complementary ap- scales (e.g., Stanley 1979; McShea 1994). The proaches that examine the first appearance of relation between potential mechanisms at the major groups in terms of derived characters or different levels has been discussed mainly in multivariate morphometrics relative to pat- broad generalities, but few workers have at- terns within clades and across environments tempted to address whether the factors that (along the lines of Eble 2000) would be valu- cause, for example, species-level stasis seen in able. many members of the horse lineage (e.g., The discordance between high and low tax- Prothero and Shubin 1989) are also responsi- onomic levels in temporal and spatial patterns ble for the slow rate of body size increase in of origination, and between morphological di- the clade. Averaged over the duration of the versification at different levels within nested entire clade, this size increase was so slow as clades and subclades, thus provides an in- to be virtually indistinguishable from drift triguing set of patterns that require a hierar- (see Lande 1976, and Stanley's [1979, 1982] chical approach. The spatial component also punctuational reinterpretation, seconded by demonstrates that large-scale evolutionary Stebbins 1982; and also Lieberman et al. 1994, processes cannot be analyzed exclusively at who found rates so slow in a Devonian bra- the global scale, because unexpected-or at chiopod lineage that they would have in- least previously undetected-structure re- volved only three selective deaths per 10 mil- sides at the regional scale and across environ- lion individuals if treated as a continuous mental gradients (see also Miller 1998; Jablon- trend). MICRO- AND MACROEVOLUTION 27

Over the past quarter-century, evolutionary interrupted by rapid anagenetic or cladoge- stasis has proven to be a pervasive morpho- netic shifts (maximum observed rates of logical pattern in the fossil record (reviewed change may also be artificially reduced by the in Erwin and Anstey 1995a; Gould and Eld- size of the time bin encompassing both stasis redge 1993; Hallam 1998; Jackson and Chee- and directional change). Less often considered tham 1999). However, few of the hypotheses is the possibility that directional selection fluc- on the forces that maintain this stasis at the tuates so rapidly that populations cannot re- species and higher levels have been conclu- spond, with the net effect of stasis at the mean sively tested and again, different mechanisms phenotype; another alternative would be may obtain in different clades. The research time-averaging of samples rather than selec- questions have shifted to testing for among- tion pressures, detectable if not geologically clade and among-habitat differences in fre- then perhaps by exceptional apparent popu- quencies of evolutionary tempo (abrupt vs. lation variances (see Kidwell and Aigner gradual change) and mode (anagenetic vs. 1985). cladogenetic, sometimes termed phyletic vs. Sustained stabilizing selection must be the branching), the roles of intrinsic and extrinsic force behind habitat tracking as a mechanism factors that might govern those differences, for stasis (Eldredge's 1985, 1989, 1995 hypoth- and whether the direction of phenotypic esis), in which species remain morphological- change during sustained anagenesis or clad- ly static as they move with a favorable envi- ogenesis is related to the morphologic behav- ronment during climatic and other changes. ior of the species or its constituent populations The tracking process seems well supported in during preceding intervals. the Pleistocene (e.g., Valentine and Jablonski Given pervasive stasis, the stunning diver- 1993; Coope 1995; Clark 1998; see also discus- sity and subtlety of biological adaptations sions in Price et al. 1997 and Jackson and Ov- must often arise episodically, in the punctua- erpeck this volume). Intrinsic differences tions between stable species, either in single among taxa in their ability to keep up with punctuational episodes-which, of course shifting environments have not been explored may encompass tens or hundreds of thou- as an explanation for differences in evolution- sands of years (e.g., Jackson and Cheetham ary tempo and mode; this may be unimpor- 1999: Table 1)-or in cumulative series. This tant, however, if we can generalize from rates process need not rely entirely on isolation it- of movement in Pleistocene plants and ani- self as the trigger for adaptive change, but mals (e.g., Clark 1998). For widespread spe- may also draw on geographic variation within cies, a more realistic model might be dine established species. Consider, for example, Fu- translocation (coined by Koch 1986), in which tuyma's (1987) very attractive but still untest- a set of populations that vary along an envi- ed suggestion that speciation events cordon ronmental gradient shift in and out of a sam- off local adaptations into discrete gene pools, pling area to give the appearance of oscilla- thereby packaging ordinarily ephemeral char- tory or even directional change as the species acters into more stable evolutionary units (see overall maintains a constant morphology (see also Eldredge 1989, 1995). The apparently ep- for example Stanley and Yang's 1987 extensive isodic nature of this process, at least in terms study of late Cenozoic bivalves, in which the of the morphologies accessible in the fossil re- total range of multivariate oscillations cord, underscores the need to understand sta- through the history of each lineage was very sis. similar to its present-day geographic varia- At the species level, stasis over geologic tion). timescales has been attributed to variation in Most species-level lineages appear to lack both rate and direction of change. Variation in directionality rather than evolutionary labili- the rate of change involves truly slow evolu- ty; that is, they show high total rates of evo- tionary rates between the punctuations, with lution while accumulating little net change. temporal stability generally attributed to con- The most frequently invoked model is that of stant selection for intermediate phenotypes, oscillating directional selection (e.g., Ginger- 28 DAVID JABLONSKI ich 1993; Sheldon 1996; Hendry and Kinnison racing speeds significantly over the past 70 1999), a process well documented in some years (Gaffney and Cunningham 1988), is not modern populations (e.g., Grant and Grant for lack of intense directional selection or high 1995; Via and Shaw 1996; among many oth- heritability of relevant traits. ers). Such evolutionary dynamics can be mod- Experimental work on host specificity in eled and in principle tested against drift and phytophagous insects suggests that intrinsic other forces, although paleontological appli- factors may be important in wild populations cations are still being developed and in some as well. Many insects exploit a restricted diet, instances seem highly model-dependent (see presumably owing to plants' defensive com- Bookstein 1987, 1988; and Roopnarine et al. pounds, but experiments in some groups have 1999; but see Cheetham and Jackson's [1995] detected no significant relation (or, less often, overview of their superb multidisciplinary a positive relation) between insects' perfor- of A analysis Neogene bryozoan evolution). mance on their host plants and their perfor- hierarchical alterna- less-explored, explicitly mance on other species, undermining a trade- tive involves the structure within spatial spe- offs hypothesis; a lack of genetic variation may cies: flow local gene among highly dynamic actually be a limiting evolutionary factor in within a allow little populations species might this instance (Futuyma et al. 1995; but see net overall change (e.g., Eldredge 1985, 1989; Keese 1998). This is not a trivial issue, given Lieberman et al. molecular 1995). Although Farrell's (1998) contention that the over- and other data that few lack suggest species whelming species richness of beetles is related some internal structure Hanski spatial (e.g., to the macroevolutionary consequences of 1999; Avise it is not clear whether the 2000), host shifts in phytophagous clades. The gen- particular metapopulation dynamics required eral relation between trade-offs, genotypic co- this model for stasis are in by truly pervasive variances, and other apparent limitations to nature S. Harrison 1998; Maurer and (e.g., evolutionary responsiveness on the one hand, Nott 1998). and patterns of morphologic change in species Also controversial is whether the apparent over geologic timescales on the other, is clear- bounds on oscillatory stasis represent intrinsic ly an attractive target for combined paleon- limits of the organisms or reversals in selec- tological/ neontological analysis of particular tion pressure. I am not going to venture into clades. To cut through the terminological mo- the dense and tangled literature of evolution- rass, all of these features can be put under the ary constraints, but the widespread existence rubric of constraints,which of trade-offs (as, for be- developmental might evolutionary example, be defined as the the tween and size at first when resistance, owing to con- age reproduction, of networks and selection favors both early reproduction and figuration developmental of the to selection in cer- large size [e.g., Stearns 1992]) seems to be a pathways, phenotype tain directions. In this can be distin- strong endorsement for some form of intrinsic principle from which be de- constraint, at least in the short run (for mor- guished canalization, might fined as the resistance, to the phological examples, see Nijhout and Emlen owing buffering or of of 1998). The detection of such trade-offs, how- redundancy developmental processes, the to mutation or to environmen- ever, generally carries little information on phenotype tal variation see Gibson and mechanisms underlying constraints, and, as (and Wagner 2000 with genotypic and phenotypic variance-co- for a valuable overview). variance matrices (e.g., Shaw et al. 1995; Ar- Distribution of Stasis and Change.-The dis- nold and Phillips 1999), we do not know how tribution of evolutionary tempos and modes at stable they are over evolutionary time. Some the species level remains poorly known, not must be nearly absolute, others may be quite least because rigorous research in this area is transient and context-dependent. Plant and such a daunting task. Few studies have fully animal breeders hit limits all the time, and the addressed all of the issues, but, drawing on failure to break the egg-a-day barrier in chick- the discussions of Gould and Eldredge (1977), ens (Lerner 1953), or to increase thoroughbred Fortey (1985), Clarkson (1988), Erwin and An- MICRO- AND MACROEVOLUTION 29 stey (1995a), and Jackson and Cheetham and other processes besides the traditional (1999), an appropriate protocol would include isolating barriers may impose or contribute to 1. Large samples in a closely spaced time- evolutionary independence as well (e.g., Van series Valen 1976; Hull 1997; among many others). 2. Objective delimitation of species as op- Analyses within paleontologically impor- erational units tant phyla where morphometrically defined 3. Stratigraphic control independent of the species correspond closely to biologically, target clade usually genetically defined ones include: the 4. Independent evidence on sedimentation cheilostome bryozoans Stylopoma,Steginoporel- and preservation rates that might vary to cre- la, and Parasmittina (Jackson and Cheetham ate artificial punctuations or protracted tran- 1990, 1994, who also used an extraordinary sitions set of breeding experiments, and see also Ha- 5. An assessment of within-species geo- geman et al. 1999); the benthic foraminifer graphic variation Glabratella(Kitazato et al. 2000, also based on 6. A phylogenetic hypothesis breeding experiments; but see below for the The characterization of morphospecies has uncertain situation with planktic Foraminif- become increasingly rigorous with the avail- era); the gastropods Amalda (Michaux 1987, ability of multivariate morphometric meth- 1989, who also found congruent phylogenies ods. An encouraging development has been using both data sets), Nucella (Collins et al. the generally good correspondence between 1996, albeit with considerable intraspecific biological units and the morphospecies of the shell variation), Littorina (Rugh 1997, who shelly macroinvertebrates used in most anal- compared shell morphology with such biolog- yses of evolutionary tempo and mode at these ical species indicators as genital and egg-cap- scales. This is not the place for an extensive sule features), and Lacuna (Langan-Cranford discussion of species concepts, but from an and Pearse 1995, again using breeding exper- evolutionary perspective species-level units iments); the corals Porites (Potts et al. 1993; are most useful if they are essentially inde- Budd et al. 1994, again with congruent phy- pendent lineages (e.g., Simpson 1961; Wiley logenies) and Montastraea(Weil and Knowlton 1981; Mayden 1997; de Queiroz 1998, 1999, 1994; Knowlton et al. 1997); the decapod Syn- and references therein). For the outcrossing bi- alpheus (Duffy 1996, using allozymes); the ar- parental species that provide most of the an- ticulate brachiopod Terebratulina(Cohen et al. imal and protistan fossil record and a sizeable 1991, using both allozymes and mtDNA); and but unknown fraction of the plant record, that even the notoriously nondescript inarticulate independence often involves reproductive iso- brachiopod Glottidia (Kowalewski et al. 1997, lation or genetic cohesion, and so coincides who lacked genetic data and relied on previ- with any broadly defined biological species ous biospecies definitions). One can only hope concept that can accommodate isolation, rec- for a steady stream of such studies, including ognition, cohesion and related viewpoints a new round on vertebrates such as Steppan's (e.g., Templeton 1989, 1998; Ghiselin 1997; work (1998) on the rodent Phyllotis, using Coyne and Orr 1998; R. G. Harrison 1998; de mtDNA versus skeletal morphometrics. Queiroz 1998). However, that evolutionary in- These accumulating results suggest that the dependence need not be compromised even if paleontologist need be at no greater remove those barriers are not absolute (to give just from biological units than any other system- two examples, the fossil record shows that cot- atist lacking a full molecular treatment of the tonwoods and balsam poplars have been gen- taxonomic units under study. And by provid- erating hybrids in western North America ing concrete support for the biological reality since the Miocene but have remained distinct of the morphological differences between re- entities [Eckenwalder 1984] and that two lin- lated fossil species, they imply that the mor- eages of Neogene cyprinid fishes hybridized phological punctuations in fossil lineages-an for 2 m.y. without subverting the evolutionary empirical pattern open to multiple interpre- identities of the parent lineages [Smith 1992]), tations-do tend to correspond to speciation 30 DAVID JABLONSKI events. Anagenetically evolving lineages lack- production among clades (particularly within ing speciation-scale punctuations can be more the same geological arena, so that many po- problematic, of course, and when broken into tential taphonomic biases are held constant), arbitrary taxonomic segments may imply an rather than depending on absolute values. Sig- artificially punctuational pattern (see Sheldon nificant differences detected in comparative 1993). However, this pitfall will be avoided as analyses will be misleading only if the fre- long as phenotypic change is the final arbiter quency of sibling species has a strong inverse on questions of evolutionary tempo and mode relation to the frequency of morphospecies at the species level, as seen in most recent origination. Little or no evidence of such a re- studies including the examples cited here and lation exists, although a formal analysis by Jackson and Cheetham (1999). would be valuable. The sparse literature on On the other hand, sibling or cryptic spe- important components of the fossil record, cies-that is, biological species that are virtu- such as marine invertebrates and terrestrial ally undetectable morphologically-are com- vertebrates, conveys the general impression mon in many taxa, both terrestrial and marine that the numbers of morphospecies and sib- (e.g., Knowlton 1993; Avise 2000). To some au- ling species are, if anything, positively corre- thors, this imperfect correspondence between lated among clades. If this is true, or if the re- morphospecies and biologically discrete spe- lation is random so that no systematic bias is cies dictates the collapse of the entire enter- introduced, then cryptic species will not be a prise (e.g., Levinton 1988; Hoffman 1989), but serious problem for comparative studies of this simply is not true, so long as the questions evolutionary tempo and mode, at least in large are posed appropriately. For example, a line- data sets. age is punctuational if most morphological Geographic variation has been the Achilles' change occurs in the context of speciation heel of many paleontological studies of evo- when viewed over geologic timescales. But lution at the species level. Analyses centered this does not require that the converse be true, on one or a few closely spaced stratigraphic that all speciation events are accompanied by sections or cores risk confounding the lateral morphological change. More problematic is movements of trends in intraspecific variation the generation of temporally and spatially with evolutionary change, the methodological persistent, discrete morphotypes that can pitfall created by the dine translocations men- arise abruptly but are not reproductively iso- tioned above (and the potential for local pop- lated, that is, are not evolutionarily indepen- ulations to exhibit independent morphologi- dent entities (e.g., Palmer 1985; Trussell and cal trajectories without net species-level direc- Smith 2000). The examples cited above sug- tionality adds another hierarchical level to be gest that paleontologists are becoming adept considered [see Lieberman et al. 1995; Bralow- at partitioning their morphological units in er and Parrow 1996]). This problem was rec- ways that are genealogically significant, but ognized over 40 years ago (Newell 1956; Ar- the ranking of discrete morphologies remains nold 1966), but its remedy is generally so labor a potential problem and needs more attention. intensive that only a few studies have risen to The same is true for character-based neonto- the challenge (but see, gratefully, Stanley and logical species concepts, of course, particular- Yang 1987; Cheetham and Jackson 1995, 1996). ly those based on "smallest diagnosably dis- A formidable obstacle is the inverse relation tinct units" (Cracraft 1989, 1997; Nixon and between acuity of stratigraphic resolution and Wheeler 1990; Davis and Nixon 1992; Luckow geographic distance, particularly along envi- 1995), where the taxonomic ranking and evo- ronmental gradients or among disjunct re- lutionary roles of those units also can be con- gions: the temporal acuity often achieved by troversial (e.g., Theriot 1992; Hull 1997; closely spaced samples in a single section de- Knowlton and Weigt 1997; R. G. Harrison clines significantly when correlating among 1998). sections (see Behrensmeyer and Hook 1992 The most robust analyses will be those that and Behrensmeyer et al. 2000 [this volume] on compare rates and patterns of morphospecies analytical time-averaging). This Paleontologi- MICRO- AND MACROEVOLUTION 31 cal Uncertainty Principle-the trade-off be- ord than the alternatives, even though it was tween temporal resolution and geographic long taken to be the dominant style of evolu- coverage-seems to be little appreciated out- tionary change! That said, distinguishing be- side the field but has implications for virtually tween true punctuated equilibrium, i.e., punc- every kind of paleobiological analysis. Quan- tuated cladogenesis, and punctuated anagen- titative stratigraphic methods, significant re- esis, in which morphological change occurs finements in radiometric dating techniques, episodically but without lineage branching, is and tuning of correlations to Milankovitch cy- not always straightforward either. This dis- cles (e.g., Shackleton et al. 1999) will yield in- tinction cuts to the heart of the question of creasingly fine correlations, but resolution speciation's role in evolutionary change: the will tend to approach a limit on the order of anagenetic mode can accommodate a broad thousands of years, if only because natural range of intraspecific evolutionary processes time-averaging operates at about this scale for (e.g., Gould 1982; Wright 1982a,b; Lande 1986; most micro- and macrofossil records (see Kid- and a host of others since then). As noted well and Flessa 1995; Martin 1999). above, however, establishing the coexistence All of the end-member combinations of evo- of ancestor and descendent species, or of mul- lutionary tempo and mode have now been ob- tiple sister species, requires a detailed phylog- served in fossil species transitions, and so the eny and well-resolved stratigraphic range challenge is to assess the frequencies of the endpoints. Like all paleontological analyses it different patterns, and to test for the influence also hinges on the ranking of morphologically of biological traits, environmental factors, and defined units: taxonomic lumpers will tend to other potential controlling variables. This ef- reduce the number of branching events, while fort is complicated by the strong imbalance in splitters are more likely to convert anagenetic the evidence required to demonstrate gradu- patterns to cladogenetic ones by increasing alism versus stasis (see Fortey 1985, 1988; the number of contemporaneous taxonomic Clarkson 1988; Sheldon 1993, 1996; Pearson units. The growing inventory of studies link- 1995; Wagner and Erwin 1995). Stasis can of- ing morphology to genetically defined species ten be convincingly documented by samples suggests that the splitters have been closer to from a succession of discrete sedimentary the biological reality (with past excesses and packages, even when the packages are sepa- missteps, of course). Although some cladists rated by depositional hiatuses or unfavorable have rejected the possibility of identifying an- environments. Further, quantifying geo- cestral species on theoretical grounds (e.g., graphic and other intraspecific variation is less Englemann and Wiley 1977; Frost and Kluge critical if even the local pattern is one of tem- 1994; Norell 1996), increasingly rigorous pro- poral stability. Stasis is unlikely to be artifi- tocols have become available for the recogni- cially generated or removed by time-averag- tion of potential ancestors for both fossil and ing, where successive populations are homog- living organisms (e.g., Paul 1992; Theriot 1992; enized within a single sedimentary bed. Fisher 1994; Smith 1994; Marshall 1995; P. J. Short-term directional changes can be col- Wagner 1995, 1996a; Foote 1996b; Omland lapsed into a single artificially variable assem- 1997). The data are still sparse but suggest that blage, but trends extending over more than ancestral species can be detected and that 10,000 years (depending on depositional en- temporal overlap with descendants, as ex- vironments, of course) and thus significant pected for punctuated cladogenesis, is not un- relative to the average duration of morphos- common. The challenge now is to refine and pecies, will generally be retained, and situa- apply methods that will permit a quantitative tions that would obliterate them can be rec- assessment of when, where, and how often the ognized by independent evidence (e.g., Kid- different evolutionary patterns obtain in na- well and Aigner 1985; Bell et al. 1987; Kidwell ture. A vast and nearly uncharted territory is and Flessa 1995). open for modeling the interplay of sampling Ironically, then, gradualism is more difficult and paleobiological pattern (see Holland and to demonstrate conclusively in the fossil rec- Patzkowsky 1999), but most urgently needed 32 DAVID JABLONSKI is a new battery of carefully designed and se- first, geographic coverage remains a weakness lected empirical studies. of many analyses of pelagic organisms, al- Attempts to assess the relative frequency of though this is becoming less true; second, sta- evolutionary tempo and mode are premature, sis and punctuations do occur in many micro- but some possibilities and problems can be fossil lineages (see tabulations in Erwin and defined. As already noted, stasis and punc- Anstey 1995a and Jackson and Cheetham tuation appear to be the pervasive phenotypic 1999), even when hiatuses are taken into ac- patterns in marine macrofossils, although the count (see MacLeod 1991); and third, so little relative proportions of anagenesis and clado- is known about the population genetics, or genesis remain unclear (e.g., Hallam 1998; even how individuals are packaged into spe- Jackson and Cheetham 1999). Although more cies, in these unicellular groups that interpre- rigorous quantification would be valuable, tation of paleontological patterns is doubly there is little reason to doubt Fortey's (1985) difficult (e.g., Tabachnick and Bookstein 1990; report that gradualism occurs in fewer than Norris et al. 1996; Huber et al. 1997; Darling 10% of the 88 trilobite species that have a et al. 1999, 2000; de Vargas et al. 1999; but see meaningful stratigraphic range in the Ordo- Kitazato et al. 2000 for encouraging results on vician Valhallfonna Formation, Spitsbergen, a genus of benthic forams, and recall that or Johnson's (1985) assessment, backed up by some genetic analyses are finding that de- his data-rich monograph (Johnson 1984), that tailed morphometry of, for example, test po- only one of the 34 scallop lineages in the rosity may help to capture genetic units [e.g., northern European Jurassic shows possible Huber et al. 1997; de Vargas et al. 1999]). gradual change in morphology. On the other The record for land vertebrates is difficult to hand, the famous Jurassic oyster Gryphaea interpret because many studies lack one or shows a more complex mixture of stasis and more of the elements enumerated above (for gradualism (Johnson and Lennon 1990; John- cautionary notes see, for example, Schankler son 1993, 1994), and whether this complexi- 1981; Heaton 1993). Some mammal lineages ty-and contrast with other contemporaneous do appear to present robust examples of grad- bivalves-reflects the intensity of research ualistic change at the species level, however prompted by Gryphaea'snotoriety as a classic (see reviews by Barnosky [1987], Martin evolutionary exemplar, difficulties of phylo- [1993], Chaline et al. [1993], and Carroll genetic analysis in a morphologically difficult [1997]). For example, Chaline and Laurin and heterochrony-prone group, or a true bio- (1986) found gradualism in a Plio-Pleistocene logical difference, remains uncertain. vole lineage over a broad geographic area, Sheldon (1993, 1996) made the intuitively with quantitative data on cheek-tooth mor- appealing suggestion that benthic species in phology in a series of time planes extending more stable offshore environments might be over an area from Spain and Britain to north- more subject to gradual change, but empirical ern Italy, Poland, and the Czech Republic, evidence is slim: Sheldon's trilobite study in- with additional qualitative data from locali- volves parallel changes in a single character in ties as far east as Moldova and western Sibe- a set of lineages from a single restricted area ria. But as with microfossils, mammals are not in which the environment is changing upsec- purely gradualistic in evolutionary tempo; in- tion, albeit subtly (see Sheldon 1987, 1988). deed analyses of entire faunas or assemblages Better documented is the long-standing ob- of clades suggests that stasis and punctuation servation that pelagic species are more likely is pervasive and perhaps prevalent (e.g., Bar- to show gradual change than benthic ones nosky 1987; Flynn et al. 1995; Prothero and (Johnson 1982; Fortey 1985; Clarkson 1988; Heaton 1996). Again the key issue is relative Jackson and Cheetham 1999). Fortey (1985) frequency and the factors that impose differ- contrasts the evolution of a pelagic trilobite ent frequencies among clades. with that of co-occurring benthic species, but Attempts to assess the frequency of differ- the richest data for gradualistic change come ent types of speciation based exclusively on from microfossils. Three caveats obtain here: modern species have their own pitfalls. As MICRO- AND MACROEVOLUTION 33

Wagner and Erwin (1995) note, phylogenetic of homogeneous directional selection, in other tree topology alone cannot reliably distin- words, true Fisherian mass selection, then this guish evolutionary tempo and mode. Infer- sets some requirements on the spatial scale of ences based on molecular data as a source of gene flow relative to that of environmental temporal estimates show considerable prom- variation and thus makes predictions on the ise but remain model-dependent, not only in distribution and genetic structure of gradu- terms of molecular-rate constancy but in as- alistic taxa. On the other hand, for those spe- sumptions about the pattern of morphological cies that maintain genetic cohesion over dif- change between nodes (e.g., Garland et al. ferent environments, or among regions with 1999). Finally, estimates of the relative fre- disparate selective pressures through time, quency of allopatric and other types of speci- the interplay of local adaptation and gene ation based on the present-day deployment of flow-intermittent or regular-will tend to modern species (e.g., Lynch 1989; Barraclough impose fluctuations around a mean rather and Vogler 2000) are undermined by the geo- than directionality (an argument raised by graphic volatility of species in the recent geo- Eldredge 1985, 1989; and also consistent with logic past and by extinction. Only species that Futuyma 1987). Such a return to the textbook have split since the last glaciation, say in the basics could explain why lineages on islands last 10,000 years, are likely to capture the rel- (e.g., Lister 1989) and in isolated basins (e.g., ative spatial distributions of sister species at Geary 1995; and Povel 1993 in part) exhibit the time of speciation. Species that split, say, 2 gradualism while related taxa in more exten- m.y. ago have been subject to perhaps 20 ep- sive or scattered habitats often show stasis and isodes of geographic shuffling with the wax- punctuation. It also provides an approach to ing and waning of Pleistocene glaciation (e.g., the presence of contrasting evolutionary pat- Valentine and Jablonski 1993; Roy et al. 1996; terns in co-occurring lineages, which would Jackson and Overpeck this volume), so that be unexpected if the physical environment the relative frequencies of geographic range alone (e.g., habitat stability [Sheldon 1993, overlap today probably say more about com- 1996]) determined tempo and mode. In our petitive interactions between close relatives present state of ignorance it may even explain than about speciation events (see also Chesser the gradualistic evolution of many planktic and Zink 1994). Taxa separated by major geo- microfossils, which may often evolve as enor- graphic barriers like the Rocky Mountains or mous populations that occupy different depth the Isthmus of Panama are reasonable candi- zones in one or more otherwise relatively ho- dates for allopatric speciation, of course, but mogeneous oceanic water masses (e.g., Laza- these more ancient splits are subject to the rus et al. 1995; but see Norris et al. 1996 and problems of extinct species more closely relat- other foraminiferal references cited above). ed to one or the other living ones-i.e., of in- The Plio-Pleistocene vole data are, however, tervening speciation events that represent the an apparent counterexample: Chaline and true spatial and temporal pattern of lineage Laurin (1986) note with surprise the gradu- splitting (e.g., Schneider 1995; Jackson and alistic trajectory of their lineage despite its Budd 1996). likely subdivision into semi-isolated popula- With all of these caveats, and in light of the tions. This may be the exception that proves sparse and uneven nature of the data, it is un- the rule, however, if the particular phenotypic surprising that no clear taxonomic or environ- changes they measured, involving increasing mental pattern has emerged for the distribu- hypsodonty and elaboration of enamel pat- tion of evolutionary tempo and mode at the terning on the tooth crown, can be attributed species level. Perhaps, in an obvious if unsa- to selection imposed by long-term vegetation tisfyingly context-specific hypothesis, species changes throughout the study area. histories depend on their geographic extent As already noted, the relative frequency of and genetic population structure-i.e., on anagenesis and cladogenesis has yet to be es- scale and hierarchy. If gradual anagenesis is tablished. Intuitively, even excluding "pseu- simply the expected paleontological outcome doextinction" (i.e., anagenetic transformation 34 DAVID JABLONSKI obscured by taxonomy), species extinction (1981) noted, differential rates can drive taxon rates seem to be sufficiently high that frequent sorting even in gradualistic systems depend- branching is required for lineages to persist ing on the extent of variation generated by over geologic timescales. A number of pale- cladogenesis and anagenesis. As in so many ontological analyses of tempo and mode that macroevolutionary questions the issues are consider clades of sufficient size and phylo- the frequency of this sorting among species, genetic resolution for analysis do show signif- the circumstances under which it occurs, and icant numbers of species arising cladogeneti- the nature of dynamics across hierarchical lev- cally, with stratigraphic range overlaps be- els, i.e., identification of focal levels and up- tween putative ancestors and descendants, or ward and downward causation (e.g., Vrba and between sister species (see Erwin and Anstey Gould 1986; and see Grantham 1995 for an es- 1995a; Jackson and Cheetham 1999; also Stan- pecially thoughtful and clear review). ley et al. 1988; Wagner 1998). Nonetheless, all Selection and Related Processes of these references, and many more besides, Species also contain examples of punctuated anagen- The term "species selection" has been used esis, so that the apparent prevalence of stasis in both broad and narrow senses, sometimes in many situations may or may not be by a single author. One approach, drawing on matched by the prevalence of cladogenesis, as the insights of Lewontin (1970) and Hull required by the punctuated equilibrium mod- (1980) and advocated by Vrba and Gould el. Clearly, analyses modeled on the Chee- (1986) among others, is to maintain the neu- tham and Jackson (1995) studies and focused tral term "species sorting" for any pattern on other groups well represented in the fossils shaped by differential origination and extinc- record, say bivalves or gastropods, would be tion. Others would apply the term "species se- valuable. Especially useful in light of the po- lection" here instead because fitness, i.e., dif- tential role of gene flow and its relation to the ferential birth and death, is being expressed at spatial scale of environmental variation would the species level, as the "emergent fitness" of be to track lineages with contrasting evolu- species-speciation and extinction rates- tionary tempo and mode through the Neo- within clades (e.g., Lloyd and Gould 1993; gene fossil record to their present-day popu- Stidd and Wade 1995; Gould and Lloyd 1999). lations. Alternatively, species sorting can be divided into two categories depending on the hierar- Taxon Sorting chical level of the characters that influence The prevalence of intraspecific oscillatory speciation and extinction rates. Then, in "ef- evolution and of evolutionary stasis means fect macroevolution" differential rates are that the direction of speciation is difficult to governed by organismal-level traits such as predict from within-species evolutionary tra- body size or habitat preferences, while in spe- jectories. Further, wherever punctuated clad- cies selection the differential rates are gov- ogenesis is prevalent, long-term evolutionary erned by emergent, heritable properties at the trends will not be simple extrapolations of in- species level (see Vrba 1984, 1989; Jablonski traspecific evolution but instead must involve 1987; Grantham 1995). some form of sorting among species (step- Emergenceand Heritability.-The concept of wise, punctuated anagenesis patterns are less emergence in evolutionary biology has been clear-cut and might also involve sorting difficult, but a simple operational approach is among populations or even highly episodic, to recognize a feature as emergent at a given species-wide changes propelled entirely at the level if its evolutionary consequences do not organismic level). That such differential spe- depend on how the feature is generated at ciation and extinction rates among clades lower levels. (This approach is similar to Bran- might in principle shape large-scale evolu- don's 1982, 1988 application of Salmon's 1971 tionary patterns appears to be generally ac- statistical concept of "screening-off," and to a cepted (e.g., Sober 1984; Maynard Smith 1989; parallel view, "multiple realizabililty," that re- Williams 1992). Equally important, as Slatkin cently has been criticized as insufficiently pre- MICRO- AND MACROEVOLUTION 35 cise in some circumstances; for discussion see level: the existence of heritable variation in a Sober 1999; Sterelny and Griffiths 1999.) A feature that, by interaction with the environ- classic example at the organismal level in- ment, imparts differential success. Cheetham volves selection experiments in Drosophila and Jackson (1996) also found widespread where Robertson (1959) concluded that equiv- species of bryozoans to be geologically long- alent changes in wing size could be achieved lived relative to restricted species; in fact their either by changes in cell size or by changes in widespread species, taken as occupying >4 cell number, with variance in wild popula- regions, have a median duration of about 7.5 tions usually owing mainly to cell number, m.y. while the narrowly distributed species a and in his experimental groups mainly to cell median duration of about 2 m.y., each re- size (see also Stevenson et al. 1995). As the or- markably close to the high- and low-dispersal ganism was the focal level of the experiment, molluscan species, respectively, as cited the large-winged phenotype was the emer- above. But here the differences in geographic gent property under selection, and not the cel- ranges presumably derive from the rafting of lular or genetic levels underpinning the evo- adults (e.g., Watts et al. 1998). Thus, differen- lutionary changes. Outside the lab, evolution tial taxonomic survival depends on the emer- of the emergent organismal property of DDT gent, species-level property, i.e., the scale of resistance is underlain by many alternative re- the species' range and not on the underlying sponses at the cellular level, from changes in organismal traits. cell walls that exclude the DDT molecule, to Genetic population structures, again not a changes in cell metabolism that neutralize property of single organisms, can be viewed DDT when it penetrates the cell, to changes in in the same way. Jablonski (1986a, 1995) attri- cell physiology that sequester DDT before it buted high per-taxon speciation rates seen in can be effective (e.g., McKenzie and Batterham gastropod lineages having low larval dispers- 1994; Feyereisen 1995). al ability, as inferred from their larval shells, By the same token, geographic range is an to their genetically fragmented populations emergent property at the species level, not (an argument broadly supported by genetic simply because most geographic ranges are analyses of benthic marine invertebrates [see determined by the overall distribution of con- Pechenik 1999; Bohonak 1999]). Similarly, Wil- specifics rather than by the movements of sin- son et al. (1975) suggested that mammals with gle bodies, but also because the evolutionary complex social structures should have genet- consequences of broad or narrow geographic ically more fragmented populations and thus ranges tend to be similar regardless of how higher speciation rates than those with more those ranges are mediated at the organismal open breeding systems. And more recently, level (at least within broad groups, such as Belliure et al. (2000) found that natal dispersal benthic marine invertebrates). For example, ability in birds is inversely related to popula- widespread species of marine gastropods are tion differentiation and therefore, they ar- geologically longer-lived than restricted spe- gued, to speciation propensity. If these very cies, and the establishment and maintenance different routes to highly subdivided popu- of these different ranges are statistically relat- lations yield similar macroevolutionary dy- ed to modes of larval development-an organ- namics, this again would argue for genetic ismal trait-that differ in dispersal capabili- population structure as an emergent property ties (Hansen 1978, 1982; Jablonski and Lutz at the clade level. The consistent relationship 1983; Jablonski 1986a, 1987, 1995; Scheltema between dispersal ability and genetic popu- 1989, 1992; Gili and Martinell 1994; Kohn and lation structure in plants (Govindaraju 1988) Perron 1994). Jablonski (1987) found geo- and animals (Bohonak 1999, in his valuable graphic range to be heritable at the species meta-analysis of 333 species across all animal level (that is, closely related species showed groups and environments) suggests that this significant correlations in the magnitudes in will be a profitable avenue for macroevolu- their geographic ranges), completing the re- tionary research. Perhaps this general mech- quirements for evolution by selection at any anism underlies the decrease in speciation rate 36 DAVID JABLONSKI observed by Dodd et al. (1999) when angio- into account empirical evidence for higher ex- sperm lineages switch from animal pollina- tinction and origination rates in low-dispersal tion to wind pollination, for example. lineages. Recent molecular work has shown that even Another unresolved problem is that marine widely dispersing marine species can some- bivalves do not exhibit the same relation be- times, perhaps usually, have subdivided rath- tween larval types and species-level dynamics er than panmictic populations (e.g., Palumbi as the co-occurring gastropods (e.g., Jablonski 1996; Geller 1998; Benzie 1999a; Avise 2000). and Lutz 1983; Stanley 1990). Perhaps this is This does not mean, however, that high-dis- because modes of larval development in bi- persal species are as readily subdivided as valves are more tightly linked phylogenetical- low-dispersal ones. The key issue is the sta- ly to feeding types, body sizes, and other fac- bility and long-term evolutionary effects of tors that might also influence evolutionary that population structure relative to taxa with rates. Jablonski (1986a, 1995) showed that lar- low dispersal abilities. The consistent relation- val modes in marine gastropods override ships among larval type, geographic extent, those of adult feeding types, and if the op- and speciation /extinction rates in Cretaceous, posite is true for bivalves then the two groups Paleogene, and Neogene taxa (which appear in tandem might provide a valuable system to be robust to sampling [Jablonski 1988; Mar- for exploring the interplay of rate-determin- shall 1991]) suggest that in at least some set- ing traits at different hierarchical levels. tings the population structures detected by The heritability of species-level traits re- mtDNA analysis may be transient or in any mains a neglected area. Jablonski (1987) and case do not have predictable macroevolution- Ricklefs and Latham (1992) found geographic ary effects (see also the diversity of analyses ranges to be heritable in marine mollusks and tabulated by Bohonak 1999). An intriguing terrestrial plants, respectively. Their compar- pattern that needs a more detailed evolution- isons of closely related species were designed ary perspective is the discovery that genetic as a phylogenetic analogue to the sib-sib com- connectedness among Pacific populations of parisons of quantitative genetics (and see also benthic invertebrates does not conform to pre- Peterson et al. 1999, who successfully predict sent-day ocean circulation patterns but may geographic distributions of sister species be a Pleistocene holdover (Benzie and Wil- based on a model of ecological niche conser- liams 1997; Palumbi et al. 1997; Benzie vatism). Gaston and Blackburn (1997) did not 1999a,b). Spatial scale may also be important find strong species-level heritability in birds here: the vast but highly discontinuous envi- using nested ANOVAs, a very different design ronments of the Indo-West Pacific may impart that also has precedents in quantitative genet- a different evolutionary dynamic from that ics but lacks a detailed phylogenetic frame- documented in the more linear shelves and work, necessarily omits extinct species and the more continuous two-dimensional epicon- Pleistocene range adjustments, and compares tinental seas that provided the paleontological taxa in different geographic situations, unlike data (see Valentine and Jablonski 1983). Jablonski's analysis, which is a macroevolu- Clearly, further analyses of evolutionary tionary analogue of a common-garden exper- sorting of taxa would benefit greatly from a iment. More work is needed to assess the more detailed phylogenetic framework. Duda strengths and weaknesses of the different ap- and Palumbi (1999) rightly note that the fur- proaches and where they might be applied ther analyses of such patterns in a phyloge- most robustly. netic context would be valuable. However, The Limits of SpeciesSelection and Species Sort- their emphasizing an evolutionary bias to- ing.-The domain of strict-sense species selec- ward the production of species having low- tion, which depends on emergent characters, dispersal larvae, rather than species sorting is much narrower than broad-sense species se- for the larval modes for Pacific Conus, is dif- lection, which depends only on emergent fit- ficult to interpret because they lack data on ex- nesses (i.e., differential origination and extinc- tinct species and their model does not take tion rates regardless of the hierarchical level at MICRO- AND MACROEVOLUTION 37 which they are determined [see Vrba and idently dominated by stasis and punctuation, Gould 1986; Lloyd and Gould 1993; Grantham other potential species-level features that 1995; Stidd and Wade 1995]). Beyond that, we might be heritable owing to factors like pop- simply do not know the relative frequencies of ulation sizes or genetic population structure different sorting processes, overall or among include relative morphological inertia (and so clades. The theoretical literature has out- the average duration of stasis in the phyletic stripped the empirical database, in part sim- mode, or the amplitude of oscillations within ply because of the scale of the databases re- stasis, if these are set intrinsically) and per- quired for rigorous analyses. However, if geo- haps even the size-frequency distribution of graphic range is arguably a species-level char- morphological divergences of daughter iso- acter, then the macroecological literature is lates. Sex ratios may be another example of rich in potential examples that might fit the higher-level trait, although possibly played species-selection paradigm, because so many out at an intermediate focal level if interdemic features of living organisms can be related to differences in sex ratios are common in some geographic range and thus are candidates for groups (e.g., Delph 1990; Graff 1999). Is the hitchhiking on species sorting processes (see relative genetic or morphological variability of for example Brown 1995; Brown et al. 1996; species an emergent species-level trait, or is it Gaston 1998). Other components of rarity as simply the summation of organismic proper- classified by Rabinowitz (1981; Rabinowitz et ties and therefore an aggregate trait as argued al. 1986) might also be examined in this list: by Lloyd and Gould (1993)? It depends on population sizes or densities may be emergent how that variation arises, and how sorting properties (e.g., Vrba and Eldredge 1984; and processes operate on that trait, and empirical here too a large macroecological literature ex- work is needed here. ists, ripe for macroevolutionary analysis, e.g., The potential for species sorting (= broad- Brown 1995; Blackburn and Gaston 1997, sense species selection) seems extensive, given 1999), whereas habitat specificity may reside the abundant evidence for differences in in- more fully at the organismal level (e.g., Vrba trinsic extinction and origination rates among 1987). clades (e.g., McKinney 1997; Kammer et al. One important issue needing more atten- 1998; Sepkoski 1998; see also "extinction risk" tion is the stability of such species-level char- studies on extant organisms, e.g., Bennett and acteristics. Jablonski (1986b, 1987) gave evi- Owens 1997 and references therein). Here, too, dence that marine species achieve their geo- phylogenetic hypotheses can provide a valu- graphic-range magnitudes rapidly relative to able framework for rigorous analysis, and their geologic durations. Tracking the mag- methods are being developed for rigorous nitude, rather than the position, of geographic testing of differential origination and extinc- ranges during Pleistocene or other environ- tion rates in a phylogenetic context (e.g., Kirk- mental oscillations would be interesting, as patrick and Slatkin 1993; Slowinski and Guyer would testing for evolutionary rate differences 1993; Sanderson and Donoghue 1996; Harvey among taxa that differ in the amplitudeof their and Rambaut 1998; Paradis 1998). These meth- range-size changes over time. Population den- ods have mostly been applied to extant taxa, sity should also be tested more fully for long- where the estimation of evolutionary dynam- term stability (e.g., Arneberg et al. 1997). Both ics is made difficult by unrecorded extinction exciting and daunting is the loose covariation that must be ignored or assumed to be con- of geographic range, abundance, and body stant through time, but some also show prom- size (Brown 1995, 1999; Gaston and Blackburn ise for the testing of species-sorting hypothe- 1999; Lawton 1999), and the question of how ses in the fossil record. these effects spanning hierarchical levels and Species sorting, including narrow-sense spatial scales interact, and become linked or species selection, will generally play a differ- decoupled on ecological and evolutionary ent evolutionary role from the microevolution- timescales. ary sorting of organisms within populations: Given that the history of most lineages is ev- it will tend to determine diversity differentials 38 DAVID JABLONSKI among clades rather than shape adaptations. the increase in predation pressure described Species sorting may not construct a complex by Vermeij (1987) as the Mesozoic Marine Rev- eye or a long neck, but it may determine how olution (MMR) would all be possible subjects. many species possess complex eyes or long To use the last of these biotic transitions as an necks over evolutionary timescales. This has example (and see also Signor and Brett 1984), two immediate implications. First, the setting long-lived bivalve or gastropod genera that of species sorting and microevolution as rival appear to persist through much of the MMR, hypotheses or mechanisms is often inappro- such as Aphrodina, Cyprimeria, or Solariella, priate. And second, the mapping of species might be targeted to test whether any given densities in morphospace need not reflect the species shows anagenetic change in antipre- topology of the adaptive landscape. That is, datory adaptations independent of local en- the frequency distribution of morphologies vironmental changes. (Kelley 1989, 1991, did within or among clades may not be a simple find intraspecific trends, but within a much indication of relative fitnesses at the organis- later, Neogene, interval.) If species tend to be mal level. static, several alternative dynamics should be But is sorting at the species level unequiv- tested. A mechanism below the species level ocally ruled out as a mechanism for organis- might involve directional, stepwise anagene- mal adaptation? Rice (1995) showed that the sis, shaped by widely spaced episodes of di- efficacy of species sorting in character evolu- rectional selection or within-species shifting- tion depends on the speciation rate per gen- balance processes. Next up the hierarchy eration, the mutation rate, and the survival would be the sorting of species to convert rate of reproductive isolates (and the genetic clades to better-defended morphologies. Op- complexity of the trait under consideration). erating at an even higher level would be clade Thus, species sorting would be more likely to sorting, in which preferential extinction of influence character evolution directly in or- poorly defended clades or preferential origin ganisms with long generation times; for ex- of well-defended ones might shape the overall ample Asian elephants fit this model, given biota. As many authors have noted (e.g., Stan- reasonable mutation rates and selection coef- ley 1973; McShea 1994; P. J. Wagner 1996b), ficients, and a very broad taxonomic domain such analyses cannot focus only on mean mor- is possible if speciation rates are sufficiently phologies or the appearance of derived char- high (Rice 1995). Perhaps a more pervasive acter states; an important component of the way for species sorting to influence the evo- sorting dynamics may involve the retention of lution of complex characters is by determining less heavily defended morphologies. Finally, the persistence and proliferation of taxa bear- spatial scale will be important in understanding characters shaped by individual selection, ing mechanisms, in terms of both the estab- so that the process of assembling those char- lishment of well-defended species-which acters can proceed beyond the duration of in- Roy (1996) found to vary regionally in timing dividual species (Raup 1994; Rice 1995). This and which may have been promoted by envi- means that rate differentials among clades ronmental perturbations (see also Miller might be important even if, as Hallam (1998) 1998)-and the fates of less derived forms argues, many individual clades generate only (which Vermeij [1987] argues have shifted a few species per unit time. geographically or environmentally through Hierarchical analyses of large-scale changes time). in morphology would be valuable for improv- Such large-scale evolutionary interactions ing our understanding of the relative roles of of predators and prey raise the broader issue processes at different levels and the potential- of clade interactions and how they might ly complex interactions between them. The in- drive taxon sorting. As Sepkoski (1996) made faunalization of bivalves, the evolution of tree- clear, negative clade interactions need not like growth habits with the initial assembly of produce straightforward reciprocal diversity terrestrial forests, and the escalation of defen- patterns (the "double wedge pattern" of Ben- sive morphologies in marine benthos during ton 1987), but instead can be manifest in com- MICRO- AND MACROEVOLUTION 39 plex coupled logistic patterns, and perhaps record of interactions that have been experi- most importantly depressed but still positive mentally dissected in modern communities diversification rates (see also Miller and Sep- (e.g., Aronson 1992, 1994; Lidgard et al. 1993; koski 1988). Still open to investigation is ex- Sepkoski et al. 2000). actly how local ecological interactions-as Incumbency.-Macroevolutionary incum- many of these clade interactions surely must bency effects, such as the damping of diver- entail-actually scale up to determine origi- sification among mammals for the first two- nation and extinction rates. Simple intuitive thirds of their history (presumably by incum- arguments are easy: competition decreases bent archosaurs), are perhaps the most com- population sizes and/or intrinsic growth pelling evidence of the macroevolutionary rates, thereby making species more vulnerable effects of competitive interactions (Jablonski to stochastic extinction; origination rates and Sepkoski 1996; Jablonski 2000a). Such ef- might be depressed in the same way, if biotic fects represent very different dynamics from interactions reduce the population sizes of iso- those underlying the reciprocal diversity pat- lates and thus decrease their probability of terns discussed above, of course: in double- surviving to achieve speciation. On the other wedge or coupled logistic models, taxon A hand, clade interactions via predation could progressively excludes taxon B by virtue of A's arguably operate in the same fashion, al- competitive superiority; in incumbency inter- though Vermeij (1994) explicitly rejects the actions, taxon A excludes B by virtue of A's role of escalation in extinction on mainly the- ecological preemption of resources, which oretical grounds. How negative ecological in- need not reflect competitive superiority on a teractions actually determine per-taxon origi- level playing field (as emphasized by Rosen- nation and extinction rates seems an impor- zweig and McCord [1991]). The double-wedge tant area for research. pattern is not exclusively the hallmark of the Such analyses in the fossil record are com- rise of a competitive dominant, however: plicated by the highly diffuse nature of many piecemeal extinction of the dominant incum- of the interactions under consideration: esca- bent may create cumulative opportunities for lation in molluscan defenses is a response to surviving taxa, for example. Other kinds of the collective diversification of durophagous progressive replacements might also be un- arthropods, mollusks, vertebrates, and other derlain by incumbency effects, as Valentine groups, so that simple responses to specific (1990) suggested for the Phanerozoic decline enemies will be unusual, difficult to detect, in evolutionary rates in the marine biota: over and probably fleeting in geologic terms. Tar- the long run, extinction-resistant clades will geting competitive interactions for combined tend to preempt high-volatility clades (see micro/ macroevolutionary analysis will also Sepkoski 1998 for a somewhat different view). be complicated by the well-established obser- The acceleration in evolutionary rates, tax- vation that taxonomic distance is not a reliable onomically and morphologically, among pre- proxy for interaction intensity (e.g., Brown viously established clades following an ex- and Davidson 1977; Brown et al. 1979a,b on tinction event (e.g., Miller and Sepkoski 1988; seed-eating ants vs. rodents; Kodric-Brown Patzkowsky 1995; Foote 1997; McKinney 1998; and Brown 1979 on hummingbirds vs. insects; Sepkoski 1998) is the primary macroevolu- Schluter 1986 on finches vs. bees; Jackson and tionary measure of incumbency effects. Con- Hughes 1985 on spatial competition in marine siderable evidence supports a spatial ana- encrusting communities among several phy- logue, in which asymmetries in biotic inter- la). Paleontologists have been aware of this- changes appear to reflect regional differences Bambach's (1983) "megaguilds" are decidedly in extinction intensities, both in the fossil re- polyphyletic, for example-but the study of cord (e.g., Vermeij 1991) and in present-day bi- the large-scale evolutionary effects of biotic in- otas (e.g., Case 1996). However, not all inva- teractions remains a difficult task. One pow- sions are mediated by prior extinction (see for erful approach deserving more extensive ap- example Williamson 1996; Lonsdale 1999), plication is the projection back into the fossil and at least for the end-Cretaceous extinction, 40 DAVID JABLONSKI invasion intensities need not correlate to local scale biotic systems, let alone global biotas, extinction intensities (Jablonski 1998). More evolve to the perpetual edge of collapse like work is needed that tackles the difficult task the canonical sandpile, as suggested by Bak of separating the effects of diversity loss per and colleagues (e.g., Sneppan et al. 1995; Sole se from regional differences in environmental et al. 1999). The resilience of these biotic sys- change; in other words, is differential diver- tems to many perturbations, and their rela- sity loss the promoter of asymmetrical biotic tively loose organization as manifested in the interchanges, or another symptom of the ef- relatively fluid composition of Pleistocene and fects of differential environmental perturba- many earlier communities, argues against a tion? Incumbency effects may represent one of state of self-organized criticality, and more the strongest bridges between ecology and generally argues that the major turnover macroevolution, and cross-scale and spatially events in the history of life were externally explicit analyses of how those effects are driven (rather than the product of internal dy- maintained, broken, or circumvented would namics). Such avalanche models may apply on be valuable, not only for theoretical reasons, local scales and the short term, but hierarchy but in order to address the pressing issues of and scale defeat their universality, because the present-day biotic interchange. necessary biotic interconnectedness falls away rapidly at larger scales. Spatially heteroge- Extinction Events As Filters and Promoters neous dynamics can be seen, for example, in So much has been written lately on the evo- the geographic complexities of macroevolu- lutionary role of extinction events that I will tionary and macroecological patterns like the touch on only a few points here (see Raup Ordovician radiations, the marine Mesozoic 1994; Jablonski 1995, 2000a,b; Erwin 1998, revolution, the recovery from the end-Creta- 2000b for an entry into this literature). First ceous mass extinction, and the demise of the and foremost, we still have much to learn Pleistocene megafauna (Roy 1996; Miller about the role of extinction events in evolution. 1997a,b, 1998; Jablonski 1998; Martin and Perturbations occur at all intensities and spa- Steadman 1999). tial scales, and as discussed above they pro- The major mass extinctions probably ac- mote biotic change in important ways, but ef- count for less than 5% of the species turnover fects are difficult to predict from magnitude in the geologic past, and their disproportion- alone (see Miller 1998). The differential re- ate evolutionary effects probably derive from sponse of large-scale biotic units like clades their removal of not just minor constituents of and regional biotas to seemingly similar per- the biota, but also established incumbents. turbations at different times-whether aster- Analyses are still sparse, but contrasts be- oid impacts or climate changes-reflects the tween survivorship patterns during mass ex- fundamental nonlinearities that typify most tinctions and those prevalent during times of complex systems. Thresholds, and especially low extinction intensity have been recorded the importance of antecedent events, are prob- for each of the major extinction events (Jablon- ably an essential component to a system ski 1995, 2000a,b). This does not mean that where four sea-level oscillations cause little certain features favored during times of change in marine community composition but "background" extinction could never also be a fifth brings significant turnover; asteroid im- advantageous during mass extinction events, pacts that form craters of 50 km have no per- but even partial discordances in survivorship ceptible effect on the global biota but a crater can have profound and lasting effects, given of 300 km corresponds to a Cretaceous/Ter- the intensities involved. The monotonic rather tiary (K/T) scale event; and even apparently than bimodal frequency distribution of extinc- similar mass extinction intensities can have tion intensities in the geologic past (e.g., Raup differing effects on biosphere structure and 1991), and some of the similarities in survi- function (Droser et al. 1997). vorship among mass extinctions despite ap- On the other hand, as Levin (1999: pp. 180- parently different triggers, suggests that the 184) notes, there is little evidence that large- scale of the perturbation and the operation of MICRO- AND MACROEVOLUTION 41 threshold effects were important factors in the ecosystems, so that the raw material for mi- observed changes in selectivity. croevolution and the web of potential biotic Patterns of selectivity are difficult to assess, interactions was profoundly shaped by the however, because traits can be lost as a by- taxonomic losses of that time (although Sep- product of selection on other features (or, of koski [1996, 1998] held that those changes course, purely stochastic survivorship [Raup were inevitable given differential turnover 1994]). For example, what was it about the among groups, and were merely hastened by end-Ordovician extinction that selected the mass extinction). Similarly, the end-Cre- against broad selenizones in snails (P. J. Wag- taceous extinction removed the rudists and ner 1996b), or about the end-Cretaceous ex- nearly exterminated the trigonioid bivalves, tinction that selected against schizodont hing- but its lasting influence can also be seen in the es in bivalves, elongate rostra in echinoids, or age distribution of living marine bivalve gen- complex sutures in cephalopods? All of these era, which shows a secondary peak corre- losses or declines are more likely to represent sponding to the early Cenozoic. This 60-m.y. correlations rather than direct causation, but evolutionary echo is less dramatic than the they had long-term morphological effects, and mammalian rise to dominance that began at additional examples are plentiful. the same time, but it reflects a similar evolu- Finally, the long-term effects of mass ex- tionary process (Flessa and Jablonski 1996). tinctions are set not only by the victims and Conclusion survivors of an event, but also by the dynamics of the recovery process. Here, of course, is The relation between micro- and macroevo- where the incumbency effects are most viv- lution is complementary and not mutually ex- idly illustrated, by the diversifications that un- clusive, with effects cascading both upwards fold with the removal of previously dominant and downwards over long timescales. The taxa. As discussed by Jablonski (2000b), how- conceptual expansion of evolutionary biology ever, clade dynamics across extinction events with the advances in our understanding of the can exhibit several different patterns, includ- origin and sorting of variation has benefited ing (1) unbroken continuity, as in the escala- many disciplines and is promoting a fuller in- tion of antipredatory defenses in marine bi- tegration across those scales and hierarchical valves across the K / T boundary (Hansen et al. levels. I have touched only indirectly on many 1999); (2) continuity with setbacks, as in the of the important methodological advances increase in cheilostome bryozoan abundance discussed elsewhere in this issue: in phylog- relative to cyclostomes across the K/T bound- eny estimation, in dissection of developmental ary (McKinney et al. 1998) or the increase in processes, in calculation of confidence limits suture complexity in Paleozoic ammonoids on diversification rates and patterns, and in (Saunders et al. 1999); (3) failure to rebound quantifying the relation of paleontological and eventual extinction, as in the demise of patterns to the fabric of the stratigraphic re- the prolecanitid ammonoids in the Early Tri- cord. These developing methodologies, and assic after surviving the end-Permian debacle the host of new questions that are emerging at (Page 1996); or (4) unbridled diversification, as the interface of biology and geology, will pro- seen most famously in the radiation of mam- vide rich research opportunities for the next mals after the end-Cretaceous demise of the 25 years of Paleobiology. dinosaurs and other reptilian groups. The ap- portionment of survivors among these differ- Acknowledgments ent trajectories needs much more analysis be- This paper benefited from discussions with fore we can understand the evolutionary roles many colleagues, most recently A. K. Beh- of extinction events. rensmeyer, B. Chernoff, D. H. Erwin, M. Foote, That said, mass extinctions have lasting ef- T. A. Grantham, S. M. Kidwell, K. Roy, A. B. fects across many scales. As Erwin (1998) ar- Smith, J. W. Valentine, P. J. Wagner, S. L. Wing, gues, the Permo-Triassic extinction perma- and, in the final throes, the NCEAS Working nently restructured marine and terrestrial Group on Ecological Processes and Evolution- 42 DAVID JABLONSKI

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