Biased extinction and evolutionary trends

Biased Extinction and Evolutionary Trends

Richard D. Norris

Paleobiology, Vol. 17, No. 4. (Autumn, 1991), pp. 388-399.

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Paleobiology, 17(4), 1991, pp. 388-399

Biased extinction and evolutionary trends

Richard D. Norris

Abstract.-The directionality of long-term trends can be strongly biased by forces intrinsic to a clade. Trends in body size and skeletal shape may be dictated more by variations in survivorship that reflect differences in ecology than by long-term directional changes in the environment. Hence, mass extinctions can help drive evolutionary trends by selectively eliminating some morphologies and permitting the survivors to found the next radiation.

Examples include repeated trends toward larger maximum body size and the evolution of keeled species from those with globose tests in planktonic foraminifera. Both the trends in size and shape develop because small species with globose tests are significantly more resistant to extinction than species that are large or have peripheral keels. Hence, the survivors of both the Cretaceous-Tertiary and Eocene-Oligocene extinction episodes are small, unkeeled taxa. Large species and species with keels evolved convergently after both mass extinctions as the founders radiated anew.

Comparison of three radiations of planktonic foraminifera suggest that the convergent evolution of similar test shapes and sizes is not due to synchronous changes in oceanography that track evolutionary trends. Instead, the reestablishment of habitat heterogeneity is needed to permit the ensuing radiation to unfold rather than to closely guide its progress. Similar evolutionary trends will develop in each radiation as long as the founders have similar morphology and the evolution of variants present in the previous radiation is not precluded by the environment.

Richard D. Norris. Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543

Accepted: May 15, 1991

Introduction forminifera can be readily placed into 1 of 10 The causes of directional evolutionary basic body plans, and each of these designs

trends have figured prominently in evolu- is known from at least two of the three most tionary debate for over a century. To what recent radiations (Fig. 2). Such striking con- extent are trends directed by environmental servatism in test structure is also exemplified forces as opposed to constraints set by a clade's by the repetitive appearance of a similar range history? Do long-term directional changes in of body sizes (Gould 1988), species longevity the environment drive these patterns, or distributions (Levinton and Ginzberg 1984), might the way a trend is initiated bias the test shapes (Cifelli 1969; Norris 1986), and result? character evolution (see Cifelli 1969; Frerichs

Examples of cyclic or iterative evolution 1971; Vincent and Berger 1981; Cifelli and can be used to determine what forces gen- Scott 1986; Bolli 1986; Leckie 1989). erate trends. Evolutionary cycles can be com- One of the best-documented cases of iter- pared with one another to determine how ative character evolution in planktonic fora- environmental factors that change continu- minifera is the repeated development of ously contribute to the development of mac- keeled species from unkeeled ancestors (Fig. roevolutionary patterns. These comparisons 2). Keeled species appear in all four major can also reveal how slowly changing factors, radiations and evolved several times within such as a clade's genetics or ecology, influ- each diversification event. Current phyloge- ence evolutionary history. nies for Cretaceous and Cenozoic foraminif-

The fossil record of planktonic forminifera era imply that keels have evolved indepen- contains numerous examples of cyclic pat- dently at least 16 times (phylogenies of Banner terns that have developed over four radia- 1982; Kennett and Srinivasan 1983; Caron tions (Fig. l; Banner and Lowry 1985). For 1985). Reversion to unkeeled state, on the instance, species with grossly similar body other hand, is known in only four cases, three plans evolve in each radiation. All planktonic of them in Neogene lineages (e.g., Kennett O 1991 The Paleontological Society. All rights reserved. 0094-8373191 11704-0005/$1.00

389 TRENDS IN PLANKTC INIC FORAMINIFERA

and Srinivasan 1983). Hence, there is a strong directional trend to evolve from unkeeled to keeled morphologies.

These trends raise two questions. First, what causes morphologic trends such as that from unkeeled morphotypes to keeled designs? A related question is why unkeeled species consistently survive the episodic mass extinctions to found the subsequent radiations, whereas keeled taxa do not? Second, why do keeled species reappear in each radiation following wholesale extinction of the previous keeled species group? In a broader context, why is it that foraminifera are so tightly con- strained to evolve a limited and stereotyped suite of test designs?

Methods

To analyze trends in morphology over time, we need accurate range data for a large number of planktonic foraminifera, and we need to assign species objectively to morphologic categories. In this study, species' geologic ranges have been compiled from published range charts for Cretaceous through Recent species. Morphologic categories have been simplified by recognizing only two: keeled and unkeeled morphotypes. Keeled species are easily distinguished from unkeeled species by the imperforate carina that rims the test in keeled forms.

This simple dichotomy between keeled and unkeeled taxa is used to test the general relationship between test structure and geologic longevity. The presence of keels correlates well with compressed test shape, smooth, macroperforate walls, and the absence of spines and thus serves as a proxy for these and other characters. There are also biological reasons to use the keeled-unkeeled dichotomy. Living keeled taxa occupy deeper levels in the water column than unkeeled forms and have different trophic ecologies, population structure, and patterns of vertical migration (see Hemleben et al. 1989). These ecologic differences are known to hold true in the recent fossil record as well. Therefore, it is plau- sible that ecological differences could alter the macroevolutionary behavior of keeled taxa relative to unkeeled forms.

Range Data. -Species-longevity data con-

' Species FIGURE1. Spindle diagram of species diversity for planktonic foraminifera through geologic time. The width of the spindle shows standing species diversity. Diver- sities calculated as number of co-occurring species found at any time in a given foraminifera1 zone. Data from range charts in Norris (1990).

sist of geologic ranges for 392 species of planktonic foraminifera. Range charts were compiled principally from Kennett and Sri- nivasan (1983) and Bolli and Saunders (1985) for Neogene species; Berggren (1977), Blow (1979), Boersma and Premoli Silva (1983), Toumarkine and Luterbacher (1985), Boersma et al. (1987), and Premoli Silva and Boersma (1988) for Paleogene taxa, and Gorbachik (1971, 1986), Robaszynski and Caron (1979), Robaszynski et al. (1984), Stam (1986), Riegraf (1987a,b), and Banner and Desai (1988) for Cretaceous and latest Jurassic faunas. Range charts and a complete list of sources are presented in Norris (1990).

I used the taxonomies of Kennett and Sri- nivasan (1983); Toumarkine and Luterbacher (1985), Robaszynski and Caron (1979) and Ro- baszynski et al. (1984) as primary sources, because these sources are comprehensive and taxonomically conservative. The Neogene and Cretaceous range charts are the most inter- nally consistent because they have been con- structed largely from group-authored publi- cations and hence use consistent species

390 RICHARD D. NORRIS

NEOGENE

ABSENT Q@$@Q PALEOGENE

CRETACEOUS

FIGURE2. Representative homeomorphs from each of the three major radiations of planktonic foraminifera. Species not drawn to the same scale. Note the close correspondence in gross morphology between species in each radiation. Keeled species are the third, fourth, and fifth shapes from the left in each row. Some morphotypes are not represented in all the radiations (e.g., spiral-convex forms in the Paleogene, and spherical shapes in the Cretaceous).

concepts and nomenclature. Paleogene and Jurassic range charts have been compiled from a larger number of sources, which frequently use conflicting nomenclature. I have account- ed for synonymies by comparing published illustrations, synonymy lists, and descrip- tions for each species in these parts of the data file. My results are just as subjective as those in my sources, but at least I have rejected the obvious synonymies and lumped the morphologically intergrading taxa to-gether. Still, ranges for species in these time periods are considered less reliable than those for Cretaceous and Neogene taxa.

Ranges were calibrated to the geologic time scales of Berggren et al. (1985, as modified by Aubry et al. [1988]) and Kent and Gradstein (1985). Species were assumed to range through any zone in which they occur and first and last appearances are keyed to the numerical ages of foraminifera1 zone boundaries.

Results

Differential survival of unkeeled species over keeled taxa could be explained by one or more factors. Possible causal factors include difference~ in: (1) species' geographic range, (2) abundance of species with un-keeled and keeled test shapes, (3) turnover rate, or (4)differential turnover between times

of mass extinction and times of background extinction. If unkeeled taxa have broader geographic ranges than keeled taxa, keeled species may be more susceptible to local catastrophes than unkeeled species. Likewise, if unkeeled morphologies are more species-rich than keeled taxa, probability would dictate that the more diverse group should be more extinction-resistant than the smaller group. Species with high rates of intrinsic turn-over-high speciation and extinction rates- might also be more susceptible to mass extinction than species predisposed to surviving hard times. Finally, as Jablonski (1989) proposed for Cretaceous molluscs, survival across mass extinction boundaries may be regulated by features that have little or noth- ing to do with survival during times of "background extinction" or clade diversification.

Geographic Range. -Despite attempts by several workers, no correlations have been found between species longevity and geographic range (e.g., Stehli et al. 1972; Wei and Kennett 1983, 1986; Stanley et al. 1988). No differences in mean species duration were found between tropical and nontropical species or between species restricted to two lat- itudinal subzones and species with broader distributions (Stanley et al. 1988). These authors did find that species ranging into polar

TRENDS IN PLANKTONIC FORAMINIFERA

Age (my) Globose Discoidal Keeled 151 -

FIGURE3. Spindle diagrams of species diversity in unkeeled taxa (with globose and discoidal tests) and keeled taxa. Species diversities plotted as occurrence in a given foraminifera1 zone. Keeled species die out at the Creta- ceous-Tertiary and Eocene-Oligocene boundaries despite having species diversities equal to or exceeding those of unkeeled groups. Note that keeled species appear shortly after the first occurrence of unkeeled taxa in each radiation.

and subpolar habitats are significantly longer-ranging than species restricted to warmer waters (Mann-Whitney U-test, P < 0.005). Yet, although temperature tolerance may be correlated with species age, there is no evidence that a taxon's geographic range is associated with species longevity.

Abundance of Species in Shape Groups.-Plots of species diversity within the major shape groups show that, although keeled shape groups never survive mass extinctions, these groups are not less diverse than surviving unkeeled shape groups (Fig. 3). Over 50% of all Upper Cretaceous species were keeled, yet relatively species-poor globose and discoidal shape groups survived the Cretaceous-Terti- ary (K-T) boundary while none of the keeled

KEELED

X = 5.59 my

u,Q,.- 5

Q,

=V) 0 5 10 15 20

Species Longevity (my) FIGURE4. Histograms of species longevity for all keeled and unkeeled taxa. Open boxes indicate partial longevities for extant species and those that became extinct at the Cretaceous-Tertiary (K-T) boundary. Species lost at the K-T boundary are included in the partial range cat- egory to show that the catastrophic extinction cut across all age cohorts of Cretaceous taxa.

species did. The same pattern is observed at the Eocene-Oligocene boundary. Keeled taxa were more diverse than co-occurring discoidal species, yet the discoidal shape group sur- vives, while the keeled taxa gradually lost diversity throughout the Late Eocene and became extinct.

These results suggest that there is little correlation between species diversity and morphotype survival. Evidently, the differential survival of keeled and unkeeled shape groups is not probabilistic. Instead, survival of shape groups probably depends on ecological differences between their constituent species.

Turnover.-Plots of mean species longevity show that unkeeled species have significantly longer taxonomic durations than keeled species (Fig. 4).Species in the keeled shape group are short-ranging with mean durations of about 5-6 m.y. Unkeeled taxa tend to have species durations in excess of 8-10 m.y. These differences in mean species longevity are highly significant (Mann-Whitney U-test; P

RICHARD D. NORRIS

l5 1 Unkeeled Keeled

Paleogene

r 50

a

5

Cretaceous

bML5:01Jhk&--O 0 10 20 30 0 10 20

Species Longevity (my) FIGURE5. Histograms of species longevity for keeled and unkeeled species in each of the three most recent radiations. Open boxes are partial ranges of extant species and species that become extinct at the Cretaceous-Tertiary boundary. Keeled taxa are consistently short-ranging (ranges <10 m.y.) whereas unkeeled shape groups include many taxa with ranges in excess of 10 m.y. Mean longevities for each group are listed in order from the Neogene to the Cretaceous as follows. Unkeeled group: 14.1 m.y., 8.8 m.y., and 11.0 m.y. Keeled group: 5.58 m.y., 5.54 m.y., and 7.18 m.y.

< 0.001). Short-ranging taxa occur in both keeled and unkeeled morphologies; thus, the difference in mean longevity must reside in the proportion of long-ranging species in both groups.

Histograms of species longevity show that the unkeeled group tends to be long-ranging by virtue of its highly skewed longevity dis- tribution (Fig. 4). Whereas the unkeeled shape group tends to include many species with durations of 10 m.y. or less, it also includes a disproportionate number of species with longevities of over 10 m.y. The keeled shape group, on the other hand, is made up nearly exclusively of species with ranges of less than 10 m.y. This keeled group contains no long- ranging survivor taxa.

Splitting up the range data among the three radiations shows that species in each shape group show similar longevity distributions through time (Fig. 5). These differences in species longevity are statistically significant. An ANOVA on species durations grouped by morphology shows significant heterogeneity in geologic range among all species of planktonic foraminifera (Welch ANOVA, P < 0.01).

The unkeeled shape group includes significantly longer-ranging species than the keeled shape group according to pairwise trimmed f-tests (P < 0.05). Indeed, the longevity distributions are strikingly similar, although there is no direct phylogenetic linkage between keeled taxa in the various radiations.

The close convergence in longevity distributions among the three radiations implies that morphology is correlated with turnover rate. All keeled species have high rates of turnover in comparison with the longer-ranging, unkeeled shape group. Keeled species are particularly susceptible to extinction and therefore must have relatively high rates of origination during each of the radiations to maintain the generally high diversity for which they are known.

These results suggest that keeled species die out in each episode of mass extinction because they are inherently prone to rapid turnover. Like the Mesozoic ammonoids (see, e.g., Ward and Signor 1983), keeled planktonic foraminifera are blessed with rapid origination and cursed with a marked sus- ceptibility to extinction. Although relatively

393 TRENDS IN PLANKTONIC FORAMINIFERA

moderate rates of extinction can be offset by abundant speciation, catastrophic extinction can easily remove all members of a shape group. Unkeeled species also include among them many short-ranging taxa, but a relatively large number of species seem to be ar- mored against extinction.

For example, the Oligocene fauna is char- acterized almost entirely by very long-ranging unkeeled globose and discoidal species. There is virtually no speciation during the Late Eocene and Early to Middle Oligocene. Isotopic evidence suggests that marine productivity crashed near the end of the Eocene, because the surface water-to-bottom water 613 C gradient dropped to near zero during this time (Premoli Silva and Boersma 1988). The productivity drop may explain the loss of some species of foraminifera. Yet the major killer seems not to have been any single event, but a marked drop in speciation, possibly related to the productivity drop, temperature changes, or reorganizaton of water masses that occurred throughout the late Paleogene (Shackleton and Kennett 1975; Kennett and Shackleton 1976; Jenkins 1986; Premoli Silva and Boersma 1988, 1989). Phytoplankton appear to show the same pattern of constant rates of extinction but reduced speciation at this time (Knoll 1989). Keeled taxa with high intrinsic turnover rates may have disap-peared because conditions were inimical to the survival of populations that, under more ordinary conditions, would have replaced the species that were regularly becoming extinct. Indeed, extinction dropped off into the Oli- gocene as the extinction-prone Late Eocene species with keeled morphologies were removed. Only the extinction-resistant, un-keeled taxa remained to found the Neogene radiation.

The situation is somewhat different across the Cretaceous-Tertiary extinction event. There, the survivors include small, globose and discoidal taxa that appear just before the extinction episode and disappear in the Early Paleocene (see, e.g., Gerstel et al. 1986; Keller 1989). The extinction removed foraminifera of all ages, from recently evolved keeled and globose species to long-ranging biserial species as seen in range charts in Caron (1985).

The survivors do not appear to be particularly long-ranging. However, the estimated ranges of these species may be too short because their average body sizes are so small that they may be overlooked by micropaleontologists. The actual survivors did not distinguish themselves before or after the extinction except through the fact of their survival. Yet the globose and discoidal shape of these taxa seems to be too much of a coincidence. Pos- sibly ecological traits shared by all globose and discoidal taxa helped Maastrichtian species weather the extinction crisis.

Background and Mass Extinction.-Evidence presented above suggests that there are no qualitative changes in extinction susceptibil- ity of different shape groups between periods of mass extinction and the background re-moval of taxa that occurs all the time during radiations. Keeled species that ordinarily show high turnover within radiations are also the ones removed at the major boundaries. Unkeeled globose species that have shown low rates of extinction throughout every radiation are the survivors of catastrophic events.

Foraminifera appear to respond differently to mass extinction than some other groups. Jablonski (1986) found that, among Creta- ceous molluscs, the longest-ranging taxa were those with planktotrophic larvae. Feeding larvae are correlated with broad geographic ranges among both living and fossil species (Jablonski and Lutz 1983). The inference is that cosmopolitan distributions should re-duce the likelihood of extinction of all populations in a species. Indeed, broadly distrib- uted Cretaceous molluscs are longer-ranging than co-occurring endemic molluscs. Yet, this advantage during the late Mesozoic was removed during the K-T event, and both endemic and cosmopolitan species suffered similar levels of extinction (Jablonski 1989). For Cretaceous planktonic foraminifera, killing was also widespread across ordinarily resistant groups of biserial, discoidal, and globose taxa, but these groups still left the only survivors of the near-total extinction.

In many respects, the macroevolutionary pattern of foraminifera is more similar to that of diatoms, brachiopods, and trilobites than


it is to that of Jablonski's molluscs. Kitchell et al. (1986) described the differential survival of diatom species across the K-T boundary, pointing out that the survivors were species that formed resting cysts. They suggested that resting cysts are a means of escaping periods of nutrient starvation and dangerously high light levels that develop in high-latitude surface waters following the spring bloom. Be- cause species without resting cysts did not survive the boundary event, Kitchell et al. suggested that characteristics of species ecology used to escape seasonality during "nor- mal" times also come in handy during biotic crises that occur on a larger and less regular scale. Johansen (1989) noted that Cretaceous brachiopods show selective extinction at the K-T boundary. Reclining and pedically at- tached species showed the highest turnover, while most other ecological groups were less affected. Chatterton and Speyer (1989) found that trilobite taxa with benthic larvae survived the Ashgillian extinction at a much higher rate than did species with planktonic larvae. Trilobites with benthic larvae also gradually increased in numbers relative to species with planktonic larvae throughout the preceding Ordovician radiation. Evidently, larval feeding mode consistently favored one group of trilobites over another during times of both background and mass extinction.

Discussion

Biasing Factors

Variations in shape longevity could be related to either taxonomic biases or to factors potentially linked to test shape such as body size. If taxonomists systematically oversplit keeled species relative to unkeeled taxa, ar- tificial differences in geologic ranges could result (Schopf el al. 1975). Alternatively, if keeled species are substantially larger in test size than unkeeled species, the frequent ten- dency for large species to have higher rates of turnover relative to smaller taxa could explain the apparent relationship between test shape and longevity (Stanley 1973). It is con- ceivable that phylogenetically linked traits could bias these results, especially if most species are in a relatively small number of dis- crete genera. Finally, unkeeled species could

be longer-ranging than keeled species simply because unkeeled taxa appear earlier in each radiation.

Skeletal Complexity.-Oversplitting certain-ly has affected the longevities of some species, but there is no clear evidence for a systematic bias. Each of the major morphologic groups are defined by roughly equivalent numbers of characters. These traits include aspects of coiling geometry, surface texture, wall structure, aperture shape and position, chamber shape and number, suture shape, and modi- fications to the aperture in the form of teeth, lips, or portici. Therefore morphotype longevity is not due to the abundance of characters used to describe the test. Indeed, species with relatively complex test designs like clavate skeletons with bulbose extensions of the chambers, or serially coiled tests with a great diversity of surface sculpture and patterns of chamber addition, are just as long-ranging as morphologically "simple" species with discoidal and globose tests.

Body Size.-To test the correlation between size and body design, I calculated body volumes for 338 species in the data set. Size was estimated as the volume of an ellipsoid with dimensions equal to the length and height of a foraminifer in axial section. Since most species are roughly discoidal, this measure of volume gives a reasonably good estimate of cross-sectional area, and is a proxy for body size. Volumes are overestimated for most keeled species because of compression at the chamber periphery. Hence, statistical tests of the relationship between body size, shape, and longevity should be biased toward find- ing that keeled species owe their short ranges simply to their larger body volumes. Biserial species were excluded from the analysis, because their volumes cannot be accurately estimated by this method.

The relationship between volume, shape, and species longevity was tested with a two- factor ANOVA (Fig. 6). Species longevity was log-transformed to produce equality of vari- ances and volume was broken into four size classes. Volume is a poor predictor of longevity (P = 0.889) and has few interaction effects with shape (P = 0.798). Keeled species do reach larger body volumes than most un-

TRENDS IN PLANKTONIC FORAMINIFERA

keeled taxa (Mann-Whitney U-test, P < 0.0001), but keeled species are always short- ranging no matter what their size. Therefore, the correlation between shape and longevity is not biased by differences in size.

Phylogenetically Linked Traits.-If most species are in a relatively small number of genera, then the effective sample sizes used in this analysis might actually be smaller than they seem at first glance. Species might have long or short ranges by virtue of belonging to a particular lineage with its particular ecology, rather than because of traits found among all members of a given shape group.

That longevity might be linked to generic membership is rejected by several observa- tions. The planktonic foraminifera in this analysis belong to some 82 genera, of which 21 include keeled species. It is hard to imag- ine all these keeled lineages evolving similar longevity spectra if species duration is con- trolled by factors individualistic to each ge- nus. Furthermore, the keeled genera have no direct phylogenetic connection across the major radiations, so that calling upon chance to produce similar patterns of longevity in all three radiations strains credulity. Last, statistical tests of longevity differences for species from all 82 genera show significant differences in longevity between the various shape groups as noted earlier.

Order of Appearance.-The order of appearance of unkeeled and keeled body plans does not affect their differences in species longevity. When the ranges of all unkeeled taxa that appeared before the first keeled species in a given radiation are removed from Fig. 6, the distributions are scarcely affected. Keeled taxa first appeared shortly after the start of both the Cretaceous and Paleogene radiations; therefore, few unkeeled species need to be removed, and most of those are short-ranging. In the Neogene, all unkeeled taxa with durations longer than 20 m.y. are removed, but even so, the remaining unkeeled species are significantly longer-ranging than keeled species.

Origin of Trends

Whatever the causal forces behind rates of foraminiferal turnover, the directions of cy-

Keeled 10 1 Unkeeledl

FIGURE6. Histograms of species longevity for taxa in four size classes. Keeled species in the left-hand histograms are short-ranging no matter what their size. Con- versely, unkeeled species in the right-hand histograms are long-ranging no matter which size class they fall in. Similar numbers of species are present in each size class.

clic trends in planktonic foraminifera are strongly biased by forces intrinsic to this clade. The repeated trend from unkeeled to keeled species could not happen any other way. Since keeled species always die out in the mass extinctions, the surviving unkeeled species are left to inherit the foraminiferal world. Keeled species have high rates of turnover at all times by virtue of their ecology and thus have little chance to initiate a radiation. The directionality of iterative trends is imposed by the differential survivorship of species in the various shape groups.

Differential extinction can also explain trends in test size within planktonic foraminifera. Trends toward larger maximum body size have been documented in the three youngest radiations. Each diversification starts from small-sized ancestors and gradually fills out the size spectrum over time (Fig. 7). Spe-cies continuously occupy the small size classes while the larger size classes are gradually filled in. Mass extinction selectively elimi- nates species in the larger size classes, permitting renewal of the trend toward in-

RICHARD D. NORRIS

0 20 40 60 80 100 120 Geologic Time (my)

FIGURE7. Iterative trends in size for planktonic foraminifera. Lines show ranges of one or more species in a given size class. Size measured as maximum test diameter. Note that each radiation is initiated by small-sized species. Small size classes remain occupied while the largest size classes are gradually filled. Data from Norris (1990).

creased maximum body size. In this case, trends toward larger maximum body size are just produced by the survival of small species. Cyclic trends in the environment that gradually permit larger and larger body sizes to appear are not required to explain the pattern.

Oceanographic conditions probably also play a role by permitting the reappearance of keeled taxa after each mass extinction. How- ever, this does not occur by reestablishing identical oceanographic conditions at the start of each radiation. Indeed, it is clear that ocean temperatures and sea levels both drop through the Cenozoic (see, e.g., Shackleton and Ken- nett 1975; Savin 1977; Haq et al. 1987) and show no iterative trends in synchrony with foraminiferal body-plan diversification. Re- peating trends in the absolute magnitude of many paleoceanographic variables are simply absent. Instead, iterative evolution may reflect the reappearance of a few basic conditions that are required before a radiation can occur.

Oceanic stratification may be one of these basic requirements for foraminiferal diversification. Many authors have suggested that foraminifera speciate by invading different levels in the water column (see, e.g., Lipps 1970,1986; Douglas and Savin 1978; Hart 1980; Lazarus 1983). Morphological diversity may be related to specialization on different depth habitats (Caron and Homewood 1983; Hart and Ball 1986; Leckie 1987, 1989). The same basic morphologic groups evolve again and again because the oceans showed similar de- grees of stratification in the Mesozoic and Ce-

nozoic. Oceanic stratificaition was main- tained by salinity contrasts in the Mesozoic and Paleogene, and by thermal contrasts in the Neogene (see, e.g., Leckie 1989; Kennett and Stott 1990). Not only is each radiation founded by species with the same architec- ture, but the oceanic environment has almost always been depth-stratified to some extent.

Although the reappearance of keeled species and other morphotypes may depend on the presence of stratified seas, this variable need not change the same way in each radiation. For example, there is little evidence that ocean stratification changed dramatically across the K-T boundary. Therefore, the habitat diversity created by stratification did not have to be reestablished after the crisis. In- stead, reestablishment of other conditions, such as trophic heterogeneity, may have been required before the various morphological groups could reappear (see, e.g., Hallock 1987).

Hallock (1987) has argued that high species diversity is promoted by the combined development of eutrophic and oligotrophic conditions in different parts of the oceans. The broad range of trophic conditions permits a wide variety of specialist and generalist taxa to evolve. Conversely, the widespread development of eutrophic conditions should depress species diversity by eliminating habitats occupied by species specialized to live in oligotrophic seas. For instance, Hallock's model may help explain the low species diversity of the Oligocene. Both stratification and trophic diversity appear to have been very low at that time (see, e.g., Cifelli 1969), probably because of high rates of oceanic overturn

397 TRENDS IN PLANKTONIC FORAMINIFERA

and consequent mixing of nutrient-rich deep waters into the surface waters (Premoli Silva and Boersma 1988; Hallock et al. 1991). Both highly stratified conditions and a combina- tion of eutrophic and oligotrophic conditions may have had to be reestablished before the Neogene radiation could begin.

Although reappearance of foraminifera1 body plans may be dependent on the reestablishment of favorable habitats, the iterative trends, themselves, do not require identical directional changes in the oceanic environment in each radiation. Cyclic evolution is not simply tracking recurrent changes in paleoceanography. Rather the initial bias created by differences in species survivorship sets up the trend, which can be replayed as long as a few basic oceanographic conditions are in place.

Still, long-term trends in oceanography can influence the diversity of species within body plans. The representation of the various body designs within these habitats has clearly changed over the course of time. Keeled species were dominant over all other groups in the Cretaceous while unkeeled, globose species were of very low species diversity. Just the opposite is true now, where globose and discoidal taxa dominate modern faunas (Fig. 3). Differences in representation of body plans are probably signals of oceanographic conditions since many keeled species are char- acteristic of warm waters that were wide-spread in the Cretaceous, while globose species have always diversified in temperate and polar seas that are at their acme today. Overall species diversity is also tied to oceanographic events such as switches in water- mass structure (Wei and Kennett 1986), temperature gradients, oxygen tensions Premoli Silva and Boersma 1989), and productivity levels (Lipps 1986). Clearly, oceanography profoundly influences species diversity and relative abundance of species in each body plan. Yet, the evolution of the body plans themselves may represent adaptations to more fundamental and more stable features of the oceanic realm such as stratification and nutrient flux.

In more general terms, many cases of iterative evolution reflect the basic ecological

and perhaps genetic conservatism of higher taxa that sets in after they first appear. Cyclic trends have been described from many groups of fossils including graptolites (Cooper and Fortey 1983; Mitchell 1987); trilobites (Mc- Namara 1982); ammonites (Haas 1942; Ken- nedy and Wright 1985); mammals (Simpson 1980); radiolarians (Riedel and Sanfilippo 1981) and many other taxa. For instance, ho- moplasy in graptolites may reflect functional limitations imposed by planktonic existence (Fortey and Bell 1987). Given the mode of colony growth, the potential array of altera- tions are limited. Landman (1989) has described the iterative appearance of small ptero- scaphitid ammonites from larger ancestors by progenetic trends. He suggests that progenetic species may have repeatedly evolved to take advantage of resources available only to the juveniles of the larger, ancestral species. As in planktonic foraminifera, particular traits in ammonites may appear iteratively to serve in exploitation of persistent resources.

Conclusions

Species longevity seems to be associated with shape in all three radiations analyzed here. Keeled species have mean durations about half as long as co-occurring unkeeled species. Both keeled and unkeeled morphologies include short-ranging species but only the unkeeled group includes substantial numbers of long-ranging taxa. Unkeeled species always survive to found the next radiation because they possess a suite of ecological traits that promote extinction resistance during times of both mass extinction and radiation. These results for marine zooplankton are similar to examples described for diatoms, trilobites, and molluscs.

Evolutionary trends in the shape and size of planktonic foraminifera, and probably other taxa as well, owe their origin to intrinsic constraints rather than repeated directional changes in oceanography. High extinction resistance of many species with small body sizes predisposes each diversification to be initiated by small-sized ancestors. Trends toward larger maximum body sizes require no special explanation aside from recognizing that small


species survive catastrophes whereas large taxa generally do not. Likewise, biases in survival dictate the morphological trend from unkeeled to keeled morphologies. Therefore, iterative trends in foraminifera are related to differential survivorship coupled with the maintenance or reestablishment of suitable habitat to permit renewed radiation after each mass extinction. Mass extinctions may have a profound effect on the directionality of trends in the subsequent radiation. Genetic conservatism may also explain part of the ten- dency to evolve similar body designs repeatedly (Norris 1991). The abundance of iterative patterns throughout the history of life may reflect great ecological and genetic conser-vatism of clades once they first evolve.

Acknowledgments

I thank S. J. Gould, A. H. Knoll, and W. A. Berggren, and two anonymous reviewers for reviews of an earlier version of this paper and fruitful discussions about the significance of cyclic patterns of evolution. Early discussions with D. Jablonski and students in his course "Macroevolution" served as the initial im- petus for this study.

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