Patterns of Evolution Among the Artiodacyla and Perissodactyla

Evolution, 35(3), 1981, pp 433-440

PATTERNS OF EVOLUTION AMONG THE ARTIODACTYLA AND PERISSODACTYLA (MAMMALIA)

R. L. CIFELLI Department of VertebratePaleontology, American Museum of Natural History, New York, New York 10024

Received March 28, 1980. Revised September 16, 1980

Diversity changes through time of the have been compiled from Romer (1966). mammalian ungulate orders Artiodactyla Current revisions might alter the data and Perissodactyla have been touted long somewhat, but it is doubtful that the dif- and widely as exemplifying ordinal level ferences would be systematic or great. taxonomic (and presumably ecologic) dis- Question-marked taxa or those not desig- placement (Simpson, 1953; Stanley, 1974) nated chronostratigraphically to subepoch since, as Van Valen (1971) has pointed were ignored. The time scale used is from out, they have a nearly identical "way of Harland et al. (1964). life" (=adaptive zone, Simpson, 1953; plus competitive interactions, Van Valen, DOMINANCE AND DISPLACEMENT 1971). The controversial assumption that Competitive interactions leading to the herbivores are food limited (cf. Hairston relative dominance of the artiodactyls are et al., 1960; Murdoch, 1966; Ehrlich and expected to be reflected in changes of di- Birch, 1967; Slobodkin et al., 1967) is im- versity and turnover rates through time. plicit to this generalization. Both orders Generic and familial diversity of the two presumably appeared in the late Paleo- orders are shown in Figures 1 and 2. Here, cene, as they are well differentiated by the as elsewhere, I have systematically over- early Eocene (Figs. 1 and 2). While peris- estimated chronologic ranges for genera- sodactyls seem to have undergone taxo- and therefore calculated standing diver- nomic diversification at both generic and sity at any given point in time-by con- familial levels somewhat earlier than ar- sidering originations to have occurred at tiodactyls, the difference is much less than the beginning of the subepoch of first ap- most authors suggest. Perissodactyls de- pearance and extinctions at the end of the clined in importance after the middle subepoch of last known occurrence. Al- Eocene, while the artiodactyls maintained though it would be desirable to conduct a stable "dominance" from the early Oli- the analysis at the species level, the fossil gocene until their apparently enormous record is inadequate to the task, and gen- Plio-Pleistocene radiation. Various deter- era are used. While sampling of families ministic hypotheses have been forwarded is doubtless better than of genera, the lat- in explanation of this pattern. Such hy- ter are more appropriate in the present potheses usually invoke the acquisition of context, since they reflect more accurately one or more characters (double trochleated events which ultimately must occur at the astragalus, selenodont molars, ruminant species level. Whereas biases in the fossil digestion) by the artiodactyls as giving record (preservation, relative exposures of that group a relative adaptive advantage. fossiliferous strata, "monographic"effects; Here I review the evolutionary histories Raup, 1972) hamper comparison through of these two orders in search of evidence time, I assume that relative diversities of supporting these hypotheses. Further, I the two orders at any given point in time analyze overall patterns to detect possible are unaffected by such biases. The possi- correspondence to or support for the var- bility of differences in geographic distri- ious "empirical" (Valentine, 1973) and bution is discussed below. "equilibrium" (Mark and Flessa, 1977) The adaptive advantage conferred by models of Phanerozoic diversity. All data the acquisition of a double trochleated as- 433 434 R. L. CIFELLI

0 es - 65 CD

o A

25 -

EEO MEO LEO EOL MOL LOLEMI MMI LMI PLI PLS R 0 0 ~~~~~~~~~~0 0 B

0 ~~~~~~~~~~~~00

N- ~ ~ ~ ~ ~ ~ ~ ~ ~ W 0

0 ~~~~~~~~~~~~02

0EEO MEO~~~~~~~~~~<0 LEO EOL MOL LOLEMI MMI LMI PLI PLS

0 0D O ~~~~~~~~~~~~o N ~~~~~~~~~~~~0 FIG. 2. Familial diversity (circles), originations (triangles), and extinctions (diamonds) of perissodactyls (A) and artiodactyls (B). Originations and ex- 0 0 tinctions are cumulative. R; Recent; other abbreviations as in Fig. 1. into (tinls an xicin(daod)o e

ochs (Raup, 1972) must be confronted: while vertical corrections to absolute time have been made in the figures, relative diversity is biased. This is because, all rissodactyls (A) and artiodactyls (B). Abbreviations: other conditions being equal, a long inter- EEO; early Eocene, MEO; middle Eocene, LEO; late Eocene, EOL; early Oligocene, MOL; middle val is expected to show greater diversity Oligocene, LOL; late Oligocene, EMI; early mio- than a short one. In the present case, high cene, MMI; middle Miocene, LMI; late Miocene, diversity in the early Miocene (duration = PLI; Pliocene, PLS; Pleistocene. 9 million years) follows low diversity in the late Oligocene (duration= 3 million years). Estimates of standing diversity tragalus (Schaeffer, 1947) cannot be eval- may be made by subtracting cumulative uated in the present context, since it ap- extinctions from cumulative originations pears as a basic ordinal character of the at any given point in time. Figure 3 shows earliest (basal Eocene) artiodactyls. There that the late Oligocene constriction and is no discernible change in pattern during the early Miocene expansion are real, al- the late Eocene, when the highly efficient though the magnitude of difference is not selenodont dentitions arose, although this great. This is further supported by might have been expected to have stimu- changes in familial diversity (Fig. 2b). lated an artiodactyl radiation. The in- The great Plio-Pleistocene artiodactyl crease in artiodactyl diversity in the early radiation (comprised mainly of bovids and Miocene corresponds roughly to the evo- cervids; Table 1) apparently had no no- lution of the fully ruminating stomach (as ticeable effect on perissodactyl diversity, projected by Janis, 1976), which is hy- which seems to have increased over this pothesized to have conferred great adap- time period (although this may be a sam- tive advantage ("eat and run") upon its pling bias, as the Plio-Pleistocene mam- bearers (see, for instance, Young, 1962). mal record is particularly good). However, the Miocene artiodactyl radia- If, as Newell (1952) suggests for Meso- tion is comprised in large part by the non- zoic nautiloid-ammonoid diversities, com- ruminating Merycoidodontidae (Janis, petitive advantage of one group is indi- 1976; see Table 1). Here, the problem of cated by its diversification occurring differences in relative duration of subep- concomitantly with the decline of its com- PATTERNS OF MAMMALIAN EVOLUTION 435

TABLE 1. Generic diversity of perissodactyl and artiodactylfamilies by subepoch, early Eocene to Pleisto- cene. Abbreviations: E; early, M; middle, L; late.

Eocene Oligocene Miocene E M L E M L E M L Plio. Pleis. A. Perissodactylfamilies Equidae 3 5 5 3 2 1 4 5 6 8 6 Palaeotheriidae 1 2 2 Brontotheriidae 3 7 22 13 3 1 Eomoropidae 1 1 4 Chalicotheriidae 1 2 1 3 4 3 2 5 4 Isectolophidae 1 1 1 1 Helaletidae 2 6 4 1 1 1 Lophialetidae 1 2 Deperetellidae 1 2 1 Lophiodontidae 3 2 2 Tapiridae 1 1 2 4 2 2 2 1 Hyracodontidae 2 4 3 1 1 1 Amynodontidae 7 3 2 1 1 Rhinocerotidae 1 10 13 10 14 7 9 10 13 7 B. Artiodactylfamilies Diacodectidae 3 Leptochoeridae 1 1 1 Homacodontidae 1 3 4 Dichobunidae 1 9 4 3 1 Achaenodontidae 1 2 Choeropotamidae 3 2 1 Cebochoeridae 2 2 2 Entelodontidae 2 3 3 1 1 Suidae 1 1 1 2 6 6 7 12 12 Tayassuidae 1 2 1 3 2 4 5 6 Anthracotheriidae 4 9 6 7 8 9 5 5 7 1 Hippopotamidae 1 2 Cainotheriidae 2 2 3 2 1 1 Anoplotheriidae 3 6 3 2 Xiphodontidae 2 3 2 Amphimerycidae 1 2 2 Agriochoeridae 1 1 1 1 1 Merycoidodontidae 7 9 8 15 7 3 2 Oromerycidae 2 1 Camelidae 1 2 3 5 3 3 12 12 Hypertragulidae 5 4 5 3 5 Protoceratidae 2 1 1 2 1 1 2 Gelocidae 3 4 3 1 Tragulidae 1 1 3 3 Palaeomerycidae 1 1 3 10 10 7 5 1 Cervidae 3 5 5 24 33 Giraffidae 3 5 15 5 Antilocapridae 1 2 9 6 Bovidae 1 3 6 8 67 105 petitor(s), the record of odd- and even- ment (Fig. 5). Although increase in artio- toed ungulates gives no such indications; dactyl diversity corresponds roughly to nor is there any apparent negative corre- perissodactyl decline in North America, lation between generic diversities of the "clades" on all other continents resemble two orders as would be predicted (Fig. 4). those of the combined data; in fact, pe- An analysis by zoogeographic province riods of increased diversity of artiodactyls might be more meaningful, but here, again, and perissodactyls seem to coincide, sug- the evidence is not supportive of displace- gesting that both are either dependent on 436 R. L. CIFELLI

_ A e- A 14- >-0 0 V) Lo A 0

0 A A A tsAAAiA C\L A 0CC)

0 25 50 75 100 125 150 175 0 ART IODACTYLS

0 FIG. 4. Correlation of perissodactyl and artiodactyl generic diversities.

EEO MEOLEO EOL MOLLOL EMI MMI LMI PLI PLS during the middle and early late Tertiary, 0 o B but this is probably due to an inadequate fossil record.

0 Changes in turnover rates, which may 0 not be indicated by generalized diversity 0 0 trends, must also be considered. If selec- tive advantage of one group causes an in- 0 0 crease in turnover rates of a competitor, 0 an increase in perissodactyl extinction rate 0 should accompany an artiodactyl radiation. Taxonomic survivorship curves, which indicate extinction rates, have been plotted for six perissodactyl cohorts (Fig. 6; vertical scale is log percent of surviving FIG. 3. Cumulative generic originations (trian- The co- gles) and extinctions (diamonds) of perissodactyls (A) genera per lineage million years). and artiodactyls (B). Abbreviations as in Fig. 1. horts are those genera originating in the early, middle, and late Eocene; early and some outside factor, such as climate, or middle/late Oligocene; and the Miocene, are the subjects of some systematic bias(es) respectively. Subepochs of the Oligocene which has (have) not been recognized. and Miocene were pooled so as to improve Africa appears to have been depauperate sampling. Increase in rate of extinction,

P A P A P A P A

0. U~~~~~~~~~~~

0 -j 25 0 w

NORTH AMERICA EUROPE ASIA AFRICA FIG. 5. Distribution of generic diversities by continent, exclusive of South America. Abbreviations: P; Perissodactyla, A; Artiodactyla. PATTERNS OF MAMMALIAN EVOLUTION 437

9~~~~~~~~~~~

A A A

H0 ^r) ~~~~~AA

s~~~~~~~ A

LUJ

z A o - AA 0<- A A (D

EEO MEOLEO EOL MOLLOL EMI MMI LMI PLI PLS R FIG. 6. Taxonomic survivorship of six perissodactyl generic cohorts. Abbreviations as in Fig. 1. 1 2 3 4 5 6 7 EXTINCTION RATE (GENERA per MY) represented by a sharp drop in the curve, FIG. 7. Correlation of origination and extinction rates of odd- and even-toed ungulates. should affect overlapping cohorts coinci- dentally, since extrinsic extinction causes adaptive zones, to which higher taxa gen- affect genera without respect to their age. erally correspond, are filled early and orig- No such trends are evident in these data. inations taper off as the amount of change Cohort survivorship appears to increase necessary to produce a new taxon becomes in the later cohorts, undoubtedly due to increasingly difficult to attain (Valentine, the fact that the two youngest cohorts rep- 1969). At lower levels, however, diversi- resent pooled samples. fication continues through progressive Van Valen (1973) has calculated penis- partitioning of ecological niches into sodactyl origination and extinction rates. smaller functional units: average niche He found extinction rates to be approxi- size of species decreases as specialization mately equal through time, and therefore increases. Extrinsic environmental factors concluded that observed perissodactyl di- (i.e., abiotic or diversity independent) pro- versity patterns resulted from differences duce periodic extinctions, opening up pre- in origination rates. Diversity and generic viously occupied niches (Newell, 1952; origination/extinction rates for perissodac- Valentine, 1969). tyls and artiodactyls are plotted in Figure Diversity and originations/extinctions 1. Little correspondence between artio- are depicted for genera and families in dactyl diversity and perissodactyl origi- Figures 1 and 2, respectively. While pe- nation/extinction rates, or between penis- rissodactyl families follow the predicted sodactyl diversity and artiodactyl pattern (all originated by the late Eocene), origination/extinction rates, is evident (see genera do not become increasingly abun- below). dant. Generic diversity closely mirrors that of families through time. The pat- PATTERNS OF TAXONOMIC DIVERSITY terns afforded by artiodactyl diversity ap- Various models have been proposed to pear to support the continuous diversifi- account for Phanerozoic diversity pat- cation hypothesis more cogently. The Plio- terns, and may be broadly categorized as Pleistocene radiation, which constitutes "continuous diversification" (Valentine, the "trend" for genera, is largely the result 1969, 1973) or "equilibrium" (Mark and of expansion of two families, the Bovidae Flessa, 1977) approaches. The former, and Cervidae. These families originated which is more nearly empirical and which in the late Oligocene and early Miocene, perhaps has historical priority, predicts an respectively, and therefore may represent early diversification of higher taxa. Major the invasion of new adaptive zones rather 438 R. L. CIFELLI than increased canalization of previously 1972) to the fossil record and an evolu- occupied niches. Except for the fact that tionary scale, assumes that diversity in rates of speciation must exceed those of any given adaptive zone or zoogeographic extinction, the continuous diversification area rises until a saturation point is hypothesis further proposes that any cor- reached, after which it will fluctuate about respondence between the two rates is for- some stable mean. Implied is that origi- tuitous. Flessa and Levinton, who argue nation and extinction rates are diversity for unbounded diversity, present a graph dependent and will be approximately (Flessa and Levinton, 1975, Fig. 3) which equal at equilibrium, which corresponds shows no correlation between origination to environmental carrying capacity. Mark and extinction rates of Phanerozoic ma- and Flessa (1977) present somewhat rine taxa (but see Mark and Flessa, 1977). equivocal data supporting evolutionary Flessa and Levinton's pooling of ecologi- equilibria in brachiopods and mammals. cally disparate taxa may not be justifiable. As Figure 1 shows, origination and ex- My Figure 7 indicates a relationship be- tinction rates of artiodactyls and perisso- tween the two rates for artiodactyls and dactyls parallel each other rather closely perissodactyls. The evidence, therefore, with, however, some important diver- does not lend credence to the continuous gences. Originations markedly outstrip diversification hypothesis. The effects of extinctions through most of the Eocene for such biases as the "taxonomic hindsight" both artiodactyls and perissodactyls. This effect (Raup et al., 1973)-the inability of may represent the rise to an equilibrium taxonomists to recognize "incipient" taxa level of diversity. Although numerous ar- (particularly at higher taxonomic levels)- chaic subungulate types were present in and the relatively better representation of the early Tertiary, the Eocene radiation lower taxa as the Recent is approached of artiodactyls and perissodactyls repre- (Raup, 1972) are unknown. sents the first important diversification of Newell (1952) proposed that periodicity large, specialized herbivorous mammals. in invertebrate evolution resulted from rap- The equilibrium model predicts such a id evolution (=increased speciation or rate pattern of diversification: initially high of origination) into niches vacated by pre- diversification rates should decrease and vious extinctions. Diversity eventually stabilize as the limiting boundary (envi- reaches a stabilization point, which is fol- ronmental carrying capacity) is reached. lowed by a more or less abrupt extinction In this case, this effect may be partially event (environmentally controlled) which an artifact of method, since originations opens niches and therefore paves the way were plotted at the beginning of each sub- to another diversification peak. Implied, epoch and extinctions at the end. The therefore, is an alternation of periods of rates for the early Eocene were therefore increased originations and extinctions. omitted from the correlation plotted in This is not evident in Figure 1, which sug- Figure 7, which shows a fairly close re- gests that the situation is somewhat more lationship between origination and extinc- complex. Increased rates of extinction (in tion rates. The rates diverge rather dras- genera per million years) accompany in- tically in the Plio-Pleistocene. Perhaps this creased originations and diversity, and is in part due to the proximity of the Re- similarly decrease with them as well; they cent, yet the relationships are not the same do not alternate. Diversity trends, as for both orders (originations exceed ex- Webb (1969) has pointed out, may result tinctions for artiodactyls, while the re- from "original pull," "extinction push," or verse is true of perissodactyls). The equi- (most likely) an interaction between the librium hypothesis predicts not only a two rates. close correspondence of turnover rates The equilibrium model, an extension of during periods of stability, but also that insular biogeographic theory (MacArthur these vary with diversity. This is broadly and Wilson, 1963; see also Simberloff, true (Fig. 6), but turnover peaks in the PATTERNS OF MAMMALIAN EVOLUTION 439 middle Oligocene for artiodactyls and late a positive correlation exists between orig- Oligocene for perissodactyls are not re- ination and extinction rates of artiodactyls flected in diversity trends; moreover, these and perissodactyls. The broad correspon- peaks correspond to decreases in diversity dence of turnover rates to diversity may of the other order, the opposite of what well represent equilibrium shifts, but the would be expected given the assumption significance of this pattern and its gener- of nearly identical adaptive zones. Webb ality among other mammalian groups are (1969) suggests that the pattern of evolu- unknown. tion for North American Plio-Pleistocene mammals represents diversity dependent ACKNOWLEDGMENTS equilibrium shifts, and it is possible that I am grateful to D. M. Raup for his the noise in this system is due to a similar advice, encouragement, and interest in shifting of equilibria throughout Cenozoic this paper. I thank L. Radinsky, L. Van time. Such equilibrium shifts, in turn, Valen, and L. Jacobs for their suggestions may be related to long term climatic and criticisms, although they do not nec- change and consequent change in the ex- essarily espouse my conclusions. I thank tent of open country "savanna" habitats also S. Stanley for helpful review com- (see review by Webb, 1977). ments.

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