8/13/2019 1330270504_ftp

1/16

YEARBOOK O F PHYSICAL ANTHROPOLOGY 2757-72 (1984)

Primate Evolution: Evidence From the Fossil Record,Comparative Morphology, and Molecular BiologyPHILIP D. GINGERICHM u s e u m of Paleontology, T he Universi ty of Michigan , A n n Arbor ,Michigan 48109

KEY WORDSMolecular clocks Primate evolution, Phylogeny, Stratophenetics, Cladistics,

ABSTRACT Our understanding of primate evolution is ultimately basedon patterns of phyletic relationship and morphological change documented inthe fossil record. Stratophenetic interpretation of living and fossil primatesyields a n objective alternative to the a rbitrary scala naturae assumed implic-itly in traditional comparative biology. Fossils provide an outline of primatehistory constraining comparative analyses incorporating taxa and morpho-logical characteristics not represented in th e fossil record. Extant taxa with-out known prehistoric relatives may be interpolated into this outline usingdeductive cladistic analysis of morphological characteristics and overall mo-lecular similarity. Cladistic analysis provides a method for eva luat ing therelative strength of stratophenetic l inks between taxa. The phyletic nodeconnecting Anthropoidea-Adapoidea-Lemuroidea is analyzed here as an ex-ample: the link between Eocene Adapoidea and primitive Anthropoidea ap-pears stronger than that between Adapoidea and Lemuroidea because it isbased on shared-derived rather th an shared-primitive characteristics. Fullintegration of molecular results with morphological information requires abetter understanding of rates of molecular change over geological time. Ratesof molecular evolution can be studied using paleontologically documenteddivergence times for Prosimii-Anthropoidea (ca. 55 m.y.B.P.1, Platyrrhini-Catarrhini (ca. 40 m.y.B.P.1, and Hominoidea-Cercopithecoidea (ca. 25 m.y.B.P.). Immunological distances combined with these divergence times indi-cate th at primate albumin, widely used as a molecular clock in primatology,has evolved nonlinearly over geological time. A nonlinear albumin clockyields divergence times of about 9 million years before present for humansand chimpanzees, and about 13 million years before present for humans andorangutans (compared with 4 m.y.B.P. and 7 m.y.B.P., respectively, based ona linear albumin clock). Apparent slowing of albumin evolution over timeremains to be fully explained. Other proteins and nucleic acids may providebetter clocks. Cladistic analysis of morphological characteristics and compar-ative study of molecular structure, interpreted in th e context of the fossilrecord, promise to contribute to a more complete understanding of primateevolution.

Evolution is a complex subject encompassing the history of life and its governingprocesses. Our understanding of evolution is based on interpretation of patterns ofdiversity, ecology, behavior, visible morphology, and invisible molecular structurethat have changed and continue to change through time. The widely varyingorganic forms that surround us are a product of diversification over hundreds ofmillions of years of geological time. Evolutionary time, on a geological scale, is the

984Alan R. Liss, Inc.

8/13/2019 1330270504_ftp

2/16

Y E A R B O O K OF PHYSICAL ANTHROPOLOGY [Vol. 27, 19848domain of paleontology, and calibration of rates for numerous important processesdepends on evidence in the fossil record. The fossil record is necessarily the ultimatetest of many systematic and evolutionary hypotheses. I t is less complete for somegroups of organisms than one would hope, and hypotheses about their evolution a reconsequently untested and untestable. Primates, and mammals in general, have arelatively dense and continuous fossil record permitting hypotheses of relationshipsand rates to be explored in more depth than would otherwise be possible.Different approaches to evolution and different scales of inquiry yield patternsappropriate for understanding different processes. Some approaches answer specificquestions, while others are more general. Some approaches ultimately fail to answerany questions. There is a disturbing tendency in modern evolutionary studies foradvocates of one narrow viewpoint to see their approach as the only possible sourceof information bearing on a question, but this is usually related to limited under-standing of the question itself. Here I shall attempt to relate diverse patterns frompaleontology, comparative anatomy, and molecular biology to the study of primateevolution, concluding that paleontologists, cladists, and molecular systematists canlearn much more working together than any one group can learn working alone.

This essay is not an exhaustive review. It is intended rather to illustrate theinterdependence of paleontology, comparative morphology, and molecular systemat-ics. The fossil record provides an outline of primate phylogeny that can be aug-mented and refined using deductive cladistic methods. Recent taxa can beinterpolated into this augmented phylogeny on the basis of their molecular distancefrom taxa of known phylogenetic relationship. The final result should be a compre-hensive phylogeny based on all evidence of relationship. Such a phylogeny can beused to interpret the evolutionary history and comparative biology of al l morpholog-ical or behavioral characteristics of the organisms being studied. A particular groupof special interes t, our own order Primates, is used to illust rate these points.FOSSIL RECORD AND PRIMATE PHYLOGENY: STRATOPHENETICS

The concept of evolution as organic transmutation is a product of 18th- and 19th-century paleontology and biostratigraphy. Evolution was first used in this modernsense by Charles Lye11 in 1832. Pa tterns of organic diversity and morphology pre-served in the geological record are the proof of evolution. It is an established factth at life has a history, yet we have much to learn about phylogeny-the course ofevolution through time, and we have much to learn about evolutionary processes-how evolution works.Fossils were necessary for development of the modern concept of evolution, butclearly they were not sufficient. Darwins Origin of Species first published in 1859,builds on paleontological evidence, but it is not a treatise on fossils nor on the fossilrecord. Rather, Darwin combined observations on variation and inheritance in livingpopulations with an awareness of finite resources and artificial selection to explainpresent organic diversity a s a product of natural selection over long intervals oftime. In recent years, the inquiry has broadened, with evolutionary biologists nowexploring structure and diversity on a molecular level as well as organismal, species,and higher levels.In the century and a half since Cuvier first described a fossil primate, the fossilrecord has improved dramatically. What does th is tell us about primate phylogeny-about the diversification and genealogical relationships of primates in the past? Aholistic approach to primate history must consider the distribution of species intime, space, and form. Reductionists sometimes claim that morphology is the onlybiological attr ibute of organisms, but existence in time and space are also intrinsicattributes of life. Primates, like other organisms, are appropriately considered interms of their age and geographical distribution a s well as their form (Fig. I).We live in the present, and the diversity of primates is best known (althoughprobably not greatest) in the present. Hence, the present is a logical start ing pointfor reconstructing primate history. Primatologists generally agree in recognizing sixmajor groups of living primates: Hominoidea (apes and humans), Cercopithecoidea

8/13/2019 1330270504_ftp

3/16

8/13/2019 1330270504_ftp

4/16

6 Y E A R B O O K O F P HY SICA L AN THRO P O L O G Y [Vol. 27, 1984TABLE 1. Traditional classification of the order Primates

Known temporalClassification distribution Geographic rangeOrder Primates

Suborder Anthropoidea (Simii)Infraorder CatarrhiniSuperfamily Hominoidea 1)Superfamily Cercopithecoidea (2)Infraorder PlatyrrhiniSuperfamily Ceboidea (3)Suborder ProsimiiInfraorder LemuriformesSuperfamily AdapoideaSuperfamily Lorisoidea (4)Suuerfamilv Lemuroidea (5)Infraorder TarsiiformesSuperfamily Tarsioidea (6)Suborder PraesimiiInfraorder Tupaiiformes

Infraorder PlesiadapiformesSuperfamily Tupaioidea (7)Superfamily PlesiadapoideaSuperfamily Microsyopoidea

Oligocene-RecentEarly Miocene-RecentEarly Oligocene-Recent

Early Eocene-late MioceneEarly Miocene-RecentPleistocene-RecentEarly Eocene-Recent

Late Miocene-RecentMiddle Paleocene-late

Africa, Europe, Asia(worldwide today)Africa, Europe, AsiaSouth America

Africa, Europe, Asia,North AmericaAfrica, AsiaAfrica (Madagascar)Europe, Asia

AsiaNorth America, EuropeEoceneEarly Paleocene-late Eocene North America, Europe

Living superfamilies ar e numbered in paren theses for emphasis. Known temporal dis tributio n and geographic rangesare listed at righ t. Subordinal grouping corresponds to primate grades 1-3 of MacPhee et al. 1983).Taxonomic group without living representatives.

plification to be effective. Phylogeny and evolution, not classification, are the sub-jects of thi s paper, but classification necessarily enters the discussion and one mustbe careful to distinguish organization of the names we give to groups of animalsfrom relationships of the groups themselves.Given the six (or seven) superfamilial groups of modern primates, we can ask whathappens as each of these is traced backward through successively earlier epochs ofth e Cenozoic. Convergence of morphology as groups are traced back in time isevidence of common ancestry, and we can use this evidence to infer how primatesuperfamilies ar e related to each other. This approach to the study of phylogeny isas old as evolution itself, and it is often labeled the evolutionary or electricapproach to systematics. I coined the term stratophenetics (Gingerich, 1976) for thisapproach principally to distinguish it from cladistics a narrower comparative methodthat is also evolutionary in principle, butis sometimes based purely on morphologywith l itt le regard for time (see below).Stratophenetics recognizes that modern organisms can be rationally grouped onthe basis of overall similarity (i.e., phenetic resemblance in form; geographicaldistribution may be included a s well). Fossils in the geological record can be trea tedin the same way, combining species within stratigraphic intervals into groups basedon overall similarity in morphology (and geographical distribution). Stratigraphicsuperposition provides evidence of temporal ordering crucial for interpreting strataand contained fossils in light of what came before and after. Stratophenetics isempirical and, where the fossil record is reasonably dense, at the scale of a givenstudy (here the superfamilial level), similar taxa i n one time in terval may be linkedphenetically to those in adjacent or nearby intervals to provide a minimum spanningtree of living and fossil primates, taking into account their ages, geographicaldistributions, and morphology (Gingerich, 1979a,b). At the same time, the empiricalnature of stratophenetics, with emphasis on th e distribution of evidence, is useful inidentifying where evidence i s lacking (see below).An outline of primate phylogeny is sketched in Figure 2, bas5d on pheneticgrouping of fossil and living primates within intervals from the Paleocene to theRecent. These groups are linked i n tu rn to other similar forms in adjacent or nearby

8/13/2019 1330270504_ftp

5/16

Gingerich] PRIMATE EVOLUTION 61

T W OIIIIIIIIIIII

I\\\\\\\

IIIIIII__ _..-.~

I

k_I\ , I

L O S Lemur

I II II II III II I

\ /\ /

/I

\ . \/

/\ /VI

... .-.a~aech hon.- - ?. r. ;.9.--;1

Fig. 2. Stratophenetically constructed outline of primate phylogeny. Form is arrayed on the abscissa,and the ordinate encompasses Cenozoic time. Superfamilies of living primates (Tupaioidea, Tarsioidea,Cercopithecoidea, Hominoidea, Ceboidea, Lorisoidea, and Lemuroidea) ar e grouped at the top of the chart.Representative fossil primates known from partial or complete skulls are ordered in time and formrelative to other known fossils. Abundant bu t less complete dental remains support the patt ern of linkingshown here, bu t lit tle is known of the evolutionary history of Tupaioidea or Lorisoidea before the Miocene,Tarsioidea from the Oligocene to Recent, or Lemuroidea before the Pleistocene. Relationships of EoceneAdapoidea (including Cantius, Smilodectes, Notharctus, Mahgurita, and Adupis shown here) to Anthropo-idea and Lemuroidea are discussed in the text; deductive cladistic analysis indicates th at character isticsshared by Anthropoidea and Adapoidea a re predominantly derived, whereas characteristics shared byLemuroidea and Adapoidea are largely primitive. Lemuroidea and Lorisoidea may have diverged from aCantius- or Donrussellia-like ancestor as ear ly a s the late Paleocene or earliest Eocene, and Adupis mayor may not be a part of this clade. Note that Cercopithecoidea and Hominoidea converge near theOligocene-Miocene boundary (ca. 25 million years before present [m.y.B.P.], these groups together con-verge with Ceboidea near the Eocene-Oligocene boundary (ca. 40 m.y.B.P.), and all three anthropoidsuperfamilies together converge with Tarsioidea and hypothesized ancestral Lorisoidea and Lemuroideanear the Paleocene-Eocene boundary (ca. 55 m.y.B.P.). Tupaioidea, if correctly included in Primates,probably diverged from primitive plesiadapiform primates near t he beginning of the Paleocene.

8/13/2019 1330270504_ftp

6/16

Y E A R B O O K OF PHYS I CAL ANTHROPOLOGY [Vol. 27, 198462intervals. The ordinate in the bivariate diagram is time, considered a t the scale ofepochs, and the abscissa is form, expressed taxonomically at a superfamilial level.A third dimension, representing geographical distribution, could be added by liftinggroups of primates from each epoch out of th e page by a distance corresponding, say,to positions of th e continents on th e ear th's surface. Any fully representative quan-titative study would require multivariate treatment, and the present version ispurposely simplified.The stratophenetic outline of primate phylogeny shown in Figure 2 indicates thatprimates have undergone a number of successive radiations through the course ofCenozoic time. The firs t radiation, beginning in the early Paleocene with Pur ga terius, or a Purgatorius-like structural ancestor, gave rise to a diversity of specializedrodentlike forms (Plesiadapis, Phenacolemur, Microsyops, etc.).?'ree shrews (Tupaioi-dea) may be living representatives of the Purgatorius-like stem giving rise to alllater primates. Plesiadapiformes, like Tupaiiformes, lack diagnostic specializationsof more advanced primates of modern aspect, and there is some reasonable doubtabout whether they belong in Primates at all. Nevertheless, Plesiadapiformes aremost similar to Tarsiiformes and Lemuriformes among Eocene mammals, support-ing their inclusion in this order, broadly defined.A second radiation of primates, beginning in the early Eocene, features twodentally similar stem genera, Teilhardina and Cantius. Teilhardina apparently gaverise to a large radiation of tarsierlike Omomyidae (including Tetonius, Necrolemur,etc.) in the Eocene, and Teilhardina or a similar form ultimately probably gave riseto living Tarsius. Cantius, on the other hand, gave rise to a large radiation oflemurlike Adapidae in the Eocene (including Notharctus, Adapis, etc.). Adapidscombine a suite of dental characteristics seen in la ter ceboid, cercopithecoid, andhominoid primates with other features of the dentition, basicranium, and postcra-nial skeleton shared by lemuroids and lorisoids. Omomyids and adapids differ in theform of their incisor and canine teeth, and also in basicranial structure and postcra-nial skeletal anatomy.

Omomyidae resemble more primitive plesiadapiform primates dentally and insome basicranial structures, and I originally thought this might be an indication ofclose relationship (Gingerich, 1976; Gingerich and Schoeninger, 1977). Recent field-work in Wyoming bearing on the origin of early Eocene primates of modern aspectindicates that there is a subs tantial faunal turnover at th e Paleocene-Eocene bound-ary, with primates of modern aspect appearing as immigran ts (Rose, 1981). Conse-quently, there is now less reason to expect faunal continuity across this boundaryand less reason to expect the ancestors of Eocene Omomyidae to be preserved inPaleocene faunas sampled to date. In addition, newly discovered specimens of earlyCantius, Donrussellia, and Teilhardina indicate that it is difficult to distinguish th emost primitive Adapidae and Omomyidae. Thus Omomyidae probably represent adistinct tarsiiform radicle within the prosimian radiation rather than part of thepraesimian plesiadapiform radiation (Gingerich, 1981).The oldest certain representatives of higher primates (Anthropoidea) ar e OligoceneApidium and Aegyptopithecus, known from part ial skulls and extensive postcranialremains found in the Fayum Province of Egypt. Amphipithecus and Pondaungiafrom the la te Eocene of South Asia (and Oligopithecus from the Oligocene of Egypt)are known only from partial dentitions, but these show features of both Adapidaeand primitive Anthropoidea (Szalay, 1970; Simons, 1971; Ba Maw et al., 1979),linking the earliest anthropoids to a probable adapid origin (see Gingerich, 1980, forfull discussion). Another primitive anthropoid, Branisella, is known from the earlyOligocene of Bolivia (Hoffstetter, 19691, indicating that Ceboidea have inhabitedSouth America since at least early Oligocene times.The relationship of Cercopithecoidea and Hominoidea to earlier anthropoids isuncertain, but Old World monkeys can be traced back in the fossil record to earlyMiocene Victoriapithecus and Prohylobates in Africa (Szalay and Delson, 1979).Hominoidea can be traced back in time to early Miocene Proconsul in Africa, whichis so similar to Aegyptopithecus th at there is li ttle question th at the Egyptian genus

8/13/2019 1330270504_ftp

7/16

Gingerich] PRZMATE EVOL UTION 63belongs in Hominoidea a s well. Aegyptopithecus is simultaneously a suitable struc-tu ra l ancestor for Cercopithecoidea, although it lacks the bilophodont cheek teethcharacteristic of Old World monkeys. Aegyptopithecus differs from Cercopithecoideain crania l and postcranial features tha t can only be regarded as primitive or gener-alized for Catarrhini (Delson, 1975; Fleagle and Kay, 1982; Fleagle and Simons,1982).Modern Lorisoidea can be traced to early Miocene Mioeuoticus and allied forms(Walker, 19741, but lit tle is known of the origin and radiation of this group. Lemu-roidea are confined geographically to Madagascar today, and nothing is known oftheir evolutionary history before the late Pleistocene. Lorisoidea and Lemuroideamay be derived from Eocene Adapidae, but this link is based on shared primitivecharacteristics (discussed below), and there is l ittle direct evidence bearing on th equestion i n the fossil record.One advantage of organizing information about fossil primates stratophenetically(as in Fig. 2) is in permitting a realistic appraisal of what we know and do not knowabout primate history. This approach identifies important gaps in the fossil record.Hominoidea and Cercopithecoidea have a reasonably dense fossil record, and theycan be traced back through the Miocene to an Aegyptopithecus-like structural ances-tor in t he late Oligocene or earliest Miocene. Primitive anthropoids like Apidiumand Aegyptopithecus are most similar to Adapidae among Eocene primates. Adapidsappear to converge struc turally with primitive tarsioid Omomyidae a t the beginningof the Eocene. Paleocene primates are almost all highly specialized Plesiadapis-likeforms filling niches occupied today by rodents. The remainder of the chart in Figure2 indicates th at Tupaioidea have a possible (and questionable) relationship to pri-mates through primitive Plesiadapiformes, while Tarsioidea can be traced with someconfidence to Eocene Omomyidae. These links are based almost entirely on struc-tural similarity of preserved parts of the anterior dentition, cheek teeth, and basi-cranium, and there is li ttle evidence of connecting intermediates in the fossil recordfrom the Eocene to the Recent. Similarly, Lorisoidea and Lemuroidea are linked toeach other and to Adapidae on th e basis of dental, cranial, and postcranial similari-ties, but there is l ittle direct evidence for this connection in the Oligocene, Miocene,or Pliocene-Recent fossil record.Hypotheses based on stratophenetic linking are robust in the sense that theyattempt to incorporate all evidence in the fossil record-temporal, geographical, andmorphological-bearing on th e evolutionary history of a given group. New evidencesabout fossils andlor new fossils are required to test stratophenetic hypotheses ofphylogeny, and fortunately new fossils are found frequently in many parts of theworld.It should be emphasized that the importance of a paleontologically based stra to-phenetic outline of phylogeny, like that presented in Figure 2, extends beyondprimate paleontology. It provides a reference framework for comparative study ofprimates at all levels. Soft-anatomical characteristics, molecular traits, and evenbehaviors known only in living primates are properly compared and interpreted inlight of this framework. Cladistics and molecular studies permit augmentation andrefinement (see below), but the fossil record is the basis of what we know aboutprimate evolution. This is not to say t ha t the fossil record provides all (or even most)evidence about primate relationships. The fossil record provides litt le more than anoutline, but th is outline necessarily constrains interpretation of all evidence fromother sources. An outline of primate phylogeny based on the fossil record is objectivein a way that the alternative, an arbitrary scala naturae based on philosophicalpreconceptions, is not.

COMPARATIVE ANATOMY AND PRIMATE PHYLOG ENY: CLADISTICSCladistics is a comparative approach to study of the structure and relationships ofclades, groups of organisms shar ing common ancestry. Cladistics is practiced in twoforms, which are distinguished by different modes of assigning primitive or derivedpolarities to morphological characters. What I shall here call deductive cladistics

8/13/2019 1330270504_ftp

8/16

64 YEARBOOK OF PHYS I CAL ANTHROPOLOGY [Vol. 27, 1984proceeds from knowledge of the generalized common ancestor of a given group oforganisms, using the form of the common ancestor to assign primitive-to-derivedpolarities to morphological characters. Taxa are ordered and grouped at successivelylower levels on the basis of thei r shared derived features. Inductive cladistics beginswith hypothesized character polarities of terminal members of an evolutionaryradiation, inferring t he structure of successively more generalized common ances-tors from characteristics of the terminal members themselves.Deductive cladistic analysis, constrained by the fossil record, is an approach tophylogeny widely used in systematic biology for many years. Deductive cladistics issimilar to phenetics in grouping organisms on the basis of similarity, but here thesimilarity is of a restricted kind: similarity of shared, evolutionarily advanced(derived) characteristics. In a purely phenetic study, no account is taken of whichcharacters are primitive and which are derived. In a deductive cladistic study, theprimitive s tates of al l characters are given by the common ancestor of the groupunder study. Similarities inherited from a common ancestor (shared primitive fea-tures) do not influence subsequent groupings. The second step in cladistic analysisis to evaluate all possible tree diagrams or abstracted cladograms consistent withgiven polarities to see which are most parsimonious; that is, which diagrams ofrelationship require the smallest number of parallel evolutionary changes and thesmallest number of reversals. Given the common ancestor and character polaritiesdetermined from this, all such analyses have solutions (sometimes multiple solu-tions). And, one drawback to cladistic algorithms is that they always give answersat all scales of inquiry. Rarely is an attempt made to identify gaps in knowledge orto compare the relative magnitudes of gaps with those inherent in other studies.In a cladistic analysis, taxa of each pair being compared, say B and C, areseparated by a gap equal to the morphological and temporal distance from one taxonB) o the pairs hypothetical common ancestor (A) and back to the other taxon 0 .In other words, the gap is the distance B-to-A plus A-to-C. The minimum possiblegap occurs when B is in fact the ancestor of C (i.e., B corresponds exactly to A, B-to-A = 01, and the total gap is the distance B-to-C. A gap of B-to-Cis equivalent to thegap one would see in comparing B and C stratophenetically. In other words, gaps incladistic analyses are never smaller than those inherent in a corresponding strato-phenetic analysis.Inductive cladistics is a more recent development in systematics, initiated by anentomologist (Hennig, 1950,1966; see also Gaffney, 19791, and most actively pursuedby entomologists, ichthyologists, and ornithologists, all of whom study enormouslydiverse and complex groups of organisms with fossil records inadequate to documentthe origin of much of their modern diversity. Inductive cladistics has influencedsome paleontologists to deny fossils any special role in reconstructing phylogeny(Schaefferet al., 1972).A central problem in applying inductive cladistic methods is determination ofinitial primitive-to-derived character polarities. There are three standard ap-proaches to this problem: 1)outgroup comparison, in which closely related taxaoutside the group being studied are assumed to retain states primitive for allcharacters in the groups under consideration; (2) commonality, in which the relativefrequency of expression of characteristics within a group is assumed to identifyprimitive characteristics; and (3) ontogeny, in which the transformation of charac-ters during growth is presumed to recapitulate and reflect the sequence of appear-ance of characteristics during phylogeny. Outgroup comparison requires tha t theappropriate outgroup be known in advance (a given in deductive cladistics; one couldreasonably argue that knowledge of the appropriate outgroup makes an inductiveproblem deductive). This outgroup must retain all character states that the lastcommon ancestor shared with the group under study. Commonality assumes thatevolutionary advancement never involves acquisition of new characteristics permit-ting broad adaptive radiations, a n assumption contrary to much evidence for teleostsamong fishes, passerines among birds, rodents among mammals, and cercopithecoidsamong primates, to cite some common examples. Ontogeny, unfortunately, yields a

8/13/2019 1330270504_ftp

9/16

Gingerich] PRIMATE EVOLUTION 65most imperfect record of evolutionary history; i.e., many steps are not represented,and those that remain are difficult to relate to adaptations in adult animals. Anadditional problem arises when outgroups, commonality, and ontogeny yield conflict-ing results.If one knows the structure of a phylogenetic t ree, a t least in outline (as in deductivecladistics), it is usually possible to derive a most parsimonious interpretation of thepolarities of morphological characters distributed on the tree. Conversely, if oneknows the polarities of all morphological characters in advance, it is often possibleto construct a parsimonious cladogram representing one or more plausible phyloge-netic trees. In purely comparative studies, one is given neither the phylogenetic treenor the polarity of morphological characters, and there is consequently insufficientinformation to begin any kind of cladistic analysis. The only objective way out ofthis dilemma is to constrain cladistic problems stratophenetically (Cartmill, 1981),making them deductive. This is the approach used, explicitly or implicitly, by manyevolutionary systematists. It requires that some initial outline of the phylogeny ofagroup be determined empirically from the fossil record. Subsequent deductive clad-istic analysis i s guided by this stratophenetic outline.

The following example illustrates a problem that can profitably be studied usingdeductive cladistic reasoning within the context of a stratophenetic outline of phy-logeny. Adapidae (placed in a distinct superfamily Adapoidea in Table 1)are one oftwo dominant groups of Eocene primates (the other being tarsioid Omomyidae).Adapids have traditionally been regarded as Eocene lemurs because they shareimportant morphological resemblances with extant lemurs. These characteristicsinclude small brain size, lack of postorbital closure, relatively broad, simple, lemur-like upper molars, presence of a free ringlike ectotympanic bone in the middle ear,and a lemur- or lorislike postcranial skeleton. However, adapids share other impor-tant morphological resemblances with primitive anthropoid primates. These char-acteristics include the vertical, spatulate form of upper and lower incisors, possessionof a fused mandibular symphysis, and presence of robust, projecting, sexually di-morphic canine teeth.Adapids first appeared in t he fossil record in t he early Eocene, some 15-20 millionyears before the firs t anthropoids, and 50 million years before the first lemuroidsar e known in the fossil record. Given the much earlier appearance of Adapoidea inthe fossil record and the phenetic resemblances cited, it is plausible that Adapoideaare related to Anthropoidea and Lemuroidea in one of the three ways shown dia-grammatically i n Figure 3. Adapoidea may be broadly ancestral to Anthropoideabut not Lemuroidea (option A); Adapoidea may be broadly ancestral to both Anthro-poidea and Lemuroidea (option B ; or Adapoidea may be broadly ancestral to Lemu-roidea but not Anthropoidea (option C). The pattern of stratophenetic linkingdiscussed above and shown in Figure 2 would suggest initially that options A, B,and C are all equally likely. All are variations of the idea that an adapoidlikeancestor gave rise to Anthropoidea and Lemuroidea.Deductive cladistic analysis provides a method of evaluating the three possiblephylogenetic hypotheses relating Adapoidea, Anthropoidea, and Lemuroidea in thecontext of established trends of morphological evolution in primates. Hypothesis Aimplies that the superfamily Adapoidea is more closely related phyletically toAnthropoidea than either group is to Lemuroidea. This relationship is shown dia-grammatically in cladogram A of Figure 3. Hypothesis B implies tha t t he superfam-ily Lemuroidea is more closely related to Anthropoidea than either is to Adapoidea.This relationship is shown diagrammatically i n cladogramB of Figure 3. HypothesisC implies that superfamilies Lemuroidea and Adapoidea are more closely related toeach other than e ither is to Anthropoidea. This relationship i s shown diagrammati-cally in cladogram C of Figure 3.Cladograms A, B, and C can be evaluated by comparing the distribution ofcharacter states in each case. Five characters representative of the cranial morphol-ogy of adapoids, anthropoids, and lemuroids are shown, as listed here:

8/13/2019 1330270504_ftp

10/16

66 Y E A R B O O K OF P H Y S I C A L A N T H R O P O L O G Y [Vol. 27, 1984

A B C

PHYLOGENETICHYPOTHESES

ADAPO IMAI IY

Fig. 3 . Cladistic analysis of th e Adapoidea-Anthropoidea-Lemuroidea node shown in Figure 2. All threepossible arrangements of taxa are shown in phylogenetic hypotheses A, B, and C. Each phylogenetic treecan be redrawn as a cladogram (lower figures), and th e distribution of characters and character statesevaluated in the context of these cladograms. Primitive-derived character polarities are most reliablydetermined from the stratophenetic outline of phylogeny of the entire order shown in Figure 2 (see text).Primitive character states are drawn as open rectangles, and derived states are shaded. Note thatAnthropoidea and Adapoidea grouped together (cladogram A) are the only clade that shares derivedcharacter states. Anthropoidea-Lemuroidea (cladogram B) do not share any character states, and Lemu-roidea-Adapoidea (cladogram C) share primitive states. Consequently, phylogenetic hypothesis A carriesmore weight than B or C, and Lemuroidea may have diverged from a broad Adapoidea-Anthropoidearadicle at or near the time this radicle diverged from Tarsioidea. Interpreted in context of the knownfossil record, deductive cladistic analysis permits more refined hypotheses of relationship than wouldotherwise be possible.

Character Primitive sta te Derived sta te1.Postorbital bar2. Mandibular symphysis3 . Canine teeth4 ctotympanic5 . Postorbital closure

AbsentUnfusedProjecting, nondimorphicFreeAbsent

PresentFusedProjecting, dimorphicFusedPresentPrimitive or derived polarities are assigned to each character on the basis of thedistribution of character states near the adapoid-lemuroid-anthropoid node shownin Figure 2. Derived character states are shaded and primitive st ate s are unshadedin Figure 3. Presence of a postorbital bar (character 1) s a derived s tate shared byall of the taxa being compared. Characters 2 and 3, conformation of the mandibularsymphysis and form of th e canine teeth, are derived states in Anthropoidea andAdapoidea but primitive in Lemuroidea. Characters 4 and 5 , conformation of theectotympanic and condition of postorbital closure, ar e derived in Anthropoidea andprimitive in Adapoidea and Lemuroidea.By deductive cladistic criteria, the cladogram grouping Adapoidea and Anthropo-idea (cladogram A carries more weight than either of th e other possibilities becauseit is supported by shared derived character states (for characters 2 and 3). GroupingAnthropoidea and Lemuroidea as sister taxa relative to Adapoidea (cladogram B) isnot supported by any shared character states , and grouping Lemuroidea and Ada-poidea as sister taxa relative to Anthropoidea is supported only by shared-primitivecharacter sta tes (for characters 4 nd 5 ) .

8/13/2019 1330270504_ftp

11/16

Gingerichl P R I M A T E E V O L U T I O N 67This example illustrates how deductive cladistic analysis can be used to evalua tecompeting hypotheses considered to be equally likely on stratophenetic grounds.Preference for phylogenetic hypothesis A over hypotheses B and C is supported bythe shared-derived states of characters 2 and 3 in cladogram A. Thus the linkbetween Anthropoidea and Adapoidea shown in Figure 2 is stronger than that

between Lemuroidea and Adapoidea. Lemuroidea could as well be derived fromforms ancestral to known Adapoidea, whereas Anthropoidea are more likely to bederived from a structural ancestor within Adapoidea. While the analysis presentedhere is not exhaustive by any means, it is worth noting that Cartmill and Kay (1978)too found all links between adapoids and lemuroids to be based on primitive char-acteristics, concluding th at adapoids may be persistently primitive Haplorhini (anhypothesized clade including Anthropoidea and Tarsioidea but excluding Lemuro-idea and Lorisoidea). This i s equivalent to extending the lineage leading to Loris(Lorisoidea) and Lemur (Lemuroidea) in Figure 2 from a question mark in theOligocene, as shown, back to common ancestry with Teilhardina and Cantius/Donrussellia in the late Paleocene or early Eocene.MOLECULAR BIOLOGY AND PRIMATE PHYL OGENY; CALIBRATION O F MOLECULAR CLOCKSIn the past 20 years, precise methods have been developed for measuring differ-ences between living animals at a molecular level. The most widely used methodsare indirect, involving immunological or electrophoretic comparison of selected pro-teins and hybridization of nucleic acids. Direct sequencing of amino acids in proteinsand nitrogenous bases in nucleic acids is too time consuming to be applicable inbroad systematic studies. The topology of branching o f primate lineages derivedfrom molecular studies is generally consistent with tha t shown in Figure 2 (see, forexample, Dene et al., 1976; Sarich and Cronin, 1976). Prosimii diverged first fromAnthropoidea, then Platyrrhini and Catarrhini diverged within Anthropoidea, andfinally Hominoidea and Cercopithecoidea diverged within Catarrhini. (It is impor-tant to remember that phylogenies and divergence times are not necessarily con-gruent with classifications, and comparison here should be made with Fig. 2 rathertha n Table 1).Another interesting problem concerns rates of molecular evolution and the possi-ble clocklike behavior of evolution a t this level. Molecular clocks are calibrated bycomparison with one or more divergence times documented in the fossil record. Inthe order Primates, three divergence times are sufficiently well established on thebasis of fossils (Fig. 2) to be of importance:

1)Prosimii-Anthropoidea, divergence in the late Paleocene to middleEocene, average of estimated divergence times ca. 55 million yearsbefore present (m.y.B.P.).2) Platyrrhini-Catarrhini, divergence in the late Eocene to early Oligo-cene, average of estimated divergence times ca. 40 m.y.B.P.3) Cercopithecoidea-Hominoidea, divergence in the late Oligocene toearly Miocene, average of estimated divergence times ca. 25 m.y.B.P.

These divergence times are consistent with times published by Radinsky (1978)with two exceptions. It seems very unlikely that platyrrhines and catarrhinesdiverged as long ago as 5 5 m.y.B.P. or that prosimians and anthropoids diverged asrecently as 45 m.y.B.P. I would suggest 45 m.y.B.P. to be a more realistic upperlimit, and 40 m.y.B.P. to be a more reasonable average for divergence of Platyrrhini-Catarrhini. In addition, 50 m.y.B.P. is a more realistic lower limit, and 55 m.y.B.P.is a more reasonable average for the estimated time of divergence of Prosimii-Anthropoidea. Younger limits given for divergence times a re generally based on th edocumented appearance of both taxa being compared in the fossil record. Olderlimits are based on reasonably good worldwide coverage of mammalian faunaslacking primates of the grade in question. Mammals are sufficiently mobile geo-graphically, mammalian faunas are sufficiently well known, and there is sufficient

8/13/2019 1330270504_ftp

12/16

Y E A R B O O K O F P H Y S I C A L A N T H R O P O L O G Y [Vol. 27, 19848progressive evolution throughout primate history to make it reasonable to datedivergence times to within about 15 .It is generally assumed that underlying ra tes of molecular evolution fluctuateabout some uniform average rate over time, and i t is further assumed that observedrates of molecular evolution should be constant when measured over differentintervals of time. While the former assumption is reasonable, th e latt er assumptionis not. Fluctuations in evolutionary ra tes play a larger and larger role over longerintervals of time, systematically damping rates calculated over longer and longerintervals. Functional limits to the range of possible variations (and our inability tomeasure extremes) also depress rates measured over longer and longer intervals(Gingerich, 1983). In molecular terms, th e number of reversals and multiple substi-tutions at the same loci will be proportional to degree of divergence, yet thesereversals and multiple substitutions cannot be detected. Existence of a functionalcomponent in DNA and protein sequences means that molecular variation is chan-neled. Thus, even if actual underlying rates of mutation ar e constant over time,perceived rates should decrease with time (as they appear to do, for example, insequence divergence of mitochondria1 DNA, Brown, 1983; and probably DNA-DNAhybridization, Sibley and Ahlquist, 1981; but see Sibley and Ahlquist, 1984). Oneimportant consequence of this is th e expectation th at molecular differences shouldnot scale linearly with time: molecular clocks should be nonlinear. Many of theseand following points have been made in one way or another by Goodman (1963,1976), Read and Lestrel(1970), Uzzell and Pilbeam (19711, Kohne (19751, Read (19751,Benveniste and Todaro (1976), and Corruccini e t al. (1980). Important points contra-dicting prevailing views of molecular evolution and its relationship to geologicaltime can be illustra ted with reference to Sarichs (1968, 1970) original data onalbumin evolution in primates.To illustra te the nonlinearity of change on a molecular level, Sarichs (1968, 1970)immunological distances (ID) for Prosimii-Anthropoidea, Platyrrhini-Catarrhini, andCercopithecoidea-Hominoidea are plotted against divergence time (DT) in Figure 4,using the divergence times (DT) of 55, 40, and 25 million years discussed above.Sarich (1968, 1970) indicates tha t a linear model relating his immunological dis-tances and divergence times has the form

ID = 1.67 DT 1)and th is equation is plotted a s a dashed line in Figure 4 Linearity can be tested byfitt ing a simple power function to th e distribution, noting the value of the exponent(linearity requires a n exponent of 1.0). Using Sarichs (1968, 1970) immunologicaldistances with divergence times given here, the best-fit power function is

ID = 0.27 DT1.49 (2)and thi s equation is plotted a s a solid line in Figure 4.Regression of log ID on logDT is appropriatefor calculation of scaling coefficients because a range of ID valuesis known for each DT. Furthermore, regression of log ID on log DT, used here topredict divergence times within Hominoidea, yields more conservative scaling coef-ficients and younger divergence times th an would regression of log DT on log ID orcomputation of principal axes. The empirically derived exponent of 1.49 for albuminID scaling in primates has a 95 confidence interval of 1.31-1.67. I t is clearlysignificantly different from 1.00, indicating th at albumin immunological distancescales nonlinearly with divergence time in primates. (It may be noted parentheti-cally that the relative ra te test often used a s evidence of linearity works equallywell whether rate s scale linearly with geological time or not; thus, i t is not a t est oflineari ty on th is time scale.)The molecular clock th at best conforms to the empirical relationship of albuminimmunological distance and divergence time in primates is that given in Equation2. This clock can be used in conjunction with Sarichs (1970) mmunological distancesfor hominoid primates to estimate divergence times that cannot be establishedpaleontologically. Table 2 provides a comparison of divergence times estimated using

8/13/2019 1330270504_ftp

13/16

Gingerich] PRIMATE EVOLUTION 69

1 20 30 4 5 6DIVERGENCE T IME mtllions of years

Fig. 4. Nonlinear scaling of albumin evolution in primates. Immunological distance (ID) values areplotted against divergence times (DT) for the Cercopithecoidea-Hominoidea divergence (25 m.y.B.P.),Catarrhini-Platyrrhini divergence (40 m.y.B.P.), and Anthropoidea-Prosimii divergence (55 m.y.B.P.).Immunological distances ar e taken from Sarich (1968, 1970) and divergence times are based on stratophe-netic interpretation of the fossil record (Fig. 2). Sarich's model for a linear albumin clock (ID = 1.67 DT)is plotted as a dashed line. The nonlinear model proposed here for the same data (ID = 0.27 DT isplotted as a solid line (see text for discussion). Divergence times for apes and humans derived from thetwo models are compared in Table 2. If the mutation rate underlying molecular evolution is constant(linear, with an exponent of L O , time averaging of neutral mutations and multiple mutations a t the sameloci will cause perceived rate s to be nonlinear, with exponents less th an 1 0 he resulting curve shouldbe concave-downward rather than upward as observed here (solid line). This anomalous behavior iscommon in published molecular studies; it remains to be adequately explained.

TABLE 2. Comparison of divergence times DT)or apes and humans calculatedfiom albumin immunological distances ID) using the linear model of Sarich (1968,1970; Equation 1 in text) a nd nonlinear model proposed here (Equation 2 in text)'Albumin ID Divergence time (millions of years)Genera comDared (Sarich. 1970) Linear clock Nonlinear clock

Homo-Pan 7 4.2 8.9Homo-Gorilla 9 5.4 10.5HomePongo 12 7.2 12.8HomeHylobates 15 9.0 14.8HomeSymphalangus 15 9.0 14.8

These models are compared graphically in Figure 4.

8/13/2019 1330270504_ftp

14/16

70 Y E A R B O O K O F P H Y S IC A L A N T H R O P O L O G Y IVol. 27, 1984Equation 1 from Sarich and divergence times estimated using Equation 2 derivedhere. The principal differences of note a re in Sarichs divergence times of 4.2 and 7.2million years for human-chimpanzee H o m e p a n ) and human-orangutan H o m ePongo , respectively, based on a linear model, compared with much older divergencetimes of 8.9 and 12.8 million years, respectively, estimated here using the same dataand a nonlinear scaling model.Divergence times calculated here based on nonlinear scaling conform to divergencetimes estimated from the fossil record of hominoid evolution much better thandivergence times based on linear scaling. However, divergence times based onnonlinear scaling of albumins still sample differences in a single protein. It is highlydesirable that other approaches like DNA-DNA hybridization (Sibley and Ahlquist,1984),based on a much broader sample of the genome, be calibrated paleontologi-cally, because once this is done, DNA-DNA hybridization promises to contribute amore refined chronology of human evolution.The scaling of immunological distances illustrated in Figure 4 raises anotherserious question. As discussed above, measures of molecular difference (like ID)should increase less rapidly over longer and longer measurement intervals (DT).One would expect the solid curve in Figure 4 to be concave downward rather thanconcave upward. The exponent of DT should be less, not greater, than 1.0. Goodman(1976; see also Goodman et al., 1983) has noted, in other contexts, the apparentslowdown or deceleration of molecular evolution over time implied by the concave-upward shape of the solid curve in Figure 4, explaining this a s a result of decreasingmutation rates and intensification of stabilizing selection in the course of primateevolution. If mutation rates are decreasing and stabilizing selection intensifying,the underlying rate of change in primate albumins might really be scaling with anexponent of 1.5 o r more (the exponent of 1.49 that we perceive empirically isnecessarily lower than the actual underlying r ate of change because of the effects oftime averaging). Explanation of observed deceleration of molecular evolution inprimates in term s of decreasing mutation ra tes and stabilizing selection may becorrect, but other explanations are also possible. We would do well to examinemolecular data that do not show expected effects of time averaging in a very criticallight.

CONCLUSIONSPaleontology plays a fundamental role in documenting the major features ofprimate evolution. Fossils will never tell the whole story, but they have uniqueimportance in relating visible morphology and molecular structure to geologicaltime, a dimension of primary importance for evolutionary studies. The fossil record,interpreted stratophenetically, provides an outline of primate phylogeny, and thisoutline can be refined and amplified using deductive cladistic principles and meth-ods, increasing our understanding of systematic relationships and character evolu-tion beyond what can be learned from fossils alone.The fossil record provides divergence times essential for measurement of ra tes ofevolution on a molecular scale. Clocklike regularities in molecular evolution, inter-preted in light of temporal scaling, can be used in tu rn to estimate divergence timesnot well constrained by fossils. Clearly paleontologists, comparative anatomists, andmolecular biologists have much to learn from each other, and integration of discov-eries from all three fields will lead to a more complete understanding of our evolu-tionary past.

ACKNOWLEDGMENTSThis essay reflects the influence of far too many colleagues to acknowledge eachindividually. I than k Drs. Daniel Fisher and David Pilbeam for discussion, and Drs.Catherine Badgley, Matt Cartmill, Charles Sibley, B. Holly Smith, and an anony-

mous reviewer for reading and improving earlier drafts of the manuscript. Figureswere drawn by Karen Klitz. This research was supported by National ScienceFoundation grant BNS 80-16742.

8/13/2019 1330270504_ftp

15/16

Gingerich] P R I M A T E E V O L U T I O NLITERATURE CITED

71

Ba Maw, Ciochon, RL, and Savage DE (1979) LateEocene of Burma yields ear liest anthropoid pri-mate Pondaungia cotteri. Nature 282;:65-67.Benveniste, RE, and Todaro, GJ (1976)Evolution ofType C viral genes: Evidence for an Asian originof man. Nature 261:lOl-108.Brown, W (1983) Evolution of animal mitochon-dria l DNA. In M Nei and RK Koehn (eds): Evolu-tion of Genes and Proteins. Sunderland SinauerAssociates Inc., pp. 62-88.Cartmill, M (1981) Hypothesis testing and phylo-genetic reconstruction. 2. 2001. Systematik Evol.Forsch. 19:73-96.Cartmill, M, and Kay, RF (1978) Cranio-dentalmorphology, tarsier affinities, and primate subor-ders. In DJ Chivers and KA Joysey (eds): RecentAdvances in Primatology. London: AcademicPress, pp. 205-214.Corruccini, RS, Baba, M, Goodman, M, Ciochon,RL, and Cronin, J E (1980) Non-linear macromole-cular evolution and the molecular clock. Evolu-tion 34:1216-1219.Delson, E (1975) Toward the or igin of Old Worldmonkeys. In: Evolution des Vertebres-Problemesactuels de Paleontologie. COIL Int. C.N.R.S.2182339-850.Dene, HT, Goodman, M, and Prychodko, W (1976)Immunodiffusion evidence on the phylogeny ofthe primates. In M Goodman, RE Tashian, andJH Tashian (eds): Molecular Anthropology. NewYork: Plenum Press, pp. 171-195.Fleagle, JG, and Kay RF (1982) New interpreta-tions of the phyletic position of Oligocene homi-noids. fn RL Ciochon and R Corruccini (eds): NewInterpretations of Ape and Human Ancestry. NewYork: Plenum Press, pp. 181-210.Fleagle, JG, and Simons, EL (1982) The humerusof Aegyptopithecus zeuris: A primitive anthropoid.Am. J. Phys. Anthropol. 59:175-193.Gaffney, ES (1979) An introduction to the logic ofphylogeny reconstruction. In J Cracraft and NEldredge (eds): Phylogenetic Analysis and Paleon-tology. New York: Columbia University Press, pp.79-111.Gingerich, PD (1976) Cranial anatomy and evolu-tion of early Tertiary Plesiadapidae (Mammalia,Primates). Univ. Mich. Pap. Paleontol. 15:l-140.Gingerich, PD (1979a) Stratophenetic approach tophylogeny reconstruction in vertebrate paleontol-ogy. In J Cracraf t and N Eldredge (eds): Phyloge-netic Analysis and Paleontology. New York:Columbia Univeristy Press, pp. 41-77.Gingerich, PD (1979b)Paleontology, phylogeny, andclassification: An example from the mammalianfossil record. Syst. Zool. 28:451-464.Gingerich, PD (1980) Eocene Adapidae, paleobi-ogeography, and the origin of South AmericanPlatyrrhini . In RL Ciochon and AB Chiarelli (eds):Evolutionary Biology of the New World Monkeysand Continental Drift. New York: Plenum Press,pp. 123-138.

Gingerich, PD (1981) Early Cenozoic Omomyidae

and the evolutionary history of tarsiiform pri-mates. J. Hum. Evol. 10:345-374.Gingerich, PD (1983) Rates of evolution: effects oftime and temporal scaling. Science 222:159-161.Gingerich, PD. and Schoeninger. MJ (1977) Thef osd record and primate phylogeny.J. Hum. Evol.6483-505.Goodman, M (1963) Mans place i n t he phylogenyof the primates as reflected in serum proteins. InSL Washburn (ed): Classification and Human Ev-olution. Chicago: Aldine, pp. 204-234.Goodman, M (1976) Toward a genealogical descrip-tion of the primates. In: M Goodman, RE Tashian,and JH Tashian (eds): Molecular Anthropology.New York: Columbia University Press, pp. 321-353.Goodman, M, Baba, ML, and Darga, LL (1983) Thebearing of molecular data on the cladogeiiesis andtimes of divergence of hominoid lineages. In RLCiochon and RS Corruccini (eds): New Interpreta-tions of Ape and Human Ancestry. New York:Plenum Press, pp. 67-86.Hennig, W (1950) Grundziige einer Theorie derPhylogenetischen Systematik. Berlin: DeutscherZentralverlag.Hennig, W (1966) Phylogenetic Systematics. Ur-bana: University of Illinois Press.Hoffstetter, R (1969) Un primate de IOligocene in-ferieur sud-americain: Branisella boliuiana gen.et sp. nov. C.R. Acad. Sci. [D](Paris)269:434-437.Kohne, D (1975) DNA evolution data and its rele-vance to mammalian phylogeny. In WP Luckettand FS Szalay (eds): Phylogeny of the Primates.New York: Plenum Press, pp. 249-264.MacPhee, RDE, Cartmill, M, and Gingerich, PD(1983)New Paleocene primate basicrania and def-inition of the order Primates. Nature 301:509-511.Napier, JR, nd Napier, PH (1967)A Handbook ofLiving Pr imates. New York: Academic Press.Radinsky, L (1978)Do albumin clocks run on time?Science 200: 1182-1183.Read, DW (1975) Primate phylogeny, neutral mu-tations and molecular clocks. Syst. Zool. 24:209-221.Read, DW, and Lestrel , PE (1970) Hominid phylo-geny and immunology: a critical appraisal. Sci-ence 168:578-580.Rose, KD (1981) The Clarkforkian Land-MammalAge and mammalian faunal composition acrossthe Paleocene-Eocene boundary. Univ. Mich. Pap.Paleontol. 26:l-196.Sarich, VM (1968) The origin of the hominids: animmunological approach. In: SL Washburn andPC J ay (eds): Perspectives on Human Evolution.New York: Holt, Reinhart, and Winston, pp. 94-121.Sarich, VM (1970)Primate systematics with specialreference to Old World monkeys: A protein per-mective. In: JR NaDier and PH NaDier (eds): OldWorld monkeys. New York: Academic Press, pp.175-226.

8/13/2019 1330270504_ftp

16/16

72 Y E A R B O O K OF P H Y S I C A L A N T H R O P O L O G Y [Vol. 27, 1984Sarich, VM, and Cronin, J E (1976) Molecular sys-tematics of the primates. In M Goodman, RETashian, and JHTashian (eds): Molecular Anthro-pology. New York: Plenum Press, pp. 141-170.Schaeffer, B, Hecht, MK, and Eldredge, N (1972)Phylogeny and paleontology. Evol. Biol. 6:31-46.Sibley, CG, and Ahlquist, J E (1981)The phylogenyand relationships of the r ati te birds as indicatedby DNA-DNA hybridization. In GGE Scudder andRL Reveal (eds): Evolution Today, Proc. SecondInt. Congr. Syst. Evol. Biol. Pittsburgh: Hunt Inst.Botanic Document., pp. 301-335.Sibley, CG, and Ahlquist, J E (1984)The phylogenyof the hominoid primates a s indicated by DNA-DNA hybridization.J. Mol. Evol. (in press).Simons, EL (1971) Relationships of Amphipithecusand Oligopithecus. Nature 232489-491.

Simons, EL (1972)Primate Evolution: An Introduc-tion to Mans Place in Nature. New York:Macmillan.Szalay, FS (1970) Late Eocene Amphipi thecus andthe origins of cata rrh ine primates. Nature227355-357.Szalay, FS, and Delson, E (1979) Evolutionary His-toryof the Primates. New York: Academic Press.Uzzell, T, and Pilbeam, D (1971) Phyletic diver-gence dates of hominoid primates: A comparisonof fossil and molecular data. Evolution 25:615-635.Walker, A (1974)A review of the Miocene Lorisidaeof East Africa. In RD Martin, GA Doyle, and AWalker (eds): Prosimian Biology. London: Duck-worth, pp. 435-447.