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Primate Origins, Human Origins, and the End ofHigher TaxaMATT CARTMILL

When people learn that I study human evolution and we start talking about it,

they sometimes ask me, ‘‘How long ago did the first humans live?’’ My answer

is usually another question: ‘‘What do you mean by ‘humans’?’’ That response

seems as baffling and wrong-headed to them as their question seems to me,

and it usually takes us a while to straighten things out.

To most people, what ‘‘human’’means is clear. Everybody can sorthumans out instantly from othersorts of things. Humans are upright,bipedal mammals with big brainsand dextrous hands. They share aunique reliance on technology, acapacity for culture, and a gift forgab. Humans draw pictures and tellstories. They look at the stars andwonder what they are and how they

got there. As far as we can tell, even

the smartest and most humanlike of other animals do none of thesethings. A few very clever birds andapes can be taught to use a rudimen-tary me-Tarzan-you-Jane sort of ‘‘protolanguage,’’ but nobody thinksthat parrots or bonobos will ever tellstories, draw pictures, or wonderabout the stars.

Most people see all these humantraits as inseparable parts of a single

distinctive package. So did the earlyevolutionary biologists. Our intelli-gence, language, and technology giveus a unique degree of control andmastery over our environment.Charles Darwin and his early fol-lowers accordingly assumed that anyevolutionary changes in a humanlikedirection — toward more perfectbipedality, bigger brains, andincreased use of tools and weapons— would have been naturally advan-tageous and more or less self-explan-atory. It was widely believed that all

these trends had gone on in parallelthroughout the course of humanevolution.

From around 1930 to 1950, thisway of thinking was reinforced andgiven a theoretical basis in the writ-ings of G. G. Simpson and W. E. LeGros Clark. In his influential books,Le Gros Clark portrayed the humanevolutionary trends as the culmina-tion of trends that had operatedthroughout primate evolution. But

after World War II, new fossil discov-eries and new themes in the work of Simpson, Le Gros Clark, and othershelped bring about a new perceptionof evolutionary change as more dis-continuous. In this new view of

things, the family Hominidae andother higher taxa were seen as hav-ing originated through adaptive shiftsthat involved and imposed new selec-tion pressures and brought new mor-phologies into existence. These sup-posed discontinuities were used bysystematists to draw grade bounda-ries between basal wastebasketgroups and descendant taxa distin-guished by what we would now callsynapomorphies. In this respect, theascendancy of cladistic reasoning,terminology, and systematics that

began in the late 1960s only codifiedand formalized a change in thinkingthat was already underway.

Our theorizing and argumentationabout the origins of higher taxa —the huge, contentious scientific liter-ature centered on such themes ashuman origins, primate origins,mammal origins, amniote origins,and so on — is rooted in these post-war habits of thought. In what fol-

lows, I want to sketch the history of these ideas, reexamine them in thelight of current paleontological

knowledge, and argue that highertaxa and their supposed evolutionaryimportance are illusory.

SIMPSON AND MESOZOIC

MAMMALS

In 1926, the young American pale-ontologist G. G. Simpson, who had

just written his thesis on NorthAmerican Mesozoic mammals, went

Matt Cartmill’s early work developed the‘‘visual predation theory’’ of early primateevolution that he proposed in his 1970doctoral thesis from the University of Chicago. His subsequent writings andongoing research include studies of pri-mate morphology and phylogeny; thecomparative anatomy of the eye, ear,and skull; theoretical systematics; theevolution of mammalian locomotorbehavior and adaptations; the biologicalcorrelates of language, morality, andconsciousness; and the history and phi-losophy of evolutionary science. He isthe co-author of textbooks of human

anatomy ( Human Structure, 1987) andpaleoanthropology ( The Human Lineage,2009), and the author of the award-win-ning history of ideas A View to a Death in the Morning (1993). He currentlyserves on the faculty of Boston Univer-sity and the emeritus faculty of DukeUniversity. Email: [email protected]

VVC 2012 Wiley Periodicals, Inc.DOI 10.1002/evan.21324Published online in Wiley Online Library(wileyonlinelibrary.com).

ISSUES

Evolutionary Anthropology 21:208–220 (2012)

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off to London to study their OldWorld counterparts in the BritishMuseum. The focus of Simpson’sattention was an enigmatic group of

animals called tritylodonts. Becausethese creatures had an orbit conflu-ent with the temporal fossa, hetero-dont dentitions, and molar teeth withmultiple cusps and roots, they weregenerally regarded as mammals. Butalthough the tritylodonts wereamong the earliest mammals known(from the uppermost Triassic), theywere already highly specialized,somewhat rodent-like herbivores,with big incisors and a postincisordiastema (Fig. 1A).

In 1926, tritylodonts were thought

to be ancestral multituberculates(Fig. 1B), and multituberculates werethought to be marsupials. Therefore,tritylodonts were marsupials. Thisimplied that marsupials must havediverged from the living monotremeswell back in the Triassic, at a timebefore mammals of any sort appearin the fossil record.

Simpson’s study of the Mesozoicmammals in the British Museum5

was a turning point in the history of

systematics. He tentatively agreedthat the tritylodonts were probablymultituberculates; but he noted thatthey retained a lot of primitive, rep-

tile-like traits not found inundoubted multituberculates fromthe Jurassic onward. And he foundno reason for thinking that any of these beasts had anything to do withthe marsupials.

Simpson’s arguments weregrounded in a cladistic approach tophylogenetic reconstruction. Thisfact needs to be stressed, because amyth has grown up that Willi Henniginvented cladistic reasoning. Thewords ‘‘apomorphy’’ and ‘‘plesio-morphy’’ are Hennig’s, but the con-

cepts were familiar to Simpson andhis contemporaries, and he usedthem in a perfectly cladistic way.Again and again in his 1928 mono-graph, Simpson examines supposedlyrelevant traits invoked by others anddismisses them as irrelevant becausethey are either symplesiomorphies(‘‘primitive characters which give noevidence of special affinity’’5:167) orconvergences. And when it came tothe then-prevalent big picture of the

ascent of mammals — through asequence of concentrically arrangedgrades, with marsupials evolvingfrom monotremes and giving rise to

placentals — Simpson said exactlywhat we would say today: ‘‘Is thisnot, in fact, simply a recrudescenceof the old naıve conception of a scalanaturae[?] ... Because there are threegreat groups of mammals todaywhich exhibit varying degrees of retention of primitive characters, itdoes not follow that they representthe survivors of so many naturalgroups of which each of the moreadvanced was derived from the onenext less so.’’5:162

Rejecting this model, Simpson

concluded that there were, in fact,four big monophyletic groups of mammals, and that they had allattained a mammalian grade of mor-phology, with a temporomandibular

jaw joint (TMJ) and three earossicles, independently of each other.The tree diagram that he presented(Fig. 2) depicts the class Mammaliaas polyphyletic, with the boundarybetween reptiles and mammals hav-ing been crossed four separate times.

Figure 1. Reconstructed skulls representing some extinct taxa mentioned in the text. A. The Jurassic tritylodont Bienotherium yunnanense ;

B. The Paleocene multituberculate Taeniolabis taoensis ; C. The Oligocene eutherian Anagale gobiensis ; D. The Paleocene plesiadapi-

form Plesiadapis tricuspidens . (Redrawn after Romer,1 Hopson,2 Simpson,3 Szalay and Delson4: not to same scale.)

ISSUES Primate Origins, Human Origins, and the End of Higher Taxa 209

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For Simpson, this was not a rea-son for discarding that importantboundary. As he saw it in 1928,higher taxa like Mammalia could bedefined not only by shared derivedtraits, but also by shared derivedtrends — by parallel development of similar features from homologousantecedents in closely related line-ages, driven by the same selectionpressures. This was not an entirelynew idea — Mivart had said similar

things 45 years earlier6

— but Simp-son’s work lent it new authority.

Thanks to Le Gros Clark, Simp-son’s 1928 approach to the definitionof higher taxa became a cornerstoneof the study of primate evolution.While Simpson was working on histhesis at Yale, Le Gros Clark hadpublished papers7,8 arguing that treeshrews should be admitted as basalmembers of the order Primatesbecause they shared a toothcomb, anintrabullar eardrum, and otherlemur-like traits with the primates of

Madagascar. Le Gros Clark’s ideasabout tree shrews meshed perfectlywith Simpson’s ideas about system-atics. For the next three decades, thetwo men acted in concert to producea body of work that established whatprimates were and what primatologymeant. In successive editions of hisbooks, Le Gros Clark 9,10 defined theorder Primates in Simpsonian terms,as a collection of lineages evolving inparallel in the same direction:

namely, towards the acquisition of grasping hands and feet, flattened

nails, bigger brains, reduced olfac-tion, keen forward-facing eyesenclosed in bone, and so on. Thesetrends were depicted as adaptiveresponses to life in the trees. All pri-mates showed these trends, but theywere differently expressed — andmust have evolved in parallel tosome degree — in different groups of primates.11–14

Primates, as classically defined,thus became an order that simplyhad no synapomorphies — no defin-ing properties. For example, in Simp-son’s canonical mammal classifica-tion in 1945,15 Anagale from the Oli-gocene of Mongolia, which is nowgenerally regarded as a relative of rodents and rabbits, became a pri-mate, because Simpson3 thought itwas related to tree shrews and LeGros Clark thought tree shrews wereprimitive lemurs — even though Ana- gale itself (Fig. 1C) bore no derived

resemblances to lemurs or any otherliving primates.

ADAPTIVE SHIFTS

But a transformation of thistrend-based sort of systematics wasalready in the making. The new wayof thinking had its roots in Simp-son’s own 1944 book Tempo andMode in Evolution,16 whichaddressed the theoretical problems

of what we would now call stasisand punctuation in the fossil record.Goldschmidt, Abel, A. H. Clark, andother saltationists had pointed tothese phenomena as evidence forthe operation of different processes

in micro- and macroevolution. Tak-ing his cue from the populationgenetics of the 1930s, and especiallyfrom Sewall Wright’s17 concept of the adaptive landscape, Simpsonargued that the apparent discontinu-ities were produced during phasesof rapid microevolutionary change,resulting from founder effect andnew selection pressures operating insmall isolated populations. ‘‘Thetheory here developed,’’ Simpsonwrote, ‘‘is that mega-evolution nor-mally occurs among small popula-

tions that become preadaptive andevolve continuously (without salta-tion, but at exceptionally rapidrates) to radically different ecologi-cal positions. The typical patterninvolved is probably this: A largepopulation is fragmented intonumerous small isolated lines of descent. Within these, inadaptivedifferentiation and random fixationof mutations occur. Among manysuch inadaptive lines one or a feware preadaptive, i.e., some of theircharacters tend to fit them for avail-

able ecological stations quite differ-ent from those occupied by their im-mediate ancestors. Such groups aresubjected to strong selection pres-sure and evolve rapidly in the fur-ther direction of adaptation to thenew status. The very few lines thatsuccessfully achieve this perfectedadaptation then become abundantand expand widely, at the same timebecoming differentiated and special-ized on lower levels within thebroad new ecological zone.’’16:123

Does all this sound familiar? It

should. As this quotation demon-strates, and as Simpson, Gould, andEldredge all acknowledged in oneway or another,18,19 Simpson’s 1944book incorporated most of the signif-icant elements of the theory of punc-tuated equilibrium,20 including nor-mative evolutionary stasis in somegroups, allopatric speciation, andrapid macroevolutionary change gen-erated by species-level selectionamong randomly generated new spe-

Figure 2. G. G. Simpson’s 1928 phylogram summarizing his hypothesis of the polyphyletic

origin of Mammalia.5:183 Simpson’s ‘‘Pantotheria’’ is roughly equivalent to the ‘‘Trechno-

theria’’ of modern systematists (Fig. 3).

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cies. In Tempo and Mode, Wright’smetaphor of the adaptive landscape— which had been a microevolution-ary concept, applied to a multidi-mensional space measured in allelefrequencies — was transformed into

a macroevolutionary concept appliedto a morphospace of phenotypictraits. By describing morphologicalchange over geological time in termsgrounded in population genetics,Simpson closed the gap betweenmicro- and macroevolution, andthereby furnished a paleontologicalcapstone for the neo-Darwinian syn-thesis.21,22

The model of ‘‘mega-evolution’’proposed in Tempo and Modebecame a key ingredient in the rede-finition of the Hominidae that took

place during the rise of the ‘‘newphysical anthropology’’ in the 1950s.With the unmasking of the Piltdownfraud23 and the discovery of surpris-ingly humanlike Australopithecuspostcranial remains from the Trans-

vaal, it became apparent that the dis-tinctive suite of traits seen inhumans today had not come intobeing as a single complex driven bypersistent evolutionary trends. Ca-nine reduction and bipedal locomo-tion had appeared long before theenlargement of the brain.

Nevertheless, the disjunctionbetween the simian past and thehuman future was maintained andreinforced by positing an adaptiveshift at the beginning of the hominidcareer. It was generally agreed thatthere must have been some changein ecology — what Simpson16 calleda ‘‘radically different ecological posi-tion’’ — that had led to bipedalityand canine reduction, and that thischange had imposed a new selectiveregime that favored the evolution of other human peculiarities. From the

mid-1950s through the 1960s, thecrucial anthropogenic change wasgenerally taken to have been a shiftto more predatory habits.24

Despite this growing consensus,the hominid pretensions of Australo- pithecus continued to be challengedby some experts who regarded itsapelike traits as barring it frommembership in the human family.Originally a skeptic himself,25 LeGros Clark was persuaded of the

hominid status of the australopithe-cines only after he went to SouthAfrica to study the original fossils.26

He then found himself defending Australopithecus as a member of thehuman family against the attacks of

people like Solly Zuckerman, whorefused to see it as a hominidbecause it resembled apes in manyways.27,28 Le Gros Clark counterat-tacked by inventing cladistics, or atany rate some new terms for talkingabout cladistic concepts. The thingsthat Australopithecus had in commonwith apes, he insisted, were only‘‘characters of common inheritance’’— what we call symplesiomorphies— and therefore irrelevant to deter-mining relationships. But thehumanlike traits of the australopithe-

cines were ‘‘characters of independ-ent acquisition’’ — that is, synapo-morphies — and those traits provedthat the man-apes were stem-grouphominids.25:23

None of this directly contradictedthe earlier writings of Simpson andLe Gros Clark. Using cladistic meth-ods to reconstruct phylogeny is com-patible with a trend-based conceptionof the boundaries and meaning of higher taxa. But Le Gros Clark’sdefense of Australopithecus was partof a bigger and more turbulent pic-

ture. During the 1960s, the wholeSimpson-Le Gros Clark synthesisbegan to disintegrate under the pres-sure of new fossil finds and new ideas.

This ferment was evident in a se-ries of papers published in 1959 and1960 in the journal Evolution, inwhich several authors reviewed theevidence for the polyphyletic originof mammals and drew differing con-clusions. Simpson29 continued toinsist that ‘‘Mammalia’’ is and oughtto be a polyphyletic class. But Olson,Reed, and Van Valen30–32 argued that

the multiple parallelisms seen amongthe mammal-like ‘‘reptiles’’ of theUpper Triassic had resulted from anearlier adaptive shift to a mamma-lian type of physiology, which couldbe used to define a more inclusivebut monophyletic class Mammalia.Van Valen concluded that ‘‘(1) tetra-pod classes should be defined on thebasis of their major adaptive differ-ences, (2) that the mammalian gradeof adaptation was largely reached in

the therapsids, and (3) that the ther-apsids should therefore be includedin the Mammalia.’’32 Reed insistedthat ‘ ‘a taxon should be a clade(whenever determinable) and not agrade.’’31

During the 1960s, Van Valen was aleading exponent of a sort of purifiedSimpsonism that paved the way forthe triumph of Hennig in the follow-ing decade. Van Valen’s systematicsadmitted grade-based higher taxa,but he insisted that they had to beboth adaptively coherent — definedby a basal adaptive shift — and notpolyphyletic. By that latter standard,Le Gros Clark’s order Primates andSimpson’s class Mammalia did notqualify. In an influential 1965 paper,Van Valen showed that if Plesiadapis

and its relatives (Fig. 1D) were pri-mates, as their cheek teeth indicated,then the postorbital bars and othersupposedly lemur-like features of tree shrews had to be either primi-tive mammalian traits or convergen-ces.33 Van Valen accordinglyremoved the tupaiids from the pri-mates. A similar move was urged byR. D. Martin in a 1968 paper, whichparalleled Van Valen’s and markedthe first appearance of the words‘‘symplesiomorphy’’ and ‘‘synapo-morphy’’ in the primate literature.34

Van Valen was one of my teachersin graduate school. I adopted hispurified Simpsonism in my doctoralthesis and early publications, and Ifollowed Van Valen and Martin inexcluding tupaiids from Primateson cladistic grounds.11,35–38 But Ialso excluded the stem-group pri-mates, the plesiadapiforms, onadaptive grounds, invoking VanValen’s criterion of the basal adapt-ive shift. Other successful arborealmammals, I argued, had shown notendency to evolve primate-like

morphology, nor was there anyfunctional reason why they should.A comparative survey convinced methat the most convergently primate-like animals were small, bush-dwell-ing marsupials, which had devel-oped grasping feet and reducedclaws for climbing around in net-

works of thin branches, and hadevolved big, convergent eyes forpredatory purposes, much like catsand many other visually directed


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predators. I accordingly posited anadaptive shift, to visually predatoryhabits in a fine-branch milieu, asthe marker for the grade boundaryseparating Primates from the basalwastebasket order Insectivora. Andsince the somewhat rodent-like ormultituberculate-like plesiadapi-forms showed none of these fea-tures or trends, I insisted that theymust have branched off from thecrown-group primates prior to the

key adaptive shift, and that they tooshould accordingly be excludedfrom the primate order.

Today, all this seems somewhatbeside the point. In the context of today’s strictly cladistic systematics,taxa are not grades defined by adapt-ive shifts, but clades defined byshared derived features (which iswhy whales are artiodactyls andducks are dinosaurs). Most defini-tions of the primates today accord-

ingly include the plesiadapiforms asstem-group primates and reserve theterm ‘‘Euprimates’’ for the crowngroup. Such definitions of Primatesexpress Van Valen’s phylogeny in thecontext of Hennig’s philosophy of

systematics.Nevertheless, debates over primateorigins continue to be couched in thesame Simpsonian terms that I laid

down in the early ‘70s. Textbooks of physical anthropology will tell youthat there are three or four theoriesof primate origins: the old arborealtheory, which describes the eupri-mate traits (or trends) as the inevita-ble outcome of life in the trees; thesimilar ‘‘grasp-leaping’’ theory of F.S. Szalay, who sees the euprimatetraits as having originated as adapta-

tions to acrobatic leaping intrees;39,40 my ‘‘visual-predation’’theory;35–38 and R. W. Sussman’s

thesis that the euprimate traits origi-nated in connection with the exploi-tation of fruit and nectar.41,42

But this narrative of conflictingtheories falls apart on closer exami-nation. Although one can imagineobservations that would count deci-sively against some of these theo-ries,43 none of them is couched interms of any defining metrics thatwould exclude the others. What per-

centage of insects in the diet does ittake to qualify (or disqualify) an ani-mal as a visually directed predator?If an extinct animal has a graspinghind foot, moderately elongated tar-sals, Microcebus-like molars, and bigfrontated orbits, but is too small torely on leaves as a protein source,does that mean that it is adapted tograsp-leaping, fruit-eating, visualpredation, or all three?

At a deeper level, all of these theo-ries seem to me to be answers to thewrong question. There is no reason

to think that primates, or any otherhigher taxa, originated through adefining adaptive shift. To show whyI believe this, I want to go back toSimpson’s original question.

MAMMAL ORIGINS?

We know far more today about theMesozoic relatives of mammals thanSimpson did in 1928. When youapply the methods of cladistic

Figure 3. Cladograms showing two possible phylogenetic hypotheses concerning the

accretion of mammalian synapomorphies and some of the synapomorphies marking

each of the hypothesized nested clades. A. Hypothesis excluding multituberculates from

crown-group mammals; B. Hypothesis including multituberculates within the crown group.

Based on Jaworowska, Cifelli, and Luo,44 with modifications and additions from other

sources.45–52

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phylogeny reconstruction to the cur-rent fossil record, something like thecladograms in Figure 3 emerges. I

say ‘‘something like’’ because, as

usual, experts differ on the contents,names, and connections of hypothet-ical clades. Some prefer to excludemultituberculates from the mamma-lian crown group (Fig. 3A); othersthink they belong inside it (Fig.3B).44 But no matter how you orderthe successive branches, the facts of the case and the rules of cladisticsystematics yield the same sort of picture. There is no adaptive shiftthat defines Mammalia. There is onlya long, geologically slow cascade of accumulating small apomorphies:

pineal foramen lost, then the unifica-tion of the prootic and opisthotic,then the TMJ established, then theappearance of the trigone and trigo-nid, and so on. In the tree shown inFigure 3A, the main feature that uni-tes the crown-group Mammalia (alldescendants of the last commonancestor of all living mammals) is aparticular arrangement of the molarcusps. If this is all it means to be amammal, then explaining mammal

origins has ceased to be a particu-larly interesting problem.

Of course, we can pick an apomor-phy that seems bigger and more im-

portant than the others and use thatto define an adaptively more mean-ingful class Mammalia. One traitthat has often been regarded asdefinitively mammalian is the pres-ence of three ear ossicles, signalingthe complete detachment of thearticular from the lower jaw and thefinal loss of the old reptilian jaw

joint. In the cladogram of Figure 3B,this is depicted as a synapomorphyof a clade Mammalia that includesmultituberculates as well as the liv-ing mammals. But there are reasons

for thinking that this is not so, andthat the definitive mammalian mid-dle-ear apparatus evolved in parallelthree or four different times in dif-ferent groups.

In the reptilian ancestors of mam-mals, the lower jaw initially formedin the embryo as a curved cartilagi-nous rod called Meckel’s cartilage,part of the skeleton of the first pha-ryngeal arch. The proximal end of this cartilage ossified as the articular

bone, which formed a jaw joint withthe quadrate at the base of the skull.Membrane bones condensing aroundMeckel’s cartilage provided attach-ment sites for teeth and muscles andtransmitted bite forces from the teeth

to the articular. A similar arrange-ment persisted in the Late Triassicancestors of all Mesozoic ‘‘mammals’’(Fig. 4). In today’s mammals, the

lower jaw is formed exclusively fromthe tooth-bearing dentary bone,rechristened the mandible. A newTMJ is formed between the dentaryand the squamous temporal (squa-mosal). Meckel’s cartilage is mostlyresorbed in the fetus, and most of theother lower-jaw bones are lost. Thethree that persist (angular, articular,and prearticular) lose their connec-

tions with the mandible and areincorporated into the middle ear asthe ectotympanic and the body andanterior process of the malleus,respectively.

However, most Mesozoic ‘‘mammals’’show a variety of intermediate condi-tions. Meckel’s cartilage may persistas a cartilaginous or bony rod lodgedin a ‘ ‘Meckelian groove’’ on themedial side of the mandible. Theangular, articular, or prearticularmay continue to transmit somechewing forces as well as sound

waves. When they do, they remainattached to a postdentary trough orsulcus behind the Meckelian groove,and the quadrate-articular joint doesdouble duty as a secondary jaw jointand as a conduit of sound vibrationsto the stapes.

One of the earliest mammal-likeforms, the shrew-sized Hadrocodium wui from the Early Jurassic of China, had a lower jaw formedentirely from the dentary and lackingthe Meckelian groove and postden-tary sulcus.55 Therefore, Hadroco-

dium had a fully mammalian middleear (MME), like those of today’smonotremes, marsupials, and euther-ians. So did all known multitubercu-lates. But many later mammaloidsretained a Meckelian groove or post-dentary sulcus, and therefore lackedan MME.56 One such creature wasthe Early Cretaceous Maotherium; itsmiddle-ear bones were still attachedto the mandible by an ossified Meck-el’s cartilage lying in a Meckelian

Figure 4. Jaws and teeth of the Triassic ‘‘mammal’’ Morganucodon . A. Lateral view of

upper and lower dentition; B. Medial view of lower jaw. Abbreviations: an, angular

(¼ectotympanic); ar, articular (¼malleus); co, coronoid; de, dentary; mg, Meckelian

groove; pa, prearticular (¼anterior process of malleus); qu, quadrate (¼incus); sp, sple-

nial; su, surangular; TMJ, temporomandibular joint. Modified from Cartmill and Smith,53 af-

ter Crompton.54


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groove.51 This is awkward becauseMaotherium is a spalacotheroid, amember of a clade closely related totherians and excluding the ancestorsof Hadrocodium, multituberculates,and monotremes (Fig. 3). If the ossi-

fied Meckel’s cartilage is a primitiveretention in Maotherium, then theMME must have evolved separatelyin each of those three groups, and afourth time in the lineage leading tomarsupials and eutherians.

The initial descriptions of Maothe- rium51,57 sought to avoid this conclu-sion by proposing that its ossifiedMeckel’s cartilage was an evolution-ary reversal, a derived adult reten-tion of fetal middle-ear morphologyin an animal having ancestors thathad possessed an MME. But this

seems unlikely for two reasons. First,the anterior part of Meckel’s carti-lage never ossifies in any extantmammals; the cartilage is resorbedor converted into a ligament in laterontogeny.58,59 In Maotherium, thereverse was the case: the embryoniccartilage became ossified in later de-

velopment, as in Morganucodon (Fig.4). This cannot simply represent apedomorphic retention of what wasonce a fetal character state in anancestor with fully modern ear anat-omy and development. Second, it is

hard to see why natural selectionwould have favored the spread of amutation that caused the malleus tolose its independence and reattach tothe mandible.

There are other facts that militateagainst seeing the MME as a mam-malian synapomorphy retained fromthe last common ancestor of Hadroco- dium and modern mammals. EarlyCretaceous monotremes from Aus-tralia may have retained a full com-plement of reptilian lower-jaw bones,with a Meckelian groove and a post-

dentary trough.46,60

The presence of postdentary dermal bones in earlymonotremes is debated,61 but themalleus was still solidly connected tothe mandible (by a persistent prear-ticular and an ossified Meckel’s carti-lage) in both basal trechnotheres(symmetrodonts) and some ‘‘tricono-donts.’’56,62 Barring multiple evolu-tionary reversals, the last commonancestor of therians and triconodonts— and also that of the crown-group

mammals — therefore must havelacked a fully mammalian middle ear.

The current evidence thus suggeststhat the MME evolved in four sepa-rate groups: therians, monotremes,multituberculates, and some ‘‘trico-

nodont’’ subgroup that included Hadrocodium. It is both significantand ironic that these are exactly thefour groups that Simpson identified in1928 as having crossed the reptile-mammal boundary in parallel (Fig. 2).

LESSONS FROM MAMMAL

‘‘ORIGINS’’

The fourfold origin of the mamma-lian ear brings two points into sharp

focus. First, we should expect thatclosely related animals will oftenevolve in parallel, especially in waysthat are related to basic adaptations.Once the TMJ is established and themalleus and incus have started trans-mitting sound waves to the stapes,the development of three auditory

ossicles and the loss of the otherbones in the lower jaw is more orless a foregone conclusion. We knowthis, because it happened four times.Likewise, once the reversed-triangle‘‘symmetrodont’’ occlusal pattern hadbeen established, the evolution of atalonid on the lower molars wasextremely probable. We know this,because functional talonids(including pseudotalonids) evolvedseparately in three or four symme-

trodont lineages.49:70,63 Once the heelprocess of the calcaneus had beendeveloped, the shift of the talus uponto the top of the calcaneus wasextremely probable. We know this,because it happened in two or three

separate lineages of Mesozoic mam-mals.48 And so on. Apomorphies thatare adaptively significant, like theMME, the talonid, or the reorganiza-tion of the tarsals, have an increasedlikelihood of appearing independ-ently in closely related lineages, sim-ply because similar animals are sub-

ject to similar adaptive pressures.(The traditional distinction betweenparallelism and convergence recog-nizes this fact, which is obscured bylumping the two together as ‘‘homo-plasy.’’) And because adaptively sig-

nificant apomorphies are heavilycanalized by antecedent evolutionarynovelties, they do not always mapaccurately onto cladogenetic events.This insight underlay Simpson’s deci-sion to accept low-level polyphyly asa component of his systematics.

The second point is an essentiallyanalytical truth. All clades begin witha cladogenetic event — a speciation— and every speciation generatestwo sister clades. Therefore, the aver-age number of systematic differencesseparating any two sister clades

must, by definition, be of exactly thesame magnitude as the average num-ber of such differences between twosister species. All differences betweensister taxa, at any level of the Lin-naean hierarchy, will ultimately befound in almost all cases to be minordifferences of the sort that distin-guish sister species within a genus.

It follows that higher taxa, andtheir supposed evolutionary impor-tance, are illusions born of pervasiveextinction and pervasive humanignorance. As that ignorance dissi-

pates, the illusion of higher taxaevaporates with it. If, following aspeciation event, major adaptive dif-ferences appear later on between the

descendants of two sister species,they do so as a result of subsequentanagenesis and cladogenesis withineach clade. Speciation events them-selves never correspond to majoradaptive innovations. Adaptive shiftsare real, but they are not abrupt; andso we cannot expect differences

. . . the average numberof systematic differencesseparating any two sister

clades must, bydefinition, be of exactly

the same magnitude asthe average number of

such differencesbetween two sister

species.

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between cladistically defined highertaxa to be adaptively significant. Theclusters of apomorphies definingthese larger groupings appeared seri-atim, and were few and minimallymarked in their early manifestations.And of course, this was anotherinsight underlying Simpson’s rejec-tion of strict monophyly in classifica-

tion. As Simpson put it in a 1960 let-ter to C. A. Reed on the subject of mammalian origins: ‘‘When you didget down to the single species or ge-nus that you are seeking in order tomake the taxon truly monophyleticin the very narrowest sense, youwould find that there were closelyrelated genera of the same family or

closely related species of the samegenus that were not ancestral to themammals. You would then, in alllogic, have to refer two species of thesame genus or two genera of thesame family to two different classes.

That obviously is not practical and inthe exigencies of the classificatorysituation you simply have to seek some different solution.’’31

The origin of mammals was not anevent. It was a gradual, widespreadhistorical process, involving the slowaccumulation over fifty million yearsof a hundred small apomorphies(and their pleiotropic correlates), of-ten driven by inevitable trends thatcaused key features to appear in par-allel in multiple lineages.50

We can sum all this up in three

words: Simpson was right. We areleft with two alternatives: eitherretain monophyletic taxa and accept

that all differences between sistertaxa will eventually turn out to betrivial, species-level distinctions — orelse define higher taxa in a Simpso-nian way that admits low levels of polyphyly.

PRIMATE ORIGINS?

The cladograms in Figure 5 derive

from recent publications about early

primate phylogeny by JonathanBloch and his colleagues.64,73 Thesecladograms were constructed in theusual way, by assembling a long listof characters, partitioning each oneinto discrete character states, andthen using various statistical andcomputational procedures to try togenerate a tree that necessitates thesmallest number of state transitions.Such methods assume that we knowwhat weights to assign to charactersand character-state transitions inassessing phylogenetic relationships,

and that we can produce objective,phylogenetically neutral descriptionsof morphology. Both assumptionsare demonstrably false,53:55-58;66,74,75

and so we are not obliged to take very seriously the trees that thesemethods produce.

But whatever we think of theirdetails, these cladograms are plausi-ble in their broad outlines, and wecan accept them provisionally for thesake of argument. As in the case of

Figure 5. Cladograms showing two possible phylogenetic hypotheses concerning the

accretion of primate synapomorphies and some of the synapomorphies marking each of

the hypothesized nested clades. A. ‘‘Maximally parsimonious’’ cladogram presented by

Bloch and colleagues.64 B. Alternative cladogram positing an unnamed carpolestid-

euprimate clade that excludes other plesiadapiforms. Some other recent analyses yield

a plesiadapiform-dermopteran clade as the sister group of euprimates.65 Based on Bloch

and coworkers,64 with modifications from other sources.49,66–72


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the early mammals, they present apicture of gradualistic accretion of small derived traits — first a clusterof changes in molar occlusal pattern,then elongation of the phalanges of the hand, then shortening of the

metatarsals, then elongation of thetarsals and a cluster of cranial innovations — with every stage in theaccretion being documented by a se-ries of stem groups branching off theline leading to the last commonancestor of the living primates. Thisis the same pattern that we find inthe early mammaloids, and one thatwe would expect to find on the basisof theory.

One seemingly important differ-ence between the two cladograms of Figure 5 concerns the placement of

the Carpolestidae. Where known,stem-group primates (Plesiadapi-formes) appear to have hands andfeet rather like those of tree shrewsor squirrels, with clawed digits andonly slightly divergent first toes. Butat least one carpolestid, Carpolestes simpsoni from the Late Paleocene,had a divergent hallux bearing a flat-tened nail. Bloch and Boyer76,77 orig-inally interpreted this as a synapo-morphy linking the family Carpoles-tidae to Euprimates (Fig. 5B).However, in more recent analyses

that incorporate more characters,Bloch and his colleagues group car-polestids in a clade with the othernonmicrosyopid plesiadapiforms(Fig. 5A).59,72 This phylogeny impliesthat grasping feet probably evolvedindependently in C. simpsoni andeuprimates.

Carpolestes retains primitivelyshort tarsal bones and laterallydirected orbits with no postorbitalbar. Bloch and Boyer concludedfrom this that ‘‘the ancestor of Eupri-mates was primitively an arboreal

grasper adapted for terminal branchfeeding rather than a specializedleaper or visually directed preda-tor.’’76:1606 But this conclusion doesnot follow , no matter w hat weassume about carpolestid affinitiesor behavior. The last common ances-tor of Euprimates must have hadapomorphies not found in its lastcommon ancestor with carpolestids.These apomorphies could have origi-nated as adaptations connected to

behaviors not shared with carpoles-tids, such as leaping or visualpredation.

Whichever cladogram we adopt,the story presented in Figure 5 seemsto document a gradual accretion of

grasping features of the feet, begin-ning with elongated manual pha-langes and proceeding through rela-tively short metatarsals and a nail onthe hallux, to an elongated tarsusand nails on all the digits. Bloch andhis colleagues now analyze these fea-tures as representing progressivestages in adaptation to grasping rela-tively small supports in the trees, cul-minating in the euprimate occupa-tion of ‘‘... a small-branch nichewhere grasping is more useful thanclaw clinging, and bridging is more

effective than bounding.’’64:1161,72

The closest nonprimate analogs, theyconclude, are found among small

marsupials. These new conclusionsseem to me to bear out what I saidin 1970.

Nevertheless, Bloch and his col-leagues still do not accept visual pre-dation as an explanation for the cul-minating peculiarities of the eupri-mates, because of ‘‘the inferredomnivorous or herbivorous habits of many early euprimates, even at smallbody size.’’64:1163 This objection is

irrelevant for two reasons. (1)Although some of the earliest eupri-mates were probably herbivores ormixed feeders, others appear to havebeen visually directed predators.78,79

We cannot determine which dietarypreference is oldest by countingnoses. (2) More fundamentally, it isnot clear how close in time the ear-liest (Lower Eocene) fossil eupri-mates are to the earliest euprimates.Most molecular-clock estimates pointto a date of around 85 million yearsago for the ancestral euprimate

node.80–82

This is some 35 millionyears before the first appearance of euprimates in the fossil record.Although the validity of these esti-mates is debated,83 the surprisingrecent discovery of a mid-Jurassicplacental mammal84 suggests thatthe molecular divergence dates maybe closer to the truth than the cur-rent paleontological estimates. If so,then Eocene fossils are not going totell us much about the ecology of the

first euprimates. In the present stateof our knowledge, the main evidencefor the ecological correlates of theeuprimate peculiarities has to comefrom functional and comparativeanatomy.

Comparative anatomy reveals nonecessary connection between grasp-ing hind feet and visual predation.Divergent, prehensile marginal toesand reduced claws have evolved in-dependently in several groups of small arboreal mammals w ithdiverse feeding habits, includingstrict herbivory ( Hapalomys, Chiro- podomys) as well as visual predation( Burramys) and mixed feeding onboth fruit and insects (Microcebusspp.).85–92 Although some think oth-erwise,93,94 the evidence seems to me

to continue to support the widelyaccepted notion13,40,95–99 that hind-foot prehensility and claw reduction

originally appeared in all these line-ages as an adaptation to locomotionin what Charles-Dominique and Mar-tin100 called ‘‘the fine branch andcreeper niche.’’ But this tells us noth-ing about diet, because the habitualuse of small-diameter supports iscompatible with eating any sort of resource available in such milieus:insects, nectar, fruits, insect andplant secretions, or some mixture of

these. Most of the living animals thathave been proposed as models forthe ancestral euprimates are mixedfeeders, and it seems likely that thefirst euprimates were too. If theywere smaller than any living prima-tes, as has been argued, we wouldexpect them to have had a corre-spondingly more insect-centereddiet.101

As Bloch and his cow orkersacknowledge,64 the visual peculiar-ities of euprimates — enlarged, fron-tated, and approximated eyes and

orbits, reduced retinal summation,enlargement of the visual parts of the brain, and a complete postorbitalbar — seem to have evolved laterthan at least the initial stages of spe-cialization for pedal grasping(Fig. 5). I continue to think that thestriking apomorphies of the eupri-mate visual system and facial skele-ton originated in connection with vis-ually directed predation on insects,not as adaptations for grasp-leaping

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or eating fruit and nectar.102 Movingthe eyes closer together makes themless, not more, effective in estimatingdistances stereoscopically duringleaping, because it reduces parallax.Close-set eyes enhance stereoscopy

only over short distances. And thenotion that the euprimate refinementsof the visual system represent an ad-aptation for feeding on fruits andnectar is contradicted by comparativeoptic anatomy. Among living prosi-mians and small marsupials, insect-eating forms (Tarsius, Microcebus,Sminthopsis) have markedly keenerretinal resolution and greater pupil-lary mobility than do specializedfruit- and nectar-feeders (Cheiroga-leus, Tarsipes).103–107 Fruit- and nec-tar-feeders do not need keen vision,

because fruits and flowers are notcryptic. After all, angiosperms evolvedfruits and flowers for animals to eat,

and they typically advertise them withshiny bright colors and sweet smells.Virtually the only nonprimate mam-mals in which both eyes point inexactly the same direction are either

visual predators (e.g., cats) or the fru-givorous descendants of visual preda-tors (e.g., kinkajous).

The kinkajou case reminds us thatfrugivory has evolved more thanonce in faunivorous mammals, usu-

ally in connection with arboreal hab-its. Similar shifts to a more exclusivediet of angiosperm products (andlarger body size) probably occurredindependently in several groups dur-ing the early radiation of the eupri-mates. The anthropoids may be sucha group. Although their affinities arewidely debated, most of the fragmen-tary early (Paleocene to mid-Eocene)fossils that have been proposedrecently as candidate basal anthro-poids ( Eosimias, Algeripithecus, Bire-tia, Altiatlasius, Anthrasimias) exhibit

some combination of diminutivesize, moderately trenchant cheek teeth, and enlarged orbits, suggestingderivation from a small, visuallypredatory ancestor.101,108–113

Can we then still attribute the ori-gin of the distinctive euprimate traitsto a basal adaptive shift involving

visually directed predation? I amnow inclined to think that the wholenotion of a defining adaptive shiftthat accounts for ‘‘primate origins’’ is

another hallucination born of igno-rance. Certainly, things happened inthis part of the cladogram to bringall this new morphology into being.But there are multiple novelties asso-ciated with the discontinuity between

the primate stem groups (plesiadapi-forms) and the crown group (eupri-mates). These include changes in thefacial skeleton, the eyes themselves,the visual and olfactory parts of thebrain, and the hands and feet.64,73 If we knew more, we would surely findthat these euprimate novelties didnot appear abruptly, but throughgradated stages. (For instance, Iwould expect to find euprimateancestors with incomplete postorbi-tal bars like those of domestic cats.)The various euprimate synapomor-

phies may have come into beingsequentially, and perhaps for differ-ent reasons. For example, the multi-ple apomorphies of the hindlimbbones that Szalay and his co-authorssee as crucial euprimate traitsrelated to leaping may have comeinto being before, after, and/or to-gether with the euprimate specializa-tions of the visual system, and mayhave a totally unrelated adaptive ba-sis or bases.

Even in the present imperfectstate of our knowledge, the defining

adaptive shift that the contestingtheories of primate origins offer toidentify has begun to evaporate.Several recent accounts64,102,114 sug-gest that the features that distin-guish primates from other mam-mals today originated through agradual accretion of small adaptivechanges, producing a cascade of more and more concentricallyarranged taxa with smaller andsmaller clusters of less and less im-portant synapomorphies (Fig. 5),

just as we saw in the early mam-

mals. And as in that case, we seemto be picking up significantamounts of parallel evolution of keytraits under similar selective pres-sures (e.g., in the opposable halluxof Carpolestes). We may eventuallyfind that some of the features thatwe think of as euprimate synapo-

morphies came into being independ-ently in different lineages of Creta-ceous or Paleocene euprimates, justas the mammalian middle ear and

tribosphenic molars evolved inde-pendently in more than one lineageof early ‘‘mammals.’’

HUMAN ORIGINS?

Similar things can be said aboutthe origins of anthropoids or homi-noids — or of ‘‘humans,’’ whateverthat means. Humanness is not acoherent package. We have knownsince the 1960s that our terrestrialbipedality evolved more than twomillion years before the onset of what was long held to be ‘‘... the fun-damental human characteristic, thatis the great development of thebrain.’’115 If Ardipithecus is a homi-nin, then canine reduction similarlypreceded terrestrial bipedality. If

Ardipithecus is a hominin and anabove-branch arboreal quadruped,many ‘‘hominoid’’ apomorphies tradi-tionally analyzed as adaptations forsuspensory posture and locomo-tion116 must have evolved in parallelin at least six different groups of Y-5catarrhines ( Homo, Gorilla, Pan,Pongo, Oreopithecus, and gibbons),sometimes for unrelated reasons.117

The affinities and adaptations of Ardipithecus remain controver-sial.118–120 But there is conclusive

evidence that a lot of supposedly

human features were acquired inparallel in different lineages of Pleis-tocene hominins. Probable parallel-isms include the increased basicra-nial flexion and other basicranialapomorphies seen in late robust Aus-tralopithecus species53:194; molarreduction and humanlike changes inthe pelvis and hand in A. sediba121–123;brain enlargement in some habilines(KNM-ER 1470) and facial and den-tal reduction in others (KNM-ER1813); and so on. If our family treewithin the genus Homo is as bushy

and speciose as some like to think,124

then parallel evolution was alsorampant throughout the later Pleisto-cene, with brain enlargement andcorrelated cranial changes takingplace independently between 1.0 and0.3 Mya in the local Homo popula-tions of Africa, Java (Ngandong),Europe (Neandertals), and perhapsin other isolated demes. Even at thespecies level, modern Homo sapiens(whatever that means) seems to have


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come into existence in Africa in acascade of fits and starts, in whichsmall novelties of anatomy andbehavior that appeared and persistedin local demes were graduallyassembled into a complex that could

be successfully exported, with someforeign admixture, to other parts of the world.125,126

In the accretion of the many smallnovelties that add up eventually to anadaptive shift, the details of each stepare contingent on the ones that wentbefore it. But this truth does not war-rant any conclusions of the sort urgedby the late Steven J. Gould127 con-cerning the overall contingency of ev-olutionary change. Examples of mul-tiple parallelisms (as in the origins of the mammalian ear or the tribos-

phenic molar) demonstrate that oncecertain apomorphies are in place,others can predictably be expected tofollow. I like to think that once an apehad come to the ground and adopteda bipedal form of locomotion thatfreed its forelimbs for other uses,humanness was more or less inevita-ble — and that any Pleistocenehuman population, from Homo ergaster onward, would, in the ab-sence of competitors, eventually haveevolved into an animal capable of pro-ducing pots, pyramids, and the Py-

thagorean theorem. I doubt that wewill ever know for sure.

CONCLUSION

The evolutionary narrative is not astory of quantum evolution andadaptive shifts. What we see in theemergence of mammals, and prob-ably in the emergence of primates,and in the origins of the subtribeHominina and its subdivisions, is anendless cascade of small apomor-phies accumulating through the fine-

tuning of ancestral morphology bynatural selection, in connection withspecies-level changes in adaptation.

If this is true, then I think thatmost higher taxa will eventually proveto be either polyphyletic or unimpor-tant. And I also think that the accu-mulating evidence to this effect indi-cates something important about evo-lution in general. Evolution is —surprise! — Darwinian. On the whole,it is gradualistic and selection-driven.

All the stories of human discontinuitythat some evolutionists have spun,involving abrupt shifts in adaptation— a sudden decisive descent from thetrees, or a crucial shift to predation,or a change in the regulatory genome

that produced humanness throughsome big heterochronic transforma-tion — all these ideas are fantasies,born ultimately of our wish to seeourselves as more decisively set off from other animals than we actuallyare. I feel confident that we will even-tually find that the basal differencesbetween the human clade and that of our closest living relatives are nogreater than those between, say,chimpanzees and bonobos, and that‘‘the gap between humans and chim-panzees, between a few termites for

lunch and Beethoven, is filled withincremental steps.’’128 As we learnmore, we can expect this to prove

true of other, higher taxa as well.

ACKNOWLEDGEMENTS

I thank John Fleagle for invitingme to write this article and for his

valuable editorial guidance. The finaldraft has benefited from the com-ments and suggestions of DougBoyer, Kaye Brown, Jeremy DeSilva,Cheryl Knott, Bill Hylander, Erik Seiffert, Ian Wallace, and an anony-mous reviewer. I am grateful to them— and to all the friends, colleagues,and students at Boston University,Harvard University, and Stony Brook University who heard and critiquedpreliminary presentations of theseideas — for their help and encour-agement.

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Evolutionary Anthropology 21:220 (2012)

CORRIGENDUM

In the article by Matt Cartmill and Kaye Brown, ‘‘Being Human Means that ‘Being Human’ Means Whatever We SayIt Means’’ (EA 21:183), the sentence beginning ‘‘In recent literature, this supposed human peculiarity has been

predicated of everything from allomothering to projectile weapons’’ should have begun, ‘‘In recent literature, thissupposed human peculiarity has been traced to causes ranging from allomothering to projectile weapons.’’ We regretthe error, which resulted from an editorial misreading of proof corrections.

CORRIGENDUM

220 Cartmill ISSUES

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