CROTCHETS & QUIDDITIES

A Metaphoric Rise to StardomKENNETH M. WEISS AND HEATHER A. LAWSON

In 1951, Sherwood L. Washburn, aleading physical anthropologist, an-nounced a landmark prospectus forwhat he called the “new physical an-thropology” (Fig. 1).1 He said thatphysical anthroplogy largely com-prised opinions on dry metric datawith little theoretical foundation.We needed that kind of foundation,and he had one to offer. Fifty-someyears later, progress in the fieldmeans that it’s time for a newerframework and again, one is waitingin the wings.

GENES IN PRINCIPLE

Washburn challenged us to adoptthe perspective of the modern evolu-tionary synthesis, which, in the 1930s,had unified paleontology, Darwinianevolution, and Mendelian inheritance.The modern synthesis defined evolu-tion as changes in the frequency ofalleles (genetic variants). This re-solved several knotty problems thathad prevented the development of aunified theory of life.

A unifying theory had become pos-sible for various reasons. Mendel’swork had shown that discretely in-herited “elements” could transmittraits from one generation to thenext and the same principles were

found to apply to plants and animalsas well. Mendel only considered sim-ple qualitative traits, but it was latershown mathematically that manygenes acting in concert could pro-duce the quantitative traits that wereso important to Darwin’s gradualis-tic view of evolution. Mendel’s ele-ments, dubbed “genes” in 1910, mu-tated occasionally, supplying thevariation that could be screened byDarwin’s natural selection to pro-duce adaptive divergence and theformation of new species. Compara-tive anatomy, functional adaptation,taxonomy, and paleontology hadbeen separate areas of research thatsometimes seemed incompatible.But now they could all be accountedfor by a single evolutionary processworking on genes. Finally, we had aconsistent, comprehensive, univer-sally applicable theory of life.

The genetic theory of life was soelegant and persuasive that it was ac-cepted even though at the time therewas little knowledge of what genes ac-tually were or how they worked. Itsufficed to assume that stable, herita-ble something-or-others existed andwere the universal cause of biologicaltraits. A deep faith in genes justifiedexplaining the phenotypes we caredabout—the fossils in the ground andthe living primates on it—in terms ofadaptive genetic evolution. The theoryprovided a program for research aswell as the confident ethnusiasm thataccompanies the pursuit of funda-mental truth. This perspective was en-thusiastically adopted as the formalframework of biological anthropol-ogy, which it still is.

EVOLUTION ON THE OUTSIDEAND IN THE FIELD

Accounting for how humans com-pare to other primates was a centralgoal of Washburn’s “new physical an-thropology,” which he said should be80% concerned with heredity and only20% with traditional approaches. Inthe subsequent half-century, primatestudies have reflected changing cur-rents in evolutionary thought: At-tempts to elucidate our place in na-ture have at times stressed how we aremore like and sometimes how we areless like other members of our taxo-nomic order. But these studies allstayed within the same theoreticalframework, the fundamental beliefthat considering more than 60 millionyears and including over 200 specieswill provide relevant and interpretableinsight into the processes responsiblefor changes leading to human physi-cal and even behavioral phenotypes.1,2

From its inception, a central objectiveof Evolutionary Anthropology hasbeen to present assessments of theseresults, for which it has been an au-thoritative source.

The idea that we can use compara-tive studies to make broader infer-ences about distinct characters in dif-ferent species requires accepting thatthe species are all subject to the samedeterminative processes. Thus, in thegeneration of primate studies follow-ing Washburn’s paper, the environ-ment was assumed to be the forcedriving the adaptive, presumably ge-netic, evolution of all sorts of physicaltraits, especially such traditional coreinterests of anthropology as skeletaland dental adaptations.

But Washburn energetically pushedhis view further, on his own and incollaboration with Irv Devore at Har-vard. They extended the theory to field

Ken Weiss is Evan Pugh Professor andHeather Lawson is a senior graduate stu-dent in anthropology at PennsylvaniaState University.

© 2005 Wiley-Liss, Inc.DOI 10.1002/evan.20080Published online in Wiley InterScience(www.interscience.wiley.com).

In the evolving theoretical basis of physical anthropology, genes always get theleading role. But stars are not the only members of a cast.

Evolutionary Anthropology 14:213–217 (2005)

studies of wild primates aimed at un-derstanding how environmental con-ditions determined the adaptation ofsocial behavior.3,4–8 The findings ofmany famous primate field studies,among them ones focusing on domi-nance hierarchies, territoriality, har-ems versus monogamous pairings,and male versus female behavior,were extrapolated to humans. Physi-cal anthropology was largely domi-nated by this new evolutionary ap-proach, which made Hollywood-likestars of field workers like Jay, Goodall,Fosse, Lancaster, and Hrdy, as well astheoretical popularizers like Tiger,Fox, Ardrey, and Morris. These starswere the most visible part of a galaxythat included numerous other prima-tologists who more quietly made con-tributions at this time.

Assuming the evolutionary synthe-sis, these personalities made genes theimplicit scientific star of the show.Primate traits were inferred to be theheritable effects of genes as the pre-sumed targets of Darwinian evolution.But because these genes were of to-tally unknown number or nature,nonhuman primates served as meta-phors of explanation for hominin di-etary, locomotor, cultural, language,and brain evolution.9–11 Derived fromthe Greek meta � pherein, whichmeans to carry beyond or to transfermeaning between two unlikes (for

example, “All the world’s astage, . . . .”),12 metaphor is a type ofabstraction that scientists usually tryto avoid. Unlike “models” in biology,metaphors assume far more than isreliably known to be directly homolo-gous or mechanistically relevant, of-ten carrying many loadings, some-times unstated, that can include valuejudgments, iconic simplifications, orbroad applications that may, at best,be more analogous than homologousas well as very subjective.

It is engaging in metaphor to at-tribute what we know about a com-plex trait from observational studiesof primates to hypothesized internalcausal factors (genes) of unknownand, especially during Washburn’stime, unknowable nature. But fromthis attribution, dominance hierar-chies or nuclear family structures inwild baboons were assumed to pro-vide biologically causal explanationsof all sorts of hierarchies, from theculture of modern nation states to hu-man kinship and marriage systems(Fig. 2). Metaphors may be built ongrains of truth but, to borrow againfrom the Bard, is this metaphoric useof genes “a tale told by an idiot, full ofsound and fury, signifying nothing,”or is it truth? If the trait were not“genetic” in this hypothetical sense,what is its causal basis? How can weknow?

EVOLUTION ON THE INSIDEAND IN THE LAB

The incredible recent progress ingenetic technologies promises directanswers to these questions by identi-fying specific genes to replace thosethat had long been abstractly hypoth-esized to exist and imbued with met-aphorically extended importance. Oneimportant area is developmental ge-netics. Development was significantevolutionary evidence to Darwin, but

Figure 1. A. Sherwood Washburn. B. Washburn’s landmark paper.1

Figure 2. Metaphors old and new. A. Spider monkey, Ateles geoffroyi, on Barro Colorado,Panama, taken by one of us (HAL). B. Homologous sequences of a gene (GGA1) fromhuman, chimp, and macaque (Source: GenBank).

214 Weiss and Lawson CROTCHETS & QUIDDITIES

was largely ignored by the modernsynthesis as an unimportant blackbox. The new physical anthropologywas about introducing the populationand historical dynamic among gener-ations of individuals, but evolutionarytheory was nearly silent on how thehypothesized genes made their re-spective traits. However, the technol-ogies of molecular biology are givingdevelopment new vibrancy, reunitingit with evolution in a union called evo-devo, or evolutionary developmentalbiology.13,14

We can now move from metaphoric“genes” hypothesized for externaltraits to the inside, where real genesare, and explicitly identify what hadheretofore only been implicit in state-ments about primate and human evo-lution. We can experimentally identifygenes that are expressed in specifictissues and at specific times duringembryogenesis; we can manipulatethose genes to see how they work.These approaches connect what hap-pens among organisms during a spe-cies’ evolutionary time to whathappens among cells during an organ-ism’s lifetime. Applications of thisnew new physical anthropology havealready included studies of limb,skull, and tooth development andvariation.13,15–19

Washburn said that combining evo-lution, comparison, development,variation, and experimental evidencein living and fossil primates would re-veal new aspects of skeletal biology.“Evolution, in a sense, has dissectedthe body for us,”1 showing that traitsthought to have evolved in a unitaryway were actually composed of evolu-tionarily independent modules. Basedon present and past hominid varia-

tion, Washburn identified several ar-eas of the jaw (Fig. 3A) that seemed tohave evolved independently, each con-trolled by different selective forces.This meant that if his observationswere “at all correct, it is theoreticallyimpossible to make any progress ingenetic understanding by taking thetraditional measurements on themandible” because they artificiallyconfounded independently controlledtraits.

We can now see the power of thenew approaches. As an experimentalmodel, Jim Cheverud and colleaguesrecently crossed two mouse strainswith somewhat different mandibularshape.20,21 They used gene mapping,in which they searched variable sitesspread across the entire genome tofind regions in which sequence differ-ences between the parents were co-inherited with mandibular shape vari-ation in their offspring. They foundgene regions that independently affectdifferent aspects of mandibu-lar shape and, remarkably, thesematched Washburn’s earlier conjec-tures (Fig. 3B). What he had empiri-cally found to be phenotypically mod-ular they showed to be directly undermodular genetic control as well. In asimilar kind of study in living ba-boons, gene regions have been foundthat affect tooth size, enamel thick-ness, and cusp variation that resem-bles variation in the anthropoid fossilrecord.22,23 However, this second ex-ample reverses Washburn’s point be-cause dental traits previously treatedas being of independent taxonomicvalue turn out to develop under thecontrol of the same genes.

“GENES” THAT BECOME GENESCAN BECOME “GENES”

In addition to “evo-devo,” new tech-nology is making possible major ad-vances in the application of the con-cepts of the classical modernsynthesis. The entire human, chim-panzee, and macaque genome se-quences have become publicly avail-able, with a stream of other species tofollow. New genomic approaches al-low us to align sequences of the same(orthologous) genes between humansand other primates and to search forchanges in particular genes that oc-curred preferentially in the human orother lineages, paying intense interestto changes that may have been due tonatural selection.24–26 For example,sequence comparisons of the primaterepertoire of olfactory receptor geneshave shown, in specific genetic terms,the degradation in the ability to smellin the ape and human lineages, alsoconfirming the long-suspected lossof pheromones for sexual attrac-tion.13,27,28

Genomes, like species, evolve overtime, so that Washburn’s suggestionthat we should begin with a frame-work developed from the fossil andcomparative records is still relevant.But now, as then, it is important tokeep in mind several cautionarypoints: Traits generally do not evolvein a simple linear way; most interest-ing traits vary continuously ratherthan discretely; primate evolutionaryrates are generally concordant withoverall mammalian evolutionaryrates; most human traits are alsopresent in other primates, especiallythe great apes; and many changes as-sociated with anatomically modernhumans occurred before the origin ofthe genus Homo, among them bipe-dalism, larger cranial capacities, andmore complex mental ability than wehave traditionally been willing tocredit to these other brutes.29

We have had many warnings aboutthis. Some early claims of primatol-ogy have not survived the subsequentfifty years of investigation. Femaleprimates are not passive and nonhier-archical, alpha males don’t have allthe mating fun or mating success,chimpanzees aren’t always nonvio-lent, and species’ mating patterns arenot predetermined. Extensive field

Figure 3. Guessing and testing about “evo” and “devo.” A. An “evo” perspective helpsidentify causally independent traits. Regions of the jaw Washburn found to evolve inde-pendently.1 B. A “devo” perspective tells us why: Each labeled region has been shownexperimentally to be under independent genetic control.20

CROTCHETS & QUIDDITIES A Metaphoric Rise to Stardom 215

work has shown that phenotypes canbe fluid. Moreover, variation for mostof our classical traits turns out to bepolygenic, often associated with genesregulating development rather than,as per the classical idea, coding for thetraits’ structural proteins.11,13,30

From a genomic viewpoint, too,evolution of the traits we care about,both phenotypic and genetic, can beexpected to be subtle and complex.However, it’s a lot easier to raise cau-tions than resist the temptation to ig-nore them. Genes are enjoying a tech-nology-driven ride to new metaphoricstardom in the genomic age. Today,perhaps more than ever, things bio-logical are widely assumed to lie di-rectly in the genome. If primate fieldstudies sometimes uncritically in-voked genetics as metaphors of expla-nation for hominin evolution, anthro-pological genomic studies—wholesalecomparisons of the 30,000 genes inprimate genomes—can slip into com-parably strong genetic assumptions.Ironically, while it was formerly ac-ceptable to invoke the role of genes inprimate evolution without botheringto look at any actual genes, it is nowacceptable to invoke the role of genesin primate evolution without bother-ing to look at any actual primates!

Unlike the original new physical an-thropology, much of the recentgenomics work is not being done byanthropoligists, who at least tend togive serious consideration to wholeorganisms. This has led to a new kindof genetic metaphor for, if not by, an-thropology. Abstraction for homininevolution has moved from the as-sumption of shared but unidentifiedinternal causal elements to the re-verse. Now actual genes serve as anew kind of metaphoric star on thestage of explanation. But rather thanusing a known trait to infer the exis-tence of causal genes, known genesare now held to stand broadly, ab-stractly, metaphorically, as icons forthe entire trait.

For example, there is irresistiblevanity in focusing on “the brain” asthe organ that made us human. It’sbecome a cottage industry to singleout individual brain-related genesfrom the mix of thousands of themexpressed in the brain, under the im-plicit suggestion that a single gene is

capable of explaining all of thechanges resulting in the human phe-notype.9,31–36 Going Washburn’s 80%solution and then some, a brain-re-lated gene that varies between hu-mans and chimpanzees is widelytaken to represent the complexity offeatures that constitute human cogni-tive behavior, even including languageand other things that clearly are notliterally due to a single gene. Indeed,such features may be so complex thateven calling them “genetic” may be tomiss their important emergent na-ture. The brain has deeply symbolicvalue, even among scientists.

In the old “new” physical anthropol-ogy, the melodrama of dominance,territoriality, and other charactersthat evolution had molded into us na-ked apes was made famous by thepopular media. Today, new genetic re-sults also sell well in the media and inthe mainline science journals, thathave moved in a popularizing direc-tion. But, like the simplistic enthusi-asm for the fitness advantages of al-pha male baboons or tribal headmen,the rush to the judgment that braingenes show special evidence of evolu-tion in the human lineage has alreadybeen tempered by more thorough ex-amination.37,38

A GALAXY OF GENOMICSTARS

The old anthropology was staid andneeded something new. The prevail-ing working model is still the oneadapted in Washburn’s day, half acentury ago. It is a strong acceptanceof classical Darwinism in the study ofimportant functional traits of pri-mates, which extend to our own verydifferent species, one with culture.Even many founding evolutionists, in-cluding Darwin himself, as well as Al-fred Wallace and Thomas Huxley,39

blinked when it came to humans,seeking special provisions or excep-tions for our evolution. While anthro-pologists wouldn’t want to leave hu-mans out of nature, we can still get introuble with oversimplified genetic ex-planations or theory applied uncriti-cally, as is shown by hot debatesabout behavior genetics or the failureof genetic data to confirm simpledominance theories.

Generally, however, the best of theunion of development with the olderevolutionary perspective is truly ener-gizing. It is also rapidly bearing fruit.Moving to the inside of the organism,we are learning a tremendous amountabout how genes are used to build theanimals we study and that we are. Be-cause this work has shown that ge-netic developmental networks aredeeply conserved and homologous,model systems like the mouse arefinding a level of real rather than met-aphoric anthropological relevancethat we haven’t seen since Washburn’sday. That’s why Figure 3B from themouse tells us about Figure 3A forhominids, and can be called “anthro-pology.” But with this progress hasalso come the tempering and subtlerealization that so many genes are in-volved in the developmental networksthat contribute to most traits of inter-est that we can’t presume that a spe-cific gene is responsible for any spe-cific version of a trait in a particularfossil or primate. A control networkprovides many ways to make a shortmandible.

Genes are providing an increasinglystellar cast of causal elements in life. Atruly new physical anthropology thataugments the genetic theory of evolu-tion with a comparable genetic theoryof development will provide a muchmore comprehensive view of the na-ture of life than the old new physicalanthropology did. In that sense, theday is here when genes should nolonger be used as metaphors. We’regaining the means, and hence the bur-den, to base genetic explanationsmore specificially on what genes doand don’t do. That knowledge willlead to a more truly modern evolu-tionary synthesis.

NOTES

Send comments on this column tokenweiss@psu.edu. There is a feed-back page at http://www.anthro.psu.edu/weiss_lab/index.html. We thankAnne Buchanan, Joseph Orkin, SamSholtis, and John Fleagle for criticallyreading this manuscript.

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© 2005 Wiley-Liss, Inc.

Articles in Forthcoming Issues

• Paleozoology in the Service of Conservation BiologyR. Lee Lyman

• On the Evolution, Life History, and Proximate Mechanisms ofHuman Male Reproductive SenescenceRichard G. Bribiescas

• Living in the Human NichePeter Bleed

• Cultural Macroevolution and the Transmission of TraitsMonique Borgerhoff-Mulder, Charles L. Nunn, and Mary C. Towner

• Niche Construction, Human Behavior and the Adaptive-LagHypothesisKevin N. Laland and Gillian R. Brown

CROTCHETS & QUIDDITIES A Metaphoric Rise to Stardom 217