CROTCHETS & QUIDDITIES

The Clergyman’s Wife and the ParrotKENNETH WEISS

The so-called central dogma of biol-ogy is that DNA sequence is a codethat specifies amino acid sequencesvia a messenger RNA (mRNA) inter-mediate in a one-way feed-forwardtransfer of information. It’s curiousthat scientists, who proclaim that ev-erything is always open to question,would name one of our views adogma, though it is certainly a well-established bedrock of biology thatour genome hides, like the Prince ofPompadoodle, “behind a castle wall,behind a moat, behind a guard, oftwenty soldiers tall,” because “some-where in the palace was a cur who’dseek his end!”1 Chromosomes aretucked safely inside the protectivebarrier of the nuclear membrane,where their genes are transcribed intomessenger RNA copies. Those copiesleave the inner sanctum to ventureinto the dangerous world of the cyto-plasm, where they are translated intoamino acid sequences, which formproteins. The mRNA can be buffeted,degraded, and otherwise abused bycytoplasmic curs, while the princelyintegrity of the DNA itself is protectedas the unchanged progenitor of theDynasty.

Actually, the central dogma doesnot require that DNA be physicallyguarded in this way. Bacteria are do-ing just fine without a nucleus (they’ll

dance on all our graves, in the end).Instead, the protection is by a logicalrather than physical moat: DNA isused as a stable source code to man-age the changing operational materialof a cell’s life. This has been viewed asa universal characteristic of genomesand in that sense is a dogma, I sup-pose. But evolutionary theory couldeasily withstand the Reformation thatwould follow the discovery that thedogma is not just so. What is muchmore critical to the current theory oflife is not that DNA is unchangeable,because mutations have to occur atleast occasionally as the fuel of evolu-tion, but rather that no such change isinstructed by the individual’s experi-ence in a way that specifically im-proves its future prospects. Evolutionis not teleological: It has no long-termgoals. The inviolate credo is that ge-netic change is random with respectto any specific needs that the environ-ment might present, and such varia-tion is screened by the experiences offuture generations to proliferate if it ishelpful (natural selection) or lucky(genetic drift).

A feedback of experience that modi-fies the DNA sequence in a specificallyadaptive way would be that ultimateevolutionary bete-noire, Lamarckian in-heritance. Most life scientists and evensocial scientists, including anthropolo-gists, explain Lamarckian inheritancewith lampooned images of giraffesmightily stretching their necks to reachthe high leaves in a way that changestheir genes so that they produce neckieroffspring. That’s an inaccurate textbookcaricature of poor Lamarck, as you caneasily see for yourself by actuallyreading his 1809 book PhilosophieZoologique, available in English—and

don’t worry, you won’t be hereticallycontaminated.2 Though ridiculed as amystic by many, including Darwin,who had a vested interest, Lamarckanticipated most important aspects ofDarwin and Wallace’s theory of evolu-tion, only he did it 50 years earlier.(Darwin knew of the work and latersuggested similar mechanisms of in-heritance.)

Lamarck stressed that his views werepurely materialistic, not animistic, buthe did believe that what an organismdoes during its life is transmitted to itsoffspring (today we’d say “in its genes”).This quite sensible way to account forfamilial resemblance can be traced atleast as far back as Hippocrates, 2,400years ago. Because Lamarck’s speciesmodified their nature according to theirneeds, his “tree” of life (Fig. 1), perhapsthe first ever drawn, did not include ex-tinction. If he had had the advantage wehave, of a better fossil record and theevidence of the dodo and passenger pi-geon, he would have had to accept thatsome lineages simply can’t stay with theprogram. But his idea that evolution isthe result of striving to do well in one’scircumstances seems obvious if youthink of what we see in everyday life:We do strive to do what we can do, andwe do it with future objectives in mind,including objectives for the success ofour children. To modern biology, this isa genetic illusion based on what we seein our short lifetimes compared to whatcan happen slowly over evolutionarytime. According to the central dogmaour behavior, or at least that of nonhu-man species, who can’t set up collegetuition savings accounts, is based onwhat we are, not on what we want to be.

Perhaps because of its intuitive ap-peal, and despite the central dogma,many investigators have searched forplausible Lamarckian mechanismsthat would, after all, give organisms a

Ken Weiss is Evan Pugh Professor of An-thropology and Genetics at Penn StateUniversity. E-mail: kenweiss@psu.edu

© 2006 Wiley-Liss, Inc.DOI 10.1002/evan.20086Published online in Wiley InterScience(www.interscience.wiley.com).

Things from the past are sometimes repeated when you least expect it.

Evolutionary Anthropology 15:3–7 (2006)

marvelously quick way to adapt tochanging circumstances. Some recentclaims have reached at least a kind ofcredibility. These claims includeevolvability mechanisms, by whichbacteria or even complex organismsunder environmental stress generatehigh rates of mutation in parts of theirgenome that code for proteins inwhich variation might be responsiveto the stress. Immune resistance andmetabolic response to nutrient stressare examples. Even if these have ele-ments of transfer from experience(stress) to genome, the idea remainsmainly Darwinian. The mutations arerandom relative to the specific stres-sor, and it’s classical natural selectionthat favors those whose new state isable to survive.

LIFE-EXPERIENCE DOES FEEDBACK ONTO GENES

At the heart of Lamarck’s ideas wasthe inheritance of acquired character-istics. If evolvability systems are inter-esting and hint at, but don’t achieve,real Lamarckian inheritance, in re-cent decades we’ve discovered moredirect and fundamental lamarckian-like aspects of life, ones that are well

known and not at all controversial. (Iuse lower-case “lamarckian” to deper-sonalize the word.)

Embryogenesis, homeostasis, andother dynamic affects on cells’ envi-ronments—that is, their experi-ence—do affect their genomes.3–6

You are a complex organism only be-cause your cells are differentiated;some make eyes, others make hair.That comes about through differencesin the subset of its 30,000 genes that agiven type of cell actually uses. Duringdevelopment, cells detect signals intheir external environment, some ofwhich are secreted by other cells. Cellsrespond to these signals by changingthe genes they use, activating someand silencing others. That’s howenamel and dentine layers differenti-ate in a tooth germ, how intestinesform absorbing or secreting cells, andso on. These changes in gene expres-sion are brought about by modifica-tion of the nuclear DNA. The changesare directed, in a meaningful sense, infunction-specific rather than randomways. That’s why, no matter hownasty you may be, your heart’s in theright place. These changes acquiredby cells’ experience are inherited, too:When the cell divides, its daughtercells retain the parent cell’s gene-ex-pression pattern until circumstancescause that pattern to change.

The fact that this is how the singlecell of a fertilized egg is turned into awhole organism has, in the last coupleof decades, been at the center of hugeadvances in our understanding of thegenetic basis of development and ho-meostasis. In fact, a greater fraction ofthe genome may have to do with reg-ulating gene use than with coding forproteins.5 This is not Lamarckian inthe sense of cells “striving” to becomefingers or ears, and it does not violateany evolutionary premises. Rather, it’sabout generations of cells within or-ganisms, not generations of organ-isms. It may have transformed whatwe know about how genes work, butit’s no threat to our overall evolution-ary “paradigm.” But something hasrecently been reported that, if true,adds a previously unknown phenom-enon that somewhat reverses the ge-netic and evolutionary dogma.

“I DON’T KNOW WHERE YOUPICK UP SUCH EXPRESSIONS,”SAID THE CLERGYMAN’S WIFE

TO THE PARROT7

It must be tough being a clergyman.You always have to watch what yousay, because weak moments fromyour forgotten past can come back tohaunt you. The past does not presentsuch a problem to organisms because,as per the central dogma, the flow ofevolution is strictly forward in time.Or so we used to think.

The mustard-family plant Arabidop-sis thaliana is a favorite laboratory-model species in plant biology. Likelaboratory mice, Arabidopsis is small,cheap to maintain, and has a shortgeneration time. Many botanists workwith this species, including a group atPurdue, who made a striking findingin the course of experiments to under-stand the genetic basis of organ devel-opment.8,9

They bred plants containing a mu-tation that caused the parts of theflower to remain fused instead ofopening normally. After a couple ofgenerations, a percentage of thesemutant plants surprisingly producedoffspring that reverted to the state oftheir normal great-grandparents (Fig.2). This was because the plants hadprecisely corrected the mutation backto the original normal DNA sequence.The striking thing is that the correc-tion occurred in plants that no longerhad a copy of the normal gene to useas a template to know how to makethe correction or even what the ances-tral state had been. This reversion toan ancestral DNA sequence could notbe due to known error-correctingmechanisms, occurred too often to bea chance reverse mutation, involvedonly correction of current variationback to missing ancestral states, andoccurred in other genes in theseplants. Most curiously, reverse muta-tions also occurred in parts of the ge-nome that don’t even code for proteinsequence. With typical melodrama,the news media immediately likenedthese new findings to the kind of“striving” for which Lamarckian in-heritance is known. The plants wereseeking to be like their ancestors,which, like your ancestors and mine,had obviously been at least partly suc-

Figure 1. Lamarck’s version of evolution: a“tree” with no dead branches.

4 Weiss CROTCHETS & QUIDDITIES

cessful in life. Had they not, none ofus would be here to tell the tale.

What mechanism could enable thisself-correction? At present we canonly guess. These days many geneti-cists’ minds are focused on gene-reg-ulating mechanisms that are broughtabout by types of RNA that aren’t in-volved in protein coding, but that havethe ability to bind to DNA. One, calledXist RNA, literally coats and inacti-vates X-chromosomes in femalemammals, leaving only one active X inany cell, to match the single X chro-mosome in male cells.10 Similarly,telomeres, the ends of chromosomesthat protect them from degradation,are established and maintained byRNA that binds to DNA sequencesthere.11

The Purdue investigators specu-lated that a previously unknown re-serve pool of DNA-binding RNA cansurvive at least two generations with-out being used (that we know of), toprovide a memory bank of prior DNAsequences. This is a logical extensionof the fact that RNA is copied from,and hence accurately matches, a DNA

template. I personally can’t remembera face or name for more than a fewminutes, but what we could callanamnestic-RNA (aRNA) might waitin the wings for a few generations andthen bind to its corresponding DNA inthe plant nucleus, triggering repairmechanisms to detect the DNA–aRNAmismatch (the mutation) and correctthe DNA. This is speculation, but largepools of nonprotein-coding and previ-ously unknown RNA are being discov-ered and seem to have importantuses.12

This remarkable result is already re-ceiving the scrutiny and skepticism itdeserves. It goes so against currentbiological theory as to be widely dis-missed as an awful publishing deci-sion by Nature. It is easy to find rea-sons for doubt. For a pool of “aRNA”to last several plant generations, itmust be replicated to avoid being di-luted out of existence over many cellgenerations between the original mu-tant seed and the cell on some stem ofa grandchild plant that makes the cor-rection. How and where is this aRNAreplicated? Also, the investigatorsfound that 5%–10% of their bb plants(i.e., bad/bad genotype with no nor-mal B), reverted to a normal trait, andof these 101 of 102 had become Bbs.But if a bb plant has a 5%–10% chanceof reverting a b to a B, why didn’t atleast 5% of them correct both their bsto become BB? Discussion and possi-ble alternative mechanisms, but as yetno refutation, have begun to appear(R. Pruitt, personal communication).

I’m writing in September, and bythe time this is published the claimmay have been refuted. But if it doesprove true in Arabidopsis, it probablyexists in other plants and, based onrecent experience in genetics, we canexpect some form of the phenomenonin animals, including mammals. Thisis because important genetic mecha-nisms are often deeply conserved,used and reused in different ways.Similar genetic strategies have oftenevolved independently in differentbranches of life.6 Since self-correctionappears to be a genome-wide ratherthan gene-specific ability in Arabidop-sis, its impact might affect complextraits due to many genes as well assimple single-gene ones.

There’s nothing new about traits

skipping generations, so that a personappears to revert to the state of one ofhis ancestors. That’s what recessivetraits are, as Mendel first formally ex-plained. In a similar way, traits due tothe interaction of many genes mightappear only occasionally, in unusualmultigene genotypes. (People have ex-plained Bach and Mozart and MichaelJordan in that way.) In these in-stances, the underlying genetic varia-tion is always circulating in the popu-lation but is expressed only in thosegenotypes. That’s very different fromthe Arabidopsis case, in which an an-cestral DNA sequence no longer in thepopulation is changed back to thatspecific former state.

Are there human traits that seem todisappear and then reappear that mightbe due to this kind of mechanism? If so,our usual gene-finding approacheswon’t identify them, because thosemethods assume that genetic variationis faithfully transmitted from parent tooffspring. That could account for prob-lems we have in forming genetic expla-nations of complex traits. Further, ourspeculations and reconstructions of in-teresting traits and their evolution arebuilt on classical notions of inheritanceand adaptation. Will we have to changethese and, if so, will new understandingresult? It’s far too early to tell. But thinkwhat that would do to our attempts tounderstand the nature of primates, in-cluding ourselves. How many of ourtraits, inheritances, and behaviorsmight have gained evolutionary benefitfrom an ability to reconstruct statesthat were successful in the past?

ON REMEMBRANCE OF THINGSPAST

Marcel Proust wrote that the smelland taste of things from the past, likethose of madeleines (since thenknown as the cliche cookie), long lin-ger as potential triggers of streams ofmemory. But if the aroma of mustardmight bring up memories of picnicspast, mustard’s memories of its ownpast won’t bring new kinds of adapta-tion to its future. The core character-istic we tend to associate with evolu-tion is future, not past, adaptation. Sowe might call what has been discov-ered reverse, or pre-verse (or per-verse?) lamarckism. It is an organism

Figure 2. Teller of tales.

CROTCHETS & QUIDDITIES The Clergyman’s Wife and the Parrot 5

rummaging through its wardrobe totry on something that at least used tobe fashionable.

This might help explain the kind ofconservatism associated with the longperiods of morphological stasis some-times observed in the fossil record andthat was controversially dubbed punc-tuated equilibrium.13 This aspect ofevolution is now known to have beenexaggerated at best, but seemed to beinconsistent with the classical Dar-winian notion (dogma?) that naturalselection drives continual incrementalchange, ever-refining the fit of organ-isms to their environmental circum-stances. If those circumstances didn’tchange, organisms would also resistchange. Did cockroaches and horse-shoe crabs consult their personal his-tories to ensure they stayed the samefor so many eons?

Restoring ancestral sequence wouldseem to be a rather automaticallyadaptive and hence safe way of life. Ifthe Arabidopsis story is true, and if ithas anything to do with the plant’slong-term history, it would be a kindof evolutionary bet-hedging. Undermost circumstances, using what re-cently worked may not make you bet-ter, but could be a good, if conserva-tive, strategy. One can see howclassical natural selection could favororganisms that had the ability to in-voke a successful past. In fact, thathas happened. I alluded earlier toDNA repair mechanisms, of whichmany are well known. Such mecha-nisms presumably evolved because

mutation is usually a threat to the ex-isting order. But this kind of DNA re-pair happens basically at the time ofthe mutation, not generations later,which is what is remarkable about theArabidopsis findings.

Such abilities may have evolvedduring stable environmental times inwhich the past really was prologue.But like armies that prepare to fighttheir previous war, it would be a ter-rible strategy, an evolutionary Magi-not Line, when environments change.And whatever this active DNA rever-sion turns out to be, we know thateven roaches and crabs continued toaccumulate divergence at the DNA se-quence level, no matter how statictheir appearance. Indeed, evolving notto evolve would stop evolution in itstracks if it worked perfectly. Thatwould be a lethal situation, since en-vironments are often, if not always,changing. In reverse lamarckism, alllineages, looking backward instead offorward, would go extinct.

It will be important to learn justhow memory-based genetic correc-tion takes place and how widespreadit is in nature. But it’s no threat to ourbasic notions of adaptive evolution. Aparrot may affect a clergyman’spresent success by reviving his pastfailures. But that’s the opposite of amustard plant, which echoes its suc-cessful past to correct its present fail-ures. A main lesson of evolution isthat in the long run there can only beecho of success. Failures are themutes of history.

NOTES

I welcome comments on this col-umn: kenweiss@psu.edu. I have afeedback and supplemental materialpage at http://www.anthro.psu.edu/weiss_lab/index.html. I thank AnneBuchanan and John Fleagle for criti-cally reading this manuscript.

REFERENCES

1 Kelly W. 1957. Pogo’s Sunday Punch. NewYork: Simon & Schuster.2 Lamarck JBd. Philosophie zoologique, ou, Ex-position des considerations relative a l’histoirenaturelle des animaux. Paris: Dentu (Englishtranslation pub. 1984, by Univ. of Chicago Press);1809.3 Weiss KM. 2005. The phenogenetic logic of life.Nat Rev Genet 6:36–45.4 Weiss KM. 2002. Good vibrations: the silentsymphony of life. Evol Anthropol 11:176–182.5 Weiss KM. 2002. Is the message the medium:biological traits and their regulation. Evol An-thropol 11:88–93.6 Weiss KM, Buchanan AV. 2004. Genetics andthe logic of evolution. New York: Wiley-Liss.7 Sayers DL. 1930. Strong poison. London: Cor-onet.8 Lolle SJ, Hsu W, Pruitt RE. 1998. Genetic anal-ysis of organ fusion in Arabidopsis thaliana. Ge-netics 149:607–619.9 Lolle SJ, Victor JL, Young JM, Pruitt RE. 2005.Genome-wide non-Mendelian inheritance of ex-tra-genomic information in Arabidopsis. Nature434:505–509.10 Weiss KM. 2005. To bde or not to bde: sex andthe bdelloid rotifer. Evol Anthropol 14:93–98.11 Weiss KM. 2004. Ponce de Leon and the telo-mere of youth. Evol Anthropol 13:82–88.12 Kiyosawa H, Mise N, Iwase S, Hayashizaki Y,Abe K. 2005. Disclosing hidden transcripts:mouse natural sense-antisense transcripts tendto be poly(A) negative and nuclear localized. Ge-nome Res 15:463–474.13 Gould SJ. 2002. The structure of evolutionarytheory. Cambridge: Harvard University Press.

© 2006 Wiley-Liss, Inc.

Figure 3. Arabidopsis self-corrects. A. The mustard-family plant (http://ukcrop.net/agr). B. Flowers in mutant plants fail to open (//news.uns.purdue.edu/UNS/html4ever/2005/050323.Pruitt.inheritance.html). C. The plant’s surprising self-correction: Two copies of eachchromosome are present in the cell. Left to right: Cross between normal and affected plants; open square, normal gene, black square,mutant gene; these plants are then “selfed” (circular arrow), nonsexual reproduction in which seeds have two random copies of the plant’sown genes, yielding 3 offspring types; when selfed again, a fraction of the homozygous mutant offspring (lower type) restored the normalgrandparental gene (asterisk). Drawing by A. Buchanan.

6 Weiss CROTCHETS & QUIDDITIES

Books Received

• Rakita, GFM, Buikstra JE, Beck,LA, Williams SR, eds. (2005) In-teracting With the Dead: Perspec-tives on Mortuary Archaeologyfor the New Millennium. xii �390 pp. Gainesville: UniversityPress of Florida. ISBN 0-813-02856-6 $75.00 (cloth).

• Marquardt, WH, Watson, PJ.(2005) Archaeology of the MiddleGreen River Region, Kentucky.xxii � 657 pp. Gainesville: Uni-versity Press of Florida. ISBN1-881-44814-2. $65.00 (cloth).

• Mazur, A. (2005) Biosociologyof Dominance & Deference. ix �197 pp. Lanham: Rowman &Littlefield Publishers. ISBN0-742-53693-9 $21.95 (paper).

• Stearns, SC, Hoekstra, RF.(2005) Evolution: An Introduc-tion 2nd edition. xx � 575 pp.Oxford: Oxford University Press.ISBN 0-199-25563-6 $59.95 (pa-per).

• Powell JF. (2005) The FirstAmericans: Race, Evolution andthe Origin of Native Americans.viii � 268 pp. Cambridge: Cam-

bridge University Press. ISBN0-521-53035-0 $35.00 (paper).

• de Duve, C. (2005) Singularities:Landmarks on the Pathways ofLife. xiv � 258 pp. Cambridge:Cambridge University Press.ISBN 0-521-84195-X $48.00(cloth).

• Strathern, M. (2005) Kinship,Law and the Unexpected: Rela-tives are Always a Surprise. x �229 pp. Cambridge: CambridgeUniversity Press. ISBN 0-521-61509-7 $24.99 (paper).

• Hamelrijk, C., ed. (2005) (2005)Self-organisation and Evolutionof Social Systems. ix � 194 pp.Cambridge: Cambridge Univer-sity Press. ISBN 0-521-84655-2$110.00 (cloth).

• Curry Rogers, KA, Wilson, JA,eds. (2005) The Sauropods: Evo-lution and Paleobiology. ix � 349pp. Berkeley: University of Cali-fornia Press. ISBN 0-520-24623-3 $65.00 (cloth).

• Burt, A., Trivers, R. (2006)Genes in Conflict: The Biologyof Selfish Genetic Elements. viii

� 602 pp. Cambridge: BelknapPress. ISBN 0-674-01713-7 $35.00(cloth).

• Brockman, DK, van Schaik, CP,eds. (2005) Seasonality in Pri-mates: Studies of Living and Ex-tinct Human and Non-HumanPrimates. xiii � 590 pp. NewYork: Cambridge UniversityPress. ISBN 0-521-82069-3$120.00 (cloth).

• Morris, B. (2005) Religion andAnthropology: A Critical Intro-duction. x � 350 pp. New York:Cambridge University Press.ISBN 0-521-61779-0 $27.99 (pa-per).

• Hovers, E., Kuhn, S. eds. (2005)Transitions Before the Transi-tion: Evolution and Stability inthe Middle Paleolithic and MiddleStone Age. xxii � 332 pp. NewYork: Springer ISBN 0-387-24658-4 $99.00 (cloth).

• Conroy, GC. (2005) Reconstruct-ing Human Origins, Second Edi-tion. xxvi � 694 pp. New York:W. W. Norton & Company ISBN0-393-92590-0 $68.75 (paper).

CROTCHETS & QUIDDITIES The Clergyman’s Wife and the Parrot 7