EPIGENETICS , PALEONTOLOGY, AND EVOLUTI ON

Stan P . Ra cho o t i n and Kei t h S t e war t Thoms onPe abo dy Museum of Na tu ra l Hi s t ory , Yale University ,

New Haven , Co nne c t i c u t 0 6511 , U. S .A .

ABSTRACT

'Three requirements of evolution are persistence with chang e, internally cohe s iveindividua l s of limi t ed dura t ion, and interaction with environment. We recas t th es eproper t i es in megaevolutionary terms. Harologous structures persist over geologicalt ime as they evo lve in f orm and func t ion . Spec ies, which arise through a greater orlesser genetic r evolution, behave as individuals. The interac t ion of genes and envi­ronments- -development- -under lies both the origin of species and the continuity of haro­logies. The properties of epigenetics- -self assemb ly , feedback, a lternative pathwaysto the sane devel opmental end, canpensati on for the inevitable irregularities of devel­opment--allow a redefinition of gene t ic revolution in terms of the establishment ofnew, stable developmental patterns : a typological r esult produced in ac ceptably popu­l ati ona l ways . Harologues, s imi larly , are the products of evo lving epigenetic sub-sys­tems. Al though developmental systems retain ancestral potentials that renain unex ­pressed for tens of millions of years, such potentials are so burdened with other devel­opmental pathways built upon them that they hold little promise for evolutionary change.But where a recent developmental change ha s occurred, no such "buf fering" exists . Aserrors occur , sane will be ep igenetically acconm:>dated and , if adaptive, gene t i callyassimilated . These are the quanta of evolution . If a r ecent adaptive breakthrough hasoccurred, i t wi ll be " suppor t ed" at first by interacting ep igenetic sub-systems. Thepoorly canalized epigenetic system roost; closely associated with the new adaptation willbe under intense selection to build up an epigenetic environment that assures the pre­dictable expression of the new trait . Until this happens, fur ther " exper iments" alongthe l ines of t he initial change can occur and be assimilated . Depend ing on eco logicalmi lieu, t his i s the stuff of adaptive r adiation , evo l u t i onary trends, or allanetri cchange. Speciation, which can occur without any adaptive change, is th e result of anal­ogous changes in the epigenetic systems responsible for mate r ecognition . We accept theneo-Darwinian reliance on natural selection acting in populations. But we choose toconcentrate on i ts action on developmental processes, rather than on traits , the obviousand experimentally tractable end -products of such processes. The normal features of epi­genet ics fortui tousl y l ay down the lines of l ea st r esistance to evo l utionary change. Wefind ourselves l ooking a t an intrinsic and emergent s i de to evolution, a view that inthe past was held, on similar gener a l grounds, by Bateson, Goldschnidt, and Waddington .The story of evolution i s perhaps less the warfare of selfish genes than the YX>rking outof the potentials of selfless epigenes.

I NTRODUCTION

The title of our paper, "Epi genetics,Paleontology, and Evolution", i s de liber­ately chosen to r eca ll the title of theconference that was held at Princeton Univ ­ersi ty in 1947 on "Genetics , Paleontology,and Evol ut i on" (Jepsen e t a l . 1949). I tincluded not only th e subjects of gene tics ,speciation, and paleontology, but canpara­tive anatany, ecology, and systematics aswell . The synthe tic theory that came ofage with that symposium ha s been the nota­ble success of organ isrnal biology of thi.scentury . In a day when theories in o therparts of biology change wi th the seasons,it i s astonishing to f ind that 33 yearslater the study of evolution is no l es svigorous for having r emained in the sanenode . We =uld be pleased if our contri -

bution i s seen as a na tural offshoot fromthe syn thet ic stock. But though the syn­thetic theory has provided many answers ,i t has not adequately framed a l l the ques­tions. llich renains to be explained , es­pecially when we take the long pa leontolo­gical per sp ective . The answers to thesequestions are, we think , t o be found in aconsidera t i on of the evolutionary implica­t ions of development and the developmentalimpl i cations of evo l ution, topics that werenotably l acking in the 1947 conference .

Our goa l in t his paper i s to se t in adevelopmental con text the problems of mega­evo lution : the nature of adaptation , thetempos and nodes of evol ution , the framingof us eful general izati ons about the originand diversifica tion of major groups . Aswe go about this , we find ourselves r ein-

G.G . E. Sc udder & J . L. Rev e a l (ed s .) I EVOLUTION TODAY, Proce edings of t he Second Inter ­na ti o na l Congress o f Sys tematic a nd Evolut i onar y Bi olo g y, pp . 18 1- 19 3 . 19 81 .

182 EVOLUTION TODAY Rachootin & Thomson

terpreting sane of the ftmdarnenta l con­cepts of evolut ion, including variation,spec ies, and what i t i s that selectionacts upon . These reinterpretations caneout of a series of generally acceptedpremises about development , which, how­ever, have unexpected impl ications whenviewed over the time scale familiar to thepaleontologist. Our paper is an outlineof a way of ret:hinking what everyone knowsabout evolution. We ask you to rearrangeyour mental furniture and consider sanechanges that we think are suitable forsane circurns tances . Al though the rear­rangement is new, the pieces are not .Those that look unfamiliar we have onlybrought down from the attic .

In the broadest terms. we ask what me­ga -evolution ought to require of theoriesat the level of genetics and development,and also at the level of speciation. Weexpect that nothing at the l evel of mega­evolution contradicts what happens atthese l ower levels, bu t that we will notfully understand these l ower l evel s un tilwe actively search them for phenCID2I1a thatmay seem peripheral to the population bio­logist, but which are required to explainthe data of the paleontologist and theroorphologist. We trace the emergent mega­evolutionary phenanena down to their hid­den roots, which we find to be developmen­tal, and then ask what this mega-evolution­ary view of development suggests about thenature of species and speciation .

We also ask you to allow us to break oneother convention of evolutionary theory,concerning intrinsic and extrinsic factorsin evolution. Extrinsic factors are therelations of an organism to the externalenvironnent- -adaptations to local condi­tions, the sorting-out of congeners insympatry by character displacement, andsuch chance effects as the genetic sampleborne by the traditional gravid female com­pared to the population from which she de­rives, or the effect of a river changingits course and cutting off a population.We accept such extrinsic factors as thecarrron property of all m:xIem evolution­ists. But although we all believe in suchfactors, they are remarkably difficult todemonstrate in anyone case . We defineintrinsic factors as the adaptation of thegenane to itself . Developmental mechan­isms, especially epigenetics, the self­organizing and correcting properties ofdevelopmental pathways, are the means bywhich the intrinsic side of evolution i smanifested . Intrinsic factors will bejust as difficult to demonstrate as ex­trinsic factors, all the roore so becausebiologists are not accustaned to t:hinkingmuch about them. But there is no a priorireason why they rrust be mystical.

"Intrinsi c" and "extrins i c" bear closerelation to the distinction that Mayr hasdrawn be tween typological and population­al thinking . Throughou t the paper, wewill be contrasting a populational, or ,rrore generally, an extrinsic approachwith a complementary intrinsic approachthat is developmental and typological.Note that both approaches are ways oft:hinking, not hypotheses about nature .The mind has a hard time holding = com­pletely different views of the worId si­mul taneously, but it is our guess thathaving two ways and switching when i tseems appropriate i s better than havingone way that we a lways be lieve to be right,and another, which we seem to fall into ,but which we have decided is always wrong.

Development is studied in a typologicalm:xIe. Development shows directedness; inan experimental manipulation, the embryo" tri es" , if you will, to develop normally,according to type, in spite of the insult.Results in a devel opment al experiment turnon the behaviour of particular, crucialembryos. This is a far cry from popula­tion thinking. The dichotomy is apparentin the 1947 symposium, which neglected de­velopmental biology, but not because therewere no evolutionists interested in it .Indeed, embryology dominated evolutionarystudies in the las t century , and was theguiding light to such twentieth centuryvorkers as William Bateson, Richard Gold ­schmidt, and C. H. Waddington. The prob­lem was that the typological and the pop­t l a t i ona l could not be fused into a sin­gle approach. How, for instance , couldGoldschmidt 's macro-evolution, which tookdevelopmental saltations as the means ofgetting from one major group to another,be reconciled with the gradual, popula­tional approach that was then being fash­ioned, an approach that accounted for me­ga -evolution by an aCCl.IIllllation of micro~

evo lutionary events? The r esolution onthe part of those who formulated and pop­ularized the synthetic view--Mayr, Dob­zhansky, Simpson, Stebbins--was to takepopulation t:hinking as right, true , andrrodern , and typological thinking as wrong,false and old-fashioned . A sympathe t i ctreatment of evolutionary development wasdifficult in this envirornnent. Neverthe­less, as of the 1947 Princeton symposium,the verdtcrwas not unanimous- -Dwight Davis(1949) made a strong case for typology anddevelopment in the study of comparativeanatomy . In this paper, we take up wherehe left off.

In our mega -eVolutionary appr oach , wemake use of three concepts that David Hull(1980) proposes for micro-evolution. Hullnotes that evolution has a component of"cont inui ty" , provided by the genes , and

Epigen etics & Evolution PROCEEDI NGS, IesES-II 18 3

a component of " int er act i on" , t he pheno ­type . One cannot be a rrore basic unit ofselection t han the other , and both mustbe contained in "individua l s" --entitiesof fixed durat i on and extension in t imeand space. The contirnlity of rrega-evolu­t ion i s expressed in persistent s truc­tures that recur in a l ineage- - cha ins ofhorrol ogous s tructures (Ri edl 1977) . Thesehomologues change over geologica l time ,in s tructure, posit i on , and function, j us tas genes change at a micro-evolutionaryl evel . The chains of homologues are theoutward manifestations of the interactivecanponent , which i s canposed of "devel op­ment al systems". Each system cons ists ofone or more integrated , part ial l y self­r egulating deve l opmental pathways l eadingt o t he s tructure we recognize as a linkin t he chain of homologues . These systemsinteract with nei ghboring developmentalsy stems , and with the external environment .All of them taken together produce the on­togeny of t he organ ism . In view of t heself-regulating properties of t hese devel­opmental systems, we ca ll them "epi genes " .Following Hull (1976), we suggest that theindividual appropriate to our analysis isthe species.

We know a devel opmental syst em or epi ­gene by i t s VJOr k . I t i s a theoretical en ­t ity, like t he gene , bu t i t i s even rroreabs t ract, becaus e it i s a process, a ser ­ies of interactions . Perhaps it i s bestt o consider it as a set of deve lopmentalfields in time and space that are jointlyresponsible f or sene useful part of an or ­ganism. The part appears gene r ation aftergener a t i on , species after species , thusproducing a cha in of horrol ogues . Overt ime , the r equirement fo r concer ted actionconstitutes se l ec t i ve pressure that knit sthe f ields t ogether . The temptations forreification and metaphor when we consider ,say , sel ecti ve pres sures on an epigeneticl and scape, are overwhelming . We oftenyield t o them in this paper , for wi thoutsuch devices camunication on t his sub jecti s impossi bly abstract and compl ex .

DEVELOPMENl'AL PRELIMINARIES

Let us turn to the properties of devel­opment that are centra l t o our analysis .To begin with a couple of truisms , devel­opment i s not a thing , or a series ofs tages . I t is a process--an int eractionbetween the expression of genet i c infor ­mat ion and environment. The internal en­vironment--what has previously developed- ­is as important as the external envir on­ment. The s impl ist i c ques tion that isinrnediately raised abou t any differencebetween individuals in a population--ist he diff er ence genetic or rrer e ly environ­mental? - -is a mis l ea ding di chotany because

any t hing that has deve l oped ha s as partof i t s genes is an environmental component.As Wadd ington ' s (1959 ) VJOrk ha s shown, anenvir onmentally induced change i s a devel­opmental r esul t with a r elatively weakgene tic component . That component can bes trengthened by selection , so that l essenvironmenta l informat i on is needed to pro­duce' t he effect . Thi s i s what he provo­cati ve ly but ap t l y termed "gene t i c as simi­l a t i on of an acquired character isti c" .

A second truism i s that devel opment i sto a considerable degree self-organizing .We do not have genes for individual ridgescompris ing our fingerpr ints ; nor do wehave genes that inform ea ch neuron in ourbr ain wher e i t wi ll synapse and wher e itsdendrites will gxos , We do have an inher ­ited program for making certain patternsof neuronal connect ions, but there i s con ­s iderable r oan fo r variation. This enve­l ope of ac ceptable variation , within whichdifferences do no t compranise the opera­tion of t he organ i sm, is bes t appreciatedfran the typological point of view.

The typological approach has played amaj or role in continental European VJOrkin evol ut i onary morphology . It has notbeen mich in evidence in the United Statesor Britain , where variability is generallyviewed s tat istical ly , as an expr ession ofpopul ation processes ; Bateson be ing t henotable exception to this t endency . Sei­l acher (1970) has set forth a valuable mod­ern vers ion of this approach- - a balancingof phyl ogene t i c , functional , and morpho­genet i c f ac t ors called constructional nor­phology . It i s under the heading of rror ­phogenetics that typology f inds i t s use .In order to under s tand t he developmenta lprocess that yields a variable structure- - say , our fingerpr ints - -one examines de­velopmental error s and their subsequen taccamndat i on , the r ange of variability ,ontogenetic changes, patterns of repairand regeneration , and especially aclaptive­ly neutral by-products of morphogenes i s .These neu t r a l bu t annipresent by-p roduc t sare traces of developmental processes .Sei l acher (19 73) has named them fabrica­tiona l noise. The amount of f abrica t i ona lnoise in a structure shows the degree offreedan that ex isted in its production .Thus , it i s a measure of the amount ofself-organization in the underlying epi­genet i c system. Seilacher 's appr oach ha sa general utilit y- -Hut chinson (1978) hasextended it t o an explanation of differ­ences in human intelligence- -and a specialva l ue to paleontology . With it, paleonto­l ogis t s can us e the pa t t erns preserved infossils as windoes on the epigenetic pro­cesses that shape those patterns, and ont he intrinsic evo l ution of such processes .

184 EVOLUTIO N TODAY Ra chootin & Thoms on

Fabricat ional noise i s a source of in­nocuous variability. A pot en t ially threat­ening source of variability is error indevel.opnental, pr ocesses . Yet , given thecanp lexity of devel.oprent , mis takes areinevitable, what ever the degree of genet i cspecifica t i on . Certain sorts of mistakesmay occur because of f ea tures of the ex­ternal envi.rorrrent , others may r esult franintrins ic susceptibilities to error. Ineither case , there i s a predi sposition fo rcertain kinds of mistakes to recur. Whent his happens , there is a select ive pres­sure either t o specify a s ingle deve l op­mental pathway a ll the rrore emphatically,or to accoom:xlate these tendencies to er­ror and turn them towards alternativepathways that lead t o the normal develop­mental end. These alternat ive pathwaysare , we expect , in large part created outof those wrong turns that a devaloprental,sys t em is peculiarl y l ikely to make- -theproblem becanes part of the so l u t ion .These r espons es to the inevitabilit y oferror are what Wadd ington (1942) calledcanalizati on . Canalized pathway s evolveso that in a variety of external and in­ternal envirorrnents the deval.oprental, sys­tem reaches its normal goa l .

We expect that alternative pathways tothe same devel.oprental, end are the rule indevel.oprental, systems . Selection will, webelieve, produce and maintain many alter­na t ive devaloprental, routes in the genane ,and the success of such canalization maywell be constant phenotypic expression inthe structure that is produced .

This suggests a paradoxica l invers i onof camonly held ideas about the na ture ofvariability. Wher e we see phenotypic con ­s t ancy , we may be dealing with underlyingdeveloprental, and genetic variability.Where we see phenotypic variability , forexample, in fingerprints, we may be l ook­ing at the results of a single gene t i ca l l yinvariant epigenetic process with a largecanponent of self-organization. In sanecases, such an epigene t i c process may belocked into a fabr i ca t i ona l mechanism thatcannot be further specified genetically .The large range of variability we see insuch cases is an extension of the inter­ac t i ve rather than the r eplica t i ve side ofor ganisms , and as such is not :innEdiatelylike l y to be t he source of fu ture evo lu­t ionary change. Unles s Fisher 's Funda ­mental Theorem i s f ramed in a wider, de ­ve l.opnental. context, it is perhaps not sofundamental .

Still, despite canalization within epi ­genes , mistakes will occur. Even a t thelevel of int er act i ons between epigenes,accoom:xlat i ons will still be made. Givent he inevitable mistakes - -a heart t oo small ,

or too large , or too far t o the side toplay i t s small r ole in the conditioning ofthe battalion of cells that induce the fo r­mat ion of lens- - there has be en a great se­l ec tive pressure t o "make do". This ac­coom:xlation- -behavioral , devel.oprental ,physiological- -is the r esult of the mul ­t itude of int er-connect ed alternat iveswi thin and be tween systems .

Occasi onal l y , gross errors occur andare still accoom:xlated . The congenitallybipedal goa t s tudied by Slij per (1942a ,1942b , 1946) i s a fallDUS example of this.Not only did the goat manage wi th its hindl egs alone , but , as it l earned to walkbi pedal l y , i t developed an S-shaped spine,modified muscle insertions, and developedsuch correlates of bipedal Locormt i on asa relatively broad neck and an oval rath­er than a V-shaped thor acic cross-section.No one would maintain that goats havegenes for devel oping an S-shaped sp ine ,"just in case". What we see her e i s abasic rnanrnalian potential, emerging frant he self-ri ghting pr operti es of the skel ­eto-muscular sy stems of a l l rnanrnals, andthe sor t exploited by our haninid ances­tors . A similar range of pot en t ial s , thistime for the skul l , is suggested by DuBruland Laskin's (1961) production of severalprimate-like features as the result of as imp'Ie nutilation of a synchondrosis in anewborn r at .

A spec trum of self-organizing develop­mental properties exists , fran alternativebiochemical pathways, to the bounded free ­dan of fabr i cat ional noise , to the canal i ­za t ion of deve lopmental systems or epi­genes, t o the ac coom:xlat ion of errors thatoccur in the inter action of epigenes , tothe behavioral and phys iological adjust­ments of the whole organism to deve lop­mental calamities . The pot en t ial to makethese accoom:xlations i s a canpon en t of theconservative force of stabilizing se lec­t i on. Such selec tion is omnipresent, butits expr ession is nearly invisible .,INI'RINSIC EVOUJrION

The epigene t i c landsca pes that are builtup for perfectly normal developrrental, r ea­sons are , fortuitously , a reserve of coor ­dinated, cohesive change . I f a mistake oc ­curs--not sanething as gross as a bipedalgoa t , but perhaps as great as t he dividedmaxillae of the bolyerine snakes describedby Frazzetta (1970) - -it may be accommo­dated . We do not know whet her t he ini t i a leffect was a response t o an internal or anexternal perturbation , but the snake YXlrk­ed, and it marked the beginning of a new,now tragically extinguished, l ineage .That such an ananaly could becane normalnust mean that after r epeated evocations ,

Epigenetics & Evolution PROCEEDINGS, ICSEB -II 185

t he response became genet i ca l ly ass imi la­t ed.

Genetic ass imi lat io n of an accommoda­ted deve l.opnen cal, change, if the changei s of imrediat e adaptive interes t , may bethe sort of r are event that marks the en­trance to a new adaptive zone . The inter­est of dcvel.oprent; to comparative anatrm­ists and paleontologists i s built on t hispossi bi l ity. But an accommodated develop­mental error that i s neutral or evens l ightly maladapt ive with r espect t o th eext ernal envir onment may still be genet i ­ca l ly assimilated i f environmental influ­ences persist in producing the error .That i s , given both intrinsic and extrin­sic selective pressures . on occasion se­lection on the internal environment canhave primacy over the demands of the ex­ternal environment. This may be a camonevent in evolution at and below the spe ­cies level.

Consider a spec ies whi ch responds de­va l.oprnentaILy to an environmenta l grad­ient by producing = phenotypes , A and B.Even if in all environments B is competi­tively inferior to A, if sore environmentexists such that the threshold for pro­duction of the B phenotype is crossed ,then there will be selective pressure toproduce the best, most harrroni.ous B pos­sible. This i s not the only outcexre; wemay also have selection to raise thethreshold of production of the B pheno­type , perhaps in the B environment itselfif the environment is wavering on the edgeof the threshold.

What is important is that, granting arecurrent environmental influence, "e canhave assimilation for intrinsic reasons.A possible example of this is the markedtrend to size reduction that occurred inmedieval cattle in Denmark (Degerb¢l 1963) .One hypothes i s to account for t his changeis that it is the result of keeping thecattle in captivity over the winter, rath­er than allowing them to range freely .This was the season that the calves werebeing carried , and the inadequate fodderthat the cows received produced small off­spring . The size change was not itselfadaptive, but while the environment calledit forth, it became a selective pressurefor smaller cattle in subsequent g~1era­

tions . Once started, the trend could notabruptly be reversed . Even wi.th improvednutrition, a large calf is no service tothe genes of too small a cow. A similarstory , involving accommodation to an inter­nal deve lopnental environment rather thanadaptation to external conditions, may ac ­count for the consistent evolution ofdwarfism in large island marrmals (Sondaar1977).

Develorxnental change is cohesive, self­integra ting and fast. It need not beadap t ive in the sense of fit ting sore as ­pect of t he external environment, thoughit may be. Adaptation may sexretimes beintrins i c ; that is, i t serves to furtherthe coordinated expression of a changethat exists mainly because that change iseasily produced . Such sorts of changesare we l L known, generally under the head­ing "a l.Loret.ry". What happens ontogenet­ically constrains and faci litates Whathappens phylogenetically . Allexretry i sr elated in turn t o t he pat t erns and pro­cesses of heter ochrony , which were so ablyrefurbished by Gould (1977). And hetero­chrony i s, simply, a special case of epi­genetic evolution: those changes that arefeasible in the interactions between epi­genes . Changes in the structure, position,function, relative size, or time of appear­ance of parts of organs are called forthfrom the usua lly cryptic variation in thepaths of their development.

In all of this we fo llow a track notoften taken fran that great marsha llingyard of evolutionary thought, Mayr's Ani­ma l Spe ci es and Evo luti on ~~yr 1963). Abreakthrough in that book is the balancingof external factors in speciation, espe­cially geography, which he had so thor­oughly established in Systema tics and theOr i gi n of S peci es (Mayr 1942), with ll1ter­nal factors- -the co-adapted gene complexes ,epigenotypes, and especially the geneticrevolution at speciation. These terms aresexretimes taken as labels for our collect­ive ignorance about species. This wethink is an unfair assessment . In thegenet i c revolution, ~~yr united the typo­logical properties of the wild type, whichshow up in the good soloist phase, withthe populational properties of balancingselection, which characterize the goodmixer phase. Thus he harnessed the theo ­retical M:>rk horses of the 1950s popula­tion genetics to the task of explainingthe emergent properties of species. In sodoing he produced a species concept thatcanbined the advantages of an intrinsicapproach, which could be applied to thebreakdown of developmental pathways in hy­brids, wi.th the advantages of an extrinsicapproach, which made sense of the geo­graphic and ecological aspects of species .This theoret ical approach to species isfar more powerful than one that is merelyoperationally convenient, say, a cut-offpoint on an electrophoretic score card.The genetic revolution is not yet very ac­cessible to study, but it is a major con­tribution to science , nonetheless.

A new emphasis on the intrinsic side ofevolution is called for today. Althoughit has been ,vith us since the biological

186 EVOLUTION TODAY Rachootin & Thoms on

spec ies concept, t his s i de of the concepthas been pl ayed down in f avor of such ex­trins ic ques t ions as al l opa try vs . sympa­t ry , t he real ity of subs pecies, l ocal ad­aptati on , charact er displacement , andantihybridization mechani sms . It i s timefor a change in perspecti ve , the sort thatcoul d be provided by uncoupling as michas possi ble the extrinsic and intrins i cas pects of evoluti on . Of special s ignif­i cance in this program i s t he odd sympat ­r ic, or morphologically sal tatory , or in­s tantaneous speciation that shows the in­trinsic evol utionary potentials of organ­i sms that are usually concealed by rroreobvious extrinsic f ac t ors. I n the 1950sand 1960s evo l utionists sought a singl et heory t hat could account fo r all the phe­norena of evol ution . Thi s has probablybeen pushed as f ar as it wi ll go . If weare t o go beyond i t, we mist; partiallydisassemble t he synthesis and experimentwi th t he potential s of i t s components .

Chi e f among thes e i s the l a t en t evol u­tionary potent ial of developmental systems .Most current considerations of epigenet icsr estrict the importance of epigeneti cmechanisms to t he reason for which theyevolve. Epigeneti c systems are conserva­t ive- - t hey prot ect the ends of a develop­mental pathway by r esor t ing t o al ternat ivedevelopmental means. But the normati veflIDctions of epigene t ic sy s t ems do not ex­haus t their pot en t ial when i t canes tot r ans - spec ifi c evol ut i on . How do epigen ­eti c systems cane together and how do theycane apart? A look at the fossil r ecordgives , we think, sane hints concerningthis problem .

PALEONl'OlDGY AND EVOUITION

I t has cons ist en t ly been the pal eont o­logists who have the hardest time in r e­conciling syn thet i c theory wi th t heirstock in t rade of evol ut ionary data . Theexistence of l ong-term trends, sane a l leg­ed ly quit e single-minded; l arge scale con­vergence and parallelism; the abrupt ap­pearance and , at some subsequen t point ,exp losive radiation of new groups ; the ap­parent abs ence of intermediates ; the in­tegri ty (in terms of rrorpho logy and r atesof evo lution) of what Simpson (1944) or i ­ginally ca lled adapt ive types ; and suchthrowbacks to Geoffroy-S t . -Hilaire asWilliston ' s Law-- these have a lways naggedat the synthet i c heart s of evo l ut ioni s ts.Ther e i s no denying t ha t these are problemsto be solved ; indeed, r ec en t pa l eon t olog­i cal work has l ed us t o take t hem rroreserious ly. As exampl es, we have Van Va­l en' s lawful r a t es of extinction fo r hi gh­er taxa (Van Valen 1973) , the arguments ofEldredge and Goul d (1972), and St anley(1975) t ha t we do not see spec iat i on in t he

f ossi l r ecord, and that many species showno change a t all between or iginati on andextinct i on, and Gingerich 's (e .g ., 1977)argumen t for uru.-dfrectdona l, changes inrrorphology . The rror e we know about theLower Cambrian diversifi cation of inverte ­brates , and the Cretace ous r ad iation ofang iosperms , the fas ter and rrore staccatothey seem to be . Directionality , salta­t ory leaps t ha t land on their feet andstay sti ll unt i.L they l eap again, adaptivetypes - -these r eca ll the irri tat ion But ler(1879) felt fo r the evol ut i on of his day-­was it really accounted f or , "by a seriesof accidental varia tions , each of whichwas thrown for , as it were, with dice? Weshall rrost; of us feel that there mist; havebeen a l i t tle cheating sanewhere . . . "

Epigenesis can provide the directional­ity, the typology , t he saltati on, in shor t ,the cheating that has in the past arousedin the breasts of our predecessors pas sionsfor neo-Lamarckianism , aristogenesi s , pan­genesis, bathmism, hopeful nonsters , and ahos t of entelechies . They saw sanethingthat generati on af ter gene rat i on of evolu­t i onists have been t aught not t o see- -anintegrative and emergent s ide to evolution .Epi genetics can bring to this phenanenona strai ght - f orward, non-mys t i cal explana­t ion . However , i t is an appr oach on whichi t i s r ather difficult to experiment .What we are about t o out l ine may not ca llt o mind 101 falsifi able hypotheses . Thisdoes no t worry us . The strai ght-forwardprobl ems of evol ut i onary biology have beena ttacked a l ready. The r esidue that r e ­mains wi ll not give up its secrets toblunt; methodological instnnnents .

MEGA-EVOLUTIONARY CHANGE

The rare produc tion of a new adapt ivet ype is not predicted fran l ower l evels ofanal ysis such as population gene t i cs; suchevents are emergent . But, if we mightadop t Needham' s (1933) metaphor that evo ­lution r equires a changing of gears , agoing t hrough neutral, then we woul d arguethat our black t r ansmiss i on box is develop­ment. And epigene s is ensures that ourtransmis s ion i s at l eas t semi - autcxnatic .Though t he "point " of canal i za t ion i s toensure t hat an expected resul t i s obt ained ,sti l l an lIDexpect ed r esul t autcxnaticallypull s rel ated devel opment al sys t ems alongwith it.

Let US suppose t ha t a developmentalmistake , and such behavioral, structural ,or phys iologi cal accommodati on as t he mis­t ake engenders , a llows an organism t o en ­t er a new adaptive zone . Then all thatis needed for i t t o pers i s t there , i s forthe l ower ing of t he developmental thres ­hol d that general ly prevents that mistake .

Epigenetics & Evol ution PROCEEDINGS , IesES-II 187

For assimilation to occur , t here must bean environment which frequently evokesthe altered phenotype. 'That envi.rorrrent;has always been assumed to be ext ernal.The epigenetic effects of external changecould be transmitted to and intensifiedby the internal envi.rorment , which couldthen be the prime rrover behind assimila­tion .

EnvirorJrrentally affected threshol ds areknown; Van Valen (1974), for instance, hasdocument ed an increase in (admit t edl yhopeless) five-legged frogs in particul ar­l y cold l akes . But if such changes wereuseful, t hey could be assimi lated into t hegenorre , Waddington (1975) suggested thatadap t ive phenot ypi c differences be tweenquiet and turbulent water r aces of th epond snai l Lymnaea stagnali s were geneti­cally assimilated in j ust such a way. Theclassic obj ection t o hopefu l rronsters - ­that a pig with wings has no chance offinding a s imil arly endowed mate- -missest he point t hat if you have one pig withwings , there are rmre where that one carnef ran- - in th e developrterital pathways of therelatives of Archaeoptopig .

When an adaptive change has occurred ,it will at f irst have but a f l ickering anduncertain phenotypic expression . Immedi­a t ely , t here will be intense se lecti on topr ot ect and buffer the express ion of thischanged state . Secondary patheays willevolve that canalize the system. It willbe fur t her stabi l ized by t ies to other de­velop:nental sys tems that are temporally,structural ly , and funct ionally related toit. This kerfuffle of evolutionary activ­ity i s only a rrore intense express ion ofthe cons t ant but cryptic se lection thatmaintains and strengthens the developrenr­a l status quo. In the end, a successfulevolutionary step will exhibit a hard,gem-l ike constancy in the express ion ofthe new feature . The adapti ve novelty willhave been pro t ected by a canalized epi­gene , assembl ed out of the predispositionsto error in the early, unstabi l ized stage .

The new adapt ive feature may lead theorganism to new behaviors and into newenvi rornnents ; these envir ornnents can theni nt er act wi th th e underlying epigene toproduce further changes. The rrodi.fi.ed epi­gene many a l so be affected greatly in itsphenotypic expression by minor changes inthe wel l cana lized develop!lffltal systemswith which i t interac t s. Both intrinsicand extrinsic fa ctors thus may lead to fur­ther changes , because t he recently alteredep igene is relatively l ess buffered bysecondary pathways or deep devel op!lfflt alchannel s than its older, rrore cons istentneighbors. Continuing changes, if adapt­ive and genet ical ly as similated, lead to

rmre and rrore changes on a single l argeadapt i ve thane . This is an adaptive r adi ­ation. Not only might such a r adiation ber apid ; we would expect it to be so. Werei t not it would be overtaken by the con­s t ant pressure of stabilizing se lect i onthat resu l ts in th e production of a matureand wel l canalized epigenet i c l andscape .The epigene need not vary in all direc­t i ons at once; perhaps certain sorts ofvari at i ons are part i cul arly easy or adapt­ive . If t he sarre sort of change occurssequentially in a s ingle epigene, thecumulat i ve effect is a l ong term trend,such as hypsodonty in horse t eeth.

ATAVISMS

We have proposed that a relatively un­s table epigenetic system might illuminat esever a l major evol ut i onary ques t ions. Butepigene t ic systems are normally s table .Where do we turn to s tudy t he actual wor k­ings of evolut i onary epigenetics ? An ob­vious area i s t he huge field of atavismsand their experimental analogues.

Horses born wit h three toes, flat f isheswith pi~ted undersides , Hamp~' s (1959)experimentally manipulat ed chick l eg thatreverted to a r eptilian state- - these arestriking signs of the sa ltato ry potentialof development . Of such cas es, Gould(1980) writes:

What el s e might the ir gene t ic s ys ­t e m maintain , normally unexpres s ed ,but ab le t o ser ve, i f act i va t ed , asa po s s i b l e focus for major and rap­id evolu t ionary chang e? [ a nd] Ano rganism' s pa s t not o nl y constrainsits fu tur e ; it a l so p rovi des as leg ­acy an enormous reservoir of poten­t ial for rapid morphologica l c hangeba sed upo n s ma l l ge ne t i c a l terat i o n .

\-Ie agr ee totally with the spirit , but theletter is slightly t roub ling .

Atavisms undoubt edly give us insightinto epigenetic processes, but t hey onlymislead when taken as examples of the pat­terns of epigenetic evolut ion . We l abela variant as an atavism because i t vio­lates some defining quality and derivedcharacter state of the group in question-­horses are expected t o have single hoovesand flatfishe s are expect ed t o have rightand left s ides unl ike . Such qual ities, inpar t , determine t he or ganism's adapt ivepotentials as wel l , so that unless theyhave only recentl y evolved their devel op­ment ought to be heavil y cana l ized. Whilevari ant s on an adapti ve thane have evol­utionary potential , th e undoing of an ad­aptive t heme does not.

188 EVOLUTION TODI\Y Rachoo tin & Thomson

The major f eatures of evol ut ion arenot conposed of s tructures withdrawn fr ana developmental legacy ; t hey are cCXllpose dof processes that shape themselves as theygo a long. Epigenes retain ances t ral poten­t ials because, to use Riedl's (1977) t erm,they ar e ' 'burdened'' with other epigeneticsystems that use t he i r products as devel­opmenta l cues. But these ancestral poten­t i als have little chance of expression int hemselves , becaus e their ancestral pheno­typic expr ess ion i s i rrel evant to the se ­lective pr essures favoring t heir r eten­t ion. The legacy exists , but t he assetsar e not converti ble . It i s becaus e of theburdens t ha t epigenes bear that they haveevolved t he capacity to accorrm:xlate eachother. And it is t he capacity for accon ­modati.on that gives epigenetic systemstheir mega- evolutionary s i gnif icance, be ­cause i t fac i litates adaptive experimenta­tion .

A genuinely l abi l e epigenetic systemought t o be of the greates t in t er est to anevolutionist, and i t i s a far, far bettert hing than an occas i ona l atavistic slip ina mature epi gene t i c system. This i s nott o say that reversion has no part to playin evolutio n , just that t he par t is small .After all , all God 's hoatzins got rmrethan wings .

ADAPrATIOO

While an epigenetic approach cannottell us what will make a new adaptation,it does suggest sanething about the sour­ces of adaptive novelty and the ease withwhich an adapt i ve change i s initially ac ­corrm:xlat ed . As Gould (1977) notes, manypew adaptations wi l l be t he r esul t of re­arrangemen t s of developmental informationalready at hand. Playing the f eatures onone age or stage or size or shape againstt hose of another i s , we do not doubt, the'pr imary material basis of evolutionarychange . Gould argues convincingly for anextrinsic, ecol ogi ca l explanation of theser eshufflings. He ~uld add that intrinsicfactors may a lso be a t ~rk .

In cases where a functional intermedi­at e i s impossible, for instance in t hemaxilla of bolyerine snakes , which is ei ­ther in one piece or = , a developmentalexplanation may be the only alternative .Simi l arly , a l ong- standing problem in theevolution of the hind limb of r ept i l es isthe explanation of the transf er of thecalcaneum fran the foot (in crocodiliansand pseudosuchians) to t he leg (in dino­saurs) , fran one functi onal unit to anoth­er . Paleonto log is ts have been hard pr ess ­ed to discover a funct ional int ermedi at estage; a gradual sequence is poss ible onlyby invoking hypothetical small, l i ght rep-

t i les with reduced ca l canea and other hope­l ess lTOns t ers. A deve lopmenta l sequencei s lTOre l i kely : a s imple rate change in de­velopmental f iel ds caused the ca lcaneumto be included in a different struc turalunit and t he r esult was functionally accan­rrodated ( in cluding shifts in nuscle in ser­tions occurring during subsequent deve lop ­ment). The capture of the calcaneumchanged the internal envi r onment of thefields invo lved in l eg development . Theinitial accorrm:xlat i on was the development­al response upon which se lection ~rked,

eventual ly producing its genetic ass imi la­t ion . The r esult becanes an adaptation inthe sense of proving adapt ive, but not inthe sense of having been sel ect ed for .The change in the pos ition of the tarsaljoint immediately gave a new range of ad­apti ve possibili ties . The new pat tern andthe new epi gene may be the origin of fur ­ther intrinsically produced ananalies ,sane of which may prove adap tive and forman adaptive radiation .

Even those adaptation s which do notarise fran r earrangements of an organism ' sdevelopment al pathways filqy somet imes beproduced by admixture with for eign devel­opmental pathways . Given t he free-float­ing abi l i ty of devel opmental systems toaccorrm:xlate to insult, it ought co be pos­sible for introgression t o be the basis ofan epigenet i c revolution. The phenanenaof hybridism are pre-eminently t he pheno­mena of developmental in cCXllpa t ibil i t y .But there is no reason to deny t he possi­bility that a mixture of related but dis­tinct developmental pathways might pr oduceadaptively in t eresting novelties, \'hichon occasion are assimilated .

Developmental shake -ups need not be re­s t r ict ed to interactions with congeners .The products of symbionts can shape devel­opment of a host so consistently that thesymbionts becane part of its intrinsicevolution . lhus, in sea lettuce ( VI va)the characteristic foliose thallus hasbeen shawn to be induced by bacterial sym­bionts. In axenic culture the a lga growsas tufts of uniseriate cel l s , and t he ad­di tion of various bact eri a pr oduces rib­bon-like forms, and tubular forms that r e­semble the related green al ga Enteromo rpha(Provasoli & Pintner 1980).

As for the tempo of adaptive change ,the epigene t ic approach suggests that ont he scale of evolving l ineages , an " imna­ture" epigene may facil itate a successionof r elated changes. At the f iner scale ofthe successio n of ind i vidual species, wesuggest that the constant evol ution of de­velopmental systems within a species ir­regularly erup t s to produce new speci es ,which then normal l y remain phenotypical ly

Epigeneti c s & Evolut i on PROCEEDI NGS , I CSEB- II 1B9

unchanging even as their developrrental sys­tems are e laborated in ways t hat fo rtui­tous ly determine t he na ture of t he i r des­cendant s pecies . Organisms are subject t ocons tant evolution, sane extrinsic , whi chproduces local adaptation , subspecies, andclines, and sane intrinsic , which producescanalized ep igenetic pathways and a llowsfo r t he production of new species, or atleast a class of species with a specialrrode of origination, and special potentialfor future evo l ution .

ClASSIFI CATIOO

Evol utionary epigenet ics may offer aresolution to t he current quandary of sys­tematics . To date, the chief contri butionof cladistics to the data of evolution hasbeen the uncovering of far nore parallel­ism (horopl.asy) than anyone could haveimagined. Only cladistic analysis couldhave made this discovery . If it holds up ,the ph i l osophical assumptions of a l lschoo ls of classification, including clad­istics, will turn out to be false. I fparallelism is the rule , then why shouldwe i dent ify parsinony as the absence ofparallelism?

Corrmmly held pr imi.t i ve developrrentaJ.pathway s, each of which have predisposi­tions that are expressed independent ofdescent, that is, paraphyletically, maywell hol d t he key to what is going on.Extreme ly detai led attention to develop­mental pa thways may help to untangle ap­parently cladal arrangements of charac­ters and the gradal processes of develop­ment that could produce them . For this ,a ser i es of developrrental stages will notin itself be sufficient: it i s the enve­l ope of epigenetic accamodations withinwhich reside the ontogenies of s is t ergroups that is no st important.

Paleontologists woul d seem to be l ef tout in t he co l d by t his program, but suchis not the ca se. They can analyze fabri ­cational no ise , which i s an appropriateintroduction to the epigenetic envelopearound the production of fossilizablestructures , and they can trace the evolu­t ion of such envelopes through time.

SPECIATION PATIERNS

Obviously , bithor ax frui t flies, what­ever t he complexity of the i r altered norph­ology, are not per se spe c ies in the senseof the reproductive isolation that is atthe heart of the b iological species con­cept . One may grant us our saltations ,and t hen deny them any s ignificance unlesswe fashion appropriate anti -hybridizationmechanisms that would make them "good"species .

To this we answer that r eproduc tivei sol a tion has a l l t he proper ties of a de ­veloprrental s ystem, one that has as i t sgoa l the pr edic t able r eproduction of thespecies . As such, i t r equires an especi­a lly large set of cues fran the externalenvironment. The environment is involvednot just during early developrrent , butthrough adult life. Not only mist struc­ture, physiology, and behavior of the or­ganism be coordinated , bu t all I1USt be co ­ordinated with the structure, physiology ,and behavior of other individuals of thesp ecies. The demand fo r t he equ ivalent ofcanalizat i on and sel f-regulation i s allthe stronger here, given the mich l argerenvironmental canponent. The argunent canbe made that mate recognition systems areintrinsic to all organisms (Paterson 1978,1980) , and that these intrinsic systemsare in many or gani sms more important inreproduction than such extrinsic factorsas anti-hybridization mechanisms . It maybe easier to learn to mate wi th like thanto learn not to mate wi t h un l ike .

I f we view the mate r ecogn i t i on systemas a kind of epigenetic system with aparticularly large environmental canpo­nent, then all that we have said about in­trinsically controlled saltatory changewill hold, except that there is in thiscase less reason to require an adaptivechange to result fran the saltation. Anychange in t he mate recognition system will"work" as l ong as i t succeeds in selec t ingl ike-minded mates and perpe tuat e s i t s e l f .This wi l l produce a new biological spe­c ies . If that species i s otherwise doingnothing different fran its parent specie s ,it may well disappear for no other reasonthan its comparative rarity .

Thus, speciation may be a case of easycane , easy go . The cryptic or siblingspecies that sanetimes turn up when agroup is c losely studied may be cases ofsuch easily produc ed , s l ightly differenti ­a ted , adaptively equivalent species . Per­haps they r epr esent the few survivors ofa vastly greater number of ephemeral spe­c ies that population biologists wouldnever find unless they had sane good rea­son to look for them.

Fran our perspective, a lineage with atruly pranising evo lut ionary future woul dbe favored wi t h both a sanewhat l abilemate recognit i on sys tem, and a sanewhatlabil e ep igenetic system for a trait thati s of adaptive interest . Both will besufficiently canalized to appear as con ­s istent, dependable characters within spe­cies, but ne ither wi ll be so burdened withother developrrental responsibilities thatthey cannot change to produce new species.Perhaps this sounds like a lot to ask fo r .

EVOLUTION TODAY Rac lloo ti n & Thomson

We think not . I f , as the foss i l r ecor dsugges ts, spec ies are general ly unchang­i ng once they are formed , then t hose line­ages which diversify and prosper will bethose that can eas i l y speciate and in sodoing capture intr ins i cally gener a t ed ad­aptations . In effect , we have spec iesse lection for modes of mate r ecognitionthat promote speciation. Species se lec­tion need not be t he tot ally pos t hocaccumulation of l ineages that happen tohave survived . I t i s in our scheme an ac ­tive, intrins ic factor, a mechanism thatover geol ogi cal time produces l ot s ofspeci es in a lineage . Adaptively indif ­ferent , ephemeral spec ies are produc ed inl ar ge number s as wel l - - t hese are a kindof spec ific l oad .

Our ideas in th i s area are an extens:'onof Carson 's (1975) theory of the open andclosed gene t i c systems. Certain lineagescan adapt only by speciat ing- - t hat i s ,shaking up their closed genetic sys tems .Others can adapt without speciati on- -theyhave relatively l ar ge open sys tems. Inl ineages of the first sort , we sugges tthat mechanisms that predispose the organ­i sms t o undergo frequent speciations willbe se l ected .

Mos t fac t ors that have been implicatedas causes of speciat i on could be rein­forced by speci es se lection unti l they be­come a favored mechanism for speciation- ­an adaptat ion at the level of l ineage .The factors include suscepti bili ty t ochr omosanal changes- -in ploidy level,chromosome number , organizat ion of sexchromosomes (for instance in bovids, seeTodd 1975), inver sions and t ranslocations ,and many permutations (see review by White1973) . The frequency of such changes de­pends on the effi cacy of mechanisms forchromosanal r epair- -a kind of canalizationlit t he cellular level. The slight est de­crease in t he ef ficacy of such r epair me­chanisms could greatly increase t he chanceof speciat i on without being an appreciableburden on the dependabilit y of meiosis.The shuffling of immunologic recognitionsystems in the gametes of plants and freespawning animals and the co-evo l ut ion ofeukaryo t es wit h r apidly evolving pathogensor symbionts in th e germ line (or meri­s t em) coul d al so have t he effect of isola­ting a popul ation by intrins i c means, andthus become a mechanism for spec ies pro­duction .

In r are instances , a mechani sm for spe­ciating and a suitably plastic , adaptivelyint eresting epigenet ic system will co-oc ­cur in an organi sm whose environment i ssufficiently complex in space and time topr ovide al l that could be asked for in t heway of extrinsic factors favorable to spe -

ciati on . Such a case i s provided by thecichl i ds of t he rift l akes of Afr ica.

Three intrinsic factors contribute tothe ease with which cichl ids gener a t e newspec ies. Their complex and pl astic behav­io r provides plenty of material t hat canbe shuffled t o make mate recogniti on sys ­t ems. The fish are int ensely visua llyor iented , as schooling fry and , as adults,in feeding and mate r ecognition. Inter­estingly , cichlids have the earliest dev­eloping opt i c placode of any teleost. Andt he f i sh are colorful , they exhibit colorpolymorphism , and th ey depend on colorcues for mate recognition . On t he appar­ently adaptive s i de, ci chl i d spec i es showa tremendous diversity of j aw and toothmorphologies . Liem (e .g . , 1973) a t t r i but estheir success to a new arrangement of thepharyngeal j aw. The array of forms , Liemwrites, calls for "minor r econs t ruct i on ofthe genot ype which i s involved in evolu­tionary changes of t he pert inent ontogene­tic mechanisms" . The ontoge netic mechan­i sms may requi re minor tun ing, indeed:the mollusc-eating cichlid Ast a t oreochro ­mis all ua undi was reported by Greenwood(1965) t o produce bicuspid teeth whenr aised on insec t s but mol ariform t eethwhen r aised on molluscs . These intrins i cfac tors , played against a success ion of"akes in t hese ancient basins, coul d pro­duce the hundreds of endemic speci es , pro ­bably during the geol ogi ca l ly shor t l ivesof the current lakes . For while the ba­s ins are ancient, the lakes th emselves,like the Triass i c r ift lakes of North Amer ­ica, fi ll with water and dry up in r esponseto climatic cycles on th e order of 20,000years (Li vingstone 1975; Olsen et al.1978).

Note that our epi genet ic approach tospec iation does not insis t that th e mech­anisms we postulat e apply to all specia­tion event s , or even to al l lineages .But if th ey apply t o some l ineages , andsome speciat i on events in other lineages,t hen , over geological time , th ey can ac­count for the existence of properties ofthe exi sting biota her et of or e inexplicableor uns een .

CXlNCWSION

We st art ed with orthodox notions of thefunction of epigenesis , whi ch we have as­sociated wit h t he intrinsic s ide of Mayr I S

concept of species. These we appl i ed tocurrent prob lems in pal eonto logy - -adapt i vezones, functional anatomy , patterns ofor iginat i on , change (or i t s absen ce) inf ossils with excellent s trat igraphic r ec­or ds . We suggest :

1 . Properties of epigenesis quite for -

Epigenetics & Evol ution PROCEEDI NGS, IeSEB- I I 191

tuitously make r apid , cohesive, and ftmc­tional change poss ible . Internal adapta­tion is as impor tant as external adapta­tion.

2. Nonnally constant features, if theyare not heavily burdened by ot her develop ­mental systems, may be the source of newevolut ionary directions because of th eirunderlying developmental variabil ity. Var­i able features may not be , because theirvariation may be fabr i cational noise.

3. A spec i es is defined by , among oth­er t hings, i t s cohesive devel opmental sys ­tems . Even t hough a spec ies need notchange phenotypicall y dur ing its life , i tis cons t ant ly accumulat ing s i gni f icant de­velopmental variabili ty, which allows (butdoes not r equire) r api d , even sa ltatorychange i f i t spec iates .

4 . Mate r ecognition systems are alsoep igenet ic sys tems- -what i sn ' t, after al l?Ma te recognition systems are nonnal l y wel lcana lized ; abnonnally t heir r earrangementproduces new species , without the con­straint of pr oducing adapt ive changes . Anew spec ies so pr oduced may for tui tous lycapture a new adaptation ; such spec ies aremor e likely to survive.

5. Once a devel opment al change has oc­curred , t he same epigenetic system, if notwel l buffered f rom developmental errors,may make related successful mistakes . Thisproduces what we r ecogni ze as t r ends, adap­t ive zones and adaptive radiati ons . Thoughper haps very rare at anyone t ime, over thewhole hist ory of l i fe, th e r esults wouldprofoundly shape the entire biota .

6. Spec i es se l ection i s an intrinsicand active proc ess- -given punctuated equil ­i br ium, those species that easily spec iatewill capture rmre adaptati ons and be rmrelikel y t o pers i s t and l eave descendant spe ­cies . Therefor e, mechanisms of speciationmay be cons idered to be adapt at i ons at thel evel of l ineage. When plastici ty in adevelopmental sys tem and the mate r ecogni­t ion system co-occur , species swarms result.

7. Horrologous structures, pr oduced byevolving developmental sys t ems or epigenes,are a basic per sis t ent feature of mega­evol ut ion, expressed in individuals of l im­i ted duration- -speci es.

8 . A t horough-going r evision and r ein­tegration of the synt hetic th eory is pos ­s ible on these gr ounds .

Although this paper is a natural exten­s ion of accepted ar t icles of the synthetictheory appl ied to the data of paleontologyand morphology, t he cumulati ve effect i s an

evol ut i onary theory that i s nearly an in­ver s i on of the usual expectations of evol u­tionists . Sal tation , typo logy , intrinsi­ca l ly directed speciati on , evol utionarytrends independent of external condit i ons,t he uncoupling of current population gene­tics and higher l eve l phenanena of rnega­evol ut ion , genetic assimi lat ion of acqui r edcharacter ist i cs, selection for the abi l ityt o speciate, t he ubi quity of paral l elism-­t hese are not i deas that figur e prominentlyin t exts , and sane of them have beengr ounds, in the r ecen t past , for excommun­ication from the scientific communi t y.

We are by no means say ing that suchideas ought to be the new dogmas of evolu­tionary biology. We are of f er ing this ap­proach not as a r eplacement, but as a com­plement t o th e existing t heory . Evol utionis pr e-eminent ly a science of contingenttruths - - t ha t i s , demonstrating th e exis ­tence of allopatric spec iation by nos tret ch of the imagination implies th enon-exis t ence of sympat r i c spec iat ion .So too, with th e i gnor ed if not proscribedevolut ionary ideas that have been ser ious­ly se t forth by such notable workers asBateson , Gol dschmidt , Waddington , and manycontinental workers. The synthetic t heoryi s sufficient ly mature to be ready to har­monize with many of its apparent oppos i tes.The r esu l t ing pluralistic approach to na­ture suggests innumerable new problemsand holds out sane hope of answers to oldproblems we have alrrosr forgott en .

We invite you to r eflect on the possi ­bili ty that sane of t he evol uti onary hypo­theses we have al l been taught to r ej ectare perhaps no rmre wrong than the al t er ­natives that are th e usual bas i s of ourday t o day wor k. If you will suspend dis­bel ief, t his can be an invigorating andexciting prospect .

We ask, ftmdamentally , that you balancethe reductionistic , generally extrinaicappr oach to evol ution, which assumes thatal l evolution i s t he warfare of self i shgenes wri t l arge , wit h an intrinsic s ideof evolution most easil y perceived fromthe higher integr ative l evel s of paleonto­l ogy and morphology . It i s from this van­tage point that certain emergent proper ­t ies of development l ead us to t ake a hewl ook at t he nature of spec ies . We ask yout o balance the selfish genes wit h t he per­sistent se r ies of horrologues whose perpetu­ation we attribute to cooperative , accom­rrodating developmental systems, which mightbe ca lled "selfless epigenes" .

Richard Gol dschmidt 's (1940) Materi alBasi s of Evoluti on made the case for de­ve lopment, saltation, and the uncouplingof micro-evolution and macr o- evol ution .

19 2 EVOLUTION TODAY Ra chootin & Thomson

l ection.332.

Writ ing of the cr i t ical r eception of thatbook in his aut obio graphy (Gol dschmidt1960) , he sa id :

Th i s t i me I wa s not o nl y c raz y , buta l most a c r i mi na l . . . [ b ut ) I a m c o n­f i dent that in twen t y years my bo ok ,whic h i s now ignored , wil l be g i venan hono rable p l a ce i n the hi s t o ry o fe volu t i onary tho ug ht.

We stand in his house , twenty years afterthose words wer e published , and f ind apro phet not without honor .

ACKNCMLEDGEMENTS

For discuss i ons and criticisms of thismamiscr ip t , we are indebted to CatherineBadgley , Anthony Bledsoe , Paul Olsen ,Kevin Padian and Scott Wing. We r eceivedthe advantages of the spec ial expertiseof Richard Harrison (population biology) ,Robert Nakarrura (botany and Scr ip ture) ,and Scott Poethig (developmental biology ).Our special t hanks go to Arrr:! McCune andLouise Roth, who not onl y provided exhaus ­tive criticisms a t every stage, but alsocontributed or inspired several importantconcept s.

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