Epigenetics, paleontology, and evolution

EP IGENETICS , PALEONTOLOGY, AND EVOLUTI ON S ta n P . Ra cho o t i n and Kei t h S t e war t Thoms on Pe a bo dy Museum of Na tu ra l Hi s t ory , Yale University , New Hav en , 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 ive individua l s of limi t ed dura t ion, and interaction with environment. We recas t th es e proper t i es in mega evolutionary terms. Harologous structures persist over geological t ime as th ey evo lve in f orm and func t ion . Spec ies, which arise through a greater or lesser genetic r evolution, behave as individuals. The interac t ion of genes and environments- -development- -under lies bo th the origin of species and the continuity of harologies. The properties of epigenetics - -self assemb ly , feedback, a lternative pathways to the sane devel opmental end, canpensati on for the inevitable irregularities of development--allow a redefinition of gene t ic revol ution in terms of the establishment of new, stab le 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 ep igene tic 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 f ering" exists . As errors oc cur , sane will be ep igenetically acconm:>dated and , if adap tive, gene t i cally assimilated . Thes e are the quanta of evo lution . If a r ecent adaptive breakthrough has oc curred, i t wi ll be " suppor t ed" at first by interacting ep igenetic sub-systems. The poorly canalized epigenetic system roost; closely associated with the new adaptation will be under intense selection to build up an epigenetic environment that assures the predictable expression of the new trait . Until this happens, fur ther " exper imen ts" along the l ines of t he initial change can occur and be assimilated . Depend ing on eco logical mi lieu, t his i s the stuff of adaptive r adiation , evo l u t i onary trends, or a llanetri c change. Speciation, which can occur without any adaptive chang e, is th e result of analogous changes in the ep igenetic systems responsible for mate r ecogni tion . We accept the neo-Darwinian reliance on natural selection acting in populations. But we choose to concentrate on i ts action on developmental processes, rather than on traits , the obvious and experimentally tractable end -products of such processes. The normal features of epigenet ics f ortui tousl y l ay down the lines of l ea st r esistance to evo l utionary change. We find ours elves l ooking a t an intrinsic and emergent s i de to evo lution, a view that in the past was held, on s imilar gen er 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 out of the potentials of selfless epigenes. I NTRODUCTION The title of our paper, "Epi gen etic s, Paleontology, and Evolution", i s de liberately chosen to r eca ll the title of the conference that was held at Princeton Univ ersi ty in 1947 on "Genetics , Paleontology, an d Evol ut i on" (Jepsen e t a l . 1949). I t included not only th e subjects of gene tics , speciation, and paleontology, but canparative anatany, ecology, and systematics as well . The syn the tic theory that came of age with that symposium ha s been the notable success of organ isrnal biology of thi.s century . In a day when theories in o ther parts of biology change wi th the seasons, it i s astonishing to f ind that 33 years later the study of evo lution is no l es s vigorous f or having r emained in the sane no de . We =uld be pleased if our contri - bution i s seen as a na tural offshoo t from the 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 pe r sp ective . The answers to thes e questions are, we think , t o be found in a considera t i on of the evo lutionary implicat ions of development and the developmental impl i cations of evo l ution, topics that were notably l acking in the 1947 conference . Our goa l in t his paper i s to se t in a developmental con text the problems of megaevo lution : the nature of adaptation , the tempos and nodes of evo l ution , the framing of us eful general izati ons about the origin and diversifica tion of major groups . As we go about this , we find ourselve s r ein- G.G . E. Sc udd er & J . L. Rev e a l (ed s .) EVOLUTION TODAY, Proc e edings of t he Second Inter na ti o na l Congress o f Sys tematic a nd Evolut i onar y Bi ol o g y, p p . 18 1 - 19 3 . 19 81 . I 182 EVOLUTION TODAY terpreting sane of the ftmdarnenta l concepts of evo lut ion, including variation, s pec ies, and what i t i s that selection acts upon . These reinterpretations cane out of a series of generally accepted premises about development , which, however, have unexpected impl ications when viewed over the time scale familiar to the paleontologist. Our paper is an outline of a way of ret:hinking what everyone knows about evolution. We ask you to rearrange your mental furniture and consider sane changes that we think are suitable for sane circurns tances . Al though the rearrangeme nt is new, the pieces are not . Those that look unfamiliar we have only brought down from the attic . In the broadest terms. we ask what mega -evolution ought to require of theories at the level of genetics and development, and also at the level of speciation. We expect that nothing at the l evel of megaevolution contradicts what happens at these l ower levels, bu t that we will not fully understand these l ower l ev el s un til we actively search them for phenCID2I1a that may seem peripheral to the population biologist, but which are required to explain the data of the paleontologist and the roorphologist. 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 the nature of species and speciation . We also ask you to allow us to break one other convention of evolutionary theory, concerning intrinsic and extrinsic factors in evolution. Extrinsic factors are the relations of an organism to the external environnent- -adaptations to local conditions, the sorting-out of congeners in sympatry by character displacement, and such chance effects as the genetic sample borne by the traditional gravid female compared to the population from which she derives, or the effect of a river changing its course and cutting off a population. We accept such extrinsic factors as the carrron property of all m:xIem evolutionists. But although we all believe in such factors, they are remarkably difficult to demonstrate in anyone case . We define intrinsic factors as the adaptation of the genane to itself . Developmental mechanisms, especially epigenetics, the selforganizing and correcting properties of developmental pathways, are the means by which the intrinsic side of evolution i s manifested . Intrinsic factors will be just a s difficult to demonstrate as ex trinsic factors, all the roore so because biologists are not accustaned to t:hinking much about them. But there is no a priori reason why they rrust be mystical. Rachootin & Thomson "Intrinsi c" and "ex trins i c" bear close relation to the distinction that Mayr has drawn be tween typological and populational thinking . Thr oughou t the paper, we wi ll be contrasting a populational, or , rrore generally, an extrinsic approach with a complementary intrinsic approach that is developmental and typological. Note that both approaches are ways of t:hinking, not hypotheses about nature . comThe mind has a hard time holding pletely different views of the worId simul taneously, but it is our guess that having two ways and switching when i t seems appropriate i s better than having one 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 typological m:xIe. Development shows directedness; in an experimental manipulation, the embryo " tri es" , if you will, to develop normally, according to type, in spite of the insult. Results in a dev el opment al experiment turn on the behaviour of particular, crucial embryos. This is a far cry from population thinking. The dichotomy is apparent in the 1947 symposium, which ne glected developmental biology, but not because there were no evolutionists interested in it . Indeed, embryology dominated evolutionary studies in the las t century , and was the guiding light to such twentieth century vorkers 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 , could Goldschmidt 's macro-evolution, which took developmental saltations as the means of getting 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 ｭｩ｣ｲｯｾ evo lutionary events? The r es olution on the part of those who formu lated and popularized the synthetic view--Mayr, Dobzhansky, Simpson, Stebbins--was to take population t:hinking a s right, true , and rrodern , and typological thinking as wrong, false and old-fashioned . A sympathe t i c treatment of evolutionary development was difficult in this envirornnent. Nevertheless, as of the 1947 Princeton symposium, the verdtcrwas not unanimous - -Dwight Davis (1949) made a strong case for typology and development in the study of comparative anatomy . In this paper, we take up where he left off. In our mega -eVolutionary appr oach , we make use of three concepts that David Hull (1980) proposes for micro-evolution. Hull notes that evolution has a component of "cont inui ty" , provided by the genes , and Epigen et ics & Evolution P ROCEEDI NGS, IesES-II a component of " int er act i on" , t he pheno type . One cannot be a rror e ba sic un it of s election t han the other , and bo th must be contained in "individua l s" --en tities of fixed durat i on and extension in t ime an d space. The contirnlity of rrega -evolut ion i s expressed in persistent s tructure s that recur in a l ineage - - cha ins of horrol ogous s tructure s (Ri ed l 1977) . Thes e homologues change over geo logica l time , in s tructure, posit i on , and function, j us t as genes change at a micro-evolutionary l evel . The chains of homologues are the outward manifestations of the interactive canponent , whi ch i s canposed of "devel opmen t al systems". Each system cons ists of one or more integrated , part ial l y selfr egulating deve l opmental pathways l eading t o t he s tructure we recognize as a link in t he chain of homologues . These systems interact with nei ghboring developmental sy stems , and with the external environment . All of them taken toge ther produce the ontogeny of t he organ ism . In view of t he self-regulating prope rties of t hese developmental systems, we ca ll them "epi genes " . Following Hull (1976), we suggest that the individual appropriate to our analysis is the spec ies. 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 rrore abs t ract, becaus e it i s a process, a ser ies of interactions . Perhaps it i s best t o consider it as a set of deve lopmental fields in time and space that are jointly responsible f or sene useful part of an or ganism . The part appears gene r ation after gener a t i on , species after spec ies , thus produc ing a cha in of horrol ogue s . Over t ime , the r equirement fo r concer ted action constitutes s e l ec t i ve pressure that knit s the f ields t ogether . The temptations for reification and metaphor when we consider , s ay , s el ecti ve pres sures on an epigenetic l and s ca pe, are overwhelming . We often yield t o them in this paper , for wi thout such devices camunication on t his sub ject i 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 of s tages . I t is a process- -an int erac tion between the expression of genet i c infor mat ion and environment. The internal en vironment--what has previously developed- is as important a s the external envir onment. The s impl ist i c ques tion that is inrnediately raised abou t any difference between individuals in a population- -is t he diff er en ce genetic or rrer e ly environ mental? - -is a mis l ea ding di chotany because 18 3 any t hing that has deve l oped ha s as part of i t s gene s is an environmental component. As Wadd ington ' s (1959 ) VJOrk ha s shown, an envir onmentally induced change i s a developmental r e sul t with a r elatively weak gene tic component . That component can be s trengthened by selection , so that l e s s environmenta 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 s to a considerable degree self-organizing . We do not have genes for individual ridges compris ing our fingerpr ints ; nor do we have gen es that inform ea ch neuron in our br ain wher e i t wi ll s ynapse and wher e its dendrites will gxos , We do have an inher ited program for making certain patterns of neuronal connect ions, but there i s con s iderable r oan fo r variation. This envel ope of ac ceptable variation , within which differences do no t compranis e the operation of t he organ i sm, is bes t appreciated fran the typological point of view. The typological approach has played a maj or role in continental European VJOrk in evo l ut i onary morpho logy . It has not been mich in evidence in the United States or Britain , where variability is generally viewed s tat istical ly , as an expr e ssion of popul a tion processes ; Bates on be ing t he notable exception to this t endency . Seil ac her (1970) has set forth a valuable modern vers ion of this app roach- - a balancing of phyl ogen e 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 l process that yields a variable structure - - say , our fingerpr ints - -one examines developmental error s and their subsequen t accamndat i on , the r ang e of variability , ontogen etic changes, patterns of repa ir and regeneration , and especially aclapti ve ly neu tral by -products of morphogene s i s . Thes e neu t r a l bu t annipresent by-p roduc t s are traces of developmental processes . Sei l acher (19 73) has named them fabricationa l no ise. The amount of f abrica t i ona l nois e in a structure shows the degree of freedan that ex isted in its production . Thus , it i s a measure of the amount of self-organization in the underlying epigenet i c system. Seilac her 's appr oach ha s a general utilit y- -Hut ch inson (1978) has extended it t o an explanation of differences in human intelligence- -and a sp ecial va l ue to paleontology . With it, paleontol ogis t s can us e the pa t t erns preserved in fossils as windoes on the epigenetic processes that shape thos e patterns, and on t he intrinsic evo l ution of such processes . 184 EVOLUT IO N TODAY Fabricat ional no ise i s a s ource of innocuous variability. A pot en t ially threatening source of variability is error in devel.opnental, pr ocess es . Yet , gi ven the canp lexity of devel.oprent , mis takes are inevitable, what ever the degree of genet i c specifica t i on . Certain sorts of mistakes may occur because of f ea tures of the ex ternal envi.rorrrent , others may r esult fran intrins ic susceptibilities to error. In either case , there i s a predi sposition fo r certain kinds of mistakes to recur. When t his ha ppens , there is a select ive pressure e ither 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 alternative pathways that lead t o the normal developmental end. These alternat ive pathways are , we expect , in large part created out of those wrong turns that a devaloprental, sys t em is peculiarl y l ikely to make- -the problem becanes part of the so l u t ion . The se r espons es to the inevitabilit y of error are what Wadd ington (1942) called canalizati on . Canalized pathway s evo lve so that in a variety of external and internal envirorrnents the deval.oprental, sys tem reaches its normal goa l . We expect that alternative pathways to the same devel.oprental, end are the rule in devel.oprental, systems . Selection will, we believe, produce and maintain many alterna t ive devaloprental, routes in the genane , and the success of such canalization may well be constant phenotypic expression in the structure that is produced . This suggests a paradoxica l invers i on of camonly held ideas about the na ture of variability. Wher e we see pheno typic con s t ancy , we may be dealing with underlying developrental, and genetic variability. Where we see phenotypic variability , for example, in fingerprints, we may be l ooking at the results of a single gene t i ca l l y invariant epigenetic process with a large canponent of self-organization . In sane cases, such an epigene t i c process may be locked into a fabr i ca t i ona l mechanism that cannot be further specified genetically . The large range of variability we see in such cases is an extension of the interac t i ve rather than the r eplica t i ve side of or ganisms , and as such is not :innEdiately like l y to be t he source of fu ture evo lut ionary change. Unles s Fishe r 's Funda mental Theorem i s f ramed in a wider, de ve l.opnental. context, it is perhaps not so fundamental . Still, despite canalization within epi gene s , mistakes will occur. Even a t the level of int er act i ons between epigenes, accoom:xlat i ons will still be made. Given t he inevitable mistakes - -a heart t oo small , Ra cho otin & Thoms on or too large , or too far t o the side to play i t s small r ole in the conditioning of the 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 ac coom:xlation- -behavioral , devel.oprental , physiological- -is the r esult of the mul t itude of int er-connect ed alternat ives wi thin and be tween systems . Occasi onal l y , gross errors oc cur and are still accoom:xlated . The congenitally bipedal 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 hind l egs alone , but , as it l earned to walk bi pedal l y , i t developed an S-shaped spine, modified muscle insertions, and developed such correlates of bipedal Locormt i on as a relatively broad neck and an oval rather than a V-shaped thor acic cross -section. No one would maintain that goats have genes for devel oping an S-shaped sp ine , "j ust in ca se". What we see he r e i s a ba sic rnanrnalian potential, emerging fran t he self-ri ghting pr operti es of the skel eto-muscu lar sy stems of a l l rnanrnals, and the sor t exploited by our haninid ancestors . A similar range of pot en t ial s , this time for the sku l l , is suggested by DuBrul and Laskin 's (1961) production of several primate- like features a s the result of a s imp'Ie nutilation of a synchondrosis in a newborn r at . A spec trum of self-organizing developmental properties exists , fran alternative biochemical pathways, to the bound ed 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 that occ ur in the inter action of ep igenes , to the behavioral and phys iological adjustments of the whole organism to deve lopmental calamities . The po t en t ial to make thes e accoom:xlations i s a canpon en t of the conservative force of stabilizing se lec t i on. Such selec tion is omnipresent, but its expr ession is nearly invisible . , INI'RINSIC EVOUJrION The epigene t i c lands ca pes that are built up for perfectly normal developrrental, r ea- sons are , fortuitously , a reserve of coo r dinated, cohesive change . I f a mistake oc curs- -not sanething as gross as a bipedal goa t , but perhaps as great as t he di vided maxillae of the bolyerine snakes des cribed by Frazzetta (1970) - -it may be accommodated . We do not know whet he r t he ini t i a l effect was a response t o an internal or an external perturbation , but the snake YXlrked, and it marked the beginning of a new, now tragically extinguished, l inea ge . That such an ananaly could becane normal nust mean that after r epeated evocations , Epigenetics & Evolution PROCEEDINGS, t he response became genet i ca l ly ass imi lat ed. Genetic ass imi lat io n of an ac commodated deve l.opnen cal, change, if the change i s of imrediat e adaptive interes t , may be the sort of r are event that marks the entrance to a new adaptive zone . The interest of dcvel.oprent; to comparative anatrmists and pa leontologists i s built on t his possi bi l ity. But an accommodated developmental error that i s neutral or even s l ightly maladapt ive with r espect t o th e ext ernal envir onment may still be genet i ca l ly as similated i f environmental influences persist in producing the error . That i s , given both intrins ic and extrinsic selective pressures . on occasion se- lection on the internal environment can have primacy over the demands of the external environment. This may be a camon event in evolution at and below the spe cies level. ICSEB -II 185 Develorxnental change is cohesive, selfintegra ting and fast. It need not be adap t ive in the sense of fit ting sore as pect of t he external environment, th ough it may be. Adaptation may sexretimes be intrins i c ; that is, i t serves to further the coordinated expression of a change that exists mainly because that change is easily produced . Such sorts of changes are we l L known, generally under the heading "a l.Loret.ry". What happens ontogenetically constrains and faci litates What happens phylogenetically . Allexretry i s r elated in turn t o t he pat t erns and processes of heter ochrony , which were so ably refurbished by Gould (1977). And heterochrony i s, simply, a special case of epigenetic evolution: those changes that are feasible in the interactions between epigenes . Changes in the structure, position, function, relative size, or time of appearance of parts of organs are called forth from the usua lly cryptic variation in the paths of their development. Consider a spec ies whi ch responds de- = va l.oprnenta ILy to an environmenta l gradient by producing phenotypes , A and B. Even if in all environments B is competitively inferior to A, if sore environment exists such that the threshold for production of the B phenotype is crossed , then there will be selective pressure to produce the best, most harrroni.ous B possible. This i s not the only outcexre ; we may also have selection to raise the threshold of pr oduction of the B phenotype , perhaps in the B environment itself if the environment is wavering on the edge of the threshold. What is important is that, granting a recurrent environmental influence, "e can have assimilation for intrinsic reasons. A possible example of this is the marked trend to size reduction that occurred in medieval cattle in Denmark (Degerb¢l 1963) . One hypothes i s to account for t his change is that it is the result of keeping the cattle in captivity over the winter, rather than allowing them to range freely . This was the season that the calves were being carried , and the inadequate fodder that the cows received produced small offspring . The size change was not itself adaptive, but while the environment called it forth, it became a selective pressure for smaller cattle in subsequent ｧｾＱ･ｲ｡ ﾭ tions . Once started, the trend could not abruptly be reversed . Even wi.th improved nutrition, a large calf is no service to the genes of too small a cow. A similar story , involving accommodation to an internal deve lopnental environment rather than adaptation to external conditions, may ac count for the consistent evolution of dwarfism in large island marrmals (Sondaar 1977). In all of this we fo llow a track not often taken fran that great marsha lling yard of evolutionary thought, Mayr's An ima l Spe ci es and Ev o lut i on ｾ ｹ ｲ 1963). A breakthrough in that book is the balancing of external factors in speciation, especially geography, which he had so thoroughly established in Syst ema ti cs and the Or i gi n of S peci es (Mayr 1942), with ll1ternal factors- -the co-adapted gene complexes , epigenotypes, and especially the genetic revolution at speciation. These terms are sexretimes taken as labels for our collective ignorance about species. This we think is an unfair assessment . In the genet i c revolution, ｾ ｹｲ united the typological properties of the wild type, which show up in the good soloist phase, with the populational properties of balancing selection, which characterize the good mixer phase. Thus he harnessed the theo retical M:>rk horses of the 1950s population genetics to the task of explaining the emergent properties of species. In so doing he produced a species concept that canbined the advantages of an intrinsic approach, which could be applied to the breakdown of developmental pathways in hybrids, wi.th the advantages of an extrinsic approach, which made sense of the geographic and ecological aspects of species . This theoret ical approach to species is far more powerful than one that is merely operationally convenient, say, a cut-off point 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 of evolution is called for today. Although it has been ,vith us since the biological 186 EVOLUTION TODAY spec ies concept, t his s i de of the concept has been pl ayed down in f avor of such ex trins ic ques t ions a s al l opa try vs . sympa t ry , t he real ity of subs pecie s, l ocal ad aptati on , charact er displacement , an d antihybridization mechani sms . It i s time for a chang e in perspecti ve , the sort that cou l d be provided by un coupl ing as mic h as possi ble the ex trinsic and intrins i c as 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 evo l utionary potentials of organi sms that are usually concealed by rrore obvious extrinsic f ac t ors. I n the 1950s and 1960s evo l utionists sought a singl e t heory t hat could account fo r a ll the phe norena of evol ution . Thi s has probably been pushed a s f ar as it wi ll go . If we are t o go beyond i t, we mis t; partially disassemble t he synthesis and experiment wi th t he potential s of i t s components . Rachootin & Thoms on f ossi l r ecord, and that many species show no change a t a ll between or iginati on and extinct i on, and Gingerich 's (e .g ., 1977) argumen t for uru.-dfrectdona l, changes in rrorphology . The rror e we know about the Lower Cambrian diversifi cation of inverte brates , and the Cretace ous r ad iation of ang iosperms , the fas ter and rrore staccato they s eem to be . Direc tionality , saltat ory leaps t ha t land on their feet and stay sti ll unt i.L they l eap aga in, adaptive types - -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 series of accidental varia tions , each of which was thrown for , a s it were, with dice ? We sha ll rrost; of us feel that there mis t; have been a l i t tle cheating sanewhere . . . " Chi e f among thes e i s t he l a t en t evo l utionary potent ial of developmental systems . Most current considerations of epigenet ics r e strict the importance of epigeneti c mechanisms to t he reason for which they evo lve. 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 i ve developmental means. But the normati ve flIDctions of epigene t ic sy s t ems do not ex ha us t their pot en t ial when i t canes to t r ans - spec ifi c evo l ut i on . How do epigen eti c systems cane together and how do they cane ap art? A look at the fos sil r ecord gives , we think , sane hints concerning this problem . Epigene sis can provide the directionality, the typology , t he saltati on, in shor t , the che ating that has in the past aroused in the breasts of our predecessors pa s sions for neo-Lamarckianism , aristogenesi s , pangenesis, bathmism, hopeful nonsters , and a hos t of entelechies . They saw sanething that gene rati on a f ter gene rat i on of evolut i onists have been t aught not t o see - -an integrative and emergent s ide to evolution . Epi genetics can bring to this phenanenon a s trai ght - f orward, non-mys t i cal exp lanat ion . However , i t is an appr oach on which i t i s r ather difficult to experiment . What we are abou t t o out l ine may not ca ll t o mind 101 f alsifi able hypothe ses . This doe s no t worry us . The s trai ght-forward probl ems of evol ut i onary biology have been a ttacked a l ready. The r es idue that r e mains wi ll not give up its s ecrets to blunt; methodological instnnnents . PALEONl'OlDGY AND EVOUITION MEGA-EVOLUTIONARY CHANGE I t has cons ist en t ly been the pal eont ologists who have the hardest time in r e conciling syn thet i c theory wi th t he ir stock in t rade of evo l ut ionary data . The existence 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 intermediate s ; the integri ty (in terms of rrorpho logy and r ates of evo l ution) of what Simpson (1944) or i ginally ca lled adapt ive types ; and such throwbacks to Geoffroy-S t . -Hilaire a s Williston ' s Law-- thes e have a l ways nagged at the synthet i c heart s of evo l ut ioni s ts. Ther e i s no denying t ha t thes e are problems to be solved ; indeed, r ec en t pa l eon t ologi cal work has l ed u s t o take t hem rrore serious ly. As exampl es, we ha ve Van Val en' s lawful r a t es of extinction fo r hi gh er taxa (Van Valen 1973) , the argumen ts of Eldredge an d Goul d (1972), and St an ley (1975) t ha t we do no t see spec iat i on in t he The rare produc tion of a new adapt ive t ype is not predicted fran l ower l evels of anal ysis such a s population gene t i cs; such events are emergent . But, if we might adop t Needham' s (1933) metaphor that evo lution r equires a changing of gears , a going t hrough neutral, then we woul d argue that our black t r ansmiss i on box is development. And epigene s is ens ures that our transmis s ion i s at l eas t semi - autcxnatic . Though t he "point " of canal i za t ion i s to en sure t hat an expected resul t i s obt ained , sti l l an lIDexpect ed r esul t autcxnatically pull s rel ated devel opment al sys t ems along wi th it. Let US suppose t ha t a developmental mistake , and such behavioral, structural , or phys iologi cal accommodati on as t he mist ake engend ers , a llows an organism t o en t er a new adaptive zone . Then all t hat is needed for i t t o pers i s t there , i s f or the l ower ing of t he developmental thres hol d that gene ral ly prevents that mistake . Epigenetics & Evol ution PROCEEDINGS , IesES-II For assimilation to occur , t here must be an environment which frequently evokes the altered phenotype. 'That envi.rorrrent; has always been assumed to be ext ernal. The epigenetic effects of external change could be transmitted to and intensified by the internal envi.rorment , which could then be the prime rrover behind assimilation . EnvirorJrrentally affected t hres hol ds are known; Van Valen (1974), f or instance, has document ed an increase in (admit t edl y hopeless) five-legged frogs in particul arl y cold l ake s . But if such changes were us eful, t hey could be assimi lated into t he genorre , Waddington (1975) suggested that adap t i ve phenot ypi c differences be tween quiet and turbulent water r ace s of th e pond snai l Lymnaea stagnali s were genetica lly assimilated in j ust such a way. The class ic obj ection t o hopefu l rronsters - that a pig with wings has no chance of finding a s imil arly endowed mate - -misses t he point t hat if you have one pig with wings , there are rmre where that one carne f ran- - in th e deve loprterital pathways of the relatives of Archaeoptopig . When an adaptive change has occurred , it will at f irst have but a f l ickering and uncertain phenotypic express ion . Immedia t ely , t here will be intense se lecti on to pr ot ect and buffer the express ion of this changed state . Secondary patheays will evolve that canalize the system. It will be fur t her stabi l ized by t ies to other develop:nental sys tems t hat are temporally, structural ly , and funct ionally related to it. This kerfuffle of evolutionary activity i s only a rrore intense express ion of the cons t ant but cryptic se lection that maintains and strengthens the developrenra l status quo. In the end, a successful evolutionary step will exhibit a hard, gem-l ike constancy in the express io n of the new feature . The adapti ve novelty will have been pro t ected by a canalized epigene , as sembl ed out of the predispositions to error in the early, unstabi l ized stage . The new adapt i ve feature may lead the organism to new behaviors and into new envi rornnents ; these envir ornnents can then i nt er act wi th th e underlying epigene to produce further changes. The rrodi.f i.ed epigene many a l so be affected greatly in its phenotypic expression by minor changes in the wel l cana lized deve lop!lffltal systems with which i t interac t s. Both intrinsic and extrinsic fa ctors thus may lead to further changes , because t he recently altered ep igene is relatively l ess buffered by secondary pathways or deep devel op!lfflt al channel s than its older, rrore cons istent neighbors. Continuing changes, if adaptive and genet ical ly as similated, lead to 187 rmre and rrore changes on a single l arge adapt i ve thane . This is an adaptive r adi ation. Not only might such a r adiation be r apid ; we would expect it t o be so. Wer e i t not it would be overtaken by the cons t ant pressure of stabilizing se lect i on that resu l ts in th e production of a mature and wel l canalized epigenet i c l andscape . The epigene need not vary in all direct i ons at once; perhaps certain sorts of vari at i ons are part i cul arly easy or adapti ve . If t he sarre sort of change occurs sequentially in a s ingle epigene, the cumulat 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 e seve r a l major evol ut i onary ques t ions. But epigene t ic systems are normally s table . Where do we turn to s tudy t he actual wor kings of evol ut i onary epigenetics ? An obvious area i s t he huge field of atavisms and t heir experimental ana logues. Horses born wit h t hree toes, flat f ishes with ｰｩｾｴ ･､ undersides , ｈ｡ｭｰｾＧ ｳ (1959) experimentally manipulat ed chick l eg that reverted to a r eptilian state- - these are striking signs of the sa ltato ry potential of development . Of such cas es, Gould (1980) writes: What el s e might the ir ge ne t ic s ys t e m maintain , normally unexpres s ed , but ab le t o se r ve, i f act i va t ed , as a po s s i b l e focus for majo r and rap id evo lu t io nary cha ng e? [ a nd] An o rga nism' s pa s t not o nl y constrains its fu tu r e ; it a l so p r ov i des as leg acy an enormous reservoir of potent ial fo r rapid morphologica l c hange ba sed up o n s ma l l ge ne t i c a l te rat i o n . \-Ie agr ee totally with the spirit , but the letter is slightly t roub ling . Atavisms undoubt edly give us insight into epigenetic processes, but t hey only mislead when taken as examples of the patterns of epigenetic evolut io n . We l abel a variant as an atavism because i t viol ates some defining quality and derived character state of the group in question-horses are expected t o have single hooves and flatfishe s are expect ed t o have right and left s ides unl ike . Such qual ities, in par t , determine t he or ganism 's adapt i ve potentials as wel l , so that unles s they have only recentl y evolved their devel opment ought to be heavil y cana l ized. While vari ant s on an adapti ve thane have evolutionary potential , th e undoing of an adaptive t heme does not. EVOLUTION TODI\Y 188 The major f eatures of evol ut ion are not conposed of s tructures withdrawn f r an a developmental legacy ; t hey are cCXllpose d of processes that shape themselves as they go a lo ng . Epigenes ret ain ances t ral potent ials becaus e, to us e Riedl's (1977) t erm, they ar e ' 'burdened'' with other epigenetic systems that use t he i r products as developmenta l cues. But these ancestral potent i als have little chance of expres sion in t hemselves , becaus e their ance stral phenotypic expr ess ion i s i rrel evant to the se lective pr essures favoring t he ir r etent ion . The legacy exists , but t he assets ar e not converti ble . It i s becaus e of the burdens t ha t epigenes bear that they have evolved t he capa city to accorrm:xlate eac h other. And it is t he capacity for accon modati.on that give s epigenetic systems their mega- evolutionary s i gnif icance, be cause i t fac i litates adaptive experimentation . A genuinely l abi l e epigenetic system ought t o be of the greates t in t er est to an evolutionist, and i t i s a far, far better t hing than an occas i ona l atavistic slip in a mature epi gene t i c system . This i s not t o say that reversion has no part t o play in evolutio n , just that t he par t is small . After a ll , all God 's hoatzins got rmre than wings . ADAPrATIOO While an epigenetic approach cannot tell us what will make a new adaptation, it does suggest sanething about the sources of adaptive novelty and the ease with which an adapt i ve change i s initially ac corrm:xlat ed . As Gould (1977) notes, many pew adaptatio ns wi l l be t he r esul t of re arrangemen t s of developmental information already at hand. Playing the f eatures on one age or stage or size or shap e against t hose of another i s , we do not doubt, the 'pr imary material basis of evolutio nary change . Gould argues convincingly for an extrinsic, ecol ogi ca l explanation of these r eshufflings. He ｾｵ ｬ､ add that intrinsic factors may a lso be a t ｾｲｫ Ｎ In cases where a functional intermediat e i s imposs ible, for instance in t he maxilla of bolyerine snakes , which is ei ther in one piece or a developmental explanation may be the only alternative . Simi l arly , a l ong- standing pro blem in the evolutio n of the hind limb of r ept i l es is the explanation of the transf er of the calcaneum fran the foot (in crocodilians and pseudosuchians) t o t he leg (in dinosaurs) , fran one functi onal unit to another . Paleonto log is ts have been hard pr es s ed to discover a funct ional int ermedi at e stage; a gradual sequence is poss ible only by invoking hypothetical small, l i ght rep- =, Rachoo tin & Thom son t i les with reduced ca l canea and other hopel es s lTOns t ers. A deve lopmenta l sequence i s lTOre l i kely : a s imple r ate change in de velopmental f iel ds caused the ca lcaneum to be included in a diff erent struc tural unit 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 calcaneum changed the internal envi r onment of the fields invo lved in l eg development . The initial accorrm:xlat i on was the development al response upon which se lection ｾｲｫ･､Ｌ eventual ly prod ucing its genetic ass imi lat ion . The r esult becane s an adaptat io n in the sense of proving adapt ive, but not in the sense of having been sel ect ed fo r . The change in the pos ition of the tarsal joint immediately gave a new range of adapti ve pos sibili ties . The new pat tern and the new epi gene may be the origin of fur ther intrinsically produced ananalies , sane of which may prove adap tive and form an adaptive radiation . Even those adaptation s which do not arise fran r earrangements of an organism ' s development al pathways filqy somet imes be produced by admixture with for eign developmental pathways . Given t he free-floating abi l i ty of devel opment al systems to accorrm:xlate to insult, it ought co be possible f or introgression t o be the basis of an epigenet i c revolution. The phenanena of hybridism are pre -eminently t he phenomena of development al in cCXllpa t ibil i t y . But there is no reason to deny t he possibility that a mixture of r elated but distinct developmental pathways might pr oduce adaptively in t eres ting novelties, \'hich on occasion are assimilated . Developmental shake -ups need not be re s t r ict ed t o interactions with congeners . The products of symbionts can shape development of a host so consistently that the symbionts becane part of its intrins ic evolution . lhus, in sea lettuce ( VI va) th e characteristic foliose thallus has been shawn t o be induced by bacterial symbionts. In axenic culture the a lga grows as 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 Ente romo rpha (Provasoli & Pintner 1980). As for the tempo of adaptive change , the epigene t ic approach suggests that on t he scale of evolving l ineages , an " imnature" epigene may facil itate a succession of r elated changes. At the f iner sc ale of the success io n of ind i vidual species, we suggest 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 Epigen eti c s & Evolut i on PROCEEDI NGS , I CSEB- II un changing 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 descen dant s pecies . Organisms are subject t o cons tant evolution, sane extrins ic , whi ch produces local adaptation , subspecies, and cl ines, an d sane intrinsic , which produces canalized ep igenetic pathways and a llows fo r t he production of new species, or at least a class of species with a special rrode of origination, and special potential for future evo l ution . ClASSIFI CATIOO Evol u tionary epigenet ics may offer a resol ution to t he current quandary of systematics . To date, the chief contri bution of cladistics to the data of evolution has been the uncovering of far nore parallelism (horopl.asy) than anyone could have imag ined. Only cladistic analysis could have made this discovery . If it holds up , the ph i l osophical assumptions of a l l schoo ls of class ification, including clad istics, will turn out to be false. I f parallelism is the rule , then why should we i den t ify parsinony as the absence of parallelism? Corrmmly held pr imi.t i ve de veloprrentaJ. pathway s, each of which have predispositions that are expressed independent of descent, that is, paraphyletically, may well 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 s er i es of developrrental stages will not in itself be sufficient: it i s the envel ope of epigenetic accamodations within which reside the ontogenies of s is t er groups that is no st important. Pa leontologists wou l d seem to be l ef t out in t he co l d by t his program, but s uch is not the ca s e. They can analyze fabri cational no ise , which i s an appropriate introduc tion to the epigenetic envelope around the production of fossilizable structures , and they can trace the evolut ion of such envelopes through time. SPECIATION PATIERNS Obviously , bithor ax frui t flie s, whatever t he complexity of the i r altered norphology, are not per se s pe c ies in the sense of the reproductive isolation that is at the heart of t he b iolog ical species concept . One may grant us our saltations , and t hen deny them any s ignificance un less we fashion appropriate anti -hybridization mechanisms that would make them " good" species . 1 B9 To this we answer that r eproduc tiv e i sol a tion has a l l t he proper ties of a de veloprrental s ystem, one that has as i t s goa l the pr edic t able r eproduction of the s pecies . As such, i t r equ ires an especia lly large set of cues fran the external environment. The environment is involved not just during early developrrent , but through adult life. Not only mist structure, physiology, and behavior of the organism be coordinated , bu t all I1USt be co ordinated with the structure, phys iology , and behavior of other individuals of the sp ecies. The demand fo r t he equ ivalent of canalizat i on and sel f- regulation i s all the stronger here, g iven the mich l arger environmental canponent. The argunent can be made that mate recognition systems are intrinsic to all organisms (Paterson 1978, 1980) , and that these intrins ic systems are in many or gani sms more important in reproduction than such extrinsic factors as anti- hyb ridization mechanisms . It may be easier to learn to mate wi th like than to learn not to mate wi t h un l ike . I f we view the mate r ecogn i t i on system as a kind of epigenetic system with a particularly large environmental canponent, then all that we have said about intrinsically controlled saltatory change will hold, except that there is in this case less reason to require an adaptive change to result fran the s altation. Any change in t he mate recognition system will "work" as l ong as i t succeeds in s elec t ing l 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 doing nothing different fran its parent specie s , it may well disappear for no other reason than its comparative rarity . Thus, speciation may be a case of easy cane , easy go . The cryptic or sibling species that sanetimes turn up when a group is c losely studied may be cases of such easily produc ed , s l ightly differenti a ted , adaptively equivalent s pecies . Perhaps they r epr es ent the few survivors of a vastly greater number of ephemeral spec ies that population biologists would never find unless they had sane good reason to look for them. Fran our perspective, a lineage with a truly pranising evo lut ionary future woul d be favored wi t h bo th a sanewhat l ab ile mate recognit i on sys tem, and a sanewhat labil e ep igenetic system for a trait that i s of adaptive interest . Both will be sufficiently canalized to appear as con s istent, dependable characters within species, but ne ither wi ll be so burdened with other developrrental responsibilities that they cannot change to produce new species. Perhaps this sounds like a lot to ask fo r . Rac llo o ti n & Thomson EVOLUT ION TODAY We think not . I f , as the foss i l r ecor d sugges ts, spec ies are general ly unchangi ng once they are formed , then t hose lineages which diversify and prosper will be those that can eas i l y speciate and in so doing capture intr ins i cally gener a t ed adaptations . In effect , we have spec ies se lection for modes of mate r ecognition that pr omote speciation. Species se lection need not be t he t ot ally pos t hoc accumulation of l ineages that happen to have survived . I t i s in our scheme an ac tive, intrins ic factor, a mechanism that over geol ogi cal time produces l ot s of speci es in a lineage . Adaptively indif f erent , ephemeral spec ies are produc ed in l ar ge number s as wel l - - t hese are a kind of spec ific l oad . Our ideas in th i s area are an extens:'on of Carson 's (1975) theory of the open and closed gene t i c systems. Certain lineages can adapt only by speciat ing- - t hat i s , shaking up their closed genetic sys tems . Others can adapt without speciati on- -they have relatively l ar ge open sys tems. In l ineages of the first sort , we sugges t that mechanisms that predispose the organi sms t o undergo frequent speciations will be se l ected . Mos t fac t ors that have been implicated as 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 f actors include suscepti bili ty t o chr omosana l changes- -in ploidy level, chromosome number , organizat ion of sex chromosomes (for instance in bovids, se e Todd 1975), inver sions and t ranslocations , and many permutations (see review by White 1973) . The frequency of such changes depends on the effi cacy of mechanisms fo r chromosanal r epair- - a kind of canalization lit t he cellular level. The s light est decrease in t he ef ficac y of such r epair mechanisms could greatly increase t he chance of speciat i on without being an appreciable burden on the dependabilit y of meiosis. The shuffling of immunologic recognition systems in the gametes of plants and free spawning animals and the co-evo l ut ion of eukaryo t es wit h r apidly evolving pathogens or 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, and thus become a mechanism for spec ies production . In r are instances , a mechani sm for speciating and a suitably plastic , adaptively int eresting epigenet ic system will co-oc cur in an organi sm whose environment i s sufficiently complex in space and time to pr ovide al l that could be asked for in t he way of extrins ic factors favo rable to spe - ciati on . Such a case i s provided by th e cichl i ds of t he rift l ake s of Afr ica. Three intrinsic factors contribute to the ease with which cichl ids gener a t e new spec ies. Their complex and pl astic behavio r provides plenty of material t hat can be shuffled t o make mate recogniti on sys t ems. The fish are int ensely visua lly or 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. And t he f i sh are col orful , they exhibit color polymorphism , and th ey depend on color cues for mate recognition . On t he apparently adaptive s i de, ci chl i d spec i es show a tremendous divers ity of j aw and tooth morphologies . Liem (e .g . , 1973) a t t r i but es their success t o a new arrangement of the pharyng eal j aw . The array of f orms , Liem writes, calls for "minor r econs t ruct i on of the 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 As t a t oreochro mis all ua u ndi was reported by Greenwood (1965) t o produce bicus pid teeth when r aised on insec t s but mol ariform t eeth when r aised on molluscs . These intrins i c f ac tors , played against a success ion of "ak es in t hese ancient basins, coul d produce the hundr eds of endemic speci es , pro bably during the geol ogi ca l ly shor t l ives of the current lakes . For while the bas ins are ancient, the lakes th emselves, like th e Triass i c r ift lakes of North Amer ica, fi ll with water and dry up in r esponse to climatic cycles on th e order of 20,000 years (Li vingstone 1975; Olsen et al. 1978). Note that our epi genet ic appro ach t o spec iation does not insis t that th e mechanisms we postulat e apply t o a ll speciation event s , or even t o al l lineages . But if th ey apply t o some l ineages , and some speciat i on events in other lineages, t hen , over geological time , th ey can account for the existence of properties of the exi sting biota her et of or e inexplicable or uns een . CXlNCWSION We st art ed with orthodox notions of the function 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 t o current prob lems in pal eonto logy - - adapt i ve zones, functional anatomy , patterns of or iginat i on , change (or i t s absen ce) in f ossils with excellent s trat igraphic r ecor ds . We suggest : 1. Prope rties of epigenesis quite for - Epigenetics & Evol ution PROCEEDI NGS, IeSEB- I I tuitously make r apid , cohesive, and ftmctional change poss ible . Internal adaptation is as impor tant as external adaptation. 2. Nonnally constant features, i f they are not heavily burdened by ot her deve lop mental systems, may be the source of new evol ut ionary directions because of th eir underlying deve lopmental variabil ity. Vari able features may not be , because their variation may be fab r 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 not change phenotypicall y dur ing its life , i t is cons t ant ly ac cumulat ing s i gni f icant developmental variabili ty, which allows (but does not r equire) r api d , even sa ltatory change i f i t spec iates . 4 . Mate r ecognition systems are also ep igenet ic sys tems- -what i sn ' t, after al l? Ma te recognition sy stems are nonnal l y wel l cana lized ; abnonnally t he ir r earrangement produces new species , without the constraint of pr oducing adapt ive changes . A new spec ies so pr oduced may for tui tous ly capture a new adaptation ; such spec ies are mor e likely to survive. 5. Once a devel opment al change has occurred , t he same epigenetic system, if not wel l buffered f rom deve lopmental errors, may make related successful mistakes . This produces what we r ecogni ze as t r ends, adap t ive zones and adaptive radiati ons . Though per haps very rare at anyone t ime, over the whole hist ory of l i fe, th e r esults would prof oundly shape the entire biota . 6. Spec i es se l ection i s an intrinsic and active proc ess - - given punctuated equil i br i um, those species that easily spec iate will capture rmre adaptati ons and be rmre likel y t o pers i s t and l eave descendant spe cies . Theref or e, mechanisms of speciation may be cons idered to be adapt at i ons at the l evel of l ineage. When plastici ty in a developmental sys tem and the mate r ecognit ion system co-occur , species swarms result. 191 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 utionary trends 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 ed character ist i cs, selection for the abi l ity t o speciate, t he ubi quity of paral l elism- t hese are not i deas that figur e prominen tly in t exts , and sane of them have been gr ounds, in the r ecen t past , f or excommunicatio n from the scientific communi t y. We are by no means say ing that such ideas 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 ution is pr e- eminent ly a science of contingent truths - - t ha t i s , demonstrating th e exis tence of allopatric spec iation by no s tret ch of the imagination implies th e non-exis t ence of sympat r i c spec iat ion . So too, with th e i gnor ed i f not pr oscribed evolut ionary ideas that have been se r ious ly se t f orth by such notable workers as Bateson , Gol dsc hmidt , Waddington , and many continental workers. The synthetic t heory i s sufficient ly mature to be ready to harmonize with many of its apparent oppos i tes. The r esu l t ing pluralis tic approach to na ture suggests innumerable new problems and holds out sane hope of answers t o old problems we have alrrosr fo rgott 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 ect are perhaps no rmre wrong than the al t er natives that are th e usua l bas i s of our day t o day wor k. If you will sus pend disbel ief, t his can be an invigorating and exciting prospect . 8 . A t horough-going r evision and r eintegratio n of the synt hetic th eory is pos s ible on these gr ounds . We as k, ftmdamentally , that you balance the reductionistic , generally extrinaic appr oach to evol ution, which as sumes that al l evolution i s t he warfare of self i sh genes wri t l arge , wit h an intrinsic s ide of evolution most easil y perceived from the 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 hew l ook at t he nature of spec ies . We as k you t 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 might be ca lled "selfles s epigenes" . Although this paper is a na tural extens ion of accepted ar t icles of the synthe tic theory appl ied to the data of paleontology and morphology, t he cumulati ve effect i s an Richard Gol dschmidt 's (1940) Mat eri al of Evoluti on made the case for deve lopment, saltation, and the uncoupling of micro- evolution and macr o- evol ution . 7. Horrologous structures, pr oduced by evolving 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 dur ation- -speci es. Basi s Ra chootin & Thomson EVOLUTION T ODAY 19 2 Writ ing of t he cr i t ical r eception of t ha t book in his aut obio graphy (Gol dschmidt 1960) , he sa id : Th i s t i me I wa s not o n l y c ra z y , but a l most a c r i mi na l . . . [ b u t ) I a m c o nf i de nt that in twen t y yea rs my bo ok , whic h i s now ignored , wil l be g i ve n an hono r abl e p l a ce i n the hi s t o ry o f e vo lu t i onary tho ug h t. We stand in his house , twenty years after t hose words wer e published , and f ind a pro phet not without honor . ACKNCMLEDGEMENTS For discus s i ons and criticisms of this mamiscr ip t , we are indebted to Catherine Badgley , Anthony Bledsoe , Paul Olsen , We r eceived the advantages of t he spec ial expertise of Richard Harrison (population biology) , Robert Nakarrura (botany and Scr ip ture) , and Scott Poethig (developmental biology ). Our special t hanks go to Arrr:! McCune and Louise Roth, who not onl y provided exhaus tive criticisms a t every stage, but also contributed or inspired several important concept s. t i on in t he mammalian f os s il r ecord , pp. 469- 500 . In : A. Hall am (ed. ) , Patterns of evol ut i on as i llustrated in the foss i l r ecord . Elsevier, Amst erdam. GCLDSCHMIDT , R. 1940. The material bas i s of evol ut i on . Yal e Univers i t y Pres s , New Haven, Connecticut. 436 pp. 1960. In and out of th e ivory tower . 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