EPIGENETICS , PALEONTOLOGY, ANDEVOLUTI ON

S tan P . Ra cho o t i n and Kei t h S t e war t Thoms on Pe abo dy Museum of Na tura l Hi s t ory , Yale University , New Hav en , Connecticut 0 6511 , U. S .A .

ABSTRACT

'Three requirements of evolution are persistence with chang e, internally cohes ive individua l s of limit ed dura t ion, and interaction with environment. We recast th es e proper t i es in megaevolutionary terms. Harologous structures persist over geological t ime as they evo lve in form and funct ion. Spec ies, which arise through a greater or lesser genetic r evolution, behave as individuals. The interact ion of genes and envi­ ronments- -development- -under lies both the origin of species and the continuity of haro­ logies. The properties of epigenetics- -self assemb ly, feedback, alternative pathways to the sane devel opmental end, canpensati on for the inevitable irregularities of devel­ opment--allow a redefinition of genet ic revolution in terms of the establishment of new, stable developmental patterns : a typological r esult produced in ac ceptably popu­ l ati ona l ways . Harologues, s imi larly, are the products of evo lving epigenetic sub-sys­ tems. Al though developmental systems retain ancestral potentials that renain unex ­ pressed for tens of millions of years, such potentials are so burdened with other devel­ opmental pathways built upon them that they hold little promise for evolutionary change. But where a recent developmental change has occurred, no such "buf fering" exists . As errors occur, sane will be ep igenetically acconm:>dated and , if adaptive, genet i cally assimilated. These are the quanta of evolution. If a r ecent adaptive breakthrough has occurred, 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 pre­ dictable expression of the new trait. Until this happens, further "exper iments" along the l ines of t he initial change can occur and be assimilated. Depend ing on eco logical milieu, t his i s the stuff of adaptive r adiation , evo l ut i onary trends, or allanetri c change. Speciation, which can occur without any adaptive change, is th e result of anal­ ogous changes in the epigenetic systems responsible for mate r ecognition . 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 epi­ genet ics fortuitousl y l ay down the lines of l ea st r esistance to evo l utionary change. We find ourselves l ooking a t an intrinsic and emergent s i de to evolution, a view that in the past was held, on similar gener al 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 bution i s seen as a na tural offshoot from the syn thet ic stock. But though the syn­ The title of our paper, "Epi genetics, thetic theory has provided many answers , Paleontology, and Evolution", i s de liber­ i t has not adequately framed a l l the ques­ ately chosen to r eca ll the title of the tions. llich renains to be explained, es­ conference that was held at Princeton Univ ­ pecially when we take the long paleontolo­ ersi ty in 1947 on "Genetics , Paleontology, gical per sp ective . The answers to these and Evol ut i on" (Jepsen et al . 1949). I t questions are, we think, t o be found in a included not only th e subjects of gene tics , considera t i on of the evolutionary implica­ speciation, and paleontology, but canpara­ t ions of development and the developmental tive anatany, ecology, and systematics as impl i cations of evo l ution, topics that were well. The synthetic theory that came of notably l acking in the 1947 conference . age with that symposium ha s been the nota­ ble success of organ isrnal biology of thi.s Our goa l in t his paper i s to set in a century. In a day when theories in o ther developmental con text the problems of mega­ parts of biology change wi th the seasons, evo lution: the nature of adaptation, the it i s astonishing to f ind that 33 years tempos and nodes of evol ution, the framing later the study of evolution is no l es s of us eful general izati ons about the origin vigorous for having r emained in the sane and diversification of major groups . As node . We =uld be pleased if our contri - we go about this , we find ourselves r ein-

G.G . E. Sc udd er & J . L. Rev e a l (eds .) I EVOLUTION TODAY, Proce edings of t he Second Inter ­ na tio na l Congress o f Systematic a nd Evoluti onary Bi olo g y, pp . 18 1- 19 3 . 19 81 . 182 EVOLUTION TODAY Rachootin & Thomson terpreting sane of the ftmdarnental con­ "Intrinsi c" and "extrinsi c" bear close cepts of evolut ion, including variation, relation to the distinction that Mayr has spec ies, and what i t i s that selection drawn between typological and population­ acts upon . These reinterpretations cane al thinking . Throughout the paper, we out of a series of generally accepted will be contrasting a populational, or , premises about development , which, how­ rrore generally, an extrinsic approach ever, have unexpected impl ications when with a complementary intrinsic approach viewed over the time scale familiar to the that is developmental and typological. paleontologist. Our paper is an outline Note that both approaches are ways of of a way of ret:hinking what everyone knows t:hinking, not hypotheses about nature. about evolution. We ask you to rearrange The mind has a hard time holding = com­ your mental furniture and consider sane pletely different views of the worId si­ changes that we think are suitable for mul taneously, but it is our guess that sane circurnstances .Al though the rear­ having two ways and switching when i t rangement is new, the pieces are not. seems appropriate i s better than having Those that look unfamiliar we have only one way that we always be lieve to be right, brought down from the attic. and another, which we seem to fall into, but which we have decided is always wrong. In the broadest terms. we ask what me­ ga -evolution ought to require of theories Development is studied in a typological at the level of genetics and development, m:xIe. Development shows directedness; in and also at the level of speciation. We an experimental manipulation, the embryo expect that nothing at the l evel of mega­ " tri es" , if you will, to develop normally, evolution contradicts what happens at according to type, in spite of the insult. these l ower levels, but that we will not Results in a devel opment al experiment turn fully understand these l ower l evel s un til on the behaviour of particular, crucial we actively search them for phenCID2I1a that embryos. This is a far cry from popula­ may seem peripheral to the population bio­ tion thinking. The dichotomy is apparent logist, but which are required to explain in the 1947 symposium, which neglected de­ the data of the paleontologist and the velopmental biology, but not because there roorphologist. We trace the emergent mega­ were no evolutionists interested in it. evolutionary phenanena down to their hid­ Indeed, embryology dominated evolutionary den roots, which we find to be developmen­ studies in the last century, and was the tal, and then ask what this mega-evolution­ guiding light to such twentieth century ary view of development suggests about the vorkers as William Bateson, Richard Gold ­ nature of species and speciation. schmidt, and C. H. Waddington. The prob­ lem was that the typological and the pop­ We also ask you to allow us to break one t l at i ona l could not be fused into a sin­ other convention of evolutionary theory, gle approach. How, for instance, could concerning intrinsic and extrinsic factors Goldschmidt's macro-evolution, which took in evolution. Extrinsic factors are the developmental saltations as the means of relations of an organism to the external getting from one major group to another, environnent- -adaptations to local condi­ be reconciled with the gradual, popula­ tions, the sorting-out of congeners in tional approach that was then being fash­ sympatry by character displacement, and ioned, an approach that accounted for me­ such chance effects as the genetic sample ga -evolution by an aCCl.IIllllation of micro~ borne by the traditional gravid female com­ evo lutionary events? The r esolution on pared to the population from which she de­ the part of those who formulated and pop­ rives, or the effect of a river changing ularized the synthetic view--Mayr, Dob­ its course and cutting off a population. zhansky, Simpson, Stebbins--was to take We accept such extrinsic factors as the population t:hinking as right, true, and carrron property of all m:xIem evolution­ rrodern, and typological thinking as wrong, ists. But although we all believe in such false and old-fashioned. A sympathet i c factors, they are remarkably difficult to treatment of evolutionary development was demonstrate in anyone case. We define difficult in this envirornnent. Neverthe­ intrinsic factors as the adaptation of the less, as of the 1947 Princeton symposium, genane to itself. Developmental mechan­ the verdtcrwas not unanimous- -Dwight Davis isms, especially epigenetics, the self­ (1949) made a strong case for typology and organizing and correcting properties of development in the study of comparative developmental pathways, are the means by anatomy. In this paper, we take up where which the intrinsic side of evolution i s he left off. manifested. Intrinsic factors will be just as difficult to demonstrate as ex­ In our mega -eVolutionary appr oach , we trinsic factors, all the roore so because make use of three concepts that David Hull biologists are not accustaned to t:hinking (1980) proposes for micro-evolution. Hull much about them. But there is no a priori notes that evolution has a component of reason why they rrust be mystical. "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 ­ any t hing that has devel oped has as part type . One cannot be a rrore basic unit of of i t s genes is an environmental component. selection t han the other , and both must As Wadd ington' s (1959 ) VJOrk has shown, an be contained in "individua l s" --entities envir onmentally induced change i s a devel­ of fixed durat i on and extension in t ime opmental r esul t with a r elatively weak and space. The contirnlity of rrega-evolu­ gene tic component . That component can be t ion i s expressed in persistent s truc­ s trengthened by selection, so that l ess tures that recur in a l ineage-- cha ins of environmental informat i on is needed to pro­ horrologous s tructures (Ri edl 1977) . These duce' t he effect. Thi s i s what he provo­ homologues change over geological time, cati ve ly but ap t l y termed "genet i c as simi­ in s tructure, posit i on , and function, j us t l at i on of an acquired character isti c" . as genes change at a micro-evolutionary l evel. The chains of homologues are the A second truism i s that devel opment i s outward manifestations of the interactive to a considerable degree self-organizing. canponent, which i s canposed of "devel op­ We do not have genes for individual ridges ment al systems". Each system cons ists of comprising our fingerprints ; nor do we one or more integrated , part ial l y self­ have gen es that inform ea ch neuron in our r egulating deve l opmental pathways l eading br ain wher e i t wi ll synapse and wher e its t o t he s tructure we recognize as a link dendrites will gxos , We do have an inher ­ in t he chain of homologues . These systems ited program for making certain patterns interact with nei ghboring developmental of neuronal connect ions, but there i s con ­ systems, and with the external environment. s iderable r oan fo r variation. This enve­ All of them taken together produce the on­ l ope of ac ceptable variation, within which togeny of t he organ ism . In view of t he differences do no t compranise the opera­ self-regulating properties of t hese devel­ tion of t he organ i sm, is bes t appreciated opmental systems, we ca ll them "epi genes " . fran the typological point of view. Following Hull (1976), we suggest that the individual appropriate to our analysis is The typological approach has played a the species. maj or role in continental European VJOrk in evol ut i onary morphology . It has not We know a devel opmental syst em or epi ­ been mich in evidence in the United States gene by i t s VJOr k . I t i s a theoretical en ­ or Britain, where variability is generally t ity, like t he gene, but i t i s even rrore viewed s tat istical ly, as an expr ession of abs t ract, becaus e it i s a process, a ser ­ popul ation processes ; Bateson being t he ies of interactions. Perhaps it i s best notable exception to this t endency. Sei­ t o consider it as a set of deve lopmental l acher (1970) has set forth a valuable mod­ fields in time and space that are jointly ern version of this approach- -a balancing responsible f or sene useful part of an or ­ of phyl ogenet i c , functional , and morpho­ ganism. The part appears gene r ation after genet i c fact ors called constructional nor­ gener at i on , species after species, thus phology. It i s under the heading of rror ­ producing a cha in of horrol ogues . Over phogenetics that typology f inds i t s use. t ime , the r equirement fo r concer ted action In order to under stand t he developmenta l constitutes sel ect ive pressure that knit s process that yields a variable structure the f ields t ogether. The temptations for - - say , our fingerprints - -one examines de­ reification and metaphor when we consider, velopmental error s and their subsequen t say , sel ecti ve pres sures on an epigenetic accamndat i on , the r ange of variability, l and scape, are overwhelming. We often ontogenetic changes, patterns of repair yield t o them in this paper, for wi thout and regeneration, and especially aclaptive­ such devices camunication on t his sub ject ly neutral by-products of morphogenesi s . i s impossi bly abstract and compl ex . These neut r al but annipresent by-p roduc t s are traces of developmental processes . DEVELOPMENl'AL PRELIMINARIES Sei l acher (19 73) has named them fabrica­ tiona l noise. The amount of fabrica t i ona l Let us turn to the properties of devel­ noise in a structure shows the degree of opment that are central t o our analysis. freedan that ex isted in its production. To begin with a couple of truisms , devel­ Thus , it i s a measure of the amount of opment i s not a thing, or a series of self-organization in the underlying epi­ s tages. I t is a process--an int eraction genet i c system. Seilacher's appr oach has between the expression of genet i c infor ­ a general utilit y- -Hut chinson (1978) has mat ion and environment. The internal en­ extended it t o an explanation of differ­ vironment--what has previously developed- ­ ences in human intelligence- -and a special is as important as the external envir on­ va l ue to paleontology . With it, paleonto­ ment. The s impl ist i c ques tion that is l ogis t s can us e the pat t erns preserved in inrnediately raised abou t any difference fossils as windoes on the epigenetic pro­ between individuals in a population--is cesses that shape those patterns, and on t he diff er ence genetic or rrer ely environ­ t he intrinsic evo l ution of such processes . mental?- -is a misl ea ding di chotany because 184 EVOLUTIO N TODAY Ra cho otin & Thoms on

Fabricat ional noise i s a source of in­ or too large, or too far t o the side to nocuous variability. A pot ent ially threat­ play i t s small r ole in the conditioning of ening source of variability is error in the battalion of cells that induce the fo r­ devel.opnental, pr ocesses . Yet , given the mat ion of lens- - there has been a great se­ canp lexity of devel.oprent , mis takes are l ec tive pressure t o "make do". This ac­ inevitable, what ever the degree of genet i c coom:xlation- -behavioral, devel.oprental , specifica t i on . Certain sorts of mistakes physiological- -is the r esult of the mul ­ may occur because of f ea tures of the ex­ t itude of int er-connect ed alternat ives ternal envi.rorrrent, others may r esult fran within and between systems . intrins ic susceptibilities to error. In either case , there i s a predi sposition for Occasi onal l y , gross errors occur and certain kinds of mistakes to recur. When are still accoom:xlated. The congenitally t his happens , there is a select ive pres­ bipedal goa t s tudied by Slij per (1942a , sure either t o specify a s ingle devel op­ 1942b , 1946) i s a fallDUS example of this. mental pathway a ll the rrore emphatically, Not only did the goat manage with its hind or to accoom:xlate these tendencies to er­ l egs alone, but , as it l earned to walk ror and turn them towards alternative bi pedal l y , i t developed an S-shaped spine, pathways that lead t o the normal develop­ modified muscle insertions, and developed mental end. These alternat ive pathways such correlates of bipedal Locormt i on as are, we expect , in large part created out a relatively broad neck and an oval rath­ of those wrong turns that a devaloprental, er than a V-shaped thor acic cross-section. sys t em is peculiarl y l ikely to make- -the No one would maintain that goats have problem becanes part of the so l ut ion. genes for devel oping an S-shaped sp ine, These r espons es to the inevitabilit y of "just in case". What we see her e i s a error are what Wadd ington (1942) called basic rnanrnalian potential, emerging fran canalizati on . Canalized pathway s evolve t he self-ri ghting pr operti es of the skel ­ so that in a variety of external and in­ eto-muscular sy stems of al l rnanrnals, and ternal envirorrnents the deval.oprental, sys­ the sor t exploited by our haninid ances­ tem reaches its normal goa l . tors . A similar range of pot ent ial s , this time for the skul l , is suggested by DuBrul We expect that alternative pathways to and Laskin's (1961) production of several the same devel.oprental, end are the rule in primate-like features as the result of a devel.oprental, systems. Selection will, we s imp'Ie nutilation of a synchondrosis in a believe, produce and maintain many alter­ newborn r at. na t ive devaloprental, routes in the genane, and the success of such canalization may A spectrum of self-organizing develop­ well be constant phenotypic expression in mental properties exists , fran alternative the structure that is produced. biochemical pathways, to the bounded free ­ dan of fabr i cat ional noise, to the canal i ­ This suggests a paradoxical invers i on za t ion of deve lopmental systems or epi­ of camonly held ideas about the na ture of genes, t o the ac coom:xlat ion of errors that variability. Wher e we see phenotypic con ­ occ ur in the inter action of epigenes , to s t ancy , we may be dealing with underlying the behavioral and phys iological adjust­ developrental, and genetic variability. ments of the whole organism to deve lop­ Where we see phenotypic variability, for mental calamities . The pot ent ial to make example, in fingerprints, we may be l ook­ these accoom:xlations i s a canpon ent of the ing at the results of a single genet i cal l y conservative force of stabilizing se lec­ invariant epigenetic process with a large t i on. Such selec tion is omnipresent, but canponent of self-organization. In sane its expr ession is nearly invisible . cases, such an epigenet i c process may be , locked into a fabr i ca t i ona l mechanism that INI'RINSIC EVOUJrION cannot be further specified genetically . The large range of variability we see in The epigenet i c landsca pes that are built such cases is an extension of the inter­ up for perfectly normal developrrental, r ea­ act i ve rather than the r eplica t i ve side of sons are, fortuitously, a reserve of coor ­ or ganisms , and as such is not :innEdiately dinated, cohesive change . I f a mistake oc ­ like l y to be t he source of fu ture evo lu­ curs--not sanething as gross as a bipedal t ionary change. Unles s Fisher 's Funda ­ goa t , but perhaps as great as t he divided mental Theorem i s f ramed in a wider, de ­ maxillae of the bolyerine snakes described ve l.opnental. context, it is perhaps not so by Frazzetta (1970) - -it may be accommo­ fundamental . dated.We do not know whether t he ini t i al effect was a response t o an internal or an Still, despite canalization within epi ­ external perturbation, but the snake YXlrk­ genes , mistakes will occur. Even at the ed, and it marked the beginning of a new, level of int er act i ons between epigenes, now tragically extinguished, l ineage . accoom:xlati ons will still be made. Given That such an ananaly could becane normal t he inevitable mistakes - -a heart t oo small, nust mean that after r epeated evocations , Epigenetics & Evolution PROCEEDINGS, ICSEB -II 185 t he response became genet i cal ly assimila­ Develorxnental change is cohesive, self­ t ed. integrating and fast. It need not be adapt ive in the sense of fit ting sore as ­ Genetic assimilat io n of an accommoda­ pect of the external environment, though ted devel.opnen cal, change, if the change it may be. Adaptation may sexretimes be i s of imrediat e adaptive interes t , may be intrinsi c ; that is, i t serves to further the sort of r are event that marks the en­ the coordinated expression of a change trance to a new adaptive zone . The inter­ that exists mainly because that change is est of dcvel.oprent; to comparative anatrm­ easily produced. Such sorts of changes ists and paleontologists i s built on this are wel L known, generally under the head­ possi bi l ity. But an accommodated develop­ ing "a l.Loret.ry". What happens ontogenet­ mental error that i s neutral or even ically constrains and facilitates What sl ightly maladapt ive with r espect t o th e happens phylogenetically. Allexretry i s ext ernal envir onment may still be genet i ­ r elated in turn t o t he pat t erns and pro­ ca l ly assimilated i f environmental influ­ cesses of heter ochrony , which were so ably ences persist in producing the error. refurbished by Gould (1977). And hetero­ That i s , given both intrinsic and extrin­ chrony i s, simply, a special case of epi­ sic selective pressures. on occasion se­ genetic evolution: those changes that are lection on the internal environment can feasible in the interactions between epi­ have primacy over the demands of the ex­ genes . Changes in the structure, position, ternal environment. This may be a camon function, relative size, or time of appear­ event in evolution at and below the spe ­ ance of parts of organs are called forth cies level. from the usua lly cryptic variation in the paths of their development. Consider a spec ies whi ch responds de­ va l.oprnentaILy to an environmenta l grad­ In all of this we fo llow a track not ient by producing = phenotypes , A and B. often taken fran that great marsha lling Even if in all environments B is competi­ yard of evolutionary thought, Mayr's Ani­ tively inferior to A, if sore environment ma l Spe cies and Evo luti on ~~yr 1963). A exists such that the threshold for pro­ breakthrough in that book is the balancing duction of the B phenotype is crossed, of external factors in speciation, espe­ then there will be selective pressure to cially geography, which he had so thor­ produce the best, most harrroni.ous B pos­ oughly established in Systema tics and the sible. This i s not the only outcexre; we Or i gi n of S pecies (Mayr 1942), with ll1ter­ may also have selection to raise the nal factors--the co-adapted gene complexes, threshold of production of the B pheno­ epigenotypes, and especially the genetic type, perhaps in the B environment itself revolution at speciation. These terms are if the environment is wavering on the edge sexretimes taken as labels for our collect­ of the threshold. ive ignorance about species. This we think is an unfair assessment. In the What is important is that, granting a genet i c revolution, ~~yr united the typo­ recurrent environmental influence, "e can logical properties of the wild type, which have assimilation for intrinsic reasons. show up in the good soloist phase, with A possible example of this is the marked the populational properties of balancing trend to size reduction that occurred in selection, which characterize the good medieval cattle in Denmark (Degerb¢l 1963) . mixer phase. Thus he harnessed the theo ­ One hypothes i s to account for t his change retical M:>rk horses of the 1950s popula­ is that it is the result of keeping the tion genetics to the task of explaining cattle in captivity over the winter, rath­ the emergent properties of species. In so er than allowing them to range freely . doing he produced a species concept that This was the season that the calves were canbined the advantages of an intrinsic being carried, and the inadequate fodder approach, which could be applied to the that the cows received produced small off­ breakdown of developmental pathways in hy­ spring. The size change was not itself brids, wi.th the advantages of an extrinsic adaptive, but while the environment called approach, which made sense of the geo­ it forth, it became a selective pressure graphic and ecological aspects of species . for smaller cattle in subsequent g~1era­ This theoretical approach to species is tions . Once started, the trend could not far more powerful than one that is merely abruptly be reversed. Even wi.th improved operationally convenient, say, a cut-off nutrition, a large calf is no service to point on an electrophoretic score card. the genes of too small a cow. A similar The genetic revolution is not yet very ac­ story, involving accommodation to an inter­ cessible to study, but it is a major con­ nal deve lopnental environment rather than tribution to science, nonetheless. adaptation to external conditions, may ac ­ count for the consistent evolution of A new emphasis on the intrinsic side of dwarfism in large island marrmals (Sondaar evolution is called for today. Although 1977). it has been ,vith us since the biological 186 EVOLUTION TODAY Rachootin & Thoms on spec ies concept, t his s i de of the concept fossi l r ecord, and that many species show has been pl ayed down in f avor of such ex­ no change at all between or iginati on and trins ic ques t ions as al l opa try vs . sympa­ extinct i on, and Gingerich 's (e .g ., 1977) t ry, t he real ity of subs pecies, l ocal ad­ argument for uru.-dfrectdona l, changes in aptati on , charact er displacement, and rrorphology . The rror e we know about the antihybridization mechani sms. It i s time Lower Cambrian diversifi cation of inverte ­ for a change in perspecti ve , the sort that brates , and the Cretace ous r ad iation of coul d be provided by uncoupling as mich ang iosperms , the faster and rrore staccato as possi ble the extrinsic and intrins i c they seem to be . Directionality , salta­ as pects of evoluti on . Of special s ignif­ t ory leaps t ha t land on their feet and i cance in this program i s t he odd sympat ­ stay sti ll unti.L they l eap again, adaptive r ic, or morphologically sal tatory, or in­ types- -these r eca ll the irri tat ion But ler s tantaneous speciation that shows the in­ (1879) felt for the evol ut i on of his day-­ trinsic evol utionary potentials of organ­ was it really accounted for , "by a series i sms that are usually concealed by rrore of accidental variations , each of which obvious extrinsic f act ors. I n the 1950s was thrown for , as it were, with dice? We and 1960s evo l utionists sought a singl e shall rrost; of us feel that there mist; have t heory t hat could account for all the phe­ been a l i t tle cheating sanewhere. . ." norena of evol ution . Thi s has probably been pushed as f ar as it wi ll go . If we Epigenesis can provide the directional­ are t o go beyond i t, we mist; partially ity, the typology, t he saltati on, in shor t , disassemble t he synthesis and experiment the cheating that has in the past aroused with t he potential s of i t s components . in the breasts of our predecessors pas sions for neo-Lamarckianism , aristogenesi s , pan­ Chi ef among thes e i s the l at ent evol u­ genesis, bathmism, hopeful nonsters , and a tionary potent ial of developmental systems . hos t of entelechies . They saw sanething Most current considerations of epigenet ics that generati on af ter gene rat i on of evolu­ r estrict the importance of epigeneti c t i onists have been t aught not t o see- -an mechanisms to t he reason for which they integrative and emergent s ide to evolution. evolve. Epigeneti c systems are conserva­ Epi genetics can bring to this phenanenon t ive- - t hey prot ect the ends of a develop­ a strai ght - forward, non-myst i cal explana­ mental pathway by r esor t ing t o al ternat ive t ion . However, i t is an appr oach on which developmental means. But the normati ve i t i s r ather difficult to experiment . flIDctions of epigene t ic sys t ems do not ex­ What we are about t o out l ine may not ca ll haus t their pot ent ial when i t canes to t o mind 101 falsifi able hypotheses . This t r ans - spec ifi c evol ut i on . How do epigen ­ does not worry us . The strai ght-forward eti c systems cane together and how do they probl ems of evol ut i onary biology have been cane apart? A look at the fossil r ecord attacked al ready. The r esidue that r e­ gives, we think, sane hints concerning mains wi ll not give up its secrets to this problem . blunt; methodological instnnnents .

PALEONl'OlDGY AND EVOUITION MEGA-EVOLUTIONARY CHANGE

I t has cons ist ent ly been the pal eont o­ The rare produc tion of a new adapt ive logists who have the hardest time in r e­ t ype is not predicted fran l ower l evels of conciling syn thet i c theory with t heir anal ysis such as population genet i cs; such stock in t rade of evol ut ionary data. The events are emergent. But, if we might existence of l ong-term trends, sane al leg­ adopt Needham' s (1933) metaphor that evo ­ ed ly quit e single-minded; l arge scale con­ lution r equires a changing of gears , a vergence and parallelism; the abrupt ap­ going t hrough neutral, then we woul d argue pearance and , at some subsequent point, that our black t r ansmissi on box is develop­ exp losive radiation of new groups ; the ap­ ment. And epigene s is ensures that our parent abs ence of intermediates ; the in­ transmis s ion i s at l eas t semi -autcxnatic . tegri ty (in terms of rrorpho logy and r ates Though t he "point " of canal i zat ion i s to of evo lution) of what Simpson (1944) or i ­ ensure t hat an expected resul t i s obt ained , ginally ca lled adapt ive types ; and such sti l l an lIDexpect ed r esul t autcxnatically throwbacks to Geoffroy-S t . -Hilaire as pull s rel ated devel opment al syst ems along Williston' s Law-- these have always nagged with it. at the synthet i c heart s of evo l ut ioni s ts. Ther e i s no denying t ha t these are problems Let US suppose t ha t a developmental to be solved; indeed, r ec ent pal eont olog­ mistake , and such behavioral, structural , i cal work has l ed us t o take t hem rrore or phys iologi cal accommodation as t he mis­ serious ly. As exampl es, we have Van Va­ t ake engenders , allows an organism t o en ­ l en' s lawful r at es of extinction for hi gh­ t er a new adaptive zone . Then all that er taxa (Van Valen 1973) , the arguments of is needed for i t t o pers i s t there , i s for Eldredge and Goul d (1972), and St anley the l ower ing of t he developmental thres ­ (1975) t ha t we do not see spec iat i on in t he hol d that general ly prevents that mistake . Epigenetics & Evolution PROCEEDINGS , IesES-II 187 For assimilation to occur, there must be rmre and rrore changes on a single l arge an environment which frequently evokes adapt i ve thane. This is an adaptive r adi ­ the altered phenotype. 'That envi.rorrrent; ation. Not only might such a r adiation be has always been assumed to be ext ernal. r apid ; we would expect it to be so. Were The epigenetic effects of external change i t not it would be overtaken by the con­ could be transmitted to and intensified st ant pressure of stabilizing se lect i on by the internal envi.rorment, which could that resul ts in th e production of a mature then be the prime rrover behind assimila­ and wel l canalized epigenet i c l andscape . tion. The epigene need not vary in all direc­ t i ons at once; perhaps certain sorts of EnvirorJrrentally affected threshol ds are vari at i ons are part i cul arly easy or adapt­ known; Van Valen (1974), for instance, has ive . If the sarre sort of change occurs documented an increase in (admit t edl y sequentially in a s ingle epigene, the hopeless) five-legged frogs in particul ar­ cumulat i ve effect is a l ong term trend, l y cold l akes . But if such changes were such as hypsodonty in horse t eeth. useful, t hey could be assimilated into the genorre , Waddington (1975) suggested that ATAVISMS adapt ive phenot ypi c differences between quiet and turbulent water r aces of th e We have proposed that a relatively un­ pond snai l Lymnaea stagnalis were geneti­ stable epigenetic system might illuminat e cally assimilated in j ust such a way. The sever al major evol ut i onary ques t ions. But classic obj ection t o hopefu l rronsters-­ epigenet ic systems are normally stable. that a pig with wings has no chance of Where do we turn to study the actual wor k­ finding a s imil arly endowed mate- -misses ings of evolut ionary epigenetics ? An ob­ t he point that if you have one pig with vious area i s the huge field of atavisms wings , there are rmre where that one carne and their experimental analogues. fran-- in th e developrterital pathways of the relatives of Archaeoptopig. Horses born with three toes, flatf ishes with pi~t ed undersides , Hamp~' s (1959) When an adaptive change has occurred, experimentally manipulat ed chick l eg that it will at f irst have but a f l ickering and reverted to a r eptilian state-- these are uncertain phenotypic expression. Immedi­ striking signs of the sa ltatory potential at ely, t here will be intense se lecti on to of development . Of such cas es, Gould pr ot ect and buffer the expression of this (1980) writes: changed state. Secondary patheays will evolve that canalize the system. It will What els e might their gene t ic s ys­ be further stabi l ized by t ies to other de­ t em maintain , normally unexpress ed , velop:nental sys tems that are temporally, but ab le t o ser ve, i f acti va t ed , as structural ly, and functionally related to a po s s i b l e focus for major and rap­ it. This kerfuffle of evolutionary activ­ id evolut ionary chang e? [ a nd] An ity i s only a rrore intense expression of o rganism' s pa s t not o nl y constrains the const ant but cryptic se lection that its fu tur e ; it a l so provi des as leg­ maintains and strengthens the developrenr­ acy an enormous reservoir of poten­ al status quo. In the end, a successful t ial for rapid morphological c hange evolutionary step will exhibit a hard, ba sed upo n s mal l gene t i c a l terati o n . gem-l ike constancy in the expression of the new feature . The adapti ve novelty will \-Ie agr ee totally with the spirit, but the have been pro t ected by a canalized epi­ letter is slightly t roub ling. gene , assembl ed out of the predispositions to error in the early, unstabi l ized stage. Atavisms undoubt edly give us insight into epigenetic processes, but they only The new adapt ive feature may lead the mislead when taken as examples of the pat­ organism to new behaviors and into new terns of epigenetic evolut ion . We l abel envi rornnents ; these envir ornnents can then a variant as an atavism because i t vio­ i nt eract with th e underlying epigene to lates some defining quality and derived produce further changes. The rrodi.fi.ed epi­ character state of the group in question-­ gene many al so be affected greatly in its horses are expected t o have single hooves phenotypic expression by minor changes in and flatfishe s are expect ed t o have right the well cana lized develop!lffltal systems and left sides unlike . Such qual ities, in with which i t interac t s. Both intrinsic par t , determine the or ganism's adapt ive and extrinsic fa ctors thus may lead to fur­ potentials as well , so that unless they ther changes , because the recently altered have only recentl y evolved their devel op­ epigene is relatively l ess buffered by ment ought to be heavil y cana l ized. While secondary pathways or deep devel op!lfflt al vari ant s on an adapti ve thane have evol­ channel s than its older, rrore cons istent utionary potential , th e undoing of an ad­ neighbors. Continuing changes, if adapt­ aptive theme does not. ive and genetical ly as similated, lead to 188 EVOLUTION TODI\Y Rachootin & Thomson The major f eatures of evol ut ion are t i les with reduced ca l canea and other hope­ not conposed of structures withdrawn fran l ess lTOns t ers. A developmenta l sequence a developmental legacy; t hey are cCXllpose d i s lTOre l i kely: a simple rate change in de­ of processes that shape themselves as they velopmental f iel ds caused the calcaneum go along. Epigenes retain ances tral poten­ to be included in a different structural t ials because, to use Riedl's (1977) t erm, unit and the r esult was functionally accan­ they ar e ''burdened'' with other epigenetic rrodated (including shifts in nuscle in ser­ systems that use thei r products as devel­ tions occurring during subsequent develop ­ opmental cues. But these ancestral poten­ ment). The capture of the calcaneum t i als have little chance of expression in changed the internal envi r onment of the themselves , becaus e their ance stral pheno­ fields invo lved in l eg development . The typic expr ession i s i rrel evant to the se ­ initial accorrm:xlat ion was the development­ lective pr essures favoring t heir r eten­ al response upon which se lection ~rked, t ion. The legacy exists , but t he assets eventually producing its genetic assimi la­ ar e not converti ble. It i s becaus e of the t ion . The r esult becanes an adaptation in burdens that epigenes bear that they have the sense of proving adaptive, but not in evolved t he capacity to accorrm:xlate each the sense of having been sel ect ed for . other. And it is t he capacity for accon ­ The change in the position of the tarsal modati.on that gives epigenetic systems joint immediately gave a new range of ad­ their mega- evolutionary si gnif icance, be­ apti ve possibili ties . The new pat tern and cause i t faci litates adaptive experimenta­ the new epi gene may be the origin of fur­ tion. ther intrinsically produced ananalies , sane of which may prove adaptive and form A genuinely l abi l e epigenetic system an adaptive radiation. ought t o be of the greates t in t er est to an evolutionist, and i t i s a far, far better Even those adaptation s which do not thing than an occas ional atavistic slip in arise fran rearrangements of an organism ' s a mature epi genet i c system. This i s not development al pathways filqy somet imes be t o say that reversion has no part to play produced by admixture with for eign devel­ in evolutio n , just that the par t is small . opmental pathways . Given the free-float­ After all, all God 's hoatzins got rmre ing abi l i ty of devel opmental systems to than wings . accorrm:xlate to insult, it ought co be pos­ sible for introgression t o be the basis of ADAPrATIOO an epigenet i c revolution. The phenanena of hybridism are pre-eminently the pheno­ While an epigenetic approach cannot mena of developmental in cCXllpat ibili t y . tell us what will make a new adaptation, But there is no reason to deny t he possi­ it does suggest sanething about the sour­ bility that a mixture of related but dis­ ces of adaptive novelty and the ease with tinct developmental pathways might produce which an adapt i ve change i s initially ac ­ adaptively in t eresting novelties, \'hich corrm:xlated . As Gould (1977) notes, many on occasion are assimilated . pew adaptations wil l be t he r esult of re­ arrangemen t s of developmental information Developmental shake -ups need not be re­ already at hand. Playing the f eatures on st r ict ed to interactions with congeners . one age or stage or size or shape against The products of symbionts can shape devel­ those of another i s , we do not doubt, the opment of a host so consistently that the 'pr imary material basis of evolutionary symbionts becane part of its intrinsic change . Gould argues convincingly for an evolution. lhus, in sea lettuce ( VI va) extrinsic, ecologi cal explanation of these the characteristic foliose thallus has r eshufflings. He ~uld add that intrinsic been shawn to be induced by bacterial sym­ factors may also be a t ~rk . bionts. In axenic culture the alga grows as tufts of uniseriate cell s , and the ad­ In cases where a functional intermedi­ di tion of various bact eri a pr oduces rib­ at e i s impossible, for instance in t he bon-like forms, and tubular forms that r e­ maxilla of bolyerine snakes , which is ei ­ semble the related green al ga Enteromo rpha ther in one piece or = , a developmental (Provasoli & Pintner 1980). explanation may be the only alternative. Simi l arly, a l ong- standing problem in the As for the tempo of adaptive change , evolution of the hind limb of r ept i l es is the epigenet ic approach suggests that on the explanation of the transf er of the t he scale of evolving l ineages , an " imna­ calcaneum fran the foot (in crocodilians ture" epigene may facil itate a succession and pseudosuchians) to the leg (in dino­ of r elated changes. At the f iner scale of saurs) , fran one functi onal unit to anoth­ the successio n of ind i vidual species, we er . Paleontolog ists have been hard pr ess­ suggest that the constant evol ution of de­ ed to discover a functional int ermedi at e velopmental systems within a species ir­ stage; a gradual sequence is poss ible only regularly erup t s to produce new speci es , by invoking hypothetical small, l i ght rep- which then normal l y remain phenotypically Epigenetic s & Evoluti on PROCEEDI NGS , I CSEB- II 1B9 unchanging even as their developrrental sys­ To this we answer that r eproduc tive tems are e laborated in ways t hat fo rtui­ i sol a tion has a l l t he proper ties of a de ­ tous ly determine t he na ture of t he i r des­ veloprrental s ystem, one that has as i t s cendant s pecies . Organisms are subject t o goa l the pr edic t able r eproduction of the cons tant evolution, sane extrinsic , whi ch species . As such, i t r equ ires an especi­ produces local adaptation, subspecies, and a lly large set of cues fran the external clines, and sane intrinsic, which produces environment. The environment is involved canalized ep igenetic pathways and a llows not just during early developrrent , but fo r t he production of new species, or at through adult life. Not only mist struc­ least a class of species with a special ture, physiology, and behavior of the or­ rrode of origination, and special potential ganism be coordinated, but all I1USt be co ­ for future evo l ution . ordinated with the structure, physiology, and behavior of other individuals of the ClASSIFI CATIOO sp ecies. The demand fo r t he equ ivalent of canalizat i on and sel f-regulation i s all Evol utionary epigenet ics may offer a the stronger here, given the mich l arger resol ution to t he current quandary of sys­ environmental canponent. The argunent can tematics. To date, the chief contri bution be made that mate recognition systems are of cladistics to the data of evolution has intrinsic to all organisms (Paterson 1978, been the uncovering of far nore parallel­ 1980) , and that these intrinsic systems ism (horopl.asy) than anyone could have are in many or gani sms more important in imagined. Only cladistic analysis could reproduction than such extrinsic factors have made this discovery. If it holds up , as anti-hybridization mechanisms . It may the ph i l osophical assumptions of a l l be easier to learn to mate wi th like than schoo ls of classification, including clad­ to learn not to mate wi t h un l ike. istics, will turn out to be false. I f parallelism is the rule , then why should I f we view the mate r ecogni t i on system we i dent ify parsinony as the absence of as a kind of epigenetic system with a parallelism? particularly large environmental canpo­ nent, then all that we have said about in­ Corrmmly held pr imi.t i ve developrrentaJ. trinsically controlled saltatory change pathway s, each of which have predisposi­ will hold, except that there is in this tions that are expressed independent of case less reason to require an adaptive descent, that is, paraphyletically, may change to result fran the saltation. Any well hol d t he key to what is going on. change in t he mate recognition system will Extreme ly detai led attention to develop­ "work" as l ong as i t succeeds in selec t ing mental pa thways may help to untangle ap­ l ike-minded mates and perpe tuat es i t se l f . parently cladal arrangements of charac­ This wi l l produce a new biological spe­ ters and the gradal processes of develop­ c ies . If that species i s otherwise doing ment that could produce them . For this , nothing different fran its parent species , a ser i es of developrrental stages will not it may well disappear for no other reason in itself be sufficient: it i s the enve­ than its comparative rarity. l ope of epigenetic accamodations within which reside the ontogenies of s ist er Thus, speciation may be a case of easy groups that is no st important. cane, easy go . The cryptic or sibling species that sanetimes turn up when a Paleontologists woul d seem to be l ef t group is c losely studied may be cases of out in t he co l d by t his program, but such such easily produc ed , s l ightly differenti ­ is not the case. They can analyze fabri ­ a ted, adaptively equivalent species . Per­ cational no ise, which i s an appropriate haps they r epr esent the few survivors of introduc tion to the epigenetic envelope a vastly greater number of ephemeral spe­ around the production of fossilizable c ies that population biologists would structures , and they can trace the evolu­ never find unless they had sane good rea­ t ion of such envelopes through time. son to look for them.

SPECIATION PATIERNS Fran our perspective, a lineage with a truly pranising evo lut ionary future woul d Obviously , bithor ax fruit flies, what­ be favored wi t h both a sanewhat l abile ever t he complexity of the i r altered norph­ mate recognit i on system, and a sanewhat ology, are not per se spe c ies in the sense labil e ep igenetic system for a trait that of the reproductive isolation that is at i s of adaptive interest . Both will be the heart of the b iological species con­ sufficiently canalized to appear as con ­ cept. One may grant us our saltations , s istent, dependable characters within spe­ and t hen deny them any s ignificance unless cies, but ne ither wi ll be so burdened with we fashion appropriate anti -hybridization other developrrental responsibilities that mechanisms that would make them "good" they cannot change to produce new species. species. Perhaps this sounds like a lot to ask fo r . EVOLUTION TODAY Rac lloo tin & Thomson

We think not.I f , as the fossi l r ecor d ciati on . Such a case i s provided by the sugges ts, spec ies are general ly unchang­ cichl i ds of the rift l akes of Afr ica. i ng once they are formed, then t hose line­ ages which diversify and prosper will be Three intrinsic factors contribute to those that can easi l y speciate and in so the ease with which cichl ids gener at e new doing capture intr ins i cally gener at ed ad­ spec ies. Their complex and pl astic behav­ aptations . In effect, we have spec ies io r provides plenty of material that can se lection for modes of mate r ecognition be shuffled t o make mate recogniti on sys ­ that promote speciation. Species se lec­ t ems. The fish are int ensely visua lly tion need not be t he tot ally pos t hoc or iented , as schooling fry and , as adults, accumulation of l ineages that happen to in feeding and mate r ecognition. Inter­ have survived. I t i s in our scheme an ac ­ estingly , cichlids have the earliest dev­ tive, intrinsic factor, a mechanism that eloping opt i c placode of any teleost. And over geologi cal time produces l ot s of the f i sh are colorful , they exhibit color speci es in a lineage. Adaptively indif ­ polymorphism , and th ey depend on color ferent, ephemeral species are produc ed in cues for mate recognition . On the appar­ l ar ge number s as wel l - - these are a kind ently adaptive si de, ci chl i d speci es show of spec ific l oad. a tremendous diversity of j aw and tooth morphologies . Liem (e .g . , 1973) at tr i but es Our ideas in th i s area are an extens:'on their success to a new arrangement of the of Carson 's (1975) theory of the open and pharyngeal j aw. The array of forms, Liem closed genet i c systems. Certain lineages writes, calls for "minor r econs truct i on of can adapt only by speciat ing-- that i s , the genot ype which i s involved in evolu­ shaking up their closed genetic sys tems. tionary changes of the pert inent ontogene­ Others can adapt without speciation- -they tic mechanisms" . The ontoge netic mechan­ have relatively l ar ge open sys tems. In i sms may requi re minor tun ing, indeed: l ineages of the first sort, we suggest the mollusc-eating cichlid Ast a t oreochro ­ that mechanisms that predispose the organ­ mis allua undi was reported by Greenwood i sms t o undergo frequent speciations will (1965) t o produce bicuspid teeth when be se l ected . r aised on insec t s but mol ariform t eeth when r aised on molluscs . These intrinsi c Mo st fact ors that have been implicated fac tors , played against a succession of as causes of speciat i on could be rein­ "akes in these ancient basins, coul d pro­ forced by speci es se lection unti l they be­ duce the hundreds of endemic speci es , pro ­ come a favored mechanism for speciation- ­ bably during the geol ogi cal ly shor t l ives an adaptat ion at the level of l ineage . of the current lakes . For while the ba­ The factors include suscepti bili ty t o sins are ancient, the lakes th emselves, chr omosanal changes- -in ploidy level, like the Triassi c r ift lakes of North Amer ­ chromosome number , organizat ion of sex ica, fill with water and dry up in r esponse chromosomes (for instance in bovids, see to climatic cycles on th e order of 20,000 Todd 1975), inver sions and translocations , years (Li vingstone 1975; Olsen et al. and many permutations (see review by White 1978). 1973) . The frequency of such changes de­ pends on the effi cacy of mechanisms for Note that our epi genet ic approach to chromosanal r epair--a kind of canalization spec iation does not insist that th e mech­ lit the cellular level. The slight est de­ anisms we postulat e apply to all specia­ crease in t he ef ficacy of such r epair me­ tion event s , or even to al l lineages . chanisms could greatly increase the chance But if th ey apply t o some l ineages , and of speciat i on without being an appreciable some speciat i on events in other lineages, burden on the dependabilit y of meiosis. then , over geological time , th ey can ac­ The shuffling of immunologic recognition count for the existence of properties of systems in the gametes of plants and free the exi sting biota her et of or e inexplicable spawning animals and the co-evo l ut ion of or uns een . eukaryo t es with r apidly evolving pathogens or symbionts in th e germ line (or meri­ CXlNCWSION st em) coul d al so have the effect of isola­ ting a popul ation by intrinsi c means, and We st art ed with orthodox notions of the thus become a mechanism for spec ies pro­ function of epigenesis , whi ch we have as­ duction . sociated with t he intrinsic side of Mayr I S concept of species. These we appl ied to In r are instances , a mechani sm for spe­ current prob lems in pal eonto logy --adapt i ve ciating and a suitably plastic , adaptively zones, functional anatomy , patterns of int eresting epigenet ic system will co-oc ­ or iginat i on , change (or i t s absen ce) in cur in an organi sm whose environment i s f ossils with excellent strat igraphic r ec­ sufficiently complex in space and time to or ds . We suggest: provide al l that could be asked for in the way of extrinsic factors favorable to spe - 1. Properties of epigenesis quite for- Epigenetics & Evol ution PROCEEDI NGS, IeSEB- II 191 tuitously make r apid, cohesive, and ftmc­ evol ut i onary theory that i s nearly an in­ tional change poss ible. Internal adapta­ ver si on of the usual expectations of evol u­ tion is as impor tant as external adapta­ tionists . Sal tation, typo logy, intrinsi­ tion. cal ly directed speciati on, evol utionary trends independent of external condit i ons, 2. Nonnally constant features, if they the uncoupling of current population gene­ are not heavily burdened by other develop ­ tics and higher l evel phenanena of rnega­ mental systems, may be the source of new evol ut ion, genetic assimilat ion of acqui r ed evolut ionary directions because of th eir character ist i cs, selection for the abi l ity underlying developmental variabil ity. Var­ t o speciate, the ubi quity of paral l elism-­ i able features may not be , because their t hese are not ideas that figur e prominently variation may be fabr i cational noise. in t exts , and sane of them have been gr ounds, in the r ecent past, for excommun­ 3. A spec i es is defined by , among oth­ ication from the scientific communi t y. er things, i t s cohesive devel opmental sys ­ tems . Even t hough a spec ies need not We are by no means say ing that such change phenotypicall y dur ing its life , i t ideas ought to be the new dogmas of evolu­ is cons t ant ly accumulat ing si gni f icant de­ tionary biology. We are of f er ing this ap­ velopmental variabili ty, which allows (but proach not as a r eplacement, but as a com­ does not r equire) r api d, even sa ltatory plement t o th e existing theory. Evol ution change i f i t spec iates. is pr e-eminent ly a science of contingent truths - - that i s , demonstrating th e exis­ 4. Mate r ecognition systems are also tence of allopatric spec iation by no epigenet ic sys tems- -what i sn ' t, after al l? stret ch of the imagination implies th e Ma te recognition systems are nonnal l y wel l non-exist ence of sympat r i c speciat ion . cana lized; abnonnally their r earrangement So too, with th e i gnor ed if not proscribed produces new species , without the con­ evolut ionary ideas that have been ser ious­ straint of pr oducing adapt ive changes . A ly se t forth by such notable workers as new spec ies so pr oduced may for tui tously Bateson , Gol dschmidt , Waddington, and many capture a new adaptation ; such spec ies are continental workers. The synthetic theory mor e likely to survive. i s sufficient ly mature to be ready to har­ monize with many of its apparent opposi tes. 5. Once a devel opment al change has oc­ The r esul t ing pluralistic approach to na­ curred, the same epigenetic system, if not ture suggests innumerable new problems wel l buffered from developmental errors, and holds out sane hope of answers to old may make related successful mistakes . This problems we have alrrosr forgott en . produces what we r ecogni ze as t r ends, adap­ t ive zones and adaptive radiations . Though We invite you to r eflect on the possi ­ per haps very rare at anyone t ime, over the bili ty that sane of the evol uti onary hypo­ whole hist ory of l i fe, th e r esults would theses we have al l been taught to r ej ect profoundly shape the entire biota. are perhaps no rmre wrong than the al t er ­ natives that are th e usual basi s of our 6. Speci es se l ection i s an intrinsic day t o day wor k. If you will suspend dis­ and active proc ess- -given punctuated equil ­ bel ief, this can be an invigorating and i br ium, those species that easily spec iate exciting prospect. will capture rmre adaptati ons and be rmre likel y t o persi st and l eave descendant spe ­ We ask, ftmdamentally, that you balance cies . Therefor e, mechanisms of speciation the reductionistic , generally extrinaic may be cons idered to be adapt at i ons at the appr oach to evol ution, which assumes that l evel of l ineage. When plastici ty in a al l evolution i s the warfare of self i sh developmental sys tem and the mate r ecogni­ genes wri t l arge , with an intrinsic side t ion system co-occur, species swarms result. of evolution most easil y perceived from the higher integr ative l evel s of paleonto­ 7. Horrologous structures, produced by l ogy and morphology . It i s from this van­ evolving developmental syst ems or epigenes, tage point that certain emergent proper ­ are a basic per sist ent feature of mega­ t ies of development l ead us to t ake a hew evol ut ion, expressed in individuals of l im­ l ook at the nature of spec ies .We ask you i ted dur ation- -speci es. t o balance the selfish genes wit h the per­ sistent ser ies of horrologues whose perpetu­ 8. A t horough-going r evision and r ein­ ation we attribute to cooperative , accom­ tegration of the synthetic th eory is pos­ rrodating developmental systems, which might sible on these gr ounds . be called "selfless epigenes" .

Although this paper is a natural exten­ Richard Gol dschmidt's (1940) Materi al sion of accepted ar t icles of the synthetic Basi s of Evoluti on made the case for de­ theory appl ied to the data of paleontology velopment, saltation, and the uncoupling and morphology, the cumulati ve effect i s an of micro-evolution and macr o- evol ution . 19 2 EVOLUTION TODAY Ra chootin & Thomson Writ ing of the cr i t ical r eception of that t i on in t he mammalian fossil r ecord , pp. book in his aut obio graphy (Gol dschmidt 469-500 . In : A. Hall am (ed. ) , Patterns 1960) , he sa id: of evol ut i on as i llustrated in the fos­ si l r ecord . Elsevier, Ams t erdam. Th i s t i me I wa s not o nl y c raz y , but a l most a c r i mi na l . . . [ b ut ) I am c o n­ GCLDSCHMIDT ,R. 1940. The material bas i s f i dent that in twent y years my bo ok , of evol ut i on. Yal e Universi t y Press , whic h i s now ignored, will be g i ven New Haven, Connecticut. 436 pp. an hono r able p l a ce i n the his t o ry o f e volut i onary tho ug h t. 1960. In and out of the ivory tower . University of Washington Press , We stand in his house , twenty years after Seattle. 352 pp. those words wer e published, and f ind a prophet not without honor . GCill.D , S.J. 1977. Ontogeny and phylo­ geny. Harvard University Press, Cam­ ACKNCMLEDGEMENTS bridge, Massachusetts . 501 pp. For discussi ons and criticisms of this 1980. Hen' s teeth and mamiscr ip t , we are indebted to Catherine hor se' s toes . Natural Hist . 89(7) :24­ Badgley, Anthony Bledsoe, Paul Olsen , 28. Kevin Padian and Scott Wing. We r eceived the advantages of the spec ial expertise GREENWOOD , P.H. 1965. Environmental ef ­ of Richard Harrison (population biology) , fects on t he pharyngeal mill of a ci­ Robert Nakarrura (botany and Scr ip ture) , chl i d f ish, Astatoreochromi s allua un di , and Scott Poethig (developmental biology ). and their taxonanic implicat ions. Proc . Our special t hanks go to Arrr:! McCune and Linn. Soc . London 176:1 -10. Louise Roth, who not onl y provided exhaus ­ tive criticisms at every stage, but also HAMPE, A. 1959. Contributi on il. l '1!tude contributed or inspired several important du d1!veloppernent et de la r1!gulation concept s. des d1!ficiences et des exc1!dents dans l a patte de l ' embryon de poul et . Arch. LITERATURE CITED d'Anat. Morphol. Exp . 48:347-478. BUTIER, S. 1879. Evolution, old and new. H1.JT.L, D.L. 1976. Are species r eally in­ Hardwicke and Posul, London. 384 pp. dividuals ? Syst. Zool . 25:174- 191. CARSON, H.L. 1975. The genet ics of spec­ 1980. Individual ity and se ­ i ation at the di ploid l evel. Amer . Na­ l ection. Ann. Rev . Ecol. Syst. 11:311- turalist 109: 83- 92. 332. DAVIS, D. 1949. Comparative anatomy and HUTCHINSON, G.E. 1978 . An introduction the evol ut ion of ver t ebr at es , pp. 64­ to population ecol ogy . Yale Univer sity 89. I n : G.L. Jep sen, G.G. Simpson, & Press , New Haven, Connecticut. 260 pp. E. Mayr (eds . ), Genetics, paleontology, and evolution. Princeton University JEPSEN ,G.L. , G.G. SIMPSON, & E. MAYR Press , Pr inceton, New Jersey . (eds . ) . 1949. Genetics, paleontology, and evolution. Princeton Univer sity DEGERB0L, M. 1963. Prehistoric cattl e in Press , Princeton, New J er sey. 474 pp . Dennark and adjacent areas. Roy. Anth­ rop . In st. Occas . Pap. 18 :68- 79. LIEM , K.F. 1973. Evolutionary str at egi es and morphological innovations : Cichl id fuBRill., E.L., & D.M. LASKIN . 1961. Pre­ pharyngeal j aws. Syst. Zool. 22:425­ adapt ive potentialiti es of the mammalian 441. skull: An experiment in growth and form, Amer. J . Anat . 109:117-132. LIVINGSTONE , D.A. 1975. Lat e Quaternary cl imat ic change in Afr ica. Ann . Rev. ELDRErGE , N., & S.J. GCill.D . 1972. Punctu­ Ecol . Syst. 6:249- 280. ated equilibria: An alt ernative to phy­ letic gradualism, pp. 82- 115. I n : T.J. MAYR, E. 1942. Systemati cs and the ori­ M. Schopf (ed.), Models in pal eobiology. gin of species . Columbia University Freeman & Co., San Francisco . Press, New York. 334 pp.

FRAZZE'ITA , T.H. 1970. Fran hopefu l non­ 1963. Animal species and sters to bolyerine snakes? Amer . Na­ evolut i on . Harvard Univer si ty Pre ss, turalist 104:55- 72. Cambridge , Massachu setts. 797 pp. GINGERICH , P.D. 1977. Patterns of evol u- NEEDHAM, J . 1933. On the dissociabi l i t y Ep i ge neti c s & Evolut i on PROCEEDI NGS , I CSES-II 193

of t he fundamental processes in onto­ Acad . U.S.A. 72:646-650 . genesis. BioI. Rev. BioI. Proc. Cam­ bridge Phil os . Soc . 8 :180-223. TODD , N.B. 1975 . Chrarosanal mechanisms in the evo l ut ion of artiodactyl s . Pa­ OLSEN, P .E., C.L . REMINGTON , B. CORNET , & l eobiol. 2 :175- 188 . K.S. lliCl1SON . 1978 . Cyclic change in Late Triass ic l acustrine ccmnmities. VAN VALEN , L. 1973 . A new evo l utionary Science 201: 729- 733 . l aw. Evo1. Theory 1 :1 - 30 .

PATERSON, H.E .H. 1978. M:>re evidence . 1974 . A natural model f or against speciation by reinforcement. ---,th"'-e-o-r""~gin of sane higher taxa. J . Her­ S. Afri can J . Sc i . 74 :369- 371 . petol . 8: 109-121.

· 1980 .A cannent on "ma t e WADD:ING'I'a< , C.H. 1942 . Canalizati on of de ­ -:::re::Cc::-:o::gru=-"tion systems " . Evo l ution 34 : vel oprent and inher itance of ac quired 330- 331. characters . Nature 150 :563- 564 .

PRDVASOLI , L. , & 1.J. PININER. 1980 . Bac­ ---;::r=-~ ' 1959 . Evolut ionary adapta­ teria induced polynnrphism in an axen ­ tion, pp . 381-402. I n: S . Tax (ed.) , ic l abor a t ory strain of Vi va i ac t uca The evolut i on of life. Chicago Univ­ (ililorophyceae) . J. Phyco1. 16: 196­ ersity Press, Chicago, Illinois . 201. . 1975 . The evo l ution of an RIEDL, R. 1977 . A syst ems-analytical --=e::vo::"lr:-u"'t""'~onis t . Cornell Uni vers ity appr oach t o macr o- evol ut ionary pheno­ Press , Ithaca, New York. 328 pp . mena . Quart. Rev . BioI. 52 :35 1-3 70 . WHITE, M.J . D. 1973 . Animal cytology and SETIACHER , A. 1970. Arbei tskonzept zur evo l ution. Third ed it. Cambridge Univ­ Konstruktions-M::Jrphologie. Lethaia 3: ersity Press, Cambridge. 961 pp . 393-396.

· 1973 . Fabricational noise in ---'a::-:aa=p"'tT.~v::e: morphology. Syst. 2001. 22 : 451 - 465.

SLIJPER, E.J. 1942a . Biol ogic- anatomical investi gations on t he bipeda l ga i t and upr ight posture in marrrnal s , wi th spec­ ial reference t o a l i t t l e goat, born wi thout forelegs. 1. Proc. Kaninkl. Ned . Akad . \;Tetensch. 45 :288-295 .

· 1942b . Biologic-anatomical --illV~' - e-s"""t ""i ga tions on the bi pedal ga it and upr ight pos ture in marrrnals , wi th spe­ cial r ef erence to a lit tle goat, born wi thout fo r el eges . II. Proc . Kanink1. Ned. Akad , We t ensch . 45 :407-415.

· 1946 . Comparative biol ogi c- - -:ana=t::-:OOll:=T'cal invest igations of the ver te­ bral co lizm and sp inal nusculature of marrrnals. Verh . .Kan. Ned. Akad. .Wetensch. Afd . Natmrrk ; , Reeks 2, 42: 1-128 .

SlMPSON, G.G . 1944. Tempo and mode in evo l ution. Columbia Uni versity Press, New York. 237 pp .

SONDMR, P. Y. 1977 . Insularit y and i t s ef f ect on marrrnal evo lut ion, pp . 671-7 07. In: M.K. Hecht, P .C. Goody, & B.M. Hecht (eds.), Major patterns of vertebrate evol ution. Plenum Press, New York .

STANLEY , S .M. 1975. A theory of evolution above t he species level . Proc. Nat l .