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Epigenetics , Paleontology, and Evolution Abstract 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.
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