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Genetics and the Origin of Species,’’ Organized by Francisco J Proc. Natl. Acad. Sci. USA Vol. 94, pp. 7691–7697, July 1997 Colloquium Paper This paper serves as an introduction to the following papers which were presented at a colloquium entitled ‘‘Genetics and the Origin of Species,’’ organized by Francisco J. Ayala and Walter M. Fitch, held January 30–February 1, 1997, at the National Academy of Sciences Beckman Center in Irvine, CA. Genetics and the origin of species: An introduction FRANCISCO J. AYALA* AND WALTER M. FITCH Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697-2525 Theodosius Dobzhansky (1900–1975) was a key author of the have the best chance of surviving and of procreating Synthetic Theory of Evolution, also known as the Modern their kind? On the other hand, we may feel sure that any Synthesis of Evolutionary Theory, which embodies a complex variation in the least degree injurious would be rigidly array of biological knowledge centered around Darwin’s the- destroyed. This preservation of favorable variations and ory of evolution by natural selection couched in genetic terms. the rejection of injurious variations, I call Natural Se- The epithet ‘‘synthetic’’ primarily alludes to the artful combi- lection.’’ nation of Darwin’s natural selection with Mendelian genetics, Darwin’s argument is that natural selection emerges as a but also to the incorporation of relevant knowledge from necessary conclusion from two premises: (i) the assumption biological disciplines. In the 1920s and 1930s several theorists that hereditary variations useful to organisms occur, and (ii) had developed mathematical accounts of natural selection as the observation that more individuals are produced than can a genetic process. Dobzhansky’s Genetics and the Origin of possibly survive. The most serious difficulty facing Darwin’s Species, published in 1937 (1), refashioned their formulations evolutionary theory was the lack of an adequate theory of in language that biologists could understand, dressed the inheritance that would account for the preservation through equations with natural history and experimental population the generations of the variations on which natural selection was genetics, and extended the synthesis to speciation and other supposed to act. Theories then current of ‘‘blending inheri- cardinal problems omitted by the mathematicians. tance’’ proposed that offspring merely struck an average The current Synthetic Theory has grown around that orig- between the characteristics of their parents. As Darwin be- inal synthesis. It is not just one single hypothesis (or theory) came aware, blending inheritance could not account for the with its corroborating evidence, but a multidisciplinary body of conservation of variations, because differences among variant knowledge bearing on biological evolution, an amalgam of offspring would be halved each generation, rapidly reducing well-established theories and working hypotheses, together the original variation to the average of the preexisting char- with the observations and experiments that support accepted acteristics. hypotheses (and falsify rejected ones), which jointly seek to The missing link in Darwin’s argument was provided by explain the evolutionary process and its outcomes. These Mendelian genetics. About the time the Origin of Species was hypotheses, observations, and experiments often originate in published, the Augustinian monk Gregor Mendel was per- disciplines such as genetics, embryology, zoology, botany, forming a long series of experiments with peas in the garden paleontology, and molecular biology. Currently, the ‘‘synthet- of his monastery in Bru¨nn, Austria-Hungary (now Brno, Czech ic’’ epithet is often omitted and the compilation of relevant Republic). Mendel’s paper, published in 1866, formulated the knowledge is simply known as the Theory of Evolution. This fundamental principles of a theory of heredity that accounts is still expanding, just like one of those ‘‘holding’’ business for biological inheritance through particulate factors (now corporations that have grown around an original enterprise, called ‘‘genes’’) inherited one from each parent, which do not but continue incorporating new profitable enterprises and mix or blend but segregate in the formation of the sex cells, or discarding unprofitable ones. gametes (3). Mendel’s discoveries, however, remained unknown to Dar- Darwin to Dobzhansky win and, indeed, did not become generally known until 1900, when they were simultaneously rediscovered by several scien- Darwin summarized the theory of evolution by natural selec- tists. In the meantime, Darwinism in the latter part of the 19th tion in the Origin of Species (2) as follows: century faced an alternative evolutionary theory known as ‘‘As many more individuals are produced than can neo-Lamarckism. This hypothesis shared with Lamarck’s orig- possibly survive, there must in every case be a struggle inal theory the importance of use and disuse in the develop- for existence, either one individual with another of the ment and obliteration of organs, and it added the notion that same species, or with the individuals of distinct species, the environment acts directly on organic structures, which or with the physical conditions of life....Canit,then, explained their adaptation to the ways of life and environments be thought improbable, seeing that variations useful to of each organism. Adherents of this theory rejected natural man have undoubtedly occurred, that other variations, selection as an explanation for adaptation to the environment. useful in some way to each being in the great and The rediscovery in 1900 of Mendel’s theory of heredity led complex battle of life, should sometimes occur in the to an emphasis on the role of heredity in evolution. In the course of thousands of generations? If such do occur, Netherlands, Hugo de Vries (4) proposed a new theory of can we doubt (remembering that many more individuals evolution known as mutationism, which essentially did away are born than can possibly survive) that individuals having any advantage, however slight, over others, would Abbreviation: MHC, major histocompatibility complex. *To whom reprint requests should be addressed at: Department of Ecology and Evolutionary Biology, University of California, 321 © 1997 by The National Academy of Sciences 0027-8424y97y947691-7$2.00y0 Steinhaus Hall, Irvine, CA 92697-2525. e-mail: FJAYALA@ PNAS is available online at http:yywww.pnas.org. UCI.EDU. 7691 Downloaded by guest on September 29, 2021 7692 Colloquium Paper: Ayala and Fitch Proc. Natl. Acad. Sci. USA 94 (1997) with natural selection as a major evolutionary process. Ac- different ways. First, the sequence of the evolutionary events cording to de Vries (joined by other geneticists such as William as they have actually taken place in the past history of various Bateson in England), there are two kinds of variation in organisms may be traced. Second, the mechanisms that bring organisms. One is the ‘‘ordinary’’ variation observed among about evolutionary changes may be studied.... Thepresent individuals of a species, which is of no lasting consequence in book is dedicated to a discussion of the mechanisms of species evolution because, according to de Vries, it could not ‘‘lead to formation in terms of the known facts and theories of genet- a transgression of the species border even under conditions of ics.’’ The book starts with a consideration of organic diversity the most stringent and continued selection.’’ The other consists and discontinuity. Successively, it deals with mutation as the of the changes brought about by mutations, spontaneous origin of hereditary variation, the role of chromosomal rear- alterations of genes that yield large modifications of the rangements, variation in natural populations, natural selection, organism and give rise to new species. According to de Vries, the origin of species by polyploidy, the origin of species through a new species originates suddenly, produced by the existing one gradual development of reproductive isolation, physiological without any visible preparation and without transition. and genetic differences between species, and the concept of Mutationism was opposed by many naturalists, and in species as natural units. The book’s organization was largely particular by the so-called biometricians, led by Briton Karl preserved in the second (1941) and third (1951) editions, and Pearson, who defended Darwinian natural selection as the in Genetics of the Evolutionary Process (14), published in 1970, major cause of evolution through the cumulative effects of a book that Dobzhansky thought of as the fourth edition of the small, continuous, individual variations (which the biometri- earlier one, but had changed too much for publication under cians assumed passed from one generation to the next without the same title. being subject to Mendel’s laws of inheritance). Dobzhansky sought to extend the evolutionary synthesis to The controversy between mutationists (also referred to at mankind in numerous articles and several books, most notably the time as Mendelians) and biometricians approached a Mankind Evolving (15), published in 1962, a book that many resolution in the 1920s and 1930s through the theoretical work judge to be as important as Genetics and the Origin of Species. of several geneticists (5). These geneticists used mathematical Dobzhansky was a leading experimentalist and prolific writer, arguments to show, first, that continuous variation (in such who published several books
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