- Email: [email protected]
What was the evolutionary synthesis?
TREE vol. 8, no. 1, January
tive
1993
Friedlander, I., eds). pp. 2 14-229, Peabody Museum, Cambridge 25 Rightmire, P. (1989) in The Human Revolution (Stringer, C. and Mellars, P., eds), pp. 109-l 22, Princeton University Press 26 Avise, J. (I 99 II Annu. Rev. Genet. 25, 2 l-44 27 Greenberg, J.H. (1963) The Languages of Africa, Indiana University Press 28 Ruhlen, M. ( I9921 in Evolution of Human Languages (Hawkins, J.A. and Cell-Mann, M.,
-
eds), pp. 159-189, Addison-Wesley 29 Sokal, R.R., Oden, N.L. and Thomson, B.A. ( 1992) Proc. Nat! Acad. Sci. USA 89, 7669-7673 30 Cavalli-Sforza, L.L., Piazza, A., Menozzi, P. and Mountain, 1. (1988) Proc. Nat/Acad. Sci. USA 85,6002-6006 31 Harding, R. and Sokal, R.R. (I 988) Proc. Nat/ Acad Sci. USA 85,9370-9372 32 Dolgopolsky, A.B. (I 989) in Reconstructing
Languages and Cultures (Shevoroshkin, V.. ed.), pp. 90-98, Brockmeyer 33 Ammerman, A.J. and Cavalli-Sforza, L.L ( 1984) The Neolithic Transition and Genetics of the Populations in Europe, Princeton University Press 34 Greenberg, 1.H. (1987) Language in the Americas, Stanford University Press 35 Green, R.C. II9891 Rec. Austral Mus. 4, 207-2 I3
What Was the EvolutionarySynthesis? There has nof been another scientific revolution that caused as much turmoil and dissension as the darwinian one. For ulmost 80 gears it was again and again pronounced to be a failure and to be totally refuted, and at least tGrree major alternatives were proposed to replace it. Yet, in the 193Os-I 940s tke opposing views were quicR/y and decisively refuted and a largely unified evolutionary theory emerged. tig and how fhis happened, however, is still rather controversial. Here I am comparing an excellent, thoroughly documented new analysis of the evolutionary synthesis by Betty Smocovitis’ with my own impressions, showing that two rather different interpretations are possible. Smocovitis studied with Will Provine, and she upholds his view of the importance of mathematics in biology. By contrast, I look at the synthesis as a naturalist and evolutionist in the tradition of Charles Darwin. It is quite fascinating how different the interpretation of the synthesis is as seen from these two very different viewpoints. The future will show which view is closer to the truth. There is no need to describe the chaotic state of evolutionary biology (a science which actually did not yet exist) prior to 1930. This has been done by the contributors to the Mayr and Provine volume2. Yet, initiated by the publication of Dobzhansky’s Genetics and the Origin of Specie&, most of the disagreements among the evolutionists disappeared in the next dozen years, documented by the publications of Huxley, Mayr, Simpson, Rensch and Stebbins. Ernst Mayr is at the Museum of Comparative Zoology, 26 Oxford Street, Harvard University, Cambridge, M A 02138, USA. El 1993, Elsewer
Science
Publishers
Lrd (UK)
Ernst Mayr Huxley called the happenings of this period the ‘evolutionary synthesis’, a designation that has frequently been questioned afterwards. I believe it indeed deserves this designation, but it was a movement that was rather more than a synthesis - a point that is clearly brought out by Smocovitis. It included, for instance, a convincing refutation of the three major antidarwinian paradigms - the typological-saltationist, the teleological- orthogenetic and the transformationist-lamarckian - and it was also a synthesis of the thinking of three major biological disciplines - genetics, systematics and paleontology. It was a synthesis between an experimental-reductionist philosophy (strongest among the geneticists) and an observationalholistic (strongest philosophy among the naturalists), and finally between an anglophone tradition with emphasis on mathematics and adaptation and a continental European tradition with emphasis on populations, species and higher taxa. Even though by 1950 the integration of the multiple differences was not yet fully completed, it had advanced sufficiently far that it could no longer be torn apart and the process of synthesis continued until the present. The rejection of the evolutionary theories that competed with darwinism was not due to the quantification of mathematical genetics, as believed by Smocovitis, but rather to the increasing demonstration that Weismann’s two great insights (reinforced by the rediscovery of the Mendelian laws), namely, that inheritance is hard (no environ-
mental influences) and that it is particulate (no blending inheritwere indeed valid. The ance), unimportance of mathematics in the synthesis is further demonstrated by the virtual absence of mathematics in the writings of three of the major architects of the synthesis, Rensch, Mayr and Stebbins. The greatest contribution made by the mathematical treatments was to reveal where the need was for good, hard data. The fact that Dobzhansky was the crucial initiator of the evolutionary synthesis does not necessarily mean that the synthesis was the work of genetics as has been claimed by some of the historians of genetics. There is no doubt as to the importance of the rediscovery of Mendel’s work in 1900. It was responsible for the founding of a new biological discipline - genetics. Yet, it was not an intellectual innovation, but only a continuation of the developments of the 1868-1899 period, particularly Weismann’s pioneering theoretical analysis. Even the term ‘gene’ was a shortening of Darwin’s term pangene. The crucial question one must ask is what actually permitted the occurrence of the synthesis? Here Smocovitis makes a claim with which I disagree quite profoundly. She says that the architects of the synthesis were able to serve as bridge builders ‘by adopting methodologies from the physical sciences to make evolution a more positive science’. Actually, the bridge builders were able to build bridges by pointing out the insufficiency of a purely experimental biology and by demonstrating the 31
TREE vol. 8, no. 7, January
failure of the strictly reductionist presentation of the material was so approach of the physicalists to chaotic. Qualified readers realized solve any of the problems at the that Huxley was not an expert in higher levels of biological inte- evolution and that he lacked the gration. The positivists were ability to organize his thought in maligning anything that was not the logical manner in which the strictly experimentalist. As is now story of evolution was presented so well understood, but was not by Dobzhansky, Mayr and in the 1920s one cannot solve Simpson. A teacher would have historical questions by experiment. found it impossible to use it as the In fact, the mechanistic-exper- basic text of a course. Did Richard Goldschmidt ‘threaten imental approach utterly failed to solve any of the problems relating to upset the emerging consensus to the origin of diversity. from within the evolutionary ranks’, Smocovitis gives us a splendid as claimed by Smocovitis? Not well-researched account of the con- in the least, in my opinion. tribution of anglophone authors to Goldschmidt rejoiced in being a the synthesis, but she mostly maverick and in proposing unorneglects the massive contribution thodox theories. Even though he to the synthesis made by continen- had a brilliant mind and perhaps tal European authors. What made a broader knowledge of biology, Dobzhansky such an important particularly experimental biology, actor in the synthesis was not his than any of his contemporaries, collaboration with Sewall Wright one must sadly concede that all of but rather his Russian background. his theories on evolution, gene His 1937 book was such a success action, sex and other aspects of precisely because of his emphasis biology are now considered failon subjects minimized or totally ures. Invariably, Goldschmidt was ignored in the contemporary anglo- so convinced of the correctness of phone literature. What Dobzhansky his own theories that he simply contributed was what he had swept under the rug all the evilearned from the Chetverikov dence refuting his ideas. His evolschool and from his experiences utionary thinking was transformas a beetle taxonomist. Having ationist, as one would expect from started life as a naturalist and his background in developmental later becoming a geneticist per- biology, and he never had the mitted Dobzhansky to produce a slightest understanding of popusynthesis between the views of the lations. The reason I took considernaturalists (those really studying able pains to refute him in my 1942 evolutionary phenomena) and the book5 was in order to prevent nongeneticists. It was he who taught taxonomic biologists from taking the members of both camps that Goldschmidt’s hopeful monster the basic beliefs of the other camp theories seriously. The argument were compatible with their own between, on one side Dobzhansky beliefs, and the other architects of and myself, and on the other side the synthesis widened the path Goldschmidt, was - Goldschmidt’s claims notwithstanding - not about which Dobzhansky had blazed. Smocovitis has some very inter- mechanism versus metaphysics but esting things to say about Iulian simply about the either typological Huxley, whose greatest contri- or populational explanation of conbution to the synthesis perhaps crete evolutionary phenomena. was that he coined the term ‘evolutionary synthesis’. Huxley was a What happened after the Synthesis? Historians (perhaps even Mayr developmental biologist but he had always had an immense and Provine’) have overemphainterest in evolution. His volume4 sized the unity achieved by the is full of brilliant insights and con- synthesis, To be sure, the antitains a more complete coverage of darwinians were so decisively deevolutionary biology than any feated that none of their theories other contemporary volume. Yet at retained any credibility. Furtherthe time it had comparatively little more, the differences between the impact - not owing to its inclusion experimentalists and naturalists of much progressionist and almost were greatly reduced, but honesty political thought but because the compels us to admit that conspicu32
1993
ous differences still remained. To begin with, evolution continued for the geneticists to be a change of gene frequencies, with the gene considered the target of selection, while for the naturalists, evolution was a series of processes resulting in adaptedness and diversity, with the individual being the target of selection. Population thinking, stressed to the utmost by the representatives of the new systematics, was still unable to make much headway in paleontology and, in a multipopulational sense, even in genetics. Geneticists almost invariably dealt with the processes taking place in a single closed gene pool. Being interested in the individual as a whole, the naturalists were particularly concerned with the genotype as a whole, including all of its epistatic interactions and all phenomena that indicate a certain ‘cohesion’ of the genotype, while the experimental geneticists concentrated on single genes and on additive inheritance, thus being unable to do justice to the bottleneck effects taking place in founder populations. As a result, the two camps also differed drastically in the evaluation of neutral evolution, that is the high frequency of base pair replacements that do not change the fitness of the phenotype. For the experimentalists, such neutral evolution is a very important evolutionary phenomenon, while for the naturalists it is little more than evolutionary ‘noise’. As far as the completeness of the synthesis is concerned, one must make a distinction between two aspects. The representatives of some biological disciplines, for instance, developmental biology, bitterly resisted the synthesis. They were not left out of the synthesis, as some of them now claim, but they simply did not want to join. Unquestionably, certain developmental aspects of evolution have therefore not yet been sufficiently analysed and explained. This is being actively repaired at the present time. A similar neglect is evident for the holistic aspects of the genotype and other biological problems. But there has also been an incompleteness of the synthesis with respect to the integration of the basic concepts of the exper-
TREE vol. 8, no. 1, January
7993
imentalists and the naturalists. Even today there are some geneticists who still act as if the gene was the only target of selection and this is the reason for their difficulties with the bottleneck effect of founder populations and with socalled neutral evolution. As is well known, Sewall Wright, alone among the mathematical geneticists, attributed much evolutionary change to stochastic processes (genetic drift). This was a result of his experiences when studying the genetics of small guinea pig laboratory populations. In this emphasis on genetic drift, he was at first followed by Dobzhansky and Simpson. By the late 1940s Wright, Dobzhansky and Simpson pulled back considerably from their previous strong emphasis on drift, a development referred to by Gould as the hardening of the synthesis. Smocovitis attributes this change to the progressionist frame of mind of the period. My own feeling is that this factor was not involved, but that the strengthening of selectionism was the inevitable consequence of the experience that one phenomenon after the other that had been attributed by Wright or Dobzhansky to drift could later be shown actually to have been the result of selection. In other words, it was due to an internal, not an external, causation. Smocovitis perceptively very points out that nearly all the architects of the evolutionary synthesis found that their scientific conclusions were suitable as the basis of a new liberal, progressive Weltanschauung. Huxley embodied this in his 1942 volume, while Dobzhansky6, Simpson’ and Stebbins expressed it in later books and other architects in various journal publications. Other architects of the synthesis eventually also wrote books or major essays on the role of man in this world and on man as the ultimate product of evolution. This endeavor was carried even further by some nonbiologists, with Teilhard de Chardin’s The Phenomenon of Man’ representing the extreme. Both Huxley and Dobzhansky praised this volume highly, while other evolutionists like G.G. Simpson and non-evolutionists like Medawar, criticized it .rnmercifully. Unquestionably, all endeavors to consider man the
almost logical endpoint of the ‘evolutionary stream’ had a considerable teleological flavor. There was no unity, in this respect, among the architects of the synthesis, with Simpson and Mayr clearly disagreeing with the teleological overtones of Huxley and Dobzhansky. Man is not explained by the achievements of the evolutionary synthesis; the evolution of man is permissible within the framework of darwinism, but it is not an inevitable consequence of it. Two questions have been asked repeatedly within the last score of years. First, were some of the theories adopted during the evolutionary synthesis erroneous? And secondly, to what extent was the synthesis incomplete? As far as the first question is concerned, the theory of neutral evolution, the punctuated equilibrium theory, and the attack on the adaptationist program are most frequently mentioned. As the subsequent discussions established, none of these three theories was actually in conflict with the synthesis. The neutral theory is clearly a product of the erroneous assumption of some geneticists that the gene is the target of selection. As soon as one returns to Darwin’s assumption that the individual as a whole is the target, the occurrence of neutral gene replacements is no longer in conflict with darwinism. Neither is the punctuated equilibrium theory, because Darwin already had realized how unequal rates of evolution can be, and he had been aware, particularly in his early work, of the evolutionary significance of isolated founder populations, and this has been confirmed by perceptive authors ever since. Finally, the occurrence of stochastic processes during the action of natural selection had been recognized long before the synthesis. If the individual as a whole is the target of selection, then there is no need to explain an adaptive significance of every aspect of the phenotype. The adaptationist program which, for that matter, preceded Darwin by several centuries is legitimate and highly heuristic, provided it is properly appliedg.
The unificationof biology Smocovitis entitles her essay ‘Unifying biology’. She is entirely
right when claiming that the evolutionary synthesis made a decisive contribution to the unification of biology. Yet, I am rather certain that this was not an objective in the minds of any of the architects of the synthesis during the 1930-l 940 period. They were busy enough straightening out their own differences and refuting the antidarwinians to have time for such a farreaching objective. It wasn’t until the 1950s when most of the previous difficulties had been resolved that one could begin to think seriously about the role of evolutionary biology in the whole of biology and about the capacity of evolutionary biology to achieve a unification of the previously badly splintered biology. Great as the contribution to the goal of unification made by the synthesis was, a complete unification was not achieved. This is made particularly evident by the early endeavors of molecular biologists to eliminate organismic biology from biology departments. George Wald’s (published) claim ‘there is only one biology, and it is molecular biology’ was taken seriously at a number of universities where the molecular biologists had achieved majority. They entirely eliminated the subject matter of organismic biology from the curriculum at these institutions. This happened during the early period of molecular biology (in the late 1950s and early 1960s) when so-called molecular biologists were actually biochemists, most of them physically located in chemistry departments. Naturally, they had little understanding of biology and were quite intolerant of real biology. In due time, molecular biology changed from biochemistry into a genuine branch of biology and this intolerance largely disappeared. At the present time there is perhaps more interest in evolution among molecular biologists than in any non-strictly other evolutionary branch of biology. Molecular biologists have discovered that every molecule has an evolutionary history; that one can establish phylogenies of molecules; and that the study of such phylogenies must use methods analogous to those of comparative anatomy. Hence, the rise of molecular biology has not. in the long run, prevented the unification
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TREE vol. 8, no. 7, January
of biology. In fact, it has strengthened it. No one interested in the history of evolutionary biology can afford to ignore the splendid &ralysis of the evolutionary synthesis presented by Smocovitis. Hers is an extremely well-researched documentation of the happenings of that period and of the specific contributions made by various leaders in this move-
Letters
ment. Even though 1 sometimes disagree with her interpretations, it is nevertheless a most important contribution to the history of that period. It should be read- by every one interested in this history.
References I Smocovitis, V.B. (1992) /. Hist. Biol. 25, l-65 2 Mayr, E. and Provine, W., eds f 1980) The Evolutionary Synthesis, Harvard University Press
1993
3 Dobzhansky, T. (I 937) Genetics and the Origin ofspecies, Columbia University Press 4 Huxley, j. (1942) Evolution: The Modem Svnthesis. George Allen E- Unwin 5 .Mayr, E. ( 19423 Systematics and the Origin ofspecies, Columbia University Press 6 Dobzhansky, T. (I 962) Mankind Evolving, Yale Universitv Press 7 Simpson. C.C. (1944) Tempo and Mode in Evo/u&on, Columbia University Press 8 Teilhard de Chardin, P. (1959) The Phenomenon of Man, Harper 9 Mayr, E. (1983) Am. Nat. 3,324-334
to the Editor Plant Phenology:Selection and Neutrality In their recent TREE article, Ollerton and Lack’ argue that much of the variation in plant phenology is selectively neutral. We are concerned with the argument used to support this conclusion. (I) Oller-ton and Lack equate selection with selection response: if a trait is far from optimal, they argue, it must not be subject to selection. However, departures from optima can be caused by variable selection2*3, environmental effectsG7, lack of genetic variation*, genetic cy;rfilations8,‘, frequency dependence ’ , maternal effects’2”3, and epistasis”. Thus, neutrality hypotheses cannot be tested by noting departures from putative optima. (2) Ollerton and Lack confuse the strength of selection with its evolutionary importance: unless selection on phenology is strong, they hold, it must not be an important evolutionary factor. Fisher and others demonstrated’4,‘5 decades ago that very small selective differences can cause evolutionary change over time. Theoretical studies on flowering time variation in annual plants have shown fitness consequences under general conditions’& ‘. This selection may often be weak”,“. As Ollerton and Lack note, many studies have shown genetically based flowering time variation corresponding with climatic gradients”,‘* (see Ref. 6 for earlier citations). These provide strong evidence that selection sometimes acts on phenology, and populations sometimes respond. (3) Noting a tendency for related species to have similar mean flowering times, Ollerton and Lack contend that this reflects biological constraints on selection response, which they equate with a lack of selection. But taxonomic correlations can result from selection. New species are always likely to resemble their ances-
34
tors23. The stronger the selection on a trait, the greater the advantage for new species that do not have to change to persist. Speciation is especially likely to outpace character evolution when: (a) there is little genetic variation in the trait (expected as a consequence of selection15); or (b) selection is strong in the new species, disallowing time for evolutionary change. Such selective explanations have been proposed for the limited variation in seed size at lower taxonomic levels24*25. Observing that most Asteraceae flower late in the year, Ollerton and Lack conclude that this is a ‘fundamentally late flowering family” such that few Asteraceae can evolve early flowering times. This involves two logical errors: taxonomic (a) correlations need not imply constraints on selection response; and (b) selection and constraint are not mutually exclusive explanations for a lack of variation in lower taxonomic levels. If selection eliminates genetic variation, a species is ‘constrained’. Such constraints mean only that populations cannot now respond to selection. (4) Ollerton and Lack argue that usually favors precise selection flowering synchrony within populations, and assert that ‘There may be advantages associated with flowering synchrony, but if precise synchrony in flowering is really rare, it suggests to us that the flowering phenology of most species is not Other strong selection.” under explanations are equally reasonable. It is possible that selection favors synchrony, but few populations achieve it. Alternatively, synchrony may only rarely be adaptive. Several advantages to asynchrony have been hypothesized by studies that Ollerton and Lack cite. Discriminating between explanations
for asynchrony - adaptive and neutral - requires data on the fitness consequences of plant phenology. Hypotheses of neutrality should be actively supported. Experimentally, one could demonstrate that variation in the trait does not generate variation in fitness26. Statistically, one could show that the trait varies as a consequence of variation in another, selectively important traitz3. We do not argue that variation in flowering phenology is always adaptive, but the arguments of Ollerton and Lack are unconvincing. There are techniques that could test the neutrality hypothesis26; unfortunately, Olletton and Lack did not use them. We recommend that these techniques be applied before drawing such conclusions. Acknowledgement
We thank cussion.
Paul
Harvey
for
dis-
Gordon A. Fox Dept of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA
Colleen K. Kelly Oept of Biological Sciences, University of North Texas, Denton. TX 76203, USA References 1 Ollerton, J. and Lack, A.J. (1992) Trends Ecol. Evol. 7. 274-276 2 Gillespie, J.H. (1973) Am. Nat. 108, 145-151 3 Turelli, M. (1987) in Proceedings of the Second international Conference on Quantitative Genetics (Weir, B.S., Eisen, E.J., Goodman, M.M. and Namkoong. G.,
eds), pp. 601-618, Sinauer 4 Best, K.F. and Mclnn/re, G.I. (1972) Bot. Gaz. 133,454-459 5 Murfet, I.C. (1977) Annu. Rev. Plant Physiol. 28, 253-278 6 Fox, G.A. (1989) Ecology70, 1294-1306
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Friedlander, I., eds). pp. 2 14-229, Peabody Museum, Cambridge 25 Rightmire, P. (1989) in The Human Revolution (Stringer, C. and Mellars, P., eds), pp. 109-l 22, Princeton University Press 26 Avise, J. (I 99 II Annu. Rev. Genet. 25, 2 l-44 27 Greenberg, J.H. (1963) The Languages of Africa, Indiana University Press 28 Ruhlen, M. ( I9921 in Evolution of Human Languages (Hawkins, J.A. and Cell-Mann, M.,
-
eds), pp. 159-189, Addison-Wesley 29 Sokal, R.R., Oden, N.L. and Thomson, B.A. ( 1992) Proc. Nat! Acad. Sci. USA 89, 7669-7673 30 Cavalli-Sforza, L.L., Piazza, A., Menozzi, P. and Mountain, 1. (1988) Proc. Nat/Acad. Sci. USA 85,6002-6006 31 Harding, R. and Sokal, R.R. (I 988) Proc. Nat/ Acad Sci. USA 85,9370-9372 32 Dolgopolsky, A.B. (I 989) in Reconstructing
Languages and Cultures (Shevoroshkin, V.. ed.), pp. 90-98, Brockmeyer 33 Ammerman, A.J. and Cavalli-Sforza, L.L ( 1984) The Neolithic Transition and Genetics of the Populations in Europe, Princeton University Press 34 Greenberg, 1.H. (1987) Language in the Americas, Stanford University Press 35 Green, R.C. II9891 Rec. Austral Mus. 4, 207-2 I3
What Was the EvolutionarySynthesis? There has nof been another scientific revolution that caused as much turmoil and dissension as the darwinian one. For ulmost 80 gears it was again and again pronounced to be a failure and to be totally refuted, and at least tGrree major alternatives were proposed to replace it. Yet, in the 193Os-I 940s tke opposing views were quicR/y and decisively refuted and a largely unified evolutionary theory emerged. tig and how fhis happened, however, is still rather controversial. Here I am comparing an excellent, thoroughly documented new analysis of the evolutionary synthesis by Betty Smocovitis’ with my own impressions, showing that two rather different interpretations are possible. Smocovitis studied with Will Provine, and she upholds his view of the importance of mathematics in biology. By contrast, I look at the synthesis as a naturalist and evolutionist in the tradition of Charles Darwin. It is quite fascinating how different the interpretation of the synthesis is as seen from these two very different viewpoints. The future will show which view is closer to the truth. There is no need to describe the chaotic state of evolutionary biology (a science which actually did not yet exist) prior to 1930. This has been done by the contributors to the Mayr and Provine volume2. Yet, initiated by the publication of Dobzhansky’s Genetics and the Origin of Specie&, most of the disagreements among the evolutionists disappeared in the next dozen years, documented by the publications of Huxley, Mayr, Simpson, Rensch and Stebbins. Ernst Mayr is at the Museum of Comparative Zoology, 26 Oxford Street, Harvard University, Cambridge, M A 02138, USA. El 1993, Elsewer
Science
Publishers
Lrd (UK)
Ernst Mayr Huxley called the happenings of this period the ‘evolutionary synthesis’, a designation that has frequently been questioned afterwards. I believe it indeed deserves this designation, but it was a movement that was rather more than a synthesis - a point that is clearly brought out by Smocovitis. It included, for instance, a convincing refutation of the three major antidarwinian paradigms - the typological-saltationist, the teleological- orthogenetic and the transformationist-lamarckian - and it was also a synthesis of the thinking of three major biological disciplines - genetics, systematics and paleontology. It was a synthesis between an experimental-reductionist philosophy (strongest among the geneticists) and an observationalholistic (strongest philosophy among the naturalists), and finally between an anglophone tradition with emphasis on mathematics and adaptation and a continental European tradition with emphasis on populations, species and higher taxa. Even though by 1950 the integration of the multiple differences was not yet fully completed, it had advanced sufficiently far that it could no longer be torn apart and the process of synthesis continued until the present. The rejection of the evolutionary theories that competed with darwinism was not due to the quantification of mathematical genetics, as believed by Smocovitis, but rather to the increasing demonstration that Weismann’s two great insights (reinforced by the rediscovery of the Mendelian laws), namely, that inheritance is hard (no environ-
mental influences) and that it is particulate (no blending inheritwere indeed valid. The ance), unimportance of mathematics in the synthesis is further demonstrated by the virtual absence of mathematics in the writings of three of the major architects of the synthesis, Rensch, Mayr and Stebbins. The greatest contribution made by the mathematical treatments was to reveal where the need was for good, hard data. The fact that Dobzhansky was the crucial initiator of the evolutionary synthesis does not necessarily mean that the synthesis was the work of genetics as has been claimed by some of the historians of genetics. There is no doubt as to the importance of the rediscovery of Mendel’s work in 1900. It was responsible for the founding of a new biological discipline - genetics. Yet, it was not an intellectual innovation, but only a continuation of the developments of the 1868-1899 period, particularly Weismann’s pioneering theoretical analysis. Even the term ‘gene’ was a shortening of Darwin’s term pangene. The crucial question one must ask is what actually permitted the occurrence of the synthesis? Here Smocovitis makes a claim with which I disagree quite profoundly. She says that the architects of the synthesis were able to serve as bridge builders ‘by adopting methodologies from the physical sciences to make evolution a more positive science’. Actually, the bridge builders were able to build bridges by pointing out the insufficiency of a purely experimental biology and by demonstrating the 31
TREE vol. 8, no. 7, January
failure of the strictly reductionist presentation of the material was so approach of the physicalists to chaotic. Qualified readers realized solve any of the problems at the that Huxley was not an expert in higher levels of biological inte- evolution and that he lacked the gration. The positivists were ability to organize his thought in maligning anything that was not the logical manner in which the strictly experimentalist. As is now story of evolution was presented so well understood, but was not by Dobzhansky, Mayr and in the 1920s one cannot solve Simpson. A teacher would have historical questions by experiment. found it impossible to use it as the In fact, the mechanistic-exper- basic text of a course. Did Richard Goldschmidt ‘threaten imental approach utterly failed to solve any of the problems relating to upset the emerging consensus to the origin of diversity. from within the evolutionary ranks’, Smocovitis gives us a splendid as claimed by Smocovitis? Not well-researched account of the con- in the least, in my opinion. tribution of anglophone authors to Goldschmidt rejoiced in being a the synthesis, but she mostly maverick and in proposing unorneglects the massive contribution thodox theories. Even though he to the synthesis made by continen- had a brilliant mind and perhaps tal European authors. What made a broader knowledge of biology, Dobzhansky such an important particularly experimental biology, actor in the synthesis was not his than any of his contemporaries, collaboration with Sewall Wright one must sadly concede that all of but rather his Russian background. his theories on evolution, gene His 1937 book was such a success action, sex and other aspects of precisely because of his emphasis biology are now considered failon subjects minimized or totally ures. Invariably, Goldschmidt was ignored in the contemporary anglo- so convinced of the correctness of phone literature. What Dobzhansky his own theories that he simply contributed was what he had swept under the rug all the evilearned from the Chetverikov dence refuting his ideas. His evolschool and from his experiences utionary thinking was transformas a beetle taxonomist. Having ationist, as one would expect from started life as a naturalist and his background in developmental later becoming a geneticist per- biology, and he never had the mitted Dobzhansky to produce a slightest understanding of popusynthesis between the views of the lations. The reason I took considernaturalists (those really studying able pains to refute him in my 1942 evolutionary phenomena) and the book5 was in order to prevent nongeneticists. It was he who taught taxonomic biologists from taking the members of both camps that Goldschmidt’s hopeful monster the basic beliefs of the other camp theories seriously. The argument were compatible with their own between, on one side Dobzhansky beliefs, and the other architects of and myself, and on the other side the synthesis widened the path Goldschmidt, was - Goldschmidt’s claims notwithstanding - not about which Dobzhansky had blazed. Smocovitis has some very inter- mechanism versus metaphysics but esting things to say about Iulian simply about the either typological Huxley, whose greatest contri- or populational explanation of conbution to the synthesis perhaps crete evolutionary phenomena. was that he coined the term ‘evolutionary synthesis’. Huxley was a What happened after the Synthesis? Historians (perhaps even Mayr developmental biologist but he had always had an immense and Provine’) have overemphainterest in evolution. His volume4 sized the unity achieved by the is full of brilliant insights and con- synthesis, To be sure, the antitains a more complete coverage of darwinians were so decisively deevolutionary biology than any feated that none of their theories other contemporary volume. Yet at retained any credibility. Furtherthe time it had comparatively little more, the differences between the impact - not owing to its inclusion experimentalists and naturalists of much progressionist and almost were greatly reduced, but honesty political thought but because the compels us to admit that conspicu32
1993
ous differences still remained. To begin with, evolution continued for the geneticists to be a change of gene frequencies, with the gene considered the target of selection, while for the naturalists, evolution was a series of processes resulting in adaptedness and diversity, with the individual being the target of selection. Population thinking, stressed to the utmost by the representatives of the new systematics, was still unable to make much headway in paleontology and, in a multipopulational sense, even in genetics. Geneticists almost invariably dealt with the processes taking place in a single closed gene pool. Being interested in the individual as a whole, the naturalists were particularly concerned with the genotype as a whole, including all of its epistatic interactions and all phenomena that indicate a certain ‘cohesion’ of the genotype, while the experimental geneticists concentrated on single genes and on additive inheritance, thus being unable to do justice to the bottleneck effects taking place in founder populations. As a result, the two camps also differed drastically in the evaluation of neutral evolution, that is the high frequency of base pair replacements that do not change the fitness of the phenotype. For the experimentalists, such neutral evolution is a very important evolutionary phenomenon, while for the naturalists it is little more than evolutionary ‘noise’. As far as the completeness of the synthesis is concerned, one must make a distinction between two aspects. The representatives of some biological disciplines, for instance, developmental biology, bitterly resisted the synthesis. They were not left out of the synthesis, as some of them now claim, but they simply did not want to join. Unquestionably, certain developmental aspects of evolution have therefore not yet been sufficiently analysed and explained. This is being actively repaired at the present time. A similar neglect is evident for the holistic aspects of the genotype and other biological problems. But there has also been an incompleteness of the synthesis with respect to the integration of the basic concepts of the exper-
TREE vol. 8, no. 1, January
7993
imentalists and the naturalists. Even today there are some geneticists who still act as if the gene was the only target of selection and this is the reason for their difficulties with the bottleneck effect of founder populations and with socalled neutral evolution. As is well known, Sewall Wright, alone among the mathematical geneticists, attributed much evolutionary change to stochastic processes (genetic drift). This was a result of his experiences when studying the genetics of small guinea pig laboratory populations. In this emphasis on genetic drift, he was at first followed by Dobzhansky and Simpson. By the late 1940s Wright, Dobzhansky and Simpson pulled back considerably from their previous strong emphasis on drift, a development referred to by Gould as the hardening of the synthesis. Smocovitis attributes this change to the progressionist frame of mind of the period. My own feeling is that this factor was not involved, but that the strengthening of selectionism was the inevitable consequence of the experience that one phenomenon after the other that had been attributed by Wright or Dobzhansky to drift could later be shown actually to have been the result of selection. In other words, it was due to an internal, not an external, causation. Smocovitis perceptively very points out that nearly all the architects of the evolutionary synthesis found that their scientific conclusions were suitable as the basis of a new liberal, progressive Weltanschauung. Huxley embodied this in his 1942 volume, while Dobzhansky6, Simpson’ and Stebbins expressed it in later books and other architects in various journal publications. Other architects of the synthesis eventually also wrote books or major essays on the role of man in this world and on man as the ultimate product of evolution. This endeavor was carried even further by some nonbiologists, with Teilhard de Chardin’s The Phenomenon of Man’ representing the extreme. Both Huxley and Dobzhansky praised this volume highly, while other evolutionists like G.G. Simpson and non-evolutionists like Medawar, criticized it .rnmercifully. Unquestionably, all endeavors to consider man the
almost logical endpoint of the ‘evolutionary stream’ had a considerable teleological flavor. There was no unity, in this respect, among the architects of the synthesis, with Simpson and Mayr clearly disagreeing with the teleological overtones of Huxley and Dobzhansky. Man is not explained by the achievements of the evolutionary synthesis; the evolution of man is permissible within the framework of darwinism, but it is not an inevitable consequence of it. Two questions have been asked repeatedly within the last score of years. First, were some of the theories adopted during the evolutionary synthesis erroneous? And secondly, to what extent was the synthesis incomplete? As far as the first question is concerned, the theory of neutral evolution, the punctuated equilibrium theory, and the attack on the adaptationist program are most frequently mentioned. As the subsequent discussions established, none of these three theories was actually in conflict with the synthesis. The neutral theory is clearly a product of the erroneous assumption of some geneticists that the gene is the target of selection. As soon as one returns to Darwin’s assumption that the individual as a whole is the target, the occurrence of neutral gene replacements is no longer in conflict with darwinism. Neither is the punctuated equilibrium theory, because Darwin already had realized how unequal rates of evolution can be, and he had been aware, particularly in his early work, of the evolutionary significance of isolated founder populations, and this has been confirmed by perceptive authors ever since. Finally, the occurrence of stochastic processes during the action of natural selection had been recognized long before the synthesis. If the individual as a whole is the target of selection, then there is no need to explain an adaptive significance of every aspect of the phenotype. The adaptationist program which, for that matter, preceded Darwin by several centuries is legitimate and highly heuristic, provided it is properly appliedg.
The unificationof biology Smocovitis entitles her essay ‘Unifying biology’. She is entirely
right when claiming that the evolutionary synthesis made a decisive contribution to the unification of biology. Yet, I am rather certain that this was not an objective in the minds of any of the architects of the synthesis during the 1930-l 940 period. They were busy enough straightening out their own differences and refuting the antidarwinians to have time for such a farreaching objective. It wasn’t until the 1950s when most of the previous difficulties had been resolved that one could begin to think seriously about the role of evolutionary biology in the whole of biology and about the capacity of evolutionary biology to achieve a unification of the previously badly splintered biology. Great as the contribution to the goal of unification made by the synthesis was, a complete unification was not achieved. This is made particularly evident by the early endeavors of molecular biologists to eliminate organismic biology from biology departments. George Wald’s (published) claim ‘there is only one biology, and it is molecular biology’ was taken seriously at a number of universities where the molecular biologists had achieved majority. They entirely eliminated the subject matter of organismic biology from the curriculum at these institutions. This happened during the early period of molecular biology (in the late 1950s and early 1960s) when so-called molecular biologists were actually biochemists, most of them physically located in chemistry departments. Naturally, they had little understanding of biology and were quite intolerant of real biology. In due time, molecular biology changed from biochemistry into a genuine branch of biology and this intolerance largely disappeared. At the present time there is perhaps more interest in evolution among molecular biologists than in any non-strictly other evolutionary branch of biology. Molecular biologists have discovered that every molecule has an evolutionary history; that one can establish phylogenies of molecules; and that the study of such phylogenies must use methods analogous to those of comparative anatomy. Hence, the rise of molecular biology has not. in the long run, prevented the unification
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of biology. In fact, it has strengthened it. No one interested in the history of evolutionary biology can afford to ignore the splendid &ralysis of the evolutionary synthesis presented by Smocovitis. Hers is an extremely well-researched documentation of the happenings of that period and of the specific contributions made by various leaders in this move-
Letters
ment. Even though 1 sometimes disagree with her interpretations, it is nevertheless a most important contribution to the history of that period. It should be read- by every one interested in this history.
References I Smocovitis, V.B. (1992) /. Hist. Biol. 25, l-65 2 Mayr, E. and Provine, W., eds f 1980) The Evolutionary Synthesis, Harvard University Press
1993
3 Dobzhansky, T. (I 937) Genetics and the Origin ofspecies, Columbia University Press 4 Huxley, j. (1942) Evolution: The Modem Svnthesis. George Allen E- Unwin 5 .Mayr, E. ( 19423 Systematics and the Origin ofspecies, Columbia University Press 6 Dobzhansky, T. (I 962) Mankind Evolving, Yale Universitv Press 7 Simpson. C.C. (1944) Tempo and Mode in Evo/u&on, Columbia University Press 8 Teilhard de Chardin, P. (1959) The Phenomenon of Man, Harper 9 Mayr, E. (1983) Am. Nat. 3,324-334
to the Editor Plant Phenology:Selection and Neutrality In their recent TREE article, Ollerton and Lack’ argue that much of the variation in plant phenology is selectively neutral. We are concerned with the argument used to support this conclusion. (I) Oller-ton and Lack equate selection with selection response: if a trait is far from optimal, they argue, it must not be subject to selection. However, departures from optima can be caused by variable selection2*3, environmental effectsG7, lack of genetic variation*, genetic cy;rfilations8,‘, frequency dependence ’ , maternal effects’2”3, and epistasis”. Thus, neutrality hypotheses cannot be tested by noting departures from putative optima. (2) Ollerton and Lack confuse the strength of selection with its evolutionary importance: unless selection on phenology is strong, they hold, it must not be an important evolutionary factor. Fisher and others demonstrated’4,‘5 decades ago that very small selective differences can cause evolutionary change over time. Theoretical studies on flowering time variation in annual plants have shown fitness consequences under general conditions’& ‘. This selection may often be weak”,“. As Ollerton and Lack note, many studies have shown genetically based flowering time variation corresponding with climatic gradients”,‘* (see Ref. 6 for earlier citations). These provide strong evidence that selection sometimes acts on phenology, and populations sometimes respond. (3) Noting a tendency for related species to have similar mean flowering times, Ollerton and Lack contend that this reflects biological constraints on selection response, which they equate with a lack of selection. But taxonomic correlations can result from selection. New species are always likely to resemble their ances-
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tors23. The stronger the selection on a trait, the greater the advantage for new species that do not have to change to persist. Speciation is especially likely to outpace character evolution when: (a) there is little genetic variation in the trait (expected as a consequence of selection15); or (b) selection is strong in the new species, disallowing time for evolutionary change. Such selective explanations have been proposed for the limited variation in seed size at lower taxonomic levels24*25. Observing that most Asteraceae flower late in the year, Ollerton and Lack conclude that this is a ‘fundamentally late flowering family” such that few Asteraceae can evolve early flowering times. This involves two logical errors: taxonomic (a) correlations need not imply constraints on selection response; and (b) selection and constraint are not mutually exclusive explanations for a lack of variation in lower taxonomic levels. If selection eliminates genetic variation, a species is ‘constrained’. Such constraints mean only that populations cannot now respond to selection. (4) Ollerton and Lack argue that usually favors precise selection flowering synchrony within populations, and assert that ‘There may be advantages associated with flowering synchrony, but if precise synchrony in flowering is really rare, it suggests to us that the flowering phenology of most species is not Other strong selection.” under explanations are equally reasonable. It is possible that selection favors synchrony, but few populations achieve it. Alternatively, synchrony may only rarely be adaptive. Several advantages to asynchrony have been hypothesized by studies that Ollerton and Lack cite. Discriminating between explanations
for asynchrony - adaptive and neutral - requires data on the fitness consequences of plant phenology. Hypotheses of neutrality should be actively supported. Experimentally, one could demonstrate that variation in the trait does not generate variation in fitness26. Statistically, one could show that the trait varies as a consequence of variation in another, selectively important traitz3. We do not argue that variation in flowering phenology is always adaptive, but the arguments of Ollerton and Lack are unconvincing. There are techniques that could test the neutrality hypothesis26; unfortunately, Olletton and Lack did not use them. We recommend that these techniques be applied before drawing such conclusions. Acknowledgement
We thank cussion.
Paul
Harvey
for
dis-
Gordon A. Fox Dept of Ecology and Evolutionary Biology, University of Arizona, Tucson, AZ 85721, USA
Colleen K. Kelly Oept of Biological Sciences, University of North Texas, Denton. TX 76203, USA References 1 Ollerton, J. and Lack, A.J. (1992) Trends Ecol. Evol. 7. 274-276 2 Gillespie, J.H. (1973) Am. Nat. 108, 145-151 3 Turelli, M. (1987) in Proceedings of the Second international Conference on Quantitative Genetics (Weir, B.S., Eisen, E.J., Goodman, M.M. and Namkoong. G.,
eds), pp. 601-618, Sinauer 4 Best, K.F. and Mclnn/re, G.I. (1972) Bot. Gaz. 133,454-459 5 Murfet, I.C. (1977) Annu. Rev. Plant Physiol. 28, 253-278 6 Fox, G.A. (1989) Ecology70, 1294-1306