Ryuichi Matsuda

Animal Evolution in Changing Environments, with Special Reference to Abnormal Metamorphosis: Bibliographical Excerpts

"Despite some apparent exceptions, it now has to be concluded that an environmentally modified phenotype could become heritable through the process of genetic assimilation, remaining at phase 1 or 2, or 3 or the latter. As I (Matsuda 1982) have discussed, the widely held belief that environmentally modified phenotypes are not heritable (and hence without evolutionary future) is misleading and it must be dismissed. The reason for the prevalence of this belief appears to have been a series of proposals and discoveries of important biological concepts that have confused biologists. Most prominently, the so-called Weismann theory was in accord with the idea of impossibility of inheritance of externally induced phenotypic changes. The theory states that only the germ plasm is continued from generation to generation, and therefore somatic (somatogenic of Weismann) modifications acquired during development by external influence cannot affect the germ plasm, and hence cannot be inherited. Against the possibility of transmission of somatic modification to the germ plasm, Weismann (1892, p. 393) asserted "we should have to assume the presence in all parts of the body a definite track along which somatic variation might be transferred back to the germ cells, in the germ plasm of which it would produce a corresponding change." This assertion was consistent with the Mendelian law of heredity that was discovered soon after, and the two theories together contributed to the development of neo-Darwinism, in which the external (environmental) influence on development is irrelevant to evolution. Further, Weismann's theory was also consistent with the central dogma of modern molecular genetics in which the relationship between the genotype and phenotype (i.e., the DNA to RNA to protein to phenotype sequence) is unidirectional and there is no mechanism by which the process could be reversed, and later repudiations of the "inheritance of acquired characters" (Dobzhansky 1970, Mahr 1976, Ayalo 1977) were based on this dogma. However, in these repudiations, as Matsuda (1982) pointed out, no distinction was made between the kinds of external agents causing modifications. In this connection, it is very important to point out here that Weismann (1892) actually recognized two kinds of somatogenic variations, namely, injuries and functional variations, and the variations depending on the so-called "influence of environment" which included mainly climatic variations. As his discussion shows, his refutation of the "inheritance of acquired characters" applied to the first two categories only. As this work abundantly shows, environmentally acquired characters can become heritable through the process of genetic assimilation, without requiring the reversal of genetic transcription and translation. Weismann found, with regard to the climatic influence, that when the pupae of the German form of a lycaenid butterfly Polymmatus phlaeas was exposed to much higher temperatures, none of the emerged adults resembled the darkest form of southern variety eleus. Further, a reverse experiment was made by subjecting caterpillars of the Naples form to very low temperature in rearing. The result was that none was as light colored as the ordinary German form. From these results Weismann concluded that German and Naples forms are constitutionally (genetically) distinct. Weismann (1892, p.401) said, 'A somatogenic character is not inherited in this case, but the modifying influence--temperature--affects the primary constituents of the wings in each individual, i.e. a part of the soma--as well as germplasm contained in the germ of animals.' Weismann (1892, p. 405) even went so far so to say, "In many animals and plants influences of temperature and environment may very possibly produce hereditary variations." Thus contrary to the prevailing belief, Weismann was a neo-Lamarckist, as Darwin was (1972, p. v.). In 1904 Weismann again referred to P. phlaeas in the same context, although he also referred to cases in which environmental impacts such as nutrition and climatic factors have not affected the germ plasm (e.g., alpine plants, plant galls). In fact, Weismann's theory as a whole was not inconsistent with the Baldwin effect (discussed in Chap. 5). However, what happened later was that his general statement of refutation of the inheritance of acquired characters alone was taken seriously, and it provided a strong theoretical basis for the development of neo-Darwinism." (Matsuda, Ryuichi (1987) Animal Evolution in Changing Environments, with Special Reference to Abnormal Metamorphosis. N.Y.: Wiley Press pp.40-41)

"It has now become clear that neo-Lamarckism has always been a reasonable theory, and it has stood the test of time for more than a century. Once some misunderstandings and inhibitions are removed, the theory can be regarded as a more complete theory (than neo-Darwinism) in that it analyses the evolutionary process in terms of both the proximate and ultimate mechanisms, and in that it is especially suited for analyzing the origin of macroevolutionary change. Through the analysis of the proximate process we come to know the cause of variation and the presumed initial stage of evolution of the structures upon which natural selection has worked. In traditional neo-Darwinism natural selection is considered to be involved throughout the whole evolutionary process (of structures), which is indeed untrue, as Mivart (1871) already knew. In practice obvious cases of overextension of the theory of natural selection, which actually results from neglect of the proximate process, have often been criticized in terms of their falsifiability. Yet the critics have never offered a solution for this dilemma. Indeed, evolutionary biology has been in a state of constipation caused by the neo-Darwinian constraint that inhibits exploration of the proximate process of evolution. It should now be realized that such a worry will be over once we accept the neo-Lamarckian approach. The application of the neo-Lamarkian analysis appears to resolve some outstanding problems and riddles in evolutionary biology. For instance, the problem of "inheritance of acquired characters" is now understood as the result of accumulation of genocopies. The age-old riddle of "Which came first, the chicken or the egg?" can now be answered from the evolutionary viewpoint (Sect. 3B2). "Adaptive response" now must be restored as a fundamental evolutionary concept, though it has been neglected. All phenomena of abnormal metamorphosis (halmatomorphosis, neoteny, caenogenesis) resulting in macroevolutionary structural changes are now attributed primarily to environmentally induced alteration in the response of the genotype (alteration in gene regulation) during the proximate process. The study of the Badwin effect as special cases of genetic assimilation must be encouraged. It should be realized that all the above problems can be more clearly understood by inquiring into the hormonal mediation that becomes involved. Indeed, the environmentally induced hormonal intervention controlling gene action was the mechanism that was unknown to the nineteenth century neo-Lamarckists, and the lack of knowledge of such a mechanism might have hindered the acceptance of neo-Lamarckism." (Matsuda, Ryuichi (1987) Animal Evolution in Changing Environments, with Special Reference to Abnormal Metamorphosis. N.Y.: Wiley Press pp.53)

[locusts] "Effects of other environmental factors (such as photoperiod, temperature, nutrition, and humidity) on development and reproduction have been known for a long time (see Mordue et al. 1970, Joly 1972 for reviews of earlier works). Among more recent studies, Albrecht and Lauga (1978) showed that increasing day length and high temperatures have a solitarizing effect in gregarious Schistocerca. Some studies show the direct effect of environmental changes on hormonal activity, which results in the change in development and reproduction. (Matsuda, Ryuichi (1987) Animal Evolution in Changing Environments, with Special Reference to Abnormal Metamorphosis. N.Y.: Wiley Press pp.172)

Some species of crickets (Gryllus, Acheta, Gryllodes, etc.) are known to be polymorphic with respect to wing development, both in laboratory experiments and in field observations. Effects of various environmental factors (photoperiod, temperature, population density, food) on wing development have been studied in laboratories. In Gryllodes sigillatus from Canada, which is micropterous in both sexes, Ghouri and McFarlane (1958) found that the optimal level (for both growth and wing development) is 20% protein in the food. They failed to see the group effect in producing macroptery (probably because of the unfavorable photoperiod). Mathad and McFarlane (1968) found that the exposure of the nymphs to a 10-hr photoperiod suppresses wing development completely, and that a 14-hr exposure is optimal for wing development. They found further that adults exposed to a 14-hr photoperiod produce more winged progeny than adults exposed to an 18-hr photoperiod. In the same species from Japan, however, Arai (1978) found that the macropterous form appears even in the isolated condition. He showed various photoperiodic effects at different temperatures. Thus all three factors, photoperiod, temperature, and population density influence wing development in Gryllodes sigillatus. Of these, photoperiod appears to be more important factor than the others." (Matsuda, Ryuichi (1987) Animal Evolution in Changing Environments, with Special Reference to Abnormal Metamorphosis. N.Y.: Wiley Press pp.177-8)

"Wing reduction has occurred in many groups of Heteroptera, and aptery sometimes became permanent. Southwood (1961), after reviewing the facts then available, postulated a theory of the cold temperature-hormonally induced wing reduction in Heteroptera. The theory was based on the endocrinological facts brought forward in the studies of Phodnius by Wigglesworth (1952, 1954). Its essential points were as follows: the short-wingedness is a juvenile character and is likely to arise through the change in the concentration of JH that is necessary for the long-winged adults. This change could be brought about either one of the two ways" (1) by excessive influence of JH leading to juvenile characters --- metathetely, or (2) by depression of the influence of JH (and thus the loss of the prothoracic glands and thus failure of molting hormone), leading to adult characters in the nymph (larva of Southwood) --- prothetely. This view of regarding wing reduction as an aspect either of metathetely (leading to metagenetic neoteny) or of prothetely (leading to progenetic neoteny) has turned out to serve as a very important concept that can be extended to explain two kinds of neoteny in insects as well as in other animals." (Matsuda, Ryuichi (1987) Animal Evolution in Changing Environments, with Special Reference to Abnormal Metamorphosis. N.Y.: Wiley Press pp.194)

"In discussing the evolutionary process constant use of the term neo-Lamarckism has bothered my conscience, because the contribution of Darwin, that is, the part of the evolutionary process played by natural selection, becomes hidden under this term. More properly, therefore, neo-Lamarckism must be called "Lamarck-Darwinism." This again, however, does not convey properly what this work advocated, for both Lamarck and Darwin wrote of many things in addition to the environmental effect on development and evolution (Lamarck) and natural selection (Darwin). To resolve this dilemma and to provide a more precise meaning of what this work emphasizes, a new term, "pan environmentalism," is proposed. In pan-environmentalism, environment consists of both morphogenetic and selective factors. It is envisaged that the former induces, by response of the genotype, variation upon which the selective factor(s) works (Fig 5). It follows, then, that there will be appreciable evolution with environmental changes. (Conversely, there will be no appreciable evolution without environmental change.) Neo-Darwinism may be retained as a method of analysis of the evolutionary process where the effect of environmental change on development is minor or negligible." (Matsuda, Ryuichi (1987) Animal Evolution in Changing Environments, with Special Reference to Abnormal Metamorphosis. N.Y.: Wiley Press pp.45)

human evolution