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2001.J . Linn. SOC.,58: 255-262. April 1 9 7 6 The environment and the genotype in polymorphism W. C. CLARK, F.L.S. Department o f Zoology, University of Canterbury, Christchurch, New Zealand Accepted f o r publication July I975 It is argued that polymorphism is a useful broad term applicable t o all forms of discontinuous variation affecting the same stages of development within populations. This unqualified term is particularly applicable when the fact of variation is known, b u t its causation is not known. The term “genetically determined polymorphism” is proposed for those polymorphisms where the genotype is paramount in morph determination, and where the environment is of little, if any importance (e.g. blood groups). Where the environment interacts with the genotype t o elicit a particular morph the term “environmentally cued polymorphism’. is apposite. Genetically determined polymorphisms result from discontinuously distributed, b u t continuously active genetic material, whilst environmentally cued polymorphisms appear to depend on universally distributed, b u t differentially active genetic resources. Environmentally cued polymorphism produces morphs congruent with current ecological conditions, and in fluctuating or alternating environments it avoids the worst effects of selection for the previously existing conditions. In fluctuating environments genetically determined polymorphism is a particularly costly method of achieving adaptation. Polymorphism is a much discussed topic, producing a crop of new references with every issue of Biological Abstracts. Despite this, the topic still seems to be a source of misunderstanding and confusion. This confusion arises from the existence of a variety of definitions of polymorphism and explicit or implicit riders to them. Even so, there seems general agreement that polymorphism is “discontinuous variation within a population with the rarest “morph” existing at a frequency greater than that which can be maintained by recurrent mutation alone”. This statement owes much to the series of subtly different definitions advanced by Ford (1937, 1940, 1945, 1955, 1957, 1961, 1964, 1965) over the past 35 years (and usually mis-attributed by Ford and others to his 1940 paper), but it omits a number of his restrictions. As defined above, polymorphism covers a great range of phenomena, but no greater than contemporary usage requires (e.g. Berrill, 1961; Deakin, 1966; Ford, loc. cit.: Lees, 1966; Lewontin, 1958; Poulson, 1973). Many geneticists (e.g. Ford, 1965; Manwell & Baker, 1970; Maynard Smith. 1970a) have distinguished what 255 256 W. C. CLARK they have termed “genetic polymorphism’’ (= “morphism” of Huxley, 1955), thereby suggesting that any other kind of polymorphism (called “polyphasy” by Ford, 1940, and “polyphenism” by Mayr, 1963) is non-genetic in nature. This is nonsense at worst, and almost tautology at best. Geneticists usually emphasize that the phenotype of an organism is the result of interaction between the genotype and the environment. It follows therefore, that any feature which gains expression in the phenotype must have a genetic basis. Most workers agree that polymorphism is not concerned with continuous variation which is generally under polygenic control, nor is polymorphism used to describe inter-population variations such as geographical races. When first introduced (1785-fide Sang, 1961a) the application of the term polymorphism was restricted to different morphs at the same ontogenetic stage. If usage is restricted to this original sense much difficulty is avoided and the sequence of morphs in an ontogeny, usually called metamorphosis, does not become synonymous with polymorphism. The tendency to extend the meaning of polymorphism so that it is almost synonymous with metamorphosis has almost diseappeared. Because the sequence of changes that occur in an individual ontogeny is usually the same for all members of a population these changes do not in themselves constitute polymorphism. Thus the sequence of haemoglobin types which are part of the normal development of the mammalian foetus do not constitute polymorphism any more than the existence of larva and pupa in the life history of a holometabolous insect constitute polymorphism. This usage is not extinct, however, for Paulson (1973 : 273) recently referred to juvenile and adult plumages as “age-related polymorphism”. The repeated attempts to restrict polymorphism to a very narrow range of phenomena where the morphological effects result from the presence or absence of a single allele (e.g. Mayr, 1963; Ford, 1964) have never been realistic or successful. A cogent reason for the failure of such limitation is that semantically “polymorphism” means “many forms’’ and is thus an appropriate term for observable differences in form between members of a population whether or not the mechanism(s) of morph determination is known. For general purposes there is much to recommend the adoption of a general term such as “polymorphism” for the observable phenomen of morphologically different forms within a population. It removes the necessity for a good measure of the knowledge as a sine qua non to discussion or description. For the purposes of discussion it is convenient to divide polymorphism into two broad classes, based primarily upon the nature of the factors which elicit the production of a particular morph. As with almost every classification of biological phenomena, intermediate or transitional examples are apparent, or occasionally better knowledge will result in the transfer of an example from one category to another. Generally, however, most examples are either ( 1 ) primarily genetically determined polymorphism with the environment playing little part in morph determination, or ( 2 )environmentally cued polymorphism’ where the environmental stimuli interact with the genotype to elicit a particular morph. As in other discussions of polymorphism, the term is used to embrace differences in behaviour and physiology, as well as differences in morphology whether gross, microscopic, or molecular in their level of expression. ENVIRONMENT AND GENOTYPE IN POLYMORPHISM 257 In practice, most examples of polymorphism are readily assigned to one category or the other. Thus environmentalljl cued polymorphism includes the production of seasonal forms such as apterae and alatae; and sexuparae and virginoparae amongst the aphids; cyclomorphosis amongst cladocerans; the rhabditiform and filariform juveniles of some nematodes (e.g. Strongyloides papillosus and S. stercoralis); solitary and gregarious phases in locusts; spring and summer and wet and dry season forms in some butterflies; trophic and pheromonal caste determination in worker and queen Hymenoptera. Similar polymorphic specializations which parallel divisions of labour occur in some Isoptera, as well as in truly colonial organisms such as the Siphonophora, the Ectoprocta and the Thaliacea. Genetically determined polymorphism includes those expressions of the genotype in which the influence of the environment is minimal or even undetectable. Such expressions would include the blood groups such as A, B , 0, M, N , S and Rh factors and most sex determination where this is not environmentally determined. The great variety of protein polymorphisms mostly fall in this category, though the genetic basis for their inheritance is as commonly assumed as it is demonstrated. Some patterns of diapause behaviour belong here, as do the chromosome polymorphisms of Drosophila studied long ago by Dobzhansky and his colleagues. De‘spite the apparent simplicity of the proposed categories, there are a number of intermediate examples of polymorphism which show characteristics of both groups. Male-type baldness in man is such a trait. I t has an undoubted genetic basis and only in the presence of the appropriate alleles will the trait appear, but at the same time, it is an environmentally cued character for it is dependent upon a high level of testosterone for its expression. This explains the apparent sex linkage of the trait. The expression of such a trait has much in common with the expressivity of much studied traits such as vestigial wing in Drosophila where phenotypic expression of the genotype is markedly influenced by the temperature at which the larvae are reared. The importance of environmental factors on the expressivity of some polymorphs is well known (Sang, 1961b). I t is also true that genetically determined polymorphism arises from the discontinuous distribution of genetic material through a population, whilst environmentally cued polymorphism is determined by discontinuous effectiveness, or the “switching on or off” of alleles which are the common property of all members of the population. Thus, genetically determined polymorphism is simply a limited aspect of the phenomenon of gene frequency in a population and the selective advantages of certain allelomorphs in particular genetical constellations and environmental circumstances. Similarly, environmentally cued polymorphism may be considered a specialized part of the spectrum of processes which form part of normal development and maintenance. Normally it may be assumed (despite some evidence to the contrary in some instances-White, 1973) that the somatic cells in an organism contain the same genotype, but despite this, and presumably in response to environmental stimuli, different parts of the spectrum of potentials contained in the genome are selectively activated or suppressed. By this means, differential specialization of cells is achieved and different tissues serving different functions arise from cells with identical genetic potential. I t matters little for the purpose of this discussion whether the environmental differentia are oestrogens and androgens, 18 258 W. C. CLARK or “head” or “tail organizers” or nutritional effects. The capacity of undifferentiated cells to differentiate in diverse ways is essential to Downey’s monophyletic theory of the polymorphic origin of erythrocytes: monocytes, granulocytes, megakaryocytes, etc. in the reticulo-endothelial systems of mammals (Downey, 1938). The production of nerve and epithelial cells from the same genome, is no less striking than the production of winged or wingless aphids from similar genetic material, or the production of tasters and non-tasters from dissimilar genetic material. Evolutionary explanations of genetically determined polymorphisms are numerous. Ford and others have been preoccupied with situations in which the heterozygote was fitter than either homozygote. Mather (195 5 ) explained polymorphism as an outcome of disruptive selection when temporal variation in the environment resulted in different optima being favoured in different generations. Levene (1953) had previously shown that polymorphism without superior fitness in the heterozygote could arise in a population if it could be divided into sub-populations in different ecological niches, experiencing different selection pressures Lewontin (1958) and Haldane & Jayakar (1963a & b) independently showed that polymorphism, dependent upon the superior fitness of either homozygote in changing environments, could be maintained by disruptive selection provided selection pressures are great enough. Mayr ( 1963) was sceptical about the possible importance of disruptive selection. Most mathematical models conclude that disruptive selection can maintain genetically determined polymorphisms if applied rigorously enough. The subject was reviewed briefly by Maynard Smith (1970b). As Levins (1961) pointed out, such disruptive selection has to be rigorous enough to override what he called the “Epaminondas effect’’ after the small boy in the nursery story who always offered the correct solution for the previously existing situation. It may be important to observe that such apparently regularly alternating forms such as summer and winter generations are not usually genetically determined, but are frequently environmentally (often photoperiodically) cued polymorphs. Both Lewontin (1957) and Levins (1961) appreciated the significance of environmentally cued morphs in achieving close adaptation in heterogeneous environments but baulked at calling them polymorphs. Williams & Mitton (1973), however, overlooked a most important role of environmentally cued polymorphism as exhibited by aphids and cladocerans (which may also show both gonochoristic and parthenogenetic reproduction) with marked polymorphism even amongst the parthenogens when they wrote: “With asexual reproduction, each generation would begin with only those genotypes that had been favourably selected for seasonal conditions opposite to those that will actually be faced.” This statement assumes all phenotypes to be genetically determined rather than genetically permitted or facilitated and further overlooked the possibilities of at least limited genetic change during “endomeiosis” as claimed by Bacci et al., (1961) and Cognetti (1960, 1961a, b, c). Williams & Mitton (1973) assumed a fixity of genetic response, with any genotype having but a single phenotypic expression. Adaptation to habitats which change fairly regularly and are thus likely to favour different phenotypes in different seasons may be of several kinds. (“Average” or “typical” years or seasons are produced by calculators, not by ENVIRONMENT AND GENOTYPE IN POLYMORPHISM 259 nature.) For this reason a strictly genetically predetermined sequence of polymorphic generations, with each highly adapted morph following the other in a predictable sequence constitutes a conceivable form of polymorphism, but one which seems to be unknown in nature. Perhaps the commonest form of adaptation to more or less regularly varying environments is not polymorphism at all; it may merely require that life histories involving a degree of metamorphosis or other marked change of phenotype during development become cued to the environmental conditions so that the organism adopts the most appropriate phenotype for the given season. In the absence of a suitably adapted active morph the species may persist in a quiescent or diapausing phase of the life history. Such “opting out” mechanisms allow survival in the absence of suitable environmental conditions and may themselves constitute environmentally cued polymorphisms especially in multivoltine insects, or may be genetically determined, especially in univoltine species. A fairly common solution to the problem of seasonal adaptation is the adoption of environmentally cued polymorphism, in which the morph that develops is largely determined by the current or immediately antecedent environmental conditions. Probably because of Ford’s and others’ attempts to restrict the scope of the term polymorphism, this extremely common kind of polymorphism (which uses the environment as the morph determinant) has gone largely unstudied by geneticists. Consequently, there is no detailed genetic theory to explain either the evolution of the phenomenon, or the mechanism necessary for its operation. On the other hand, entomologists and others who have ignored attempted semantic restrictions have found this kind of polymorphism a rewarding field. Whilst attempts at discovering the nature of the switch mechanism have not yet been successful, the precise nature of the diverse environmental stimuli which activate the switch mechanisms are well established in many instances. I t is tempting to speculate that polymorph determination is achieved through the effects of neurosecretions and the turning on and off of genes as in the control of chromosome puffing by juvenile hormone levels in many insects (Ashburner, 1970; Berendes, 1971). Much genetically determined polymorphism is a somewhat ephemeral phenomenon which exists while a gene spreads through a population or tends to an equilibrium frequency in the population. Except where the favoured morph is dependent upon heterosis one allelomorph or the other could be removed from the population and the polymorphism thus eliminated. In environmentally cued polymorphism, however, one morph may depend upon the occurrence of the other for its re-creation; for example, sexual aphids can only be produced by parthenogenetically produced aphids. These considerations apply particularly to reproductive polymorphisms in which different “generations” reproduce in different ways. It does not apply in the same way to seasonal forms of butterflies, or to host-induced differences as in some of the microhymenoptera (e.g. Trichogramma semblidis Salt, 1937), or to much wing, or wing muscle polymorphism in the Hemiptera (Young, 1965). Sexual dimorphism (perhaps the most frequently cited example of a genetically determined polymorphism) is of particular interest on two grounds. First, despite the common insistence that polygenic characters or effects do not constitute polymorphism in the sense of Ford and others, there seems little doubt that sex is polygenic in many organisms (e.g. Habrobrucon Whiting, 260 W. C. CLARK 1940, 1943), and that it is an environmentally cued polymorphism in other organisms, especially those which show consecutive sexuality. Secondly, sexual dimorphism is important as one of the few genetically determined polymorphisms which appear to have persisted for a long time in a balanced state. I t is also important as an example in which it is difficult to establish an argument for superior fitness in the heterozygote, and in which only one kind of “homogametous” condition exists (no y y genotypes). Polymorphism of the genetically determined type can be a very expensive way of achieving a goal (Lewontin, 1957; Levins, 1961; Mayr, 1963). Where, as in sickle cell trait, the selective advantage depends on the superiority of the heterozygote, even with the continuation of the conditions in which superior fitness is achieved this advantage is only realized by half of the offspring of any pair of heterozygotes. If the environment changes so that the heterozygotes lose their superior fitness the homozygous dominants will be favoured and selection against the sickle cell genes will tend to establish a new and lower frequency of this gene. Because genetically determined polymorphism throws up variant morphs without relation to the current selection pressures or environmental conditions the system will produce many maladapted individuals. Similarly, environmentally cued polymorphism is largely protected from such wastage. Where superior fitness derives from heterozygotes the price to be paid is high. When fitness depends upon a homozygous condition if the conditions in which the superior fitness is achieved occur consistently enough selection will remove, or at least decrease the frequency of the less fit alleles. If this occurs the genetic resources of the population are likely to be restricted. By contrast, the environmentally cued polymorphs do not normally suffer an equivalent restriction of their genetic resources and they avoid the Epaminondas effect. The worst that can befall them in these circumstances is for the environmental conditions to call for the repeated re-evocation of a particular morph to the extent that the capacity to produce the alternative morph is permanently lost. This has apparently happened in several aphid species in New Zealand. Myzus persicae exists in New Zealand in two forms, one which produces sexuals in the autumn and overwinters as diapausing eggs and one which is perpetually parthenogenetic (Cottier, 1953). Similarly, Rhopalosiphum padi exists only in the parthenogenetic morph. (A. D. Lowe, pers. comm.), but here the adaptive significance of this condition is apparent. Firstly, the overwintering host for this species, Prunus padus is extremely rare in New Zealand and was possibly totally absent when the aphid was first introduced. Secondly, by reproducing parthenogenetically, albeit at a fairly low level on autumn and winter sown cereals, this aphid has a marked numerical advantage in the spring over any aphid which overwinters in the egg state. Confronted with examples such as this it is not difficult t o see how under different selection pressures both kinds of polymorphism could result in reproductive isolation, and thus in speciation of parts of a population. Because environmentally cued polymorphism is attuned to environmental conditions, and thus approximately at least to selective pressures, it is unlikely to prove as expensive as chancedependent genetically determined polymorphism. To the extent that the system avoids the production of overtly ENVIRONMENT AND GENOTYPE IN POLYMORPHISM 261 maladapted morphs it could conceivably be more advantageous than genetically determined polymorphism. I t is concluded that the term polymorphism is a useful broad term applicable to all forms of discontinuous variation regardless of the causative agent. I t is further suggested that for convenience of discussion two broad categories are recognizable, that in which the singular features of the genome determine the morph, genetically determined polymorphism, and that in which the environment interacts with the genome, usually similar in all important respects in all members of the population, to evoke a phenotype which is congruent with the environmental circumstances. Environmentally cued polymorphism has its effect through differentially activating some parts of the genome and wholly or partially suppressing the action of other parts. Polymorphisms operate through two quite different mechanisms, the first is simply normal change in gene frequency, and the other through differential gene activity which constitutes an important part of normal processes of development and differentiation. REFERENCES ASHBURNER, M., 1970. Function and structure of polytene chromosomes during insect development. A d v . Insect Physiol. 7 : 1-95. BACCI, G., COGNETTI, G. & VACCARI, G., 1961. Endomeiosis and sex determination in Daphniu pulex. Experientia, 1 7: 505-6. BERENDES, H. D., 1971. Gene activation in dipteran polytene chromosomes. S y m p . Soc. Exp. Biol.,25: 145-61. BERRIL, N. I., 1961 Growth, development and pattern. San Francisco: W. H. Freeman. COGNETTI G., 1960. Selezione per le forme attere in linee partenogenetiche di Myzodes persicae. Boll. ZOO^. 27: 107-13. GOGNETTI, G., 1961a. Endomeiosis in parthenogenetic lines of aphids. Experientia 17: 168-9. COGNETTI, G., 1961h. Endomeiosis e selezione in ceppi partenogenetici di Afidi. A t t i Ass. genet. ital., 6 : 449-54. COGNETTI, G., 1961c. Citogenetica della partenogenesi negli Afidi. Archo zool. ital. 4 6 : 89-122. COTTIER, W., 1953. Aphids of New Zealand. N.Z. Dept. sci. indust. Res. Bull. I06. DEAKIN, M. A. B., 1966. Sufficient conditions for genetic polymorphism. A m . Nut. 100: 690-2. DOWNEY, H., 1938. In H. Downey (Ed.), Handbook of hematology. New York: Hafner Press. FORD, E. B., 1937. Problems of heredity in the Lepidoptera. Biol. Rev. 12: 461-503. FORD, E. B., 1940. Polymorphism and Taxonomy In J . S. Huxley (Ed.), N e w systematics: Oxford: Clarendon Press. FORD, E. B., 1945. Polymorphism. Biol. Rev., 20: 73-88. FORD, E. B., 1955. Polymorphism and Taxonomy. Heredity, 9: 255. FORD, E. B., 1957. Polymorphism in plants, animals and man.Narure, 180: 1315-9. FORD, E. B., 1961. The theory of genetic polymorphism. In J . S. Kennedy (Ed.), Insectpolymorphism: Symp. 1 , R. ent. SOC.Lond.: 11-9. FORD, E. B.. 1964. Ecological genetics. London: Methuen; FORD, E. B. 1965. Genetic polymorphism. London: Faber & Faber. HALDANE, J . B. S. & JAYAKAR, S. D., 1963a. Polymorphism due to selection of varying direction. J . Genet., 58: 237-42. HALDANE, J . B. S. & JAYAKAR, S. D., 1963h. Polymorphism due to selection depending on the composition of a population. J. Genet., 58: 318-23. HUXLEY, J . S., 1955. Morphism and evolution. 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