Download The environment and the genotype in

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. Heredity, 9: 1-52
KENNEDY, J . S. 1961. Continuous polymorphism in locusts In J . S. Kennedy (Ed.), Insect
polymorphism: Symp. 1 , R. ent. SOC.Lond.: 80-90.
LEES, A. D., 1966. Control of polymorphism in aphids. A d v . Insect physiol., 3: 207-77.
LEVENE, H., 1953. Genetic equilibrium when more than one ecological niche is available. A m . Nat. 87:
331-3.
LEVINS, R. 1961. Mendelian species as adaptive systems. General Systems Yearbook 6: 33-9.
LEWONTIN, R. C. 1957. The adaptations of populations t o varying environments. S y m p . quant. Biol.,
22: 395-408.
262
W. C. CLARK
LEWONTIN, R. C., 1958. A general method for investigating the equilibrium of gene frequency in a
population. Genetics, 4 3 : 419-34.
MANWELL, C. & BAKER, C. M. A., 1970. Molecular biology and the origin of species-heterosis, protein
polymorphism and animal breeding. London: Sidgwick & Jackson.
MATHER, I., 1955. Polymorphism as an outcome of disruptive selection. Evolution, 9: 52-61.
MAYNARD SMITH, J., 1970a. Genetic polymorphism in a vaned environment. A m . Nat.,.lO4: 487-90.
MAYNARD SMITH, J., 1970b. The causes of polymorphism. In R. J . Berry & H. N. Southern (Eds),
Variation in mammalian populations. Symp. zool. SOC.Lond. 26: 371-83.
MAYR, E., 1963. Animal species and evolution. Harvard: Belknap Press.
PAULSON, D. R., 1973. Predator polymorphism and apostatic selection. Evolution, 27; 269-77.
SALT, G., 1937. The egg-parasite of Sialis lutaria: a study of the influence of the host upon a dimorphic
parasite. Parasitology. 29: 539-5 3.
SANG, J . H., 1961a. Contribution t o discussion p. 7. In J . S. Kennedy (Ed.), Insect polymorphism.
Symp. 1 , R. ent. SOC.Lond.
SANG, J. H. 1961b. Environmental control of mutant expression. In J. S. Kennedy (Ed.). Insecr
polymorphism: Symp. 1, R . ent. SOC.Lond.': 91-102.
WHITE, M. J . D., 1973. Animal cytology and evolution. Cambridge University Press.
WHITING, P. W., 1940. Multiple alleles in sex determination in Habrobracon. J. Morph. 66: 323-55.
WHITING, P. W.,1943. Multiple alleles in complementary sex determination of Habrobracon. Genetics,
28: 365-82.
WILLIAMS, G. C. & MITTON, J . B., 1973. Why reproduce sexually? J. theor. Biol., 39: 545-54.
YOUNG, E. C., 1965. Flight muscle polymorphism in British Corixidae: ecological observations. J. Anim.
Eco~.,3 4 : 353-90.