Polymorphism (biology)

(Redirected from Genetic polymorphism)
Jump to: navigation, search

Please Take Over This Page and Apply to be Editor-In-Chief for this topic: There can be one or more than one Editor-In-Chief. You may also apply to be an Associate Editor-In-Chief of one of the subtopics below. Please mail us [1] to indicate your interest in serving either as an Editor-In-Chief of the entire topic or as an Associate Editor-In-Chief for a subtopic. Please be sure to attach your CV and or biographical sketch.

Light-morph Jaguar (typical)
Dark-morph or melanistic Jaguar (about 6% of the South American population)

Polymorphism in biology occurs when two or more clearly different types exist in the same population of the same species— in other words, the occurrence of more than one form or morph. The caste system in ants is an example.

Polymorphism (Greek: poly = many, and morph = form) is defined as discontinuous[1] variation in a single population[2] — meaning, the population is in the same location and is interbreeding. The term was first used to describe visible forms, but by extension we now use the term to include cryptic morphs, for instance blood types, which can be made visible by a test.

The shorter term morphism may be more accurate that polymorphism, but is not often used. It was the preferred term of the evolutionist Julian Huxley.[3]

Polymorphism is extremely common; it is a kind of variation related to biodiversity, genetic variation and adaptation. Polymorphism usually functions to retain variety of form in a population living in a varied environment. The most common example of polymorphism is the sexual dimorphism of most higher organisms; this retains diversity by the process of genetic recombination. Other examples are mimetic forms of butterflies (see mimicry) and certain cryptic forms of moths, the banding pattern on snail shells, human blood groups and many other cases.

Polymorphism results from an evolutionary process, as does any aspect of a species. Polymorphism is heritable, and is modified by selection (either artificial or in the wild). In polyphenism, an individual's genetic make-up allows for different morphs, and the switch mechanism that determines which morph is shown is environmental. In genetic polymorphism or balanced polymorphism, the genetic make-up determines the morph.

Polymorphism as described here involves morphs of the phenotype. The term is also used by molecular biologists to describe certain point mutations in the genotype, such as SNPs and RFLPs. This usage is not discussed in this article.


What polymorphism is not

Although polymorphism is potentially quite a broad term, in biology it has been given a specific meaning. This section indicates its proper use.

  • The term omits continuous variation (such as weight) even though this has a heritable component. Polymorphism deals with forms in which the variation is discrete (discontinuous) or strongly bimodal or polymodal.
  • Morphs must occupy the same habitat at the same time: this excludes geographical races and seasonal forms.[4] The use of the words morph or polymorphism for what is a visibly different geographical race or variant is common, but incorrect. The significance of geographical variation (allopatry) is that interbreeding between different locations is reduced or eliminated, a possible prelude to species splitting. True polymorphism takes place in panmictic populations, and has to do with the adaptation of a species to its environment.
  • Rare variations are not classified as polymorphisms; and mutations by themselves do not constitute polymorphisms. To qualify as a polymorphism there has to be some kind of balance between morphs underpinned by inheritance. The criterion is that the frequency of the least common morph is too high simply to be the result of new mutations[5][2] or, as a rough guide, that it is greater than 1 percent (though that is far higher than any normal mutation rate for a single allele).[6]

Nomenclature

The different forms can be called morphs or morphotypes; trait (biology) and characters are also possible descriptions, though they imply just a limited aspect of the body. Phase is sometimes used, but morph or form is best, since many of the examples greatly change the appearance of an individual (e.g. sex; mimicry).

In zoology the word "morpha" plus a Latin name for the morph can be added to a binomial or trinomial name. However, this invites confusion with geographical variation, especially with sub-species. Morphs have no formal standing in the ICZN.

In botany, morphs may be named with the terms "variety", "subvariety", and "forms" which are formally regulated by the ICBN. There might be confusion with the term variety.

Ecology

Selection, whether natural or artificial, changes the frequency of morphs within a population; this occurs when morphs reproduce with different degrees of success. A genetic (or balanced) polymorphism usually persists over many generations, maintained by two or more opposed and powerful selection pressures.[5] Diver (1929) found banding in Cepaea nemoralis could be seen in pre-fossil shells going back to the Mesolithic Holocene.[7] [8] Apes have similar blood groups to humans: human and chimpanzee blood, with compatible blood groups, can be exchanged through transfusion (Great Ape Project). This suggests rather strongly that this kind of polymorphism is quite ancient, at least as far back as the last common ancestor of the apes and man, and possibly even further.

The relative proportions of the morphs may vary; the actual values are determined by the effective fitness of the morphs at a particular time and place. The mechanism of heterozygote advantage assures the population of some alternative alleles at the locus or loci involved. Only if competing selection disappears will an allele disappear. However, heterozygote advantage is not the only way a polymorphism can be maintained. Apostatic selection, whereby a predator consumes a common morph whilst overlooking rarer morphs is possible and does occur. This would tend to preserve rarer morphs from extinction.

A polymorphic population does not initiate speciation; it has little or nothing to do with species splitting. However, it has a lot to do with the adaptation of a species to its environment, which may vary in colour, food supply, predation and in many other ways. Polymorphism is one good way the opportunities get to be used; it has survival value, and the selection of modifier genes may reinforce the polymorphism.

The switch

The decision mechanism which decides which of several morphs an individual displays is called the switch. This switch may be genetic, or it may be environmental. Taking sex determination as the example, in man the determination is genetic, by the XY sex-determination system. In Hymenoptera (ants, bees and wasps), sex determination is by haplo-diploidy: the females are all diploid, the males are haploid. However, in some animals an environmental trigger determines the sex: alligators are a famous case in point. In ants the distinction between workers and guards is environmental, by the feeding of the grubs. Polymorphism with an environmental trigger is called polyphenism.

The polyphenic system does have a degree of environmental flexibility not present in the genetic polymorphism. However, such environmental triggers are the less common of the two methods.

Investigative methods

Investigation of polymorphism requires a coming together of field and laboratory technique. In the field:

  • detailed survey of occurrence, habits and predation
  • selection of an ecological area or areas, with well-defined boundaries
  • capture, mark, release, recapture data (see Mark and recapture)
  • relative numbers and distribution of morphs
  • estimation of population sizes

And in the laboratory:

  • genetic data from crosses
  • population cages
  • chromosome cytology if possible
  • use of chromatography or similar techniques if morphs are cryptic (for example, biochemical)

Both types of work are equally important. Without proper field-work the significance of the polymorphism to the species is uncertain; without laboratory breeding the genetic basis is obscure. Even with insects the work may take many years; examples of Batesian mimicry noted in the nineteenth century are still being researched.

Genetic polymorphism

Since all polymorphism has a genetic basis, genetic polymorphism has a particular meaning:

  • Genetic polymorphism is the occurrence together in the same locality of two or more discontinuous forms of a species in such proportions that the rarest of them cannot be maintained just by recurrent mutation [5]. It is sometimes called balancing selection, and is intimately connected with the idea of heterozygote advantage.

The definition has three parts: a) sympatry: one interbreeding population b) discrete forms, and c) not maintained just by mutation.

Sexual dimorphism

We meet genetic polymorphism daily, since our species (like most other eukaryotes) uses sexual reproduction, and of course, the sexes are differentiated. The system is relatively stable (with about half of the population of each sex) and heritable, usually by means of sex chromosomes. Every aspect of this everyday phenomenon bristles with questions for the theoretical biologist. Why is the ratio ~50/50? How could the evolution of sex occur from an original situation of asexual reproduction, which has the advantage that every member of a species could reproduce? Why the visible differences between the sexes? These questions have engaged the attentions of biologists such as Charles Darwin, August Weismann, Ronald Fisher, George C. Williams, John Maynard Smith and W.D. Hamilton, with varied success.

Although this huge topic cannot be treated here in detail, it is fair to say there is widespread agreement on the following: the advantage of sexual reproduction over asexual reproduction lies in the way recombination increases the genetic diversity of the ensuing population. This enables the population to better meet the challenges of infection, parasitism, predation and other hazards of the varied environment. [9] [10] [11]

Other human polymorphisms

There are a large number of less spectacular examples of human genetic polymorphisms. All the common blood types, such as the ABO system, are genetic polymorphisms. Here we see a system where there are more than two morphs: the phenotypes are A, B, AB and O are present in all human populations, but vary in proportion in different parts of the world. The phenotypes are controlled by multiple alleles at one locus. These polymorphisms are seemingly never eliminated by natural selection; the reason came from a study of disease statistics.

Statistical research has shown that the various phenotypes are more, or less, likely to suffer a variety of diseases. For example, an individual's susceptibility to cholera (and other diarrheal infections) is correlated with their blood type: those with type O blood are the most susceptible, while those with type AB are the most resistant. Between these two extremes are the A and B blood types, with type A being more resistant than type B. This suggests that the pleiotropic effects of the genes set up opposing selective forces, thus maintaining a balance. [12] [13]

Such a balance is seen more simply in sickle-cell anaemia, which is found mostly in tropical populations in Africa and India. An individual homozygous for the recessive sickle haemoglobin, HgbS, has a short expectancy of life, whereas the life expectancy of the standard haemoglobin (HgbA) homozygote and also the heterozygote is normal (though heterozygote individuals will suffer periodic problems).

So why does the sickle-cell variant survive in the population? Because the heterozygote is resistant to malaria and the malarial parasite kills a huge number of people each year. This is balancing selection or genetic polymorphism, balanced between fierce selection against homozygous sickle-cell sufferers, and selection against the standard HgbA homozygotes by malaria. The heterozygote has a permanent advantage (a higher fitness) so long as malaria exists; and it has existed as a human parasite for a long time. Because the heterozygote survives, so does the HgbS allele survive at a rate much higher than the mutation rate (see [14][15] and refs in Sickle-cell disease).

The Cuckoo

Over fifty species in this family of birds practise brood parasitism; the details are best seen in the British or European Cuckoo (Cuculus canorus). The female lays 15-20 eggs in a season, but only one in each nest of another bird. She removes some or all of the host's clutch of eggs, and lays an egg which closely matches the host eggs. Although, in Britain, the hosts are always smaller than the Cuckoo itself, the eggs she lays are small, and coloured to match the host clutch but thick-shelled. This latter is a defence which protects the egg if the host detects the fraud.

Reed warbler feeding a cuckoo chick (Cuculus canorus)

The intruded egg develops exceptionally quickly; when the newly-hatched Cuckoo is only ten hours old, and still blind, it exhibits an urge to eject the other eggs or nestlings. It rolls them into a special depression on its back and heaves them out of the nest. The Cuckoo nestling is apparently able to pressure the host adults for feeding by mimicking the cries of the host nestlings. The diversity of the Cuckoo's eggs is extraordinary, the forms resembling those of its most usual hosts. In Britain these are:

  • Meadow Pipit (Anthus pratensis): brown eggs speckled with darker brown.
  • Robin (Erithacus rubecula): whitish-grey eggs speckled with bright red.
  • Reed warbler (Acrocephalus scirpensis): light dull green eggs blotched with olive.
  • Redstart (Phoenicurus phoenicurus): clear blue eggs.
  • Hedge Sparrow (Prunella modularis): clear blue eggs, unmarked, not mimicked. This bird is an uncritical fosterer; it tolerates in its nest eggs that do not resemble its own.

Each female Cuckoo lays one type only; the same type laid by her mother. In this way female Cuckoos are divided into groups (known as gentes), each parasitises the host to which it is adapted. The male Cuckoo has its own territory, and mates with females from any gente; thus the population (all gentes) is interbreeding.

The standard explanation of how the inheritance of gente works is as follows. The egg colour is inherited by sex chromosome. In birds sex determination is ZZ/ZW, and unlike mammals, the heterogametic sex is the female.[16] The determining gene (or super-gene) for the inheritance of egg colour is believed to be carried on the W chromosome. The W chromosome, of course, is directly transmitted in the female line. The female behaviour in choosing the host species is set by imprinting after birth, a common mechanism in bird behaviour.[17] [18]

Ecologically, the system of multiple hosts protects host species from a critical reduction in numbers, and maximises the egg-laying capacity of the population of Cuckoos. There are some other advantages, too: it extends the range of habitats where the Cuckoo eggs may be raised successfully. Detailed work on the Cuckoo started with Chance in 1922 [19] and continues to the present day; in particular, the inheritance of gente is still a live issue.

Grove snail

The Grove Snail, Cepaea nemoralis, is famous for the rich polymorphism of its shell. The system is controlled by a series of multiple alleles. The shell colour series is brown (genetically the top dominant trait), dark pink, light pink, very pale pink, dark yellow and light yellow (the bottom or universal recessive trait). Bands may be present or absent; and if present from one to five in number. Unbanded is the top dominant trait, and the forms of banding are controlled by modifier genes (see epistasis).

Grove snail, dark yellow shell with single band.

In England the snail is regularly predated by the Song Thrush Turdus philomelos, which breaks them open on thrush anvils (large stones). Here fragments accumulate, permitting researchers to analyse the snails taken. The thrushes hunt by sight, and capture selectively those forms which match the habitat least well. Snail colonies are found in woodland, hedgerows and grassland, and the predation determines the proportion of phenotypes (morphs) found in each colony.

Two active Grove snails

A second kind of selection also operates on the snail, whereby certain heterozygotes have a physiological advantage over the homozygotes. In addition, aposematic selection is likely, with the birds preferentially predating the most common morph. So, despite the predation, the polymorphism survives in all habitats, though the proportions of morphs varies considerably. The alleles controlling the polymorphism form a super-gene with linkage so close as to be nearly absolute. This control saves the population from a high proportion of undesirable recombinants, and it is hypothesised that selection has brought the loci concerned together. To sum up, in this species physiological and cryptic diversity is preserved mainly by heterozygous advantage in the super-gene. [20] [21] [22] [23] [24]

A similar system of genetic polymorphism occurs in the White-lipped Snail Cepaea hortensis, a close relative of the Grove Snail.

Scarlet Tiger Moth

The Scarlet Tiger Moth Callimorpha (Panaxia) dominula (Family Arctiidae) occurs in continental Europe, western Asia and southern England. It is a day-flying moth, noxious-tasting, with brilliant warning colour in flight, but cryptic at rest. The moth is colonial in habit, and prefers marshy ground or hedgerows. The preferred food of the larvae is the herb Comfrey (Symphytum officinale). In England it has one generation per year.

Callimorpha dominula morpha typica with spread wings. The red with black rear wings, revealed in flight, warn of its noxious taste. The front wings are cryptic, covering the rear wings at rest. Here the moth is resting but alert, and has jinked the front wings forward to reveal the warning flash.

The moth is known to be polymorphic in its colony at Cothill, about five miles from Oxford, with three forms: the typical homozygote; the rare homozygote (bimacula) and the heterozygote (medionigra). It was studied there by E.B. Ford, and later by P.M. Sheppard and their co-workers over many years. Data is available from 1939 to the present day, got by the usual field method of capture-mark-release-recapture and by genetic analysis from breeding in captivity. The records cover gene frequency and population-size for much of the twentieth century. [25]

In this instance the genetics appears to be simple: two alleles at a single locus, producing the three phenotypes. Total captures over 26 years 1939-64 came to 15,784 homozygous dominula (ie typica), 1,221 heterozygous medionigra and 28 homozygous bimacula. Now, assuming equal viability of the genotypes 1,209 heterozygotes would be expected, so the field results do not suggest any heterozygous advantage. It was Sheppard who found that the polymorphism is maintained by selective mating: each genotype preferentially mates with other morphs.[26] This is sufficient to maintain the system despite the fact that in this case the heterozygote has slightly lower viability.[27]

Peppered Moth

The Peppered Moth, Biston betularia, is justly famous as an example of a population responding in a heritable way to a significant change in their ecological circumstances.

Although the moths are cryptically camouflaged and rest during the day in unexposed positions on trees, they are predated by birds hunting by sight. The original camouflage (or crypsis) seems near-perfect against a background of lichen growing on trees. The sudden growth of industrial pollution in the nineteenth century changed the effectiveness of the moths' camouflage: the trees became blackened by soot, and the lichen died off. In 1848 a dark version of this moth was found in the Manchester area. By 1895 98% of the Peppered Moths in this area were black. This was a rapid change for a species that has only one generation a year.

Biston betularia morpha typica, the standard light-coloured Peppered Moth.
Biston betularia morpha carbonaria, the melanic Peppered Moth.

In Europe, there are three morphs: the typical white morph (betularia or typica), and carbonaria, the melanic black morph. They are controlled by alleles at one locus, with the carbonaria being dominant. There is also an intermediate or semi-melanic morph insularia, controlled by other alleles (see Majerus 1998[28]).

A key fact, not realised initially, is the advantage of the heterozygotes, which survive better than either of the homozygotes. This affects the caterpillars as well as the moths, in spite of the caterpillars being monomorphic in appearance (they are twig mimics). In practice heterozygote advantage puts a limit to the effect of selection, since neither homozygote can reach 100% of the population. For this reason, it is likely that the carbonaria allele was in the population originally, pre-industrialisation, at a low level. With the recent reduction in pollution, the balance between the forms has already shifted back significantly.

Another interesting feature is that the carbonaria had noticeably darkened after about a century. This was seen quite clearly when specimens collected about 1880 were compared with specimens collected more recently: clearly the dark morph has been adjusted by the strong selection acting on the gene complex. This might happen if a more extreme allele was available at the same locus; or genes at other loci might act as modifiers. We do not, of course, know anything about the genetics of the original melanics from the nineteenth century.

This type of industrial melanism has only affected such moths as obtain protection from insect-eating birds by resting on trees where they are concealed by an accurate resemblance to their background (over 100 species of moth in Britain with melanic forms were known by 1980[29]). No species which hide during the day, for instance, among dead leaves, is affected, nor has the melanic change been observed among butterflies.[30][31][32]

This is, as advertised in many textboks, 'evolution in action'. Much of the work was done by Bernard Kettlewell, whose methods came under scrutiny later on. The entomologist Michael Majerus discussed criticisms made of Kettlewell's experimental methods in his 1998 book Melanism: Evolution in Action.[33] This book was misrepresented in some reviews, and the story picked up by creationist campaigners. In her controversial book Of Moths and Men, Judith Hooper (2002) implied that Kettlewell's work was fraudulent or incompetent. Careful studies of Kettlewell's surviving papers by Rudge (2005) and Young (2004) found that Hooper's allegation of fraud was unjustified, and that "Hooper does not provide one shred of evidence to support this serious allegation”.[34][35] Majerus himself described Of Moths and Men as "littered with errors, misrepresentations, misinterpretations and falsehoods".[33]

Conclusion: The Peppered Moth is a valid example of evolution in action, especially for the type of evolution called adaptation.

Hoverfly polymorphism

Hoverfly mimics can be seen in almost any garden in the temperate zone. The Syrphidae are a large (5600+ species) family of flies; their imagos feed on nectar and pollen, and are well-known for their mimicry of social hymenoptera. The mimicry is Batesian in nature: hoverflies are palatible but hymenoptera are generally unpalatable and may also be protected by stings and/or armour.

Many social wasp species (Vespidae) exhibit Mullerian mimicry, where a group of unpalatable species benefit from sharing the same kind of warning (aposematic) colouration. Clusters (or rings) of wasp species showing Mullerian mimicry are often accompanied by clusters of hover-fly species mimicking them. Observers in a garden can see for themselves that hoverfly mimics are quite common, usually many times more common than the models, and are relatively poor mimics, easy to distinguish from real wasps. Also (this does require real entomological skill) polymorphism is completely absent from these mimics, and is absent in the wasps.

The situation with bumblebees is quite different. They too are unpalatable, and their body is armoured (they rarely sting). They also form Mullerian rings of species, and they do often exhibit polymorphism. The hoverfly species mimicking bumblebees are accurate mimics, and many of their species are polymorphic. Many of the polymorphisms are different between the sexes, for example by the mimicry being limited to one sex only.

The question is, how can the differences between social wasp mimics and bumblebee mimics be explained? Evidently if model species are common, and have overlapping distributions, they are less likely to be polymorphic. Their mimics are widespread and develop a kind of rough and ready jack-of-all-trades mimicry. But if model species are less common and have patchy distribution they develop polymorphism; and their mimics match them more exactly and are polymorphic also. The issues are currently being investigated.[36][37][38]

Chromosome polymorphism in Drosophila

In the 1930s Dobzhansky and his co-workers collected Drosophila pseudoobscura and D. persimilis from wild populations in California and neighbouring states. Using Painter's technique [39] they studied the polytene chromosomes and discovered that the wild populations were polymorphic for chromosomal inversions. All the flies look alike whatever inversions they carry: this is an example of a cryptic polymorphism. Accordingly, Dobzhansky favoured the idea that the morphs became fixed in the population by means of Sewall Wright's drift.[40] However, evidence rapidly accumulated to show that natural selection was responsible:

Drosophila polytene chromosome

1. Values for heterozygote inversions of the third chromosome were often much higher than they should be under the null assumption: if no advantage for any form the number of heterozygotes should conform to Ns (number in sample) = p2+2pq+q2 where 2pq is the number of heterozygotes (see Hardy-Weinberg equilibrium).

2. Using a method invented by L'Heretier and Teissier, Dobzhansky bred populations in population cages, which enabled feeding, breeding and sampling whilst preventing escape. This had the benefit of eliminating migration as a possible explanation of the results. Stocks containing inversions at a known initial frequency can be maintained in controlled conditions. It was found that the various chromosome types do not fluctuate at random, as they would if selectively neutral, but adjust to certain frequencies at which they become stabilised. With D. persimilis he found that the caged population followed the values expected on the Hardy-Weinberg equilibrium when conditions were optimal (which disproved any idea of non-random mating), but with a restricted food supply heterozygotes had a distinct advantage.

3. Different proportions of chromosome morphs were found in different areas. There is, for example, a polymorph-ratio cline in D. robusta along an 18-mile transect near Gatlingsburg TN passing from 1,000 feet to 4,000 feet.[41] Also, the same areas sampled at different times of year yielded significant differences in the proportions of forms. This indicates a regular cycle of changes which adjust the population to the seasonal conditions. For these results selection is by far the most likely explanation.

4. Lastly, morphs cannot be maintained at the high levels found simply by mutation, nor is drift a possible explanation when population numbers are high.

By the time Dobzhansky published the third edition of his book in 1951 he was persuaded that the chromosome morphs were being maintained in the population by the selective advantage of the heterozygotes, as with most polymorphisms. Later he made yet another interesting discovery. One of the inversions, known as PP, was quite rare up to 1946, but by 1958 its proportion had risen to 8%. Not only that, but the proportion was similar over an area of some 200,000 square miles in California. This cannot have happened by migration of PP morphs from, say, Mexico (where the inversion is common) because the rate of dispersal (at less than 2km/year) is of the wrong order. The change therefore reflected a change in prevailing selection whose basis was not yet known.[42][43][44]

Heterostyly

Dissection of thrum and pin flowers of Primula vulgaris

An example of a botanical genetic polymorphism is heterostyly, in which flowers occur in different forms with different arrangements of the pistil and the stamens. The system is called heteromorphic self-incompatibility, and the general 'strategy' is known as herkogamy.

Pin and thrum heterostyly occurs in dimorphic species of Primula, such as Primula vulgaris. There are two types of flower. The pin flower has a long style bearing the stigma at the mouth and the stamens half-way down; and the thrum has a short style, so the stigma is half-way up the tube and the stamens are at the mouth. So when an insect in search of nectar inserts its proboscis into a long-style flower the pollen from the stamens stick to the proboscis in exactly the part that will later touch the stigma of the short-styled flower. And vice versa.[45][46]

Another most important property of the heterostyly system is physiological. If thrum pollen is placed on a thrum stigma, or pin pollen on a pin stigma, the reproductive cells are incompatible and relatively little seed is set. Effectively, this ensures out-crossing, as described by Darwin. Quite a lot is now known about the underlying genetics; the system is controlled by a set of closely linked genes which act as a single unit, a super-gene.[47][48][49]

Between 1861 and 1863 Darwin found the same kind of structure in other groups: flax (and other species of Linum); and in purple loosestrife and other species of Lythrum. Some of the Lythrum species are trimorphic, with one style and two stamens in each form.[50] Heterostyly is known in at least 51 genera of 18 families of Angiosperms.[51][52]



See also

References

  1. Clark, W. C. (1976). "The environment and the genotype in polymorphism". Zool. J. Linn. Soc. 58: 255–262. 
  2. 2.0 2.1 Ford, E. B. (1964). Ecological Genetics. London: Chapman & Hall. 
  3. Huxley J.S. 1955. Morphism and evolution. Heredity 9, 1-52.
  4. Sheppard P.M. 1975. Natural selection and heredity. 4th ed, Hutchinson, London.
  5. 5.0 5.1 5.2 Ford, E.B. (1940). "Polymorphism and taxonomy". In J. Huxley, ed. The New Systematics. Oxford: Clarendon Press. pp. 493–513. 
  6. Wyandt, Herman E. (2004). Atlas of Human Chromosome Heteromorphisms. Dordrecht: Kluwer Academic Publishers. p. 3. ISBN 1-4020-1303-5. Retrieved 2007-03-24. 
  7. Diver C. 1929. Fossil records of Mendelian mutants. Nature 124, 183.
  8. Cain A.J. 1971. Colour and banding morphs in subfossil samples of the snail Cepaea. In Creed R. Ecological genetics and evolution: essays in honour of E.B. Ford. Blackwell, Oxford.
  9. Fisher R. 1930. The Genetical Theory of Natural Selection
  10. Hamilton W.D. 2002. Narrow Roads of Gene Land vol. 2: Evolution of Sex. Oxford
  11. Maynard Smith J. 1978. The evolution of sex. Cambridge
  12. Clarke C.A. 1964. Genetics for the clinician. Blackwell, Oxford
  13. Crow J. 1993. Felix Bernstein and the first human marker locus. Genetics 133, 1, 4-7
  14. Allison A.C. 1956. The sickle-cell and Haemoglobin C genes in some African populations. Ann. Human Genet. 21, 67-89.
  15. Ford E.B. 1942; 7th ed 1973. Genetics for medical students. Chapman & Hall, London.
  16. Ellegren, Hans 2001. Hens, cocks and avian sex chromosomes: a quest for genes on Z or W? EMBO reports 2, 3, 192-196.
  17. Ford E.B. 1975. Ecological genetics, 4th ed. Chapman & Hall, London.
  18. Ford E.B. 1981. Taking genetics into the countryside. Weidenfeld & Nicolson, London.
  19. Chance E. 1922. The Cuckoo's secret. London.
  20. Cain A.J. and Currey J.D. Area effects in Cepaea. Phil Trans B 246: 1-81.
  21. Cain A.J. and Currey J.D. 1968. Climate and selection of banding morphs in Cepaea from the climate optimum to the present day. Phil Trans B 253: 483-98.
  22. Cain A.J. and Sheppard P.M. 1950. Selection in the polymorphic land snail Cepaea nemoralis (L). Heredity 4:275-94.
  23. Cain A.J. and Sheppard P.M. 1954. Natural selection in Cepaea. Genetics 39: 89-116.
  24. Ford E.B. 1975. Ecological genetics, 4th ed. Chapman & Hall, London
  25. Ford E.B. 1971. Ecological genetics. 3rd ed London 1971, chapter7.
  26. Sheppard P.M. 1952. A note on non-random mating in the moth Panaxia dominula (L.). Heredity 6: 239-41.
  27. Sheppard P.M. and Cook L.M. 1962. The manifold effects of the medionigra gene in the moth Panaxia dominula and the maintainance of polymorphism. Heredity 17:415-26.
  28. Majerus, Michael 1998. Melanism: evolution in action. Blackwell, Oxford.
  29. Ford E.B. 1981. Taking genetics into the countryside. Weidenfeld & Nicolson, London.
  30. Ford E.B. Genetic polymorphism Faber & Faber, London.1965
  31. Kettlewell H.B.D. 1973. The evolution of melanism. Oxford.
  32. Majerus, Michael 1998. Melanism: evolution in action. Blackwell, Oxford.
  33. 33.0 33.1 Majerus, M.E.N. (2004)The Peppered moth: decline of a Darwinian disciple. (.doc download)
  34. Rudge D.W. (2005). "Did Kettlewell commit fraud? Re-examining the evidence.", Public Understanding of Science 14 (3) (pp. 249–268).
  35. Young, M. (2003). Moonshine: Why the Peppered Moth Remains an Icon of Evolution.
  36. Gilbert, Francis. 2004. The evolution of imperfect mimicry in hoverflies. In Fellows M., Holloway G. and Rolff J (eds) Insect evolutionary biology.
  37. Sherratt T.N. The evolution of imperfect mimicry. Behavioral Ecology 13, 6, 821-26. CABI
  38. Mallet J. and Joron M. 1999. The evolution of diversity in warning color and mimicry: polymorphisms, shifting balance, and speciation. Annual Review of Ecology and Systematics 30: 201-33.
  39. Painter T.S. 1933. A new method for the study of chromosome rearrangements and the plotting of chromosome maps. Science 78: 585-586.
  40. Dobzhansky T. 1937. Genetics and the origin of species. Columbia University Press, New York. (2nd ed 1941; 3rd ed 1951)
  41. Stalker H.D and Carson H.L. 1948. An altitudinal transect of Drosophila robusta. Evolution 1, 237-48.
  42. Dobzhansky T. 1970. Genetics of the evolutionary process. Columbia University Press N.Y.
  43. [Dobzhansky T.] 1981. Dobzhansky's genetics of natural populations. eds Lewontin RC, Moore JA, Provine WB and Wallace B. Columbia University Press N.Y.
  44. Ford E.B. 1975. Ecological genetics. 4th ed. Chapman & Hall, London.
  45. Darwin, Charles 1862. On the two forms, or dimorphic condition, in the species of Primula, and on their remarkable sexual relations. Journal of the Proceedings of the Linnaean Society (Botany) 6, 77-96.
  46. Darwin, Charles 1877. The different forms of flowers on plants of the same species. Murray, London.
  47. Ford E.B. Ecological genetics. 3rd ed, Chapman & Hall, London 1971 chapter 10.
  48. Sheppard P.M. 1975. Natural selection and heredity. 4th ed Hutchinson, London.
  49. Maynard Smith J. Evolutionary genetics. 2nd ed, Oxford 1998 p86.
  50. Barrett PH (ed) 1977. The collected papers of Charles Darwin. Chicago University Press.
  51. Darlington C. 1971. The evolution of polymorphic systems. In Creed R. (ed) Ecological genetics and evolution. Blackwell, Oxford.
  52. Charlesworth B & D. 1979. The evolutionary genetics of sexual systems in flowering plants. Proc Royal Soc B 205, 513-30.

External links

de:Polymorphismus lt:Polimorfizmas nl:Polymorfisme (genetica)



Linked-in.jpg