GENETICS OF THE COMMON CARP (CYPRINUS CARPIO L) AND OTHER EDIBLE FISHES

by

V.S. Kirpichnikov
Scientific Research Institute on Lake and River Fisheries
Leningrad, U.S.S.R.

1 INTRODUCTION

Among the edible fishes the carp has been the object of most of the studies undertaken so far on genetics of morphological and physiological characters. There are some data available on the genetics of the crucian carp (Carassius auratus L.) but these are concerned chiefly with the inheritance of differences between the aquarium races of the goldfish - a domesticated variety of the crucian carp. The information available on other edible fishes (mainly on the inheritance of single traits) is fragmentary.

Consideration of all categories of hereditary differences found in fish enables one to distinguish four basic groups of traits, namely:

1. Large qualitative morphological-anatomical differences, which are distinctly segregating and rather independent of environment. Hereditary differences in colour and scale patterns of the common and crucian carp belong, in particular, to this category.

2. Quantitative differences in morphological and physiological traits, which are inherited polygenically and affected by environment to a great extent. In this case the expression of the character is determined by the combination of many genes adding to each other (additive action) and to environmental conditions. Variation of body weight, vertebrae number, number of fin rays, variation of many physiological traits, etc., come under this category of hereditary differences in fish.

3. Biochemical differences which are expressed in the variation of blood groups, presence of different forms of haemoglobin and transferring in blood, the presence of some allied forms of enzymes (isozyms) etc. The differences in all these indices are inherited quite distinctly and are determined by a small number of completely segregating genes. In the majority of such cases, codominance is observed - each homozygote is provided with one protein corresponding to the given gene, whereas the heterozygote has both protein characteristic of homozygotes. Usual complete dominance is rarely found.

   The new methods for the detection of fine distinctions in the structure of protein molecules (electrophoresis, serological reactions, transplantation of organs, etc.) enable research of the genetical variability of a population without crossings and hybrid analysis. Direct biochemical examination of the great number of individuals in any population provides the researcher with knowledge of the genetic structure of the population. When applying this method one studies not the specimen's phenotypes but the initial or primary products of gene activity.

4. Phenodeviants, which are deviations (in structure) and malformations found in many domesticated and natural fish populations. Both the number of phenodeviants and degree of deviation grow under inbreeding and unfavourable environmental conditions. As a rule the inheritance of phenodeviants is complicated, and the character often expressed incompletely, sometimes apparently returning to the normal structure. Distinct Mendelian relations are seldom observed in these cases.

As we shall try to show further, these types of hereditary differences are found in all fish irrespective of their systematic position. However, it will be more convenient to consider subsequently the genetics of separate species rather than types of hereditary peculiarities.

2 GENETICS OF POND FISHES

2.1 Common carp and crucian carp

Currently the works by Kirpichnikov and Balkashina (1935, 1936), Golovinskaya (1940), Kirpichnikov (1937), and Probst (1949) demonstrate two pairs of autosomal unlinked genes which determine the type of scaliness in carps. The following carp genotypes are possible:

Carp with genotypes SSNN, SsNN and ssNN are not viable. N gene is lethal in the homozygous state and embryos die in the hatching stage. This gene has a reducing effect on many organs of heterozygous carp (Golovinskaya, 1940; Kirpichnikov, 1945; Probst, 1953).

The data on the heredity of basic types of scaliness have been corroborated by recent works. It is obvious that S and N genes arose in European carp (C. carpio L) as a result of two independent mutations. Later their combination produced the leather carp which is without or almost without scale. There are linear and leather forms among the Japanese carp, C. carpio haematopterus (oral communication). According to K.A. Golovinskaya, the principles for heredity of scale patterns for these carps are identical to that of the European sub-species (C. carpio carpio). Tran dinh Trong (1967) and Kirpichnikov (1967a) have described the mirror and linear carps of Vietnam (sub-species of C. carpio fossicola). Thus, analogous scale genes have arisen among carp belonging to three sub-species which differ quite distinctly. This may serve as a striking example of how Vavilov's law on homologous hereditary variation is expressed in fish (Vavilov, 1935).

Table 1 gives the results of all possible crossings of carp having different types of scale patterns. Segregation corresponds to the expected pattern; but the number of linear and leather carps is low due to their lower viability. At lower mortality rates, the correspondence of the actual and theoretical frequencies may be closer.

Table 1

Scale cover inheritance in common carp

Sc: scaled, St: scattered, Lin: linear, Leath: leather

	Fig.1 Types of scale cover in common carp: a) - scaled, b) - scattered, c) - linear, d) - leather.
Fig. 2 Electrophoregram of haemoglobins in fish (scheme). a and b - homozygous, c - heterozygous geno-types.

Golovinskaya (1946) crossed a female linear carp with two leather males and obtained the following:

Two heterozygous linear spawners, when crossed, yielded the following segregation (Wohlfarth, Lahman and Moav, 1963):

In both cases, the number of linear and leather fingerlings was less, whereas the scaled and scattered ones were more numerous than expected. The lower viability of carps with N gene is due to the pleiotropic effect of this gene. Alleles of another series, S and s, have the pleiotropic effect as well: many organs of carps are affected by the scale genes and many morphological and physiological characters are changed (Table 2). Most striking is the difference between carp with and without N gene (one linear and leather, the other scaly and scattered). Among the characters which are affected by N gene, the one to be mentioned particularly is the number of pharyngeal teeth, as can be seen in linear and leather carps.

Table 2 ¹

Pleiotropic effect of scale genes in carp. Sc: scaly, St: scattered, Lin: linear, Leath: leather carps

¹ Literature source: 1. Golovinskaya, 1940; 2. Kirpichnikov, 1945, 1948; 3. Probst, 1953; 4. Steffens, 1966; 5. Chan mai-Tchien, 1968.
²Expressed as percentages of the values of incidence of the same characters in scaly carp.

Instead of the usual three rows of pharyngeal teeth (1.1.3–3.1.1) we often find two or only one row of them (1.3–3.1; 1.3–3 and 3–3 respectively).

According to Probst (1953) the reduction of many organs observed in linear and leather carp is accompanied by a defect in the mesenchyme development. There is doubt that N gene represents a major mutation (perhaps of the deletion type) completely destroying the synthesis of one or more proteins of vital importance. This may explain the decrease in viability in heterozygotes with N gene and mortality of all homozygotes. The difference in the structure of the swim bladder is to be considered a result of one of the pleiotropic effects of s gene. When s gene is present the back chamber is shorter than the front one (scattered carps); with normal allele S it is, on the contrary, longer (scaly carp).

Carp with different scale genes may be distinguished by means of serological methods as well. Altuchov et al. (1966) and Pochil (1967) have been able to differentiate between all the four genes by means of erythrocyte antigens.

The colour of carp is a character inherited distinctly and, in the majority of cases, simply. Most numerous and varied are the types of colours found in carps of Japan, Vietnam and Indonesia.

The heredity of blue colour of Polish carp has been analysed. A ratio near 3:1 has been obtained for the second generation, the number of blue fingerlings varying from 20.3 to 23.8 percent (Wlodek, 1963). Blue carp were characterized by somewhat lower viability. They at first grow better than common carp and then lag behind them. For the German blue carp, the ratio of F₂ and F_b (backcross) proved to be near to that expected (3:1 and 1:1 respectively) and no differences in viability were found. Blue Israeli carp (b gene), similar to Polish ones, were inferior to non-coloured carp both in viability and growth rate. In all the three cases the mutant form was recessive. Two more recessive mutations for colour - gold (g gene) and grey (gr gene), were found in Israeli carp. In one of them, all were homozygous by g gene and, in another, by b and gr genes. Although both lines fell behind the non-coloured ones in viability and growth rate, the crossings between them produced non-coloured (yellowish) carp with high fishery management indices:

non-coloured (heterozygotes)

All three genes proved to be autosomal and not linked with each other.

There are many coloured variations of carp in Japan, including yellow, blue, red, red and white, spotted, etc. The heredity of these types of colour has not yet been analyzed, but it is known that they are determined by both dominant and recessive mutations. Studies of the red, brown, violet, black and multicoloured variations of Vietnam and Indonesian carp, and carp of China, Korea and other countries of east and south Asia are needed. One may only note that similar mutations of colouring arise among carp inhabiting various countries and belonging to various sub-species. Thus, homologous variability is being presented by this character also (Kirpichnikov, 1967a).

Quantitative differences, inherited polygenically, compose the second rather numerous category of hereditary differences in carp. The best study is that concerned with the heredity of the number of rays in the dorsal fin and vertebrae number. There are some data on the heredity of other characters including growth rate and body shape. While crossing one female having 20 soft rays in the dorsal fin with different males, the results were as follows (Kirpichnikov, 1961):

Correlation between the number of rays in the offspring and in the males proved to be low, but quite reliable (r=0.326 ± 0.021). The correlation was more significant (+0.76 ± 0.07) when the cultured carp, Amur wild carp and the hybrids between the two (various generations) were compared. If we consider one generation (for example the third hybrid generation) the correlation coefficient is slightly lower (r=+0.60 ± 0.14).

The inheritance of vertebrae number has a polygenic character as well. We have analyzed six crossings which can be sub-divided into two groups:

The volume of the material was too small to estimate the correlation coefficients; however, it was clear that the number of vertebrae in carp was determined by the large number of genes and was dependent to a great extent on environment. According to Nenashev (1966) the heritability coefficient of these two characters is equal for carp (0.4–0.6), i.e., the values of the environmental and genotypical effects are approximately equal.

The body height of carp is inherited polygenically as well. Israeli breeders selected carp with different height indices (H/1). Offspring of these carp had the following means (Moav and Wohlfarth, 1967):

Body weight index (H/1 percent)
(Height in percent of length)

Realized heritability proved to be equal to 0.42. Thus the genetic differences between the various carps were rather considerable in this case as well.

Growth characters (weight and length increments) are most important characters in this group of traits. The heritability of body weight of carp fingerlings is not high (0.1–0.2) and the influence of environment on this character is rather great (Kirpichnikov, 1966a, 1967b; Nenashev, 1968). Heritability indices for weight in carp of older age are somewhat higher, but their exact values are not stated (Kirpichnikov, 1966b). Selection for weight is effective in the negative direction but, at the same time, rather often there is no manifestation in the positive direction (Moav and Wohlfarth, 1963, 1967). The differences in growth rate are inherited non-additively. It is quite probable that there exist, in carp populations, heterozygous systems balanced for this character, and heterozygotes grow, as a rule, better than homozygotes (Kirpichnikov, 1958). Inbreeding, responsible for the increase of homozygosity in carp, brings forth the drop in its growth rate (Moav and Wohlfarth, 1967).

Numerous physiological indices are to be considered among the characters of carp inherited polygenically; unfortunately no data are available so far on the mechanism of their heredity. There is no information on the heredity of fine biochemical differences as well. The existence of polymorphism of transferrins has been found (Creyssel et al., 1964). One may only point out that when crossing common carp with crucian carp the differences in the characters of esterase are inherited codominantly (Takayama et al., 1966).

Phenodeviants have been discovered in many highly inbred populations and stocks of carp. While selecting the Ropsha carp we observed, as a result of some crossings, the appearance of mirror carp characteristic of a peculiar coating on the body and an extremely low growth rate (Kirpichnikov, 1961).

Malformations of vertebral column, various degrees of reduction of gill cover, deformations of fins, etc., are recorded for many families of carp. Similar abnormalities are often found in the carp of central regions of the Russian Soviet Federal Socialist Republic, North Caucasus and other regions of the U.S.S.R. The deviations of one type vary from 0.1–0.2 percent to 20–30 percent or more, the frequency depending on the degree of inbreeding and the environmental conditions under which the fry are reared. In all these cases, we may say that there exists a certain hereditary predisposition to malformations; to be more exact, they are determined both by environment and genotype (Tatarko, 1961, 1966).

No gene linkage has been found in carp so far. The mechanism of sex determination has not yet been determined either. This is due mainly to the large number of chromosomes in carp (2n=104). Diploid number of chromosomes of many cyprinids is equal to 50–52, which allows us to consider the common carp as a natural (very ancient) tetraploid (Ohno et al., 1967).

Most essential studies on genetics of goldfish have been carried out by Japanese and Chinese scientists. Chen (1928, 1934) has shown that the blue and brown colours characteristic of some strains, as well as transparency of cutaneous covering, are inherited by means of a small number of genes. Absolute and mosaic transparency are determined according to Matsui (1934b) by the combination of two pairs of genes. Semi-dominant T gene (absolute transparency) is epistatic in homozygous state to recessive n gene (from another pair) causing frame location of coloured and non-coloured sections. Eyes of goldfish may be telescopic due to the presence of one recessive gene, while elongated, bifurcate fins arise in goldfish as a result of interaction of not less than two or three pairs of genes (Matsui, 1934a and c).

Many peculiarities of goldfish have not yet been studied from the genetic point of view, though some varieties of goldfish have existed for many centuries, in particular the red forms which appeared in the 10th century (Chen, 1956). Numerous small and large mutations had accumulated in all strains during past centuries. Hence it is clear that the differences between strains must be of polygenic character and it is rather difficult to analyze them.

According to the results of the experiments on scale transplantation it may be assumed that not less than four genes of histological incompatibility are present in one population of goldfish (Hildemann and Owen, 1956). The comparative analysis of morphological (quantitative) and biochemical variation of unisexual and bisexual forms of the crucian carp is of great interest from this point. The fact that male chromosomes do not participate in embryo development must cause (in unisexual lines) a sharp increase of homozygosity in populations, i.e., almost a complete exclusion of hereditary variation. It enables one to distinguish a pure paratypical (environmental) variation of fish and compare its value with that of total (phenotypical) variation in usual bisexual panmictic populations.

2.2 Other fishes: tench, orfe, catfish, trout and tilapia

No data are available on the genetics of tench (Tinca tinca L.). It is only known that the growth rate of tench has considerably improved due to selection operating through a number of generations. Differences in growth rate are inherited apparently polygenically.

Orfe (Leuciscus idus L var. orfus), cultivated in some European countries, is an albino form of a common lake-river ide. Evidently, orfe appeared as a result of recessive mutation selected by man. Identical albino forms were found in channel catfish (Ictalurus punctatus), which is at present the main species used for warm-water pond fish culture in the U.S.A. In this fish, the lack of black pigment is due to the presence of one recessive gene (Nelson, 1958). Albino mutants are found in other pond fishes as well.

The American breeders of the rainbow trout Salmo gairdneri Roch. and char (Salvelinus fontinalis) have succeeded in improving their growth rate, rate of maturing, increase in fertility and resistance to diseases (Hayford and Embody, 1930; Donaldson and Olson, 1955). The differences for all these characters in salmonids are determined by the large number of genes. Polygenic inheritance of many morphological and physiological characters is apparently characteristic of Tilapia and other pond fishes.

Only few genetic studies have been conducted on the cyprinids of India (Catla, Labeo, Cirrhina) and China (Ctenopharyngodon, Mylopharyngodon, Hypophthalmichthys, Aristichthys), the sunfish cultured in America (Centrarchidae), as well as a number of species cultured in Indonesia, Philippines and other Asian countries. However, undoubtedly, the basic categories of hereditary variation found in carp will soon be discovered in all fishes cultured in ponds. Differences in the biochemical level are reported so far only in trout, carp and some sunfishes.

3 GENETICS OF EDIBLE FISH INHABITING NATURAL WATER BODIES

Striking quantitative differences have been found in many species of wild fishes, but only in a few cases were they analyzed from a genetic point of view. In all those cases, heredity proved to be monofactorial. The quantitative (polygenic) differences of fish have also been insufficiently studied.

Schmidt (1920) conducted experiments to test the heredity of vertebrae number in Zoarces viviparus L, a trait which depends on the combination of many genes. Each local population of Z. viviparus L is characterized by a certain average number of vertebrae fixed by heredity. Svärdson (1952, 1957) has stated the hereditary nature of differences in the number of gill rakers between the whitefish populations of the genus Coregonus. In this case successful selection in both positive and negative directions is indicative of the polygenic nature of hereditary variation. By analogy we may expect to find, in all fresh-water and sea fish, large groups of quantitative characters inherited polyfactorially.

More data are available on biochemical hereditary polymorphism of natural fish populations. New methods of research, especially electrophoresis and serological reactions, have increased the collection of information on genetical structure of fish populations during the last 10–15 years. All fishes under investigation have shown intraspecific genetic variation of blood groups. The presence of two or more blood groups in one population has been demonstrated for the herring and pilchard (Cushing, 1964; Vrooman, 1964; Altuchov et al., 1968), Norway haddock (Sindermann, 1962), anchovy and horse mackerel (Limansky, 1964). Large variation of blood groups is characteristic of different salmonid species. After Taliev (1941) a number of studies relating to the problem has been undertaken. Californian gold trout (Salmo aguabonita) has shown individual and population differences in blood groups. At the same time, no considerable serological alterations were recorded for the species during the 90 years which passed after acclimatization of that trout in a water body new to it. An inbred trout population in Summit Lake, Nevada, is immunologically homogenous, while pond rainbow trout have several serologically distinguishable groups.

Each population of Katsuwonus pelamis L, Thunnus germo Gm and other Pacific tuna proved to be polymorphous in regard to one, two or three erythrocyte-antigen systems. Most typical of tuna (as well as of the other fishes) are 3-allele systems of ABO type similar to the same system of blood groups in man; the latter are characteristic of the presence of four serologically distinguished phenotypes (A, B, AB and O). Various populations differ distinctly in the proportion of phenotypes.

The results of research on blood groups of fish are presented in detail in the reviews of Cushing (1964) and Altuchov (1968). A most important result of this field of research is the evidence of the presence of wide intrapopulation polymorphism for blood groups in fish.

Genes of each allele system are, as a rule, in equilibrium. Homozygote and heterozygote frequencies correspond to the Hardy-weinberg equilibrium:

p²(AA) + 2pq(AA₁) + q²(A₁A₁) = 1

Single local populations have stable distinctions for allele concentrations.

The application of the electrophoretic method permits the study of genetical variation of fish for haemoglobins, transferrins, muscle and serum proteins. Let us consider the results of the most interesting investigations.

Norwegian scientists, K. Sick and others, have discovered the presence of genetical polymorphism for genes Hb_1-1 and Hb_1–2 in cod (Frydenberg, et al., 1965; Sick, 1965a). The concentration of Hb_1–2 gene regularly decreases from east to west in the Baltic Sea and coastal zone of Norway. The number of heterozygotes for which haemoglobins have been determined with electrophoresis (Fig.2) correspond, in the majority of cases, to expectation according to Hardy-Weinberg equilibrium. It is reasonable to assume that alteration in the structure of haemoglobin is determined for cod, as well as for man, by point mutation - alteration of one base in the gene chain of DNA, which is responsible for haemoglobin synthesis. Specimens with other genetical types of haemoglobin occur in the North Sea and coastal zone of Greenland and America (Sick, 1965b).

The American species of eel (Anguilla rostrata (Le Sueur) unlike the European one, is polymorphic. There is in its population an additional haemoglobin gene in concentration of about 3.3 percent. The frequencies of genotypes proved to be in equilibrium. Studies have been made of 623 homozygotes for normal allele, 42 heterozygotes with two bands in electrophoretic field and one homozygote for mutant allele, at theoretical figures 622:43:1. Thus two species of eel are to be considered as two generatively isolated populations (Sick et al., 1967).

Polymorphism for haemoglobin genes has been discovered in other edible fish as well. It should be noted that when crossing allied fish species the hybrids show the hybrid haemoglobins in addition to parental ones. The haemoglobin molecule of both fish and higher vertebrates is a polymer. Hybrid haemoglobin was discovered by Manwell et al. (1963) in offspring from crossing between the different species of sunfish, and by Sick et al. (1963) while crossing two species of plaice.

Genetical polymorphism for transferrins has been recorded for cod and four species of tuna. Tuna are polymorphic for serum esterase. Three species of tuna (Barrett and Tsuyuki, 1967; Jamieson, 1967) have been studied and were found to be provided with two, three and four alleles of esterase respectively (Sprague, 1967). Herring proved to be variable for lactate dehydrogenase and aspartate aminotransferase (Odense et al., 1966); roach for esterase (Nyman, 1965); walleye (Stizostedion vitreum) for myogens, and trout for lactate dehydrogenase (Morrison and Wright, 1966).

A large number of works concerning the above problems have appeared recently. Apparently all fishes are characterized by the large genetic variation for protein structure, while many allele systems are in equilibrium. The electrophoretic method is especially convenient for the study of genetic structure of a population due to the simplicity of detection of heterozygotes (the presence of two bands on the paper). The heredity of biochemical differences in fish is primarily codominant. We deal with the initial products of gene activity or with their derivatives in these cases. Codominance is a result of the presence in heterozygotes of two such products instead of one.

Additional information on the biochemical polymorphism of fish populations may be provided with the experiments on tissue transplantation. So far, the experiments of such type have been conducted chiefly on aquarium fish; however, this method proved to be advantageous when analyzing the degree of homogeneity of small populations (for example, local stocks of reds and other anadromous Salmonidae). Recently, a comparison was carried out between heat resistance of muscles and muscular proteins of some races of salmonid fish (Coregonus autumnalis and Thymallus arcticus) of Baikal Lake (Ushakov et al., 1962) and that of Norway haddock from different parts of the northwestern Atlantic (Altuchov et al., 1967). Intraspecific differences have been discovered for this trait which also may be considered as biochemical polymorphism.

After the discovery of the biochemical polymorphism of genetic origin in fish the question arose about the factors responsible for it. The following explanations were put forward:

1. polymorphism is connected with the selective preference of heterozygotes for the single genes (Ford, 1966);

2. polymorphism is a result of an alternating (in time and space) adaptation of two closely relate, but biochemically distinguishable, homozygotes (AA and A₁A₁) or homozygote and heterozygote (AA and AA₁). In this case, the first genotype is better adapted to one environment, and the second one to another environment (Timofeeff-Ressovsky and Svirezhev, 1967).

3. polymorphism is transient - in the past, individuals of one genotype were better adapted, but at present, another one is better (one allele has been substituted for another).

The first two mechanisms are undoubtedly found in fish. Examples of transient polymorphism are not known for fish at present. The application of the new methods for genetic analysis of fish populations inhabiting natural water bodies resulted in the quick development of research on fish genetics and selection. Laws for the inheritance of many variable characters, especially biochemical peculiarities, have been discovered. The most recent genetic works provide us with valuable information on the intraspecific differentiation in fish, nature of differences between populations and variation within populations. Many species seemed to consist of sub-species or smaller systematic groups which proved to be sufficiently isolated and well distinguishable genetically. The introgression between those groups was not large in the majority of cases.

We shall not consider the problem of genetics of aquarium fish. There are numerous special works dealing with it. We may refer to the recent surveys by Gordon (1957); Petzold (1967); and Kirpichnikov (1968). The problems of karyology shall not be considered either. We shall only note that variability of chromosomes based on so-called Robertson translocations is rather frequently found in fish (Simon, 1963; Roberts, 1964). However, the variation of chromosome number occurring in case of such translocations is not accompanied by the change of the number of arms, and it is apparent that the amount of DNA in a chromosome set does not vary either. Sometimes this type of difference in chromosome number is observed within one population; in others, two different populations may be distinguished by this character. Karyological variability of this type is to be considered as one more highly essential form of hereditary differences in fish.

4. REFERENCES

Altuchov, Iu.P., 1968 On immunogenetic approach to the analysis of intraspecific differentiation in fishes. Usp.sovrem.Genet. (in press)

Altuchov, Iu.P., A.N. Matveeva and B.M. Pusanova, 1966 Heat-resistance of muscular tissues and antigens properties of erythrocytes in some cultured carp varieties. Tsitologia, 8(1):100–4 (In Russian)

Altuchov, Iu.P., G.N. Nefiodov and A.N. Pajusova, 1967 A cytophysiological analysis of divergence between Sebastes marinus and S. mentella (redfishes) from north-west Atlantic. In Izmenchiv. teploustoych. kletok zhyvotn. v ontogen. i phylogen., Leningrad, Nauka, pp.82–98

Altuchov, Iu.P., et al., 1968 A system of blood groups in Atlantic herring. Genetika, 4(2): 155–67 (In Russian)

Barret, J. and H. Tsuyuki, 1967 Serum transferring polymorphism in some scombroid fishes. Copeia, 3:551–7

Chan-Mai-Tchien, A new data for pleiotropy of scale genes in carp. Trudy Soveshch.genet., Selekts. Gibridiz.Ryb. (in press)

Chen, S.Ts., 1928 Transparency and mottling, a case of mendelian inheritance in the goldfish, Carassius auratus. Genetics, Princeton, 13:434–52

Chen, S.Ts., 1934 The inheritance of blue and brown colours in the goldfish, Carassius auratus. J.Genet., 29:61–74

Chen, S.Ts., 1956 A history of the domestication and the factors of the varietal formation of the common goldfish, Carassius auratus. Scientia sin., 5(2):287–321

Creyssel, R. et al., 1964 Etude du serum de carpe (Cyprinus carpio) par electrophorese en gel d'amidon. Bull.Soc.Chim.biol., 46:149–59

Cushing, J.E., 1964 The blood groups of marine animals. Adv.mar.Biol., 2:85–131

Donaldson, L.R. and P.R. Olson, 1955 Development of rainbow trout breed stock by selective breeding. Trans.Am.Fish.Soc., 85:93–101

Ford, E.B., 1966 Genetic polymorphism. Proc.R.Soc., (B), 164(995):362–89

Frydenberg, O. et al., 1965 Haemoglobin polymorphism in Norwegian cod populations. Hereditas, 53:255–71

Golovinskaya, K.A., 1940 Pleiotropic effect of scale genes in carp. Dokl.Akad.Nauk SSSR 28(6):533–6

Golovinskaya, K.A., 1946 On the linear form of cultured carp. Dokl.Akad.Nauk SSSR, 54(7):637–40

Gordon, M., 1957 Physiological genetics of fishes. In The physiology of fishes. Behaviour, edited M.E. Brown, New York, Academic Press Inc., Vol.2:431–501

Hayford, C.O. and G.C. Embody, 1930 Further progress in the selective breeding of brook trout at the New Jersey State Hatchery. Trans.Am.Fish.Soc., 60:109

Hildemann, W.N. and B.D. Owen, 1956 Histocompatibility genetics of scale transplantation. Transplantn.Bull., 3(4)

Jamieson, A., 1967 New genotypes in cod in Greenland. Nature, Lond., 215(5101):661–2

Kirpichnikov, V.S., 1937 Principal genes of scale in carp. Biol.Zh., 6(3):601–32

Kirpichnikov, V.S., 1945 The influence of environmental conditions on viability, rate of growth and morphology of carp (of) different genotypes. Dokl.Akad,Nauk SSSR, 47(7):521–5

Kirpichnikov, V.S., 1948 The comparative characteristic of four principal forms of cultured carp by their breeding in North USSR. Izv.vsesoiuz.nauch.-issled.Inst.ozer.rech.ryb. khoz., 26(2):145–70

Kirpichnikov, V.S., 1958 Heterogeneity in populations of wild carp and of hybrid between cultured and wild carp. Dokl.Akad.Nauk SSSR, 122(4):716–9

Kirpichnikov, V.S., 1961 Die genetischen Methoden der Selektion in der Karpfenzucht. Z.Fisch., 10(⅓):137–63

Kirpichnikov, V.S., 1966a Goals and methods of carp selection. Izv.gosud.nauchno-issled.Inst.ozer. rech.ryb.Khoz., 61:7–27

Kirpichnikov, V.S., 1966b The methods of progeny testing in carp breeding. Izv.gosud.nauchno-issled. Inst.ozer.rech.ryb.Khoz., 61:40–61

Kirpichnikov, V.S., 1967a Homologous genetic variability and evolution of wild carp. Genetika, 3(2):34–47 (In Russian)

Kirpichnikov, V.S., 1967b The general theory of heterosis, I. genetic mechanisms. Genetika, 3(10): 167–79 (In Russian)

Kirpichnikov, V.S., 1968 The modern state of genetics of fishes. Trudy Soveshch.Genet.Selekts. Gibridiz.Ryb. (in press)

Kirpichnikov, V.S. and E.J. Balkashina, 1935 Materials on genetics and selection of carp. 1. Zool.Zh., 14(1):45–78 (In Russian)

Kirpichnikov, V.S., 1936 Materials on genetics and selection of carp. 2. Biol.Zh., 5(2):327–76 (In Russian)

Limansky, V.V., 1964 The analysis of intraspecific differentiation in some fishes of Black and Azov seas by means of precipiting reaction. Vop.Fiziol.Ryb chern.azov. Morey, pp.31–9

Manwell, Cl., C.M.A. Baker and W. Childers, 1963 The genetics of hemoglobin in hybrids. 1. A molecular basis for hybrid vigor. Compar.Biochem.Physiol., 10:103–20

Matsui, Y., 1934a Genetical studies on goldfish of Japan. 2. On the Mendelian inheritance of the telescope eyes of goldfish. J.imp.Fish.Inst., Tokyo, 30(1):37–46

Matsui, Y., 1934b Genetical studies on goldfish of Japan. 3. On the inheritance of the scale transparency of goldfish. J.imp.Fish.Inst., Tokyo, 30(1):47–66

Matsui, Y., 1934c Genetical studies on goldfish of Japan. 4. On the inheritance of caudal and anal fins of goldfish. J.imp.Fish.Inst., Tokyo, 30(1):67–96

Moav, R. and G.W. Wohlfarth, 1963 Breeding schemes for the genetic improvement of edible fish. Prog.Rep., Israel-U.S. Fish Wildl.Serv., 1962:39 p.

Moav, R., 1967 Breeding schemes for the genetic improvement of edible fish. Prog.Rep., Israel-U.S. Fish Wildl.Serv., 1964–5:61 p.

Morrison, W.J. and J.E. Wright, 1966 Genetic analysis of three lactate dehydrogenase isozyme systems in trout: evidence for linkage of genes coding subunits A and B. J.exp.Zool., 163(3):259–70

Nelson, B., 1958 Progress report on golden channel catfish. Proc.stheast.Ass.Game Commrs, 12:75–7

Nenashev, G.A., 1966 Heritability of some morphological (diagnostic) characters in Ropsha carps. Izv.gosud.nauchno-issled.Inst.ozer.rech.ryb.Khoz., 61:125–35

Nenashev, G.A., 1968 Heritability of some selective characters in carp. Izv.gosud.nauchno-issled. Inst.ozer.rech.ryb.Khoz., 65:185–92

Nyman, L., 1965 Inter- and intraspecific variations of proteins in fishes. Ann.Acad.Rega sci. Uppsala, 9:1–18

Odense, P.H., T.M. Allen and T.C. Leung, 1966 Multiple forms of lactate dehydrogenase and aspartate aminotransferase in herring (Clupea harengus harengus L.). Canad.J. Biochem., 44:1319–26

Ohno, S. et al., 1967 Diploid-tetraploid relationship among old-world members of the fish family Cyprinidae. Chromosoma, 23(1):9 p.

Petzold, H.-G., 1967 Der Guppy (Poecilia, Lebistes) reticulata. Wittenberg, Lutherstadt, A. Ziemsen Verl., 142 p.

Pochil, L.J., 1967 The erythrocytes antigens of carp (Cyprinus carpio L.), grass carp Ctenopharyngodon idella Vall.) and crucian carp (Carassius auratus gibelio Bloch). Trudy Vsesoiuz.nauchno-issled.Inst.prud.ryb.Khoz., 15:278–83

Probst, E., 1949 Vererbungsuntersuchungen beim Karpfens. Allg.Fischztg., 21:436–43

Probst, E., 1953 Die Beschuppung des Karpfens. Münch Beitr.Abwass.-Fisch.u.Flussbiol., 1:150–227

Roberts, F.L., 1964 A chromosome study of twenty species of Centrarchidae. J.Morph., 115(3): 401–18

Schmidt, J., 1920 Experimental investigations with Zoarces viviparus L. C.R. Trav.Lab. Carlsberg, 14(9):1–14

Sick, K., 1965a Haemoglobin polymorphism of cod in the Baltic and the Danish Belt sea. Hereditas, 54(1):19–48

Sick, K., 1965b Haemoglobin polymorphism of cod in the North Sea and the North Atlantic Ocean. Hereditas, 54(3):49–69

Sick, K., O. Frydenberg and J.T. Nielsen, 1963 Haemoglobin patterus of plaice, flounder and their natural and artificial hybrids. Nature Lond., 198:411–2

Sick, K. et al., 1967 Haemoglobin polymorphism of the American fresh water eel Anguilla. Nature Lond., 214(5093):1141–2

Simon, R.C., 1963 Chromosome morphology and species evolution in the five North American species of Pacific salmon (Oncorhynchus). J.Morph., 112:77–97

Sindermann, C.J., 1962 Serology of Atlantic clupeoid fishes. Am.Naturalist, 96:225–31

Sprague, L.M., 1967 Multiple molecular forms of serum esterase in three tuna species from the Pacific Ocean. Hereditas, 57(½):198–204

Steffens, W., 1966 Die Beziehungen zwischen der Beschuppung und dem Wachstum sowie einigen meristischen Merkmalen beim Karpfen. Biol.Zbl., 85(3):273–88

Svärdson, G., 1952 The coregonid problem. IV. The significance of scales and gillrakers. Rep.Inst.Freshwat.Res., Drottningholm, 33:204–32

Svärdson, G., 1957 The coregonid problem. VI. The palearctic species and their intergrades. Rep.Inst.Freshwat.Res., Drottningholm, 38:267–356

Suzuki, A., 1962 On the blood types of yellowfin and bigeye tuna. Am.Naturalist, 96(889): 239–46

Takayama, S., Y. Ojima and A. Hamaguchi, 1966 Cytogenetic studies in lower vertebrates. III. Some aspects of esterase pattern in the carp (Cyprinus carpio), buna (Carassius auratus) and their hybrids. Annot.zool.jap., 39(4):211–4

Taliev, D.N., 1941 Serological analysis of races of Baikal Omul (Coregonus autumnalis migratorius Georgi). Trudy zool.Inst., Leningr., 6(4):68–92

Tatarko, K.I., 1961 The aberrations in structure of gill cover and fins in carp. Vop.Ikhtiol., 1(3):412–20

Tatarko, K.I., 1966 Anomalies of the carp and their causes. Zool.Zh., 45(12):1826–34 (In Russian)

Timofeeff-Ressovsky, N.W. and Iu. M. Svirezhev, 1967 On the genetic polymorphism in populations, experimental and theoretical studies. Genetika, 3(107):152–66 (In Russian)

Tran dinh-Trong, 1967 Data on the intraspecific variability, biology and distribution of the carps in North Vietnam (Democractic Republic of Vietnam). Genetika, 3(2): 48–60 (In Russian)

Ushakov, B.P., A.N. Vinogradova and A.A. Kusakina, 1962 Cytophysiological analysis of intraspecies differentiation of Coregonus autumnalis and Thymallus arcticus of the Baikal Lake. Zh.obshch.Biol., 23(1):56–63 (In Russian)

Vavilov, N.J., 1935 The law of homologous lines in hereditary variation. Teoret.osnovy selekts. rast., 1:75–150

Vrooman, A.M., 1964 Serologically differentiated subpopulations of the Pacific sardine, Sardinops caerulea. J.Fish.Res.Bd.Can., 21(4):691–701

Wlodek, J.M., 1963 Der blaue Karpfen aus der Teichwirtschaft Landek. Acta hydrobiol., Krakow, 5(4):383–401

Wohlfarth, G.W., M. Lahman and R. Moav, 1963 Genetic improvement of carp. IV. Leather and line carp in fish ponds of Israel. Bamidgeh, 15(1):3–8