The Journal of Heredity 2001:92(1)
© 2001 The American Genetic Association 92:74-78
Brief Communication |
A Second Acromelanistic Allelomorph at the Albino Locus of the Mongolian Gerbil (Meriones unguiculatus)
Fred Petrij is affiliated with the Department of Clinical Genetics, Erasmus University, Westzeedijk 112, 3016 AH Rotterdam, The Netherlands.
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Abstract |
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 Top Abstract IntroductionDescription of the MutantBreeding DataDiscussionReferences |
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A new autosomal recessive coat color mutant in the Mongolian gerbil (Meriones unguiculatus) is described: chinchilla medium (symbol cchm). The mutant has typical acromelanistic features similar to those of several acromelanistic c locus mutants of other species of mammals. Previously a more severe form of acromelanism (chch) has been described in the Mongolian gerbil. The new allele shows to be allelic with this form. On a nonagouti background compound heterozygotes (aacchmch) show an intermediate phenotype that is very similar to that of the Siamese mouse (Mus musculus) and rat (Rattus norvegicus). Homozygotes (aacchmcchm) display a very dark acromelanistic phenotype reminiscent of that of the sable rabbit (Oryctolagus cuniculus). The gray phenotype (gg) in the Mongolian gerbil resembles the albino locus phenotype chinchilla (cchcch) in mice. We show that the new mutant is not allelic with gray. Fertility and viability of the new mutant are within normal range.
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Introduction |
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TopAbstractIntroductionDescription of the MutantBreeding DataDiscussionReferences |
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In 1866 the French Father Armand David sent some specimens of an unknown rodent species to the Musée d'Histoire Naturelle in Paris. At that time "père Armand" was staying in "la Mongolie chinoise," perhaps what is now known as northwestern Shansi, China (Allen 1940). In 1867 Milne Edwards described these specimens as Gerbillus unguiculatus (Milne Edwards 1867). Later, in 1908, they were reassigned by Thomas to Meriones and denominated Meriones unguiculatus (Thomas 1908). Popular names are Mongolian gerbil and clawed jird (Gulotta 1971). Observations of these animals in their natural environment are described by Åren et al. (1989).
Mongolian gerbils have been bred in laboratories since 1935, when Dr. C. Kasuga caught 20 pairs in the basin of the Amur River in eastern Mongolia. They were sent to the Kitasato Institute with the intention of using them for rickettsial studies. Miss Michiko Nomura (Central Laboratories for Experimental Animals) obtained some animals from the Kitasato Institute in 1949, and in 1954 she sent four pairs of their offspring to Dr. Victor Schwentker at Brant Lake, New York. He established the first commercial colony in America at the Tumblebrook Farm. At that time many if not all investigators obtained their stock from Dr. Schwentker's colony (Rich 1968). Since then Mongolian gerbils are used in scientific research all over the world.
Mongolian gerbils can be managed quite easily and thrive on a diet of commercial rodent pellets. They are curious, gentle, easy to handle, and stress resistant. They can be transported without problems, reproduce throughout the year and are economical with water consumption, consequently their urine production is low. Their cages remain relatively dry and odorless unlike those of mice (Mus musculus) and rats (Rattus norvegicus). Mongolian gerbils can tolerate high population densities in captivity. All these features, combined with the fact that Mongolian gerbils are active both day and night, have made them very popular as pets and for fancy breeding mainly in Europe and the United States.
Gerbils have been used in pharmacological, parasitological, endocrinological, and cancer research. Their susceptibility to different types of bacteria and viruses has also been studied (Gulotta 1971; Rich 1968). They seem to have an unexpectedly high resistance to radiation (Chang et al. 1964). Because of their naturally high incidence (1 in 5 animals) of seizures (Thiessen et al. 1968) they have been used in many types of neurological research (Ellard et al. 1990; Gray-Allan and Wong 1990; Loskota et al. 1974a,b). Probably because of their distinct social behavior, they were used in many types of behavioral studies as well (Kaplan and Hyland 1972; Thiessen and Yahr 1977; Walter et al. 1963).
Surprisingly enough, Mongolian gerbils have rarely been used in genetic research. Their diploid number of chromosomes is 44, containing 22 metacentric, 10 submetacentric, and 10 acrocentric autosomes, a large submetacentric X and a smaller submetacentric Y chromosome (Nadler and Lay 1967). Between 1970 and 1985 seven mutants arose in scientific laboratory and pet populations (see Table 1). Recently we discovered four new coat color mutants in the Mongolian gerbil, three in pet populations and one in a laboratory population. Two of them are allelic and possibly related to the extension locus (Petrij F, unpublished data). The third one seems to be the dilution mutation (Pund T and Petrij F, unpublished data), a well-known coat color mutation, which is described in many other mammalian species (Searle 1968). The fourth one has proven to be allelic to the albino locus and will be discussed here.
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Description of the Mutant |
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TopAbstractIntroductionDescription of the MutantBreeding DataDiscussionReferences |
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In November 1994 a British fancier discovered animals with two new phenotypes in a pet shop in the Republic of Ireland. Both phenotypes were of an acromelanistic type, although one was lighter than the other. He brought one dark- and three light-colored animals to the United Kingdom (Barker J, personal communication). About 1 year later offspring of these animals were imported to The Netherlands and Germany by fanciers. These animals formed the nucleus of our breeding experiments.
The darker version has a light brown body (see Figure 1A). The ventral side is slightly lighter in color in comparison to the dorsum. No clear demarcation line can be determined. The color is clearly lighter and more creamy than that of the dark sepia (Leiper and Robinson 1985) Mongolian gerbil (aagg). Compared with the typical brown coat color (aabb) of other rodents, such as mice (Searle 1968; Silvers 1979), the coat color of the new mutant is a lighter shade of brown. Nose, ears, and feet are covered with dark sepia hairs and the tail hairs are almost black. The scrotum is dark colored and covered with hairs that resemble the color of the ventral side. The color slowly fades out toward proximal. The nails are dark. The eyes are almost black but under bright illumination they show a dark red glow. The typical white patches on the upper lip, under the chin, and across the front feet of nonagouti animals are also recognizable in this new mutant. This, together with the nonagouti tail and the absence of the typical white belly produced by the agouti allele in this species, makes it likely that this phenotype has a nonagouti background.
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The lighter version (see Figure 1B) can be described as a diluted form of the darker one and is reminiscent of the phenotype of the Siamese mouse (Green 1961) and rat (Moutier et al. 1973). The body color is a very creamy type of brown and the extremities are light brown. The tail, however, is quite dark and of a dark sepia coloration. The eyes are dark ruby and are clearly darker than those of pink-eyed dilution (pp) and pink-eyed white (chch) animals.
Juveniles don't show the full acromelanistic features like the adults do (see Figure 2). Until their first molt the dark phenotypes have a more grayish-brown color with only a darker-colored tail. Nose, ears, and feet are the same color as the body. Similarly the juvenile of the lighter version also shows no dark coloration except for the tail. Both phenotypes develop dark extremities, ears, and nose as they reach maturity. Under the influence of low temperatures (<15°C) the mid-dorsal area tends to become darker than the rest of the body. Altogether both phenotypes are clearly acromelanistic.
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Another acromelanistic phenotype of the Mongolian gerbil has previously been described (Leiper and Robinson 1984; Robinson 1973). In that case the pigmentation is more severely affected. The animals of this phenotype are pink-eyed whites with some light brown hairs on the tail (AAchch). On a pink-eyed dilution background (chchpp) these animals are pseudoalbinos. On a nonagouti background (aachch) the tail can become quite dark, therefore we would like to call this latter phenotype "dark-tailed white" (see Figure 1C).
Complete albinism (cc) was reported by Matsuzaki et al. (1989). However, no subsequent reports on this phenotype have been published. The question arises whether this mutation has been lost. It cannot be excluded that the pink-eyed dilution mutation (pp) or other modifying genes were involved in this specific stock.
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Breeding Data |
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TopAbstractIntroductionDescription of the MutantBreeding DataDiscussionReferences |
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At first the darker animals were checked for their assumed nonagouti background. Crossings with nonagouti produced only nonagouti offspring (51 of 51), showing that the dark version is actually a nonagouti variant of the new mutant. In order to show that the dark mutant breeds true, dark individuals were mated with each other producing only dark variant F1 animals (104 of 104). A similar experiment with animals of the light phenotype, subsequently called Siamese, resulted in three different phenotypes: dark variants, Siamese, and dark-tailed whites. This indicates that the Siamese were in fact compound heterozygotes of the new mutation and the earlier described more severe form of acromelanism.
To investigate the phenotypic effects of the new mutation on a wild-type agouti background, dark variants were mated to agouti animals and produced only agouti animals (51 of 51), and F1 agouti animals were inbred or backcrossed to dark variant animals. F1 x F1 matings resulted in 22 agoutis, 6 blacks, 2 dark variants, and 4 animals of a new phenotype. The new phenotype can be described as a light gray agouti with a somewhat diluted wild-type agouti tail (further referred to as chinchilla medium). F1 agouti x dark variant animals resulted in 14 agoutis, 5 blacks, 12 dark variants, and 6 chinchilla medium animals. Both results are within the expected ratios of 9:3:3:1 and 1:1:1:1, respectively (see Table 2).
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In the chinchilla medium animals it seems that the pheomelanin, which is almost completely washed out on the body, is less affected on the tail. The nose and ears of some individuals are slightly darkened. On close examination the mid-dorsal banded hairs (mainly awls) have a light sepia base, a creamy white subapical band, and light sepia tips. When compared to wild-type agouti it is clear that the new mutation dilutes pheomelanin more than eumelanin. Because the different phenotypes are more pronounced on a nonagouti than on an agouti background, all further experiments were performed on anonagouti background.
Dark-variant animals were mated with pink-eyed white and gray agouti (gg) animals. Since acromelanism is a typical feature of the albino locus, pink-eyed white was chosen. For the same reason gray agouti was chosen: it mimics the chinchilla mutation at the albino locus of other rodent species (Leiper and Robinson 1985). Crossings between dark variants and pink-eyed whites only produced animals with the Siamese phenotype (118 of 118). Crossings between dark variants and gray agoutis only produced agoutis (39 of 39). Siamese F1 animals were inbred to produce an F2 of 40 dark variants, 59 Siamese, and 42 pink-eyed whites. Siamese backcrossed to dark animals produced 56 dark and 48 Siamese animals, and Siamese backcrossed to pink-eyed whites produced 12 pink-eyed whites and 12 Siamese. Segregation ratios and statistical analyses of all crosses are summarized in Table 2.
Our breeding data indicate an autosomal inheritance: no significant differences between distribution of phenotypes over the sexes could be observed. Fertility and viability seem to be within normal range.
In view of the fact that the (darker) homozygous phenotype has an acromelanistic expression, which is a typical feature of mutations at the c locus, and also because it is allelic with pink-eyed white (ch), this new mutation can be located at the c locus with confidence. In comparison to the acromelanistic mouse and rat the new gerbil mutation differs in phenotype. Although similar acromelanistic phenotypes in rabbits (sable rabbits) show a darker coloration, their color characteristics and inheritance pattern have more resemblance with the here described mutation in the gerbil (see Table 3). Therefore we would like to propose to designate the gene symbol cchm (chinchilla medium).
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Discussion |
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TopAbstractIntroductionDescription of the MutantBreeding DataDiscussionReferences |
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The breeding data indicate that the mutation we describe is inherited as an autosomal recessive trait since all F1 animals of mutant x agouti matings are of an agouti phenotype. In other words cchm is fully recessive to C. Since all F1 animals from black chinchilla medium x pink-eyed white matings are of an intermediate phenotype, cchm is shown to be codominant to ch.
Because in the Mongolian gerbil the c locus is linked to the p locus (Leiper and Robinson 1986) this will have consequences for the distribution of phenotypes in the F2 progeny of, for instance, a black chinchilla medium (aacchmcchmPP) x argente golden (AACCpp) mating. These types of experiments were not performed by us, but it is surely worth testing in order to confirm the linkage. Another interesting question to investigate would be whether pp has a dominance modifying effect on the dominance of C over cchm, like it has on the dominance of C over ch (Leiper and Robinson 1984). Preliminary data indicate that this is indeed the case. Both the A-Ccchmpp and the aaCcchmpp animals are of a lighter color than the corresponding CCpp animals. In comparison to the argente creme (A-Cchpp) the A-Ccchmpp animal has a richer cast of yellow. In comparison to the silver (aaCchpp), the aaCcchmpp animal is of a more bluish cast. Both varieties have darker red eyes. We propose to call these phenotypes argente fawn and sapphire, respectively.
Furthermore, it would be interesting to see whether cchmcchm has a dominance modifying effect on the dominance of P over p. In the mouse it has been reported that albinism (cc) and pink-eyed dilution (pp) have a reciprocal dominance modifying effect (Silvers 1979). In case of the pink-eyed whites (chch), this would be difficult to test because of the severe dilution of body color, only on the tail of dark-tailed white animals the difference between aachchPP and aachchPp might be visible. In chinchilla medium animals, however, the amount of remaining pigmentation will be easier to assess.
Mutations at the c locus affect the synthesis of tyrosinase (monophenol oxygenase). This copper-containing enzyme plays a major role in the synthesis of melanin by the catalyzation of the oxidation of tyrosine to L-dopa (3,4 dihydroxyphenylalanine) and the dehydrogenation of L-dopa to dopaquinone. These two catalytic reactions form the first two steps in the melanin biosynthetic pathway. Dopaquinone is a common precursor for eumelanin as well as pheomelanin. Certain tyrosinase mutations produce an extreme unstable and thermosensitive form of the enzyme (Halaban et al. 1988). In these cases melanin production is greater in colder areas of the body, leading to the typical acromelanistic phenotype seen in several mammalian species (Searle 1990), including humans (Giebel et al. 1991).
Because of the above described similar phenotype, inheritance pattern, and comparable interaction with the earlier described severe form of acromelanism assigned to the c locus, it is likely that the new mutation occurred at the albino locus of the Mongolian gerbil. Ultimate proof has to come from molecular studies, which will become possible as soon as the tyrosinase gene of the Mongolian gerbil has been cloned.
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Acknowledgments |
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The authors wish to thank Julian Barker for critical reading.
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Footnotes |
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Address correspondence to Fred Petrij at the address above or e-mail: fp{at}wxs.nl.
Corresponding Editor: Neal Copeland
Received April 14, 2000
Accepted August 31, 2000
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References |
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TopAbstractIntroductionDescription of the MutantBreeding DataDiscussionReferences |
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