37. on the Origin of the Tortoiseshell Male

150 [Vol. 28,

37. On the Origin o f the Tortoiseshell Male Cat -- a Correction`.

By Taku KOMAI, M.J.A. National Institute of Genetics, Misima, Sizuokaken. (Comm. March 12, 1952.)

Inheritance of Common Coat Colors. The origin of the tortoiseshell male cat is an old puzzle of genetics. Some years ago, the writer became interested in this problem, and has since been endeavoring to solve it. By consulting literature relating to this subject, it had become apparent that the fundamental facts of inheritance of common coat colors in cats remained unsettled. In her review of the genetics of domestic cats, Bamber (1927) states:--"Clearly the problem of the tortoiseshell male and of the unexpected black females is by no means settled. Indeed, the normal mode of inheritance of black, yellow and tortoiseshell is only very imperfectly understood.--That black is sex-linked is widely accepted, but has never actually been proved. Either yellow or black or both are certainly sex-linked". (p. 43). The writer thought that one way of solving this question was to take census of cats, and this was done in some towns in Japan. It has thus become perfectly clear that the gene for orange (yellow) color 0 is sex-linked, whereas the gene for black (b) or tabby (b+) color is in one of the autosomes (Komai, 1950, also in press). 0, either in the homozygous (0/0) or homozygous (0) state, is completely epistatic to b or b~, and produces an orange coat, while in the heterozygous state (0/0+), it allows the effect of b or b+ to appear partially-hence the tortoiseshell coat. Accordingly, the genetic formulae of these colors should be:-orange female 0/0 b/b (or b/b+, b+/b+), black female=0~/0+ b/b, tortoiseshell female=0/0* b/b (or b/b+, b4/b), orange male=0 b/b (or b/b~, b~/b~), black male=0~ b/b, tabby male=0+ b}/b+ (or b+/b). Coincidentally, Searle (1949) took a similar census for cats in London, and reached the same conclusion as to the location of genes for these colors. He also found evidence for random mating among the cats of different colors.

Origin of Tortoiseshell Male. Concerning the origin of the rare tortoiseshell male, the writer

* Contributions from National Institute of Genetics . No. 10. The writer is indebted to Prof. S. Makino for generous help in many ways. No. 3.] On the Origin of the Tortoiseshell Male Cat. 151 conceived some years ago a working hypothesis which postulated an unequal crossing-over between two X-chromosomes in a tortoiseshell mother cat. By this process, both the 0 and 0+ possessed by such a cat would be brought into one of the X's. Also it would transfer the factor for femaleness lying close to the color gene from one X to another. Thus, one of the X's would acquire duplicate sets of color genes and factors for femaleness; the son that receives this chromosome should become tortoiseshell and also sterile, owing to the presence of a factor for femaleness in excess. The writer published this hypothesis in the September 1946 Number of the present Proceedings (22, 265-268), as well as in a few other journals (1946 a, 1947). Ever since then, he has been looking for cases of tortoiseshell males. So far, twelve of them have come under his examination (Table 1). Most of these were actually observed by the writer; a few reported from distant locali- ties were seen by the writer's friend biologists at his request, and descriptions of coat colors, with color-sketches and photographs

Table 1. Tortoiseshell males found by the writer : B - black, 0-orange, T - tortoiseshell, unknown whether tabby or black, T (b) - black tortoiseshell, T (ta) - tabby tortoiseshell, Ta - tabby. 152 m. 1<0MM. CVo1.2$, were sent to the writer. All of these cats, except one died a few days after birth, were more than four months old, so there was no danger of their sex being mistaken. They had the same type of markings as those of ordinary tortoiseshell females, with orange and black or tabby patches scattered here and there on the coat. According to this working hypothesis, the mother of a tortoiseshell male should be tortoiseshell herself. Out of the twelve cases, nine had this kind of mother. Two, however, had orange mothers, and one a black mother. In literature also, there are a few cases where a tortoiseshell male was born of the mating blank female >< orange male (Doncaster 1913, Tjebbes and Wriedt 1926, Bamber 1927). Furthermore, the sections of the gonads of two of these cats showed no feature reminding of intersexuality; rather they were of testes of complete sterility. Similar observations are recorded by some previous authors (Doncaster and Cutler 1915, Ohshima and Oyama 1925). These findings could hardly be reconciled with this hypothesis. Thus, the working hypothesis is no longer tenable.

The New Hypothesis. According to this new hypothesis, the cause of the production of a tortoiseshell male should be found in the father instead of the mother. The chromosome complex of the cat has been studied by sevCi al cytologists. The diploid set of the male is composed of 38 chromosomes including an X-Y pair. Opinions, however, are varied about the precise configuration and structure of this pair. While some authors, e.g. Minouchi 1928, Minouchi and Ohta 1934 Makino and Tateishi (in press), show a highly unequal pair as the X-Y, Koller (1941) assigns an equal pair to be the sex-chromosomes. All cytologists, however, apparently agree in that both X and Y are differentiated into pairing and differential segments, and a chiasma is formed only in the former. Fig. 1 is a diagram of mammalian XY-chromosomes copied from Darlington (1939). This is rather different from the diagram of cat's sex-chromosomes shown by Koller. Still, it may be used for illustrating the writer's hypothesis. The gene for orange color is sex-linked, so it must be located in X. By crossing-over, this gene may be transferred to Y. If a sperm bearing the 0 gene in its Y fertilizes an egg bearing 0~ either of a tortoiseshell or a black female, a tortoiseshell male will be produced. To explain the sterility of a male tortoiseshell which is almost without exception, it is necessary to assume that some factor or factor-complex for fertility of the male is lost from Y by this No. 3.J On the Origin of the Tortoiseshell Male Cat. 153 crossing-over process. This can take place if there is such a factor or factor-complex near the locus corresponding to the 0-locus in X. It is true that the presence of such a factor of factor-complex has never been demonstrated in the Y-chromosome of any mam- mal. In Drosophzla, however, two such factor-complex are known (Philip 1935). It seems plausible that some day the presence of such factor-complex in mammalian Y-chromosome will be shown. This crossing-over hypothesis can also account for the birth of exceptional black females from the mating black female x orange male or tortoiseshell female >< orange male, which has been another enigma of cat genetics. If crossing-over occurs between the sex-chromosomes in the sper- matocyte of the father cat, then the X will lose the 0 gene. If an egg with an 0k-carrying X is fertilized by a sperm having such an X, a black daughter wi 11 be produced,

Remarks. Of previous authors, Doncaster (1913), Hayes (1923), Tjebbes and Wriedt (1927), Crew (1927) and Plate (1933) have proposed hypotheses postulating the crossing-over between X and Y in the father. None of them, however, was able to explain the cause of sterility of the tortoiseshell male. For this, it seems necessary to postulate the presence in Y a factor or factor-complex for fertility which is lost by this process. As far as the writer can see, there is no other way of accounting for this curious phenomenon. Koller (1941) states :"It is not improbable that the low frequency of tortoiseshell males, their rare fertility, and the occurrence of exceptional black females from yellow males (Bamber, 1927) are al related phenomena. At present, however, it is not feasible to for- mulate a hypothesis based upon the structual peculiarities of the sex-chromosomes alone which would satisfactorily explain the physical 154 T. KOMAI. [Vol. 28, basis underlying the genetical behaviour of these exceptional types. We must assume that the genic contents of the sex-chromosomes constitute highly complex complementary systems and that the various units of complementary gene systems, concerning viability and fertility (or sterility), are distributed in the pairing and differential segments. Crossing-over in the pairing segments of X and Y necessarily leads to the disruption of these complementary systems. It is not improbable that there exist various X and Y chromosomes which differ in respect of the genes constituting these complementary systems. A particular kind of combination of the sex-chromosomes would account for the exceptional types". (p. 92). This ac- cords in principle with the writer's view stated above.

Summary.

1. The gene for orange coat color in cats is sex-linked, while the gene for black or tabby is autosomal. The former, in the homozygous or homozygous state, is completely epistatic to the effect of the latter, while, in the heterozygous state, the former covers only partially the effect of the latter, and a tortoiseshell female is produced. 2. The exceptional tortoiseshell male may be borne of either a tortoiseshell, or an orange, or a black mother. It is a male of complete sterility, but not an intersex. 3. As to the cause of such an exceptional male and its sterility, the writer's working hypothesis postulating an unequal crossing-over between the X-chromosomes of a tortoiseshell mother is untenable. Instead, crossing-over between X and Y of the father which trans- fers the gene for orange color from X to Y, and reciprocally the factor-complex for fertility from Y to X, seems to be a more plausible explanation. This hypothesis also can account for the origin of exceptional black females from a black or tortoiseshell mother and an orange father.

Literature Cited.

Bamber, R. C. 1927. Genetics of domestic cats. Bibl. Genet. 3, 1-86. Crew, F. A. E. 1927. The Genetics of Sexuality in Animals. Cambridge, England. Darlington, C. D. 1939. The Evolution of Genetic Systems. Cambridge, England. Doncaster, L. 1913. On sex-limited inheritance in cats, and its bearing on the sex-limited transmission of certain human abnormalities. J. Genet 3,11-23. Doncaster, L. and Cutler, D. W. 1915. On the sterility of the tortoiseshell tomcat. J. Genet. 5, 65-73. Hayes, F. A. 1923. The tortoiseshell cat. J. Hered. 14, 369-376. Koller, P. C. 1941. The gentical and mechanical properties of the sex chromosomes. VIII. The cat (Felis domestica). Proc. Roy. Soc. Edinburgh Sec. B. Biol., 61, 7$-94. No. 3.] On the Origin of the Tortoiseshell Male Cat. 155

Komai, T. 1946. On the inheritance of black, yellow and tortoiseshell colour in cats, and the problem of the tortoiseshell male. Proc. Jap. Acad. 22, 265-268. -- 1946 a. On the inheritance of black, yellow and tortoiseshell colour in cats, with special reference to the problem of the tortoiseshell male. (in Japanese). Seibutu 1, 1-7. 1947. A new hypothesis on the origin of tortoiseshell male cat. Mem. Coll. Sci. Kyoto Univ. ser. B, 19, 17-21. 1950. Heredity of coat colors in cats. (in Japanese). Coord. Res. Genet. 1, 73-74. (in press). Incidence of the genes for coat colors in Japanese cats. Annot. Zool. Japon. 25. Makino, S. and Tateishi, S. (in press). A comparison of chromosomes in the lion, leopard cat and house cat. Minouchi, 0. 1928. On the chromosomes of the cat. Proc. Imp. Acad. 4, 128-130. Minouchi, 0. and Ohta, T. 1934. On the chromosome number and sex-chromosomes in the germ-cells of male and female cats. Cytologia 5, 355-362. Ohshima, H. and Oyama, J. 1925. On a tortoiseshell male cat with odd eyes. (in Japanese). Toyogakugei-zasshi 507, 9-18. Philip, U. 1935. Crossing-over between X- and Y-chromosomes in Drosophila melanogaster. J. Genet. 31, 341-352. Plate, L. 1933. Vererbungslehre. II. Sexualitat and allgemeine Probleme. Jena. Searle, A. G. 1949. Gene frequencies in London's cats. J. Genet. 49, 214-220. Tjebbes, K. and Wriedt, C. 1926. Dominant black in cats and its bearing on the question of the tortoiseshell males. J. genet. 17, 207-209.