I recently found a test answers paper from Union County Vocational-Technical Schools, New Jersey that still get it wrong. It stated that calico (tortoiseshell and white) is due to a sex-linked co-dominant allele and used the symbols B for black, R for orange and BR for calico (XB, XR and XBXR). Yellow is epistatic to black. The corresponding allele to yellow is “non-yellow” (or wild-colour). Black is a different gene, is not on the X chromosome and the alleles of black are “chocolate” and “cinnamon.”

1904. DONCASTER L: On the Inheritance Of Tortoiseshell And Related Colours in Cats, Proc Camb Philol Soc13:35, 1904.

1912. DONCASTER L: Sex-limited Inheritance in Cats, And its Bearing on the Sex-Limited Transmission Of Certain Human Abnormalities. Science, N.S. 36, 144.1912.

1916. IBSEN, H.L. Tricolour Inheritance III. Tortoiseshell Cats. Ibsen posited that the tortoiseshell coat was due to one definite factor, which he called “T”, and which could act only in the presence of black, B, causing the black to be restricted to spots and leaving orange areas between. He denoted orange as b. (T is now used in notation of tabby patterns)

1919. LITTLE CC. Colour inheritance in cats, with special reference to colours, black, yellow and tortoiseshell. J Genet. 1919;8: 279–90.

1922. SIRKS, M.J. “Handbook der algemeene Erfelijkheidsleer.” Martinus Nijhoff, The Hague. 1922. p. 256, also in later editions) considers black and yellow to be sex-linked but not allelic. He gives the symbols B and Y.

1927. BAMBER, R. “Genetics of Domestic Cats.” Bibliographia Genetica 3:1-86, 1927. P. 6: Bamber’s theory and symbols were Y for yellow and y for “extension of black.” (also BAMBER, R. C. and E. C. HERDMAN 1931. Jour. Genet. 24: 353-357; BAMBER, R. C. and E. C. HERDMAN 1932. Jour. Genet. 26: 115-128.)

1927. BAMBER RC, HERDMAN EC. The Inheritance of Black, Yellow and Tortoiseshell Coat Colour in Cats. J Genet. 1927;18: 87–97

1935. SNYDER, L.H. “The Principles of Heredity”. D.C. Heath, Boston. p. 68 “In cats, a factor for yellow is allelomorphic to one for black, and they are carried on the X-chromosome.”

1946. SNYDER, L.H. “The Principles of Heredity,” 2nd Edn., D.C. Heath, Boston. P. 91 assigns the symbols B to yellow, b to black, and Bb to tortoiseshell. (Fifth ed. with P. R. DAVID. 1957.)

1950. CROW, J. F. “Genetics Notes,” Burgess, Minneapolis. 1950. p. 17 says “In cats the genotype BB is black. Bb is tortoiseshell, and bb is yellow. The gene is on the X-chromosome,” but he revised this in the 7th (1976) Edition p. 34 “tortoiseshell cats [. . . ] are heterozygous for an orange colour gene. The orange spots contain cells where the dark colour gene is inactivated, and the dark parts have the orange gene inactivated.” (Lyon hypothesis).

1952. SRB, A.M. and R.D. OWEN. “General Genetics.” W.H. Freeman, San Francisco. P. 97 use the symbol Y for black and y for yellow, with Yy being the tortoiseshell female. They base their theory on Bamber (1927) but Bamber’s symbols were the other way round: Y for yellow and y for “extension of black.”

1956. DODSON, E.O. “Genetics.” W.B. Saunders and Co., Philadelphia, 1956. p.81.. “In cats, the gene B subserves yellow coat colour, while its allele b subserves black.” Bb resulted in tortoiseshell. This accords with SNYDER (1946) rather than with CROW (1950).

1956. ISHIHARA T: CYTOLOGICAL STUDIES ON TORTOISESHELL MALE CATS, Cytologia 21:391, 1956.

1957. KOMAI, T. “Supplementary Notes on the Genetics of Tortoiseshell Male Cat,” Jour. Fac. Sci, Hokkaido Univ. 'Ser. VI, Zool. 13, 1957. “The gene which is allelic to the sex-linked gene for orange (0) is the one for non-orange or wild-type of orange (0+), and not the gene for black (b) or tabby (b+) which is located on one of the autosomes. It is rather striking that this plain fact has escaped notice of some recent geneticists including Sprague and Stormont (1956).”

1959. SEARLE, A.G. “A Study of Variation in Singapore Cats.” “In Eastern Asia, the gene for yellow fur-colour is three to four times as common as in London; in Japan this has meant that the tortoiseshell male occurs often enough to be the object of certain superstitions.” Based on his work in 1949, he uses “+” for black, and y for sex-linked yellow. “Tortoiseshells are +/y and therefore normally female.” However, he also uses a for black in one table, having previously defined it as denoting non-agouti (agouti being +).

1962. LYON MF. Sex chromatin and gene action in mammalian X-chromosome. Am J Hum Genet. 1962;14: 135–48.

1962. KING, R.C. “Genetics.” Oxford Univ. Press, N.Y. 1962. p. 110. Black and yellow are sex-linked alleles. His second edition (1967), and his “A Dictionary of Genetics” (Oxford Univ. Press, N.Y. 1967 and 1974) both follow CROW in using BB for black. Bb for tortoiseshell, and bb for yellow.

1964. HUTT, F. B. “Animal Genetics,” Ronald Press, NY. 1964. p. 143 follows CROW in using BB for black. Bb for tortoiseshell, and bb for yellow. “Black and yellow coats in cats are determined by the sex-linked alleles B and b.” Second Edition (HUTT, F. B. and B. A. RASMUSEN, “Animal genetics” 2nd Edition, John Wiley, NY. 1982) refers to ROBINSON and changes the symbols to o and O (non-orange, orange respectively).

1964. CHU EHY, THULINE HC, NORBY DE: Triploid-Diploid Chimerism in a Male Tortoiseshell Cat, Cytogenetics 24:1, 1964.

1964. THULINE HC: Male tortoiseshell, chimerism and true hermaphroditism, J Cat Genet 4:2, 1964.

1967. MALOUF N, BENIRSCHKE K, HOEFNAGEL D. XX-XY chimerism in a tricolored male cat. Cytogenetics. 1967;6(3): 228-41.

1967. SINGLETON, W.R. “Elementary genetics,” Van Nostrand, Princeton, N.J., 1962 and 1967. p.221 Cats have a sex-linked “gene pair causing black or yellow hairs.” P. 558 “The gene for black and yellow is sex-linked.” He uses B for black, Y for Yellow. A yellow male is shown as Y- (i.e. no gene on the Y-chromosome). Using Y in this way is confusing as it is both a chromosome and a gene symbol.

1968. STRICKBERGER, M. W. “Genetics,” Macmillan, NY. 1968. p. 478 followed SRB and OWEN using Y for the black allele and y for the yellow allele. On p. 707 Strickberger reviews a gene-frequency report by TODD and says “In the heterogametic XY males. The presence of the yellow gene produced yellow fur, while its normal allele (y+ or simple +) produces a darker colour whose particular shade and pattern depends on the presence of other genes.” This is repeated in later editions (3rd Ed. 1985). It causes confusion because Strickberger refers to Y, y and y+ i.e. 3 alleles!

1968. COMMITTEE ON STANDARDIZED GENETIC NOMENCLATURE FOR CATS. Standardized genetic nomenclature for the domestic cat. J. Hered. 59:39-40. 1968. This gave a standard set of symbols, thus removing the confusion of B, b, Y, y and y+ in papers and text books. However many authors continued to use the older symbols copied from pervious authors.

1971. PYLE RL, PATTERSON DF, HARE WC ET AL: XXY sex chromosome constitution in a Himalayan cat with tortoise-shell points, J Hered 62: 220, 1971. Since males have only one X chromosome they are normally either black or orange, but not both; however, tortoise-shell males have been reported and most of them are known to be sterile. The occurrence of such cats was not clearly understood until 1961 when Thuline and Norby described two male cats: one with the tortoise-shell coat pattern and lacking testicular tissue; the other not tortoise-shell, with testes, but not producing sperm. Both cats had 39 chromosomes (2n + 1). The authors suggested that the coat color and sterility were compatible with an extra X chromosome. They mentioned a number of other tortoise-shell male cats being mosaics. Their report described a tortoise-shell point Himalayan male. It was the first case of XXY reported in a colourpoint cat, and through pedigree analysis of coat color patterns they identified the parent in which nondisjunction of the sex chromosomes occurred.

1971. GREGSON NM, ISHMAEL J: Diploid Triploid Chimerism in Three Tortoiseshell Cats, Res Vet Sci 12:275, 1971.

1973: CENTERWALL W. R. et BENIRSCHKE K., (1973). Male tortoiseshell and calico (T-C) cats. Animal models of sex chromosome mosaics, aneuploids, polyploids, and chimerics. The Journal of Heredity., Vol(64), no.5, pp. 272-278.

1975. MERRELL. D. J. “An Introduction to Genetics,” W. W. Norton. NY. 1975. p.110 follows Plate in designating b for black and B for yellow.

1975: CENTERWALL WR, BENIRSCHKE K: Animal Model for the XXY Klinefelter’s Syndrome in Man: Tortoiseshell And Calico Male Cats, American Journal of Veterinary Research., Vol. 36, no.9, pp. 1275-1280. A review of the chromosome findings in 25 male tortoiseshell or calico (T-C) cats showed a variety of aneuploidy, polyploidy, mosaicism, and chimerism. An XXY-complement was included in the chromosome makeup of 16 of the 25 cats [some of the cases reviewed might not have identified XY/XY or XX/XY as XXY]. Almost all of these cats were sterile. Testicular pathologic changes, when recorded were comparable to human XXY Klinefelter's syndrome. 2 male T-C cats were presented as representative models of XXY Klinefelter's syndrome in man. An explanation of cat coat-color genetics clarified why "black" and sex-linked "orange" coloration can appear together normally in XX females and in rare males with 2 different X chromosomes. Male T-C cats were visual indicators of sex-chromosome aberrations which could also occur completely independent of coloration.

1980. WAGNER, R. P., B. H. JUDD, B. G. SANDERS, and R. H. RICHARDSON. “introduction to Modern Genetics,” John Wiley, NY. 1980. p. 112 refer back to CROW’s earlier edition and say: “a pair of alleles, B and b, appear to be sex-linked in cats. In females BB gives black coat colour, homozygous bb gives yellow, while the ‘hybrid’ animal (Bb) is the familiar ‘tortoiseshell’.”

1984. MORAN C, GILLIES CB, NICHOLAS FW. Fertile Male Tortoiseshell Cats. Mosaicism Due to Gene Instability? J Hered. 1984 Sep-Oct;75(5):397-402. Two fertile male tortoiseshell Burmese cats with atypical coat color distribution were found to have normal 38XY karyotypes. They produced normal sperm. Progeny data indicated that both cats were transmitting both alleles at the sex-linked orange locus, but with unequal frequencies. For one of these cats, analysis of pedigree and progeny data indicated that gene instability at the orange locus was the only possible explanation for its mosaicism. A third male tortoiseshell Burmese cat with typical tortoiseshell phenotype was found to be 39XXY and sterile.

1985. SNYDER, L. A., D. FREIFELDER. and D. L. HARTL. General Genetics. Jones and Bartlett, Boston. 1985. p. 59 says: “The black and yellow pigments in the coats of cats are determined by an X-linked pair of alleles. Males are either black or yellow." They use novel gene symbols: cb and cy. (cb is the recognised symbol for Burmese colour dilution).

1986. MILLER, W.J. and W.F. HOLLANDER, “The Sex Linked Black Cat Fallacy: A Textbook Case,” Journ. Heredity 77: 463-464, 1986. This highlighted the confusing use of symbols and noted that authors of teaching textbooks tended to follow each other rather than referring to technical literature. They believed that the source of the fallacy that black (not yellow) was sex-linked to a misunderstanding in BAMBER’s (1927) study. Bamber used the same terms and symbols as LITTLE (1912) and DONCASTER (1913). Little did not mention “wild type.” Doncaster wrote that black “corresponds with ‘normality’." Bamber recognized that self-black i.e. “non-ticked" was a simple autosomal (non-sex-linked) recessive to tabby (wild-type colour). This was designated “a”, the generally used symbol for recessive black (nonagouti) in mammalian genetics. “Tabby” or “tiger-striped” meant the phenotype of small wild cats i.e. the “wild type.” Both black and yellow (orange) were distinct and independent mutations. Combining non-agouti “aa” with yellow, hemizygous or homozygous, looked the same as yellow on its own due to masking or epistasis (ROBINSON, SEARLE).

They suggested that textbook authors could have avoided misunderstanding by using the term “mutant” in describing sex-linkage and the tortoiseshell coat of the heterozygote e.g. “The yellow or orange mutant coat-colour type in cats is sex-linked. The modern symbol is O (Committee on standardized genetic nomenclature for cats, (Standardized genetic nomenclature for the domestic cat. J. Hered. 59:39-40. 1968). The heterozygous female, O/o+, shows the tortoiseshell effect, a yellow (O) and non-yellow (o+) patchwork.” There was a failure to identify which genes were mutants and which were standard/normal/wild type.

They noted that most textbooks paid only lip-service to the usefulness of the “+” symbol to denote wild type and that because textbook publishing is a lucrative business, deviating from dogma was unwelcome (MILLER, W. J. “Appropriate Gene Symbols in Teaching Genetics,” Proc. Iowa Acad. Sci. 92:115-118, 1985) hence fallacies are passed to yet another generation.

1999. LONG, SE. 38,XX/38,XY Chromosome Chimaerism in Three Feline Siblings. The Veterinary Record, October 2, 1999,145: 404-405. The author noted that sex chromosome chimaerism was not an uncommon finding in tortoiseshell males, but had only previously been reported in other cats if they were hermaphrodites. Chromosome studies usually only took place where the coat pattern and gender indicated an anomaly. The author noted that approximately 19 per cent of male tortoiseshell cats reported in the literature had 38,XX/38,XY chimaerism and some were fertile. In this study, a tortoiseshell male, its litter mates and mother were all studied. The 3 siblings were an 11-month-old tortoiseshell male (tortie-tabby with extensive white spotting), a tabby male, and a tabby and white female. The mother was tabby and white. The sire was unknown. The tortie-tabby male was 38,XX/38,XY and fertile. The tabby male was 38,XX/38,XY, but had already been castrated. The tabby and white female sibling was 38,XX/38,XY and had produced a litter of 5 kittens before being spayed. The tabby and white mother was not a sex chromosome chimera, but some of the cells examined had an extra D4 chromosome (trisomy). This was the first report of sex chromosome chimaerism in siblings of a tortie male. The tortie male was a whole body chimaera. The siblings might have been haemopoetic chimaeras (microchimerism, only blood cells affected), but only blood samples were examined and no other tissues. This could occur if their placentas had fused, something considered unlikely in cats.

1999. LEAMAN T, ROWLAND R, LONG SE. Male Tortoiseshell Cats in the United Kingdom. Vet Rec. 1999 Jan 2;144(1):9-12: A questionnaire concerning the coat colour and sex of cats being vaccinated or neutered was sent to 2585 veterinary practices; 393 (15.2 per cent) were returned and information was obtained about 9816 cats. Of 4598 males, 20 were recorded as tortoiseshell (0.43 per cent). The frequency of the orange gene was 19.7 per cent assuming that male tortoiseshell cats had two X chromosomes. The chromosome complement and/or gonadal histology of 14 male tortoiseshell cats is described. Cytogenetic analysis of 11 animals revealed six with a 38,XX/38,XY complement (CHIMERA), two with 39,XXY, two with 38,XX, and one with a 38,XY complement.

2001. KOSOWSKA B, JANUSZEWSKI A, TOKARSKA M ET AL: Cytogenetic and histologic studies of tortoiseshell cats, Med Weter 57:475, 2001.

2003. KUIPER H, HEWICKER-TRAUTWEIN M, DISTL O: Cytogenetic and Histologic Examination of Four Tortoiseshell Cats, Dtsch Tierarztl Wochenschr 110:457, 2003. Tortoiseshell tomcats are uncommon and mostly caused by an aberration of sex chromosomes. This studied four tortoiseshell tomcats. In two cases, an XXY syndrome could be proven. Another tortoiseshell tomcat had an XX/XY chromosomal constitution. One had an exclusively male XY karyotype. In two cases the testes were histologically examined. In one XXY phenotypically male cat there was no sperm production. In the XX/XY-chimerism sperm was produced.

2010. SCHLAFER DH, VALENTINE B, FAHNESTOCK G, FROENICKE L, GRAHN RA, LYONS LA, et al. A case of SRY-Positive 38, XY true hermaphroditism (XY sex reversal) in a cat. Vet Pathol. 2011;48:817–22. Epub 2010 Sep 22

2012. LYONS LA. Genetic testing in domestic cats. Mol Cell Probes. 2012;26(6):224-230.

2014. PEDERSEN AS, BERG LC, ALMSTRUP K, THOMSEN PD. A Tortoiseshell Male Cat: Chromosome Analysis and Histologic Examination Of The Testis. Cytogenet Genome Res. 2014;142(2):107-11. Tortoiseshell coat color is normally restricted to female cats due to X-linkage of the O gene. Tortoiseshell male cats can occur at a low frequency because of 39,XXY chromosome aberrations similar to the Klinefelter syndrome in man. They analyzed the chromosome complement and testicular tissue from a single tortoiseshell male cat. No sperm production was detected and they concluded it was a classic case of a sterile, male tortoiseshell cat with a 39,XXY chromosome complement (Klinefelter).

2018. IZABELA SZCZERBAL,PAULINA KRZEMINSKA,STANISLAW DZIMIRA,TUIRE MARIA TAMMINEN,SEPPO SAARI,WOJCIECH NIZANSKI,MACIEJ GOGULSKI,JOANNA NOWACKA-WOSZUK,MAREK SWITONSKI, Disorders of sex development in cats with different complements of sex chromosomes, Reproduction in Domestic Animals, Vol 53, Issue 6, December 2018, Pages 1317-1322. An investigation of 3 cases of disorders of sex development (DSDs), something poorly understood in cats. The first was an Oriental Shorthair cat with a rudimentary penis, abdominal atrophic testicles and no uterus; this appeared to be a freemartin, since leucocyte chimerism XX/XY and a lack of Y-linked genes (SRY and ZFY) were identified. The second was a tortoiseshell male Devon Rex with atrophic scrotal testicles and a normal penis; XXY trisomy was identified. The third was a European Shorthair cat with atrophic testicles in a bifid scrotum, rudimentary penis and no uterus; this had normal XY chromosomes, but a low testosterone level.

2020. JARAUD A, BOSSÉ P, DUFAURE DE CITRES C, TIRET L, GACHE V, ABITBOL M. Feline chimerism revealed by DNA profiling. Anim Genet. 2020 Aug;51(4):631-633. In the domestic cat, the tortoiseshell coat colour that combines red and non-red hairs is the most obvious way to identify CHIMERAS in males. Several cases of tortoiseshell males have been reported, some of which were diagnosed as chimeras without any molecular confirmation. The study reported the case of a female feline CHIMERA identified due to its coat colour and confirmed by DNA profiling. It ruled out mosaicism and aneuploidy.

2020. BUGNO-PONIEWIERSKA M, KIJ B, WITARSKI W, WOJTASZEK M, RADKO A, PODBIELSKA A, SZCZERBAL I, MURPHY WJ. FERTILE MALE TORTOISESHELL CAT WITH TRUE CHIMERISM 38,XY/38,XY. Reprod Domest Anim. 2020 Sep;55(9):1139-1144. Tortoiseshell coat colour is characteristic of female cats, it rarely occurs in tomcats and is associated with chromosome abnormalities (additional copy of X chromosome). The study investigated a fertile tortoiseshell Maine Coon tomcat. Cytogenetic analysis revealed only a single set of sex chromosomes typical for male - 38,XY. Other results showed three alleles in locus FCA201 and four alleles in loci FCA149 and FCA441 in different tissues indicating 38,XY/38,XY CHIMERISM. This was the first case of a 38,XY/38,XY CHIMERA cat confirmed by genetic analysis.

Sadly, as the test answers paper from Union County Vocational-Technical Schools, New Jersey demonstrates, schools genetics classes are still not teaching the relationship between black and yellow correctly!