homologous genetic variation in the felidae

Genetica 46:1-31 February 15, 1976

HOMOLOGOUS GENETIC VARIATION IN THE FELIDAE

ROY ROBINSON

St. Stephens Road Nursery, Ealing, London, England.

Received June 28, 1974/Accepted November 25, 1974

CONTENTS

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 Principles of homologizing genetic mutants . . . . . . . . . . . . . . . . 2 The primary gene loci . . . . . . . . . . . . . . . . . . . . . . . . . 4 Karyological considerations . . . . . . . . . . . . . . . . . . . . . . . 9 Hybridization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13 Gene conservatories . . . . . . . . . . . . . . . . . . . . . . . . . . 15 Known mutant genes of the domestic cat . . . . . . . . . . . . . . . . . 16 Mutant forms in wild Felids . . . . . . . . . . . . . . . . . . . . . . 19 Bibliography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28

Introduction

The investigation of genetic variation in wild species of the Felidae presents a problem because experimental breeding in the usual meaning of the term is excluded. This does not mean that the situation is entirely hopeless. Two approaches may be adopted which can yield useful information. The first by inquiry of zoos which are breeding Felids in the hope that pertinent information is available that could explain a given situation. This approach has proved successful for the elucidation of the heredity of the black form of the leopard. Conclusive data were obtained which showed that the black variant is inherited as a recessive to spotted (Ro- BINSON 1970a). This approach, however, has limitations. In short, it is opportunist, in that enquiries can only be made if the variation under consideration is one known to be possessed by zoos.

The second approach makes use of the concept of homologous variation, that is to say, by the examination of parallel variation in related species. Many species owe their similarity to common ancestry and this implies the possession of common genetic material, namely, chromosomes of homologous content and the capacity to produce comparable mutant genes. Thus, a black form of one species could have a homologue in a variety of other species because the chromosome endowment of the spe-

2 ROY ROBINSON

cies was derived from a common ancestor and retaining all or most of its physiological processes. The concept could be visualized as a continu- ation of the principles of form and function of comparative anatomy into the domain of chromosome morphology and of gene mutation.

The zoological nomenclature followed here is that of MORRIS (1965), largely because of its simplicity. The gene symbols are those standardized by convention and common usage for mammalian genetics as employed by CASTLE (1940) and SEARLE (1968).

Principles of Homologizing Genetic Mutants

The concept of gene homology has long ceased to be mere speculation. Laboratory rodents exhibit the phenomena to a high degree and for two reasons. First, many of the species are phylogenetically related and, second, because they are bred in the laboratory, mutants which appear can be analysed in detail. The mode of inheritance can be determined and their physiological action can be investigated by ever more sophisticated techniques. The result has been a general confirmation of the homology concept. From this, the perceptive observer can extend the concept to em- brace diverse groups of mammals, the rodents, lagomorphs and carnivores yielding up some remarkable examples. Today, the concept of homologous genes is generally accepted, even if the attribution of certain parallel mutants to such genes for some species is open to dispute. The reader may be referred to the penetrating monograph of SEARLE (1968) on the subject.

The criteria for homology of gene loci have been outlined elsewhere (ROBINSON 1970C). In brief, there are six in number. (1) Similarity of mutant phenotype is an obvious first step towards the establishment of homology and often the only means readily available. (2) Similar mode of inheritance would be confirmatory but not necessarily decisive. (3) The existence of several similar alleles at a locus. The greater the number of alleles, the greater will be the power of discrimination. The problem of mimetic loci (loci giving rise to mutants with similar phenotypes) may be resolvable by examination of multiple alleles of each locus. (4) Linkage of similar genes. If two homologous loci reside in the same chromosome in different species, this would be confirmatory but not conclusive. Ho- mologous genes could be separated during evolution and it is conceivable that mimetic genes could exhibit linkage, indeed, if the concept of gene duplication is correct, short sequences of loci with similar effects is a factor to consider. (5) If interspecies crosses can be obtained, crosses between animals homozygous for similar recessive genes would be revealing. If the

G E N E T I C S O F FELIDAE

T A B L E 1

INTERSPECIES VARIATION OF EXPRESSION OF ACROMELANIC ALBINISM

Species

Expres- Gene Extrem- sion of sym- Eye ities Age of Yellow bol Colour coloured onset Pigment

Cav iaporce l lus c a Pink All 2-3 days None (Domestic guinea-pig)

Felis domes t icus c s Blue All 1-2 days Abundant (Domestic cat)

M e r i o n e s unguiculatus c h Pink Tail 3 weeks ? (Mongolian gerbil)

Mesocr i ce tu s auratus c a Pink Ears 4 weeks ? (Syrian hamster)

M u s musculus c h Pink All 7 days None (House mouse)

M u s t e l a vison c n Pink Nose/tail ? ? (American mink)

Oryc to lagus cunicutus c h Pink All 3-4 weeks None/some (Domestic rabbit)

offspring show the recessive phenotype, this will constitute the strongest case for homology. Finally, (6) in v i t r o physiological and biochemical analysis of material from presumptive homologous phenotypes may produce confirmatory evidence.

It will be appreciated that, in general, exact phenotypic correspondence is not to be expected for homologous mutants in different species. This aspect is strikingly exemplified by the expression of acromelanic albinism. The typical expression of this form of incomplete albinism (e.g., in the rabbit) is easily recognisable. When, however, various features of the acromelanism are examined and tabulated as in Table 1 (ROBINSON 1973), differences are immediately apparent. There is a discernible pattern to the differences. The greater the amount of pigment expressed, the earlier is the age of onset and the larger is the number of extremities involved, despite the secondary differences.

It may seem contrarious at first sight that two of the more frequent trans-species variants, to wit, self black and complete albinism, should possess identical phenotypes. But this is merely due to the fact that each of these is so uniform in appearance. Acromelanic albinism is but one step removed genetically from complete albinism, yet immediately species differences of phenotype are apparent.

The existence of interspecies differences of expression immediately poses the question: are the differences due to slightly different homologous

4 ROY ROBINSON

genes or to the different species genomes in which essentially identical genes have to function ? The throughgoing homologist would undoubtedly opt for the latter answer, in fact, there is something to be said for this approach if it leads to a practical solution. Unless two species can produce fertile hybrids, a direct genetic answer is excluded. However, the problem may be resolved by delicate biochemical experiments with products of homologous genes. For example, by measuring the rate of enzymatic conversion of a substrate by tissue from different species but of putative homologous mutants.

A good case can be made for the postulate that either complete or acromelanic albino phenotypes are due to homologous genes. It may also be that the majority of self black variants in different species are due to non- agouti mutants. It is legitimate to make this assumption until events prove otherwise. Yet, the easily recognizable black phenotype may be used to emphasize the fact that similarity of phenotype cannot guarantee similarity of genotype. Self black phenotypes can be produced by dominant alleles of the extension locus (see later). However, the non-agouti gene is mainly (probably always) recessive to wild type. Therefore, the results of a few crosses can discriminate between a black phenotype due to recessive non-agouti or dominant supra-extension of black.

The coat of the greater majority of mammals is known as agouti, after the small rodent of this name. The colour is usually grey in tone, commonly drab but sometimes pale or richly hued. Often, the colour may vary regionally over the body (paler stomach fur is frequent) and be inter- rupted by white or dark patterns. The feature of agouti fur is that the hairs are banded with yellow (i.e. the tip is black, followed by yellow, then black which pales rapidly to blue as the pigment granules become sparse in number). The band may vary in position, width and intensity of yellow for different parts of the body. The light stomach fur may follow from dorso-ventral variation. The agouti colour is produced by the backward slope of the hair exposing part of the band and causing an intermingling of yellow band and black tipping. Agouti is manifested in Felids as the grey colour between the typical pattern of stripes, spots or rosettes. This is certainly true of the smaller cats (e.g., domestic and European wild cat) and probably for the larger species. Even those species which are not ob- viously agouti may display the effects of the gene in subtle ways.

The Primary Gene Loci

The number of gene loci giving rise to the commonly recurring mutant forms of mammals is few - far fewer than the uninitiated would perhaps

GENETICS OF FELIDAE

credit at first blush. Traditionally, six loci are depicted as responsible for the majority of mutant alleles. In summary, there are Agouti (A), Black pigmentation ( B), Full expression of colour ( C) , Dense pigmentation ( D ) , Extension of black (E), and Dark-eyed (P). This is the so-called ABCDEP system, promulgated by such authors as WRIGHT (1917), HALDANE (1927), CASTLE (1940), LITTLE (1958), SEARLE (1968) and ROBINSON (1970C). The more recent authorities have attempted to define other loci which can be sensibly assumed to give rise to mutant alleles with trans-species phenotypes.

A. The Agouti locus frequently mutates to two alleles: black and tan (a'), where the dorsum is black but the venter is light or creamy-yellow in colour. The nostrils and eyes may be outlined with light coloured fur, as is often the inside or the back of the ear pinnae. The other mutant allele is non-agouti (a), where the whole animal is black. In both of these forms, the characteristic yellow agouti band of the hair is absent. The a allele is a common mutant and is rightly regarded as productive of the melanic forms found in most species.

B. The locus for Black pigmentation may mutate to an allele (b), producing brown or chocolate pigment. The brown or chocolate phenotype is produced in combination with a, viz., aabb. In combination with agouti (AAbb), the phenotype is a brighter coloured agouti because all the normally black pigmented portions of the hair are now brown. The eyes may remain dark but it is not unusual for the iris to be light rather than dark brown and for the pupil to have a dull red glimmer in bright light.

C. The Full colour locus can give rise to three distinctive classes of mutant allele. These are chinchilla (cCh), acromelanic albinism (e h) and complete albinism (c). The three classes of mutant represent steps in the progressive loss of pigmentation. The C locus, in fact, is fundamental in the physiology of melanin production. The chinchilla (or chinchillation) mutant permits eumelanin to be produced but typically not phaeomelanin. The phenotype is an agouti minus yellow pigment as found in Chin- chilla lanigera. The white tiger of Rewa is an example of a chinchillated animal. Two degrees of chinchillation are common. With some alleles, the quality of the black pigment is unaffected but, with others, the black pigment may appear as a dark sepia. The domestic rabbit has the dis- tinction of possessing both categories of mutant (one is designated as dark chinchilla c chd and the other, light chincilla cC~; terminology which is re- commended for general usuage). The iris may be bluish or whitish, with reddish pupils, because of an impairment of normal pigmentation.

6 ROY ROBINSON

The differences of expression of acromelanic albinism between species have been discussed earlier (ROBINSON, 1973). These differences, however, are minor compared with the characteristic phenotype. Complete albino is fully devoid of pigment for all tissues. The eyes are pink because the blood vessels are no longer obscured by pigment. Most albino animals tend to be dazzled by light and frequently exhibit a nystagmus. The order of dominance for the albino alleles is C > C chd > C chl > e h > c.

D. The Dense pigmentation locus often mutates to an allele (d) which produces a pale or wash-out colour. The eye colour is normally unchanged but the coat has a bluish cast. In combination with non-agouti (aadd), a grey-blue phenotype is engendered hence the designation of blue dilution for the mutant allele. The bluish colour is produced by a disruption of the normal manufacture of the pigment granules. Instead of being uniformly distributed throughout the hair length they occur as clumps, with pigmen- less areas in between. The result is a greater scattering of light and an op- tical effect of weakening the colour.

E. The Extension o f black locus commonly produces two classes of mutant. The locus is directly concerned with the distribution of black pigment in the hair and the two classes of mutant determine whether the black pigment is not extended, to produce a yellow phenotype, or greatly extended to produce a black or blackish phenotype. The two classes of mutant are inherited as recessive or dominant to wild type (normal extension) respectively, and are known as non-extension (e) and supra-extension (Ea), respectively. Of the two, the non-extension gene is the better known, since its presence results in the yellow, red or erythritic variants. The variation of intensity of phaeomelanin is considerable and is not trivial, The variation of colour is due to polygenes inherited independent- ly of E; certainly for within species differences and almost certainly for between species differences. The supra-extension alleles produce dark phenotypes, either fully black or agouti black where the coat is black but with yellowish agouti flecking (occasionally with a vestigial agouti banding). The fully black form mimics the non-agouti phenotype and it is impossible for these to be separated without breeding tests. Although the existence of two forms of black mutants must be remembered, it is con- ventional to presume that black variants are due to non-agouti until evidence is available to indicate the contrary.

P. The Dark-eyed locus typically produces a mutant allele (p) which gives rise to a pink-eyed phenotype. The eye colour may vary from pink to dull red, depending upon the degree to which the eye is depigmented.

GENETICS OF F E L I D A E

The coat colour is often paler than normal, sometimes bluish-cream in tone but, at other times, yellowish with light ticking. The coat colour is variable because the p gene can dilute both phaeomelanin and eumelanin but often the latter more strongly than the former. The mutant phenotype is stable for any given species but the expression can vary between species. In fact, to a greater extent than the phenotypes of those mutants described previously.

Wb. One of the determinants (probably the most important) of the colour of the agouti coat is the width of the band. Generally, the wider the band, the lighter, or more yellow, the coat. This feature is under the control of a major locus designated as Wide band (wb). Among the Felids, only the jaguarondi may have produced a mutant of this nature. On the other hand, the sandy versus grey morphs of some species could be due to a wide band gene. It may be mentioned that animals with very wide agouti bands have a close resemblance to the non-extension (e) phenotype.

Several loci producing a full white phenotype are known. These differ from complete albinism by having either brown or blue eyes. Also, these genes are frequently inherited as dominant to type. The main reason for describing these genes is that, unless the eye colour can be examined, it is easy to confuse the phenotype with albinism. The possession of an all- white coat is not itself conclusive evidence of albinism, the eye colour should be particularly noted.

S. The presence of white areas in the coat is known as piebald in genetic parlance (partial albinism in zoological). Piebald spotting is known in the domestic cat, where it produces highly variable and often extensive white areas. The condition is due to a dominant gene S. Similar genes may occur in other Felids (e.g., the lion) although these may not necessarily be inherited as a dominant. Some piebald mutants produce erratic patterns while others tend to have fairly regular expression (e.g., midriff bands).

Silvering is usually due to the presence of all-white or white tipped hairs in the coat. The condition is termed silvering when the coloured hairs greatly outnumber the white, but roan when the white hairs are so numerous that the coat appears whitish. These genes may be inherited either as dominant or recessive. POLAND (1892) has described a number of instances of Felid skins showing various degrees of silvering. The presence of a few white hairs here and there in the coat may be due to local failures of the pigmentary system and is often not inherited.

Most of the Felid species have a characteristic and, in the main, con- sistent striped, spotted or rosetted pattern (cf. WEIGEL 1961) of dark pig-

8 ROY ROBINSON

ment over drab background coloration. Even subspecies variation rarely (never?) results in sharp departures from type. The background colour is usually agouti while the dark pattern consists of concentrations of eumelanin. The pattern may be functionally useful as concealment. In the domestic cat, three variations of the pattern are known. The type tabby pattern (as manifested by Felis silvestris, for example) is mackerel tabby. The other two are known as Abyssinian (where the pattern is absent from the body but persists on the head, limbs and tail) and blotched tabby (where the body pattern consists of blotches and whorls instead of regular stripes).

The interesting aspect of this variation in the domestic cat is that the three patterns are produced by three alleles of a single locus. That is, simple allelic changes at a single locus are responsible for three very different patterns. The type or mackerel form is phenotypically relatively stable. Such variation as occurs is in the direction of attenuating or break- ing up of the stripes into spots, similar in general terms, in fact, as the variation shown by the silvestris-libyca complex of subspecies (PococK 1951, WEIGEL 1961). On the other hand, the pattern manifested by the blotched tabby is very variable, both in amount and peculiarities of formation. Some, at least, of the variation is due to polygenes, dependent for their expression upon the presence of the blotch tabby allele.

On the basis of this situation in the domestic cat, one may advance the hypothesis that the characteristic Felid dark eumelanic pattern is primarily under the control of a single locus. Thus far, distinctive changes of pattern have been described for the cheetak and leopard, and probably for the Canadian lynx and serval. Experimental evidence for the hypothesis is lacking at this time but the concept has the merit of being genetically simple. The melanoid pattern is so basic to the Felidae that its progressive variation from species to species can be plotted (see WEIGEL 1961, EWER 1973). The inference is that the pattern is primordial, being modified to suit the evolutionary needs of different species. Even those species which are apparently devoid of the pattern may still carry the main gene. This is shown by characteristic facial markings of some species, on the one hand, and the presence of spots in the juvenile pelage of other species on the other hand. The postulated primary locus for Felid pattern will be designated as T (after the domestic cat).

The "restricted" pattern shown by the jungle cat, puma and probably others, has a sufficiently close resemblance to the Abyssinian tabby of the domestic cat, that it may be asked if the pattern is determined in a similar manner. However, there are differences which make the possibility un- likely. The results of crosses between the leopard and puma indicate that the absence of a pattern is recessive to its presence. This is contrary to the

GENETICS OF F E L I D A E

situation in the domestic cat, where the Abyssinian pattern is dominant. However, the results are inconclusive because, if the restricted pattern is due to an allele of T, it does not necessarily have to behave as a dominant in the genetic milieu of leopard and puma genomes.

However, a more convincing reason for thinking that an allelic difference at the postulated T locus is not involved is that cubs of both the jungle cat and puma display a spotted pattern on the body, whereas the kittens of the Abyssinian cat do not. This suggests that the jungle cat and puma have a spotted pattern which is supressed in the adult coat by the action of other genes. It is these which appear to be inherited as recessives in the hybrids of crosses between various Felid species.

It may be noted that a melanoid pattern of spots or stripes is present in certain other families of carnivora, namely, in certain species of Hy- aenidae and Viverridae (and Procvonidae, if the banded tail of several species is taken to be indicative of a vestigial melanoid pattern). These families are regarded as fairly closely related to the Felidae; a fact which implies that the pattern has been derived from a common ancestor. The similarity of pattern for certain species of all three families is striking and would seem to be indicative of direct evolutionary descent rather than of convergence. The fundamental nature of the postulated locus T is therefore not confined to the Felidae.

A very real problem in homologizing mutant loci is the existence of "mimics", that is, genes with similar phenotypes at different loci. Such genes are known to exist in many species although to appreciate the extent ofgene mimicry, it is necessary to turn to a species with a large number of mutants. The obvious mammal is the house mouse (or rodents in general). It is possible to perceive that most of the mutants of the ABCD- EP loci have mimics; some more so than others. The least affected loci are A and C. To allow for mimicking loci, it is possible that saltational variation should be taken as representing groups of mimic loci, of which certain mutant phenotypes may be taken as representative. On the other hand, most of the reported mutant phenotypes for Fields so closely resemble recurring mutants at the ABCDEP loci that there is little need to seek further afield at this time.

Karyological Considerations

Karyologically, the Felids appear to constitute a relatively closeknit group. The gross morphology of the chromosomes displays surprising similarities. Table 2 summarizes the salient details of the karyotypes for 29 species, based upon the observations of Hsu et al. (1963), Hsu &

10 ROY ROBINSON

TABLE 2

KARYOLOGICAL DATA ON THE FELIDAE

Species Haploid number

Meta-and Acro-and submeta- subacro- No. of centric centric chromo-

chromo- chromo- some somes somes arms

Old World species A c i n o n y x j u b a t u s Schreber

(Cheetah) F e l i s a u r a t u s

(African golden cat) - b e n g a l e n s i s Kerr

(Leopard cat) - c a r a c u l Schreber

(Caracul lynx) - - c h a u s Guldenstaedt

(Jungle cat) - d o m e s t i c u s Linnaeus

(Domestic eat) - l i b y c a Forster

(African wild cat) - m a r g a r i t a Locke

(Sand cat) - n i g r i p e s Burchell

(Black footed cat) - o r n a t a Gray

(Indian desert cat) - s e r v a l Schreber

(Serval) - s i l v e s t r i s Schreber

(European wild cat) - t e m m i n c k i Vigors & Horsfield

(Temminck's golden cat) N e o f e l i s n e b u l o s a Griffith

(Clouded leopard) P a n t h e r a l e o Linnaeus

(Lion) - o n c a Linnaeus

(Jaguar) - p a r d u s Linnaeus (Leopard)

- t i g r i s Linnaeus (Tiger)

- o n c i a Schreber (Snow leopard)

19 18 1 37

19 17 2 36

19 18 1 37

19 17 2 36

19 17 2 36

19 17 2 36

19 17 2 36

19 17 2 36

19 17 2 36

19 17 2 36

19 17 2 36

19 17 2 36

19 17 2 36

19 17 2 36

19 17 2 36

19 17 2 36

19 17 2 36

19 17 2 36

19 17 2 36

T a b l e 2 c o n t i n u e d

GENETICS OF F E L I D A E 11

Meta-and Acro-and submeta- subacro- No. of

centric centric chromo- Haploid chromo- chromo- some

Species number somes somes arms

New World Species Fel i s c a n a d e n s i s Linnaeus 19 17 2 36

(Canadian lynx) - co loco la Molina 18 18 0 36

(Pampas cat) - c o n c o l o r Linnaeus 19 18 1 37

(Puma) - g e o f f r o y i D'Orbigny & Gervais 18 18 0 36

(Geoffroy's cat) - p a r d a l i s Linnaeus 18 17 1 35

(Ocelot) - r u f u s Guldenstaedt 19 17 2 36

(Bobcat) - t i g r ina Schreber 18 18 0 36

(Tiger cat) - v iverr ina Bennett 19 18 1 37

(Fishing cat) - w i e d i Schinz 18 17 1 35

(Margay cat) - y a g o u a r o u n d i Desmarest 19 19 0 38

(Jaguarondi)

REARDEN (1965), WURSTER t~ BENIRSCHKE (1968), WURSTER (1969), JOTTERAND (1971) and WURSTER-HILL (1973).

The chromosomes of the domestic cat have been repeatedly examined and there is now an extensive bibliography (ROBINSON 1959, 1971, 1972). The consensus of opinion is that the cat has five large and three small metacentrics, together with eight large to medium submetacentrics and two small acrocentric autosomes. The X chromosome is a medium sized metacentric and the Y is a small submetacentric. These 19 chromosomes comprise a total of 36 chromosome arms (fundamental number). The presumed ancestors of the domestic cat (either F. silvestris or F. libyca, probably the latter) have karyotypes which are identical with the above.

It is not to be expected that all of the Felid species will have exactly identical karyotypes but the punished photographic representations indicate a considerable degree of similarity. Table 2 shows that the majority have 19 chromosomes and 36 chromosome arms. Actually, the similarity is closer than these figures would suggest, for the numbers of large, medium and small autosomes are comparable. The similarity is apparent for

12 ROY ROBINSON

even those species with less than 19 chromosomes. The reason is that the changes have been at the expense of the small acrocentrics. In four species (A. jubatus, F. bengalensis, concolor and viverrina) one of the acrocentrics has been modified to a metacentric, presumably by a pericentric inversion (19 chromosomes, 37 arms). In the case ofF. yagouaroundi, both of the small acrocentrics have been modified in this manner (l 9 chromosomes, 38 arms).

However, there are five interesting species with only 18 chromosomes. In three (F. colocolo, geoffroyi and tigrina), all of the 18 chromosomes are metacentric (36 arms), as if the two acrocentdcs had fused into a single metacentric, the number of arms remaining unchanged. In the case of the other two species (F. pardalis and wiedi), one of the small acrocentrics has disappeared but with no increase in the number of metacentrics. These species possess 18 chromosomes but 35 arms. It is possible that the pair of acrocentrics have been lost during evolution but it is more probable that the missing chromosome has fused with one of the metacentrics.

WURSTER (1969) has argued that the modern species of Felids are probably derived from a common ancestor in the upper pliocene, as recently as five million years ago. She conjectures that this putative ancestor may have arrived at a fairly stable gene arrangement. The karyotypic similarities, of course, are the basis for the conjecture. There is a rather conspicuous and readily recognisable autosome, a small submetacentric satellited on the short arm, which is present in all those Felids so far karyologically investigated; with the possible exception of the African golden cat. The existence of one chromosome apparently common to all species is not conclusive that all or most of the chromosomes are to be regarded as homologous in all species. However, it is to be hoped that this possibility can be largely resolved by the application of the new karyological techniques which bring out banding patterns specific to individual chromosomes. Such a study should clarify a number of problems; in particular, the extent to which the species appear to have chromosomes in common and whether or not the small acrocentrics have transformed by the processes of inversion and fusion in the manner speculated above.

It is noteworthy that the five species with 18 chromosomes all belong to Central and South America. It is tempting to assume that this is no accident and that the processes which led to the reduction of chromosome number were related to the colonization of the Americas. The jaguarondi, which has the most aberrant Felid karyotype so far discovered, is also a Central and South American cat. South America is usually depicted as being populated by Felids crossing the Bering Straits and slowly find- ing their way via North America. This would imply that the South Ame- rican species have a more recent evolution but not necessarily a more

GENETICS OF FELIDAE 13

highly evolved karyotype. Selection pressures were doubtless different from those of the Old World, perhaps even from those of North America, and may have been less severe for certain critical periods so that divergent karyotypes and speciation could have occurred. The evolution of the five distinctive felid karyotypes has been discussed by ROBINSON (1974).

Hybridization

Where a difference of body size is not an obstacle to copulation, many of the species will produce hybrid offspring. The most spectacular hybrids are those from the big cats. It is very doubtful if hybridization will occur naturally in the wild, even in those cases where the territorial ranges of two or more species overlap. Differences of general and sexual behaviour are probably too great. The situation is otherwise in zoos, where individuals of different species can be familiarized with each other and the usual sexual behaviour subtly modified.

GRAY (1972) has conveniently summarized the literature on hybrids among the Felidae. Most of the larger species will hybridize with each other, producing viable and often vigorous offspring, for example tigons (from the cross of male tiger with female lion), ligers (from a male lion with female tiger) and leopons (from leopard and lion). These hybrids are well known and have been produced on numerous occasions. Less well known are hybrids (or alleged hybrids) of leopard with jaguar, puma and tiger, lion with jaguar, and jaguar with puma. In most cases, the fertility of the hybrid has not been adequately checked but it seems that the male hybrids are nearly always (if not invariably) sterile but the females may be weakly fertile. This seems to be definitely the situation for tigons and ligers.

A similar picture emerges for the smaller sized species. For instance, hybrids have been obtained between the domestic cat and bob cat, black footed cat, leopard cat and tiger cat, and between jungle cat and leopard cat (LEYHAUSEN t~ TONKIN 1966, GRAY 1972). Again, no adequate assess- ment has been made of the fertility of most of these hybrids. A most interesting cross is that between the domestic cat and the tiger cat (LEY- HAUSEN • FALKENA 1966), for the former has 38 chromosomes and the latter 36. Despite this difference, seven hybrids were produced. Of these, three were still-born (unsexed) while the four survivors were females. The numbers are small but it is possible that the male hybrid is less viable than the female. Sterility seems to be the rule for all of the above hybrids.

Hybrids between the domestic cat and the European wild cat have been obtained repeatedly. These offspring are fertile although apparently more

14 ROY ROBINSON

susceptible to diseases which would not seriously harm a domestic cat. Hybrids of domestic cat and steppe cat (F. lybica caudata) are reported to be fertile. Offspring from crosses of European wild cat and various subspecies of F. lybica have been obtained but little information seems to be available on the fertility. A cross between the domestic cat and jungle cat has produced viable offspring of both sexes and the female hybrids are fertile (JACKSON & JACKSON 1967). The fertility of hybrids from the domestic cat and either the European or African wild cat is not surprising since either or both are thought to be the wild ancestor of the domestic. However, the fact that the female hybrids between the domestic cat and jungle cat are fertile is interesting. These two forms may be more closely related than they are often represented.

To summarize the above results, it would seem reasonable to hypo- thesize that, physical barriers apart, all of the Felid species are capable of producing hybrids. The karyotypes are apparently sufficiently compatible to support normal development (i.e. mitosis) but not compatible enough in all cases that meiosis can be completed.

Some observations on hybrid phenotypes concern pattern formation. The stripes of the tiger are a distinctive pattern among Felids since spots or rosettes appear to be more general. The meagre data available imply that tiger type striping behaves as "dominant" to the leopard type spotting or to absence of pattern as found in the lion. Obvious stripes are present although they may be less intensive, less well-formed or broken up into spots on some regions of the body. it is impossible to judge how many genes are involved in the development of stripes versus spots since no F 2 generation young have been produced. The fact that the stripe pattern of the F~ is less well-formed than that of the tiger merely suggests that polygenes may be involved which stabilize the pattern. It is possible that these are absent in the leopard and lion. If the hypothesis made earlier of a single major locus controlling the development of the Felid pattern is true, it may be suggested that the striped versus spotted pattern is due in the main to a simple allelic difference.

The offspring from crosses of leopard with lion showed the spotted pattern of the leopard, although somewhat attenuated. Very similar results have been obtained for the hybrid offspring from leopard and puma. Both the lion and puma lack spots as adults but have the pattern as cubs. The ability to produce the pattern is thus not absent but is suppressed in the adult coat by other genes. The leopard has evidently introduced genes which almost fully counteract the effects of these suppressors. Likewise, in the cross of tiger with lion of the preceding paragraph, the tiger introduced genes which nullified the suppressor genes present in the lion.


Gene Conservatories

Geneticists who work with laboratory animals are aware that many of the more interesting genes tend to be less viable than normal and have to be consciously safeguarded against loss. This fact has prompted the idea of gene conservatories. Groups of workers sharing a common interest mutually agree that each one shall be primarily responsible for maintain- ing specific genes.

A combination of world wide social and economic events is forcing zoos into thinking along the same lines, as regards species conservation. In their case, it is the encroachment of human activity on the habitat of certain species which is causing concern. This activity ranges all the way from incidental destruction of the environment or food supply, to active persecution of the species. Because of their position in the animal hier- achy, life-style, often need for a specialized habitat and their size, the carnivores are being particularly threatened. The Felids, especially the larger species, are seriously endangered. Fortunately (if the word can be used), the larger Felids are of considerable economic importance for zoos and efforts are being made to breed them in captivity. This is highly desirable but the need is so great and the margin of safety is so small in terms of perfecting breeding techniques for "difficult" species, that there is no room for complacency.

It is the dream of many conversationists that game reserves can be established where the remnants of threatened species may survive under natural or near natural conditions. This is a splendid concept, of necessity a compromise between the needs of human and animal communities. Whether the concept can endure is dependent upon various factors, primarily economic in the last analysis. Most of the reserves must be situated in the so-called underdeveloped countries whose resources are meagre in relation to their difficulties. On the other hand, many governments are coming round to the proposition that game reserves can be a lucrative tourist attraction. This fact gives rise to hope, but the outcome is far from settled and in the long term there is little ground for real optimism. There is no sign that the pressures on the environment will relax in the future but, on the contrary, that they will probably intensify.

Currently, lists of endangered species are being compiled and in.some instances active steps are being taken to breed certain species in captivity. The object is three-fold, to breed sufficient numbers to meet the require- ment of zoos for new stock, obviate the need to capture wild specimens, and eventually to produce a surplus for refurbishing depleted habitats and for supplying stock to game reserves. To this extent, as far as the larger

16 ROY ROBINSON

Felids are concerned, zoos are of crucial importance for conservation. The question is whether these institutions can take over this function. It will require a high level of co-ordination to tackle the task efficiently. Fortunately, many zoos have expressed willingness to meet the challenge.

It is right that endangered species should have priority but it should be appreciated that rare variants are also in the same predicament. If these are not nursed in the early stages, there is the danger of accidental loss. The plea is made that, as part of the policy to breed animals in captivity, animals of unusual genetic qualities need special consideration. Where a Felid is a rare genetic form, as well as being an endangered species, pre- servation of both will serve a double purpose. The case of the white tigers of Rewa is a fine example of a genetic mutant being preserved for posterity. There are obvious scientific and economic justifications for preserving rare forms of any species. The point to emphasize is that zoological gardens of the developed world may eventually be the only ones with the capability to properly conserve rare species and forms.

Known Mutant Genes of the Domestic Cat

The domestic cat (Felis domesticus) is the only Felid which can be subject to experimental breeding on any scale. The genetics of the various colours have been largely elucidated (ROBINSON 1959, 1971). These pro- vide a convenient frame of reference for genetic forms which may arise in other species.

The tabby pattern of the cat is made up of two main components; (1) agouti ground colour and (2) tabby striping. The agouti background forms the brown-grey colour underlying the melanoid tabby pattern. Agouti is produced by black hairs which are banded with yellow; the brown-grey effect resulting from overlapping of the hair fibres. Imposed upon this is the tabby pattern, consisting in the main of all-black hairs. The border between the tabby and agouti areas is not abrupt but reasonably definite because of rapid displacement of the agouti hairs by the all-black. It may be remarked, however, that this is a variable quantity, some individuals have a well defined tabby pattern which other do not. This variation is discernible in both the domestic population and in geographical races of the silvestris-libyca species complex, the putative ancestor of the domestic cat.

Black cats are due to the elimination of the yellow band from agouti hairs. The tabby pattern is unaffected, as may be verified by careful examination of the coat in bright light. In kittens, and often in adults, the pattern can be seen as a dark adumbration. The responsible gene is termed


non-agouti (a) and is inherited as a recessive allele at the agouti locus. Black is by far the most well known variant for Felids, as may be seen by the first column of Table 4. In the leopard, the black form is inherited as a recessive and the typical pattern of spots can been seen as a dark shadow, precisely as in the cat. The same adumbration typical for the species, has been observed for four other species and this may be regarded as cir- cumstantial evidence that a similar mutant gene is involved in each case.

Chocolate brown (b) is due to a recessive allele of the brown locus. This colour is known for the domestic cat but not reliably for any other species.

The albino locus has produced several interesting mutant alleles. The most well known is the Siamese cat, an example of acromelanic albinism (c~). The eyes are blue, while the extremities (nose, ears, feet and tail) are pigmented. The body fur may be off-white or cream coloured but also light sepia in many animals. This difference is sometimes taken to indicate that more than one acromelanic allele exists but there is no experimental evidence for this. The variation in amount of body fur pigmentation is probably due to polygenes.

Complete albinism (c) has been reported in the cat on several occasions. Curiously, it has not been possible at present date to perform a genetic analysis and this implies a modicum of doubt.

A chinchillated allele (c b) is known and produces the Burmese breed of cat. The phaeomelanin pigment is modified to light yellow and eumelanin to a dark sepia-black. Although both c b and c s are inherited as recessive to wild type (C), c b is incompletely dominant to c ~, so that the heterozygote cbc ~ is lighter than cbc b but darker than c~c ~. The order of dominance is conventionally taken to be C > c b > c ~ > c.

Mutation of the D locus has produced an allele (d) which "dilutes" both black and yellow pigment to slate-blue and cream, respectively. The blue tabby cat can only be described as "drab" in colour. The self blue is due to the combination of non-agouti and dilute ( a a d d ) . Various bluish or drab coloured variants have been reported for several Felid species and these could be due to mutants of the d type.

The non-extension of black mutant produces a yellow phenotype, with deeper areas corresponding to the tabby pattern. A recessive yellow phenotype is described by DYTE (1962) and has been attributable to an e mutant. This observation requires confirmation (since other explanations are possible) but yellow variants have been observed in a number of Felid species (Table 4) and the simplest hypothesis is that these are caused by mutants at the e locus.

It is possible that a mutant comparable to supra-extension of black was discovered by TJEBBES (1924). In his crosses, matings of black animals

18 ROY ROBINSON

produced tabby offspring. However, these results have not been confirm- ed and it is probably that the dominant black gene was confined to one particular stock of cats and has been lost.

It is curious that in the cat, the gene (O) producing the commonplace ginger animal is sex-linked, whereas in almost all other mammals, the phenotype is autosomal. This raises the intriguing question whether or not some of the yellow variants of other felids might be sex-linked. A few simple breeding experiments would decide the issue but even if these are excluded, it should be possible to uncover evidence for sex-linkage. In the female, the heterozygote would be expected to be a parti-coloured animal of wild type and yellow areas (tortoiseshell in the cat). The yellow patches may not always be as prominent as the type. If parti-coloured animals occur in company with all-yellow, it may be surmised that a sex- linked gene is involved.

A presumptive mutant of the pink eyed dilute (p) form is described in the cat by TODD (1961). The eye colour is pink and the coat a light tan. The eye colour must always be inspected in the case of suspected pink eyed mutants because the coat often resembles that due to d.

The tabby pattern of the cat has three fairly easily identifiable forms. These are: the striped, with vertical and slightly curving stripes, defined as the wild type (genetic definition) for the animal (it is also manifested by Felis silvestris). The blotch, when the pattern forms whorls and blotches of heavy pigmentation; lastly, the Abyssinian, where the pattern is absent from the body but persists on the head and as barring on the limbs and tail. These forms are inherited as alleles of a single locus T. The order of dominance is Abyssinian (Ta), striped (T ÷) and blotched (tb). Note, that the sequence is from a lighter to a darker pattern. There is the remote possibility of another allele, the spotted tabby, but this may be merely a polygenic modification of striped, parallel to the transitional variation of the silvestris-libyca pattern.

Piebald spotting is a term applied to white areas anywhere on the body but especially on the breast and belly. There is a certain regularly in the expression of the spotting. The nose, feet and belly are usually the focal sites for appearance of the white. With increasing amounts of spotting, the head region, much of the leg, shoulders and hips, and the lateral regions of the body become involved. With high grade spotting, the distribution of white is extensive, until eventually the animal can be predomin- ately white, with the pigment areas restricted to blotches or spots. The white spotting is ascribable to a single incompletely dominant gene S, such that S+ have less white than SS on the average (KuHN & KRONING 1928).

"Restricted white" spotting also occurs in the cat, as small tufts or spots


of white on the undersurface of the chin, breast and mid-venter. The axillary region of the legs is often involved. There is doubt if this minor of spotting is monogenic (as has been proposed) or if it is largely nongene- tic. The depigmented areas may simple represent those areas of the skin which failed to receive the normal complement of migrating melanoblasts during embryogenesis.

The fully white cat with yellow, blue or odd yes (one yellow, one blue) is due to a dominant gene W. The variation of eye colour is due to the fact that W may fail to induce blue eyes in all animals. These cats are often deaf, especiaily those with at least one blue eye, but yellow eyed individuals have been known to be afflicted. Small spots of pigment may occur on the head of kittens, sometimes persisting into the adult coat but often disappearing. The W gene appears to produce a syndrome of white coat, blue eyes and deafness but only the white coat attains full expression in every animal.

For many years it was believed that the silver and chinchilla breeds of cat were due to a mutant allele of the albino locus (KEELER ~; COBB 1933). However, recent work has shown that the phenotype is a mimic of the typical chinchillated animal and is due to a dominant gene/, independent of the albino series (TURNER & ROBINSON 1973). The gene inhibits the formation of pigment in the coat, particularly the basal portions of the hair (so-called undercolour) and other areas of the coat which are lightly pigmented. There are the agouti areas between the tabby pattern and the outcome, at first sight, is a phenotype deficient in yellow pigment. No comparable form has yet been described for other Felids.

Mutant Forms in Wild Felids

Acynonyx jubatus (Cheetah)

PococK (1927a) gives details of a notable variation of pattern for the cheetah, in which the typical spotted pattern is replaced by stripes and blotches. The form was considered at first to be a new species (A. rex) but this seems doubtful (PococK 1939). Disregarding the actual change of pattern (spots to stripes), the change is comparable to that from striped tabby to blotched tabby in the domestic cat. In other words, the rex form in the cheetah is probably due to a mutation.

Felis aurata (African golden cat)

The African golden cat exists in two colour phases, a yellow and a grey (MENSCH & BREE 1969). However, it is not altogether clear if the

20 ROY ROBINSON

T A B L E 3

SUMMARY OF KNOWN COAT COLOUR MUTANT GENES IN THE DOMESTIC CAT

Symbol Designation Symbol Designation

a Non-agouti I Inhibition of pigment b Brown O Orange (sex linked) c b Burmese p ? Pink eyed dilution c* Siamese S Piebald c Albino T a Abyssinian tabby d Dilution t b Blotched tabby D b ? Dominant black W Dominant white e Non-extension of black

The query sign (?) indicates tha t the existence of this mu tan t requires confirmation.

difference between the two phases is saltational, for animals of intermedia- te colouring between the two phases are known.

Felis bengalensis (Leopard cat)

The occurrence of a melanistic individual is briefly mentioned by ULMER (1941) for the species.

Fells canadensis (Canadian lynx)

Several variants are described by POLAND (1892) for skins of the Cana- dian lynx. He lists a drab blue, yellow and fawn, as well as a specimen with large spots on the back. These forms are suggestive of a blue dilution, an e type replacement of black pigment by yellow and a mutation at a locus controlling the nature of the Felid pattern. The amount of spotting in the Canadian lynx is variable and many animals may have very little. The change in the present case, therefore, is apparently in the direction of greater development. SCHWARZ (1938) has described a pale variant with a phenotype typical of blue dilution.

Felis caracul (Caracul)

UL~IER (1941) mentions a single report of a black specimen of caracul; possibly a non-agouti form. POLAND (1892) describes a skin as being of a yellowish-drab colour. This could represent an e type mutant or, possibly, a pink-eyed dilute type. A recent article (Anon. 1970) has described the occurrence of a grey form of the caracul from Nigeria.

POLAND (1892) has described skins with white or silvered hairs. Whether or not this variant is likely to be monogenically inherited is open to ar- gument but such mutants are known for several rodent species.

GENETICS OF FEL1DAE 21

Felie chaus (Jungle cat)

COLEMAN (1974) reports the occurrence of black specimens of the species. Piebald spotting has been noted in animals exhibited at the Na- tional Zoological Park, Washington, D.C. by Nell B. Todd (personal communication 1974). The spotting occurred on the chest and forepaws.

Felis colocolo (Pampas cat)

A black male is reported by COLEMAN (1974).

Felis concolor (Puma)

YOUNG & GOLDMAN (1946) mention that black pumas have been reported on rare occasions and, apparently more rarely still, instances of albinism. Grey and reddish phases are recognised in wild populations (GRINNELL, DIXON & LINSDALE 1937, SANBORN 1954), the latter conceiv- ably being due to e type mutation.

Felie geoffroyi (Geoffroy's cat)

All black forms are recorded by COLEMAN (1974) which probably represent non-agouti mutants.

Felis jagouaroundi (Jaguarondi)

The jaguarondi has a red form which is said to be common in certain regions of South America (TATE 1931). According to BURTON (1962), the grey and red forms can occur in the same litter of cubs. This implies monogenic control of the red colour; hence an e type gene may be involved.

SEARLE (1968) mentions that a reddish form, with an extra-ordinary wide agouti band to the hair, a dark melanic form (not black since grey agouti hairs persist on the head and neck) and a form with much reduced red pigment, to become almost chinchillated, are known for the species. The implication is that these could be mutants to wide-band, dominant black and chinchilla, respectively.

Felis libyca (African wild cat)

DREUX (1967) has examined skins in the museum of Paris of this species and found yellow speciments which resemble e type phenotypes.

22 ROY ROBINSON

Felis pardalis (Ocelot)

POLAND (1892) records that skins with red stripes are known. These may represent mutants of the e type.

Felis rufus (Bobcat)

Black variants have been observed by ULMER (1941) and by HAMILTON (1941). Under strong light, the typical bobcat pattern of spots could be seen as an adumbration to the melanism. In this respect, the black bobcat shares a common property with black forms in several other species. YOUN6 (1948) has reported the occurrence of an albino specimen. SCHANTZ (1939) has described a bobcat with two white front feet. Only the toes and tip of the foot are affected and it would seem that the condition represents minor white spotting.

POLAND'S (1892) compilation of unusual colours observed among fur bearing animals lists the occurrence of light blue and reds of various shades for skins of the bobcat. These forms could represent phenotypes stemming from mutant genes of the dilution (d) and non-extension of black (e) types. An "almost white" form is also mentioned by Poland. This could be a possible chinchillated mutant but the description is too vague for certainty.

Felis serval (Serval)

Five reports of black servals are noted by SHORTRIDGE (1934). This is probably the source of HUXLEY'S (1955) brief citation of the occurrence of black individuals in this species. In one animal, the spots could be seen standing out as a darker pattern in certain lights. This latter comment brings the black form into line with the non-agouti forms of the domestic cat and leopard.

Two distinctive colour phases of the species are recognized. The serval or large spotted, which has some striping as well as spots and the servaline or small spotted which has fine spots and no striping. The difference of pattern could be due to geographical isolation, although DORST & DAN- DELOT (1970) state that both phases can occur in the same litter. If the difference is not polygenic, mutation at the postulated primary locus for Felid pattern may be proposed.

Felis silvestris (European wild cat)

PococK's (1951) monograph on the genus Felis describes a number of forms in which the amount of yellow pigment is greatly reduced. Pocock


describes these as "silvery" in general terms but comments that the amount of yellow pigment is variable. This variation could easily be due to chinchilla type mutants, as noted by SEARLE (1968).

However, the chinchillated phenotype has been found in the domestic cat to be due to a dominant gene I which is distinct from the albino locus. Since silvestris may have the ancestral genome of the domestic cat, the chinchilla forms noted above could be instances of recurrent mutants of I rather than of c oh. This aspect must be remembered for all species but particularly for the silvestris-libyca group,

DREUX (1967) has observed that 15 out of 21 skins ofsilvestris examined in the museum of Paris had small tufts of white hairs, corresponding to "restricted white" spotting of the domestic cat. These could represent the heterozygous expression of a single gene or be due to irregular failures of the melanoblastic tissue to reach all parts of the body during embryogenesis.

Felis temmincki (Temminck's cat)

Several early reports of black individuals of this golden cat are cited by DAMMERMAN (1930), who also describes a newly discovered specimen. Subsequently, a black specimen is reported by WENDNAGEL (1938). COLEMAN (1974) could not find any new cases.

Panthera leo (Lion)

POLAND (1892) briefly mentions the occurrence of skins of the lion with yellow instead of black manes. It seems possible that these could be due to e type mutants.

White spotting affecting both the front and hind feet is described by SCHNEIDER (1930). The expansion of white is minor, producing white hair on the toes and flesh coloured markings on the pads of the feet. Inheritan- ce appears to be that of a simple dominant. All of the matings are between white marked and normal animals. This fact could explain the restricted nature of the spotting since the expression is that of an heterozygote. Ho- mozygosity of the white spotting gene could result in an animal with extended white markings. Incomplete dominance is so common to be almost the rule for white spotting genes.

A possible chinchilla mutant has been discovered recently (personal communication from the Director of the Birmingham Zoo, Alabama, 1974). The cub is described as having white or light grey fur, with scattered black guard hairs. The muzzle and paw pads are as darkly pigmented as normal. The eyes do not differ in colour fIom those of a normal 5 - week old cub.

24 ROY ROBINSON

Panthera onca (Jaguar)

Black individuals of the jaguar are a well known recurrent variant of the species (PERRY 1970, COLEMAN 1974). POLAND (1892) even includes the form in his compilation. ULMER (1941) states that the jaguar pattern of rosettes can be clearly seen in the black coat. This makes the condition very similar to the black forms of the domestic cat and the leopard. Thus, the colour could be due to a mutation to non-agouti.

Panthera pardus (Leopard)

The black variety (black panther) of the leopard must be the most wide- ly documented variant among the Felids (PoCOCK 1929b, 1930, 1939, PIZEY 1932, THOM 1944, BAHADUR 1942, EATES 1943, SCHOUTEDEN 1945, 1957, GEE 1948, 1964a, FORAN 1952, TWEEDIE & HARRISON 1965). GEE (1948) speculates that the black form is due to a recessive gene but his data are too inadequate to be conclusive. Since then, however, data have become available and the suggestion of recessive heredity is upheld (Ro- BINSON 1970a, b).

The black form has the appearance of being a non-agouti mutant. The fur is black (glossy when new, brownish when old) and the typical leopard rosette pattern can often be seen in strong light as a darker shadow. The pattern can sometimes be seen in the coat of young cubs. In this connec- tion, the black form resembles non-agouti of the domestic cat.

The normal spotted or rosetted pattern of the leopard is variable and two kinds of variation may be noted. One is the variation associated with sub-speciation (PoCOCK 1930) and the other is abrupt variation which prima facie could be due to gene mutation. Thus far, the latter saltations seem to be in the direction of greater amounts of melanic pigmentation. POLAND (1892) had noted that the typical rosettes may fuse to form a pattern such as might be called a dark tabby in the domestic cat. POCOCK (1927b, 1930) has featured several "nigrescent" forms in which heavy black spots cover most of the animal and are coalescing on the back and sides into blotches and streaks. The more extreme variants appear as a black animal speckled and streaked with yellow. ULMER (1941) has described a skin which matches the above description.

It is to be appreciated that more than one mutant gene could be responsible for the above forms but the situation parallels that observed in the cat. The silvestris pattern of stripes can be modified into the blotched tabby (form catus) where the stripes fuse into whorls and blotches of black pigmentation. In some animals the fusion can be extensive and the


animal very melanistic. Despite the variation shown by catus the difference is monogenic.

Chinchilla type variation is descri bed by PococK (1930), FooKs (1941), INGEN & INGEN (1941) and CRANDALL (1964). POCOCK studied skins and stated that these have pale sandy ground colour, with tan or sepia spots. In Fooks' specimen, the eyes were said to be sky-blue while the ground colour is pale buff, with dull orange spots. Crandall describes his animal as having a pale buff, almost white, coat with light brown spots while the eyes are pink. No mention is made of eye colour by the van Ingens but the body colour is described as white with a pale tan background and rosettes of a dark shade of tan. Evidently, the chinchilla mutants involved are of the more extreme types which degrade the black pigment to a sepia. In Crandall's case, it would seem that the eye is exceptionally depigmented.

POCOCK (1930) has observed a skin which was completely white although the typical leopard pattern of spots could be discerned by reflected light. Unfortunately, the eye colour is not recorded, so the colour could be due to a mutation to either albinism or a form of dominant white.

TURNBULL-KEMP (1967) briefly comments that albino leopards are extremely scarce variants. He also notes the occurrence of a "semi-albino" from the Mwinilungu district of Zambia. it is possible that the latter may be a chinchilla form as described more fully above.

An orange variant is described by POCOCK (1930) in which the spotted pattern is very indistinct, as a result of assimilation into the ground colour. The effect is that of a uniform red. Recently, a similarly coloured animal is reported from South Africa (personal communication from the Director of the National Zoological Gardens, Pretoria, 1969). Mutations of the e type are implicated.

Panthera tigris (Tiger)

The existence of black tigers has been doubted but there is circumstan- tial evidence for the occurrence of such beasts as rare variants (POLAND 1892, HAUXWELL 1914, BURTON 1927, 1928, POCOCK 1929a, 1939, PRA- TER, 1937, REED 1963, GEE 1964a, PERRY 1964, STONOR 1964). Apart from errors of observation, the most valid criticism seems to be that the black animal is really a large leopard. However, granted the element of doubt, it is interesting that one account describes how the tiger pattern of stripes could be discerned in the black animal, in the same manner as it is possible to see this leopard spotted pattern by reflected light in the black form. This observation would seem to constitute good evidence for the existence of a black form.

The event of the Rewa white tigers has rightly excited considerable in-

26 ROY ROBINSON

terest (GEE 1959, 1964a, b, PERRY 1964, HUSAIN 1966, STRACEY 1968, LEYHAUSEN & REED 1971). What is remarkable about this variation is the long history of recurrence, amply documented, and the constancy of phenotype. Even POLAND (1892) records skins which are white with drab or light brown stripes. Editors (1910) recount five incidences extending from 1820 to 1910. Other reports are PO¢OCK (1911), D'ABREU (1916), Editors (1921), ROBINSON (1928), POCOCK (1929a, 1939) and INGEN & INGEN (1941).

GEE (1959) reviews briefly the older literature and presents the first account of the origin of the white tiger of Rewa. Records show that white animals have been known in Rewa for 50 years. In 1951, a white male was captured and successfully bred with a normal yellow tigress. An analysis of the pedigree of the numerous descendants of this union by THORNTON, YEUNG & SANKHALA (1967) showed that the white colour is inherited as a recessive.

The appellation of white for the Rewa mutant form is not strictly appropriate. The ground colour is whitish or white flushed with pale cream, while the stripes are dark sepia brown. The iris of the eyes is bright blue. This description accords very closely to the familiar chinchilla type of mutant and the Rewa tiger may be regarded as such (ROBINSON 1969a). The symbol w was originally given to the mutant gene but the explicit symbol c ch is to be preferred.

Description of other chinchillated tigers indicate that the amount of orange pigment of the ground colour may vary and the intensity of the stripes may vary from blackish to tan. This variation could be due either to modifying genes independent of the main chinchilla mutant or to different chinchilla mutants. It is not unusal for several different chinchilla alleles to occur in the same species, each producing a slightly different grade of chinchillation, and such a situation cannot be ruled out for the tiger.

An apparent clear-out instance of albinism has been reported by NARAYAN (1922). TWO cubs were seen and described as pure albinos. The eyes were said to be pink and, while no mention is made of coat colour, this is presumably uniformly white.

It may be wondered if the specimen noted by PococK (1929a), in which the stripes are said to be reddish-brown and only a little darker than the ground colour, could be an example of a brown mutation. However, probably not, for Pocock refers to the animal as a red tiger and the colour could equally well be due to a yellow e type mutant.


TABLE 4

HOMOLOGOUS MUTANT GENES IN FELID SPECIES.

Degree of homology is indicated as follows: + + almost certain, + probable and ? suspected. The meaning of the gene symbols are defined in the text. A (+) sign under T

indicates a major change of the typical Felid melanoid pattern for the species.

Species Mutant Gene a b c cn e h c d e p S T

+ ( + ) A c y n o n y x j u b a t u m

(Cheetah) Felis bengalensis +

(Leopard cat) - eanadensis

(Canadian lynx) - earaeul +

(Caracul) - ehaus +

(Jungle cat) - e o l o e o l o +

(Pampas cat) - eoneolor +

(Puma) - domes t i cus + +

(Domestic cat) - geo f f roy i +

(Geoffroy's cat) - jagouaround i

(Jaguarondi) - pardal is

(Ocelot) - rufus +

(Bobcat) - serval +

(Serval) - silvestris

(European wild cat) - t e m m i n e k i +

(Temminck's cat) Panthera leo

(Lion) - onca +

(Jaguar) - pardus + +

('Leopard) - t igris +

(Tiger)

+ +

?

+

(+)

+ + + + + + + + + ( + )

+

+ +

+ + +

+

+

+

+

+

+ +

+

+

+

+

+

+

+

+ +

(+)

(+)

28 ROY ROBINSON

References

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