Genetics of the feline diaspora
Recently, strong evidence has suggested that cat domestication occurred in the Near Eastern part of the Fertile Crescent pursuant to agricultural development [14
]. The Mediterranean basin has been previously suggested as the site for cat domestication based on archeological evidence [1
]. Driscoll and colleagues (2007) used mitochondrial sequence and microsatellites markers to elucidate the origin of cat domestication. Because microsatellite markers are a better indicator of more recent genetic diversity, this study focused on microsatellite markers to evaluate the more recent breed origins. Based on the present study, genetic diversity was not substantially decreased by the subsequent diaspora of modern cats from the Mediterranean to other areas of the ancient world. However, there were interesting regional differences in their genetic makeup. FCA, Bayesian clustering and neighbor-joining phylogenetic trees divided all of the world's cats into four distinct groups; Asia, Mediterranean basin, Western Europe and East Africa. American cats consistently grouped with cats from Western Europe, suggesting European settlers probably brought cats to the New World and the cats' time in America has been too brief for significant genetic differentiation.
Genetic diversity remained fairly uniform among various areas within the Mediterranean region. The constant movement of ships and caravans, as well as cats, in this key region of early civilization would have promoted a constant interchange of cats. Although Mediterranean cats tended to be genetically uniform, there were some interesting differences and relationships between certain areas within the Mediterranean region. Bayesian analysis indicated that Italian and Tunisian cats were an admixture of Western European and Mediterranean cats. This mixing supported the historical ties between Tunisia and Western European countries. Cats from Sri Lanka and Singapore were an admixture of cats from Southeast Asia, Europe and everywhere else when defined with K = 3 (). However, some Singapore cats did not appear to be hybrids, but rather a mixed sampling of genetically different cats. This may have been a relic of British colonialism or recent importation. According to the FCA analysis (), Sri Lankan cats and the Abyssinian breed bridged cats of the East and West, perhaps resulting from maritime trade routes in the Arabian Sea or again from recent British colonialism. The most interesting difference involved the Asian cluster of cats, which was genetically distinct from cats of the Mediterranean basin, Western Europe, and Africa. This pattern of genetic diversity indicates that the first domestic cats reached the Far East relatively early, followed by a long period of relative isolation. This isolation may have been caused by the waxing and waning of trade between successions of great ancient empires. The Asian population was of further interest because it was internally segregated. Populations of cats from different parts of Asia (random bred and purebred) were more genetically divergent from each other than local populations within the Mediterranean basin or Western European clusters. This partitioning of genetic diversity within the Asian population was also corroborated by the longer branch lengths within the Asian clade on the phylogenetic tree (). This suggests that not only was the Asian population relatively isolated from the three other regional clusters, but that cats within various regions of Asia were also kept separate.
Genetic variation across random bred and purebred populations
The sub-structuring of populations is important for parentage analyses, forensic applications, individual matching, and disease studies. Random bred cats have the largest within population variance, consistent with their larger population sizes, freedom to migrate, and no artificial selection. However, the various breeds of cats exhibit the largest among population variance, reflecting their distinctness. The within population variance component of random bred cats was 86%, compared to 93-95% in humans [22
], suggesting that individual cat populations are less genetically variable than human populations. Purebred cats, with a within population variance component of only 61%, were less genetically variable than the random bred populations, which was also reflected in the estimates of average heterozygosity. The average heterozygosity of the breeds was 10% lower than the random bred populations (), which in turn was 10% lower than the average for human populations. Worldwide human populations range from 0.50 to 0.78 in average heterozygosity, most being above 0.70. The among populations between regions variance of cat populations was approximately twice that seen in humans (6% in cats, 2.5% in humans) as was the among regions variance (8% in cats, 3.6-4.3% in humans). This increase suggests that cat populations are more genetically isolated due to geography than human populations. The large among populations (24%) and among regions (15%) variance of the breeds is likely a result of the intensive artificial selection and isolation imposed by breeding practices. The Burmese and Singapura breeds have the lowest heterozygosity and the highest FIS
of any breed, reflecting the most intense inbreeding (). The newest CFA breed, the Siberian, had the highest variation, comparable to random bred populations. This indicated that it was derived from a broad foundation stock. The Sphynx, which is a derivative of the Devon Rex breed, also had high genetic diversity. Given these results, Burmese and Singapura breeders should be concerned about genetic diversity, while Siberian breeders should be encouraged to retain existing diversity as their breed becomes more established. Similar to the conservation efforts in captive exotic felid populations, genetic analyses, breed histories and population dynamics could be used to develop breed management or survival programs to maintain genetic variation within the breed gene pool for an extended period of time. In addition, these regional differences in the genetic variation of cats suggest that the genetic markers used in cat DNA profiling should be tested in the diverse populations to validate their efficiency.
Genetic structure and origins of cat breeds
We have demonstrated that genetic diversity following domestication was regionalized in areas of the ancient world, and even within localities within those regions. Some differences could be explained by isolation, while others were best explained by interchanges of animals between clusters and localities. All of these differences involved human activities, but were probably not strictly intentional. However, intentional changes in the genetics of cats ultimately occurred during the development of breeds.
Unlike breeds of domestic horses, dogs, cattle, sheep, etc., some of which are thousands of years old, most cat breeds were developed within the past 150 years, mainly in Europe and the United States [12
]. Although documentation for nearly 80 cat breeds exists, the largest cat fancy association recognizes only 41 breeds [23
]. The Persian, Russian Blue, Siamese, and Angora were among the first cat breeds registered by cat associations. The Cat Fanciers' Association (CFA) designates sixteen cat breeds as “natural” or “foundation”. Fifteen of the foundation breeds are included in this study, lacking only the Manx, the tailless breed of cat that was developed on the Isle of Man.
Purebred cats had similar structuring to the random bred cats of their regions. The Southeast Asian breeds, including Birman, Burmese, Havana Brown, Korat, Siamese and Singapura, form a grouping that is distinct and at the opposite end of the genetic spectrum from the Western breeds, as depicted by the FCA. The Abyssinian and Japanese Bobtails were exceptions and possessed genetic markers common to both Southeast Asian and Western breeds. This indicates that cats from both Asia and Europe were used to create these breeds.
Each of the foundation breeds was genetically distinguishable with 95% accuracy from the others. One of the oldest recognized cat breeds, the Persian, has been used in the development of several other breeds. Cross breeding with Persian cats is often being used to produce a more brachycephalic head type. The Exotic Shorthair is essentially a shorthaired variant of a Persian, which is demonstrated by the complete clustering of these two breeds as one group. The most dolichocephalic breed, the Siamese, has also been used to create numerous other breeds, including Colorpoints, Orientals, Havana Browns, and longhaired breed variants. Although listed as different, most of these derived breeds vary only by a single gene variant, such as hair length, color patterns, and fur coloration; thus, these derived breeds will likely be inseparable as distinct breeds, as was shown with the Havana Brown and Siamese. The Burmese and Singapura grouping proved to be an additional example of recent breed derivations. The close associations of the Persian and Exotic, the Siamese and Havana Brown, and the Burmese and Singapura resulted in the highest branch supports in the neighbor-joining tree and the inability to separate members of each pair by the genetic markers used in this study. However, it is important to remember that most breeds have a written/oral history in addition to a genetic fingerprint. Cat breeding folklore contends that both Burmese and Singapura are indigenous to ancient Burma. Folklore also suggests that Burmese cats from the USA were taken to Singapore, purposely bred with native cats, and then, later returned to the USA as the new breed, the Singapura. Havana Browns are considered a separate breed in the USA; however, European cat breed associations consider them only a color variant of Siamese.
These data show that most, but not all, foundation or modern breeds appeared to have originated from random bred cats of the purported region of origin. The Southeast Asian breeds were strongly associated with the random bred cats from Vietnam, China, Korea, and Singapore. The Siberian is one of the newest cat breeds from Russia and is actively under development. Random bred cats from Russia were not available, but the Siberian had strong associations with cats from the nearby countries of Germany and Finland. Turkish Vans grouped with regional random bred cats from Turkey, Israel, and Egypt. Likewise, cats from the Kenyan islands of Lamu and Pate group with the Sokoke breed, which was developed in Kenya. The Kenyan islands and the mainland were accessed via shipping routes in the Arabian Sea, allowing exchange between India, the Near East, the Arabian Peninsula and Africa. All other breeds and random bred populations form a network of closely related and less distinctive cats of Western European grouping. Surprisingly, the Persian breed was not genetically associated with random bred cat populations from the Near East, but grouped with random bred cats of Western Europe. The Persian is perhaps the oldest recognized cat breed and has undergone selection for an extreme phenotype, which likely involved complex gene interaction. Even though the early Persian cat may have in fact originated from ancient Persia, the modern Persian cat has lost its phylogeographical signature. Similarly, the Japanese Bobtail does not appear to hail from its stated origins of Japan. Although cats were not indigenous to Japan, they migrated to the islands as part of Asian trade routes hundreds of years ago. Introduced as a breed in the USA in 1968, Japanese Bobtails from the USA appear to have been influenced more in their gene pool by European cats rather than by Asian cats. Egyptian Maus also appear to be on the verge of losing their historical origins via genetic influences from Europe. Overall, these results indicate that both the random bred and breed populations group in a manner largely concordant with geography. Breed histories, for the most part, appear to be accurate.
The present study reconfirmed that the Mediterranean was the likely site of domestication of the modern cat. Genetically distinguishable clusters of cats were found in the Mediterranean, Europe, Asia, and Africa. North American cats were closely linked to European cats. The Asian cluster was genetically unique, indicating that it became isolated following its introduction. Genetic diversity remained surprisingly broad among cats from various parts of the world. Genetic data demonstrated that most, but not all, foundation breeds originated from indigenous cats of the regions of purported origin and that this was associated with some loss of diversity. Researchers should recognize the relative recent development of the breeds, which influences linkage disequilibrium and the power of association studies. This study also provides a warning to modern cat fanciers that breed development must be done slowly and with the maintenance of a broad genetic base. Over 20 deleterious genetic disorders have been recognized in modern cats, and all have been identified in pure breeds. The elucidated genetic relationships of the cat breeds can be used by cat breeders to develop more efficient breed management plans.