Proc. Indian Acad. Sei.. Vol. 88 B, Part I, Number 5, October 1979, pp. 311-323, printed in India.
Inbreeding in white tigers
A K R O Y C H O U D H U R Y and K S SANKHALA* Bose Institute, Calcutta 700 009 * Department of Agriculture, Government of India, New Delhi
MS received 14 June 1978
Abstract. One of the problems of breeding of endangered species in captivity is inbreeding, An exemplary illustration is the inbreeding in the white tigers of Rewa. Genealogies and other relevant information on white tigers were collected from four Zoological Parks to investigate whether matings between close relatives were res- ponsible for the reduction in litter size and increase in early mortality which has been observed. Inbreeding coefficients were calculated for different types of mating. It was generally found that tigers failed to survive, if their inbreeding coefficient attained a level of 0.4687 or higher. Regression analysis reveals a tendency for the average litter size to decrease and the early mortality rate to increase with an increase in the value of the inbreeding coefficient.
Keywords. Genealogy; inbreeding coefficient; linear regression; litter size; mortality rate; white tigers.
Inbreeding is known to increase the degree of homozygosity of gone pairs in a population. The closeness o f relationship between individuals mated determip.es the speed of attaining homozygosity. The deleterious recessive genes which are hidden in heterozygous forms are revealed when they become homozygous as a result of inbreeding. There is abundant evidence in guinea pigs, poultry, pigs and cattle that inbreeding is often accompanied by increased early mortality, decreased growth rate, reduction in litter size at birth and pronounced increase in sterility and ,.'n the freqttortcy of congenital malformations (Johansson and Rondel 1968).
To increase the number of animals with a rare character, matings are sometimes made between close relatives. Recently, there has been a sudden decrease in the number of white tigers in captivity, posing a threat to their survival. Reduced fertility and increased early mortality have become common occurrences. In the Zoological Parks of the world there are 30 white tigers of which Calcutta has eight, Delhi nine, Bristol and Washington DC have five each and Gauhati, Hyderabad and Lucknow in India have one each. In July 1970 Delhi and Bristol had 16 and 10 tigers respectively while in August 1974 Calcutta had 13. Between 1969 and 1970 seven cubs were born to one white tigress in Washington DC of which only one survived. It is, therefore, of interest to investigate whether matings between
312 A K Roychoudhury and K S Sankhala
close relatives practised in different zoos have had a role in causing the smaller size of litter and higher rate of mortality now observed.
2. Materials and method
All the white tigers found in zoos today are descendants of one white male, named Mohan, captured ia May 1951 from the forests of Rewa, Madhya Pradesh, India. They are not completely white. They have varying shades of white and cream colour with black or chocolate stripes and their eyes are icy blue. They are generally bigger in size than normal coloured tigers.
Mohan first mated with a normal ooloured tigress, named Begum, also captured from the forests of Rewa. She produced tea normal coloured cubs in three litters. Ia the second litter, one female cub named Radha, whoa grown, was mated to her father, Mohan. Ia her four litters Radha produced 14 cubs of which eleven were white and three yellow. The genealogy of the white tigers at Govindgarh Palace in Rewa is shown in figure 1. The dates of births and deaths of the tigers are indi- cated where available.
A short description of the history and propagation of the white tigers in the Delhi Zoological Park, Calcutta Zoological Garden, National Zoological Park, Washington DC, USA and Bristol Zoo, Bristol, England is given below:
2.1. Delhi Zoological Park, New Delhi
Radha in her first litter produced one male and throe female white cubs named, respectively Rain, Rani, Sukeshi and Mohini (figure 1). Raja and Rani were brought from Rewa to Delhi in 1963. Mated to each other they produced 20 white cubs in seven litters. There were thirteen deaths of which four were acci- dental. Rukko, a white female of the first litter died after being mauled by her mother. Two cubs of the second litter died within a day due to careless handling and neglect of their mother. Ravl, a white male in the third litter died due to sun stroke. The remaining nine deaths are non-accidental. Besides two stillborn cubs, five died at an early age, while two males, Bahadur and Jagl~ in the fourth and fifth litter died of congested lungs ar, d lumber paralysis respectively. Raja mated with his mother, Radha who gave birth to five and four cubs, respectively in her first and second litters and within seven months all the five cubs of her first litter died of pneumonia. Two cubs of her second litter died of starvation shortly after their birth. One white male named Roop was sent to Bristol Zoo in exchange for a white tigress, named Sceta. Rani was then mated to her son Dalip and she produced one white female cub who died of Parkimouse syndrome and pneumonia within nine days after birth. Hari and Ashima born to Rani and Raja in separate litters, had only one stillborn white male.
'In other line, Mohan mated with his grand daughter, Sukeshi, who produced five litters of two cubs each. Out of ten cubs, only two survived. Two cubs of th0 first litter died because they were not cared by their mother. The death of Gautam, a white male of the third litter, was accidental. At the age of 8 years, V|rat, a tiger of the fifth litter, died after a prolonged illness. The remaining four deaths including one stillborn are considered to be non-accidental. Gautam and Heron, the son and daughter of Sakeshi and Mohan had two whim male cabs in
Inbreeding in white tigers 313
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314 A K Roychoudhury and K S Sankhala
one litter but both died of pernicious anaemia shortly after their birth. Homa when mated to Tippu, the son of Rav.i and Raja, produced four cubs in two litters and all of them died of uv.known causes within a few days after their birth. All the white tigers born in Delhi Zoological Park are shown in figure 2. The main causes of early mortality in Delhi have been pneumonia, trauma of the abdomen, conges- tion of the lungs, feline entritis and negligence of the mother.
2.2. Calcutta Zoological Garden, Calcutta
Radha in her second litter, produced two male white cubs (Neeladri and Himadri) and a normal coloured female cub (Malini) (figure 1). All the cubs were brought from Rewa in 1963. They are the progenitors of the white tigers in Calcutta. Malini was mated to Neeladri and she produced seven litters comprising 14 cubs of which seven were normal coloured and the rest white. A male cub of her third litter was put to sleep because he was suffering from gangrene. A female cub (Kiranmala) of her fourth litter was killed by the cub's brother, Barun. Chandni, a white tigress of Malini's first litter, was mated to Himadri and she pro- duced 20 white cubs in six litters. All the six cubs in the first two litters and three cubs in the third litter died in infancy; they were not v.ursed by their mother. Two yellow heterozygotes, Ravi and Sushi, the son av.d daughter of Malini and Neeladri, produced three white and ten normal coloured cubs in three li~ters but all of them died of unknown causes within five days after birth. The majority of deaths in the Calcutta Zoo have been due to feline entritis but a few animals were victims of trypanosomiasis. The genealogy of the white tigers at Calcutta Zoological Garden is shown in figure 3.
2.3. National Zoological Park, Washington DC, USA
Mohini, the daughter of Radha and Mohan in the first litter was brought from Rewa in December 1960 (figure 1). Later she was mated to Radha's normal coloured brother, Samson. In her first litter she had one white male, Rajkumar, one normal coloured male, Ramana, and one normal coloured female, Ramani. All of them con- tracted art acute form of feline distemper. Rajkumar and Ramani died but Ramana recovered. Mohini was pregnant again by Samson and produced two normal colourod female cuba, one of which was stillborn. The normal coloured cub that survived was named Kesari. After the death of Samson, Mohini was mated to her sort, Ramana and she produced two litters. In her first litter a normal coloured male and a white female cubs were born. The male died shortly after birth but the female named Rewati survived. She had crossed eyes and short legs. The male that died had shortened t0ndons cf the forelegs which precluded the arfimal from a normal "treading action " during nursing. In the second litter, there were five cubs consisting of two white males, two normal coloured females and one normal coloured stillborn female. Mohini inadvertently crushed three of her tiny cubs to death. There is a supposition that the cubs were too weak to survive even if they were not crushed. The remaining one, a white male named Moni, died whoR he was 16 months old. His death was attributed to a neurological pheno- menon of the brain (persorml communication). When heterozygous normal coloured Kesari and Ramana mated, they had three, white and one normal coloured cubs. All the white tigers in the National Zoological Park are shown in figure 4.
Inbreeding in white tigers 315
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2.4. Bristol zoo, Bristol, England
A pair of white tigers, namely Champak and Chameli, born to Radha and Mohan in the third litter was sold to the Bristol Zoo in 1963 (figure 1). Mated to each other they produced three litters comprising 14 cubs of which three still survive. All the four cubs of the first litter died within ten days after their birth. A cub in the second litter died and was devoured very shortly afterwards by the mother. Two cubs irt the third litter died in infancy. The artimals Champak, Akbar, Sarala, Shusrnita and Seem died from loss of appetite artd swelling of the abdomeI~.. Sumati was mat0d to Akbar; she produced one white male named Salim, whose kidney was not properly developed. H0 was put to sleep before he was two years old. The genealogy of the white tigers at Bristol Zoo is shown in figure 5.
The skirt colour of white tigers is known to be recessive, to the normal yellow. Thornton et al (1967) demonstrated that when a wild yellow tigress was mated to a white tiger, all their offspring were yellow. When these offspring were back- crossed with the white parent, their progeny segregated into yellow and white coloured cubs lit the ratio o f 1 : 1. Since the publication of the paper by Thornton et al (1967), a number of crossing betweorL heterozygous yellow and white tigers a~d betwoort two heterozygot~s yellow tigers have been made. They confirm the earlier findings. Pooled data show art expected segregation of yellow and white cubs ir~ ratio of 1 : 1 in the former and 3 : 1 in the latter type of crossings (table 1).
Table 1. Test for goodness of fit in two types of crosses.
Phenotypes of offspring Crosses Total
I. Between heterozygous yellow and white parents
Radha Mohan, Delhi Radha Raja, Delhi Malini Neeladri, Calcutta Mohini Samson, Washington, DC Mohini x Ramana, Washington, DC Observed Total Expected total (1 : 1)
3 11 14 5 4 9 7 7 14 4 1 5 4 3 7
23 26 49 24.5 24.5 49
Z 8 = 0 . 1 8 4 d.f. = 1
II. Between two heterogygou8 yellow parents
Sashi Ravi, Calcutta Kesari Ramana Washington, DC Observed total Expected total (3:1)
10 3 13 1 3 4
11 6 17 12"75 4"25 17
Z 2 0-960 d.f. = 1
318 A K Roychoudhury and K S Sankhala
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Inbreeding in white tigers 319
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To examine the relationship between the degree of inbreeding, average litter sizo and non-accidental mortality rate, the inbreeding coefficients (F) for different types of mating wore determined following Wright's (1951) method. These values wore checked by another method given by Kudo (1962). The inbreeding coefficient is defiued as the probability that allelic genes in an individual are identi- cal by descent, i.e. both are descended from a single gone present in one of the ancestors common to both the parents. The values of the inbreeding coefficient for different rantings are shown in table 2.
Sometimes the cubs at the time of their birth wore devoured or neglected by their mothers and as a result all of them died. These accidental deaths have been excluded from the analysis. The non-accidental deaths include all stillbriths and deaths of cubs or tigers caused by known or unknown diseases at an early age. For each coupM, the non-accidental mortality rate was obtained by dividing the number of non-accidental deaths by the total number of cubs they produced. The average litter size and the mortality rate of the cubs for each couple are given in table 2. After pooling together the inbreeding coefficients of similar value and arranging them in ascending order, linear regressions of average litter size and mortality rate on the degree of inbreeding were calculated.
3. Results and discussion
One common feature observed is that the grandsons of Mohan and Radha when mated with their grand daughters have produced litters but no offspring have sur- vived. In all these matings the inbreeding coeificient of the offspring is 0.5000 (table 2). If an offspring is born whose inbreeding coefficient is higher than or equal to 0.5000, there is a great likelihood that it will not survive. There are also instances where offspring having inbreeding coefficients less than 0.5000 met with premature death. For example, all of the four cubs (F = 0.3750) of Homa and Tippu and one of the two cubs (F = 0-4687) of Homa and Gantam in D01hi died within a few days after birth (figure 2). An exception was found in the mating between Kesari and Ramana in Washington DC (Figure 4). All the four cubs ( F = 0.4062) they produced are still surviving.
The linear regressions of average size of litter and mortality rate of inbreeding coefficient (F) are shown below:
Average size of litter :
Mortality rate :
4.0635 -- 2-5443 F
-- 0.5352 + 2.8348 F.
In both the cases, variation due to regression was not found to be significantly higher than the deviation from regression. Lack of sufficient data and the exclu- sion of some data due to accidental deaths might have an influence on the results of this analysis. It is difficult to conjecture what would have been the fate of the cubs, if there were no accidental deaths. However, there is a tendency for the average litter size to decrease and the mortality rate to increase with an increase in the value of inbreeding coefficient as shown by the signs of the regression coefficients. It might be noted that all the offspring (F = 0.4062) of Kesari and Ramana in Washington, DC survived and they had a great impact on the regres-
Inbreeding in white tigers 321
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322 A K Roychoudhury and K S Sankhala
sion analysis. If these offspring were not considered in the analysis, the regression of mortality rate on inbreeding coefficient (F) would have been as follows:
Mortality rate : -- 0.4117 q- 2.8342 F.
In this case, variation due to regression was found to be significant at 5~o. Note that the regression coefficient o f the above equation is same as that of earlier one upto three decimals and this similarity is considered to be fortuitous. To study the effects of inbreeding on the fertility and viability of the guinea pigs, Wright (1922) made similar regression analysis and concluded that at least a share of the degene- ration in fitness was due to inbreeding.
It was recorded in the diaries of the white tigers in Delhi that copulation between Tippu and Homa, Haft and Ashima, Dalip and Sukeshi and Dalip and Homa was observed several times but no pregnancies occurred. Before Virat's death at the Govirtdgarh Palace, his mate, Chameli was there (figure 2). They mated to each other a number of times but there was no result. Similarly, Arun and Rupa (figure 3) in Calcutta were kept in the same enclosure for some time but they did not produce arty offspring. It was noted, at least in Delhi, that the male white tigers were unable to fertilise while the female white tigers were fertile as has been proved by subsequent rantings and conceptiov.s. In Bristol, when Ckameli was mated to Champak, Shusmita to Akbar and Nirmala to Roop, all of them miscarried twice at about 42 days. Sumati was mated to Akbar and Roop, she aborted thrice (figure 5) (personal communication).
Weakening of the eyes and shortness of legs of Rewati in Washington DC (figure 4), rteck twisting of some white cubs in Delhi, lack of development of kidneys irt Salim in Bristol (figure 5), arching of the backborte of Arun in Calctttta (figure 3) artd the occurrence of stillbirths in Delhi and Washington, DC are noticed. These manifestations are no doubt physiological disorders of one form or other. It is further observed that early mortality in inbred white tigers is very common. They are supposed to be more susceptible to diseases than normal coloured tigers. In the absence of arty data from control o.on-iabred lines, all these defects and diseases might be ascribed to environmental rather than genetic causes. But there is no denying that at least a part of the degeneratiot in fitv.ess is due to inbreeding as indicated by the negative sign of the regression coefficient in the case of litter size and the positive sign iv. the case of the mortality rate.
When the inbreeding coefficient is suspected to be correlated with litter size and mortality rate, a breeding plan should be adopted which minimises the inbreeding coefficient of the offspring. The existing white tigers in the zoos are already highly inbred. If art attempt is made to cross them, no improvement in fitness of white tigers is likely to ensue. If a new blood line is introduced to the degenerative white or heterozygous tigers, it is expected that the cubs will not meet with premature death. An attempt has already been made in this direction in the National Zoological Park, Washington DC as well as in the Delhi Zoological Park, New Delhi. When Kesaxi was mated to a normal coloured male, named Poona, she had a litter o f six normal coloured cubs of which only one female named Marvin survived (figure 4). Four of the cubs died from a viral (unspecified) type of pneumonia. The cause of death of the fifth cub was not diagnosed. All of them died within four months of their birth (personal communication). It is difficult to comment unless a number of similar experiments are conducted. Recently, Homa was mated to Moti, a
Inbreeding in white tigers 323
coloured tiger outside the lineage of the white tigers (figure 2). She produced four cubs, of which one was stillborn. Another male cub died within 24 hr of his birth due to starvation as mother 's lactation potemiov, was poor. The growth, development and fate of the remaining two cubs will be interesting to watch.
We are grateful to the authorities of Calcutta Zoological Garden, Calcutta, Delhi Zoological Park, New Delhi, National Zoological Park, Washington DC, USA and Bristol, Clifton & West of E;.glartd Zoological Society, Bristol, England, for supplying the relevant information. We are greatly indebted to Professor W. J. Schull of Center for Demographic al:d Population Gep.etics, The University of Texas Health Soience Centre at Houston, USA for critically going through the manuscript and pointirLg out errors in some values of inbreeding coefficient.
Johansson I and Rendel J 1968 Genetics and Animal Breeding (London: Oliver and Boyd) Kudo A 1962 A method for calculating the inbreeding coefficient; Am. J. Hum. 14 426-432 Thornton I W B, Yeung K K and Sankhala K S 1967 The genetics of white tigers in Rewa;
J. Zool. 152 127-135 Wright S 1922 The effects of inbreeding and crossbreeding on guinea pigs. I. Decline in vigor.
II. Differentiation among inbred families; U.S.D.A. Bull. 1090 p. 65 Wright S 1951 The genetieal structure of populations; Ann. Eugen. 15 323-354