Chromosome Studies of a Fertile Mammalian Hybrid: The Offspring of the Cross Bongo Sitatunga. (Bovoidea)
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1 Chromosoma (Berl.) 41, (1973) 9 by Springer-Verlag 1973 Chromosome Studies of a Fertile Mammalian Hybrid: The Offspring of the Cross Bongo Sitatunga (Bovoidea) L. Koulischer, J. Tijskens, and J. Mortelmans Institnt de Morphologie Pathologique, Loverval, and t~oyal Society of Zoology, Antwerpen Abstract. The offspring of the cross bongo (Boocercus euryceros), 2n= 33 sitatunga (Tragelaphus spekei), 2n=30, has proved to be fertile. This fertility shows that the relationship between the karyotypes of the parental species is a simple one, despite the different diploid numbers and a different sex chromosome determinism, XX/XY in the sitatungu, XX/Y-to-autosome translocation in the bongo:meiotic processes and gametogenesis are not impaired in the hybrid. Introduction Particular sex chromosome rearrangements have been observed in all species of the tribe Strepsicerotini, family Bovoidea, investigated so far (Wurster, 1972). The diploid number of the kudu, Tragelaphus strepticeros, is 2n=31 in the male and 2n=32 in the female (Wallace and Fairall, 1967); the eland, Taurotragus oryx, shows a similar karyotype, 2n~--31 in the male (Koulischer, 1969) and 2n=32 in the female (Taylor and Taylor, 1970); in the bongo, Boocercus euryceros, a diploid number of 33 has been observed in the male and 2n~34 in the female (Wurster, 1972). Sex determinism in these 3 species and probably also in the nyala, Tragelaphus angasi (Wurster and Benirschke, 1968), does not follow the usual XX/Xu pattern. As supported by meiotic studies of the kudu (Wallace and Fairall, 1967) and autoradiographic studies of somatic chromosomes of other species (Wurster, 1972), a u translocation is present, as is a pericentric inversion of the X chromosome. The sitatunga, Tragelaphus spekei, has unusually large sex chromosomes (Wurster et al., 1968), but the diploid number is the same for both sexes, 2n=30. The present report concerns another unusual observation in the Strepsicerotini. A cross between a male bongo and a female sitatunga, has resulted in an unexpected fertile hybrid, the "bongsi". Undoubtedly, the fertility of the bongsi supports the hypothesis of a close and simple relationship between the karyotypes of the parental species. Despite the
2 266 L. Koulischer et al. : different diploid numbers and the different mechanisms of sex determination, no "cytogenetic reproductive barrier" has been observed. Chromosome studies of P, F 1 and F 2 generations, actually living in the Antwerp Zoo, are reported here. Material and Methods The cross bongo sitatunga was successful twice, and twice the "bongsis" were females. A female bongsi was fecundated in 1969 by a male sitatunga and gave birth to a young "3/4 sitatunga". The bongsis and the young are normal and in perfect health. Chromosomes were studied using peripheral blood. The male bongo which fathered the bongsis died in 1966; only recently a new male bongo was available in Antwerp for chromosome studies. Thirty mitoses were counted for each specimen. Results Chromosome counts are listed in Table 1, according to decreasing diploid numbers. The karyotypes show the following characteristics: 1. Bongo. The diploid number is 2n~33 as observed by Wurster (1972). There are 12 meta- or submetacentric pairs, 3 acrocentric pairs and 3 chromosomes which cannot be paired: a middle sized metacentric, the largest acrocentric and a large submetacentric. The X chromosome is the large unpaired submetacentric (the female showing two such Table 1 Specimen Sex 2n Bongo )lale 33 Bongsi Female 32 3/4 Sitatunga Female 31 Sitatunga Female 30 Fig. 1. Karyotypes of the parental species, F 1 and F~ generations. The u chromosome of the bongo is translocated to an autosome (first arrow) ; the X chromosome is almost acrocentric and medium sized (second arrow); the diploid number is 33. The diploid number of the sitatunga is 30; the X chromosomes are the largest of the set; only one pair is aerocentric. The "hongsi" shows 32 chromosomes; the four last autosomes are unpaired; the small metacentric is of maternal origin, the 3 acrocentrics are of paternal origin; one X chromosome is the large "sitatunga X "; the other (arrow) is from the bongo. The "3/4 sitatunga" has 2n~31 chromosomes; the whole set, including the sex chromosomes, is similar to the karyotype of the sitatunga, except for a supernumerary acrocentric characteristic of the bongo (arrow)
3 Chromosomes of the Offspring of Bongo X Sitatunga 267 Fig. 1
4 268 L. Koulischer et al. : chromosomes), and the Y is fixed by centromeric fusion, on an acrocentric autosome, very likely the homologue of the unpaired one. The NF is 59 (Fig. 1). 2. Sitatunga. The diploid number is 2n~30; 14 pairs are recta- or submetacentric and one is a small acrocentrie; all chromosomes can be paired. The X chromosomes are among the largest of the set. The NF is 58. Compared to the bongo, there are 3 pairs of acrocentric autosomes less, and one pair of submetacentrics more; moreover, the short arms of the X chromosomes are larger. The origin of this karyotype could be the following: two pairs of acrocentric autosomes of the bongo have fused following a Robertsonian mode, while a third one was fixed by tandem fusion to the short arms of the sex chromosomes, which appear then metacentric and larger than usual. 3. Bongsis. Both specimens studied showed 2n--~32 chromosomes. As these are female specimens, 17 chromosomes come from the bongo and 15 from the sitatunga. Among the autosomes, 4 cannot be paired: 3 acrocentrics transmitted by the father and one submetacentric transmitted by the mother (one acrocentric autosome of the bongo is arbitrarily paired with the corresponding acrocentric of the sitatunga). The sex chromosomes are morphologically different: the large metacentric is characteristic of the sitatunga, while the smaller submetacentric stem from the bongo. Very likely, 2 of the unpaired acrocentrics of paternal origin correspond to the unpaired small metacentric of maternal origin, and the third one to the distal part of one of the arms of the sitatunga's X chromosome: this specimen is thus cytogenetically balanced. Indeed, if the relationship between the karyotypes of the sitatunga and the bongo is the simple one proposed above, meiosis in the hybrid should not be difficult. Synaptic pairing and achievement of meiosis should be possible, the "free" chromosomes of the bongo pairing with the homologue translocated segments of the sitatunga. The facts support this view, the bongsis having proved to be fertile. 4. 3/4 Sitatunga. The diploid number of this back-cross, sitatunga bongsi, is 31, i. e., the intermediate number between the parental species. The whole chromosome set is similar to the karyotype of the female sitatunga, except for a small supernumerary acrocentric. There is a chromosome imbalance, which apparently does not affect the perfectly healthy specimen. Discussion The study of the fertility of mammalian hybrids indeed appears as an interesting approach to elucidate the mechanisms of new karyotype formation inside a given family. If a hybrid is sterile, very likely complex
5 Chromosomes of the Offspring of Bongo Sitatunga 269 structural chromosome rearrangements occurred in the ancestral species : no synaptic pairing is possible any more between homologous segments; meiosis and gametogenesis cannot be achieved because of the formation of a "cytogenetic reproductive barrier" (Wurster and Benirschke, 1968). This is the case for the mule and the hinny; indeed the somatic karyotypes of the horse and the donkey are morphologically very different, and already suggested complex chromosome rearrangements linked with speciation. On the contrary, if simple chromosome rearrangements (or no rearrangements at all) have taken place during speciation in parental species, the hybrid should be fertile. This is certainly the case for the bongo and the sitatunga. Morphologically, the relationship between the somatic karyotypes of the two species already appeared to be a simple one. This was, however, a speculative opinion; now the fertility of the bongsi indeed supports the view that this hypothesis corresponds to the facts. The presence of a small supernumerary autosome in the 3/4 sitatunga shows that chromosome segregation in the hybrid is not necessarily perfect; not all "bongo chromosomes" migrated to the same pole. A possible explanation is the following; the small unpaired "bongo chromosome" corresponds to the distal part of one of the arms of the sitatunga's X chromosome. It was expected to migrate with the X chromosome of the bongo, but it failed to do so. This could be in relation with a particular behaviour of sex chromosomes at meiosis, although no equivalent of the male sex vesicle is observed in mammalian females (Ohno, 1967). As has been pointed out above, the apparent excess of chromosome material does not seem to affect the animal. The karyotype of the bongsi studied here is only one out some other possibilities. Indeed, a bongsi could be a male, instead of a female, with a different karyotype and a different chromosome number. On the other hand, back-crossed with a bongo, the offspring could present a new karyotype not yet found. Interspecific crosses are perhaps very rare in normal conditions. However, this possibility cannot be ruled out, and has to be considered if "unexplained" karyotypes are found in some isolated specimens. The fertility of hybrids could mean that speciation occurred only during recent evolution. References I~2oulischer, L.: Concept of cellular clonal evolution of karyotypcs applied to evolution of species. Acta Zool. Path. Antwerp. 48, (1969). Ohno, S. : Sex chromosomes and sex linked genes. _~V[onogr. on Endocrinology, vol. 1. Berlin-tfeideIberg-New York: Springer 1967.
6 270 Kouliseher et al. : Chromosomes of the Offspring of Bongo Sitatunga Taylor, K. M., Taylor, B.K.: The chromosomes of the eland, Taurotragus oryx Pallas. Mammal. Chrom. Newsl. 11, (1970). Wallace, C., Fairall, N. : The chromosomes of the kudu. S. Afr. J. med. Sci. 32, 61 (1967). Wurster, D. It.: Sex chromosome translocations and karyotypes in bovid tribes. Cytogenetics ll, (1972). Wurster, D. It., Benirschke, K. : Chromosome studies in the superfamily Bovoidea. Chromosoma (Berl.) 25, (1968). Wurster, D. H., Benirsehke, K., Noelke, H. : Unusually large sex chromosomes in the sitatunga (Tragelaphus spekei) and the blackbuck (Antilope cervicapra). Chromosoma (Berl.) 211, (1968). Received November 21, 1972 / Accepted by H. Bauer Ready for press November 26, 1972 Dr. L. Koulischer Institut de Morphologie Pathologique All6e des Templiers, 29 bis B-6270 Loverval (Charleroi) Belgium Dr. J. Tijskens, Dr. J. Mortelmans t~oyal Society of Zoology 26 Koningin Astridplein B-2000 Antwerpen Belgium
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