Robertsonian chromosome polymorphism in the Arabian oryx (Ovyx

-
Cytogenetics and Cell Genetics
Separatum
~dzor-in-chief:H.P.Klinger, Bronx, N.Y.
Publisher: S. Karger AG, Basel
Printed in Switzerland
1990 S. Karger AG. Basel
0301-0171;90~05Jl-0161S 1.75.0
Cytogenet Cell Genet 54:161-163 (1990)
Robertsonian chromosome polymorphism in the Arabian oryx
(Ovyx leucoryx)
E.P. Cribiu, ' J. F. Asmondt., ' V. Durand, ' A. Greth,' a n d S. Anagariyah2
' Institut National de la Recherche Agronomique, Centre de Recherche de Jouy-en-Josas, Laboratoire de CytogCnetique, Jouy-en-Josas (France), and
'National Wildlife Research Center, TaYf (Saudi Arabia)
Abstract. A Robertsonian translocation was found in a herd of
Arabian oryx (Oryx leucoryx). The translocated chromosome,
when analyzed by G-banding, seemed to involve the fusion of
chromosomes 17 and 19. The results of C-banding suggested that
the fused chromosome is dicentric. The translocation was traced
back through two generations and occurred in a total of 8 of 62
animals in the herd.
The Arabian oryx, 0ry.u 1eucory.u (Pallas, 1777),belongs to the
Hippotraginae tribe. The Oryx genus also includes, according to
Honacki (1982), two other species: the scimitar-horned oryx, 0 .
dammall (Crestzschmar, 1826), and the gemsbok, 0 . gazella
(Linne, 1758).
The karyotypes of these three species were established by con.entional staining (Newnham and Davidson, 1967; Hsu and Benirschke, 1968; Wurster and Benirschke, 1968; Wurster, 1972)
and, later, by application of GTG- and CBG-banding (Hsu and
Benirschke, 1977; Buckland and Evans, 1978a, b; Maia et al.,
1987;Cribiuet al., 1989). Karyotypes aresimilar and seem to differ
only by one centric fusion; the gemsbok has 56 chromosomes,
while the scimitar-horned and Arabian oryx have 58.
The present communication describes a centric fusion (Robertsonian translocation) in the Arabian oryx.
in the late 1950s and early 1960s. Until now, this population has remained
completely isolated, without any introduction of foreign animals, and.
therefore, constitutes a line different from the American line.
Materials and methods
Animals
The 54 Arabian oryx studied are held at the National Wildlife Research
Center (Taif, Saudi Arabia), to be reintrodxed into the wild. Thiscaptive population originated from the Riyadh Zoo (Saudi Arabia), the San Diego Zoo
(USA), and various Arabian Gulf countries (Abu-Zinada et al., 1988).
During the 1970s, the Arabian oryx became extinct in the wild due to degradation of the habitat and overhunting. The oryx was saved from total extinction by "Operation Oryx" (the capture of wild animals for breeding in captivity),
held in 1962. Nineindividuals, the founders oftheso-called "World Herd," were
transported to the United States and successfully bred (Grimwood, 1988;
Homan, 1988; Mace, 1988).
A sample of eight animals from the Shaumari Wildlife Reserve (Jordan) was
also studied. The Shaumari herd started with eight animals from the United
States (four males and four females) and three animals from Qatar (one male
and two females) (Jones, 1988). The Qatar herd originated from a number of
capture expeditions south of Rub Al Khali in Saudi Arabia and western Oman
Received 14 November 1989; accepted 2 April 1990.
Request reprints from Dr. Edmond P. Cribiu, Institut National de la Recherche Agronomique, Centre de Recherche de Jouy-en-Josas, Laboratoire de Cytoginitique,
78352 Jouy-en-Josas Cedex (France).
Cytogenetic merhods
Chromosome preparations of 26 males and 36 females were made from
peripheral blood lymphocytes by the standard whole-blood technique (de
Grouchy et al., 1964) and were G-banded using a modification of Seabright's
(1971) method. C-bands were stained by the barium hydroxide method of
Sumner (1972).
Karyotypes were prepared according to the standardized G-band karyotype
of the goat (Ford et al., 1980; Cribiu and Matejka, 1987).
Results
In 1989, the oryx herd at Tai'fincluded 62 animals (26 males and
36 females); of these, eight (four males and four females) had been
imported from Jordan to be reintroduced in the Mahazat Al Sayd
protected area.
Three different chromosome numbers were observed among
this herd. Fifty-four animals (25 males and 29 females) had a diploid number of 58. All autosomal pairs except the largest, which
was submetacentric, were acrocentric. The X chromosome was the
largest acrocentric and displayed a minute, but prominent, short
arm. The Y was a small acrocentric.
Seven animals (one male and six females) appeared to have 57
chromosomes, including two submetacentrics, 54 acrocentrics,
and one mid-sized metacentric chromosome. G-banding showed
that the short arms of the metacentric chromosome corresponded
to chromosome 19 and the long arms to chromosome 17 (Fig. 1).
C-banding revealed two heterochromatin blocks in the pericentromeric region (Fig. 2).
One animal had a chromosome number of 56. The karyotype of
this female exhibited two mid-sized metacentric chromosomes.
Among the eight animals from the Jordan herd, two were translocation carriers, and one, a female, was a homozygous carrier of
the translocation, suggesting that both parents were carriers and
that the dam, which came from Qatar, was at least heterozygous.
Cytogenetics and Cell Genetics
Separatum
~dGor-in-chief:H.P. Klinger, Bronx, N.Y.
Publisher: S. Karger AG, Basel
Printed in Switzerland
$ 1990 S. Karger AG. Basel
03014171~9O1O544016IS 2.75.0
Cytogenet Cell Genet 54:161-163 (1990)
Robertsonian chromosome polymorphism in the Arabian oryx
(Ovyx leucoryx)
E.P. Cribiu, J. F. Asmondk,' V. Durand, ' A. Greth,' a n d S. Anagariyah2
' Institut National de la Recherche Agronomique, Centre de Recherche de Jouy-en-Josas, Laboratoire de Cytoginetique, Jouy-en-Josas (France), and
National Wildlife Research Center, Ta'if (Saudi Arabia)
Abstract. A Robertsonian translocation was found in a herd of
Arabian oryx (Oryx leucory.~).The translocated chromosome,
when analyzed by G-banding, seemed to involve the fusion of
chromosomes 17 and 19. The results of C-banding suggested that
the fused chromosome is dicentric. The translocation was traced
back through two generations and occurred in a total of 8 of 62
animals in the herd.
The Arabian oryx, Oryx leucorys (Pallas, 1777), belongs to the
Hippotraginae tribe. The Oryx genus also includes, according to
Honacki (1982), two other species: the scimitar-horned oryx, 0.
dammah (Crestzschmar, 1826), and the gemsbok, 0. gazella
(Linne, 1758).
The karyotypes of these three species were established by con.entional staining (Newnham and Davidson, 1967; Hsu and Benirschke, 1968; Wurster and Benirschke, 1968; Wurster, 1972)
and, later, by application of GTG- and CBG-banding (Hsu and
Benirschke, 1977; Buckland and Evans, 1978a, b; Maia et al.,
1987;Cribiu et al., 1989). Karyotypes are similar and seem to differ
only by one centric fusion; the gemsbok has 56 chromosomes,
while the scimitar-horned and Arabian oryx have 58.
The present communication describes a centric fusion (Robertsonian translocation) in the Arabian oryx.
in the late 1950s and early 1960s. Until now, this population has remained
completely isolated, without any introduction of foreign animals, and.
therefore, constitutes a line different from the American line.
Materials and methods
Animals
The 54 Arabian oryx studied are held at the National Wildlife Research
Center (Tail, Saudi Arabia), to be reintrodnced into the wild. Thiscaptive population originated from the Riyadh Zoo (Saudi Arabia), the San Diego Zoo
(USA), and various Arabian Gulf countries (Abu-Zinada et al., 1988).
During the 1970s, the Arabian oryx became extinct in the wild due to degradation of the habitat and overhunting. The oryx was saved from total extinction by "Operation Oryx" (the capture of wild animals for breeding in captivity),
held in 1962. Nine individuals, the founders of theso-called "World Herd," were
transported to the United States and successfully bred (Grimwood, 1988;
Homan, 1988; Mace, 1988).
A sample of eight animals from the Shaumari Wildlife Reserve (Jordan) was
also studied. The Shaumari herd started with eight animals from the United
States (four males and four females) and three animals from Qatar (one male
and two females) (Jones, 1988). The Qatar herd originated from a number of
capture expeditions south of Rub Al Khall in Saudi Arabia and western Oman
Received 14 November 1989; accepted 2 April 1990.
Request reprints from Dr. Edmond P. Cribiu, Institut National de la Recherche Agronomique, Centre de Recherche de Jouy-en-Josas, Laboratoire de CytogWtique.
78352 Jouy-en-Josas Cidex(France).
~
Cytogenetic mefhods
Chromosome preparations of 26 males and 36 females were made from
peripheral blood lymphocytes by the standard whole-blood technique (de
Grouchy et al., 1964) and were G-banded using a modificat~onof Seabright's
(1971) method. C-bands were stained by the barium hydroxide method of
Sumner (1972).
Karyotypes were prepared according to the standardized G-band karyotype
of the goat (Ford et al., 1980; Cribiu and Matejka, 1987).
Results
In 1989, the oryx herd at Tai'fincluded 62 animals (26 males and
36 females); of these, eight (four males and four females) had been
imported from Jordan to be reintroduced in the Mahazat Al Sayd
protected area.
Three different chromosome numbers were observed among
this herd. Fifty-four animals (25 males and 29 females) had a diploid number of 58. All autosomal pairs except the largest, which
was submetacentric, were acrocentric. The X chromosome was the
largest acrocentric and displayed a minute, but prominent, short
am]. The Y was a small acrocentric.
Seven animals (one male and six females) appeared to have 57
chromosomes, including two submetacentrics, 54 acrocentrics,
and one mid-sized metacentric chromosome. G-banding showed
that the short arms of the metacentric chromosome corresponded
to chromosome 19 and the long arms to chromosome 17 (Fig. 1).
C-banding revealed two heterochromatin blocks in the pericentromeric region (Fig. 2).
One animal had a chromosome number of 56. The karyotype of
this female exhibited two mid-sized metacentric chromosomes.
Among the eight animals from the Jordan herd, two were translocation carriers, and one, a female, was a homozygous carrier of
the translocation, suggesting that both parents were carriers and
that the dam, which came from Qatar, was at least heterozygous.
Fig. 1. G-banded karyotype from a female oryx with the 17;19 Robertsonian
translocation.
Fig. 2. CBG-banded metaphase showing constitutive heterochromatin as
two blocks in the 17;19 translocation (large arrow).
Discussion
Fig. 3. Pedigree showing the inheritance of the 17;19 Robertsonian translocation. Half-shaded symbols indicate presence of heterozygote for the 17;19
translocation, N indicates the translocation was not observed, and ? indicates
the animal was unknown.
Pedigrees involving individuals carrying the 17;19 translocation were drawn from'the Arabian Oryx Studbook (Dolan, 1988)
(Fig. 3). It was not possible to obtain accurate information regarding the transmission of the 17;19 translocation after the second
generation.
The metacentric chromosome in this herd results from the fusion of two acrocentric chromosomes, 17 and 19, and therefore can
be called a centric fusion or Robertsonian translocation (Robertson, 1916). In most of Bovoidea and, in particular, in the Arabian
oryx, where C-bands representing constitutive heterochromatin
are localized exclusively in the pericentromeric region of acrocentric autosomes, Robertsonian translocations involving two
heterochromatin blocks could be considered dicentrics (Beriand et
al., 1988; Cribiu et al., 1989). Dicentric and monocentric Robertsonian translocations are the most frequent types of chromosomal
abnormality reported in domestic species of Bovidae, including
cattle, sheep, and goats (Eldridge, 1985).
Based on the assumption that structural chromosome anomalies, unlike recurrent genetic mutations, are unique events (White,
1968), the 17;19 translocation appears to be transmitted as a Mendelian codominant trait. The origin of this Robertsonian translocation is theoretically traceable. Since the Qatar herd had been
reproductively isolated since its beginning, one member of the original breeding stock, captured in the Rub Al Khali, must have
been a carrier of the translocation. The origin of the translocation
in the Saudi herd is more uncertain, since this population is more
heterogeneous and is constituted of animals shipped from the
United States and neighboring Arabian countries; the introduction of animals from Qatar could not be excluded. A cytogenetic
study involving the oryx derived from the San Diego herd would
show whether the translocation also exists in this line. The presence of the 17;19 translocation in both the Qatar and American
.
,.
163
R t h e r t s o n i j n chromosome polymorphism in Oryx
lines would suggest that the translocation originated prior to the
constitution of these two lines and that it existed in the wild before
the herd was threatened with extinction.
In most of the species of the superfamily Bovoidae that have
e e n studied cytogenetically, the preservation of the fundamental
(Matthey, 1954) and the conservation of chromosome
banding-pattern homology between chromosome arms of these
species provide evidence that the primary mechanism of karyotype
.
..
evolution in Bovoidae has been Robertsonian translocations
(Wurster and Benirschke, 1968; Buckland and Evans, 1978a, b).
Acknowledgements
We wish to thank H. R.H. Prince Saud Al-Faisal, Managing Director of the
National Commission for Wildlife Conservation and Development in Saudi
Arabia, Prof. Abdulaziz Abu-Zinada. Secretarv General of the Commission.
.
.~.
and Mr. Jacques Renaud, ~ i r e c t oof
r the ~ a t i o ~wildlife
al
~ e s e a r c hCenter fo;
access to the animals and moral support during our study. The collaboration of
Dr. A. Bouvet (Postdoctoral Research Fellow, INRA) in the preparation of the
manuwript is also gatelully acknowledged.
~
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References
Abu-Zinada AH. Habibi K, Seitre R: The Arabian oryx
programme in Saudi Arabia, in Dixon A, Jones D (cds):
Conxrvation and Biology of the Desert Antelopes.
Proceedings of the 25th Anniversary Celebration of
"Operation Oryx" Symposium, pp 41-46 (Christopher
Helm, London 1988).
Berland HM, Sharma A, Cribiu EP, Darre R, Boscher J,
Popescu CP: A new case of Robertsonian translocation
in cattle. J Hered 79:33-36 (1988).
Buckland RA, Evans HJ: Cytogenetic aspects of phylogeny
in the Bovidae. I. G-banding. Cytogenet Cell Genet
21:42-63 (1978a).
Buckland RA, Evans HJ: Cytogenetic aspects ofphylogeny
in the Bovidae. 11. C-banding. Cytogenet Cell Genet
21:64-71 (1978b).
Cribiu EP, Durand V, AsmodC JF, Greth A, Anagariyah S:
The G- and C-banding karyotype of the Arabian oryx
(Oryx Iacoryx). Annls GCnet 32:200-203 (1989).
C 'iu EP, Matejka M: ldiogram and standardized G-band
karyotype af the goat (Copra hireus). Zuchthygiene
22:l-7 (1987).
Cribiu EP, Marejka M, Darre R, Durand V, Beriand H M ,
Bouvet A: Identification of chromosomes involved in a
Robertsonian translocation in cattle. Genet Sel Evol
21:555-5aO (1989).
Dolan J: Arabian Oryx Studbook: Historical Edition. p 55
(Zoological Society of San Diego, San Diego 1988).
Eldridge FE: Cytogenetics of Livestock, p 298 (Avi Publishing Co, Westport, CT 1985).
Ford CE, Pollock DL,Gustavsson I: Proceedings ofthe first
international conference for the standardisation of
banded karyotypes of domestic animals. Hereditas
92:14>162 (1980).
Grimwood 1: Operation Oryx: The start ofit all, in Dixon D.
Jones D (eds): Conservation and B i o l o ~of rhe D e x n
Antelopes. Proceedings of the 25th Anniversary Celebration of "Operation Oryx" Symposium, pp 1-8
(Christopher Helm, London 1988).
de Grouchy J, Roubin M, Passage E: Microtechnique pour
l'itude des chromosomes humains a partir d'une culturede lymphocytessanguins. AnnlsGinet 7:45 (1964).
Homan WG. The es:ablishment of the World Herd, in
Dixon A, Jones D (eds): Conservation and Biology of
the Desert Antelopes. Proceedings of the 25th Anniversary Celebration of "Operation Oryx" Symposium,
pp 9-13 (Christopher Helm, London 1988).
Honacki J H, Kinman KE, Koeppl J W: Mammal Species of
the World: A Taxonomic and Geographic Reference,
p 694 (Allen Press and Association of Systematics Collections, Lawrence, KS 1982).
Hsu TC, Benirschke K: An Atlas of Mammalian Chromosomes, pp 89-96 (Springer Verlag. BerliniHeidelberg/New York 1968).
Hsu TC, Benirschke K: An Atlas of Mammalian Chromosomes, p 506 (Springer Verlag, BerliniHeidelbergl
New York 1977).
Jones DM. The Arabian oryx in captivity with particular
reference to the herds in Arabia, in Dixon A, Jones D
(eds): Conservation and Biology of the Desert Antelopes. Proceedings ofthe 25th Anniversary Celebration
of "Operation Oryx" Symposium, pp47-57 (Christopher Helm, London 1988).
Mace GM: The genetic status of the Arabian oryx and the
design of cooperative management programmes, in
Dixon A, Jones D (eds): Conservation and Biology of
the Desert Antelopes. Proceedings of the 25th Anniversary Celebration of "Operation Oryx" Symposium,
pp 58-74 (Christopher Helm, London 1988).
Maia V, Pathak S, Blasdel TL. Flanagan F: Karyotypic
analysis of the scimitar-horned oryx. Oryx tao
(Bovidae, Artiodactyla). Rev Brasil Genet 1053-61
(1987).
Matthey R: L'evolution de la formule chromosomiale chez
les vertcbres. Experientia I:%-56 (1954).
Newnham RR, Davidson WM: The karyotype of the South
Arabian oryx, Oryx leueorys (Pallas). Mammal Chrom
News1 8:15 (1967).
Robertson W RB: Chromosome studies. I. Taxonomic relationships shown in the chromosomes ofTettigidae and
Acrididae: V-shaped chromosomes and their significance in Acrididae, Locustidae and Gryllidae: chromosomes and variation. J Morphol27:179-331 (1916).
Seabright M: A rapid banding technique for human chromosomes. Lancet 1i:971-972 (1971).
Sumner AT: A simple technique for demonstrating centromeric heterochromatin. Expl Cell Res 75:304-306
(1972).
Whire M J D: Models of speciation. Science 159:1065-1070
(1968).
Wunter DH: Sex chromosome translocations and karyotypes in bovid tribes. Cytogenetics 11:197-207 (1972).
Wunter DH. Benirschke K: Chromosome studies in the
superfamily Bovoidae. Chromosoma 25152-171 (1968).