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Cytogenetic study of a female Lemur coronatus Lemur macaco hybrid.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 67:123-126 (1985)
Cytogenetic Study of a Female Lemur coronatus x
Lemur macaco Hybrid
S. WARTER AND Y.RUMPLER
Faculte de M@decine,Institut d’Embryologie, 67085 Strasbourg
Ceder, France
KEY WORDS
Lemur macaco
Karyotype, Hybrid, Lemur coronatus,
ABSTRACT Two species of lemur, Lemur rnacaco and Lemur coronatus,
which do not hybridize in the wild, have produced a first, “definite” female
hybrid in captivity. Its karyotype contains one haploid set from each parent.
The analogy with the parental chromosomes is such that the pairing of the
corresponding chromosomal arms leads to the formation of a n open chain and
a ring. The difficulty in obtaining hybrids between these two species could
reflect the existence of a prezygotic barrier. The presence of multivalents, with
probably a negative action on the gametogenesis, would introduce a postzygotic barrier.
Lemurs of the genus Lemur comprise six
species, of which three have produced numerous hybrids in captivity, despite sometimes
considerable morphological differences (Albignac et al., 1971; Saint-Pie, 1970). A possible hybridization between two particularly
distinct species, Lemur coronatus t C 0 ) and
Lemur macaco &MA) had been announced
at Frankfurt am Main Zoo (de Boer, 1973). It
concerned a n animal of unknown origin,
slightly resembling a hybrid between LMA
and Lemur fuEuus (LFU), with a diploid number equal to 45 and a karyotype without
banding, compatible with this hypothesis. We
report here on the karyotype of a second hybrid between LMA and LCO.
MATERIALS AND METHODS
The hybrid, a female, was born in 1983 a t
the Duke Primate Center, of a male LCO and
a female LMA housed together during a reproductive season in a collaborative research
program between the Duke Primate Center
and the University of Strasbourg. Fibroblast
cultures were prepared from skin biopsies,
using our usual technique. The karyotype
was established after R-band (Dutrillaux and
Lejeune, 1971) and C-band (Sumnet., 1972)
marking.
RESULTS
The hybrid, “Galliope” presents a shiny
brown-red pelage like that of a LMA female,
but with the top of the head darker, and a
tail similar to that of LCO. At the head there
0 1985 ALAN R. LISS, INC.
are lateral white tufts, less developed than
in LMA. The muzzle resembles that of LMA,
while the ears are like those of LCO, but
with darker fur.
The karyotype of “Galliope” (Fig. 1) comprises 45 chromosomes: 19 meta- and submetacentrics, 2 large acrocentrics, representing
the X chromosomes, and 22 acrocentrics
smaller than the sex chromosomes. Two of
these acrocentrics do not have homologues
but correspond to the short arms of two submedian chromosomes. Among the submetacentric chromosomes are the two pairs
common to all of the lemurs, but with a slight
difference at the juxtacentromeric region of
the two chromosomes of pair 1. This results
from the importance of the heterochromatin
of the juxtacentromeric region of chromosome 1 from LCO, evidenced by the C-bands.
The karyotype of the hybrid contains one
haploid set of LMA and one of LCO. According to previously established correspondences (Table 1) (Rumpler and Dutrillaux,
1976,1979), it appears that the pairing of the
corresponding chromosomal arms forms two
multivalents. One is a n open chain of 11
chromosomes, terminating with a n acrocentric a t each extremity, the other is a ring
closing back on itself, comprising six chromosomes (Figs. 1,2). The differences in size
Received August 30,1984; accepted January 14, 1985.
124
S . WARTER AND Y.RUMPLER
A
B
Y
Y
4'
h
Fig. 1. A) R-banded karyotype of Lemur macaco x Lemur coronatus hybrid female with a
chain of eleven elements and a ring of six elements ; m = macaco; c = coronatus. B) C-banded
metaphase of the same hybrid. Note the enlarged C-band material in the Lemur coronatus
125
CYTOGENETIC STUDY OF LEMUR HYBRID
TABLE 1. Correspondences between the chromosomes
ofLemur fulvus fulvus (LFU), Lemur macaco fLMA),
Lemur coronatus (LCO), and the hypothetical ancestral
karvotvoe IANC)
ANC
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
X
8 min
LFU
LMA
LC 0
LMA
LCO
1q
10
4q
Iq
5
3
8
6
7
9
10
4
6P
3q
5P
5q
2P
2q
9q
IP
3P
6q
8q
7P
7q
8P
4P
2q
1P
11
12
14
15
13
16
17
19
18
23
20
21
h1:i
7 min
9P
Xshi
12 min
'shi = shift.
between the homologous arms of the chromosomes involved in these multivalents are
due to the presence of a large quantity of
juxtacentromeric heterochromatin on the
LCO chromosomes LC1, LC2, LC3, LC4, LCs,
LC7.
DISCUSSION
Fig. 2. Scheme of the chromosomal evolution of the
lemurs studied. The evolution probably started out with
an ancestral karyotype composed only of acrocentric autosomes and gave rise to the karyotype of Lemur fuluus.
It is a turning point of chromosomal evolution of most
Lemuridae, including Lemur coronatus and Lemur macuco. The numbers indicate the chromosomes involved,
using the nomenclature of the ancestor (ANC) except for
LMA7 and LC04. Open square, Robertsonian translocation; half-solid circle, centromeric shift; H, heterochromatin change.
It is at present more difficult to confirm the
existence of a postzygotic barrier, since this
hybrid has not yet reached sexual maturity.
Given what we know about other lemur hybrids, this hybrid is probably sterile. In fact,
even if large numbers of Robertsonian translocations per se do not appear to disturb gametogenesis in hybrids such as by producing
trivalents, they are associated with important disturbances when they give rise to important meiotic multivalents. The genic
environment likewise plays a significant role
in the development of gametogenesis, such
that chromosomal multivalents have more
serious repercussions in males than in females, in both mice (Gropp and Winking,
1981) and lemurs (Ratomponirina et al.,
1982). It thus appears probable that the existence of two multivalents has a negative
effect on gametogenesis, especially in such
distinct genic backgrounds.
There are considerable morphological and
ethological differences between LMA and
LCO, which indicate a fairly ancient divergence between these two distinct species. In
the north of Madagascar (Foret de la Montagne d'Ambre), LCO is sympatric with another lemur ethologically very similar to
LMA, namely, Lemur fulvus sanfordi No
natural hybridization has ever been observed
between these two species, which often meet
in the same forest strata (Arbelot-Tracqui,
1983). A prezygotic barrier separates the two
species; they remain in their respective
groups, whereas within a species there are
often movements of individuals from one
group to another between breeding seasons
(Arbelot-Tracqui, 1983). The difficulty in obtaining hybrids between LMA and LCO, even
CONCLUSIONS
in captive mixed pairs housed apart from
other animals, also illustrates the prezygotic
Two species of lemurs differing in very imbarrier between the two species.
portant chromosomal rearrangements are
S. WARTER AND Y.RUMPLER
126
capable of hybridization. It seems probable
that such hybrids have reduced fertility. Inasmuch as such hybrids would have gonads
containing germinal cells capable of division,
a study of meiosis in males would be of considerable interest.
ACKNOWLEDGMENTS
The authors thank Duke Primate Center
for the loan of the hybrid, Mr. M. Hauwy for
technical assistance, and Mme. M. Lavaux
for secretarial assistance.
LITERATURE CITED
Albignac, R, Rumpler, Y, and Petter, JJ (1971) L'hybridation des Mmuriens de Madagascar. Mammalia
35: 358-368.
Arbelot-Traqui, V (1983) Etude Qcoethologique de d e w
primates prosimiens: Lemur coronatus Gray et Lemur
fuluus sanfordi Archbold These d'Etat, Universite de
Rennes, 18juillet.
Boer, LEM de (1973) Studies in the cytogenetics of F'rosimians. J. Hum. Evol. 2.271-278.
Dutrillaux, B, and Lejeune, J (1971) Sur une nouvelle
technique dailalyse du caryotype humain. C.R. %antes Acad. Sci. (Paris) 272t2638-2640.
Gropp, A, and Winking, H (1981) Robertsonian translocations: Cytology, meiosis, segregation pattern and biological consequences of heterozygosity. Symp. Zool.
Soc. (Lond)47t141-181.
Ratomponirina, Ch, Andrianivo, J, and Rumpler, Y
(1982)Spermatogenesis in several intra- and interspecific hybrids of the Lemur (Lemur). J. Reprod. Fertil.
66: 717-721.
Rumpler, Y, and Dutrillaux, B (1976) Chromosomal evolution in Malagasy Lemurs. I. Chromosome banding
studies in the genuses Lemur and Microcebus. Cytogenet. Cell Genet. 17t268-281.
Rumpler, Y, and Dutrillaux, B (1979) Chromosomal evolution in Malagasy Lemurs. IV.Chromosome banding
studies in the genuses Phaner, Varecia, Lemur, Micre
cebus and Cheirogaleus. Cytogenet. Cell Genet. 24:
224-232.
Saint-Pie, J (1970) Birth and rearing of a brown-lemur X
red bellied Lemur fuluus x Lemur rubriventer and
breeding of grey gentle lemur Hapalemur griseus at
Asson Zoo. Int. Zoo Yb. IOr71-72.
Sumner, AT (1972) A simple technique for demonstrating centromeric heterochromatin. Expl. Cell Res.
75r304-396.
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