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Chromosomes of lemuriformes. I. A chromosome complement of Lepilemur mustelinus (I. Geoffroy 1851)

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Chromosomes of Lemuriformes
I. A CHROMOSOME COMPLEMENT OF LEPlLEMUR MUSTELlNUS
(I. GEOFFROY 1851)
JOHN BUETTNER-JANUSCH,l ANDREW E. HAMILTON 1 AND
JAN A. BERGERON
Departments of A n a t o m y , Zoology, and Anthropology, Duke University.
D u r h a m , North Carolina 2771 0
KEY WORDS Chromosomal satellites
type . Lemur chromosomes.
.
Cytogenetics . Karyo-
ABSTRACT
The diploid chromosome number of two specimens of Lepilemur
m u s t e l i n u s (I. Geoffroy 1851) is 2 N = 20. All of the chromosomes, except the Y
chromosome, are metacentric or submetacentric; the Y chromosome is acrocentric and is the shortest chromosome in the complement. Satellites on autosoma1 pair 5 provide marked chromosomes for the animals studied and may be
a marked pair for the species.
The chromosomes of primates are significant data in the study of phylogenetic
relationships among various living species
in this mammalian order. Each karyotype
enables us to increase the number of statements we can make about the probable
direction of karyotype evolution in the
primates (Bender and Chu, '63; Rumpler
and Albignac, '70). The data available in
the literature on primate chromosomes
support the view that variation in chromosome complements is one of the mechanisms by which differentiation of populations into species occurs. Rearrangements
in chromosome complements may eventually produce a reproductive barrier between two segments of what had been a
single species.
The purpose of this report is to describe
the chromosome complement of two male
individuals of Lepilemur mustelinus (fig.
l), a small nocturnal member of the family
Lemuridae. The diploid number we report,
2N = 20, is at the lower end of the range
of diploid numbers reported by Rumpler
('72). Rumpler reports diploid numbers
ranging from 2 N = 2 0 to 2 N = 3 8 from a
number of specimens of Lepilemur m u s telinus (Rumpler, '72 and personal communication).
The variety of diploid numbers and karotypes found within what is considered a
single mammalian species is a remarkable
example of intraspecific variation and imAM. J. PHYS. ANTHROP., 39: 1-6.
plies that we must consider the systematics
of that species, so we shall make a few
remarks here about the systematics of
Lepilemur. In 1960 Petter and PetterRousseaux revised the nomenclature and
systematics of the genus. They concluded
that the number of species that ForsythMajor (1894) constructed was not valid.
Instead they defined one species, LepiLem u r mustelinus, with two subspecies, L.
m. mustelinus and L. m . ruficaudatus. A
discussion of the confusion produced by
Forsyth-Major is to be found in Petter and
Petter-Rousseaux ('60) and in Schwarz
('31). As we said, variation in diploid numbers and karyotypes of the sort reported
by Rumpler is unusual for a single mammalian species, and it is possible that
Forsyth-Major recognized valid specific
distinctions despite the internal inconsistencies in his work noted by Schwarz ('31).
MATERIALS AND METHODS
Two male Lepilemur mustelinus (probably L. m. mustelinus, fig. 1) captured in
Madagascar were sent to the Duke University Primate Facility in October 1969.
Blood samples were taken immediately
upon arrival. Both animals appeared to be
in good health, and one of the two is still
1 Present address. Department of Anthropology, New
York University, New York, New York 10003.
1
2
BUETTNER-JANUSCH, HAMILTON AND BERGERON
Fig. 1
Lepilemur mustelinus, male (animal 1202, Duke University Primate Facility).
3
CHROMOSOMES OF LEPILEM U R M U S T E L I N U S
alive and well, but the other died shortly
after arrival for reasons not determined
upon autopsy.
Standard techniques for culturing leukocytes were used (Moorhead et al., '60).
The cultures were prepared with TC Chromosome Microtest reagents (Difco). Slides
were made by placing three or four drops
of the suspension of cells on clean, dry
microscope slides. The fixative was ignited
and the slides allowed to dry (Moorhead
et al., '60). Slides were stained for 30 minutes in a 2% Giemsa solution in phosphate
buffer at pH 6.4, dried, and mounted in
Permount (Fisher). Photomicrographs at
a magnification of 720 X were taken on a
Zeiss research microscope equipped with
a Wild Photo-automat. Kodak high-contrast copy firm was used.
Measurements were made on well-spread
metaphase chromosomes with clearly defined centromeres. The figures were photographed and enlarged to a magnification
of 3450 X , and the chromosomes were
measured with calipers. Both arms of each
chromosome were measured in 23 spreads.
These results were verified by measuring
the chromosomes visually at a magnification of 1000 X with a calibrated eyepiece.
Chromosomes were classified as metacentric, submetacentric (subtelocentric), or
acrocentric according to the definitions of
Bender and Chu ('63).
RESULTS AND DISCUSSION
We counted 42 cells, 40 of which had a
chromosome number of 20 (table 1). The
autosomes were arranged in order of decreasing size and the sex chromosomes
determined by elimination (fig. 2). The
mean lengths of the autosomes in the
metaphase figures vary between 2.8 pm
and 10.5 pm. The mean arm ratios of the
autosomes vary from 1.36 to 4.26 (table 2).
The longest chromosomes in the compleTABLE I
Diploid chromosome n u m b e r s of two m a l e
Lepilemur mustelinus
Diploid n u m b e r
Animal
Cells
counted
19
20
21
1
20
0
20
0
2
22
1
20
1
ment, pairs 1, 2, and 3 (fig. 2), are not
easy to distinguish from one another. They
are similar in length and have similar arm
ratios; the ratios for pairs 1 and 2 fall
within the range defined as submetacentric; the ratio for pair 3 is in the metacentric range. Pairs 4 and 6 are submetacentric and are easily distinguished from
each other by length and arm ratios (table 2).
The chromosomes of pair 5, which are
metacentric, are the most distinctive in
the karyotype. In the distal third of the
short arm, each has a conspicuous secondary constriction forming a characteristic satellite that marks the chromosome
(fig. 2). Pairs 7, 8, and 9 (table 2) are the
shortest autosomes, from one-third to onehalf the length of any one of the first six
pairs. Pair 7 is submetacentric; pairs 8
and 9 are metacentric.
The X chromosome, 3.29 0.17 pm in
length, is submetacentric. The Y chromosome is the shortest in the karyotype,
0.7220.09 pm, and it represents only
1.3% of the total complement length. Its
minuscule short arms make it the only
acrocentric member of the karyotype ( r =
12.06).
The fundamental number, NF (Matthey,
'49), calculated by assigning a value of
two to metacentric and submetacentric
autosomes and one to acrocentric and sex
chromosomes, is NF = 38. Rumpler ('72)
reports NF ranging from 36 to 42 among
the specimens of Lepilemur he examined.
The values of NF for other members of the
Lemurinae, the genera Hapalemur and
Lemur, range from 62 to 70, outside the
range of values reported for Lepilemur.
When more results are available, the fundamental numbers should enable us to
interpret the direction of evolution of the
karyotypes of Lemurinae, if karyotype
evolution proceeds primarily by the Robertsonian mechanism of centric fusion.
The two animals whose karyotypes are
reported here were captured in their native habitat and probably represent normal
members of the species. However, karyotypes of only two individuals of a population must be considered tentative, especially for a species that appears to have
so much karyotypic variation. The diploid
number for Lepilemur mustelinus, 2N = 20,
is the smallest reported for members of
*
4
BUETTNER-JANUSCH, HAMILTON AND BERGERON
Fig. 2 Karyotype and chromosome spread from male Lepilemur mustelinus. Arrows in chromosome spread indicate pair 5, the two chromosomes with secondary constrictions and satellites.
5
CHROMOSOMES OF L E P I L E M U R M U S T E L I N U S
TABLE 2
Morphology of the chromosomes of two male Lepilemur mustelinus
Relative length
2
Chromosome
1
2
3
4
5
6
7
8
9
X
Y
Mean
S.E.
0.155
0.147
0.135
0.124
0.122
0.093
0.057
0.055
0.051
0.062
0.013
0.001
0.003
0.001
0.003
<0.001
< 0.001
< 0.001
0.002
0.001
0.001
0.002
5
1
Ratio ( r ) 3
Mean
S.E.
2.29
2.16
1.95
3.78
1.76
4.26
2.01
1.36
1.69
2.84
12.06
0.05
0.06
0.04
0.10
0.04
0.30
0.07
0.07
0.08
0.20
0.30
5
Morphological
classification 4
SM
SM
M-SM
SM
M
SM
SM
M
M
SM
A
Calculations are based on measurements of 23 metaphase spreads.
Relative length is the length of the chromosome as a proportion of the length of the haploid complement including the X chromosome.
3 r = Z/s where 1 is mean length of the long a r m and s is mean length of the short arm.
4 M, metacentric, r = 1.0-1.9; SM, submetacentric (subteloceutric), r =2.0-4.9;
A, acrocentric, r =
5.0-m (Bender and Chu, ' 6 3 ) .
5 S.E., standard error of the mean.
1
2
the order Primates. The chromosome pair
(pair 5 ) that characteristically has satellites may be a marked chromosome that
will enable us to evaluate similarities and
differences among karyotypes from individuals of the genus Lepilemur.
Because of the intraspecific or intrageneric variation in diploid numbers, NF,
and karyotypes reported for Lepilemur
(Rumpler, '72), comparisons of many individuals of the genus are desirable and
necessary. Techniques of chromosome
banding (Finaz and de Grouchy, '71; Lomholt and Mohr, '71; Utakoji, '72) will certainly be useful.
ACKNOWLEDGMENTS
We wish to thank M. Georges Ramanantsoavina, Ingenieur en Chef des Eaux
et For& de la Direction des Eaux et
For& et de l a Conservation des Sols, Republique Malgache, for the two animals
studied. We are particularly grateful to
Dr. Yves Rumpler of the Laboratoire dHistologie, Embryologie-Cytogenetique, Ecole
Nationale de Medecine, Universite de
Madagascar, €or his advice and assistance.
Mr. Victor Lukas and Mr. Richard Hackel
provided invaluable advice with photographic techniques. The work was supported in part by NIH GM16722 (RCDA),
NIH RR00388, and NSF GS2508 (BuettnerJanusch); by a n NIMH training grant to
the Department of Sociology-Anthropology
(Hamilton); and by Duke Endowment research funds (Bergeron).
LITERATURE CITED
Bender, M. A , , and E. H. Y . Chu 1963 The
chromosomes of primates. In: Evolutionary and
Genetic Biology of Primates. Vol. 1. J. BuettnerJanusch, ed. Academic Press, New York, pp.
261-31 0.
Finaz, C., and J. de Grouchy 1971 Le caryotype humain aprks traitement par l'a-chymotrypsine. Ann. Genet., 1 4 : 309-311.
Forsyth-Major, C. I. 1894 Diagnosis of a new
species of the genus Lepidolemur. Ann. Mag.
Nat. Hist., 6 (13): 211-219.
Lomholt, B., and J. Mohr 1971 H u m a n karyotyping by heat-giemsa staining a n d comparison
with fluorochrome techniques. Nature New
Biology, 234: 109-110.
Matthey, R. 1949 Les Chromosomes des Vertebres. F. Rouge, Lausanne.
Moorhead, P. S., P. C. Nowell, W. J. Mellman,
D. M. Battips a n d D. A. Hungerford 1960
Chromosome preparations of leukocytes cultured from h u m a n peripheral blood. Exper.
Cell Res., 20. 613416.
Petter, J. J., and A. Petter-Rousseaux 1960 Remarques sur la systematique du genre Lepilemur. Mammalia, 24: 76-86.
Rumpler, Y. In press Cytogenetic contributions
to a new classification of lemurs. Research Semin a r on Prosimian Biology, 1972, London.
Rumpler, Y., and R. Albignac 1970 Evolution
chromosomique des lemuriens malgaches. Ann.
Univ. Madagascar, 12-13: 123-131.
Schwarz, E. 1931 A revision of the genera and
species of Madagascar Lemuridae. Proc. Zool.
SOC.London: 399-428.
Utakoji, T. 1972 Differential staining patterns
of h u m a n chromosomes treated with potassium
permanganate. Nature, 239: 168-170.
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