L. E. M. de Boer
Marked Chromosomes Associations in
Catarrhine Monkeys, with a Note on
Chromosome Associations in Other
Primate Groups
Institute ofGenetics,
University of Utrecht,
Utrecht, The Netherlands
Received
10 March
In numerous
In metaphase figures, obtained from cultures ofwhole blood, associations
of the marked chromosomes were found in species of the following
genera : Macaca, Cercocebus, Cercopithecus and Sjmjhalangus.
The different
types of these associations are discussed. A note is given on chromosome
associations found in some species of Prosimii and Platyrrhinae.
1971
studies on the cytogenetics
the past 15 years,
the term “marked
pair of chromosomes,
large satellites
presenting
of the Old War Id monkeys
chromosomes”
a deep secondary
these elements
are present
a single pair occurs per cell, the homologues
In the Cercopithecidae
can be distinguished
&l-3),
a
in every metaphase
figure.
Since only
distinct
types of marked
chromosomes
with the constriction
in the short arm [cf. Figure
subfamily
Papinae,
1966a.)
and
subspecies
genus Erythrocebus;
The constant
diploid
usually with
Macaca, Cercocebus and Pa&o;
Subterminal, with the constriction
species
connected
can be easily recognized.
three morphologically
(All species of the genera
Chiarelli,
during
indicating
:
Submetacentric (arm ratio
1 (b)]
constriction,
that appeared
a concept,
In all species of the families Cercopithe-
in one of the chromosome-arms.
cidae and Hylobatidae
has become
Chiarelli,
morphology
chromosome
in the long arm [Figure
of Cercopithecus subfamily
Almost metacentric [Figure
including
the
1963.)
of the marked
number
1 (a)] (In the numerous
Cercopithecinae,
chromosomes
in this group,
in which
the
varies from 54 to 72, is striking.
l(c)]
(subfamily
Colobinae,
as far as karyotypes
known : several species of Colobus, Presbytis and Nasalis larvatus Wurmbs,
are
182 1).
of
According
to Chiarelli
( 19666)) who measured a number of marked chromosomes
various Old World monkeys, the marked arm in the three types is of about the same size,
whereas
the not-marked
In the gibbons
arm varies in length between
(family
All investigated
Hylobatidae)
species
the different
of Hylobates have matecentric
approximately
the same length as those in the Colobinae
1 (c)l*
The
type,
second
marked
chromosome
(Chiarelli,
19666).
marked
chromosomes,
(Chiarelli,
1 9666)
of Symphalangus syndactylus, is not always
comparable
to that
seen
in the other
As Figure 1 (c) shows, they are acrocentric,
on their short arms.
animal
that
groups.
two types can be distinguished:
This is the only acrocentric
For these reasons they can be considered
ence is that the satellites are much smaller.
bearing
pair in the karyotype
(2n = 50), and there are no other chromosomes
as marked
with secondary
chromosomes.
(In our material
regarded
catarrhine
there are two notes on the existence
monkeys.
small satellites
of this small
constrictions.
The only differ-
of Symphalangus syndactylus
of associations
The first observation
as a
monkeys
there is some doubt about the length of the short arms; it varies markedly
ing on the grade of spiralization of the achromatic
region.)
In the literature
of
[Figure
between
was made by Klinger
chromosomes
of catarrhine
in metaphase
plates of SymphaEangus syndactylus (“. . . both partners
Journal of Human Evolution (1972) 1, 834%
bear satellites
dependmarked
(1963)
on the
84
L.
E.
M.
BOER
DE
Figure 1. Schematic representation of marked chromosome types
in the families Cercopithecidae (a,
b, c) and Hylobatidae (d, e), (a)
Cercopithecus species; (b) Genera
Macaca, Cercocebusand Pa+;
(c)
Subfamily Colobinae;
(d) Genus
zFob;;ur;
(e) Ajvnphalangus
~yn-
ib)
(a)
short arms and some metaphase
aridez-Donoso
(1970)
In metaphase
number
recorded
figures,
of Old World
observed
in the
(Raffles,
1821),
182 1).
obtained
from
monkeys,
following
(Sykes,
species:
1831),
in question
in the metaphase
however,
blood
(Pocock,
(de Boer,
(Raffles,
fascicularis
frequency
Some association
l-parts
whereas
Fern-
1907)
1971)
chromosomes
182 I),
of a
were often
M.
nemestrina
(Schreeber,
t&pin
and Symphalangus
was found in Symphalangw
plates showed a characteristic
1774))
syndactylus
syndactylus;
configuration
of the two
7,8,9).
are no longer
by thread-like
recognizable
and
the chromosomes
seem
to be
structures.
types in Cercocebus torquatus are shown in Plate
seems clear that the associations
the satellites;
of whole
1792)) Cercopithecus
C. hamlyni
(e)
When these elements lie independently
plate they bear small, but clearly visible satellites. If they are associated
the satellites
connected
(Plate
association”.),
of the marked
Macaca
The highest associative
satellite
(d)
in Macaca fascicularis.
cultures
(Kerr,
more than 40 o/oof 95 metaphase
chromosomes
showed
associations
C ercocebus torquatw
C. mitis albogularis
(Raffles,
figures
the phenomenon
(cl
are formed
though less frequently,
by the achromatic
1 (parts
1, 2, 3).
regions rather
than
It
by
the same types were found also in Macaca fascicularis
and M. nemestrina.
Association
between
the acrocentric
type of marked
(parts 4, 5, 6) (Cercopithz cus talapoin).
achromatic
regions.
A similar
In all species considered
(none of which satellited),
situation
bearing
acrocentric
(Chimpanzee
was found in C. mitis albogularis
chromosomes
no other associations
between
are found,
in associations.
is in agreement
chromosomes
between
homologous
chromosomes
forming
eight pairs, Orang-utan
Mutton & Lang, 1963).
The observation that the associations
not on the satellites,
were involved
not-homologous
apes, where no marked
chromosomes
six pairs, Gorilla
on the
and C. hamlyni.
by the presence of many acrocentrics
were found. In this way, contrary to the
we are always dealing with associations
In the anthropoid
are shown in Plate 1
species, characterized
in man, where associations
our material,
parts.
situation
only the marked
Even in the three Cercopithecw
chromosomes
Again it is clear that they are concentrated
are concentrated
with the experiences
occur,
associations
ten pairs)
also exist, in
chromosome
several satellite-
of the human
(Hamerton,
on the achromatic
of Van Hemel
type
Klinger,
regions, and
( 197 1) for human
associations.
Whether the thread-like structures in Symphalangus syndactylus associations
are comparable
to those sometimes found in man (Zang & Back, 1968) is not certain.
The physiological function of the achromatic region in the marked chromosomes might
lie in the organization of the nucleolus during interphase, but this has never been proved.
Nevertheless,
the occurrence of asssociations between these regions fortifies this idea, the
of
metaphasth
Plate
1. Details
figures (obtained
from blood cultures)
showing
associations
between
three
different
types of marked
chromosomes
of
catarrhine
monkeys
(4000X)
: l-3 : Cercocebus torquatu.\
(Kerr,
179’2) ; 4-6 : Cercopithecta
tnlapoirr
(Schreeber,
1774) ; 7-9:
\ymfm!slr/r
(Raffles,
,S)mphnlnn,qrt.v
1821,.
MARKED
CHROMOSOMES
more so since one comes across the same situation
At any rate,
chromosomes
19666;
the evidence
suggests,
Egozcue
& Vilarasau
least the achromatic
chromosome
nothing
is known
should approach
The
factors,
of associations
in future research
The
note
Grant
No. 82-34
(Z.W.O.).
disposal she monkeys
Thanks
on primate
parts
metaphase
types of marked
(Chiarelli,
homologization
of at
evolution
of the
Since
of these chromosomes,
1969).
This
one
should
project,
and the
be taken
into
supported
financially
by
of Pure
Re-
for the Advancement
Health,
on many
1970)
associations.
(Artis Zoological
for Public
is dependent
(Nankin,
evidence
chromosome
Organization
Institute
plates
culture
on a broader
to Dr E. F. Jacobi
Gardens,
Bilthoven),
Amsterdam)
and to
who placed
at our
used in this study.
are due to Dr J.
0.
Van
J. M. Van Brink and Dr B. Kiauta
Mr D. Smit
1961).
a few simple translocations.
on the other
St Zang,
of the Netherlands
(National
85
(Ohno,
homologization
also a functional
of the lymphocyte
is the first report
I am greatly obliged
Dr B. C. Kruyt
material
to trace the morphological
in human
viz. the duration
of the slides (Back
search
MONKEYS
very carefully.
consideration
present
morphological
1) by postulating
on the information
the problem
frequency
pre-treatment
types (Figure
in the human
1967),
It is attractive
CATARRHINE
in species with different
to the
de Ecozcue,
regions.
marked
technical
on the associations
in addition
OF
(Utrecht)
Hemel,
for discussions
(all of this Institute)
made the illustrations
on the problem
for reading
and to Dr
the manuscript.
in this paper.
Addendum. While this paper was in press, additional data were obtained on chromosome association
in some prosimians
and platyrrhines.
In metaphase
plates of G&go crussicaudutus (2n = 62), two medium sized acrocentric
chromosomes were found to associate very frequently.
Since the karyotype of this animal contains a large
number of acrocentrics,
it is not sure if the two chromosomes
in question are homologues.
No
further elements seem to associate regularly.
A sirnilar situation
is met with in G&go senegulensis, though its karyotype
(2n = 38) differs
essentially from that of the closely related G. crussicaudutus.
The associating elements are approximately equal in length in both species.
Since they are the only medium sized acrocentrics
in the
karyotype of G. senegalensis, they certainly are homologues.
In the third prosimian investigated,
Perodicticus potto (2n = 62, karyotype very similar to that of
G&go crussicaudutus), more complex associations
were found.
They consist of three or four acrocentrics of at least two pairs.
Finally,
there is some evidence that the marked chromosomes
of platyrrhines
are involved in
associations
(based on material of Aotes trivirgutus, Saimiri sciureus and LEontocebus rosulia).
Unlike
the situation
in catarrhines,
where the marked chromosomes
seem to be the only associating
elements, in platyrrhines
other associations
of acrocentrics
were found together with those of the
marked chromosomes.
References
Bac:k, E. & Zang, K. D. (1969). Q uantitative studies on the arrangement of human metaphase chromosomes. II. Influence of the preparation technique on the association pattern of the acrocentric chromosomes. Cyrogenetics 8, 304-314.
de Boer L. E. M. (1971).
Cytology of the Cercopithecidae
with special reference to the karyotype of
Cercopithecus humlyni (Pocock, 1907). Proceedings of the Third International Congress of Primatology (in press).
Chiarelli, B. (1963). Primi resultati di recerche di genetica e cariologia comparata in primati e loro interesse
evolutivo. Rivistu di Antropologicu 50, 87-124.
Chiarelli, B. (196&z). Caryology and taxonomy of the Catarrhine monkeys. American Journal of Physical
Anthropology 24, 155-170.
Chiarelli, B. (19666). Marked chromosome in Catarrhine monkeys. Folia primutologicu 4, 74-80.
Egozcue, J. & Vilarasau de Egozcue, M. (1967). The marked cl~romosomrs of primates:
Origin and
evolutionary significance.
In (D. Starck, R. Schneider & H. .J. Kuhn, Eds).
Neue Ergebnirse rlr,Primutologie Stuttgart:
G. Fischer.
Fernandez-Donoso, R., Lindsten, J. & Norrby, E. (1970). The chromosomes of the (1ynomologus macqur
(Macaca jkicularis)
. Zfereditas 65, 269-276.
Hamerton, J. L., Klinger, H. P., Mutton, D. E. & Lang, E. M. (1963). The somatic chromosomes of tlw
Hominoidea. Qtogenetics 2, 240-263.
van Hemel, J. 0. (1971). Studies on human chromosome associations. Thesis. University of Utrccht.
Klinger, H. P. (1963). The somatic chromosomes of some primates (Tupaia glis, Tarsius bancanus, Cercoccbrrs
aterrimus, Symphalangus syndactyius). Qtogenetics 2, 140-151.
Nankin, H. R. (1970). In vitro alteration of satellite association and nucleolar persistence in mitotic human
lymphocytes. cylogenetics 9,42 -5 1.
Ohno, S., Trujillo, J. M., Kaplan, W. D. & Kinosita, R. (1961). Nucleolus organizers in the causation of
chromosomal anomalies in man. Lancet 65, 123-126.
Zang, K. D. & Back, E. (1968). Quantitative studies on the arrangement of human metaphase chromosomes.
I. Individual features in the association pattern of the acrocentric chromosomes of normal males and
females. Cytogenetics 71, 455-470.