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Constitutive heterochromatin polymorphism in Lagothrix lagothricha cana Cebus apella and Cebus capucinus.

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American Journal of Primatology 4:117-126 (1983)
Constitutive Heterochromatin Polymorphism in Lagothrix
lagothricha cana, Cebus apella, and Cebus capucinus
M. GARCIA1.’, R. MIRO1-’, A.
‘Instituto de Biologiu Fundamental, ‘Department of Biology, Faculty of Medicine, and
“Depurtment of Cell Biology, Faculty of Science, Uniuersidad Autonoma de Barcelona, Spain
We describe the C-bands in the karyotypes of Lagothrix lagothricha CURU,
Cebus apella and Cebus capucinus. The C-banding patterns show both a
high degree of polymorphism as well as the presence of terminal and
interstitial C-bands. Varying amounts of heterochromatin result in dimorphism of some chromosome pairs. The high incidence of chromosome
rearrangements found in the Cebidae may be due to the presence of terminal and interstitial C-bands.
Key words: Lugothrix lagothricha cana, Cebus apella, Cebus capucinus, cytotaxonomy,
constitutive heterochromatin, NOR, banding polymorphism
Comparative studies of banded chromosomes have shown that the organization
of euchromatic genetic material is extremely conservative [Rubio et al, 1973; Stock
and Hsu, 19731. The situation is quite different with regard to constitutive heterochromatin [Deaven et al, 1977). The amount and staining characteristics of constitutive heterochromatin may show wide variation among species and subspecies with
a similar or even identical distribution of euchromatin [Ma and Jones, 1975: Ponsa
et al, 19811. In some cases, whole chromosome arms are composed of constitutive
heterochromatin [Pathak et al, 1973a], producing changes in the fundamental number [nombre fondamental or N.F. in Matthey, 19591 of a species. According to the
classification of Miro, [1981], the different types of heterochromatin in primates are
as follows:
(1) centromeric heterochromatin: C + , G, and Q positive or negative;
(2) short arm heterochromatin: (a) C+, G+, Q-, and (b)C’, G-, Q’;
(3) interstitial heterochromatin: (a) C’, G’, Q+ and OD) C+, G-, Q-;
(4)telomere heterochromatin: (a)C f , G+, Q+, and (b) C+, G-, Q-;
(5) paracentric heterochromatin: (a) C + , G+, Qf, (b) C+, G’, Q-, and (c) C + ,
G-, Q-;
(6) secondary constriction heterochrornatin: (a) C +,G-, Q-, and (b) C + , G+, Q-;
(7) bright fluorescence heterochromatin; and
(8) C- heterochromatin (very late replicating) [Dutrillaux et al, 19791.
Received April 23, 1982; revision accepted November 1: 1982.
Address correspondence to Dr. M. Garcia, Instituto de Biologia Fundamental, Universidad Aut6noma de
Barcelona, Avda San Antonio Mfl Claret, 171 Barcelona-25, Spain.
01983 Alan R. Liss, Inc.
Garcia et a1
In this paper, we describe the C-, G-, and Q-bands as well as the nuclear
organizing region (NOR) distribution in Lagothrix lagothricha canq Cebus capucinus, and Cebus apella, and compare them to those described by Dutrillaux et a1
Blood samples were obtained from a male Lagothrix lagothricha canq three
female Cebus ape& and one female Cebus cupucinus, in the Barcelona Zoo (specimens identified by J. Sabater Pi, Curator of Mammals).
Leukocyte cultures were carried out according to standard methods, G-, Q-, and
C-bands and NOR were obtained following the techniques of Gallimore and Richardson [1973], Sumner [1972], Polani & Mutton [1971], and Bloom & Goodpasture
[19761, respectively.
Lagothrix Zagothricha c a m
The karyotype showed terminal, interstitial, and centromeric C-bands (Fig. 1).
In some chromosome pairs the C-bands were heteromorphic or polymorphic. Pair
number 1 lacked a centromeric C-band in the 75 metaphases studied. Pair number
4 lacked a centromeric C-band in 40% of the metaphases studied. In pairs number
16 and 22 centromeric heterochromatin was seen in only 5% of the metaphases
Pairs number 1 , 3 , 5 , 7 , and 9 had terminal C-bands in the short arm: With the
exception of pair 7 the size of the C-positive band was different between the two
homologues of each pair.
Pairs number 15, 16, 18, 19, 21, 23, 24, and 25 had interstitial C-bands of
variable size in the long arms. A comparison of C-banded karyotypes with the Gand Q-banding patterns of this species described by Dutrillaux et al [1980] and
Garcia et al [1980], showed that C-bands may be partially G- and Q-positive, Qnegative, or partially Q-positive and negative (Fig. 2). Centromeric terminal and
Fig. 1. C-banded karyotype of Lagothrix Zagothricha cuna Note heteromorphic terminal C-bands in pairs
1,3, and 9. Pair 9 lacks centromoric heterochromatin.
Heterochromatin Polymorphism in Cebidae
Garcia et a1
Heterochromatin Polymorphism in Cebidae
interstitial C-bands are G- and Q-variable (Fig. 2). Figure 3 shows the presence of
NOR in 5 acrocentrics of different size (a), in a single submetacentric chromosome
(b), and in one chromosome of the marker pair (c).
Cebus apella
The karyotype showed centromeric, terminal, and interstitial C-bands (Fig. 4).
All chromosome pairs had centromeric C-bands. Pair 11 had a terminal C-band and
was clearly dimorphic. Interstitial C-bands were observed in the long arms of pairs
4, 12, 14, 19, and 21. In the three females studied, these chromosome pairs were
dimorphic (Fig. 5).
Figure 6 shows the NOR, always present in three acrocentric marker chromosomes, and in a small percentage of cells also present in a long acrocentric and in a
long submetacentric chromosome.
Cebus capucinus
The karyotype also showed centromeric, terminal, and interstitial C-bands. (Fig
7). All chromosome pairs had centromeric C-bands. The terminal C-bands were
observed in pairs 1and 2, and in a single member of pair 3 and in pair 9, they were
clearly dimorphic. Interstitial C-bands were found in the long arms of pairs 5, 10,
11,12, 13, 18, and 19, and were also dimorphic. Figure 8 shows the NOR, present in
four acrocentric chromosomes.
The only data available on the distribution of C-bands in Lagothrix lagothricha
were published by Dutrillaux et a1 [1980] for a single female. The authors did not
indicate the subspecies studied and did not include a C-banded karyotype. However,
Fig. 5. C-band heteromorphism in pairs 4, 11 (from 2 different females), 12,14 (only in one chromosome),
19. and 21.
Garcia et a1
Fig, 6. NOR regions (arrows) in three small acrocentrics (a),a long acrocentric (b),and a submetacentric
chromosome (c), of Cehus upella
since the diploid number and the G- and Q-banding patterns were identical to those
found by us, we compared our results with their description. We found several
chromosomal differences that are apparently due to a marker polymorphism in this
species, comparable to that found in other Platyrrhini [Ma et al, 1974; Lau and
Arrighi, 19761.
Though Dutrillaux et a1 [1980] observed interstitial C-bands in two submetacentric pairs, we found only terminal C-bands. The difference might be due to the fact
that the R-banding technique used by Dutrillaux et a1 [1980] permits better visualization of the telomeres; thus our terminal C-bands could be subterminal. However,
we observed terminal C-bands in six submetacentric pairs.
Dutrillaux et a1 [1980] described interstitial C-bands in only four acrocentric
pairs, while in our specimen these were seen in eight.
The C-bands of Cebus apella have not been previously studied. Dutrillaux et a1
[1978a] described the C-bands of a single specimen of Cebus capucinus, but did not
publish a photograph. The diploid number (2n = 54) and the morphology of the
chromosomes (eight pairs of nonacrocentrics "As] and 18 pairs of acrocentrics [As])
found in our animals partially confirm their results, but the distribution of C-bands
is different. While Dutrillaux et a1 [1980] described the presence of terminal C-bands
only in pairs 2 and 3, we have found terminal and interstitial C-bands in a large
number of chromosomes, with a high degree of heteromorphism.
Fig 8. NOR regions (arrows) in four acrocentric chromosomes of C.c~pucinus.
Fig. 7. C-banded karyotype of Cebus cupucinus. Note heteromorphic intcrsitital or terminal bands in
pairs 1,2, 3 (only one chromosome), 5,9,10,11,12,13,18,and 19.
x x
Garcia et a1
A review of C-banding studies in primates indicates that the presence of interstitial C-bands in several chromosome pairs is infrequent. So far, this distribution
has been described in Aotus [Ma et al, 19761, Cebus capucinus [Dutrillaux et al,
1978a1, and Lugothrix [Dutrillaux et al, 19801. The presence of an interstitial C-band
in a single chromosome pair has been observed in Sairniri sciureus [Ma et al, 1974;
Lau & Arrighi, 19761, a gibbon [Tantravahi et al, 19761, Cullicebus torquatus [Benirschke & Bogart, 19761, Pygathrix nemaeus [Bogart & Tukamoto, 19781 and in two
chromosome pairs in Cheirogaleus [Dresser & Hamilton, 19791.
The origin of interstitial heterochromatin is unknown. Since the first studies on
the distribution of constitutive heterochromatin showed predominantly a centromeric location [Pardue and Gall, 19701, the presence of interstitial C-bands has been
causally related to structural rearrangements (inversions) [White, 19751. However,
this interpretation is unlikely, since interstitial bands are often quite large, and
centromeric bands are generally small. Interstitial C-bands might originate by
heterochromatinization of previously euchromatic regions [King, 19801, as if the
chromosomes have a structural tendency to heterochromatinization in an orthoselective sense [King & John, 19801, or through a n increase in the amount of constitutive
heterochromatin, perhaps by a mechanism of saltatory replication [Shaw et al,
19761. The increase in the amount of constitutive heterochromatin is probably a
massive phenomenon, regulated at the cellular level, because it affects all or most
chromosome pairs [Dutrillaux et a1 [1978b; Ponsa et al, 19811.
The relationship between interstitial and terminal heterochromatin and structural chromosome rearrangements can be interpreted in two different ways not
mutually exclusive [Dolfini, 19761. According to some authors, the breakpoints
involved in structural rearrangements are sites of heterochromatin accumulation.
Another suggestion is that the presence of interstitial andior terminal C-bands
facilitates the occurrence of structural rearrangements such as inversions, insertions, and fusions, because chromosome breaks could take place at their level
without affecting informative DNA. In our opinion, the second explanation seems
more logical. In fact, the Cebidae have the most unstable karyotypes among the
Primates [Garcia 1979; Koiffman & Saldanha, 19811; their chromosomes contain a
large number of interstitial and terminal C-bands, and many rearrangements affect
C + regions (eg, Saimiri as described in Ma et a1 119741 and Lau & Arrighi [1976)).
Chromosome heteromorphism has been described in several species of Platyrrhini. Such heteromorphism has been interpreted as due to translocations according
to the interpretation of Koiffman & Saldanha 119741 or to a differential coiling of
the chromosomes [Garcia et al, 19761. In fact, the differences in length between the
members of a pair in these cases are due to differences in the amount of constitutive
heterochromatin found in the two homologues (Figs. 4,5, 7).
Finally, it is interesting to note the variability in the distribution and activity
of the NORs. A t least one of the so-called nucleolar organizing chromosomes may
not show NOR activity. The observation that a secondary constriction is not necessary for an NOR to exist is confirmed. Some NORs are only active in some cells.
Thus, some NORs cannot be used as markers in cytological studies.
We thank Dr. A. Jonch, Director, and Dr. J. Sabater Pi, Curator, of the Barcelona
Zoo for their permission to obtain and collaboration in obtaining the samples, and
Justo Garisa and the staffof the Centro de Biologia Animal Aplicada y Primatologia,
Barcelona Zoo, for their technical help.
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constitution, polymorphism, canan, cebus, capucinus, heterochromatin, lagothrix, apella, lagothricha
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