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Chromosome studies of Cebus apella The standard karyotype of Cebus apella paraguayanus Fischer 1829.

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American Journal of Primatology 10:185-193 (1986)
BRIEF REPORT
Chromosome Studies of Cebus apella: The Standard
Karyotype of Cebus apella paraguayanus, Fischer, 1829
TETSUJI MATAYOSHI, EDGARDO HOWLIN, NORA NASAZZI, CARLOS NAGLE,
ENRIQUE GADOW, AND HECTOR N. SEUANEZ*
Seccwn Genktica, Departamento de Ginecologia y Obstetriciq Centro de Educacion Mkdica e
Investigaciones Clinicas (CEMIC), Buenos Aires, Argentina;* Department of Genetics,
Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil
Chromosome studies were performed on 40 specimens identified as Cebus
apella paraguayanus, Fischer, 1829, which had been wild-caught in Santa
Catalina (Republic of Paraguay). Elongated chromosome spreads obtained
from lymphocyte cultures were sequentially stained with different techniques, and a constant pattern of 382 bands was identified in all specimens.
A standard karyotype based on the measurements of the total chromosome
length and the G-Q banding pattern is proposed.
Key words: Cebus apella, chromosomes, standardization
INTRODUCTION
Cebus apella is a platyrrhine species extensively distributed in the tropical
forests of South America and commonly used in biomedical research. Feral populations of Cebus apella, ranging from 5" north to some 30" south of the equator line,
are subdivided into different subspecies on the basis of their gross morphological
characteristics and geographic distribution [Napier & Napier, 19671.
Chromosome studies of Cebus apella subspecies are scarce and fragmentary
because the geographical origin andlor the phenotypic characteristics of the specimens under study are rarely mentioned. Moreover, the karyological characterization
of this species has been based so far on very few specimens [Bender & Chu, 1963;
Chiarelli & Barberis, 1966; de Boer, 1974; Garcia et al, 1976, 1978; Cambefort &
Moro, 19781 without a common criterion of chromosome nomenclature and ordination and with different techniques of chromosome analysis. None of these previous
reports refers specifically to Cebus apella paraguayanus, Fischer, 1829, also known
as Cebus apella cay, Illiger, 1815, a subspecies which was originally described in the
Chaco forests of the Republic of Paraguay in a clearly delimited region between the
Parana and Paraguay rivers. More recent studies of Cebus apella subpopulations,
such as the report of Freitas and Seuanez [1982], are restricted to specimens from
three different regions of Brazil on the Atlantic coast. Furthermore, the only report
on Cebus apella cay [Mudry de Pargament et al, 19841 is based on specimens
captured outside the limits of their original distribution in the northern provinces
of Argentina, across the Parana river, where the range of Cebus apella cay partially
overlaps with that of Cebus apella nigritus and crossbreeding between them has not
been excluded.
Received May 20,1985; revision accepted October 6, 1985.
Address reprint requests to T. Matayoshi, Seccion Genetica, CEMIC, Galvan 4102, 1431-Buenos Aires,
Argentina.
0 1986 Alan R. Liss, Inc.
186 I Matayoshi et a1
Fig. 1. The arrow shows the area where the specimens were wild-caught. Santa Catalina (Republic of
Paraguay) latitude 26" 30' S, longitude 57" 44'W.
Herewith we present our studies on the chromosome complement of a large
number of Cebus apella paraguayanus which had been wild-caught within the
boundaries of their natural habitat, a region where this subspecies is not sympatric
with any other subspecies of Cebus apella. Well spread, elongated chromosomes were
sequentially stained with different procedures. The level of resolution at the chromosome band level allowed us to standardize the karyotype of this subspecies, which
can be used as a reference karyotype for other Cebus apella subspecies.
METHODS
Subjects
Forty specimens (20 males and 20 females) of Cebus apella paraguayanus were
studied. The animals had been wild-caught in Santa Catalina (Republic of Paraguay), a region included in the Paraguayan Chaco forest between the Parana and
Paraguay rivers (Fig. 1).All specimens were unequivocally identified following the
descriptive criterion of Hill [1960] for the identification and distinction of Cebus
apella subspecies [see also Napier & Napier, 19671.
Procedure
Blood cultures were grown in TC 199 or Hams' F-10 media with 2%PHA (Difco)
supplemented with fetal calf serum (15%)for 70 hours a t 37°C. Colcemid (0.2 wg/ml)
was added for the last 60 minutes of incubation before harvesting. Well-spread
preparations showing elongated chromosomes were sequentially stained with quinacrine [Caspersson et al, 19701 and conventional Giemsa staining (Fig. 2). Following
Q-band identification, conventionally stained chromosomes were photographed, and
Cebus apella paraguayanus Karyotype f 187
their relative chromosome length (RCL) was estimated as the ratio between chromosome length of each homologue x100 and the total haploid chromosome length
including the X chromosome. For karyotyping, autosomes were divided into two
groups on the basis of their morphological attributes (biarmed or acrocentric). Within
each of these groups, homologue pairs were ordered in decreasing size (Table I). Gbanding was done following the procedure of Seabright [1971]. An idiogram was
constructed on the basis of the morphometric characteristics and the specific Q-Gband pattern of each homologue pair.
RESULTS
All animals had a diploid chromosome number of 54 chromosomes consisting of
ten biarmed (numbers 1-10) and 16 acrocentric autosome pairs (numbers 11-26); of
the sex chromosomes, the X was biarmed and the Y was a n acrocentric chromosome
(see Fig. 3). A standard karyotype of this subspecies was constructed on the basis of
the Q-G-banding of each homologue pair, both techniques producing basically the
same pattern of staining. Within each autosome group, pairs were ordered in decreasing size on the basis of the measurements shown in Table number I. Chromosome band resolution in elongated chromosomes allowed for the precise identification
and characterization of 382 chromosome subregions that were numbered similarly
to the High Resolution Human Karyotype (see “An International System for Human
Cytogenetics Nomenclature, ISCN” [1981]).
TABLE I. Relative Chromosome Length (RCL)
Group
Biarmed
Acrocentric
Sex
Chromosome
pair
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
X
Y
RCL
6.08
5.58
5.07
4.72
4.42
4.26
3.67
3.17
2.29
2.29
5.95
5.00
4.51
4.34
4.23
3.88
3.82
3.56
2.95
2.92
2.43
2.35
2.29
1.96
1.55
1.55
4.54
1.35
188 I Matayoshi et a1
Fig. 2. Metaphase sequentially stained with quinacrine [Caspersson et al, 19701 and conventional
Giemsa staining.
Fig. 3. See page 191 for legend
190 I Matayoshi et a1
Figure 3.
Cebus apella paraguayanus Karyotype I 191
Fig. 3. Ideogram illustrating the G-banding pattern of the Cebus apella paraguayanus chromosomes
arranged according to the proposed standardization.
192 I Matayoshi et a1
DISCUSSION
Banding techniques are the only reliable procedures for the precise and unequivocal identification of chromosomes and of subregions within them. High-resolution
patterns can be obtained in enlongated chromosomes, which permits better characterization of subregions. This analysis when applied to Cebus apella paraguayanus
has allowed identification of 382 different subregions and unequivocal identification
of each chromosome pair with a higher degree of resolution than that of any previous
report on the chromosomes of this species. Moreover, a morphometric analysis of
individual chromosome pairs has permitted us to order them precisely in decreasing
size order within each autosome group. By carrying out measurements on conventionally stained chromosomes, we have, moreover, eliminated possible errors in
length estimations which result from the appearance of G-negative regions on the
telomeres or from other distorting effects produced by trypsin digestion on chromosome structure.
Two aspects deserve a special comment with respect to the proposed standardization. One is that it represents a set of karyotypic characteristics of one subspecies of
Cebus apella which might not be necessarily extrapolated to the whole species level.
Partial evidence suggests that several Cebus apella subpopulations share the same
basic karyotype [Freitas & Seuanez, 19821, implying that Cebus apella might comprise a rather karyotypically uniform group. However, this report does not include
every subspecific group within the species, and the possibility that some of the
variant chromosome types described could actually be subspecies-specific cannot be
ruled out. More recently, Seuanez et a1 (in press) have shown that a t least one
subspecies (Cebus apella xanthosternos, Wied, 1820) can be distinguished by the
presence of a n intercalar heterochromatic region in one autosome pair (number 11
in our standard karyotype). For this reason, extrapolations of findings from the
subspecies to the whole species level can only be tentative until more population
studies are carried out, with a comparable level of technical resolution, to analyze
the degree of chromosome variation within Cebus apella.
The second point that is worth mentioning is that chromosome ordination and
nomenclature have followed, in our study, very strict morphological and morphometric criteria regardless of the presumptive chromosome similarities between these
species and others of the same genus. For this reason, our standardization criterion
differs from that of Torres de Caballero et a1 [1976], by which the chromosomes of
Cebus apella were ordered as in Cebus capucinus. Since presumed morphological
homologies between different primate species might not always be coincident with
syntenic homologies, a n independent criterion of karyotypic standardization is preferable. Anthropocentric criteria are further biased by the fact that nonhuman
primates must contain several gene loci which are absent in humans and vice versa.
The use of a n anthropocentric criterion for Cebus apella chromosomes would require
an indirect extrapolation with Cebus capucinus chromosomes for which a comparative gene assignment chart exists with respect to the genetic map [Creau-Goldberg
et al, 19811. Finally, we wish to emphasize that our findings are based on the largest
number of Cebus apella specimens studied in the literature; the karyotype standardization of this subspecies might be valuable for further comparisons at the chromosome level of different Cebus apella subspecies or populations and for the
establishment of a potential correlation between karyological and phenotypic characteristics in relation to their geographic distribution.
CONCLUSIONS
1. Cytogenetic studies of Cebus apella paraguayanus, with different staining
techniques sequentially applied, allowed precise identification of each chromosome
pair.
Cebus apella paruguayanus Karyotype I 193
2. The Q-G-banding showed a constant pattern of 382 chromosome subregions
in the 40 specimens.
3. The karyotype standardization we have proposed might be valuable for
comparisons with other Cebus apella subspecies.
ACKNOWLEDGMENTS
This work was supported in part by grants from the Subsecretaria de Estado de
Ciencia y Tecnica 192, 1982 (Argentina), UNESCO Regional Programme for PostGraduate Training in Biological Sciences RLA 78/028, and FINEP (Brazil) grant
number 4384073400. The authors thank Mr. Armando Gette from the primate
colony for technical assistance and Miss Irene Spinadel for typing this manuscript.
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