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Cytogenetic studies of Aotus from Eastern Amazonia. YAutosome rearrangement

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American Journal of Primatology 14:255-263 (1988)
Cytogenetic Studies of Aotus From Eastern Amazonia:
Y/Autosome Rearrangement
JULIO CESAR PIECZARKA AND CLEUSA YOSHIKO NAGAMACHI
Departamento de Genbtica, Centro de CGncias Bwl6gicas, Universidade Federal do Pard,
Belkm, Pard, Brazil
Twenty-one specimens of Aotus were captured on both sides of the Tocantins
river when the hydroelectric reservoir of Tucurui, Brazil, was filled. The
males had a diploid number of 49 chromosomes, and the females had 50.
The observed difference is a consequence of the fusion of the Y chromosome
with an autosome. The karyotype is similar to that of the Bolivian Aotus
(A. azarae boliviensis). It differs, however, in the G- and C-bandingpatterns
of the chromosome resulting from the Mautosome fusion. The nucleolar
organizing region is located on the secondary constriction of a pair of
submetacentric chromosomes. Considerations are presented on the classification of A. infulatus as a separate species.
Key words: cytotaxonomy, Y chromosome, fusion, owl monkey
INTRODUCTION
The subfamily Aotinae (family Cebidae) has a single genus, Aotus. Until recently it was assumed that the only species of this genus was A. trivirgatus, which
had a widespread geographical distribution and a variable fur pattern [Cabrera,
1958; Napier & Napier, 1967; Napier, 1976; Mittermeier & Coimbra-Filho, 19811.
Cytogenetic studies, however, have demonstrated that the genus Aotus has at least
12 different karyotypes, with a diploid number ranging from 46 to 56 chromosomes
[Brumback, 1974; de Boer, 1974; Koiffmann & Saldanha, 1974; Ma, 1981; Mudry De
Pargament et al., 1984; Ma et al., 1978, 19851. Indeed, Ma et al. [1976b] established
correlations between the karyotypes and the fur patterns. Based on characteristics
such as fur pattern, karyotype, and geographical distribution, Hershkovitz [19831
reclassified the genus Aotus into eight species. Two populations with the same
karyotype but different fur patterns are considered to be subspecies. If a population
has a characteristic fur pattern but its karyotype is still unknown, it is considered
to be a species.
Among the karyotypes listed in Table I, A. nigriceps, A. a boliviensis, and A. a
azarae show a difference in chromosome numbers between males and females as a
consequence of a fusion of the Y chromosome with an autosome. Ma et al. [1980] and
Received June 12,1986;revision accepted November 23,1987.
Address reprint requests to Julio Cesar Pieczarka, Departamento de Genbtica, Centro de Cibncias Biolopicas, Universidade Federal do Para, Campus do Guam&,66000 Belbm, Pard, Brazil.
0 1988Alan R. Liss, Inc.
256 I Pieczarka and Nagamachi
TABLE I. Species and Karyotypes of Aotus*
Group
Gray neck
Red neck
Species
A. lemurinus
A. 1. lemurinus
A. L griseimembra
A. brumbacki
A. trivirgatus
A. uociferans
A. azarae
A. a boliviensis
A. a azarae
A. nigriceps
A. infulatus
A. miconax
A. nancymai
Region
Karyotype
Panama
Northwest of Colombia
North of Colombia
Venezueldnorth of Brazil
Colombidnorthwest of Brazil
2n = 55;56
2n = 52;53;54
2n = 50
?
2n = 46;47;48
Bolivia
Paraguaylnorth of Argentina
Central Perdwest of
Brazilian Amazonia
East of Brazilian Amazonia
Peru
North of Perdwest of
Brazilian Amazonia
2n
2n
2n
= 49M,50F
= 49M;50F
= 51M;52F
?
?
2n = 54
*The classification and geographical distribution are from Hershkovitz [1983]. Cytogenetic data may he
found in Brumback et al. [1971], de Boer [1974], Ma et al. [1976b, 1978, 19851, Yunis et al. [1977],
Hershkovitz [1983], and Mudry de Pargament [1984]. M = male; F = female.
Ma [1981] compared the karyotypes of A. nzgrcceps and A. a boliviensis. It was
shown that in both the fusion of the Y chromosome occurs with the short arm of a
medium-size subtelocentric autosome. G-banding (Ma et al., 1980; Ma, 19811 and
gene mapping [Ma, 19841 provided evidence that this autosome is the same on both
karyotypes. In addition, in A. a boliviensis the fusion of the Y with the short arm of
the autosome is followed by a pericentric inversion, whereby the short arm bearing
the Y chromosome becomes a portion of the long arm of the resulting submetacentric. These species further differ by three autosomic rearrangements. In A. a azarae,
the Y fusion is to a small acrocentric autosome, but all other chromosomes are
identical on G- and C-banding level to A. a boliviensis chromosomes [Mudry de
Pargament et al., 19841. Galbreath [1983] assumed on the basis of geographic
distribution and similarities in fur pattern that the karyotype of A. infulatus should
not be very different from the karyotypes of A. nigriceps and A. azarae.
The present study aimed to analyze cytotaxonomically the karyotypes of Aotus
infulatus specimens captured on both sides of the Tocantins river in Tucuruf, State
of Para, Brazil.
METHODS
Twenty-one Aotus specimens (11males and 10 females) from both sides of the
Tocantins river were captured during flooding of the lake of the hydroelectric
reservoir of Tucurui, 60 km upstream from the township of Tucurui, Para. The
specimens obtained Pig. 1)were classified as A. infulatus according to parameters
that included the fur pattern and geographicaI distribution presented in the phenetic
key for Aotus species and subspecies proposed by Hershkovitz [1983]. It is relevant
to emphasize some of the findings, such as 1)the orange color of the belly of these
Aotus, which extended from the ventral portion of the throat to the elbow and
ankles; 2) the light orange color of the tail in the proximal dorsal part and throughout the ventral portion, and 3) the absence of an interscapular whorl.
Blood (3 ml) was collected by femoral puncture using heparinized syringes, and
the chromosomes were obtained by culturing lymphocytes according to the method
Karyotype of Aotw From Eastern Ammonia I 257
Fig. 1. Aotus from the Tocantina river.
described by Moorhead et al. [1960]. G-, C-, and nucleolar organizer region (NOR)
bands were obtained by methods previously described [&heres, 1972; Sumner, 1972;
Goodpasture & Bloom, 19751. Sequential banding was performed by submitting the
material to G-banding, followed by destaining and C-banding. The chromosomes
were arranged according to Ma et al. [1976b], with modifications, for the preparation
of the karyotypes.
RESULTS
Males had 49(2n) chromosomes and females 50(2n). No Y chromosome was found
by conventional staining. The males showed three unmatched chromosomes: 1) the
X, (2) a medium-sized subtelocentric, which corresponds to the B12 of females; and
3) a submetacentric chromosome. This submetacentric is larger than B12, but its
long arm is slightly shorter than the long arm of B12.
Figure 2 shows the G-banding pattern found in the specimens studied. The
banding pattern of the male-specific submetacentric is similar to the banding pattern of the B12, but it shows an additional dark G-band on the short arm.Another
difference between these chromosomes is the pericentromeric pattern. On both
chromosomes there is one dark G-band on the short arm and one dark G-band on
the long arm near the centromere. These bands do not have the same shape. On Y/
B12 the larger band is on the short arm, and on B12 the larger band is on the long
arm.
The correspondence of C- and G-banding patterns is seen in Figure 3.
Figure 4 shows the C-banding pattern. All chromosomes show centromeric
bands. In group B, all chromosomes have a heterochromatic short arm, excepting
pairs B7, B9, and B11. Intercalary bands are also observed in pairs B12, B16, and
B23. Some variation was seen in the C-band size between homologues, especially in
the A2, B15, B16, B20, and B23 chromosomes.
A comparison of the C-banding pattern of the male-specific submetacentric and
the B12 chromosome shows that the submetacentric has a large band at the terminus of the short arm, which is absent on B12. In addition, the centromeric band has
the same shape on both the long and short arms of the submetacentric. The band is
larger, however, on the short arm than on the long arm of Bl2. There is an intercalar
band on the long arm of the submetacentric chromosome that is closer to the
centromere than is the corresponding band on the B12 (Fig. 5b).
258 I Pieczarka and Nagamachi
A
1
2
3
4
5
7
8
9
10
11
6
5
E
B
x
Y/12
12
m
B
13
14
15
16
17
18
19
20
21
22
X
12
J
B
23
24
Fig. 2. G-banding pattern in Aotus from the Tocantins river. The boxed chromosomes are from a female
karyot ype.
Fig. 3. Sequential G-C banding in Aotus. The arrow indicates the YB12 chromosome.
Fifty metaphases with NOR labeling were analyzed per animal. Silver staining
occurred exclusively in the secondary constriction of pair A6. An average of 89.9%
of the metaphases showed labeling in both A6 homologues. The intensity of labeling
was frequently identical in both homologues (Fig. 6a), but uneven labeling was also
observed (Fig. 6b). Associations between acrocentrics were observed in 24.66% of the
metaphases investigated; however, they were not silver stained.
Karyotype of Aotus From Eastern Amazonia I 259
1
2
3
4
5
7
8
9
10
11
13
14
15
16
17
18
19
20
21
22
6
59!!!L
x
23
Y/12
12
24
Fig. 4. C-banding pattern in Aotus from the Tocantins river. The boxed chromosomes are from a female
karyotype.
V
Y
Fig. 5. Rearrangements involving the YO312 chromosome. After fusion of the Y with the autosome, there
was a pericentric inversion. a: G-banding. b: C-banding. According to our model, the large C band on the
terminus of the short arm of YO312 is composed by the Y chromosome and part of a C band found on the
short arm of the B12.
DISCUSSION
The results described here permit the characterization of the karyotype of Aotus
infulutus from the Tucurui region, State of Para, Brazil. Before the availability of
NOR silver staining technique, it was assumed that chromosome pair A6 represented the nucleolar organizing chromosomes because of the secondary constriction,
as do some chromosomes in group B as a function of the associations observed [de
Boer, 19741. Studies using this technique, however, showed only one pair of submetacentrics as the nucleolar organizing chromosomes in A. nigriceps [Ma et al., 19801
and A. lemurinus griseimembru [Miller et al., 19771. This chromosome corresponds
to the pair A6. The present results confirm this observation, since silver staining
260 I Pieczarka and Nagamachi
Fig. 6. NOR in Aotus. a: The small arrows indicate the stained chromosomes. The large arrow indicates
an association of acrocentric chromosomes without silver incorporation. b: Nucleolar organizing chromosomes with unequal staining.
Karyotypr
I
INV. 1
I
'7'
Fig. 7. Phylogenetical relationship among A. infulatus, A. a boliviensis, and A. nigriceps supported by
chromosomic analysis. 3AR = three autosome rearangements; INV.1 = pericentric inversion of the Y/
autosome of A. infulutus; INV.2 = pericentric inversion of the Y/autosome of A. a boliviensis. See text for
further details.
Karyotype of Aotus From Eastern Amazonia I 261
occurred exclusively in this pair. The absence of silver staining on acrocentric
chromosomes suggests that they are not related to the formation of nucleolus.
G- and C-banding patterns suggest that the Y chromosome is not absent in the
karyotype of males but is linked to the short arm of one homologue of pair B12. It is
possible that the large heterochromatic band observed by C-banding in the short
arm of the YE312 chromosome represents the location of the Y. The resulting
chromosome of this fusion is the male-specific submetacentric. The Y/autosome
fusion hypothesis is supported by the difference in diploid number between males
and females.
There are other differences between the chromosomes B12 and YB12 other than
the Y fusion. These differences can be observed during the analyses of conventional
staining (the long arm of YB12 is shorter than the long arm of B12), G-banding(the
pattern of dark bands near the centromere of YB12 is the inverse of the B12
pattern), and C-banding (the difference on the centromeric band pattern; an intercalar band on YE312 is closer to the centromere than is the corresponding band in
B12). Chromosomic condensation cannot be responsible for these dissimilarities
because they are present in all the metaphases found. These chromosome differences?however? could be explained by a small pericentric inversion in which the
breakpoints of the inversion would neighbor the centromere; the inverted region
would include only the autosomic portion (B12) of the YB12 chromosome (Fig. 5).
When the karyotype of the Aotus studied here is compared with those previously
published? it can be seen that except for pair B12, all the autosomic chromosomes
and the X chromosome of A. infulatus are identical on G- and C-banding levels to
the corresponding chromosomes of A. a boliviensis described by Ma et al. [1976a].
The only differences between A. infulatus and A. a boliuiensis are on the G-banding
pattern of B12 and on the G- and C-banding patterns of the Y/autosome. Pair B12,
with three dark G-bands on its long arm, is slightly different from the corresponding
B14 chromosome pair of A. a boliuiensis, which is characterized by having four dark
G-bands on its long arm. However, pair B12 is identical with pair B17 ofA. nigriceps.
In addition? Ma et al. [1980] showed that in two animals pair B17 of A. nigriceps
was marked by four G-bands and was analogous to B14 of A. a boliuiensis. Using
this information, we were able to show that the autosome involved in the fusion
with the Y was the same in both karyotypes of A. infulatus and A. a boliuiensis.
However, different pericentric inversions occurred on the Ylautosome in each karyotype. The inversion observed in A. infulatus was small and involved only the region
near the centromere, while in A. a boliuiensis the inversion involved nearly all the
short arm of the Y/autosome. After this inversion, the Y is transferred to the long
arm of the resulting submetacentric chromosome [Ma et al., 1976a, 19801.
The differences in the karyotypes of A. a azarae and A. nigriceps and the
karyotype of A. a boliuiensis are valid to A. infulatus, since the latter is quite
simiIar to A. a boliuiensis.
The information obtained suggested that the pericentric inversion on YB12 of
A. infulatus possibly occurred after the fusion of the Y with the B12 chromosome
(Fig. 5). It is possible that the inversion occurred before fusion, but the fact that
fusion of the Y occurred with the same autosome in Aotus infulatus, A. a boliuiensis,
and A. nigriceps indicates that this rearrangement should have occurred before
these populations became isolated. Furthermore, since the pericentric inversion in
A. infulatus is not equal in breakpoints to the inversion detected in A. a boliuiensis
[Ma et al., 1976a1 and since it was not found in A. nigriceps [Ma et al., 19801, it is
reasonable to assume that this event occurred after the separation of the population
and, therefore, is more recent than the Ylautosome fusion.
262 I Pieczarka and Nagamachi
The origin of the Ylautosome of A. infulatus and A. a boliviensis is tentatively
explained if it is assumed that an ancestral population with a karyotype similar to
that of A. nigriceps (2n = 51,521 gave rise to a group of animals that fixed three
autosomal rearrangements, originating the 2n =49,50 karyotype and maintaining
the Ylautosome chromosome of the ancestral population. This newly derived population was further divided, with a pericentric inversion of the Ylautosome (nVv.1,
Fig. 7), becoming fixed in one subgroup, and another pericentric inversion of the Yl
autosome (INV.2, Fig. 7), becoming fixed on the other subgroup. One of these
subgroups may have originated A . infulatus and the other A. a boliviensis (Fig. 7).
The chromosomic differences discussed above are helpful for understanding
Aotus phylogeny. However, they are not conclusive from a cytotaxonomic point of
view. There are not enough differences between A. infulatus and A. a boliviensis to
support two distinct species. On the other hand, different species can have identical
karyotypes. Considering the amount of chromosomic variation in the genus Aotus
as well as the rare events described where two animal species have equal karyotypes, it is possible that both groups are of the same species.
A. infulatus and A. a. boliviensis have karyotypes that are more similar to each
other than to the karyotype of A. a azarae. This information clearly demonstrates
the need to revise the systematic classification of this taxonomic group.
CONCLUSIONS
1. The karyotype of Aotus infulatus is 2n = 49 for males and 2n = 50 for
females. The difference is due to a fusion of the Y with an autosome.
2. The karyotype of Aotus infulatus is quite similar to the karyotype of A. azarae
boliviensis, except for pair B12 and for an inversion on the Ylautosome chromosome.
3. The Ylautosome fusion in A. infulatus, A. a boliviensis, and A. nigriceps
apparently occurred before these populations became isolated.
4. The karyotypes of A. infulatus and A. a boliviensis are closer to each other
than to the karyotype of A. a azarae.
ACKNOWLEDGMENTS
We are grateful to Dr. Regina M.S. Barros for her valuable suggestions; to the
Centro Nacional de Primatas-FSESP for their help in the taxonomic identification
of the specimens studied and to FINEP, FADESP, CNPq, PIG, ELETRONORTE,
and UFPa for financial support.
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