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Comparative chromosome painting in Aotus reveals a highly derived evolution.

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American Journal of Primatology 65:73–85 (2005)
RESEARCH ARTICLE
Comparative Chromosome Painting in Aotus Reveals a
Highly Derived Evolution
AURORA RUIZ-HERRERA1, FRANCISCA GARCÍA1,2, MARISOL AGUILERA3,
MONTSERRAT GARCIA1,2, and MONTSERRAT PONSÀ FONTANALS1,2n
1
Departament de Biologia Cellular, Fisiologia i Immunologia, Universitat Autònoma de
Barcelona, Barcelona, Spain
2
Institut de Biotecnologia i Biomedicina (IBB), Universitat Autònoma de Barcelona,
Barcelona, Spain
3
Grupo BIOEVO, Universidad Simón Bolı´var, Caracas, Venezuela
The genus Aotus represents a highly diverse group with an especially
intricate taxonomy. No standard cytogenetic nomenclature for the genus
has yet been established. So far, cytogenetic studies have characterized 18
different karyotypes with diploid numbers ranging from 46 to 58
chromosomes. By combining G-banding comparisons and molecular
cytogenetic techniques, we were able to describe the most likely pattern
of chromosome evolution and phylogenetic position of two Aotus
karyomorphs (KMs) from Venezuela: Aotus nancymai (KM3, 2n ¼ 54)
and Aotus sp. (KM9, 2n ¼ 50). All of the proposed Platyrrhini ancestral
associations (2/16, 3/21, 5/7, 8/18, 10/16, 14/15) were found in the Aotus
KMs studied, except 2/16 and 10/16. In addition, some derived
chromosomal associations were also detected in both KMs (1/3, 1/16, 2/
12, 2/20, 3/14, 4/15, 5/15, 7/11, 9/15, 9/17, 10/11, and 10/22). Although
some of these associations have been found in other New World monkeys,
our results suggest that Aotus species have undergone a highly derived
chromosomal evolution. The homologies between these two Aotus KMs
and human chromosomes were established, indicating that KM3 has a
more derived karyotype than KM9 with respect to the ancestral
Platyrrhini karyotype. Am. J. Primatol. 65:73–85, 2005. r 2005
Wiley-Liss, Inc.
Contract grant sponsor: DGI; Contract grant number: BXX2000-0151; Contract grant sponsor:
Ministerio de Ciencia y Tecnologı́a; Contract grant sponsor: AIRE; Contract grant number: 140122;
Contract grant sponsor: DURSI, Generalitat de Catalunya; Contract grant sponsor: DID,
Universidad Simón Bolivar; Contract grant number: G-026; Contract grant sponsor: Universitat
Autònoma de Barcelona.
n
Correspondence to: Montserrat Ponsà Fontanals, Departament de Biologia Cellular, Fisiologia i
Immunologia, Unitat de Biologia Cellular, Facultat de Ciències, Universitat Autònoma de
Barcelona, 08193-Cerdanyola del Vallès, Barcelona, Spain. E-mail: Montse.Ponsa@uab.es
Received 26 May 2004; revised 16 September 2004; revision accepted 3 November 2004
DOI: 10.1002/ajp.20098
Published online in Wiley InterScience (www.interscience.wiley.com).
r
2005 Wiley-Liss, Inc.
74 / Ruiz-Herrera et al.
INTRODUCTION
The owl monkey (Aotus) is the only genus in the subfamily Aotinae (F.
Cebidae, Platyrrhini, Primates) and is considered to be currently undergoing
subspeciation [Ma, 1981]. This primate genus is widely distributed in Central and
South America, from western Panama through the northern part of Argentina.
The taxonomy of the genus Aotus is especially intricate because there is no
consensus about the exact number of species and subspecies. However, different
revisions of the genus are considering nine or 10 different species based on
phenotypic and karyotypic characters and geographic distribution (Table I).
From the cytogenetic point of view, the genus Aotus represents a highly
diverse group in which many specific chromosomal variations have been described
[Ma, 1981, 1983; Mudry et al., 1984; Pieczarka et al., 1993]. Given this diversity in
karyotypes, cytogenetic studies based on G- and C-banding comparisons have
been extremely useful for clarifying the taxonomy of this group during the past
three decades [Hershkovitz, 1983; Ma, 1981; Ma et al., 1976a]. So far, 18 different
karyotypes have been characterized, with chromosome diploid numbers ranging
from 46 to 58 chromosomes [Torres et al., 1998]. In addition, some authors have
reported a sex determination XX/‘‘XO’’ for the A. infulatus, A. azarae, and A.
nigriceps species [Ma, 1981; Ma et al., 1976a, 1980; Mudry et al., 1984; Pieczarka
& Nagamachi, 1988] due to a translocation of chromosome Y in one autosome.
Although great efforts have been made to construct a systematic relationship
among the different Aotus species, a standard and uniform cytogenetic
nomenclature for the genus has not yet been established. To date, three
nomenclature systems have been published [Ma et al., 1976a; Reumer & de Boer,
1980; Torres et al., 1998]. Only Torres et al.’s [1998] system accommodates all
existing information based on size, chromosome morphology, and sequential
banding pattern (Table I).
Molecular studies have not been able to establish the exact phylogenetic
position of the genus Aotus within New World monkey species [Ford, 1986;
Rosenberger, 1984]. Rosenberger [1984] considers that Aotus, together with
Callicebus, is closely related to Pithecinae (Pithecia, Chiropotes, and Cacajao),
whereas Ford [1986] placed Aotus and Callicebus as a basal lineage for
Callithrichidae, Pithecinae, and Atelinae. In the last revision, Schneider et al.
[2001] proposed an association among Aotus, Cebus, Saimiri, and Callithrichidae
(Callithrix, Sanguinus, Leontopithecus, Cebuella, and Callimico), with Aotus
being a basal lineage.
With the development of molecular cytogenetic tools, a large database of
comparative chromosome painting in New World monkeys (Platyrrhini, Primates) has accumulated in recent years (Cebus [Garcı́a et al., 2000; Richard et al.,
1996], Ateles [Garcı́a et al., 2002; Morescalchi et al., 1997], Lagothrix [Stanyon
et al., 2001], Saimiri [Stanyon et al., 2000], Callicebus [Barros et al., 2003;
Stanyon et al., 2000, 2003], Callithrix [Neusser et al., 2001; Sherlock et al., 1996],
Callimico [Neusser et al., 2001], Cebuella [Neusser et al., 2001], Saguinus [Müller
et al., 2001], Alouatta [Consigliere et al., 1996; de Oliviera et al., 2002], and
Leontopithecus [Gerbault-Serreau et al., 2004]), and has been used to infer the
ancestral Platyrrhini karyotype [Neusser et al., 2001]. However, some species
that are important for the delineation of the Platyrrhini phylogeny, especially
those belonging to subfamilies Aotinae (Aotus) and Pithecinae (Pithecia,
Chiropotes, and Cacajao), remain untested. In an attempt to clarify the
chromosomal relationships among Aotus species in relation to the rest of the
New World monkey species, human chromosome-specific paints have been used to
55
56
52
53;54
50
46
47;48
54
51#/52~
49#/50~
49#/50~
49#/50~
50–54
?
58
50
A. lemurinus lemurinusa
A. vociferansa
nancymaia,d
nigricepsa
azarae boliviensisa
azarae azaraea
infulatusa
trivirgatusa
miconaxa
hershkovitizib
sp.c,d
–
K-V
K-X; K-XI
K-I
K-VIII
K-VI
–
–
–
–
–
–
K-VIII
K-IX
K-IV
K-III; K-IV
Ma et al. [1976a]
nomenclature
KM
KM
KM
KM
KM
–
–
–
–
–
–
KM
KM
KM
KM
KM
7
7
3
4
5
1
1
2
2
6
Reumer and de Boer [1980]
nomenclature
KM
KM
KM
–
KM
–
–
KM
KM
8
9
10
3
4
5
KM 7
KM 6
KM 2
KM 1
Torres et al. [1998]
nomenclature
b
According to Hershkovitz [1983].
According to Ford [1994].
c
According to Torres et al. [1998].
d
Karyomorphs analyzed in this study.
e
1, Ma et al. [1978]; 2, Ma [1981]; 3, Pieczarka and Nagamachi [1988]; 4, Torres et al. [1998]; 5, Ma et al. [1976b]; 6, Brumback et al. [1971]; 7, Ma et al. [1980].
a
A.
A.
A.
A.
A.
A.
A.
A.
A.
A. brumbackia
A. l. griseimembraa
2n
Species
TABLE I. Summary Data Reported for Aotus Karyotypes
2,
2,
2,
3,
4
4
3,
4
4
4
3, 4, 5, 6
3, 4, 5, 7
3, 4, 5
4
2, 3, 4, 5
3, 4, 6
2, 3, 4, 5
1, 2, 3, 4
Referencee
ZOO-FISH in Aotus / 75
76 / Ruiz-Herrera et al.
delineate the homologous chromosomal segments present in Aotus. In this report,
for the first time, two Aotus KMs based on chromosome painting using human
probes are described. In addition, chromosome rearrangements between both
KMs are described, and the direction of chromosomal evolution in Aotus is also
discussed.
MATERIALS AND METHODS
Cell Cultures and Chromosome Preparations
Heparinized peripheral blood samples were taken from one male A.
nancymai (2n ¼ 54) and one male Aotus sp. (2n ¼ 50) from an uknown location
in Venezuela (Parque Zoológico Bararida, Barquisimeto). RPMI-1640, supplemented with phytohemagglutinin, pokeweed, 25% fetal bovine serum, Lglutamine, penicillin, streptomycin, heparin, and Hepes buffer were used for
the blood cultures. After 72 hr, colcemid (10 mg/ml) was added to the cultures for
the final 30 min. Cells were harvested and chromosomal preparations obtained
using standard protocols. Both specimens were chromosomally characterized
after sequential G-banding [Seabright, 1971] and C-banding [Sumner, 1972]. For
the chromosome assignment and numeration, we employed the cytogenetic
nomenclature revision published by Torres et al. [1998].
Fluorescence ‘‘In Situ’’ Hybridization (FISH)
Whole human chromosome paints (WCPs; provided by R. Stanyon) were used
for FISH on Aotus metaphases. Degenerate oligonucleotide primer PCR (DOPPCR) was performed as previously described [Stanyon et al., 2001] for the
labeling of DNA with Biotin and Tamra. For two-color FISH, we combined the
probes by mixing differently labeled WCPs and precipitating them with
competitor DNA (Cot-1 human DNA), salmon sperm DNA, ethanol, and 3M
sodium acetate overnight at –201C as previously described [Ruiz-Herrera et al.,
2004]. The precipitated mix was resuspended in 14 ml hybridization buffer,
denatured at 801C for 10 min and preannealed at 371C for 30 min. Chromosome
preparations were denatured in 70% formamide/2 SSC at 651C for 1 min, and
hybridization was performed at 371C for 72 hr. Post-hybridization washes were
performed in 50% formamide/2 SSC at 451C for 10 min, followed by three
washes in 2 SSC at 451C for 5 min. Chromosomes were counterstained with
DAPI and observed with an Olympus BX60 microscope equipped with a CCD
camera. Digital images were taken with the use of GENUS System software
(version 2.75; Applied Imaging Corporation, Santa Clara, CA). The G-banding
pattern was generated using the DAPI counterstain.
RESULTS
Karyotypes of Aotus Species
The Aotus sp. specimen studied has a diploid number of 2n ¼ 50, and
according to the cytogenetic analysis performed in the present study (sequential
G- and C-banding), this specimen corresponds to KM9 as described by Torres et
al. [1998]: 12 pairs of metacentric and submetacentric chromosomes, and 12 pairs
of acrocentric chromosomes (Fig. 1). The X chromosome is metacentric, whereas
the Y chromosome is acrocentric. Chromosome 13q shows an interstitial
heterochromatic band, whereas chromosomes 13–19, 21, and 22 have heteromorphic, heterochromatic small p-arms. In addition, chromosome 8 shows a
ZOO-FISH in Aotus / 77
Fig. 1. G-banded karyotype of Aotus sp. (KM9) showing the location of human chromosome
paintings. The Aotus chromosomes are numbered below, and the homologous human chromosomes
are numbered on the right. The bars located on the left of each chromosome represent the
heterochromatic regions, and the interrupted black bars on the right of chromosome 7 indicate the
location of NOR regions.
terminal heterochromatic band in the p-arm, whereas chromosome 11 shows a
pericentromeric, heterochromatic band. This KM, including the C-banding
pattern, was previously described by Torres et al. [1998] in a specimen of
unknown origin, and does not correspond to any Aotus species classified by
Hershkovitz [1983].
The A. nancymai specimen studied has a diploid number of 2n ¼ 54 and
corresponds to KM3 as described by Torres et al. [1998], which is equivalent to
karyotype I (K-I) described by Ma [1981] and Ma et al. [1976a], and to KM3
described by Reumer and de Boer [1980]. This karyotype has 11 pairs of
metacentric and submetacentric chromosomes, and 15 pairs of acrocentric ones
(Fig. 2). Whole heterochromatic p-arms were observed in chromosomes 12-15, 18,
19, and 21-23, as described by Torres et al. [1998]. The sexual chromosome pair
morphology is equivalent to that of Aotus sp.
FISH
Homologies between the chromosomes of two Aotus KMs and those of
humans were established (Figs. 1 and 2), and some examples of the chromosomal
syntenies are represented in Fig. 3. All human chromosome-specific painting
probes were hybridized on Aotus chromosomes, and the human chromosome Y
probe was the only one that failed in giving a hybridization signal.
78 / Ruiz-Herrera et al.
Fig. 2. G-banded karyotype of A. nancymai (KM3) showing the location of human chromosome
paintings. The Aotus chromosomes are numbered below, and the homologous human chromosomes
are numbered on the right. The bars located on the left of each chromosome represent the
heterochromatic regions.
Aotus sp. (KM9).
Figure 1 summarizes the hybridization results of WCPs on Aotus sp.
chromosomes. The hybridization results have allowed us to identify different
kinds of relationships between human and Aotus sp. chromosomes: 1) human
chromosomes (6, 12, 13, 14, 17, 18, 19, 20, 21, 22, and X) represented in one Aotus
sp. chromosome; 2) human chromosomes homologous to two Aotus sp. chromosomes (4, 8, 9, 10, 11 and 16); and 3) human chromosomes homologous to more
than two Aotus sp. chromosomes (1, 2, 3, 5, 7, and 15). The following chromosomal
associations were found in Aotus sp.: 1/3, 1/16, 2/12, 2/20, 3/21, 4/15, 5/7, 5/15, 7/
11, 8/18, 9/15, 10/11, 10/22, 14/15, and 16/22.
A. nancymai (KM3).
The hybridization results of WCPs on A. nancymai chromosomes are
summarized in Fig. 2. The human chromosome syntenies conserved in A.
nancymai are also detected in Aotus sp., except for human chromosome 17, which
is split into two different chromosomes. When the chromosomal associations are
analyzed, all of those found in Aotus sp. are conserved in A. nancymai, plus
associations 3/14 and 9/17 (Fig. 2).
Chromosome Homologies Between the Two Aotus Species
Based on G-banding comparisons and FISH results, the chromosomal
homologies between Aotus sp. (KM9, 2n ¼ 50) and A. nancymai (KM3, 2n ¼ 54)
have been established. The A. nancymai karyotype differs from that of Aotus sp.
by diverse intra- and interchromosomal rearrangements (Fig. 4). The
ZOO-FISH in Aotus / 79
Fig. 3. Examples of FISH using WCPs to metaphases of A. nancymai (KM3) (a–c) and Aotus sp.
(KM9) (d–f). a: Human chromosome 9 in green, and human chromosome 15 in red. b: Human
chromosome 3 in green, and human chromosome 21 in red. c: Human chromosome 7 in green, and
human chromosome 5 in red. d: Human chromosome 9 in red, and human chromosome 15 in green.
e: Human chromosome 3 in red, and human chromosome 21 in green. f: Human chromosome 7 in
green, and human chromosome 5 in red.
interchromosomal reorganizations detected were five fusion/fissions, implicating
KM9 chromosomes 4, 8, 13, 21, and 24. In addition, the G-banding comparisons
revealed the presence of some intrachromosomal reorganizations, with the most
likely interpretation of the reorganizations being one paracentric inversion to
homologue KM3 chromosome 4 with KM9 chromosome 5, and a centromeric shift
to homologue KM3 chromosome 9 with KM9 chromosome 20.
80 / Ruiz-Herrera et al.
Fig. 4. Presumed chromosome reorganizations between Aotus sp. (KM9) and A. nancymai (KM3)
based on chromosome comparative painting and G-banding comparisons. The dark bars located on
the side of each chromosome represent the heterochromatic regions. Inv: paracentric inversion. The
arrowheads indicate the centromere position, whereas the arrows follow the direction of the
reorganization.
DISCUSSION
The aims of the present work were to establish, for the first time, the
chromosome homologies between Aotus and human chromosomes based on
chromosome comparative painting, to contribute to the study of Aotus chromosome phylogeny, and to bring new data to the picture of Platyrrhini chromosome
evolution.
Implications for the Ancestral Platyrrhini Karyotype
Recent publications have inferred that the ancestral Platyrrhini karyotype is
that found conserved in Cebus apella and C. capucinus, which has a diploid
number of 2n ¼ 54 [Neusser et al., 2001]. One of the most informative methods for
interpreting comparative chromosome painting data is to analyze chromosomal
syntenies. Of the proposed ancestral chromosomal associations (2/16, 3/21, 5/7, 8/
18, 10/16, and 14/15), all were found in the Aotus KMs studied, except for 2/16 and
10/16 (Table II). In addition, some derived chromosomal associations were
detected in both KMs: 1/3, 1/16, 2/12, 2/20, 4/15, 5/15, 7/11, 9/15, 10/11, 10/22, and
16/22. Associations 3/14 and 9/17 were found only in A. nancymai.
Twelve human chromosomes (4, 6, 9, 11, 12, 13, 17, 18, 19, 20, 21, and 22) are
conserved without disruption in the putative ancestral Platyrrhini karyotype.
Eight of these (6, 12, 13, 18, 19, 20, 21, and 22) are also present in Aotus
karymorphs as an undisrupted chromosome segment. Regarding ancestral
chromosomes 4, 9, and 11, all are split into two different chromosomes in both
Aotus karymorphs (Figs. 1 and 2) and associated with other chromosomes,
ZOO-FISH in Aotus / 81
TABLE II. Chromosomal Homologies Detected by Comparative Chromosome Painting
Between Aotus Species and Those of Human With Respect to the Ancestral karyotype of
New World Monkeys (NWM)n
Ancestral NWM karyotype
1a
1b
1c
16b/2b
2a
3b
3a/21
3c
4
7a/5
6
7a/5
7b
8a/18
8b
9
10b
16a/10a
11
12
13
14/15
Aotus sp. (KM9)
Aotus nancymai (KM3)
1a
1b/3a/21
1c/16b
12/2b
20/2a2
2a1
3b
1a
1b/3a/21
1c/16b
12/2b
20/2a2
2a1
3b
3b/14/15/14
1/3a/21
3c
4c1
(4a+4b+4c2)/15/5b
10b/11b/7a/5a
(4a+4b+4c2)/15/5b
5b/15
6
10b/11b/7a/5a
7b
7b
8a/18
8b
15/9a/17b
9b/15
10b/11b/7a/5a
16a/22/10a
10b/11b/7a/5a
11a
12/2b
13
3b/14/15/14
5b/15
9b/15
15/9a/17b
(4a+4b+4c2)/15/5b
14/15
16a/22/10a
16b/1c
15/9a/17b
17a
8a/18
19
20/2a2
3a/21
16a/22/10a
X
1/3a/21
3c
4c1
(4a+4b+4c2)/15/5b
10b/11b/7a/5a
(4a+4b+4c2)/15/5b
5b/15
6
10b/11b/7a/5a
7b/11a
7b
8a/18
8b
9a/15
9b/15
10b/11b/7a/5a
16a/22/10a
10b/11b/7a/5a
7b/11a
12/2b
13
15/14/15/14
5b/15
9b/15
9a/15
(4a+4b+4c2)/15/5b
16a/10a
16b/2b
17
16a/22/10a
16b/1c
17
8a/18
19
20
3a/21
22
X
8a/18
19
20/2a2
3a/21
16a/22/10a
X
n
The alphabetic denomination a, b and c corresponds to the primate ancestral segments homologous to human
chromosomes described in Ruiz-Herrera et al. [2005]. In the case of the homologues to human chromosomes 11
and 17, a represents the human p-arm whereas b corresponds to the human q-arm. Aotus chromosomes
homologous to 5b, 7b, 14 and 15 are split into different chromosomes.
82 / Ruiz-Herrera et al.
whereas ancestral chromosome 17 is split into two different chromosomes only in
A. nancymai (Table II).
When comparing our results with previous reports, an important feature to
consider is that two of the Platyrrhini ancestral associations common to New
World monkeys (2/16 and 10/16) are absent in both Aotus species studied. In the
case of ancestral association 2/16, the lack of this synteny has also been observed
in Callithrix jacchus [Neusser et al., 2001] and in the presumed ancestral
karyotype of Alouatta [Consigliere et al., 1996; de Oliviera et al., 2002]. The
separation of association 2/16 in these three different phylogenetic lineages
indicate a convergence of independent fission events. In contrast, and in light of
the hybridization results, Aotus is the only New World monkey in which
association 10/16 has been interrupted by, in this case, the insertion of human
homologous chromosome 22. Thus, the lack of association 10/16 would be
considered a derived characteristic of the Aotus genus. It seems that ancestral
chromosome 16 has undergone a different evolutionary history, being associated
with different chromosomes (16/22/10 and 2/16), with respect to the rest of the
Platyrrhini species studied so far. By analyzing previous cytogenetic studies in
Aotus, we found that the morphology of the chromosomes that contain association
16/22/10 (KM9 chromosome 3 and KM3 chromosome 3), and the chromosomes
that contain the association 2/16 (KM9 chromosome 9 and KM3 chromosome 8)
have been conserved in other Aotus KMs [Ma, 1981; Torres et al., 1998],
suggesting an ancestral characteristic of Aotus.
The derived associations of New World monkeys homologous to human
chromosomes 1/3, 2/12, 4/15, and 10/11 are also present in Atelinae, Cebidae, and
Callithrichidae. However, some aspects must be taken into account. The 1/3
association has also been found in Callicebus lugens [Stanyon et al., 2003] and
Callimico goeldii [Neusser et al., 2001], but it seems that these 1/3 associations do
not represent the same segments of chromosome 3. Considering the ancestral
New World monkey karyotype, and based on G-banding comparisons, Callimico
goeldii would present the association 1b/3c, whereas Aotus species have the
association of different segments: 1b/3a/21 (Table II). Thus, although Callimico
goeldii and Aotus share the 1/3 association, it seems that the translocations are
not the result of the same event. In the case of Callicebus lugens, although the
authors [Stanyon et al., 2003] do not provide any karyotype with which to
compare it, it seems that neither corresponds to the case of Aotus.
Association 2/12 is present only in the most cytogenetically derived titi
monkeys, Callicebus lugens [Stanyon et al., 2003]. In this case, there is
insufficient information to define the segments involved in the association.
Both of the Aotus KMs analyzed in this study share association 4/15 with
Atelinae species (Lagothrix lagothricha [Stanyon et al., 2001], Ateles [Garcı́a et al.,
2002; Morescalchi et al., 1997], and Alouatta [Consigliere et al., 1996; de Oliviera
et al., 2002]). However, in contrast to what occurs in all Platyrrhini species
studied, ancestral chromosome 15 has undergone a huge number of translocations in the Aotus karyotypes (Table II).
The fragments involved in association 10/11 appear to be the same in the
Aotus and Callicebus species studied so far (10b/11). This 10/11 association is
presumably ancestral for all Callicebus [Stanyon et al., 2003]. Therefore, the
presence of the derived association 10/11 in Callicebus and Aotus can be
considered a landmark that relates Aotus and Callicebus phylogenetically. This
fact would support the hypotheses of Ford [1986] and Rosenberger [1984], which
closely relate Callicebus and Aotus. Nevertheless, in the light of our comparative
chromosomal results, we are not able to conclude that Aotus has a basal position
ZOO-FISH in Aotus / 83
in the Platyrrhini phylogenetic tree. On the contrary, Aotus species would have a
derived chromosomal history, with respect to the putative New World monkey
ancestral karyotype. Further comparative studies including more Aotus species
and the subfamily Pithecinae would be extremely useful for discarding either
Rosenberger’s or Ford’s hypothesis, and clarifying the final position of these
Platyrrhini species.
Mechanisms and Direction of Chromosomal Evolution in Aotus
In the present study, the chromosomal reorganizations detected between the
two Aotus KMs are predominantly fusion/fission events, as also happens in
Cercopithecus and Alouatta [Consigliere et al., 1996; Ponsà et al., 1986]. This fact
contrasts with what occurs in other Primate phylogenetic branches. For instance,
in Cebus and Ateles genera, the most frequent rearrangements are inversions
[Garcı́a et al., 2002].
After they compared nine different karyotypes, Ma et al. [1981] postulated
that the putative ancestral Aotus would show a karyotype of 2n ¼ 54, which would
correspond to the A. nancymai KM (KM3) studied in the present work. However,
the data obtained with the use of human chromosome probes revealed some
support for the hypothesis that KM9 shares more ancestral chromosome
characteristics with the putative New World monkey ancestral karyotype than
does KM3. Based on our chromosome painting results, both KMs differ due to a
different signal distribution of WCPs from human chromosomes 3, 14, 15, and 17,
which are the result of interchromosomal reorganizations.
Human chromosome 3 is represented as three different chromosomes in the
ancestral Platyrrhini karyotype (3a/21, 3b, and 3c; Table II). The Aotus
chromosomes homologous to ancestral chromosome 3b are different in both
KMs; that is, KM9 has maintained the ancestral form as one whole chromosome
(chromosome 8; Fig. 1), whereas within KM3 this chromosome has a derived
state, as two different chromosomes (chromosomes 14 and 18; Fig. 2).
Regarding chromosomes homologous to HSA 14 and 15, the situation is more
complex. As has been reported in other Platyrrhini species, although association
14/15 is always present, in some cases (e.g., the Saimiri and Cebus species) it has
undergone intrachromosomal reorganizations, such as inversions [Garcı́a et al.,
2002]. Nevertheless, the case of Aotus is quite different because human
chromosome 15 is split into five and six different chromosomes in KM9 and
KM3, respectively (Table II). This feature supports the highly derived situation of
Aotus regarding the ancestral New World monkey karyotype.
Concerning human chromosome 17, in KM9 one whole chromosome is
homologous to HSA 17 without any disruption (chromosome 21), whereas in KM3
the ancestral chromosome 17 is split into two different chromosomes (chromosomes 6 and 26). The situation present in KM9 is also conserved in all Platyrrhini
species analyzed thus far.
In addition, revising the classic cytogenetic data, Aotus karyotypes K-III, KV, K-VI, and K-VII [Ma, 1981] share the same chromosome morphology for
chromosomes homologous to KM9 chromosome 5. In KM3, chromosome 4 shows a
derived morphology, which differs from those mentioned above, by a paracentric
inversion (Fig. 4).
Although we studied only two different Aotus KMs, we consider the most
parsimonious hypothesis to be that which considers KM3 a more derived
karyotype than KM9 with respect to the ancestral Platyrrhini karyotype.
84 / Ruiz-Herrera et al.
Nevertheless, further studies based on comparative chromosome painting with
different Aotus KMs are required before any hypothesis can be rejected.
ACKNOWLEDGMENTS
The authors are grateful to R. Stanyon for providing the human chromosome
probes, A. Exposito for technical assistance, and the Zoological Garden Bararida
(Barquisimeto) of Venezuela for supplying blood samples. This study was
supported in part by a grant from the Universitat Autònoma de Barcelona to A.
Ruiz-Herrera. The English in this manuscript was revised and corrected by an
instructor of English at our university.
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