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Cytogenetic analysis shows extensive genomic rearrangements between red howler (Alouatta seniculus Linnaeus) subspecies.

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American Journal of Primatology 35171-183 (1995)
RESEARCH ARTICLES
Cytogenetic Analysis Shows Extensive Genomic
Rearrangements Between Red Howler (Alouatta
seniculus, Linnaeus) Subspecies
R. STANYON'.. S.
- TOFANELLI'. M.A. MORESCALCHI'. G. AGORAMOORTHY3.
O.A. RYDER4, AND J. WIENBERG'
~~
'Institute of Physical Anthropology, university of Genoa, Genoa, Italy; 2Znstitute of
Anthropology, University of Florence, Italy; 3Conseruation a n d Research Center, National
ZooloPical Park, Smithsonian Institution, U.S.A.; *Center for Reproduction ofEndanpered
Speci&, Zoological Society of Sun Diego, U.S.A.; 51nstitute. for Anthropology a n d Human
Genetics, University of Munich, Germany
A comparison of the G-banded karyotypes of two red howler subspecies,
Alouatta seniculus arctoidea and A. s. sara, showed that they differed by at
least 14 chromosomal rearrangements. Genomic reshuffling is so great
that homologs between subspecies could not be found for some chromosome, while the assignment of homology for other chro'mosomes remains
uncertain. The two red howlers, however, share a n unusual X,X,Y lY2/
XlXlX2X, sex-chromosome system that resulted from a Y-autosome translocation, probably in a common ancestor. The great chromosomal variability resulting from rapid chromosomal evolution in howlers indicates that
cytogenetic data could make an important contribution to resolving phylogenetic and conservation problems in this group of highly conspicuous
New World Monkeys. o 1995 Wiley-Liss, Inc.
Key words: new world monkeys, platyrrhini, phylogeny, speciation,
chromosomes, Y-autosome translocation
INTRODUCTION
Cytogenetic studies of New World primates (Playtrrhini) have demonstrated
that karyological data can provide essential evolutionary information for primatologists and taxonomists. Chromosomal studies of the genus Alouatta (howler
monkeys) have revealed an unexpected amount of variability both between and
within traditionally recognized species. However, considering th a t howler monkeys are highly conspicuous with the widest geographic distributions of any neotropical monkey, cytogenetic reports are few and far from complete. There is no
information for some recognized species and karyological description of subspecies
are wholly inadequate.
The genus is traditionally divided into six species: Alouatta belzebul, A. caraya, A. fusca, A , palliata, A . pigra, and A . seniculus. Their distribution runs from
Received for publication January 24, 1994; revision accepted J u n e 14, 1994.
Address reprint requests to R. Stanyon, Institute of Physical Anthropology, University of Genoa, Via
Balbi 4, Genoa, Italy.
0 1995 Wiley-Liss, Inc.
172 I Stanyon et al.
southern Mexico to northern Argentina, including parts of Peru and Bolivia [Hill,
1960; Wolfheim, 19831.
Karyological studies even before the introduction of banding methods suggested that howler monkeys were karyologically variable [Chu & Bender, 1961;
Bender & Chu, 1963; Egozcue & Egozcue, 19661. This karyological variability was
confirmed when chromosomal banding methods were used to study the several
species of the single subfamily genus, Alouatta [Koiffmann & Saldanha, 1974; Ma
e t al., 1975; Yunis e t al., 1976; Armada et al., 1987; Lima & Seuanez, 1989, 19911.
Briefly, diploid numbers in these monkeys range from 2n = 43 to 2n = 54, and
fundamental numbers (FNs, number of chromosome arms) go from 56 to 76. The
number of NOR (nucleolar organizing region) bearing chromosomes has been reported as 2 (A. seniculus stramineus, A. belzebul nigerrima), 6 (A. belzebul belzebul),or 8 ( A . belzebul) [Armada et al., 1987; Lima & Seuanez, 1989, 19911. Howler
monkeys also have unusual karyological traits such as microchromosomes and
various Y-autosome translocations.
Alouatta seniculus (red howler) has previously been the subject of five research
reports: two reports used classical staining [Chu & Bender, 1961; Bender & Chu,
19631 while the other three employed banding techniques [Yunis et al., 1976;
Minezawa et al., 1985; Lima & Seuanez, 19911. If we accept the division of A.
seniculus into 9 subspecies [Hill, 1960; see Fig. 11, then there have been reports on
4 subspecies: A. s. seniculus [Chu & Bender, 1961; Bender & Chu, 1963; Yunis et
al., 19761,A. s. stramineus [Lima & Seuanez, 19911,A. s. macconnelZi [Lima et al.,
19901, and A. s. Sara [Minezawa et al., 19851. In red howlers, the diploid numbers
vary from 43 to 51 and FNs vary from 56 to 76. Various sex chromosome systems
have been reported: the typical mammalian XY/XX (male/female) sex determination system, and a number of Y-autosome translocations.
Here we present the first cytogenetic data for A. seniculus arctoidea and compare these chromosomes with those of A. s. Sara. Both subspecies present Y-autosome translocations and a n identical X,X,Y 1Y2/X,X,X,X2 (male/female) sex determination system. However, their karyotypes are surprisingly different.
MATERIALS AND METHODS
The Alouatta seniculus arctoidea (ASA) samples consisted of four heparinized
blood draws that were taken immediately after capture at Mato Masaguaral
(8'31" 67'35'W), Estado Guarico, Venezuela, from two males and two females.
The samples were hand-carried to the Institute of Anthropology, Florence, Italy,
where standard whole-blood cultures were established [Small et al., 19851. The
tissue culture consisted of 0.3 ml of whole blood inoculated into 8 ml of tissue
culture medium (RPMI 1640,15% FCS, 50 ug/ml Concavalin-A type I11 [SIGMA]).
After 90 hours of culture a t 38.5"C, colcemid (0.05 ug/ml) was added for 60 minutes.
The cultures were then harvested according to standard methods (hypotonic treatment with 0.075 M KC1 for 15 minutes and fixation in methanol: acetic acid).
Fibroblasts from a single male Alouatta seniculus Sara (ASS) were established
by traditional methods. This A . s. Sara was captured from the wild in Bolivia and
purchased by the San Diego Zoo from World Wide Primates. The cells were cultured in DMEM supplemented with 10% fetal bovine serum. Cell harvesting was
a s previously reported [Stanyon & Galleni, 19911.
Chromosome spreads were banded as follows: G-banding with trypsin according to Small et al. [1985], C-banding according to Sumner 119721, Ag-NOR banding
according to Goodpasture and Bloom [1975]. The Ag-NOR preparations were sequentially G-banded with trypsin to identify the NOR bearing chromosomes.
To aid comparisons between individuals and subspecies, photographic enlarge-
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Fig. 2. a: Shows the G-banded karyotype and b: Shows the idiogram of Alouatta seniculus arctoidea (ASA).
The asterisks in the idiogram show the location of nucleolar organizing regions (NORs).
RESULTS
G-banded Karyotypes of Alouatta seniculus arctoidea
Figure 2a shows the G-banded karyotype and 2b shows the idiogram of ASA.
The two male ASAs had a diploid number of 2n = 45, while the two females had
a diploid number of 44. The difference in diploid numbers was due to microchromosomes (four in the females and five in the two males). Therefore, the diploid
number of both sexes, if microchromosomes are not considered, is 40.
The fundamental number (FN) of both males is 58 (10 biarmed chromosomes,
26 acrocentric autosomes, 4 microchromosomes, and 4 sex chromosomes (the Xs are
biarmed, while one Y is acrocentric and the other is submetacentric)).The fundamental number for females is also 58 due to the fact that our two females had one
less microchromosome. If microchromosomes are not considered, then the FN is 53
in males and 54 in females.
Sex chromosome system. The male sex chromosome complement can be
described a s X,X,Y,Y, and the female complement a s X,X,X,X,. The X, is a
typical primate X-chromosome, while X, was originally a submetacentric autosome. The Y, chromosome is a borderline submetacentric while Y, is a n acrocentric. The Y, derives from the q arm of the same autosome as X,, and Y, is the
translocation product of the original Y chromosome with the p arm of this autosome.
G-banded Karyotypes of Alouatta seniculus Sara
Figure 3a shows a G-banded karyotype and 3b the idiogram from ASS. The
single male ASS had a diploid number of 2n = 50 and a FN of 67 (14 biarmed and
28 acrocentric autosomes, 4 microchromosomes and 4 sex chromosomes (the Xs are
biarmed, while 1 Y is acrocentric and the other is submetacentric)). The sex chromosome system was the same as in ASA. If microchromosomes are not considered
then the diploid number is 46 and the FN = 63.
Sequential G and AG-NOR Staining
In ASA, three chromosome pairs show AG-NOR banding. One NOR is located
on the short arm of chromosome 3 next to the centromere. Another NOR is located
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176 I Stanyon et al.
Fig, 3. a: Shows the G-banded karyotype and b: Shows the idiogram of Alouatta seniculus Sara (ASS).
The asterisks in the idiogram show the location of nucleolar organizing regions (NORs).
a t the centromere of the medium acrocentric chromosome (n 9) and is polymorphic
with Ag-NOR staining. Finally, a small acrocentric pair of chromosomes (n 17)
shows a polymorphism for the NOR location. The NOR can be located either at the
centromere or a t the terminal part of the long arm (see Fig. 4).
In ASS, two pairs of biarmed chromosomes showed NORs: n 9 and n 20 (Figure
4). There is a polymorphism for the size of the NOR regions, but not for position as
in ASA.
Comparison of Karyotypes in A. s. arctoidea and A. s. Sara
A comparison of diploid and fundamental numbers makes i t clear that these
two howlers have quite distinct karyotypes: 2n = 44, 45, FN = 58 in A. s. arctoidea, and 2n = 50 and FN = 67 in A . s. Sara. If microchromosomes are not
included in the diploid numbers would be 40 and 46 respectively. On the basis of
G-banding, homologs between the chromosomes of the two red howlers can be
proposed for a majority of the chromosomes with the exception of ASA18 and
ASS13. However, it must be noted that the homologies proposed are working
hypotheses that need to be verified by molecular methods. In some cases more than
one hypothesis could be proposed, with one author or another favoring alternate
solutions. Here we present only one set of proposals (Fig. 5).
Whole chromosomal homologs. There are very close if not identical banding patterns between chromosomes ASAIASS: 4 5 , 9/8,11/14, 16/12, 17/20, and the
sex chromosomes. A paracentric inversion apparently has occurred between ASA
8 and ASS 7. ASA 14 appears similar to ASS 17 except for the location of the
centromere. Other proposed homologs are not as clear cut: ASA13 could derive
from ASS11 by a pericentric inversion; ASAl2 may differ by a paracentric inversion from ASS18.
Homologs involved in translocations. Two clear Robertsonian translocations have occurred between ASA and ASS: Chromosome ASAlp is homologous to
ASS4 while ASAlq is homologous to ASS3; ASA l o p = ASS21 and ASAlOq =
ASS19. Additionally, there appears to have been 7 tandem translocations: ASA2p
and a small part of the long arm next to the centromere derive from ASSlp, the
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178 I Stanyon et al.
Fig. 4. A The sequential NOR and trypsin G-banding of NOR bearing chromosomes in Alouatta seniculus
arctoidea (ASA); B: A partial metaphase from Alouatta seniculus Sara (ASS) after sequential NOR and G-banding. The arrows point to the NORs.
remainder of the long arm is composed of ASS10 and ASS6; ASA3p and the 3q next
to the centromere is composed of ASS9 while most of the long arm is homologous
to ASSlq; ASA5 may derive from ASS16 and ASS23; ASA7 may derive from
ASS15 and ASS22. Finally, ASS2 may derive from a fusion of ASA6 and ASA15.
NOR-bearing chromosomes. We found six NOR-bearing chromosomes in
ASA and four in ASS. If the between taxon homologs are correct then four NORs
were derived from a common ancestor: NORs on ASA31ASS9 and ASA171ASS20.
There are additional NORs on ASA9 not present in ASS.
DISCUSSION
Our results confirm that howler monkeys have high karyological variability.
However, the extent of differences we revealed between supposed subspecies of red
howlers was beyond that expected. The number of chromosomal mutations is impressive. A conservative estimate would include: 9 translocations (2 Robertsonian
translocations, 7 tandem translocations); 4 intrachromosomal rearrangements (1
pericentric inversion and 3 paracentric inversions); a n additional NOR site in
ASA; a number of unidentified changes to account for the chromosomes for which
no homologs were found, ASA18 and ASS13.
Sex Chromosome System in Howlers
On the other hand, both subspecies have apparently conserved a n unusual
X,X,Y ,Y,/X,X,X,X,
sex-chromosome system. An identical system has been reported for some other red howler subspecies, A. seniculus stramineus and A . s.
macconnelli, and the published chromosomes appear to have very similar banding
patterns to the sex chromosomes of our two “subspecies.” In this previous report
Red Howler Subspecies Genomic Rearrangements / 179
Fig. 5. A comparison of Alouatta seniculus arctoidea (ASA) and A. s. Sara (ASS) G-banded chromosomes. The
homologies proposed here are one set of working hypotheses. The ASA chromosomes are numbered below in bold
numbers and the ASS chromosomes are numbered to the side.
the Y-autosome translocation was confirmed by meiotic studies [Lima & Seuanez,
19911. However, the only prior report on A. s. Sara proposed a Y-autosome translocation which resulted in a X,X,Y/X,X,X,X, sex-chromosome system. The Y was
a large acrocentric that resulted from a n insertion of the Y with a n autosome; male
and females differed in chromosome number 46 in females and 45 in males (if
microchromosomes are not counted). Our single male had, not counting microchromosomes, 46 chromosomes. However, we were not able to directly compare banding
patterns with the A. s. Sara previously published and it is unclear if any other
difference exists between these samples.
A. seniculus seniculus has been reported to have a normal mammalian XYIXX
sex chromosome system [Yunis et al., 19761. However, Y-autosome translocations
have been reported for other howler species: A. palliata [Ma et al., 19751;A. fusca
clamitans [Lima & Seuanez, 19911; A. belzebul belzebul with a X,X,Y/X,X,X,X,
system [Armanda et al., 19871.
In primates, Y-autosome translocations are rare. In catarrhines there is only
one report [Presbytis cristatus, Dutrillaux et al., 19841. In platyrrhines there have
been a number of reports of Y-autosome translocations in several species (i.e., in
Aotus triuirgatus [Ma et al., 19761; Cacajao caluus rubicundus [Dutrillaux et al.,
19861, C . melanocephalus [Koiffmann & Saldanha, 19813), and Callimico goeldii
[Seuanez et al., 19891. There are no reports on Y-autosome translocations in prosimians.
Microchromosomes
Red howlers, including our samples of A . seniculus arctoidea and A. s. Sara, are
all distinguished by having microchromosomes (MCs). This cytogenetic trait is
180 I Stanyon et al.
unknown in other monkeys, including other howler species, but i t is common in
lemurs [Rumpler & Dutrillaux, 19861.
The difference in the number of MCs between males (5) and females (4) in our
sample of ASA is probably more apparent than real. We studied only two individuals from each sex and further studies with larger samples are needed to establish
the actual variability in the number of MCs in ASA. Previous reports (cited above)
show that the number of MCs in red howlers may vary from one to five. However,
it is clear that the MCs are responsible for the major part of the variability in
diploid numbers within red howler populations. If MCs are not considered the
diploid numbers in A. seniculus range from 40 to 46. On this basis Columbian
populations of A. s. seniculus (40) are closest to the Venezuelian populations of A .
s. arctoidea (401, while the other populations of A . seniculus (A. s. Sara, A . s.
stramineus, A. s. macconelli) studied so far all have a diploid number of 45 or 46.
The similarity in diploid numbers, however, may hide profound karyological differences. Studies using banding methods should be used to compare various subspecies and local populations.
The origin and significance of the MCs is not known. The within population
variability in the number of MCs in red howlers, suggests that they contain little,
if any, essential genetic information. Future research is needed to determine if
they are composed of repetitive DNA sequences (i.e., late replication heterochromatin). Theoretically, MCs could be produced during Robertsonian translocations,
but they are then usually lost [King, 19931. The presence of MCs in red howlers
may indicate that their origin is recent.
Significance of the Cytogenetic Variability Within AZouuttu seniculus
The cytogenetic differences shown between A. s. arctoidea and A . s. Sara are
more typical of differences seen between species belonging to different genera. For
example, the differences in karyotypes are greater than those found between humans and any great ape [Stanyon, 19921. It is most likely that the cytogenetic
differences that separate the two red howler “subspecies” are sufficient to insure
reproductive isolation.
Minezawa et al. [1985] state that a t least 10 chromosomal rearrangements
separate A . s. Sara (2n = 45,46 not counting MCs) from A. s. seniculus (2n = 401,
and this is in line with the difference we found between A. s. Sara (2n = 46) and
A. s. arctoidea (2n = 40). Armanda e t al. [1987] in their original report on Alouatta
belzebul belzebul (2n = 49, 50) and A . b. nigerrima (2n = 50) report that the
karyotypes were “drastically different”: no homologs were found for four chromosome pairs in each subspecies. Although Lima et al. [1990] describe the karyotype
of A. s. macconnelli (2n = 46) and Lima and Seuanez [19911 present chromosomal
data from A . s. stramineus (2n = 46), outside of the sex chromosomes, there is no
direct comparison of these two red howlers. Lima and Sueanez [1991] do state,
however, that these two species are more similar to each other more than either is
to A. s. seniculus or to A . s. Sara.
Taxonomic implications. The most obvious implication of the marked karyological variability in red howlers is that i t would be worthwhile to investigate
with a fuller range of criteria, the taxonomic status of A. seniculus “subspecies”
[Minezawa et al., 1985; Lima & Seuanez, 19911. The conservation implications are
clear: as for other organisms in tropical forest regions, i t is probable that the
biological diversity and number of species have been underestimated.
The use of cases of rapid karyological evolution for phylogenetic studies. A second significance of the chromosome data is that the variability between
howler species and “subspecies” indicates that the karyotype in these primates has
Red Howler Subspecies Genomic Rearrangements / 181
evolved rapidly. It is well appreciated that rapidly evolving systems permit high
phylogenetic resolution. However, counting this report, only five of the nine seniculus “subspecies” have been examined, unfortunately in most cases by different
workers using different methods with a bare minimum of comparisons. It is probable that cytogenetic data in howlers could provide significant evolutionary information and help clarify how chromosomes are related to population divergence and
speciation. Clearly, i t would be worthwhile to study cytogenetically additional
howler species, “subspecies”, and populations, preferably sampled from the wild.
Possible general implications for platyrrhine evolution. In general, New
World monkeys appear to be karyotypically variable. In squirrel monkeys
(Saimiri) three different pericentric inversions have distinct geographic distribution among subspecies [Jones et al., 1973; Moore e t al., 19901. Within and between
the various species and subspecies of Ateles four different pericentric inversions
can be found [Kunkel et al., 1980; de Boer & de Bruijn, 19901. Subspecies of Ateles
paniscus (A.p . paniscus, 2n = 32, and A . p . chamek, 2n = 34) differ by a probable
tandem fusion and two pericentric inversions [de Boer & de Bruijn, 19901. Among
primates, the howler cytogenetic situation most closely resembles that of the owl
or night monkeys, genus Aotus [Brumback et al., 1971; Reumer & de Boer, 1980;
Ma, 1981; Galbreath, 1983; Hershkovitz, 1983; Ma e t al., 19851. This genus is one
of the most karyotypically diverse genera of mammals and there are 14 karyotypically definable populations [Ma et al., 19911. It is probable that when howler
monkeys are better known they will prove to be a t least, if not more, karyotypically
differentiated than the owl monkeys.
Hypotheses can be developed to help explain why New World monkeys and
especially Aotus and Alouatta are so chromosomally variable. One hypothesis is
that chromosomal differentiation occurred as a result of isolation in forest refugia
during the quaternary [Ma, 1981, 1976; Kunkel e t al., 19801. Chromosomal mutations would have been more easily fixed due to inbreeding among small groups
of isolated monkeys [Ma, 19801. A . seniculus is a forest monkey and can be found
in a range of forest habitats including small isolated patches. Even when other
species of primates have disappeared because of deforestation, the red howlers are
found occupying the last isolated stands of timber [Wolfheim, 19831. The fact that
two different subfamilies have undergone extensive genomic rearrangements may
suggest a common cause and similar adaptive capacities. Since chromosomal variability is still found within populations, it is an open question whether the karyological transformation process is punctuated or still taking place.
On the other hand, the striking karyological diversity in both Aotus and A l ouatta may be more apparent simply because traditional taxonomic methods based
on morphology, especially pelage, have not been sufficient to recognize the real
biological divisions and diversity of South American primates. Clearly, taxonomic
and phylogenetic decisions must attempt to explain and integrate all available
data, including the chromosomes.
CONCLUSIONS
1. We found that the karyotypes of two “subspecies” of red howlers were surprisingly different. Alouatta seniculus arctoidea had a diploid number of 2n = 44,
45 with a fundamental number (FN) of 58. A . seniculus Sara had a diploid number
of 2n = 50 with a FN = 67.
2. A conservative estimate of chromosomal rearrangements between these two
red howlers would include nine translocations and four inversions, but homologs
could not be proposed for several chromosomes. Further, work using molecular
182 I Stanyon et al.
methods, particularly in situ hybridization, will be needed to completely define the
differences between karyotypes.
3. On the other hand, these two seniculus taxa are both characterized by unusual cytogenetic traits, such as microchromosomes and a XlX,Y,Y,/X,XlX2X,
sex-chromosome system (resulting from a Y -autosome translocation), that were
probably inherited from a common ancestor.
4.The variability between howler species and “subspecies” indicates that the
karyotype in these primates has evolved rapidly and that cytogenetic data in
howlers could help clarify how chromosomes are related to population divergence
and speciation. It is most likely that the cytogenetic differences that separate the
two red howler “subspecies” are sufficient to insure reproductive isolation. It would
be worthwhile to have more complete cytogenetic data on Alouatta, in part because
rapidly evolving systems permit high phylogenetic resolution.
5. Taxonomic and phylogenetic decisions must attempt to explain and integrate all available data, including the chromosomes.
ACKNOWLEDGMENTS
R.S. and M.A.M. thank the director and personnel of the Institute of Comparative Anatomy, University of Genoa, for access to the institute’s facilities. The
authors also thank the three unnamed reviewers for valuable suggestions. This
research was funded in part by the MURST 60% Grants, 1992.
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extensive, rearrangements, cytogenetic, howler, red, linnaeus, analysis, subspecies, alouatta, genomics, seniculus, show
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