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Atelinae phylogenetic relationships The trichotomy revived.

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Atelinae Phylogenetic Relationships: The
Trichotomy Revived?
A.C. Collins*
Department of Anthropology, University of Wisconsin, Madison, Wisconsin 53706, and Department of Conservation
Biology, Daniel F. and Ada L. Rice Conservation Biology and Research Center, Brookfield Zoological Institution,
Brookfield, Illinois 60513
taxonomy; cladistics; systematics; molecular; Atelini; Cebidae; Platyrhinne
This research examines phylogenetic relationships between members of the Atelinae subfamily
(Alouatta, Ateles, Brachyteles, and Lagothrix), based on
analysis of three genetic regions. Two loci, cytochrome c
oxidase subunit II (COII) and the hypervariable I portion
of the control region, are part of the mitochondrial genome. The other is a single-copy nuclear gene, Aldolase A
Intron V. Analysis of these genetic regions provides support for tribe Alouattini containing the Alouatta species,
while tribe Atelini contains the other three genera. However, these three genetic regions produce conflicting results for relationships among tribe Atelini members. Previous genetic studies supported grouping Brachyteles with
Lagothrix, leaving Ateles in a separate subclade. The
present data sets vary based on the genetic region analyzed and method of analysis suggesting all possible cla-
distic relationships. These results are more consistent
with investigations of morphology and behavior among
these primates. The primary cause of discrepancy between
this study and previous genetic studies is postulated to
reside in increased sampling in the present study of genetic variation among members of the Atelinae, specifically Ateles. The present study utilized samples of Ateles
from all postulated species for this genetically variable
primate, while previous studies used only one or two species of Ateles. This paper demonstrates that shifting relationships are produced when different species of Ateles are
used to reconstruct phylogenies. This research concludes
that a trichotomy should still be supported between members of tribe Atelini until further analyses, which include
additional Atelinae haplotypes are conducted. Am J Phys
Anthropol 124:285–296, 2004. © 2004 Wiley-Liss, Inc.
Most authors agree that the genera Alouatta
(howler monkeys), Ateles (spider monkeys),
Brachyteles (woolly spider monkeys, or muriqui),
and Lagothrix (woolly monkeys) are monophyletic
descendants of a single common ancestor, constituting the subfamily Atelinae (Dunlap et al., 1985;
Ford, 1986; Rosenberger and Strier, 1989; Kay,
1990; Paterson, 1991; Strier, 1992; Ford and Davis,
1992; Schneider et al., 1993; Harada et al., 1995;
Schneider and Rosenberger, 1996; Canavez et al.,
1999; von Dornum and Ruvolo, 1999; Meireles et al.,
1995, 1999). Early taxonomists grouped the members of the Atelinae together primarily on the basis
of their unique prehensile tail (Gray, 1870). Comparison of these genera shows that they all share a
number of morphological traits, including: 1) large
body size (Brachyteles is the largest Platyrrhine), 2)
a prehensile tail with ventral grasping surfaces, and
3) frequent suspensory behaviors (Rosenberger and
Strier, 1989; Ford and Davis, 1992). In most other
aspects they display a wide array of morphological
and behavioral traits (Rosenberger and Strier, 1989;
Strier, 1992). Members of the Atelinae are the most
geographically widespread subfamily among all
New World primates, ranging from southern Mexico
to the Uruguayan-Brazilian border (Rosenberger
and Strier, 1989; Rowe, 1996). See Figure 1.
Morphological studies arranged the three genera
of tribe Atelini (Ateles, Brachyteles, and Lagothrix)
in every possible taxonomic relationship (Dunlap et
al., 1985; Ford, 1986; Rosenberger and Strier, 1989;
Kay, 1990; Ford and Davis, 1992; Strier, 1992), suggesting a trichotomous relationship between the
three genera. Cytogenetic research of tribe Atelini
does not completely resolve this issue. Chromosomal
evolution (Dutrillaux, 1979) suggests Ateles and
Lagothrix are sister taxa; however, comparison of
chromosome number and implied amount of rearrangement would support Brachyteles and Lagothrix as more closely related genera (Koiffman and
Grant sponsor: Chicago Zoological Society; Grant sponsor: Institute
of Museum and Library Services; Grant number: 1C-40190-94; Grant
sponsor: Sigma Xi.
*Correspondence to: A.C. Collins, Department of Anthropology,
125A Sabin Hall, 3413 N. Downer Ave., University of Wisconsin,
Milwaukee, WI 53211. E-mail:
Received 10 September 2001; accepted 16 June 2003.
DOI 10.1002/ajpa.10358
Published online 19 November 2003 in Wiley InterScience (www.
Fig. 1. Geographic distribution of tribe Atelini members in southern and eastern portions of the Amazon Basin and Atlantic coastal
forests of South America. Both species of Lagothrix (shaded line) and disjunct populations of Brachyteles are indicated. Four species
of Ateles (patterned line) are included. Approximate geographic locations of samples utilized in this study are indicated with numerals
that correspond to those found in Table 1. Species identities are based on taxonomy of Groves (1989), Rowe (1996), Pope (1998), and
Collins and Dubach (2000, 2001).
Saldanna, 1974; Pequignot et al., 1985; Rumpler
and Strasbourg, 1992).
A steadily growing number of genetic studies support a phylogeny in which Brachyteles and Lagothrix
are sister taxa, with Ateles as the outgroup (Schneider et al., 1993; Harada et al., 1995; Schneider and
Rosenberger, 1996; Barroso et al., 1997; Porter et
al., 1997; Canavez et al., 1999; von Dornum and
Ruvolo, 1999; Meireles et al., 1999; Schneider,
2000). These genetic studies are based on sequence
information from a variety of nuclear genes as part
of large-scale studies to determine higher-level relationships among all Platyrrhine primates. Figure 2
summarizes the relationships supported, the morphological characteristics or genetic regions investigated, and the taxonomy suggested by previous
The present study investigated phylogenetic relationships among the Atelinae, based on DNA sequence variation for a mitochondrial, protein-coding
region, cytochrome c oxidase subunit II (COII), as
well as the hypervariable I area of the mitochondrial
control region. In addition, a single-copy nuclear
gene, Aldolase A intron V, was sequenced. The
higher mutation rate and associated increase in genetic substitutions in these loci, compared to more
conserved nuclear genes utilized in previous Platyrrhine-wide studies, were hypothesized to produce a
more discriminate measure of variation among the
Atelinae relationships were investigated using
only one or two haplotypes from each genus in the
previous genetic studies, since their primary focus
was Platyrrhine-wide relationships (Schneider et
al., 1993; Harada et al., 1995; Schneider and Rosenberger, 1996; Barroso et al., 1997; Porter et al., 1997;
Canavez et al., 1999; von Dornum and Ruvolo, 1999;
Meireles et al., 1999; Schneider, 2000). However,
Alouatta has 6 or 7 species (Groves, 1989), Ateles has
3– 6 species (Kellogg and Goldman, 1944; Groves,
1989; Froehlich et al., 1991; Collins and Dubach,
2000), Lagothrix has 2 species (Groves, 1989), and
Brachyteles is comprised of 1 or possibly 2 species
(Groves, 1989; Pope, 1998).
The results of the genetic studies contrast with
the trichotomous relationship supported by sampling multiple members of each genus for morphological traits. I propose that significant intrageneric
variation among Atelinae genera, especially in Ateles (Collins and Dubach, 2000), prohibits the use of
the limited sampling approach for phylogenetic
studies of this subfamily. Ruvolo (1997) suggested
that the very close, previously trichotomous, genetic
relationships among the Hominoidea can be adequately discriminated using single-haplotype representatives from each genus. But genetic distances
between genera are closer for the Hominoidea, their
last common ancestor lived more recently, and their
geographic distributions are more limited than
members of the Atelinae. All of these factors are
Alouatta spp., Alouatta seniculus, Alouatta caraya,
and Lagothrix spp. were obtained from GenBank
(Adkins and Honeycutt, 1994; Figueiredo et al.,
1998; Ascunce et al., 2001). Table 1 and Figure 1
detail the geographic locations and sources of samples from the various Atelinae genera and species
used in this study.
DNA isolation and nucleotide sequencing
Fig. 2. Various different cladistic arrangements among tribe
Atelini genera in a wide variety of previous and present morphological and genetic studies. Source of analysis is indicated in
parentheses after each author, in boxes below various clades.
hypothesized to reduce genetic variation in the
Hominoidea as compared to the Atelinae.
To increase inclusion of genetic variation sampled
in the Atelinae, the present study included haplotypes of Ateles from each of the six species suggested
by Groves (1989) in the most expansive taxonomy
for this genus. Alouatta, consistently the basal taxon
in all previous genetic studies and most morphological studies, was represented in the present research
by one species, except for COII, where additional
sequence information from GenBank allowed expanded analysis. Both Brachyteles and Lagothrix
are represented by samples from the single most
widely distributed species. This study omitted only
the minimally distributed Lagothrix flavicauda
among traditionally recognized tribe Atelini species.
This research is an extension of phylogenetic studies
of Ateles phylogenetic relationships conducted by
Collins and Dubach (2000, 2001).
Samples of DNA and/or tissue were obtained directly from wild specimens for most haplotypes. Additional whole-blood samples were obtained from
various zoological and research institutions
throughout North America. Only specimens with
wild origins from known geographic locations, confirmed by karyotype analysis, were utilized (Table
1). Subspecies names were used as labels to identify
haplotypes, but all haplotypes were analyzed and
grouped irrespective of any previous taxonomic
identities. Additional DNA sequences for COII from
Total genomic DNA was isolated from blood and
tissue samples, using standard phenol/chloroform
extraction techniques with ethanol precipitation
(Sambrook et al., 1989). DNA was amplified using
the polymerase chain reaction (PCR). Conserved
primers located in the lysine and asparagine tRNA
were used to amplify the COII gene. The control
region was amplified using conserved primers located in the proline tRNA and a conserved location
near the origin of replication (Kocher et al., 1989).
Primers reported by Hillis et al. (1996) were used for
amplification of the Aldolase A intron.
All double-stranded DNA amplification products
were directly sequenced on both model 377 and 377A
automated DNA sequencers (ABI). All samples were
sequenced in both directions, and random samples
were repeated to ensure sequence accuracy. For specific details of PCR conditions and sequencing of
DNA, refer to Collins and Dubach (2000, 2001).
DNA sequences obtained for all three genetic regions used in this study were deposited in GenBank
under the following sets of accession numbers: control region, AF213940 –AF213966; COII, AF216225AF216253; and Aldolase A, AF242395–AF242410.
See Table 1 for exact sequences utilized.
DNA sequence alignment and
phylogenetic analysis
Atelinae sequences were aligned using the MacDNASIS version 3.2 (Hitachi Software Engineering,
America Ltd.) contig option to align sequences from
opposite orientations, and then were compiled by
inspection. Gaps were introduced in order to align
haplotypes, as dictated by a Higgins-Sharp multiple
alignment program.
Sequences were analyzed using Phylogeny Analysis Using Parsimony (PAUP), version 4.0b1 (Swofford, 1998). Trees were produced using both unweighted and weighted ratios of transversions to
transitions. Exhaustive searches were performed to
identify the best-fit tree in most cases. Bootstrap
analysis was carried out using heuristic searches,
with random-sequence addition to assess support for
various branches in the phylogram, based on 5,000
For analysis of various genetic regions, midpoint
rooting was initially performed to assess that Alouatta was the most basal member among Atelinae
haplotypes. Alouatta was then utilized as an outgroup for further analyses of relationships among
members of tribe Atelini and bootstrap confidence
TABLE 1. Geographic location and specific identification of Atelinae haplotypes1
Subspecies population
Ateles paniscus
Ateles belzebuth marginatus
Ateles belzebuth chamek
Ateles belzebuth chamek
Ateles hybridus
Ateles geoffroyi (fusciceps) robustus
Ateles geoffroyi yucatanensis
Alouatta palliata
Alouatta spp.
Alouatta seniculus
Alouatta caraya
Brachyteles arachnoides hypoxanthus
Lagothrix lagotricha
Lagothrix spp.
GenBank ID
Geographic area
Rio Trombetus, Para State, Brazil
Tocantins River, Para State, Brazil
Rio Jiparana, Rondonia State, Brazil
Magdalena River Valley, Colombia
Darien Peninsula, Panama
Yucatan Peninsula, Mexico
Central America
From Adkins and Honeycutt (1994)
From Figueiredo et al. (1998)
From Ascunce et al. (2001)
Fazenda Esmerelda, Sao Paulo State, Brazil
From Adkins and Honeycutt (1994)
Provides information on species/subspecies identity of various haplotypes utilized in this study. GenBank accession numbers are
provided for each haplotype. Accession numbers are for COII, control region, and Aldolase A regions from top to bottom. Identical
haplotypes were not sequenced for some animals for Aldolase A. Geographic information indicates broad area each sample came from
in the wild, or references published source of sequence information. Map locations correlate to numbers in Figure 1 on source of Ateles
Maximum likelihood analysis was performed using the likelihood option of PAUP, version 4.0b1
(Swofford, 1998), with heuristic searches and addition of samples as presented in the data set. The
transition transversion ratio was estimated from the
data. Data sets were randomly rearranged manually
and reanalyzed, to insure that order of addition was
not affecting the resultant phylogeny.
Sequences were also analyzed using the neighborjoining optimization in PAUP, version 4.0b1 (Swofford, 1998), to produce a distance-based phylogenetic tree. Bootstrap analysis was performed with
random sequence addition on 10,000 replications of
the data set.
The computer phylogeny program MEGA, version
1.02 (Kumar et al., 1993), was also used to compute
the standard error test of neighbor-joining tree
branch lengths from zero H0:BL ⫽ 0. The confidence
probabilities (CP) reported are equivalent to 1 ⫺ ␣,
where ␣ is the significance level of type I error. Thus,
CP ⱖ 0.95 corresponds to ␣ ⱕ 0.05 and is considered
significant. When bootstrapping favored an arrangement seen in the neighbor-joining tree and the confidence probability favored another relationship, no
confidence probability is reported for that node.
Congruence between various data sets was examined with the incongruence length difference (ILD)
or partition-homogeneity test (Farris et al., 1995), as
implemented in PAUP (Swofford, 1998). Congruence
between all tribe Atelini data sets (past and present)
was also implemented in the same manner, but with
only one species of each genus, as occurs in many of
the data sets. The test was implemented on 1,000
partition sample replicates with a heuristic search
and random addition of haplotypes. Topological congruence between possible gene trees was evaluated
using the two-tailed test of Templeton (1983) and
the winning sites test (Prager and Wilson, 1988), as
implemented in PAUP.
The computer program MacClade, version 3.05
(Maddison and Maddison, 1992), was used to analyze base composition frequency, set character
weights, determine nucleotide coding positions for
protein coding regions, calculate transition/transversion ratios, and trace character-state evolution.
The Ateles haplotypes used in this study consistently produced the taxonomy reported by Collins
and Dubach (2000), and were collapsed into those
four species: A. paniscus, A. belzebuth (including A.
b. chamek and A. b. marginatus), A. hybridus (formerly A. b. hybridus), and A. geoffroyi (including A.
g. yucatanensis and A. f. robustus) for graphic presentation.
COII gene
The analysis of the COII gene included seven Ateles haplotypes, two haplotypes of Lagothrix, four
Alouatta haplotypes from three different species,
and one haplotype of Brachyteles (See Table 1). The
data set has 143 phylogenetically informative characters, with a ratio of 5.1 transitions per transversion (Maddison and Maddison, 1992). Sequences
from Alouatta and Lagothrix obtained from GenBank are shorter than those in this study and include fewer characters, which were treated as missing data.
A branch-and-bound analysis (PAUP) of unweighted data produced six equally parsimonious
trees, where four trees supported a Brachyteles-Ateles clade and the other two trees actually supported
an Ateles-Lagothrix clade. Either clade was supported by an identical number of synapomorphies.
The Brachyteles-Lagothrix clade had six fewer synapomorphies than the alternative clades. Bootstrap
support for the Brachyteles-Ateles clade was 51% in
the unweighted data set, using all available DNA
sequences. Weighted analysis with the observed 5:1
ratio and experimental ratios as high as 20:1 supported the Ateles-Lagothrix clade. The 20:1 weighting produced two trees that varied only among the
Ateles haplotypes, with better bootstrap support for
the Ateles-Lagothrix clade of 62% (Fig. 3).
Neighbor-joining analysis favored the Brachyteles-Ateles clade with bootstrap support of 70% (Fig.
3). A maximum likelihood analysis of this data set
also favored a clade containing Brachyteles and Ateles, with an ln likelihood of ⫺2,554.6.
Assigning coding positions to the weighted data
set and analyzing each position separately produced
support for a Brachyteles-Ateles clade for position 1,
using both parsimony and neighbor-joining analysis. Position 2 does not favor relationships between
any members of tribe Atelini. The third position
reflects the complete data set relationships varying
depending on the analysis method. Analysis of only
the transversions in the Atelinae COII data set is
unable to differentiate among the members of tribe
Control region
The portion of the control region sequenced
ranged from 497–522 base pairs among Ateles haplotypes. This variance was due to a 25-base pair
deletion in A. paniscus, A. b. marginatus, and some
A. b. chamek haplotypes. The complete aligned data
set was 541 base pairs long, with appropriate insertions made. The control region sequence contained
124 phylogenetically informative characters and a
transition to transversion ratio of 2.56 (MacClade,
version 3.05).
Parsimony analysis of the control region sequences produced six equally parsimonious trees.
All six trees related Brachyteles more closely to
Lagothrix, contradictory to the COII gene tree, with
weak bootstrap support of 56% (Fig. 3).
Weighting the data set as high as 20:1 produced
only one tree identical to one of the six unweighted
trees, but with no bootstrap support for the
Brachyteles-Lagothrix clade. Due to the contradictory topology of the two-phylograms, an analysis
which eliminated the more frequent and possibly
homoplasic transitions was undertaken. Analysis of
transversions only produced 21 trees and resulted in
a Brachyteles-Lagothrix clade in 11 of the 21 trees
without any bootstrap support.
Neighbor-joining analysis produced a tree with a
very short branch length (less than 0.5% of the total
length) leading to a Brachyteles-Lagothrix clade.
Bootstrap support was similar to the parsimony tree
(Fig. 3). To try and resolve possible variable rates of
change among sites in the control region, a maximum likelihood search was preformed. The resultant topology related Brachyteles to Lagothrix, with
an ln likelihood of ⫺2,448.4. Since the mitochondrial
genome is inherited as a single unit, the relationships should reflect the same heritage. The fact that
they do not is likely due to increased homoplasy in
the more variable control region sequences and the
possibility of nonequal rates of variation among
sites. However, a plot of transitions vs. genetic distance for all pairwise comparisons in this data set
had a high correlation coefficient (R2 ⫽ 0.941)
Aldolase A Intron V
Aldolase A Intron V is a variable nuclear region
that had only five parsimony informative characters
in the 466 bp sequenced. An exhaustive search
(PAUP) using midpoint rooting united all members
of tribe Atelini with Alouatta as the most divergent
genus. Parsimony analysis produced only one tree
which grouped Brachyteles and Ateles, leaving Lagothrix as the sister taxa to this clade, with bootstrap
support of 63% (Fig. 4). No informative transversions occurred in the data set, so no weighted analysis was carried out.
Distance-based analyses supported grouping
Brachyteles with Ateles in a clade joined basally by
Lagothrix. Bootstrap analysis supported this relationship 68% of the time (Fig. 4). Maximum likelihood analysis of the Aldolase data set produced a
tree that also related Brachyteles more closely to
Ateles, with an ln likelihood value of ⫺821.7.
Complete mitochondrial and nuclear
DNA analysis
To search for clarity of relationships among tribe
Atelini members, all nuclear and mitochondrial data
from the present study were subjected to the parti-
Fig. 3. Trees A and C. Tree A is maximum parsimony (PAUP) COII tree from weighted data set, with tree length of 493 steps.
Discovered using a branch-and-bound search with furthest addition sequence; consistency index ⫽ 0.7333. Tree C is maximum
parsimony control region tree from weighted data set, with tree length of 547 steps. Discovered using an exhaustive search; consistency
index ⫽ 0.7459. Bootstrap values are percentages out of 5,000 bootstrap replications supporting a given grouping. Values indicated
along each branch correspond to following node. Values below diagonals indicate number of synapomorphies supporting clade. Trees
B and D. Tree B is distance-based tree from neighbor-joining analysis of COII sequences. Tree D is distance-based tree from
neighbor-joining analysis of control region sequences. Both trees were derived from a distance matrix constructed using Kimura
two-parameter distance method (Kimura, 1980). Frequency of grouping among clades is based on 10,000 bootstrap replications.
Confidence probabilities testing significance level of corresponding branch lengths from zero were assessed using MEGA (version 1.02).
Bootstrap values are indicated along each branch. Below diagonals are confidence probabilities.
tion homogeneity (ILD) test (PAUP) to discern if the
data from these varied genetic regions could be combined for analysis. The data were partitioned into
their respective data sets, and invariant characters
were set to zero weight. This test indicated that data
in all three genetic regions were congruent (P ⫽
The combined data set includes 1,715 bp and 207
phylogenetically informative characters, with a ratio of 3.03 transitions per transversion (MacClade,
version 3.05). An exhaustive search (PAUP) with
either midpoint rooting, or Alouatta as the outgroup
to tribe Atelini, produced two equally parsimonious
trees, differing only within the Ateles genus.
Brachyteles is joined with Ateles in both of the most
parsimonious trees to form a clade with Lagothrix as
the sister taxa, but without any bootstrap support.
An exhaustive search (PAUP) of the data set with
transversions weighted from 5:1 to as high as 20:1
over transitions produced the same two trees, which
related Brachyteles to Ateles and provided weak
bootstrap support of 51% (Fig. 4).
Neighbor-joining analysis of the weighted, complete data set produced a tree which related
Brachyteles and Lagothrix as a clade, with Ateles as
the sister taxa. This relationship received no bootstrap support, however (Fig. 4). Analysis of this data
set using maximum likelihood analysis produced a
tree that supported Brachyteles as more closely related to Ateles, with an associated ln likelihood of
The three data sets produced trees with different
relationships among the Atelini depending on region
and method of analysis, and are incongruent upon
visual inspection. The significance of this topological
incongruence was assessed using the test of Templeton (1983) and the winning sites test (Prager and
Wilson, 1988), using the topology of each independent data set as a constraint for the combined mitochondrial and nuclear data. The test of Templeton
(1983) did not detect any significant incongruence
between any comparisons (P ⫽ 0.9130 for comparison between the two mitochondrial trees, P ⫽ 0.2513
for the Aldolase tree compared to the COII tree). The
winning sites test also did not discover any significant incongruence (P ⫽ 1.0 and 0.4545 for the above
Fig. 4. Trees A and C. Tree A presents maximum parsimony (PAUP) Aldolase A Intron V phylogeny from data set, with tree length
of 30 steps. Discovered using an exhaustive search; consistency index ⫽ 1.00. Tree C presents maximum parsimony combined
mitochondrial and nuclear DNA phylogeny from weighted data set, with tree length of 1,128 steps. Discovered using an exhaustive
search; consistency index ⫽ 0.7624. Bootstrap values are percentages of 5,000 bootstrap replications supporting a given grouping.
Values indicated along each branch correspond to following node. Values below diagonals indicate number of synapomorphies
supporting clade. Trees B and D. Tree B is distance-based tree from neighbor-joining analysis of Aldolase A Intron V sequences. Tree
D is distance-based tree from neighbor-joining analysis of combined mitochondrial and nuclear DNA sequences. Both trees were
derived from a distance matrix constructed using Kimura two-parameter distance method (Kimura, 1980). Frequency of grouping
among clades is based on 10,000 bootstrap replications. Confidence probabilities testing significance level of corresponding branch
lengths from zero were assessed using MEGA (version 1.02). Bootstrap values are indicated along each branch. Below diagonals are
confidence probabilities.
Reexamination of previous genetic studies
An attempt was made to differentiate between the
alternate and poorly supported phylogenies produced by the different genetic regions and analysis
methods in the present study. This involved further
examination of Atelinae relationships by combining
sequence data from Atelinae haplotypes from previous Platyrrhine-wide nuclear phylogenetic studies
with the data from this research project.
The ⑀-globin sequences reported by Schneider et
al. (1993) for the Atelinae were downloaded from
GenBank (accession numbers L25358, L25366,
L25367, L25369, and L25370) and aligned according
to that study. Additional sequence information from
other available studies was downloaded and analyzed in the same manner as the present study: 1)
␥-globin (Meireles et al., 1998) (accession numbers
AF030092, AF030093, AF030094, AF030095,
AF030097, and AF030098); 2) interstitial retinolbinding protein (IRBP) (Harada et al., 1985) (accession numbers U18602, U18603, U18605, and
U18614); 3) ␤2 microglobulin (Canavez et al., 1999)
(accession numbers AF032047, AF032050, AF032053,
AF032086, AF032048, AF032049, AF032051,
AF032052, AF032054, AF032055, AF032087, and
AF032088); and 4) G6PD (von Dornum and
Ruvolo, 1999) (accession numbers AF289989,
AF289985, AF028502, AF028501, AF028513,
AF028498, AF028478, AF028477, AF028489, and
AF028473). Sequence data for the von Willebrand
Factor Gene Intron II for all Atelinae (Vieria et
al., 1997; Chaves et al., 1999) were not available
on GenBank.
Analysis of only the Atelinae haplotypes for ⑀-globin, ␥-globin , ␤2 microglobulin, and G6PD (Schneider et al., 1993; Meireles et al., 1998; Canavez et al.,
1999; von Dornum and Ruvolo, 1999) all supported a
Brachyteles-Lagothrix clade, with bootstrap support
ranging from ⬍50 –100%. The G6PD sequences produced no bootstrap support using the weighting
scheme of von Dornum and Ruvolo (1999). The
weighted IRBP data equally supported either a
TABLE 2. Comparative support among possible subclades in tribe Atelini1
Templeton P
sites P
ME score
⫺Ln likelihood
Three possible subclades within tribe Atelini for combined present and previous data sets. There is no weighting of data. For
parsimony comparisons, favored subclade is labeled as “best,” and P values for test of Templeton (1983) along with N and z values are
presented, followed by P value for winning sites test (Prager and Wilson, 1988). Significant values of P ⬍ 0.05 are in bold. For
distance-based comparisons, minimum evolution (ME) score is presented. For likelihood comparisons, ⫺Ln likelihoods of each tree are
also presented. All data were produced using the tree-scores option of PAUP.
Brachyteles-Ateles or a Brachyteles-Lagothrix clade,
using parsimony analysis for only Atelinae samples.
This is contradictory to the full data-set results of
Harada et al. (1995). Neighbor-joining results for
the reduced IRBP data set do favor the BrachytelesLagothrix clade as supported by Harada et al.
(1995), and provide 77% bootstrap support for the
clade. The inclusion of additional haplotypes from
other genera in the Platyrrhine-wide studies
(Schneider et al., 1993; Harada et al., 1995; Schneider and Rosenberger, 1996; Barroso et al., 1997;
Porter et al., 1997; Canavez et al., 1999; von Dornum
and Ruvolo, 1999; Meireles et al., 1999; Schneider,
2000) acted to modify Atelini relationships in the
full studies.
In a final attempt to differentiate among tribe
Atelini members, all nuclear and mitochondrial data
from the present study and additional sequences
from all other studies were subjected to the partition
homogeneity (ILD) test (PAUP) to discern if the data
from these varied genetic regions could be combined
for analysis. The data were partitioned into their
respective data sets, and invariant characters were
set to zero weight. The test indicated that data in all
eight genetic regions were congruent (P ⫽ 0.75).
Analysis of this complete data set contained only
one member of each Atelinae genus due to the limitations of some of the studies. The total combined
data set included 15,177 base pairs of DNA for eight
genetic regions. Parsimony analysis of the unweighted data set produced a tree (1,300 steps; CI
excluding uninformative characters ⫽ 0.653) that
related Brachyteles most closely to Lagothrix, with
Ateles as the sister taxa. Neighbor-joining analysis
produced the same tree, and both had bootstrap
support ranging from 98 –100%. The alternate
Brachyteles-Ateles tree required an additional 27
steps to render.
The various data sets produced trees that sometimes differed in relationships among tribe Atelini
genera, and are thus topologically incongruent upon
visual inspection. The significance of this incongruence was assessed using the test of Templeton
(1983) and the winning sites test (Prager and Wilson, 1988). The complete data set had only single
representatives from each taxon; thus, any phylogram had only four possible OTUs. There were only
three possible arrangements of tribe Atelini members in phylograms. The test of Templeton (1983)
scored the Brachyteles-Lagothrix tree as the “best”
tree and indicated significant incongruence when
comparing to the other possible trees, as did the
winning sites test (Prager and Wilson, 1988). The
results of these comparisons are presented in Table
This seeming confirmation of subtribe Brachytelina
is tempered by the fact that investigations of ⑀-globin
(Schneider et al., 1993) and ␥-globin (Meireles et al.,
1999) used only two species of Ateles, while IRBP, ␤2
microglobulin, and G6PD (Harada et al., 1995; von
Dornum and Ruvolo, 1999; Canavez et al., 1999) utilized only one species of Ateles in their analyses. Only
one Lagothrix and Brachyteles with no more than two
Alouatta haplotypes were used in these studies as
well. This sampling approach does not adequately
measure genetic diversity among these widely dispersed genera, as demonstrated below.
To examine the effects of using limited Ateles haplotypes to construct phylogenies among Atelinae
genera, the complete mitochondrial and nuclear
data set from the present study was reanalyzed with
the restriction of including only one or two haplotypes of spider monkeys. The reduced set of Ateles
haplotypes clearly does not represent the wide degree of genetic variation present among the various
populations of spider monkeys seen in the complete
data set.
Using only one Ateles haplotype, 2 of the 6 haplotypes produced relationships, using parsimony analysis, that favored a Brachyteles-Ateles clade, with
the other 4 favoring a Brachyteles-Lagothrix clade
(Table 3). Neighbor-joining analyses of these data
sets produced only trees favoring a BrachytelesLagothrix clade (Table 3).
Analysis of the data set including only the two
species of Ateles used by Schneider et al. (1993)
produced two equally parsimonious trees, indicating
equal support for either a Brachyteles-Ateles clade or
a Brachyteles-Lagothrix clade. A neighbor-joining
analysis of this data set favored a Brachyteles-Lagothrix clade, but this received no bootstrap support
(Table 3).
Examination of all possible combinations of only
two Ateles species using parsimony produced relationships of Brachyteles to both Ateles and to Lagothrix (Table 3). Of the 15 possible combinations, 8
phylograms favored a Brachyteles-Lagothrix clade,
and 5 trees favored a Brachyteles-Ateles clade, with
TABLE 3. Effect of different Ateles species on phylogenies1
Ateles species included
A. paniscus5
A. hybridus
A. belzebuth chamek
A. belzebuth marginatus2
A. geoffroyi yucatanensis
A. geoffroyi robustus6
A. g. robustus and A. g. yucatanensis
A. paniscus and A. b. chamek
A. b. chamek and A. b. marginatus
A. paniscus and A. g. yucatanensis4
A. g. yucatanensis and A. hybridus
A. b. chamek and A. hybridus
A. paniscus and A. b. marginatus
A. paniscus and A. hybridus
A. g. robustus and A. hybridus
A. b. chamek and A. g. robustus
A. b. chamek and A. g. yucatanensis
A. g. robustus and A. b. marginatus
A. b. marginatus and A. hybridus
A. b. marginatus and A. g. yucatanensis3
A. paniscus and A. g. robustus
All Ateles specimens
Equal support
Equal support
Details shifting support for two most likely clades among tribe Atelini, based on number and composition of Ateles species included,
following most inclusive taxonomy (Groves, 1989) in an exhaustive parsimony search (PAUP) and with neighbor-joining analysis
(PAUP). Includes all possible trees with inclusion of only one or two Ateles haplotypes. Bootstrap support is based on 1,000 replications.
One species utilized by Harada et al. (1995).
Two species utilized by Schneider et al. (1993).
Two species utilized by Meireles et al. (1999).
One species used by Canavez et al. (1999).
One species used by von Dornum and Ruvolo (1999).
At bottom, information with inclusion of all Ateles specimens is repeated for comparative purposes.
none of these receiving ⬎75% bootstrap support.
Two haplotype combinations produced identical support for the relationship of Brachyteles to either
Ateles or Lagothrix (Table 3).
Distance-based analyses using only two species of
Ateles produced trees that were sometimes contradictory to the parsimony trees (Table 3). Analysis of
the 15 haplotype combinations produced 3 trees relating Brachyteles and Ateles, while 12 trees related
Brachyteles to Lagothrix with variable, relatively
low levels of bootstrap support (Table 3). These examples demonstrate how relationships can change,
based on the number and composition of Ateles haplotypes included. Results and comparisons for all
these combinations are presented in Table 3.
Results based on the new data presented in this
study demonstrate the high similarity between Atelini genera. All of the genetic regions investigated
support different relationships among tribe Atelini
genera, which vary by region, weighting scheme,
and analysis method. The control region sequences,
which support a Brachyteles-Lagothrix clade, may
possibly be too homoplasic for discrimination between separate, yet closely related genera. Even
combined analysis of all three loci supports different
relationships, depending on the method of analysis.
These findings demonstrate the very close relationships between these genera. They further demonstrate the associated difficulty in differentiating
the actual phylogenetic relationship, even with multiple haplotypes and species/subspecies of Ateles,
and Alouatta for COII, in the data sets. Some readers might suggest that these results demonstrate
the overall poor resolving power of the loci chosen in
this study. While this could be the case, it is more
likely to be indicative of the very close genetic relationships among all three genera and the increased
need for inclusion of multiple samples from different
species/subspecies or genetically distinct populations in the determination of relationships in tribe
In reanalysis using only Atelinae DNA sequences
from previous studies (Schneider et al., 1993;
Harada et al. 1995; Canavez et al., 1999; Meireles et
al., 1999; von Dornum and Ruvolo, 1999), there was
a total of 44 phylogenetically informative characters
when all data sets were reduced to just one member
of each genus. This is compared to 70 phylogenetically informative characters for the present data set
with only one member of each genus. This suggests
that the resolving power of this data set is at least as
good as the combination of previous data sets or
better. The low bootstrap support for clades and the
variable relationship of Brachyteles in these trees
are indicative of the extreme similarity between
these genera, and not the lack of phylogenetically
informative sites in the sequences chosen.
Even though the test of Templeton (1983) and the
winning sites test (Prager and Wilson, 1988) found
significant support for the Brachyteles-Lagothrix
tree in the combined data set, these same tests detected no significant differences between the possible trees for analysis of the present data set alone.
The inclusion of additional Atelinae haplotypes in
this study likely contributed to the lack of significant
differences between possible trees in the present
data set.
Ateles is a genetically variable genus with significant intra- and interspecific variation (Collins and
Dubach, 2000). When only limited samples of such a
genetically and geographically diverse taxon are included, it is possible to omit the genetic variation
needed to discern taxonomic relationships. Limited
sampling of the Atelinae genera would seem likely to
affect the outcome of phylogenetic reconstructions.
The effects of sampling only a portion of the genetic
variation in Ateles were demonstrated in Table 3,
with comparisons of phylogenies with limited Ateles
haplotypes included. Support switched back and
forth in the limited haplotype analysis of the present
data, depending on species/populations included,
thus suggesting that similar results might occur if
the previous data sets could be examined in a similar fashion.
Since this data set was not originally gathered to
address Atelinae phylogenetics, the COII data set
was the only one where multiple samples of other
non-Ateles genera were available for phylogeny construction via the use of sequences deposited in GenBank. Analysis of this locus goes further in demonstrating the impact of multiple vs. single samples of
all genera on Atelini relationships. Inclusion of all
available Atelinae haplotypes, using the weighted
data set, produced 62% bootstrap support for a Lagothrix-Ateles clade, but inclusion of only the more
complete Alouatta haplotype determined in this
study produced a tree with only a Brachyteles-Ateles
clade, with bootstrap support of 56%. In earlier versions of this research, the Alouatta caraya haplotype
was not available, and all trees analyzed supported
a Brachyteles-Ateles clade. It was only with inclusion
of this new sample and reweighting of newly informative transversions that the data supported the
Ateles-Lagothrix clade. These results clearly indicate the importance of including not only additional
haplotypes of Ateles in future analyses, but also
additional haplotypes of the geographically widespread and genetically variable members of Alouatta, and likely Lagothrix and Brachyteles too.
The possibility that several of the gene trees do
not represent the actual species tree is feasible, especially given the limited number of samples utilized for each genus. A great deal of support for a
Brachyteles-Lagothrix clade comes from studies of
the ⑀-globin, ␥-globin, and ␤2 microglobulin genes
(Schneider et al., 1993; Schneider and Rosenberger,
1996; Porter et al., 1997; Canavez et al., 1999; Meireles et al., 1999). ⑀-globin and ␥-globin are part of the
␤-globin gene cluster, where ⑀-globin is embryonically expressed and ␥-globin is fetally expressed in
anthropoids (Meireles et al., 1995; Chiu et al., 1996).
The mode of expression and organization of these
genes is unique among the Atelinae (Meireles et al.,
1995; Chiu et al., 1996). Among Atelinae, the ␥1
portion has been inactivated due to a 1.8-kb deletion. Gene conversions between ␥1 and ␥2 are common among many Platyrrhine species (Meireles et
al., 1995), but Meireles et al. (1999) found only two
conversions between loci in Atelinae. They eliminated these stretches from their analyses, but it is
interesting to note that one of the conversions occurred in only one of the two spider monkeys they
sampled. If they had sampled more species/subspecies of Ateles, it seems possible that more conversion
events might have been discovered. Imagine a scenario where only one species of Ateles had been
sampled and this conversion would have been
missed, and the data would have then been incorporated into phylogenetic reconstructions. This suggests that other gene conversions in other regions
may have occurred in additional populations of
Lagothrix and Brachyteles, which might be acting to
confound the results and skew the relationships between the limited haplotypes chosen. Additionally,
it is clear that ⑀-globin and ␥-globin are closely
linked loci, and the ␤2 microglobulin gene is possibly
linked. Thus it is not surprising that they produce
similar phylogenies.
As can be seen in examination of the various distance-based cladograms, the shared branch length
between all of the Atelini is very short. The results of
this study and the morphological analysis of Ford
(1986) suggest a very close relationship among the
three genera of tribe Atelini, a suggestion that was
also proposed by Schneider and Rosenberger (1996).
This research provides additional support for the
similarity of members of tribe Atelini, providing validity for the cladistic arrangement of two tribes,
Alouattini and Atelini, among the Atelinae subfamily. The relationship of Brachyteles to either Ateles
or Lagothrix is demonstrated to be unresolved due to
the lack of inclusion of genetically variable samples
among Atelini genera in previous genetic studies
and possibly this study as well.
Based on the evidence from this study on the
importance of the inclusion of multiple Atelinae species, the assertions of Harada et al. (1995), Schneider and Rosenberger (1996), Canavez et al. (1999),
Meireles et al. (1999), and von Dornum and Ruvolo
(1999) that Brachyteles and Lagothrix should constitute a subtribe Brachytelina need to be reviewed. It
appears that, while this may be the actual relationship, the evidence presently available is not clear
enough to support any specific Atelini subtribes.
Future studies should also attempt to obtain additional specimens of the different Alouatta species,
various Lagothrix species and subspecies, and samples from both disjunct populations of Brachyteles. A
large amount of sequence data exists to address the
relationships among tribe Atelini, but until this
amount is obtained on a greater number of populations and species within the Atelinae, no definitive
relationships among tribe Atelini can be determined.
I thank the Conservation Biology Department of
Brookfield Zoo (Chicago, IL) for providing research
support at the Daniel F. and Ada L. Rice Conservation Biology and Research Center’s Genetics Laboratory for this project. Grant support was awarded
to J.M. Dubach and the Brookfield Zoo by SEACON
(Chicago Zoological Society Conservation Research
Grant) and the Institute of Museum and Library
Services (1C-40190-94). Funding was also provided
by a Sigma Xi Grant in Aid of Research to A.C.C. I
thank J.M. Dubach, Trudy Turner, and Karen Strier
for comments about this manuscript at varying
stages of its progress. The comments of two anonymous reviewers also served to strengthen and focus
this paper. Invaluable samples of spider monkeys
were provided by the following individuals and institutions: Horacio Schneider and the Universidade
Federal do Para in Belem, Brazil, who provided most
of the wild-caught samples; Morris Goodman at
Wayne State University; Theresa Pope at Duke University; Guy Hoelzer at Utah State University;
Robin Brockett, who helped obtain the Belizean
samples; the Lubee Foundation; Bruce Patterson at
the Field Museum of Natural History in Chicago; La
Merida Zoo in Mexico; Club Auto Safari in Guatemala; the National Zoo in Washington, DC; Scott
Carter at the Detroit Zoo; and the Charles Paddock
Zoo (Atascadero, CA).
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