Genomic data support the hominoid slowdown and an Early Oligocene estimate for the hominoid-cercopithecoid divergence.
ABSTRACT Several lines of indirect evidence suggest that hominoids (apes and humans) and cercopithecoids (Old World monkeys) diverged around 23-25 Mya. Importantly, although this range of dates has been used as both an initial assumption and as a confirmation of results in many molecular-clock analyses, it has not been critically assessed on its own merits. In this article we test the robusticity of the 23- to 25-Mya estimate with approximately 150,000 base pairs of orthologous DNA sequence data from two cercopithecoids and two hominoids by using quartet analysis. This method is an improvement over other estimates of the hominoid-cercopithecoid divergence because it incorporates two calibration points, one each within cercopithecoids and hominoids, and tests for a statistically appropriate model of molecular evolution. Most comparisons reject rate constancy in favor of a model incorporating two rates of evolution, supporting the "hominoid slowdown" hypothesis. By using this model of molecular evolution, the hominoid-cercopithecoid divergence is estimated to range from 29.2 to 34.5 Mya, significantly older than most previous analyses. Hominoid-cercopithecoid divergence dates of 23-25 Mya fall outside of the confidence intervals estimated, suggesting that as much as one-third of ape evolution has not been paleontologically sampled. Identifying stem cercopithecoids or hominoids from this period will be difficult because derived features that define crown catarrhines need not be present in early members of these lineages. More sites that sample primate habitats from the Oligocene of Africa are needed to better understand early ape and Old World monkey evolution.
- Human Biology 06/1961; 33:131-62. · 1.52 Impact Factor
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ABSTRACT: The application of maximum likelihood techniques to the estimation of evolutionary trees from nucleic acid sequence data is discussed. A computationally feasible method for finding such maximum likelihood estimates is developed, and a computer program is available. This method has advantages over the traditional parsimony algorithms, which can give misleading results if rates of evolution differ in different lineages. It also allows the testing of hypotheses about the constancy of evolutionary rates by likelihood ratio tests, and gives rough indication of the error of ;the estimate of the tree.Journal of Molecular Evolution 02/1981; 17(6):368-76. · 2.15 Impact Factor
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ABSTRACT: For almost a decade now, a team of molecular evolutionists has produced a plethora of seemingly precise molecular clock estimates for divergence events ranging from the speciation of cats and dogs to lineage separations that might have occurred approximately 4 billion years ago. Because the appearance of accuracy has an irresistible allure, non-specialists frequently treat these estimates as factual. In this article, we show that all of these divergence-time estimates were generated through improper methodology on the basis of a single calibration point that has been unjustly denuded of error. The illusion of precision was achieved mainly through the conversion of statistical estimates (which by definition possess standard errors, ranges and confidence intervals) into errorless numbers. By employing such techniques successively, the time estimates of even the most ancient divergence events were made to look deceptively precise. For example, on the basis of just 15 genes, the arthropod-nematode divergence event was 'calculated' to have occurred 1167+/-83 million years ago (i.e. within a 95% confidence interval of approximately 350 million years). Were calibration and derivation uncertainties taken into proper consideration, the 95% confidence interval would have turned out to be at least 40 times larger ( approximately 14.2 billion years).Trends in Genetics 03/2004; 20(2):80-6. · 9.77 Impact Factor
Genomic data support the hominoid slowdown
and an Early Oligocene estimate for the
Michael E. Steiper†‡§, Nathan M. Young‡¶, and Tika Y. Sukarna?
Departments of†Anthropology and?Biological Sciences, Hunter College of the City University of New York, 695 Park Avenue, New York, NY 10021; and
¶Department of Cell Biology and Anatomy, University of Calgary, Calgary, AB, Canada T2N 4N1
Edited by David Pilbeam, Harvard University, Cambridge, MA, and approved October 27, 2004 (received for review September 30, 2004)
humans) and cercopithecoids (Old World monkeys) diverged
around 23–25 Mya. Importantly, although this range of dates has
been used as both an initial assumption and as a confirmation of
results in many molecular-clock analyses, it has not been critically
assessed on its own merits. In this article we test the robusticity of
the 23- to 25-Mya estimate with ?150,000 base pairs of ortholo-
gous DNA sequence data from two cercopithecoids and two
hominoids by using quartet analysis. This method is an improve-
ment over other estimates of the hominoid–cercopithecoid diver-
gence because it incorporates two calibration points, one each
within cercopithecoids and hominoids, and tests for a statistically
appropriate model of molecular evolution. Most comparisons re-
ject rate constancy in favor of a model incorporating two rates of
evolution, supporting the ‘‘hominoid slowdown’’ hypothesis. By
using this model of molecular evolution, the hominoid–cercopithe-
coid divergence is estimated to range from 29.2 to 34.5 Mya,
significantly older than most previous analyses. Hominoid–cerco-
pithecoid divergence dates of 23–25 Mya fall outside of the
confidence intervals estimated, suggesting that as much as one-
third of ape evolution has not been paleontologically sampled.
be difficult because derived features that define crown catarrhines
need not be present in early members of these lineages. More sites
that sample primate habitats from the Oligocene of Africa are
needed to better understand early ape and Old World monkey
evolution ? molecular clock ? primates
the oldest hominoid or cercopithecoid (Fig. 1). Proconsul is often
cited as the oldest hominoid at ?20 Mya (5, 6), although there is
some evidence of earlier apes: Morotopithecus is dated to ?20.6
is radiometrically dated to 24–27.5 Mya (8). Fossil cercopithecoids
are found at a number of Early Miocene African sites but are not
found in any context that predates the oldest hominoids (9–11).
time (12), Morotopithecus is the oldest undoubted hominoid or
cercopithecoid at ?21 Mya (13, 14). Molecular-clock analyses yield
interpolated hominoid–cercopithecoid divergence dates that are
largely congruent with the fossil record. Kumar and Hedges (3)
interpolated a divergence time of 23 Mya by using a combination
and rodents (110 Mya). Glazko and Nei (4) also calculated a date
at 90 Mya. The congruence of fossil and genetic estimates is
a 23- to 25-Mya estimate either as an initial assumption (15–17) or
as a confirmation of results (3, 18). If this estimate were found to
oth the fossil record and analyses of molecular data have been
crown catarrhine evolution. However, until now the robusticity of
the estimate has not been directly tested by any analysis. A more
23- to 25-Mya date is not as well supported as would first appear,
suggesting that a more specific test of the estimate is warranted.
First, whereas it is possible to estimate from fossils when a split
Mya) that the divergence must have occurred by this time, but it is
difficult to know just how much earlier the divergence might have
from the Fayum are well located in both time (36–33 Mya) and
space (Africa) to address this question. Primates from the Fayum
living catarrhines, and neither hominoids nor cercopithecoids ap-
pear among the Fayum fauna, suggesting that 33 Mya is a reason-
rest of this 33- to 21-Mya time span is so fossil poor in Africa,
particularly for primates (21, 22), that it is impossible to pinpoint
when the divergence had not occurred. Given this scarcity of
evidence, the fossil record is equally supportive of any divergence
time between 32 and 21 Mya.
Second, data sets that either interpolated a 23–25 Mya homi-
noid–cercopithecoid divergence date from an older calibration
16, 24, and 25) underestimate portions of the hominoid tree for
which we have good fossil evidence (14). For example, Kumar and
Hedges (3) estimate the human–chimpanzee divergence at 5.5 ?
0.2 Mya, a date that is at odds with recent discoveries of hominin
fossil material dating to as early as 7 Mya (26). When the afore-
mentioned data sets are instead calibrated by using a 7-Mya
hominin date, the hominoid–cercopithecoid split is pushed back
between 29–31 Mya (mean ? 30.1 Mya), significantly older than
23–25 Mya (1, 14). Reliance on a single fossil calibration point can
also be problematic if it is not well supported. For example, Kumar
and Hedges (3) have been criticized for the use of questionable
fossil calibrations for the divergence of both birds?mammals and
rodents?primates as well as their methodology (27). This criticism
evidence for evolutionary rate heterogeneity, with different mam-
has been questioned (38). While some studies run contrary to this
finding (39, 40), there is also considerable evidence for rate
heterogeneity within primates, particularly that hominoids are
This paper was submitted directly (Track II) to the PNAS office.
Abbreviation: Mya, million years ago.
‡M.E.S. and N.M.Y. contributed equally to this work.
§To whom correspondence should be addressed. E-mail: email@example.com.
© 2004 by The National Academy of Sciences of the USA
www.pnas.org?cgi?doi?10.1073?pnas.0407270101 PNAS ?
December 7, 2004 ?
vol. 101 ?
no. 49 ?
evolving slower than cercopithecoids (the ‘‘hominoid slowdown’’)
(15, 32, 34, 41–47). These findings conflict with the proposition of
a global molecular clock for mammals (23). Divergence dates
estimated with a constant rate of molecular change among all
lineages are likely complicated by such rate heterogeneity. Local
molecular clocks have been used to control for the rate variations
to date primate divergences (35, 48), but the heterogeneity within
catarrhine primates (i.e., the hominoid slowdown) has not yet been
incorporated into analyses specifically to estimate the hominoid–
Together these caveats suggest that from both molecular and
paleontological perspectives, the 23- to 25-Mya date for the homi-
noid–cercopithecoid divergence is not as strongly supported as is
frequently supposed. There is reason to believe that (i) fossil data
from the Oligocene and Early Miocene are much more equivocal,
(ii) interpolated molecular clock dates based on single fossil cali-
brations are not entirely consistent with the more robustly sup-
ported hominin fossil dates, and (iii) rate heterogeneity within
divergence using a method that has four major improvements over
previous studies. First, this method incorporates two fossil calibra-
tion points, one from within hominoids and one from within
cercopithecoids, to date a single divergence point. Second,
?150,000 base pairs of orthologous DNA sequence data are
analyzed to estimate the divergence time, a large increase over
maximum likelihood analyses, confidence intervals can be placed
around the date estimates, enabling a statistical test of the 23- to
25-Mya divergence of hominoids and cercopithecoids.
The divergence date for the hominoid–cercopithecoid split is
estimated by using a maximum likelihood-based quartet analysis
(49), a method that has found widespread taxonomic utility in
calculating divergence times (33, 49–56). Here this method is
expanded to large genomic contigs sequenced in catarrhine
primates. Quartet analyses use DNA sequence data from four
species, two species each from two clades that are monophyletic
with respect to one another. Within each pair, an independent,
paleontologically derived divergence date is used to calibrate the
divergence between the two pairs. In this case the two pairs are
hominoids (human and chimpanzee) and cercopithecoids (ma-
caque and baboon), and the divergence date estimated is the
hominoid–cercopithecoid split (Fig. 1). These four species were
chosen for two reasons: Within both pairs, fossil data are
available to estimate the divergence of the two species pairs with
reasonable confidence, and within each of these four species a
number of genomic contigs have been sequenced, allowing
alignment and analysis of large regions of orthologous DNA.
Divergence Dates. The split between the hominoid pair (human–
chimpanzee divergence) is calibrated by using the earliest known
hominin, Sahelanthropus tchadensis, which has been dated between
6 and 7 Mya by using faunal comparisons (26). This date is
supported by two other early hominins, Orrorin tugenensis (?5.8
Mya) (57) and Ardipithecus kadabba (5.2–5.8 Mya) (58). Although
there are no known fossil chimpanzees to date, this evidence
by at least 6 Mya, and possibly as early as 7 Mya. However, the lack
of an African ape fossil record in the late Miocene does not
preclude earlier dates. To reflect this uncertainty, divergence dates
of 6 and 7 Mya will be used as the human–chimpanzee divergence
date. The split between the cercopithecoid species is calibrated by
using an estimate for the split between macaques and baboons?
mangabeys (together known as papionins). According to Delson et
al. (9), the earliest fossil evidence of papionins is from teeth found
in North Africa and Kenya of late Miocene age (6–8 Mya).
Macaques are known from North Africa (77) and Europe (78) by
5.5 Mya, and there is evidence of their arrival in Asia at about the
the middle to late Pliocene: ?4–2 Mya. Delson (10) and Delson et
al. (9) estimate the split at ?7–8 Mya. Conservatively, we use
macaque–baboon divergence dates of 5 and 7 Mya.
Assembly of Genomic Contigs.Wedesignedamethodtoidentifyand
in humans (Homo sapiens), chimpanzees (Pan troglodytes), rhesus
macaques (Macaca mulatta), and anubis baboons (Papio anubis).
The data assembly method had five steps. First, a database was
constructed of all of the completely sequenced genomic contigs
from both Papio and Macaca available in GenBank. All of the
repeat elements (e.g., Alu insertions, LINEs) were removed from
these contigs by using REPEATMASKER (available from Smit and
Green at http:??repeatmasker.org), resulting in a database of
‘‘masked’’ contigs. Second, each Papio contig was compared to the
masked Macaca database by using BLAST (59) to find contigs that
were orthologous between the two species. A reciprocal BLAST
of corresponding contigs, five nonoverlapping pairs were chosen.
Third, BLAST was used to identify the contigs available in GenBank
from humans and chimpanzees that were orthologous to the five
cercopithecoid contig pairs. Once identified, the repeat elements
were removed from the hominoid contigs. In total, 39.51% of the
contig base pairs were identified as repeat elements. Fourth, these
five sets, each containing one contig each from human, chimpan-
††Delson, E. (1996) in Abstracts, International Symposium: Evolution of Asian Primates
(Primate Research Institute, Inuyama, Japan), p. 40.
and the dates and names of fossil taxa relevant to the divergences among
Phylogeny of the four taxa analyzed by using the quartet method,
www.pnas.org?cgi?doi?10.1073?pnas.0407270101 Steiper et al.
common to all four species. These five sets were aligned by using
CLUSTALW and CLUSTALX (60, 61) and reviewed to remove any
remaining regions of nonhomology. Finally, all non-point muta-
tions, such as mutated CpG sites, mononucleotide repeat stretches,
and other complex mutations, were removed from the alignments.
case of CpG sites (62). Omission of these sites, which totaled 1.5%
of the total data set, had no significant impact on the results (when
greater than the estimate presented here). This method resulted in
five alignments of orthologous, nonrepeat DNA sequences, each
referred to as a ‘‘contig set’’ (Table 1).
Likelihood Ratio Testing and Quartet Dating Analysis. These contig
sets, in conjunction with the two divergence dates, were used to
QDATE program (Version 1.1) (49). The method calculated likeli-
hoods assuming the HKY model of molecular evolution (63) with
a gamma correction for site-specific rate heterogeneity (64)
(HKY??) and a user-defined transition?transversion ratio [both
parameters estimated by using maximum likelihood in PAUP* (65)]
impact on estimation of divergence dates (66), in the present case
estimated divergence dates were robust to the use of different
models (data not shown). Likelihood values were calculated under
three different conditions of lineage specific rate heterogeneity.
this condition, a single rate of molecular evolution was assumed for
all of the branches of the tree, a constant (or global) molecular
clock. Second, the likelihoods of the ‘‘two-rate’’ condition were
calculated, assuming one rate of molecular evolution for the
hominoid branches and a second rate for the cercopithecoid
‘‘free-rate’’ condition was examined, where each branch was al-
lowed to evolve at its own rate and no molecular clock is assumed.
Comparing the likelihoods under these different conditions, rate
constancy can be examined with a likelihood ratio test (67) using a
likelihood values between the given conditions, as implemented in
QDATE. First, the one-rate condition is tested against the free-rate
condition, to test whether one rate of molecular evolution charac-
free-rate condition, to test whether a model where cercopithecoids
and hominoids are evolving at two different rates is a statistically
better fit than a model with each branch allowed to evolve at a
different rate (essentially a test of the hominoid slowdown hypoth-
esis). Subsequently, when using comparisons where rate constancy
holds (one-rate or two-rate), the branch lengths will be converted
to ordinal dates, using the calibration points discussed above. The
statistically defined confidence intervals on these dates are calcu-
lated as described in Rambaut and Bromham (49). Here, an
additional degree of uncertainty in the date estimates of the
hominoid and cercopithecoid divergence is incorporated in the
within hominoids and cercopithecoids (discussed above).
Results and Discussion
Likelihood ratio tests were constructed to assess whether one or
more molecular clocks characterized the evolution of the hominoid
and cercopithecoid lineages with each of the four different fossil
divergence date estimates (Table 2). In none of the contig sets did
all four comparisons support rate constancy among the hominoids
and cercopithecoids. In three contig sets (A, C, and E), two of the
four comparisons were consistent with rate constancy, and in the
remaining two contig sets (B and D) there were no comparisons
consistent with rate constancy. In total, 6 of 20 comparisons were
evolving in a clock-like fashion. Overall, these data do not support
However, decreasing the hominoid calibration to dates younger
than 6 Mya would be inconsistent with the hominid fossil record,
and increasing the cercopithecoid calibration substantially past 7
Mya has no fossil justification.
The comparisons that exhibited rate constancy allow an estimate
of the hominoid–cercopithecoid divergence with a constant mo-
lecular clock. Within each contig set, only contig set A had a
confidence interval overlapping a 23- to 25-Mya divergence. In no
Table 1. Summary contig set information
Contig setContigsBase pairs
B 23,3741.87 1.16
C 11,8561.66 3.03
D 63,965 2.190.55
†Parameter for the gamma rate heterogeneity correction.
Steiper et al.
December 7, 2004 ?
vol. 101 ?
no. 49 ?
cases did the average estimated confidence intervals overlap a 23-
to 25-Mya hominoid–cercopithecoid divergence. The global aver-
age of the hominoid–cercopithecoid divergence dates consistent
with rate constancy was 32.2 Mya, with an average lower bound of
divergence date for hominoids and cercopithecoids.
Under a constant molecular clock, rate estimates for all five
contig sets ranged from 5.20 ? 10?10to 9.83 ? 10?10substitutions
five distinct contigs, but also incorporates paleontological uncer-
tainty for both the hominoid and cercopithecoid divergence dates.
However, as shown, the assumption of a constant molecular clock
is not valid for most of the comparisons, and these estimates are
therefore not preferred. When restricted to the comparisons fitting
the one-rate model, the global average is 6.28 ? 10?10substitutions
per site per year. This estimate is ?3 times slower than a global
nuclear molecular clock estimated for placental mammals (22.2 ?
10?10) (23), estimated in part by using a 5.5-Mya divergence for
humans and chimpanzees and a 23-Mya divergence for hominoids
and cercopithecoids. The rates derived here are more similar to
those estimated exclusively from humans and chimpanzees, 7.9 ?
10?10, which used a 7.5-Mya divergence for these taxa (34). When
both cercopithecoids and hominoids are analyzed, Yi et al. (34)
estimated a rate of 15 ? 10?10substitutions per site per year when
using a 23-Mya divergence between these taxa and 11.7 ? 10?10
when using a 30-Mya divergence date. Rates estimated here with a
one-rate model are more similar to those estimated from only
primates, suggesting that within mammals, different groups evolve
at different rates.
Unlike the above cases, there were no significant differences
found between the two- and the free-rate models for any
tests show that when each branch is allowed to evolve at a
different rate, they fall into two rate categories, with one rate for
hominoids and a second rate for cercopithecoids. Of the five
contig sets, four show cercopithecoids evolving more quickly
than hominoids. When partitioned, hominoids are evolving at an
average rate of 5.86 ? 10?10substitutions per site per year,
whereas cercopithecoids are evolving 1.45 times faster at 8.52 ?
10?10. These tests and the rates of molecular evolution derived
Table 2. Likelihood ratio tests and estimated divergence dates for the hominoid–cercopithecoid split
One-rate tests Two-rate tests
One-rate vs. free-rate
estimates, Mya Two-rate vs. free-rate
34.3 29.8 39.9
†Substitution rate per site per million years ? 10?10.
‡Differences between likelihood values in the two models.
§Significance as determined by a likelihood ratio test (?, P ? 0.5; ??, P ? 0.01). n.s., not significant.
¶Maximum likelihood estimate of the divergence date for hominoids and cercopithecoids.
?Lower 95% boundary.
**Upper 95% boundary.
††Substitution rate in hominoids per site per million years ? 10?10.
‡‡Substitution rate in cercopithecoids, expressed as a ratio in terms of rate 1.
www.pnas.org?cgi?doi?10.1073?pnas.0407270101 Steiper et al.
for these species strongly support the hominoid slowdown hy-
pothesis as first proposed by Goodman (41).
By using the two rates estimated for these taxon pairs, a date for
the hominoid–cercopithecoid divergence can be estimated. Within
each contig set, the average divergence dates yield different esti-
mates for the hominoid–cercopithecoid divergence. By examining
the within-contig set averages, the uncertainty of the paleontologi-
split. Contig A has the youngest average for the maximum likeli-
hood estimates (27.0 Mya), and contig E has the oldest (36.2 Mya).
The youngest average lower bound was 24.9 Mya, and the highest
Oligocene. However, of the 20 comparisons, only 2 had confidence
intervals that overlap a 23-Mya divergence with 3 additional
comparisons overlapping a 25-Mya divergence (Fig. 2). When
incorporating the paleontological uncertainty in the divergence
within each pair, these estimates underscore the heterogeneity in
divergence estimates between each of the contig sets.
The average dates within each contig set were further averaged
to reduce the heterogeneity due to differences among the contig
within the hominoids and cercopithecoids. The youngest average
date of the hominoid–cercopithecoid divergence, 27.7 Mya, was
found by using the youngest hominoid and cercopithecoid calibra-
tion points (6 Mya and 5 Mya, respectively). The average lower
bound for this estimate was 25.6 Mya. Divergence dates of 7 Mya
for hominoids and 7 Mya for cercopithecoids produced the oldest
average estimate, 36.0 Mya, with an average lower bound of 33.2
Mya. In averaging across the contig sets, none of the divergence
dates have average confidence intervals that encompassed a 23- to
from 29.2 to 34.5 Mya. This range reflects both statistical and
paleontological uncertainty, as discussed in Methods. With addi-
tional fossil evidence, the fossil calibration points within cerco-
pithecoids and hominoids may be revised, refining this estimate
may preclude a human–chimpanzee divergence younger than 7
It is interesting to note that the only contig set that was evolving
close to a constant rate, set A, yielded the youngest divergences for
the hominoid–cercopithecoid split. However, as shown from the
remaining contigs where rate heterogeneity is considerable, the
estimated divergence estimates are significantly older. This con-
Two findings suggest possible biases for our estimate of the
hominoid–cercopithecoid divergence. First, simulations show that
early single calibration points can bias clock estimates of older
divergence dates upwards (68). In these simulations, the estimated
dates begin to converge on the actual dates when the length of the
simulated data sets approached 500 aa. Our study likely overcomes
this bias, because each of the five contig sets analyzed is ?12,000
base pairs. A second potential for bias is in the sample of contigs
analyzed, which are all homologous to human chromosome 7.
Evidence shows that the substitution rate differs among hominoid
chromosomes (69). However, these substitution regimes are con-
served over large phylogenetic distances (69) and therefore it is not
correspondence of the present data to two other studies further
suggests that the present study is not biased. A study of mitochon-
drial genomes (35) suggested a 30- to 40-Mya cercopithecoid–
hominoid divergence when employing local molecular clocks.
DNA–DNA hybridization studies (24, 70) when recalibrated with a
7-Mya human–chimpanzee divergence, date the hominoid–
cercopithecoid divergence to ?30 Mya (14). These findings are
within the confidence intervals presented here.
A 29.2- to 34.5-Mya range for the hominoid–cercopithecoid split
is significantly older than is usually estimated, implying that ?10
million years of ape and Old World monkey evolution are largely
unsampled. The most obvious reason for this underestimation is
that the lack of definitive hominoid or cercopithecoid fossils from
the Early and Late Oligocene has been erroneously viewed as
sites in the period between 33 and 21 Mya on which to make this
assessment (the Fayum, Lothidok, and Chilga). Of these, only
Lothidok (24–27.5 Mya) has produced a possible hominoid or
cercopithecoid primate (Kamoyapithecus), although it cannot be
definitively linked to either catarrhine group. Our estimate of the
divergence time suggests that the absence of hominoid or cerco-
pithecoid fossils is likely due to other factors: current sites sample
inappropriate fauna?environments, are taphonomically biased
(only large-bodied fauna), or are incompatible with the preserva-
tion of primate fossils (low densities of hominoids?cercopithecoids
compared with other mammals).
In addition, identifying stem hominoids or cercopithecoids from
this 33- to 21-Mya gap is potentially problematic. Derived features
used to characterize these groups may not be present in early
members, making it difficult to determine whether a catarrhine
from the Early or Late Oligocene is a stem catarrhine, stem
Divergence date estimates for the hominoid–cercopithecoid split based on the two-rate model for each contig set (A–E) and the weighted mean
Steiper et al.
December 7, 2004 ?
vol. 101 ?
no. 49 ?
this problem: dental similarities of hominoids are primitive for
catarrhines (71–74), complicating any assessment of its phyloge-
netic position. Even Proconsul, which is often considered to be a
stem hominoid ancestral to all other known apes, has been sug-
it has few derived features linking it to hominoids other than the
absence of a tail and large body size (72, 76). Compared with
Aegyptopithecus, cercopithecoid taxa are more postcranially and
features such as bilophodonty are not present in the earliest
members of this lineage. Indeed, at the time of their divergence
similar as sister species and virtually unrecognizable as precursors
to more distinct groups, raising the possibility that easily recogniz-
able traits such as the absence of a tail or the presence of
cercopithecoids. In this context, supposed stem catarrhines such as
Dendropithecus or Limnopithecus (72) may be more closely related
to either hominoids or cercopithecoids than previously thought.
members of two closely related lineages, but a reassessment of
the distance between our estimated divergence and what is known
from the fossil record. This gap in our knowledge underscores how
poorly we understand the earliest portions of ape and Old World
monkey evolution and indicates that finding new sites within
will be critical to reconstructing the earliest portions of their
We thank W.-G. Qiu, C. Roos, J. Rossie, and two anonymous reviewers
for comments on the manuscript. T.Y.S. thanks W.-G. Qiu and the
Evolutionary Bioinformatics Laboratory at Hunter College for compu-
tational support. Some of the sequence data used were generated by the
National Institutes of Health (NIH) Intramural Sequencing Center
(www.nisc.nih.gov). This work was supported by Research Centers in
Minority Institutions Award RR-03037 (to M.E.S.) from the National
Center for Research Resources (NCRR) of the NIH, which supports the
infrastructure of the Anthropological Genetics Laboratory at Hunter
College, and by Cora du Bois Charitable Trust and American School for
Prehistoric Research graduate fellowships (to N.M.Y.).
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www.pnas.org?cgi?doi?10.1073?pnas.0407270101 Steiper et al.