Macroevolutionary Dynamics and Historical Biogeography of Primate Diversification Inferred From A Species Supermatrix

Macroevolutionary Dynamics and Historical
Biogeography of Primate Diversification Inferred from a

Species Supermatrix
Mark S. Springer1*, Robert W. Meredith1,2, John Gatesy1, Christopher A. Emerling1, Jong Park1,3,
Daniel L. Rabosky4,5, Tanja Stadler6, Cynthia Steiner7, Oliver A. Ryder7, Jan E. Janečka8,
Colleen A. Fisher8, William J. Murphy8*
1 Department of Biology, University of California Riverside, Riverside, California, United States of America, 2 Department of Biology and Molecular Biology, Montclair State
University, Montclair, New Jersey, United States of America, 3 Department of Biology, University of Washington, Seattle, Washington, United States of America,
4 Department of Integrative Biology, University of California, Berkeley, California, United States of America, 5 Department of Ecology and Evolutionary Biology, University
of Michigan, Ann Arbor, Michigan, United States of America, 6 Institut für Integrative Biologie, Eidgenössiche Technische Hochschule Zurich, Zurich, Switzerland, 7 San
Diego Zoo Institute for Conservation Research, San Diego Zoo Global, San Diego, California, United States of America, 8 Department of Veterinary Integrative Biosciences,
Texas A&M University, College Station, Texas, United States of America
Abstract
Phylogenetic relationships, divergence times, and patterns of biogeographic descent among primate species are both
complex and contentious. Here, we generate a robust molecular phylogeny for 70 primate genera and 367 primate species
based on a concatenation of 69 nuclear gene segments and ten mitochondrial gene sequences, most of which were
extracted from GenBank. Relaxed clock analyses of divergence times with 14 fossil-calibrated nodes suggest that living
Primates last shared a common ancestor 71–63 Ma, and that divergences within both Strepsirrhini and Haplorhini are
entirely post-Cretaceous. These results are consistent with the hypothesis that the Cretaceous-Paleogene mass extinction of
non-avian dinosaurs played an important role in the diversification of placental mammals. Previous queries into primate
historical biogeography have suggested Africa, Asia, Europe, or North America as the ancestral area of crown primates, but
were based on methods that were coopted from phylogeny reconstruction. By contrast, we analyzed our molecular
phylogeny with two methods that were developed explicitly for ancestral area reconstruction, and find support for the
hypothesis that the most recent common ancestor of living Primates resided in Asia. Analyses of primate macroevolutionary
dynamics provide support for a diversification rate increase in the late Miocene, possibly in response to elevated global
mean temperatures, and are consistent with the fossil record. By contrast, diversification analyses failed to detect evidence
for rate-shift changes near the Eocene-Oligocene boundary even though the fossil record provides clear evidence for a
major turnover event (‘‘Grande Coupure’’) at this time. Our results highlight the power and limitations of inferring
diversification dynamics from molecular phylogenies, as well as the sensitivity of diversification analyses to different species
concepts.
Citation: Springer MS, Meredith RW, Gatesy J, Emerling CA, Park J, et al. (2012) Macroevolutionary Dynamics and Historical Biogeography of Primate
Diversification Inferred from a Species Supermatrix. PLoS ONE 7(11): e49521. doi:10.1371/journal.pone.0049521
Editor: Roscoe Stanyon, University of Florence, Italy
Received May 17, 2012; Accepted October 9, 2012; Published November 16, 2012
Copyright: ß 2012 Springer et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by NSF (EF0629860 to MSS and JG; EF0629849 to WJM). The funders had no role in study design, data collection and analysis,
decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: [email protected] (MS); [email protected] (WJM)
Introduction Groves [4] recognized 233 primate species in his 1993

classification. Since that time, the number of primate species has
Primates comprise an ecologically, morphologically, and taxo- increased steadily, with 354 and 376 species in Groves’ 2001 [5]
nomically diverse order of mammals. The oldest stem primates and 2005 [6] classifications, respectively. We estimate that the
(i.e., ‘‘Plesiadapiformes’’) are from the earliest Paleocene of North number of living primate species is at least 450 when Groves’ [6]
America [1], whereas the fossil record of crown primates begins classification is augmented with newly recognized species (Text
with the appearance of taxa in Western North America, Western S1). The increase in the number of primate species has been
Europe, Africa, and Asia at or near the Paleocene/Eocene driven by widespread adoption of the phylogenetic species concept
boundary [1,2]. Extant primates are widely distributed throughout by primate taxonomists and the application of genetic methods
tropical and subtropical regions of Africa, Madagascar, Asia, and that allow for the discovery of young evolutionary lineages that
the New World, although the fossil record is depauperate in would otherwise go undetected [5–11].
several regions where extant primate diversity is highest including Analyses of phylogenetic relationships and divergence times
Madagascar, the Congo Basin, Southeast Asia, and the Amazon among primate species are critical for understanding the
Basin [3]. evolutionary and biogeographic history of this group, including
PLOS ONE | www.plosone.org 1 November 2012 | Volume 7 | Issue 11 | e49521

Primate Biogeography and Diversification
patterns of diversification in relationship to environmental changes matrix, 7,140,500 (31.4%) are filled by nucleotides and the
throughout the Cenozoic and the role of dispersal to previously remainder are either missing or gaps (68.6%). The mean number
uncolonized areas in promoting diversification. Accurate phylog- of nucleotides per taxon is 19,194.9. Taxon completeness for the
enies also provide an essential framework for informing decisions concatenated data set ranged from 34 taxa (ABO) to 276 taxa
in conservation biology and understanding the emergence of (cytochrome b), with a mean of 138.3 taxa per locus. Gene
zoonotic diseases [12]. completeness for the concatenated data set ranged from one locus
Purvis [13] provided the first comprehensive estimate of per taxon to 77 loci per taxon with a mean of 29.4 loci per taxon.
phylogenetic relationships among living primates based on super- The nuclear data set included 243 taxa and 51,801 bp. Mean
tree methods and included all 203 species that were recognized by completeness for the nuclear data set was 136 taxa per gene
Corbett and Hill [14]. The most comprehensive analyses of segment (taxon completeness) and 25.1 loci per taxon (gene
primate relationships based on molecular supermatrices are those completeness). The mitochondrial data set included 355 taxa,
of Chatterjee et al. [15], Fabre et al. [3], and Perelman et al. [12], 9398 bp, and mean completeness of 154.2 taxa per mitochondrial
who included 219, 271, and 186 primate species, respectively. gene (taxon completeness) and 4.1 mitochondrial genes per taxon
Fabre et al.’s [3] data set included the greatest number of primate (gene completeness). In almost all cases where a taxon was
species, but Perelman et al.’s [12] data matrix comprised the represented by a single locus, the singleton was a mitochondrial
largest number of gene loci (54 nuclear segments) and had the gene (cytochrome b, cytochrome oxidase II, 12S rRNA, or 16S
lowest percentage (18) of missing data. The majority of nodes were rRNA) with overlapping sequences among congeners in the data
recovered with 100% bootstrap support in Perelman et al.’s [12] set. The only exception is Gorilla beringei, which is represented by a
analysis, although these authors only included 41–49% of extant CXCR5 sequence that shares both congeneric (G. gorilla) and
primate species if we allow that there are 376–450 living species. confamilial (Homo sapiens, Pan troglodytes) overlap.
Recent studies have also estimated divergence times among
primate species based on relaxed clock methods [3,12,15]. Phylogenetic Analyses
Molecular divergence estimates are in good agreement for some Figure 1 shows the maximum likelihood bootstrap tree for 70
nodes (e.g., Simiiformes, Catarrhini, Platyrrhini) but show more primate genera that were included in our analysis. Species level
disagreement deeper in the tree (e.g., Primates, Strepsirrhini, trees for Strepsirrhini, Tarsiiformes+Platyrrhini, Cercopithecoi-
Haplorhini). For example, relaxed clock estimates for the base of dea, and Hominoidea are shown in Figures 2, 3, 4, and 5,
primates range from 63.7 Ma [15] to 87.2 Ma [12]. These respectively. The ML phylogram for 367 primate species is
differences have profound implications for interpreting the history provided in Text S2. Primate suborders (Haplorhini, Strepsir-
of primate diversification in relationship to important events in rhini), infraorders (Simiiformes, Tarsiiformes, Lemuriformes,
earth history such as the Cretaceous-Paleogene (KPg) mass Lorisiformes), parvorders (Catarrhini, Platyrrhini), and superfam-
extinction. ilies (Hominoidea, Cercopithecoidea) (sensu [12]) were recovered
The biogeographic history of Primates is also contentious. Beard with 99–100% bootstrap support. All primate families were
[16] suggested that the common ancestor of living primates was recovered as monophyletic with 100% bootstrap support except
Asian; Silcox [2] suggested that Africa, Asia, Europe, and North for Cebidae (99%), Lorisidae (63%), and Cheirogaleidae (56%).
America are all possible places of origin; and Bloch et al. [1] Bootstrap support for most primate genera was 100%, but in a few
concluded that the common ancestor of living primates was either cases support was slightly lower (Hapalemur = 99%, Miopithe-
Asian or North American. All of these studies used Fitch cus = 99%, Callithrix = 98%, Saguinus = 98%, Chlorocebus = 90%) or
parsimony to reconstruct ancestral areas, but this approach has genera were not recovered as monophyletic (Trachypithecus,
shortcomings when applied to ancestral area reconstructions Semnopithecus, Cercopithecus, Galago). Mean bootstrap support per-
[17,18]. centages for all primate nodes, primate nodes at and above the
In the present study we assembled a molecular supermatrix, level of genus, and primate nodes below the level of genus were
primarily from previously published GenBank sequences, for 367 86.2%, 95.5%, and 82.1%, respectively.
extant primate species and reconstructed phylogenetic relation-
ships using maximum likelihood. We also performed timetree Timetree Analyses
analyses with relaxed clock methods and a more comprehensive Divergence times for 367 primates based on analyses with
assemblage of calibrations than previous studies. Ancestral area autocorrelated rates and soft-bounded constraints are shown in
reconstructions were performed with methods that were developed Figures 1, 2, 3, 4, 5. Mean divergence dates and composite 95%
specifically for historical biogeography [17–19], and the resulting credibility intervals for key nodes are provided in Table 1. Median
ancestral area chronograms were used as a framework for dates, mean dates, and 95% credibility intervals for analyses with
understanding the history of trans-continental dispersal in the autocorrelated rates and hard-bounded constraints (AUTOhard),
ancestors of primates with extant descendants. Finally, we autocorrelated rates and soft-bounded constraints (AUTOsoft),
performed diversification analyses to determine if a molecular independent rates and hard-bounded constraints (IRhard), and
phylogeny for primates retains the signature of historical events independent rates and soft-bounded constraints (IRsoft) are given
that have increased or decreased diversification rates, and in Table S1 for all primate nodes (numbered in Fig. S1). Newick
ascertained if diversification rate changes are sensitive to the timetrees based on each analysis are provided in Text S2.
application of the phylogenetic species concept. Mean divergence dates based on four molecular dating analyses
ranged from 71.4262.8 Ma for Primates, 55.3253.3 Ma for
Results Strepsirrhini, and 64.2258.4 for Haplorhini (Table S1). Analyses
with hard-bounded constraints provided younger dates
Primate Supermatrix (58.6258.5) for Haplorhini than did soft-bounded analyses
The concatenated data set included 372 taxa (367 primates, five (64.2263.3 Ma). Within Strepsirrhini, the basal split among
outgroups) and was 61,199 base pairs (bp) after excluding Malagasy taxa (Chiromyiformes to Lemuriformes) was dated at
ambiguous regions of the alignment for the mitochondrial 12S 50.5249.2 Ma whereas Galagidae and Lorisidae separated from
and 16S rRNA genes. Among the 22,766,028 cells in the data each other at 37.4231.4 Ma. The base of Tarsiiformes was dated

Figure 1. A timetree for 70 primate genera based on mcmctree with autocorrelated rates and soft-bounded constraints. The tree was
rooted with five outgroups from Lagomorpha, Scandentia, and Dermoptera (not shown). All nodes without filled circles were recovered with$95%
bootstrap support in maximum likelihood analyses with RAxML. Black, gray, and white filled circles indicate nodes that were recovered with 70
to,95% bootstrap support, 50 to,70% bootstrap support, and,50% bootstrap support, respectively. The full timetree with 367 primate species and
five outgroups is provided in Text S2. Also see Figure 2 (strepsirrhines), Figure 3 (tarsiiforms+platyrrhines), Figure 4 (cercopithecoid), and Figure 5
(hominoids). Calibrated nodes are indicated with numbers and are cross-referenced to Text S3. Paintings by Carl Buell.
doi:10.1371/journal.pone.0049521.g001

Figure 2. Strepsirrhine portion of mcmctree timetree (autocorrelated rates, soft-bounded constraints). Nodes without filled circles and
nodes with black, gray, and white filled circles are as in Figure 1. Primate species that were represented by a single locus in the RAxML analysis with
the combined (nuclear+mitochondrial) data set are denoted with asterisks. Paintings by Carl Buell.

Figure 3. Tarsiiform and platyrrhine portion of mcmctree timetree (autocorrelated rates, soft-bounded constraints). Nodes without
filled circles and nodes with black, gray, and white filled circles are as in Figure 1. Primate species that were represented by a single locus in the
RAxML analysis with the combined (nuclear+mitochondrial) data set are denoted with asterisks. Paintings by Carl Buell.
at 24.9223.0 Ma in analyses with autocorrelated rates but only older than dates based on independent rates for Simiiformes
13.5213.2 Ma in analyses with independent rates. Similarly, (44.5242.8 versus 37.7237.4 Ma) and most of its constituent
molecular dates based on autocorrelated rates were consistently clades including Catarrhini (28.8227.7 versus 22.5221.3 Ma),

Figure 4. Cercopithecoid portion of mcmctree timetree (autocorrelated rates, soft-bounded constraints). Nodes without filled circles
and nodes with black, gray, and white filled circles are as in Figure 1. Primate species that were represented by a single locus in the RAxML analysis
with the combined (nuclear+mitochondrial) data set are denoted with asterisks. Paintings by Carl Buell.

Figure 5. Hominoid portion of mcmctree timetree (autocorrelated rates, soft-bounded constraints). Nodes without filled circles and
nodes with black, gray, and white filled circles are as in Figure 1. Primate species that were represented by a single locus in the RAxML analysis with
the combined (nuclear+mitochondrial) data set are denoted with asterisks. Paintings by Carl Buell.
Cercopithecidae (15.7215.6 versus 11.4210.1 Ma), Hominoidea summarized in Figures 6 and 7, respectively, and in Table 2. Asia
(20.9220.2 versus 14.7213.6 Ma), Hominidae (18.0217.3 versus was reconstructed as the ancestral area of Primates, Haplorhini,
13.0212.1 Ma), Hylobatidae (7.8 versus 6.025.2 Ma), Platyrrhini Catarrhini, and Hominoidea by both methods. The ancestral area
(24.3224.0 versus 23.4221.5 Ma), Cebidae (20.7220.6 versus of Strepsirrhini was reconstructed as Asia+Madagascar by DEC
19.6218.1 Ma), Pitheciidae (20.9220.7 versus 19.7218.1 Ma), (Fig. 6) and Asia or Africa or Madagascar by MAC parsimony
and Atelidae (17.3 versus 13.6212.5 Ma). Among monophyletic (Fig. 7). Lorisiformes was reconstructed to have an ancestral area
genera the oldest basal divergences were in Cheirogaleus that included both Asia and Africa by DEC (Fig. 6) and one or
(11.627.6 Ma) and Lepilemur (10.227.3 Ma), whereas basal both of these areas by MAC parsimony (Fig. 7). The ancestral area
divergence dates were less than one million years in all analyses for Simiiformes was either Asia+New World (DEC) (Fig. 6) or Asia
for Loris, Varecia, Mirza, Leontopithecus, and Lophocebus (Figs. 2, 3, 4, (MAC parsimony) (Fig. 7).
Table S1). DEC results suggest that there have been seven dispersal events
Using soft bounds, six timetree dates were either younger than between the four areas: one dispersal to Madagascar in the
the minimum date or older than the maximum date. AUTOsoft ancestor of Strepsirrhini, one dispersal to the New World in the
and IRsoft analyses returned dates of 31.4 and 32.8 Ma for ancestor of Simiiformes, three dispersals to Africa (ancestors of
Lorisiformes, respectively, both of which are younger than the Lorisiformes, hominids, and cercopithecids, respectively), and two
minimum age of 37.1 Ma. The maximum age of Haplorhini dispersals to Asia (ancestors of Macaca and Papio hamadryas,
(58.9 Ma) was also violated in both the AUTOsoft (63.3 Ma) and respectively) (Fig. 6), although we note that the occurrence of P.
IRsoft (64.2 Ma) analyses. Finally, IRsoft analyses returned dates hamadryas in Asia is restricted to the Arabian Peninsula. Other
for Macaca to other Papionini (4.5 Ma) and Theropithecus to changes in area are the result of range inheritance at cladogenic
Papio+Rungwecebus+Lophocebus (2.4 Ma) that were slightly younger events. MAC parsimony results suggest that there have been 18
than minimum constraints for these clades (5.5 and 3.5 Ma, gains or losses of area in the evolutionary history of extant
respectively). primates lineages, with a minimum of seven gains of area
(Madagascar, New World, Asia 6 2, Africa 6 3) and a maximum
Ancestral-Area Reconstructions of ten gains of area (Madagascar, New World, Asia 3 to 5 times,
The results of dispersal-extinction-cladogenesis (DEC) [17,19] Africa 3 to 5 times). However, the only gains or losses of area that
and minimum area change (MAC) parsimony [18] analyses are were reconstructed unambiguously were gain of the New World in

Table 1. Mean divergence dates and 95% composite credibility intervals in millions of years for select nodes based on four
mcmctree chronograms (autocorrelated rates with hard-bounded constraints, autocorrelated rates with soft-bounded constraints,
independent rates with hard-bounded constraints, independent rates with soft-bounded constraints).
Mean Divergence Composite 95% Composite 95%

Clade Date Credibility Minimum Credibility Maximum
Primates 67.84 60.99 76.72

Strepsirrhini 54.23 48.75 57.22
Lorisiformes 34.74 27.9 38.24
Galagidae 22.67 16.2 32.22
Galago+Otolemur 15.08 11.18 21.06
Lorisidae 32.28 25.58 36.31
Loris 0.43 0 2.56
Nycticebus 5.27 3.54 7.91
Arctocebus 0.83 0.04 3.51
Lemuriformes+Chiromyiformes 49.96 45.16 53.78
Lemuriformes 31.77 26.73 36.64
Lemuridae 20.73 15.28 25.97
Varecia 0.70 0.28 1.68
Hapalemur 4.09 1.54 8.1
Eulemur 6.21 4.21 9.47
Indriidae+Cheirogaleidae+Lepilemuridae 30.65 25.62 35.45
Lepilemuridae 8.51 6.15 12.71
Cheirogaleidae (w/o Phaner) 21.84 17.39 26.62
Mirza 0.50 0.05 2.13
Microcebus 6.92 4.97 8.81
Cheirogaleus 9.34 4.86 17.77
Indriidae 18.45 11.71 25.51
Avahi 6.45 2.72 11.37
Propithecus 6.04 3.93 9.39
Haplorhini 61.16 57.62 69.59
Tarsiiformes 18.64 8.75 37.19
Tarsius 5.14 1.29 13.52
Simiiformes 40.60 33.55 49.48
Platyrrhini 23.32 19.26 27.49
Pitheciidae 19.85 15.97 23.83
Cacajao 2.90 1.6 4.42
Chiropotes 2.67 1.1 5.03
Pithecia 3.46 1.97 6.01
Callicebus 7.64 5.16 10.38
Atelidae 15.17 10.94 20.18
Alouatta 3.68 2.44 5.15
Brachyteles 2.65 1.3 5.12
Lagothrix 1.038 0.34 2.89
Ateles 2.82 1.58 4.43
Cebidae 19.73 16.07 23.56
Saimiri+Cebus 17.25 13.76 20.79
Saimiri 1.75 1.06 2.88
Cebus 5.7 3.55 8.33
Saguinus 6.65 4.82 8.69
Leontopithecus 0.52 0.21 1.1
Callithrix 6.51 3.81 11.44
Aotus 3.31 2.09 4.43

Table 1. Cont.
Mean Divergence Composite 95% Composite 95%

Clade Date Credibility Minimum Credibility Maximum
Catarrhini 25.07 19.67 32.83

Hominoidea 17.36 12.44 23.9
Hominidae 15.09 11.04 20.8
Pongo 1.28 0.51 2.99
Homininae 8.03 5.53 11.66
Homo+Pan 6.66 4.74 9.5
Pan 1.62 0.67 3.5
Gorilla 1.69 0.01 4.64
Hylobatidae 6.68 3.92 9.73
Hoolock 1.96 0.22 4.4
Hylobates 2.99 1.62 4.68
Nomascus 2.66 1.22 4.19
Cercopithecidae 13.17 8.93 18.27
Cercpithecinae 8.35 5.41 11.6
Papionini 6.47 3.94 9.13
Macaca 3.8 2.34 5.47
Papio 1.07 0.55 1.66
Lophocebus 0.24 0.01 0.65
Cercopithecini 6.15 3.78 8.96
Cercopithecus+Cercocebus+Erythrocebus 5.68 3.45 8.36
Miopithecus 2.96 0.85 6.73
Colobinae 8.85 6.25 12.04
Presbytini 6.69 4.59 9.29
Trachypithecus+Semnopithecus 4.17 2.08 6.84
Rhinopithecus 2.54 1.27 3.79
Pygathrix 1.49 0.59 3
Presbytis 3.81 2.14 5.73
Colobini 6.83 4.68 9.46
Piliocolobus 3.41 1.97 4.66
Colobus 3.79 1.99 6.13
Median dates, mean dates, and 95% credibility intervals for individual chronograms are given in Table S2.
doi:10.1371/journal.pone.0049521.t001
the ancestor of Platyrrhini, gain of Africa in the ancestor of recent common ancestor of Strepsirrhini was reconstructed as
Homininae, gain of Asia in Papio hamadryas, and gain of Asia in the African, Madagascan, or equivocal (at least three of North
common ancestor of Asian Macaca (Fig. 7). America, Africa, Europe, Madagascar, Asia). All of the analyses
MAC parsimony analyses with a combination of extinct and that reconstructed Madagascar as the exclusive area of Strepsir-
extant taxa and eight different topologies from Seiffert et al. [20] rhini were based on topologies with paraphyletic Lemuriformes.
are summarized in Table 2. Analyses with five areas (North Finally, the ancestral area for crown+stem primates was recon-
America, Eurasia, Africa, Madagascar, South America) suggest structed as Eurasian in analyses with five areas and Asian or
that the most recent common ancestor of crown primates resided equivocal (four or more of North America, Europe, Asia, North
in Eurasia. Analyses with six areas (same as above but with Eurasia America+Asia, Europe+Asia) in analyses with six areas.
split into Europe and Asia) reconstructed the common ancestor of
crown primates as Asian or were equivocal and recovered different Diversification Analyses
combinations of Asia, Europe, North America, North Amer- The results of 12 diversification analyses with TreePar are
ica+Europe, North America+Asia, and Europe+Asia as the summarized in Table 3. Figure 8 shows representative lineage
ancestral area for crown primates. Analyses with five different through time plots for analyses with Groves05+taxon sampling.
areas reconstructed Eurasia as the common ancestral area of Eleven of 12 diversification analyses supported a significant rate
Haplorhini whereas analyses with six areas either reconstructed increase in the late Miocene/Pliocene (mean = 7.0 Ma). Analyses
Asia as the sole area for this clade or were equivocal and suggested with the AUTOsoft timetree, whether with Groves93, Groves95,
that the common ancestor of Haplorhini occurred in North or Groves05+taxon sampling, supported a second rate increase at
America, Europe, Asia, or North America+Europe. The most 19.8 Ma. Two analyses (IRhard and IRsoft with Groves05+taxon

Figure 6. Ancestral area reconstructions for extant primates based on dispersal-extinction-cladogenesis (DEC). Ancestral area
reconstructions were performed under a simplified DEC model that allowed a maximum of two areas at internal nodes. Internal nodes with a single
square were reconstructed to include a single area, whereas internal nodes with two squares were reconstructed to include two areas. Dashed lines
between adjacent nodes indicate that alternative area reconstructions at the basal-most node fall within two log-likelihood units of the optimal

scenario shown in the figure. Multi-colored names denote taxa that occur in more than one area. Range transitions on branches indicate inferred
dispersal events. Numbers in triangles indicate the number of species in each collapsed clade.
sampling) supported a second rate increase in the Pleistocene occurred in analyses with mitochondrial DNA [15,65,66], but
(0.620.5 Ma). Finally, 12/12 analyses supported a rate decrease are eliminated when the mitochondrial and nuclear DNA data are
in the Pleistocene between 1.9 and 0.1 Ma (mean = 0.6 Ma). combined. In addition, the separate mitochondrial and nuclear
Analyses based on the same timetree but with alternate taxon trees (Text S2) failed to recover the monophyly of Pithecia
sampling (Groves93, Groves05, Groves05+) showed only minor (mitochondrial tree) and Lepilemur (nuclear tree), respectively,
differences, whereas differences were more apparent in analyses probably because of problems with nonoverlapping sequences
with different timetrees (i.e., AUTOhard, AUTOsoft, IRhard, [67]. However, these problems were eliminated through the
IRsoft) and equivalent taxon sampling. inclusion of both mitochondrial and nuclear DNA sequences.
All of the relationships among genera and families that were
Discussion strongly supported in Perelman et al’s [12] analysis were also
recovered in the present study. Differences between Perelman
Primate Phylogeny et al.’s [[12, fig. 1] phylogeny for primate families and genera and
The phylogeny for 367 primates (Figs. 1, 2, 3, 4, 5) provides the the phylogeny in Figure 1 pertain to clades with bootstrap support
most complete molecular phylogeny to date for primate genera that was less than 90% in one or both studies. Perelman et al. [12]
and species. Phylogenetic relationships in Figures 1, 2, 3, 4, 5 are included 61 genera in their study (60 if Mico and Cebuella are
largely confirmatory of recent studies on higher-level relationships treated as subgenera of Callithrix [6] and Tarsius is split into three
among primates [3,12,15,21,22], as well as relationships within genera (Tarsius, Carlito, Cephalopachus) following Groves and
Lorisiformes [3,12,15,23,24], Lemuriformes [3,7,8,11,12,15,25– Shekelle [68]), whereas the present analysis includes ten additional
38], Tarsiiformes [39,40], Catarrhini [3,12,15,41–50], and Platyr- genera (Allocebus, Euoticus, Hoolock, Indri, Phaner, Procolobus, Prolemur,
rhini [3,12,15,51–62]. Our supermatrix expands upon these Rungwecebus, Simias, Tarsius [sensu 68]), many of which were
previous studies by bringing together sequences from a wide array positioned with robust support relative to their sister taxa and
of molecular studies, supplemented by new data for four genes, to closest outgroups: (1) Allocebus is the sister taxon to Microcebus+-
yield a single primate phylogeny with strong support for the Mirza in Cheirogaleidae; (2) Euoticus groups with other galagids; (3)
monophyly of most primate genera, families, and higher-level taxa Hoolock groups with other hylobatids, although relationships
(Primates, Strepsirrhini, Lemuriformes, Lorisiformes, Haplorhini, among the four hylobatid genera are not well supported; (4) Indri
Tarsiiformes, Simiiformes, Catarrhini, Platyrrhini). This phylog- is the sister taxon to Avahi+Propithecus in Indriidae; (5) Phaner groups
eny combines a robust framework for primate families and most with other cheirogaleids on the bootstrap tree, although not on the
genera based on nuclear genes with the expanded taxonomic best ML tree; (6) Procolobus is the sister taxon to Piliocolobus in
coverage for genera and species that results from the inclusion of Colobini; (7) Prolemur groups with Lemur and Hapalemur in
mitochondrial DNA sequences. Our primate phylogeny also Lemuridae, although relationships among these three genera are
provides an appropriate framework for timetree and diversification not well resolved; (8) Rungwebus groups with Papio in Papionini; (9)
analyses of Primates. Simias and Nasalis are sister taxa in Presbytini; and (10) Tarsius is
Missing data (including gaps) comprise ,69% of the total data the sister taxon to Cephalopachus+Carlito in Tarsiidae. The only
set, but the distribution of missing data is decidedly nonrandom. genera missing from the present analysis are the atelid Oreonax and
Rather, families and most genera have one or more exemplars the lorisid Pseudopotto, both of which are monotypic and remain to
with high gene completeness (Fig. S2), whereas gene sampling be sampled for gene sequences. Further, Pseudopotto martini is a
among species with only one or a few sequences is focused on a few controversial taxon and is based on only two specimens of
mitochondrial genes so that gene overlap is generally high among uncertain provenance [69].
congeneric species and closely related genera. Wiens [63] Three genera (Galago, Cercopithecus, Trachypithecus) were recovered
suggested that it should be possible to design phylogenetic analyses as paraphyletic in our analyses, but in each case these results are
that will resolve higher-level relationships with large numbers of consistent with previous studies that have included broad taxon
slow-evolving characters and then place additional taxa on this sampling within these taxa. Chatterjee et al. [15] and Fabre et al.
scaffold through the use of a smaller number of more rapidly [3] recovered Otolemur and Euoticus inside of Galago based on their
evolving characters. Along these lines, Sánchez-Gracia and supermatrix studies. Perelman et al. [12] also recovered Otolemur
Castresana [64] suggested that combined data sets may be more inside of Galago, but Euoticus was not included in their study. Our
efficient than nuclear only or mitochondrial only data sets of the analyses placed Otolemur inside of Galago, and Euoticus as the sister
same size for species tree inference when there are both deep and taxon to Galago+Otolemur. However, bootstrap support for the
shallow divergences. This design characterizes the present study, monophyly of Galago+Otolemur to the exclusion of Euoticus
which includes a large number of slow-evolving characters (i.e., was,50%. Numerous studies have recovered Cercopithecus as
nuclear loci) for families and genera, and a smaller number of paraphyletic [3,12,43,70]. Our results agree with these studies
more rapidly evolving characters (i.e., mitochondrial loci) that are by placing Erythrocebus and Chlorocebus, both of which are terrestrial,
added onto this scaffold for an expanded assemblage of primate in a clade with terrestrial Cercopithecus species. This collective group
species. At the same time, nuclear and mitochondrial loci require is the sister taxon to an arboreal Cercopithecus clade [3]. Retroposon
heterogeneous substitution models to avoid problems with model insertions [70] and Perelman et al.’s [12] supermatrix further
mis-specification and it is important to analyze combined suggest that Miopithecus is nested inside of Cercopithecus, specifically
nuclear+mitochondrial supermatrices with mixed model partition- as the sister taxon to arboreal Cercopithecus, whereas Fabre et al. [3]
ing. recovered Miopithecus as the sister taxon to Cercopithecus+Chlorocebu-
The ML tree based on mitochondrial genes (Text S2) failed to s+Erythrocebus. Our results suggest that Miopithecus and Allenopithecus
recover the monophyly of several higher-level clades, including are sister taxa and together comprise the sister taxon to
Primates and Haplorhini. These problems have previously Cercopithecus+Chlorocebus+Erythrocebus. Finally, Trachypithecus para-

Figure 7. Ancestral area reconstructions for extant primates based on minimum area change (MAC) parsimony. Nodes with
unambiguous ancestral area reconstructions are shown with a single colored square; nodes with ambiguous reconstructions are shown with two or
more squares, and each colored square corresponds to a different reconstruction. Bi-colored squares indicate reconstructions that included two
areas. Multi-colored names denote taxa that occur in more than one area. Range transitions on branches indicate inferred dispersal events. Numbers
in triangles indicate the number of species in each collapsed clade.

Table 2. Results of ancestral area reconstructions with minimum area change (MAC) parsimony and eight topologies from Seiffert
et al.
Seiffert et al. [20]

Topology Crown Primates Strepsirrhini Haplorhini Stem Primates
5 areas 6 areas 5 areas 6 areas 5 areas 6 areas 5 areas 6 areas
Figure 2A EA NA, EU, AS, AF AF EA NA, EU, AS, NA+EU EA NA, EU, AS
NA+E, EU+AS
Figure 2B EA AS AF, EA, MA AF, EU, EA AS EA AS
MA, AS
Figure 2C EA AS MA MA EA AS EA AS
Figure 2D EA AS MA MA EA AS EA AS
Figure S2A EA NA, EU, AS, NA+EU, MA MA EA NA, EU, AS, NA+EU EA NA, EU, AS,
NA+AS, EU+AS NA+AS, EU+AS
Figure S2B EA NA, EU, AS, EU+AS AF, EA, MA NA, AF, EU, EA NA, EU, AS, EU+AS EA NA, EU, AS, EU+AS
MA, AS
Figure S2C EA NA, EU, AS, NA+EU, MA MA EA NA, EU, AS, NA+EU EA NA, EU, AS,
NA+AS, EU+AS NA+AS, EU+AS
Figure S2D EA NA, EU, AS, NA+EU, AF, EA, MA AF, EU, EA NA, EU, AS, NA+EU EA NA, EU, AS,
NA+AS, EU+AS MA, AS NA+AS, EU+AS
Abbreviations: AF = Africa; AS = Asia; EA = Eurasia; EU = Europe; MA = Madagascar; NA = North America.

[20]. Areas delimited by commas indicate alternate reconstructions.
phyly, with one or more species of Semnopithecus nested inside of this older than maximum constraints in soft-bounded analyses. The
genus, has been recovered with mitochondrial data, Y chromo- mean violation was 3.6 Ma, which suggests that there are only
somal data, retroposon insertions, and nuclear supermatrices minor inconsistencies among the calibrations that were employed
[12,45]. Taxonomic revisions are required to parcel these in this study.
paraphyletic genera, as well as their embedded subtaxa (i.e., We estimate that crown primates last shared a common
Otolemur in Galago, Erythrocebus and Chlorocebus in Cercopithecus, ancestor ,71–63 million years ago. This date is slightly older
Semnopithecus in Trachypithecus) into monophyletic units. In some than Chatterjee et al.’s [15] relaxed clock date of 63.7 Ma for
cases these revisions are underway. For example, Karanth [71] has Primates, but markedly younger than most timetree dates
suggested a classification wherein langurs of the Indian subcon- (Table 4), some of which are as old at 85–90 Ma [12,25]. Latest
tinent are placed in Semnopithecus, whereas leaf monkeys of Cretaceous dates for Strepsirrhini and Haplorhini are also
Southeast Asia are placed in Trachypithecus. However, the common among relaxed clock studies, but our analyses suggest
placement of northern species remains less clear [71]. that strepsirrhines last shared a common ancestor 55.3253.3 Ma
A potential shortcoming of supermatrices that include both near the Paleocene-Eocene boundary, and that haplorhines last
mitochondrial and nuclear data is that combined analyses mask shared a common ancestor 64.2258.4 Ma in the Paleocene. Both
genuine cytonuclear dissociation (i.e., mito-nuclear discordance), of these dates are in good agreement with Meredith et al.’s [22]
which occurs when nuclear and mitochondrial genes have timetree estimates for these clades. With the exception of the basal
different evolutionary histories owing to processes such as split among extant Primates, which is latest Cretaceous in age in
introgression of mtDNA, demographic disparities, and sex-biased some analyses, our timetree estimates are concordant with the
asymmetries including male-biased dispersal [72–75]. It will be hypothesis that the KPg mass extinction opened up ecospace that
important in future studies to improve both gene and taxon promoted intraordinal diversification [22]. Our timetree estimates
sampling for primate species, to construct separate trees based on also reduce the disagreement between paleontological and
mitochondrial and nuclear loci, and to tease apart differences that molecular estimates for the most recent common ancestor of
arise from incomplete lineage sorting versus other types of Primates, and agree with Steiper and Seiffert’s [79] estimated
discordance including introgression and sex-biased dispersal [75– divergence times (70263 Ma). Steiper and Seiffert [79] showed
77]. Among primates, mito-nuclear discordance has been that molecular evolutionary rates in primates are inversely
suggested for Asian colobines belonging to Presbytis, Trachypithecus, correlated with three life history variables (body size, absolute
and Semnopithecus [46,77,78], and the Malagasy mouse lemurs endocranial volume, relative endocranial volume), and that the last
common ancestor of living primates had a very small body size,
Microcebus griseorufus and M. murinus [73].
absolute endocranial volume, and relative endocranial volume.
They subsequently reconstructed a timescale for primates by
Primate Divergence Times predicting molecular rates from the reconstructed phenotypic
Relaxed clock methods have previously been used to estimate values for a large phylogeny of living and extinct primates.
divergence times among primate lineages, but these studies were Importantly, Steiper and Seiffert’s [79] analysis was an attempt at
based on smaller data sets (taxa and genes) and employed fewer correcting for the effects of convergent rate slowdowns in primates
calibrations than the present study. Further, we performed [80–83]. Our results suggest that relaxed clock methods can also
analyses with two different models for evolutionary rates address convergent rate slowdowns, as is the case for primates [79–
(autocorrelated, independent). There were only six instances of 83], provided that there are sufficient calibrations throughout the
timetree dates that were younger than minimum constraints or tree.

Figure 8. Lineage through time (LTT) plots for Primates and Simiiformes based on Groves05+taxon sampling. (A) LTT plot based on
timetree with autocorrelated rates and soft-bounded constraints. (B) LTT plot based on timetree with independent rates and hard-bounded
constraints. Arrows denote statistically significant rate increases and decreases that were detected with TreePar [120] (see Table 3). Green
background = Cretaceous; pink background = Paleogene; yellow background = Neogene.

Table 3. Diversification rate shifts detected by TreePar [120] with different combinations of four timetrees and three taxonomies.
Groves93 Taxonomy Groves05 Taxonomy Groves05+Taxonomy
AUTOhard Timetree 8.0 Ma (increase) 1.9 Ma (decrease) 8.0 Ma (increase) 0.5 Ma (decrease) 8.0 Ma (increase) 0.5 Ma (decrease)
AUTOsoft Timetree 19.8 Ma (increase) 8.7 Ma (increase) 19.8 Ma (increase) 8.1 Ma (increase) 19.8 Ma (increase) 8.5 Ma (increase) 0.5 Ma
1.7 Ma (decrease) 0.5 Ma (decrease) (decrease)
IRhard Timetree 3.4 Ma (increase) 0.4 Ma (decrease) 6.3 Ma (increase) 0.3 Ma (decrease) 6.3 Ma (increase) 0.6 Ma (increase) 0.1 Ma
(decrease)
IRsoft Timetree 5.7 Ma (increase 0.3 Ma (decrease) 5.8 Ma (increase) 0.2 Ma (decrease) 0.5 Ma (increase) 0.1 Ma (decrease)
We recovered divergence dates within Strepsirrhini, including divtime program. Hodgson et al. [59] concluded that the fossil
Lorisiformes, Madagascan Strepsirrhini, and Lemuriformes that platyrrhines Dolichocebus, Tremacebus, and Chilecebus, which date to
are similar to dates from Meredith et al. [22], but younger than ,20 Ma, must be stem platyrrhines because they are older than
dates from other studies (Table 4). Divergence dates for Hodgson et al.’s [59] estimate for the most recent common
Simiiformes and its subclades, in turn, are generally in good ancestor of extant platyrrhines at 19.5 Ma. Poux et al. [85] and
agreement with other relaxed clock studies including Chatterjee Fabre et al. [3] also recovered dates for Platyrrhini that are too
et al. [15], Fabre et al. [3], and Perelman et al. [12] (Table 4). For young for the inclusion of the aforementioned fossil in crown
example, our mean date for Simiiformes based on four different Platyrrhini. However, our timetree dates for Platyrrhini leave open
analyses is ,41 Ma whereas Chatterjee et al. [15], Fabre et al. the possibility that these fossil taxa are members of the crown
[3], and Perelman et al. [12] recovered dates of ,43, ,38, and clade.
,43 Ma, respectively. By contrast, Meredith et al. [22] recovered Our results also demonstrate that timetree analyses are sensitive
younger dates for Simiiformes, Catarrhini, Hominoidea, and to different clock models (i.e., autocorrelated versus independent
Platyrrhini (Table 4). Meredith et al.’s [22] younger dates for these rates), as Meredith et al. [22] previously reported in their analyses
clades may reflect the difficulties of timetree analyses for clades of divergence times among mammalian families. In comparison to
such as Mammalia that include taxa with a wide range of life analyses with an autocorrelated rates model, timetree dates based
history characters (e.g., baleen whales versus muroid rodents) and on an independent rates model yielded older dates for the base of
a correspondingly wide range of molecular evolutionary rates. Primates, similar dates for the suborders Strepsirrhini and
The mean timetree date for Platyrrhini based on our analyses Haplorhini, and younger dates for almost all other primate nodes
was 23.3 million years, which is slightly older than Hodgson et al.’s (Table S1).
[59] date of 19.5 Ma that was obtained with complete mitochon- Finally, we note that the potential complication of modeling
drial genome sequences and Thorne and Kishino’s [84] multi- older divergences with nuclear data and more recent divergences
Table 4. A comparison of mean divergence dates for select nodes in the present study and previous studies. Dates are in millions
of years.
Meredith Perelman Fabre Chatterjee Steiper and

Clade This study et al. [22] et al. [12] et al. [3] et al. [15] Young [83]
Primates 67.8 71.5 87.2 82.2 63.7 77.5

Strepsirrhini 54.2 55.1 68.7 71.9 51.6 57.1
Lemuriformes+Chiromyiformes 50.0 51.6 58.6 63.3 46.2 NI
Lemuriformes 31.8 29.6 38.6 44.8 32.4 40.9
Lorisiformes 34.7 35.4 40.3 40.9 37.5 NI
Haplorhini 61.2 62.4 81.3 74.5 NI NI
Simiiformes 40.6 30.1 43.5 39.8 42.8 42.9
Catarrhini 25.1 20.6 31.6 25.0 29.3 30.5
Hominoidea 17.4 14.4 20.3 19.5 21.5 NI
Hominidae 15.1 NA 16.5 15.4 15.9 18.3
Homininae 8.0 NA 8.3 10.1 10.7 8.6
Homo+Pan 6.7 NA 6.6 7.5 8.1 6.6
Cercopithecoidea 13.2 NA 17.6 14.5 23.4 NI
Colobinae 8.9 NA 12.3 9.6 18.4 NI
Cercopithecinae 8.4 NA 11.5 10.5 NA 9.9
Platyrrhini 23.3 14.6 24.8 15.9 26.6 20.8
NI, divergence date not included in study.


with mitochondrial data, as in the present study, can be addressed Most authors have also concluded that Africa is the ancestral
in future studies with increased nuclear sampling at the species area for crown Hominoidea, and that Eurasian hylobatids and
level. ponginines represent independent dispersals from Africa [91,92].
However, Stewart and Disotell [93] and Begun [94] suggested that
Ancestral-Area Reconstructions crown hominids originated in Asia and that the ancestor of African
Beard [16] suggested an Asian origin for crown primates based apes and humans (Homininae) re-entered Africa in the late
on an analysis that coded the total geographic area of five extant Miocene. Folinsbee and Brooks’ [95] PACT analysis of area
(Strepsirrhini, Tarsiidae, Simiiformes, Cynocephalidae, Scanden- cladograms for hominoids, proboscideans, and hyaenids provides
tia) and eight extinct (Paromomyidae, Micromomyidae, Carpo- additional support for the hypothesis that crown hominoids last
lestidae, Plesiadapidae, Saxonella, Altanius, Omomyidae, Altiatlasius) shared a common ancestor in Asia, and that the ancestor of crown
euarchontan lineages in three different areas (Africa, Asia, North Hominidae re-entered Africa. Finally, our results suggest that
America). As discussed by Silcox [2], Beard’s [16] topology was Africa and Asia are equally likely ancestral areas for Cercopithe-
not based on an explicit matrix, but instead was cobbled together coidea, whereas the fossil record suggests that Old World monkeys
from different sources. Silcox [2] expanded Beard’s [16] have a most recent common ancestor in Africa [96].
taxonomic sampling and used a matrix-based topology as the In two instances the results of DEC analyses suggest that
framework for her ancestral area reconstructions. She concluded dispersal events occurred on older branches than implied by any of
that an origin for crown primates in Africa, Asia, Europe, or North the MAC parsimony reconstructions. First, DEC results suggest
America was possible. Bloch et al. [1] performed analyses using that the most recent common ancestor of Simiiformes occupied a
the total geographic distributions of the taxa in questions, as in geographic range that included Asia and the New World, and that
Beard [16] and Silcox [2], as well as the location of a taxon’s first the ancestral range of this taxon was sundered in conjunction with
fossil occurrence. Bloch et al. [1] recovered Asia or North America the cladogenic separation of catarrhines and platyrrhines. These
as the ancestral area for crown primates based on the former results imply that Primates were present in South America prior to
approach, and North America as the ancestral area based on the the most recent common ancestor of Simiiformes, ,44237 Ma,
latter approach. whereas the oldest primate fossils from South America are from
These authors all used Fitch parsimony to infer ancestral areas. the early Miocene and are either stem [59] or crown platyrrhines
Fitch parsimony was coopted from phylogenetics rather than [97]. Putative stem Simiiformes, in turn, are known from Asia and
developed explicitly for historical biogeographic reconstruction. A Africa [98–104]. We favor the MAC parsimony results, which are
disadvantage of monomorphic ancestral area reconstruction more compatible with the fossil record and support dispersal to the
methods, including Fitch parsimony, is that these methods disallow New World after platyrrhines diverged from catarrhines. Howev-
geographic ranges at ancestral nodes that include more than one er, MAC parsimony results suggest that dispersal occurred from
area [18]. By contrast, an advantage of both DEC and MAC Asia to South America rather than from Africa to South America
parsimony is that these methods explicitly allow ancestors to have as is more commonly assumed [85]. An ancestral area of Asia for
geographic ranges that encompass two or more areas. The crown Simiiformes may be an artifact of not including stem
application of DEC and MAC parsimony with our molecular simiiforms in our analyses. Second, DEC results suggest an earlier
phylogeny suggests that Asia played a prominent role in the early dispersal of macaques to Asia than MAC parsimony. DEC results
evolutionary history of crown primates. Asia was reconstructed as suggest that dispersal to Asia occurred in the common ancestor of
the ancestral area of Primates, Haplorhini, Catarrhini, and crown Macaca, and that this ancestor occupied both Africa and
Hominoidea, and was among multiple areas or one of the Asia. MAC parsimony results, in turn, suggest that the ancestor of
alternate reconstructions for Strepsirrhini, Simiiformes, and Asian macaques dispersed from Africa to Asia after Macaca sylvanus
Cercopithecoidea. As discussed below, these results must be separated from the latter clade. The fossil record of Macaca sylvanus
tempered against the backdrop of the fossil record given that includes northern Africa (e.g., Tunisia) and much of Europe (e.g.,
ancestral area reconstructions are sensitive to taxon sampling and Italy, France, Germany, Austria) [96] and supports the DEC
the inclusion of fossils [18], whereas our molecular phylogeny is hypothesis that the common ancestor of living macaques dispersed
sans fossils. from Africa to Asia (or at least Eurasia) before M. sylvanus diverged
Previous studies [1,2,16] that included Asia as one of the from other Macaca species.
possible ancestral areas for crown Primates are generally consistent Extinct taxa were not included in our molecular phylogeny, but
with our results. DEC and MAC parsimony reconstructions that are critical for understanding the historical biogeography of crown
place the most recent common ancestor of haplorhines in Asia are primates. MAC parsimony analyses with phylogenetic trees from
also consistent with prevailing views based on the fossil record Seiffert et al. [20] that included fossil and living taxa provide
[86]. additional support for the hypothesis that crown primates last
By contrast, ancestral reconstructions that place the most recent shared a common ancestor that resided in Eurasia in analyses that
common ancestors of Simiiformes, Catarrhini, Hominoidea, allowed for five areas, but were equivocal in analyses with six
Hominidae, and Cercopithecoidea in Asia are in varying degrees areas. Unfortunately, existing morphological data sets with
of conflict with predominant views based on the fossil record. The extensive taxon sampling for key fossil groups are difficult to
oldest simiiform fossils are eosimiids from Asia, and it is generally combine with molecular data sets because extant taxa are not well
held that stem simiiforms originated in Asia before migrating to sampled in the former. Future analyses of primate historical
Africa in the Middle or Late Eocene [87,88]. Stem catarrhines, in biogeography will benefit from combined sets that include a broad
turn, are exclusively Afro-Arabic with the possible exception of assemblage of fossils in the morphological partition, and broad,
Asian amphipithecids [86,88]. In the case of both Simiiformes and overlapping taxon sampling between the molecular and morpho-
Catarrhini, DEC and MAC parsimony results are potentially logical partitions for extant taxa.
impacted by the absence of key fossil taxa in our molecular
phylogeny including Oligopithecidae, Parapithecoidea, Proteo- Diversification Analyses
pithecidae, Propliopithecidae, and Saadaniidae, all of which are Analyses with Groves 93, Groves05, and Groves 05+all provide
stem simiiforms and/or stem catarrhines [89,90]. support for a diversification rate increase in the late Miocene/

Pliocene (mean = 7 Ma). This rate shift corresponds to the onset of analyses to address the possibility that Pleistocene rate changes are
an increase in fossil primate diversity at approximately the same obscuring pre-Pleistocene dynamics. This result contrasts with the
time (Fig. 8). The late Miocene was characterized by elevated fossil record, which suggests that primate diversity was relatively
global mean temperatures [105,106], which may have promoted high in the early Eocene, plummeted in the Oligocene, and
primate diversification. The increase in fossil diversity beginning at gradually rebounded thereafter (Fig. 9). The high diversity of
,7 Ma is attributable, in part, to an increase in the diversity of primates in the Eocene is associated with warm temperatures and
Old World monkeys, which became more widespread in Africa an expansion of tropical and subtropical habitats during this
and occur for the first time in Eurasia in the late Miocene [107]. epoch. The decrease in primate diversity at the Eocene-Oligocene
All of our diversification analyses provide support for a boundary corresponds to the ‘‘Grande Coupure’’ in Europe and
Pleistocene rate slowdown, although in two cases this rate its temporal equivalents in Africa, Asia (‘‘Mongolian Remodel-
slowdown was preceded by a slightly earlier Pleistocene rate ing’’), and North America [121] (Fig. 9). The Grande Coupure
increase. Pleistocene rate slowdowns have been documented in represents a major terrestrial faunal turnover and coincides with
other diversification studies and may result from our inability to the onset of Oligocene glaciation and cooling [122,123]. The
recognize recently separated lineages [108]. Viewed from the Oligocene decrease in diversity was largely driven by the demise of
perspective of species concepts, rate decreases in the recent past two clades, Adapiformes and Omomyiformes, which were the
may be expected when lineages are defined by the biological most diverse crown primate groups during much of the Cenozoic
species concept (BSC) because incipient lineages on the road to [89,124]. The post-Oligocene rebound in fossil diversity, in turn,
eventual reproductive isolation have had insufficient time to owes mainly to an increase in the number of simiiform species.
acquire the hallmarks of ‘‘good’’ biological species. The proclivity TreePar analyses with four Groves05+timetrees that compared
of the BSC to discount incipient lineages suggests that de Queiroz’ one-rate models to two-rate models, with the additional require-
[109,110] general lineage concept of species, wherein alternate ment that the rate shift was forced to occur within 0.5 Ma of the
species concepts represent different stages in the speciation Eocene-Oligocene boundary (i.e, 33.9+/20.5 Ma), resulted in log
process, provides a more appropriate framework for defining likelihood differences (0.90 to 4.26) that were insignificant after
lineages in diversification analyses. Along these lines the ‘‘diag- adjusting the Type 1 error rate to a = 0.05 (Methods). In addition,
nosable’’ version of the phylogenetic species concept (PSC), in we compared diversification rates based on the fossil record with
which a species is defined as ‘‘the smallest diagnosable cluster of diversification rates based on molecular timetrees for 11 consec-
individuals within which there is a pattern of ancestry and utive five million year intervals from 55 to 0 Ma, and in every case
descent’’ [111], represents the earliest recognizable stage in the r values were insignificant (Table 5).
emergence of a new lineage. Even the diversification analyses with Clearly there is a discrepancy between the fossil record, which
Groves05+taxonomy, which has been strongly influenced by provides evidence of a major turnover event in primate diversity
widespread adoption of the PSC by primate taxonomists beginning with the Grande Coupure, and diversification analyses
[5,6,9,11], detected rate decreases in the Pleistocene. However, of living taxa that failed to uncover evidence for this turnover.
the average age of the Pleistocene rate decrease becomes McInnes et al. [125] have also discussed the inadequacies of
progressively younger from Groves93 (1.1 Ma) to Gro- molecular phylogenies for detecting ancient diversification shifts.
ves05+(0.3 Ma), which suggests that the PSC is effective at By contrast, Morlon et al. [126] have shown that diversification
discriminating among all but the most recent incipient lineages. dynamics inferred from molecular phylogenies can be concordant
The discovery and proper vetting of newly proposed primate with the fossil record if rate variation through time and among
species, especially in groups with rapidly increasing taxonomic major taxonomic groups is taken into account. However, the
diversity such as Malagasy lemurs, is critical for obtaining accurate application of Morlon et al.’s [126] approach is arbitrary and
estimates of diversification rates in the recent past. presently lacks a systematic framework for implementation. Also,
Two of four diversification analyses with Groves05+provide unlike Cetacea where taxonomic groups inferred by Morlon et al.
support for a rate increase in the Pleistocene that precedes the [126] to have declining diversity still have extant representatives,
subsequent rate decrease. The possibility of a rate increase in the Adapiformes and Omomyiformes are extinct clades that are
Pleistocene is consistent with the Pleistocene Refugia hypothesis. entirely missing from molecular chronograms for extant Primates.
Living primates have distributions that are centered in four Rabosky [127] has previously shown that phylogenetically
geographic regions: Africa, Madagascar, Asia, and South America. clustered extinction events (i.e., entire clades) erase the signature
Each of these regions includes tropical/subtropical habitats that of extinction from molecular phylogenies.
may have contracted and expanded in synchrony with Pleistocene Apparent discrepancies between fossil diversity and the signa-
glaciation cycles [112–117]. Pleistocene glaciations in Asia may ture of molecular phylogenies may also be attributed to sampling
have promoted speciation among primates through the lowering of bias in the fossil record given that rates of fossil preservation have
sea level, which facilitated travel among Asian islands, rather than varied through time and in different geographic regions [128–
through isolation as in Africa and South America [118]. Another 132]. The fossil record of primates is a case in point and it has
possible cause for the Pleistocene rate increase is the ‘‘pull of the been estimated that only ,7% of Cenozoic primate species have
Recent’’, which is a consequence of an excess of newly emergent so far been discovered [133,134]. Sampling biases in the primate
lineages that have insufficient time to go extinct [119]. Stadler’s fossil record include better sampling in North America and Europe
[120] method explicitly accounts for the pull of the Recent, but than in Africa and Asia [132], and notoriously poor fossil
may still detect a rate increase if there is artificial oversplitting. preservation during the middle of the Oligocene, especially in
Clearly, diversification analyses of lineages through time are Africa [132,135]. The latter sampling bias may account for the
fundamentally linked to our concept of ‘‘lineage’’, and conclusions decrease in diversity across the early Oligocene-middle Oligocene
pertaining to relatively recent rate increases or decreases must transition (,29228 Ma, Fig. 9), whereas the earlier plummet in
confront this issue. diversity at ,34 (i.e., Grande Coupure, Fig. 9) represents a major
None of our diversification analyses detected pre-Miocene rate terrestrial faunal turnover associated with real climatic changes at
increases or decreases, even when the timetrees were truncated at the Eocene–Oligocene transition [133]. A challenge for future
the beginning of the Pleistocene (2.6 Ma) before running TreePar studies is to assess whether or not molecular phylogenies retain any

Figure 9. Standing diversity of fossil primate species throughout the Cenozoic. Total primate diversity includes all crown primate fossils
found within the Paleobiology Database and Hartwig [149]. Adapiformes and Omomyiformes are extinct lineages. The position of the Grande
Coupure at , 33.9 Ma is indicated by a dashed black line. Pink background = Paleogene; yellow background = Neogene.
Table 5. Diversification rates ([speciation – extinction]/lineage/million years) for 11 five million years intervals based on molecular
timetrees and the fossil record.
AUTOhard Timetree AUTOsoft Timetree IRhard Timetree IRsoft Timetree

Time Interval (Ma) Fossil Rate Rate Rate Rate Rate
5 to 0 1.39E-01 2.11E-02 2.98E-01 23.63E-04 22.95E-01

10 to 5 2.86E-02 2.68E-01 5.91E-02 2.71E-01 2.98E-01
15 to 10 4.84E-02 1.64E-02 6.60E-02 4.41E-04 22.23E-01
20 to 15 1.65E-01 8.00E-02 8.01E-05 6.94E-02 2.10E-01
25 to 20 1.25E-01 4.19E-02 1.03E-02 5.66E-02 22.95E-04
30 to 25 21.14E-01 2.03E-02 8.68E-04 1.60E-02 21.11E-01
35 to 30 25.34E-02 5.97E-02 3.35E-03 2.08E-01 1.29E-01
40 to 35 21.96E-03 1.24E-02 7.52E-03 1.89E-01 2.23E-06
45 to 40 21.28E-02 9.16E-02 8.03E-04 1.70E-01 6.34E-02
50 to 45 1.36E-02 1.01E-06 6.64E-03 1.76E-01 1.07E-01
55 to 50 2.25E-01 1.64E-01 1.43E-03 2.15E-01 4.54E-02
Correlation coefficient, r 0.249 0.272 20.087 20.019

signature of major turnover events such as the Grande Coupure with Se-Al [136]. Ambiguous regions of the 12S and 16S rRNA
that impacted Primates and other mammalian taxa, while at the genes were excluded prior to phylogenetic analysis. Alignments for
same time accounting for sampling bias in the fossil record. 79 different partitions were combined with SequenceMatrix 1.7.8
[137]. The resulting alignment comprised 61199 bp and has been
Materials and Methods deposited in TreeBase (ID 13451).
Gene and Taxon Sampling Phylogenetic Analyses

We assembled a data set comprising segments of 69 nuclear Maximum likelihood analyses were performed with RAxML
genes and ten mitochondrial genes. Sequences for 54 nuclear 7.2.8 on Cipres [138,139]. Each of seventy-nine different gene
genes were taken from Perelman et al.’s [12] nexus file with segments was allowed to have its own parameter estimates under
modifications to eliminate problems with probable contaminants the GTR+C model of sequence evolution. Rapid bootstrapping
and misidentified sequences (Table S2); sequences for 15 (500 replications) and a search for the best ML tree were
additional nuclear genes (ABO, CXCR4, CXCR5, Epsilon globin, performed in a single program run. Bootstrap replications were
FGA, IRBP intron 1, IRBP intron 3, MC1R, NRAMP, PRNP, VWF performed with a GTRCAT approximation to the GAMMA
intron 11) were obtained from GenBank; and new sequences distribution and 25 distinct rate categories. The search for the best
(JX856181-JX856283, JX869897-JX869930) for exons of four tree was conducted under GTRGAMMA rather than GTRCAT.
nuclear genes (GHR, IRBP, VWF, TTN) were combined with Default parameters were employed for all other settings.
previously published GenBank sequences for these loci. Mito-
chondrial sequences included eight protein-coding genes (COB, Timetree Analyses
COI, COII, COIII, ND2, ND3, ND4, ND4L) and two RNA genes
The mcmctree program in PAML 4.4b [140] was used to perform
(12S rRNA, 16S rRNA). Accession numbers for previously published
molecular dating analyses. Mcmctree implements the MCMC
sequences are provided in Table S3.
algorithms of Rannala and Yang [141]. Gene segments were binned
Groves recognized 233, 354, and 376 primate species in his into eight categories: mitochondrial protein-coding genes, mito-
1993, 2001, and 2005 classifications, respectively [4–6]. More chondrial rRNA, X-linked nuclear genes, Y-linked nuclear genes,
recent studies suggest that the number of extant primate species is and four groups of autosomal genes based on rates of evolution
a least 450 (Text S1). We searched GenBank for mitochondrial (Table S4). Analyses with usedata = 3, which is used to calculate
and nuclear gene sequences belonging to these taxa, which Hessian matrices, allowed each of the eight partitions to have its own
resulted in a final data set that included at least one gene for 367 of GTR+C model. Analyses with usedata = 2 were performed with
450 primate species. We excluded mitochondrial protein-coding autocorrelated rates and hard-bounded constraints (AUTOhard),
sequences with numt (nuclear mitochondrial DNA) signatures autocorrelated rates and soft-bounded constraints (AUTOsoft),
including frameshift mutations and stop codons. A few taxa were independent rates and hard-bounded constraints (IRhard), and
represented by a single sequence in GenBank, but were omitted independent rates and soft-bounded constraints (IRsoft). We set 1
from our data set because of potential problems with non- time unit = 100 million years following Rannala and Yang [141].
overlapping sequences when there was no sequence overlap with Analyses were run with cleandata = 0 in PAML. Shape (a) and scale
congeneric species. Outgroup taxa were the same as Perelman (b) parameters for rgene_gamma, which describes the gamma prior
et al. [12] and included two dermopterans (Cynocephalus volans, for the overall rate parameter m, were calculated as in Meredith et al.
Galeopterus variegatus), two scandentians (Tupaia glis, T. minor), and a [22]. Calculations for the shape and scale parameters for
composite lagomorph, all of which are from the same superordinal sigma_gamma, which describes the gamma prior for the rate-drift
group (Euarchontoglires) that also includes Primates [22]. Of parameter (s2), assumed an age of 85.9 million years for the most
these, dermopterans are the sister taxon to primates [22].
recent common ancestor of Euarchontoglires [22]. Analyses were
Given that there have been significant changes to primate run for 100,000 generations after a burn-in of 10,000 generations.
taxonomy during the history of GenBank, we updated older Chains were sampled every 20 generations. Each analysis was run
GenBank entries to the newer Groves 05+taxonomy. This twice to check for convergence.
frequently involved elevating taxa with subspecific status on Minimum and maximum fossil calibrations were applied to 14
GenBank to full species status. There are also GenBank entries
nodes (Text S3), seven of which were taken from Meredith et al.
that lack new species names, which can only be found in the [22]. Minimum ages were based on the age of the oldest
original papers, e.g., numerous Lepilemur species of Louis et al.
unequivocal fossils belonging to each clade. Maximum ages were
[36]. In some cases older GenBank sequences for primates were based on the maximum of stratigraphic bounding, phylogenetic
avoided because they could not be satisfactorily updated to the
bracketing, and phylogenetic uncertainty [18,22,142]. Stratigraph-
new Groves05+taxonomy. ic bounding encompassed two successive chronologic units that did
not contain any fossils from the clade of interest. Dates used in
PCR and DNA Sequencing stratigraphic bounding are from Gradstein and Ogg [143]. We
Methods and primers described by Meredith et al. [22] were recognized the following chronologic units in succession from
used to amplify segments of IRBP, GHR, TTN, and VWF for 32 youngest to oldest: Pleistocene, Pliocene, late Miocene (Torto-
(TTN), 34 (IRBP, VWF), and 35 (GHR) primate species. nian+Messian stages), middle Miocene (Langhian+Serravallian
stages), early Miocene (Aquitanian+Burdigalian stages), late
Alignments and Data Concatenation Oligocene (Chattian stage), early Oligocene (Rupelian stage), late
We employed unaltered alignments or alignments with minor Eocene (Priabonian stage), late middle Eocene (Bartonian stage),
adjustments for 53/54 nuclear genes that were included in early middle Eocene (Lutetian stage), early Eocene (Ypresian
Perelman et al.’s [12] nexus file. ADORA3 sequences were aligned stage), late Paleocene (Thanetian stage), middle Paleocene
from scratch given numerous problems with Perelman et al.’s [12] (Selandian stage), and early Paleocene (Danian stage). Phyloge-
alignment (Table S2) and the availability of additional ADORA3 netic bracketing encompassed the age of the oldest stem fossils that
sequences for Lemuriformes. Alignments for all of the other were up to two nodes below the divergence event. Phylogenetic
nuclear genes, as well as mitochondrial genes, were performed bracketing allowed for the possibility that taxa of uncertain

phylogenetic affinities belong to the crown clade, first outgroup, or represent a single species. Species ranges were taken to include the
second outgroup. complete time interval spanned by first and last occurrence data.
Ancestral-Area Reconstructions Supporting Information

Ancestral areas were reconstructed with dispersal-extinction-
cladogenesis (DEC) [17,19] and minimum area change (MAC) Figure S1 Node labels for Table S1.
parsimony [18]. The DEC analysis used the timetree based on (PDF)
autocorrelated rates and soft-bounded constraints. DEC is a Figure S2 Graphical representation of gene and taxon
likelihood-based approach that takes account of both the topology completeness. Black 6 = gene present in data set; red 6 = gene
and branch lengths, whereas MAC parsimony ignores branch present in data set, but sequence length,50% of the length of the
lengths and only takes into account the underlying topology. We longest sequence.
recognized four geographic areas (Africa, Madagascar, Asia (PDF)
[including the Arabian Peninsula], New World) for extant
Table S1 Mean, median, and 95% credibility intervals for four
primates and scored the presence or absence of living primate
different methods. Node numbers are given in Figure S1.
species in each of these four areas. Geographic area information
(XLS)
for most species was extracted from Groves [6]. Species
distributions for recently described species were culled from Table S2 Compendium of modifications to Perelman et al.’s
additional sources [9,11,68,144–148]. Ancestral area reconstruc- [12] data set.
tions were performed with a maximum of two areas per internal (DOCX)
node given that all living primates excepting Homo sapiens have
Table S3 List of GenBank accession numbers.
distributions that are restricted to one or at most two areas. H.
(DOC)
sapiens was coded as present in Africa and Asia given that our own
species occupied these areas before migrating to Madagascar or Table S4 List of genes that were included in eight different
the New World. We also performed MAC parsimony ancestral mcmctree partitions.
area reconstructions for taxa that were included in Seiffert et al.’s (DOCX)
[20] phylogenetic analysis of fossil and living primates. These Text S1 Compendium of primate species that have been
analyses were performed with eight phylogenetic trees from recognized subsequent to Groves [6].
Seiffert et al. [20, fig. 2], all of which were rooted with Tupaia, and
(DOCX)
either five (North America, Africa, Eurasia, Madagascar, South
America) or six (North America, Africa, Europe, Madagascar, Text S2 Timetrees and RAxML phylograms in Newick
Asia, South America) geographic areas with a maximum of two format. 1. Newick timetree with autocorrelated rates and hard-
areas per internal node. Area coding for fossil taxa was based on bounded constraints. 2. Newick timetree with autocorrelated rates
Hartwig [149] and the Paleobiology Database (http://paleodb. and soft-bounded constraints. 3. Newick timetree with indepen-
org). dent rates and hard-bounded constraints. 4. Newick timetree with
independent rates and soft-bounded constraints. 5. RAxML
Diversification Analyses phylogram based on the 61199 bp concatenation of 69 nuclear
TreePar [120] was used to detect temporal shifts in the and ten mitochondrial loci. 6. RAxML phylogram based on ten
diversification rate under a birthdeath model. Analyses were mitochondrial genes. 7. RAxML phylogram based on 69 nuclear
executed with four different timetrees (autocorrelated rates with genes.
hard-bounded constraints, autocorrelated rates with soft-bounded (DOCX)
constraints, independent rates with hard-bounded constraints, Text S3 Fourteen minimum and 14 maximum calibra-
independent rates with soft-bounded constraints). We performed tions that were employed in primate timetree analyses
analyses with the full complement of primate species (i.e., with mcmctree [140,141]. Minimum calibrations were based
Groves05+taxonomy) and with pruned trees that eliminated on the oldest crown fossil belong to each clade. Maximum
species that were not included in Grove05 and Groves93. Taxon calibrations were based on stratigraphic bounding (two chrono-
completeness for these analyses was 81.6% (367/450 species) for logic units), phylogenetic bracketing (two outgroups), and
Groves05+, 81.1% for Groves05 (305/376 species), and 90.6% phylogenetic uncertainty [18,22].
(211/233 species) for Groves93. Likelihood ratio tests were (DOCX)
employed to detect statistically significant rate shifts at P#0.05.
The results of simulations under a constant rate birthdeath model Acknowledgments
were employed to assess and correct for the real Type 1 error rate,
i.e., how often the constant model was rejected using a likelihood We thank John Alroy and Kay Behrensmeyer for their major contributions
ratio test. to the Paleobiology Database for Euprimates, and six anonymous referees
for helpful comments on previous versions of this manuscript. We thank
Leona Chemnick for her crucial role in banking, coordinating permissions
Fossil Diversity and shipments, and oversight of quality control and assurance of many
The standing diversity of fossil primate species throughout the samples.
Cenozoic was estimated with a database for crown primates that
combined temporal ranges for species from the Paleobiology Author Contributions
Database (http://paleodb.org; data downloaded on 16 October
Conceived and designed the experiments: MSS RWM JG DLR TS OAR
2011) with additional taxon ranges from Hartwig [149] for species
JEJ WJM. Performed the experiments: MSS RWM CAE JP CS JEJ CAF
that were missing from the Paleobiology Database. The combined WJM. Analyzed the data: MSS RWM CAE JP WJM. Contributed
database was pruned to exclude taxa that were not identified to the reagents/materials/analysis tools: MSS JG DLR TS OAR WJM. Wrote
species level except in cases where all occurrences of a genus were the paper: MSS RWM WJM. Provided comments on manuscript: JG CAE
species indeterminate, in which case the genus was considered to JP DLR TS CS OAR CAF JEJ.

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Macroevolutionary Dynamics and Historical

Biogeography of Primate Diversification Inferred from a

Introduction Groves [4] recognized 233 primate species in his 1993

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Mean Divergence Composite 95% Composite 95%

Primates 67.84 60.99 76.72

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Mean Divergence Composite 95% Composite 95%

Catarrhini 25.07 19.67 32.83

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Seiffert et al. [20]

5 areas 6 areas 5 areas 6 areas 5 areas 6 areas 5 areas 6 areas

Abbreviations: AF = Africa; AS = Asia; EA = Eurasia; EU = Europe; MA = Madagascar; NA = North America.

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Groves93 Taxonomy Groves05 Taxonomy Groves05+Taxonomy

Meredith Perelman Fabre Chatterjee Steiper and

Primates 67.8 71.5 87.2 82.2 63.7 77.5

NI, divergence date not included in study.

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AUTOhard Timetree AUTOsoft Timetree IRhard Timetree IRsoft Timetree

5 to 0 1.39E-01 2.11E-02 2.98E-01 23.63E-04 22.95E-01

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Gene and Taxon Sampling Phylogenetic Analyses

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Ancestral-Area Reconstructions Supporting Information

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