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CHAPTER FIFTEEN
Mammalian Biogeography
and Anthropoid Origins
K. Christopher Beard
ABSTRACT
The continuity of phylogenetic descent requires that sister taxa originate in the same
place and at the same time. Resolving phylogenetic relationships can therefore aid in
reconstructing remote paleobiogeographic events. The order Primates is hierarchically
nested within an exclusively Asian branch of the mammalian family tree, suggesting that
Primates originated in Asia. Likewise, an Asian origin for Anthropoidea is supported by
the geographic distributions of its sister group (Tarsiiformes) and various stem anthro-
poid taxa (Eosimiidae and Amphipithecidae). Although an African origin for Primates
and/or Anthropoidea has been advocated repeatedly in the past, potential sister groups
for either Primates or Anthropoidea are conspicuously lacking from the living and fossil
biotas of that continent. The dispersal history of Malagasy lemurs and South American
platyrrhines demonstrates that primate dispersal into new terrains often sparks adaptive
radiation and morphological innovation. The precocious (Paleocene) dispersal of basal
anthropoids from Asia to Africa may have instigated an adaptive radiation that yielded
the modern anthropoid bauplan.
Key Words: Africa, China, Primates, Eosimiids, Laurasiatheria, Euanchonta, Coloniza-
ton
K. Christopher Beard rSection of Vertebrate Paleontology, Carnegie Museum of Natural History,
4400 Forbes Avenue, Pittsburgh, PA 15213
Primate Biogeography, edited by Shawn M. Lehman and John G. Fleagle.
Springer, New York, 2006.
439
440 Primate Biogeography
INTRODUCTION
Paleontologists have long believed that Africa played a pivotal role during the
course of primate evolution (e.g., McKenna, 1967; Walker, 1972; Gingerich,
1986, 1990; Sig´e et al., 1990). Though the African origin of such familiar pri-
mate groups as Catarrhini and Hominidae is widely accepted, pinpointing the
continent on which earlier and more basal primate clades arose has proven to be
far more contentious. For example, recent attempts to determine the geographic
roots of Anthropoidea—living and fossil catarrhines and platyrrhines (“crown
anthropoids”) as well as the extinct species that are more closely related to this
clade than is Tarsius (“stem anthropoids”)—embrace a wide range of controver-
sies. These include debates about the phylogenetic affinities of putative basal
anthropoid taxa, divergent opinions on how the taxon Anthropoidea should
be defined, disagreements regarding the relevance and reliability of the fossil
record versus neontological data sets (especially long sequences of nucleotides),
as well as the methods followed to reconstruct historical biogeography at such
deep phylogenetic nodes. Regardless of these ongoing disputes, many paleo-
primatologists have looked to Africa as the most promising locus of anthropoid
origins (Hoffstetter, 1977; Fleagle and Kay, 1987; Holroyd and Maas, 1994;
Ciochon and Gunnell, 2002). Among the most important factors contributing
to this Afrocentric perspective has been the sequence whereby early fossil an-
thropoids have been recovered. For decades, late Eocene and early Oligocene
strata in the Fayum region of Egypt yielded the only uncontested Paleogene fos-
sils for reconstructing early anthropoid evolution (Simons, 1995). This limited
occurrence in space and time led many authors to conclude that anthropoids
originated in Africa sometime near the Eocene-Oligocene boundary (e.g., Ras-
mussen and Simons, 1992).
The discovery of substantially older, though highly fragmentary, anthropoid
fossils in middle Eocene strata in Algeria overturned the chronology of this clas-
sical hypothesis of anthropoid origins (Godinot and Mahboubi, 1992, 1994;
Godinot, 1994). At the same time, these early Algerian anthropoids merely
corroborated the prevailing notion that anthropoids originated in Africa. The
precocious record of African anthropoids, along with paleogeographic and pa-
leobiogeographic evidence for significant endemism among African Paleogene
mammals as a whole, continues to persuade some workers that Africa is the
most probable ancestral homeland for anthropoids (Holroyd and Maas, 1994;
Ciochon and Gunnell, 2002, 2004).
Mammalian Biogeography and Anthropoid Origins 441
Shortly after the middle Eocene anthropoids from Algeria were described,
fossils pertaining to a previously unknown group of stem anthropoids—
designated as eosimiids—began to be unearthed in Asia (Beard et al., 1994,
1996; Jaeger et al., 1999; Beard and Wang, 2004). The discovery of Eosimias
and closely related forms at middle Eocene sites in central and eastern China,
along with the discovery of Bahinia at slightly younger sites in Myanmar, has
revived the possibility that anthropoids originated in Asia—an old idea that
was previously thought to be discredited. Paleontological support for an Asian
origin of anthropoids was originally founded on Pondaungia and Amphipithe-
cus from Myanmar, both of which belong to a second group of Asian Eocene
primates known as amphipithecids (Pilgrim, 1927; Colbert, 1937; Ba Maw
et al., 1979; Ciochon et al., 1985). Although anatomical evidence bearing on
amphipithecids has improved markedly in recent years, their anthropoid affini-
ties continue to be debated (Ciochon and Holroyd, 1994; Jaeger et al., 1998,
2004; Chaimanee et al., 2000; Ciochon et al., 2001; Beard, 2002; Gunnell
et al., 2002; Ciochon and Gunnell, 2002, 2004; Marivaux et al., 2003; Kay
et al., 2004; Takai and Shigehara, 2004). As a result of these latest discoveries
in Asia, the fossil record now offers an ambiguous signal regarding the birth-
place of the anthropoid clade.
Recently, substantial progress has been achieved in resolving the molecular
systematics of placental mammals and charting the fossil record of early Ceno-
zoic mammals in Africa. Advances in both of these areas provide a fresh means
of evaluating the geographic component of anthropoid origins. After reviewing
some of the recent developments in these fields, I will summarize how the new
data clarify the biogeography of anthropoid origins. I will conclude by explor-
ing some possible links between the dispersal history of early anthropoids and
the evolution of their diagnostic suite of morphological synapomorphies.
MAJOR FEATURES OF PLACENTAL MAMMAL PHYLOGENY
Although many details of placental mammal phylogeny remain to be re-
solved, phylogenetic analyses of long sequences of nucleotides routinely sup-
port four broad associations of taxa (Springer et al., 1997, 2004; Madsen et al.,
2001; Murphy et al., 2001a, 2001b). These groups include Xenarthra (primar-
ily South American sloths, anteaters, and armadillos), Afrotheria (elephants,
sirenians, hyracoids, elephant shrews, aardvarks, tenrecs, and golden moles),
Laurasiatheria (perissodactyls, artiodactyls, cetaceans, carnivorans, pangolins,
442 Primate Biogeography
bats, hedgehogs, shrews, moles, and solenodons), and Euarchontoglires (pri-
mates, tree shrews, flying lemurs, rodents, and lagomorphs). Many, though
certainly not all, of these groupings are consistent with evidence from paleon-
tology and comparative anatomy (e.g., Domning et al., 1986; Beard, 1993;
Gingerich et al., 2001; Meng et al., 2003).
Even a cursory examination of the taxa comprising each of the four ma-
jor groups of placental mammals reveals a strong biogeographic imprint on
group composition. Xenarthrans, for example, can confidently be regarded as
a South American clade of placental mammals, both because of the group’s ex-
tant diversity there and its early appearance in the South American fossil record
(Rose and Emry, 1993). Likewise, both phylogenetic and biostratigraphic evi-
dence supports an African origin for afrotheres and a Laurasian birthplace for
laurasiatheres, just as their names would suggest (Springer et al., 1997, 2004;
Beard, 1998a; also see below). Euarchontoglires, the group that includes the
order Primates and its nearest relatives, also appears to carry a strong biogeo-
graphic signal.
From a purely biogeographic perspective, it is clear that primates evolved
from an exclusively Asian branch of the mammalian family tree. Primates are the
most diverse and successful living members of the clade Euarchonta, which also
includes tree shrews (order Scandentia) and flying lemurs (order Dermoptera).
Both scandentians and dermopterans are currently restricted to southern and
southeastern Asia. The fossil record of tree shrews and flying lemurs is meager,
but the only fossils that can be attributed with confidence to these groups like-
wise come from Asia (Chopra et al., 1979; Jacobs, 1980; Tong, 1988; Ducrocq
et al., 1992). We can safely conclude, then, that at least two of the three ordinal-
level members of Euarchonta originated in Asia. This information alone does
not allow us to infer that Primates also arose in Asia, because there is no consen-
sus regarding the phylogenetic relationships among the three major euarchon-
tan clades. Parsimony would suggest that Primates originated in Asia if the sister
group of Primates could be shown to be either Scandentia or Dermoptera. On
the other hand, if the sister group of Primates turns out to be a Scandentia +
Dermoptera clade, broader phylogenetic context would be required to ascer-
tain the most parsimonious birthplace for Primates. Molecular phylogenetic
studies indicate that the sister group of Euarchonta is Glires (rodents and lago-
morphs) (Madsen et al., 2001; Murphy et al., 2001a, 2001b). In contrast to tree
shrews and flying lemurs, Glires eventually achieved a widespread distribution.
However, the fossil record of such basal Glires as Heomys,Tribosphenomys, and
Mimotona in Asia is sufficiently dense and ancient to indicate that this group
Mammalian Biogeography and Anthropoid Origins 443
too must have originated on that continent (Meng et al., 1994, 2003; Dawson,
2003).
Following the methodology outlined by Beard (1998a), one can generate a
“phylogenetically derived biogeographic reconstruction” for Primates and their
relatives simply by optimizing the biogeographic distributions of terminal taxa
onto internal nodes of the cladogram for Euarchontoglires (Figure 1). This
Figure 1. A phylogenetically derived biogeographic reconstruction for the five
ordinal-level crown groups of Euarchontoglires and some key fossil taxa. The geographic
ranges of Scandentia and Dermoptera are restricted to Asia, while those for Rodentia,
Lagomorpha, and Primates include Asia (actually Laurasia) and Africa. Relatively recent
range extensions for Rodentia, Lagomorpha, and Primates into South America and/or
Australia are ignored here. Likewise, the European and North American records of
living and fossil rodents, lagomorphs, and primates are excluded from this analysis, be-
cause the fossil record reveals that each of these groups dispersed to North America
and Europe during the early Cenozoic, after having originated elsewhere (e.g., Beard,
1998a; Beard and Dawson, 1999). A posteriori optimization of the geographic character
onto interior nodes of the cladogram indicates that the last common ancestors of Eu-
archontoglires, Glires, and Euarchonta are most parsimoniously interpreted as having
lived in Asia, with subsequent (and independent) dispersal of rodents, lagomorphs, and
primates from Asia to Africa.
444 Primate Biogeography
procedure unambiguously supports an Asian origin for Primates. The geo-
graphic distributions of certain key fossil taxa corroborate this finding. Ple-
siadapiforms, which are often regarded as “archaic primates,” are well docu-
mented and diverse on the three northern continents (Gingerich, 1976; Szalay
and Delson, 1979; Gunnell, 1989; Beard and Wang, 1995), but undoubted
plesiadapiforms have never been found in Africa [contrary to Tabuce et al.
(2004), the morphologically aberrant Azibiidae from the Eocene of Algeria are
not regarded as plesiadapiforms here]. Likewise, Altanius, which is commonly
cited as a stem euprimate (that is, a sister group of the Strepsirhine +Haplorhini
clade) is only known to occur in Mongolia (Gingerich et al., 1991).
Despite the overwhelming phylogenetic evidence that Primates originated in
Asia, the oldest euprimate currently documented in the fossil record hails from
Africa. The source of this apparent conflict between phylogeny and the fossil
record, late Paleocene Altiatlasius from Morocco, will be discussed at length
later in this chapter. At present, it is sufficient to note that what little is known
about the morphology of Altiatlasius indicates that it lies nested deeply within
Primates. Evaluated within the broader context of mammalian phylogeny and
primate biogeography, Altiatlasius signifies surprisingly early dispersal rather
than any deeper phylogenetic history of Primates on the African continent.
THE FOSSIL RECORD AND AFRICAN BIOGEOGRAPHY:
GARDEN OF EDEN OR MELTING POT?
One way to assess the conflicting biogeographic signals yielded by phylogeny
and the fossil record is by comparing them with the broader pattern of mam-
malian evolution in Africa. In other words, if we momentarily ignore the debate
over Africa’s role as a potential cradle for Primates and/or Anthropoidea, how
important was Africa as a biogeographic source for other living and extinct
mammalian clades? Did Africa function as a constant wellspring of mammalian
diversity throughout the late Mesozoic and Cenozoic? Or did the modern
African mammal fauna develop by a process of accretion, through the step-
wise addition of immigrant taxa to a core fauna dominated by endemic African
forms?
Paleontologists and molecular systematists agree that a significant fraction
of living placental mammal clades originated in Africa. For example, pale-
ontologists have long advocated a common African ancestry for elephants
(Proboscidea), dugongs and manatees (Sirenia), and hyraxes (Hyracoidea)
Mammalian Biogeography and Anthropoid Origins 445
(Simpson, 1945; McKenna, 1975). Recent advances in molecular systemat-
ics have shown that this central group of African endemic mammals can now be
extended to include elephant shrews (Macroscelidea), aardvarks (Tubuliden-
tata), golden moles (Chrysochloridae), and tenrecs (Tenrecidae), yielding the
anatomically heterogeneous assemblage known as Afrotheria (Springer et al.,
1997; Madsen et al., 2001; Murphy et al., 2001a, b). Although the monophyly
of Afrotheria would likely never have been suspected on the basis of morpho-
logical criteria alone, the African fossil record corroborates an African origin for
most, if not all, afrotherian taxa. Africa has yielded the world’s only fossil ele-
phant shrews, golden moles, and tenrecs (Butler and Hopwood, 1957; Tabuce
et al., 2001). By wide margins, the earliest representatives of Proboscidea, Hyra-
coidea, and Tubulidentata are also confined to Africa (Patterson, 1975; Court
and Hartenberger, 1992; Court and Mahboubi, 1993; Gheerbrant et al., 2002).
Presumably because of their aquatic lifestyle, sirenians were able to disperse
widely during the early phases of their evolutionary history (Domning, 2001).
Nevertheless, their phylogenetic position as close relatives of proboscideans and
hyracoids is uncontested, suggesting that they too originated in Africa.
Besides afrotheres and several extinct taxa that are difficult to place on the
mammalian family tree (e.g., Palaeoryctidae), the early Cenozoic fossil record
of Africa is remarkable for lacking several groups of mammals that are oth-
erwise widespread and abundant. Apparently, these taxa (various groups of
laurasiatheres and euarchontoglireans) originated elsewhere and invaded Africa
multiple times during the Cenozoic. Primates, first documented by late Pale-
ocene Altiatlasius from Morocco, were among the first of these exotic mam-
mals to disperse to Africa successfully. Rodents—by far the most diverse and
ecologically successful group of mammals alive today—invaded Africa at least
twice (and more likely, three or more times) during the Eocene (Jaeger et al.,
1985; Marivaux et al., 2002; Dawson et al., 2003). Primitive zegdoumyid ro-
dents (which have been cited as potential relatives of anomalurids, but which
are more plausibly linked with glirids) first appear in early-middle Eocene strata
of Tunisia and Algeria (Vianey-Liaud et al., 1994). As noted previously, rodents
are known to have originated in Asia, so this first appearance of rodents in Africa
serves as an important biogeographic datum. It either reflects dispersal directly
from Asia to Africa or indirectly from Asia to Africa via Europe. Subsequent
episodes of rodent dispersal to Africa emit less ambiguous biogeographic sig-
nals. Undoubted anomalurids appear alongside the earliest African phiomyids at
the late-middle Eocene site of Bir el Ater in northeastern Algeria (Jaeger et al.,
446 Primate Biogeography
1985). Both anomalurids and phiomyids seemingly dispersed directly from Asia
to Africa (Marivaux et al., 2002; Dawson et al., 2003). The earliest African
artiodactyls—the hippo-like anthracotheres—appear alongside anomalurid and
phiomyid rodents in the late-middle Eocene, thus providing a further example
of the successful invasion of Africa by an Asian group of mammals (Ducrocq,
1997). By the time the first anthracotheres show up in Africa, a wide diversity
of artiodactyl groups is established on the northern continents. Given our cur-
rent understanding of Tethyan paleogeography, each of the preceding groups
of mammalian immigrants to Africa—primates, rodents, and anthracotheres—
must have arrived there via sweepstakes dispersal from the north.
A major episode of African faunal turnover occurred near the Oligocene-
Miocene boundary, when a land bridge became established that connected
Africa with Eurasia for the first time (Jolivet and Faccenna, 2000; Kappelman
et al., 2003). Utilizing this direct overland route, numerous additional groups
of Laurasian mammals—including perissodactyls (rhinos and chalicotheres),
artiodactyls other than anthracotheres (pigs, giraffes, and tragulids), carnivo-
rans (cats, viverrids, and amphicyonids), true lipotyphlans (hedgehogs and
shrews), and lagomorphs (pikas)—invaded Africa during the early Miocene.
Other ecologically important groups of extant African mammals (including
bovids, equids, canids, and leporids) dispersed to Africa later in the Miocene.
Like most of the Laurasian mammals that preceded them, the earliest records
of these taxa on the northern continents significantly antedate their first occur-
rences in Africa.
The preceding overview of the African fossil record demonstrates that what
we currently know about African paleontology agrees with results from molec-
ular systematics regarding the endemism of living afrotheres. The flip side
of this coin also holds. That is, those groups of mammals currently residing
in Africa that are not afrotheres all seem to have originated elsewhere, no-
tably Asia. Moreover, in terms of their diversity and abundance, these exotic
mammalian groups—including primates, rodents, lagomorphs, lipotyphlans,
carnivorans, artiodactyls, and perissodactyls—have come to dominate modern
African ecosystems. Since their heyday in the early Cenozoic, afrotheres have di-
minished in abundance and diversity, almost certainly as a result of competition
and/or predation at the hands of these northern invaders. The modern African
mammal fauna therefore evolved as successive groups of Laurasian mammals
insinuated themselves into native African ecosystems harboring fewer and fewer
endemic afrotheres. Primates are but one of the Laurasian mammal groups that
Mammalian Biogeography and Anthropoid Origins 447
attained high taxonomic diversity and ecological prominence after dispersing
into this African melting pot.
PRIMATE DISPERSAL AND ADAPTIVE RADIATION
There are many examples in evolutionary biology whereby dispersal fosters
an adaptive radiation among the organisms that succeed in colonizing a new
terrain. Among primates, this pattern is best exemplified by the colonization of
Madagascar by ancestral lemurs and the colonization of South America by early
platyrrhine monkeys. Both of these evolutionary radiations were instigated by
“sweepstakes” dispersal of an ancestral stock of primates into an ecologically
appropriate region harboring few, if any, potential mammalian competitors.
Given that primates were among the first Laurasian mammals to invade Africa
in the early Cenozoic, we can only assume that the initial colonization of Africa
by primates such as Altiatlasius would have triggered its own adaptive radiation.
To appreciate the potential significance of this poorly documented radiation of
early Cenozoic primates in Africa, let us first review briefly what happened when
primates colonized two other isolated landmasses, the island of Madagascar and
the island continent of South America.
Because the fossil record of Madagascar is so inadequate, little is known
about the early colonization of that island by ancestral lemurs. Geographic
proximity to Africa, where the sister group of Malagasy lemurs still survives
in the form of lorises and galagos, suggests that early lemurs probably rafted
across the Mozambique Channel. Once these early lemurs arrived on Mada-
gascar, they spawned a broad, monophyletic radiation that significantly ex-
panded the envelope of primate ecomorphospace (Tattersall, 1982; Yoder et al.,
1996). Various lemur taxa developed novel anatomical structures, allowing
them to exploit unique ecological niches. Daubentonia, for example, combines
a vaguely rodent-like dentition, enlarged external ears, and highly elongated,
claw-bearing manual third digits to achieve its ecological convergence upon
woodpeckers (Cartmill, 1974). Palaeopropithecus and its close relatives evolved
strongly curved phalanges and other postcranial autapomorphies as part of a
sloth-like adaptation for suspensory folivory (Jungers et al., 1997). Archaeole-
mur and Hadropithecus share a bilophodont molar pattern and various postcra-
nial features with terrestrial cercopithecoid monkeys (Godfrey et al., 1997).
Other groups of Malagasy lemurs retain suites of anatomical traits in common
with early Cenozoic primates. Living lemurids, for example, share numerous
448 Primate Biogeography
features in common with Eocene notharctids, while the postcranial adaptations
of Eocene omomyids are often compared with those of modern cheirogaleids
(Gregory, 1920; Gebo, 1988; Dagosto et al., 1999). Considered as a whole, the
breadth of the Malagasy lemur radiation is astonishing, particularly in light of
the fact that it occurred within the confines of an island encompassing roughly
2% of the area subsumed by Africa.
Compared with the lemuriform example, the adaptive radiation that fol-
lowed the colonization of South America by early platyrrhine monkeys was
relatively modest. Nevertheless, it produced the only primates to be equipped
with a prehensile tail (atelines), a clade of specialized seed predators with
unique dental adaptations (the pitheciines), a small-bodied clade bearing claws
rather than nails on their digits (the callitrichines), and the only nocturnal
anthropoid (Aotus). Despite the morphological and ecological innovations
forged by platyrrhines, the large disparity in area between South America and
Madagascar suggests that the platyrrhine radiation might well have been more
expansive than it actually was. A potential explanation lies in the antiquity of the
lemuriform and platyrrhine radiations (Fleagle and Reed, 2004). In the absence
of direct information from the fossil record, Yoder and Yang (2004) interpret
molecular phylogenetic data as indicating that lemurs have been radiating in
Madagascar since the Paleocene, some 62 Ma. This is more than twice the
age of the earliest known South American monkey (late Oligocene Branisella
boliviana, roughly 25 Ma).
Regardless of their relative breadths, the lemuriform and platyrrhine radi-
ations suffice to illustrate the basic concept that primate dispersal into a new
territory often sparks an adaptive radiation. Beyond simply generating addi-
tional taxonomic diversity, these adaptive radiations also yield novel anatomical
features and unique ecological strategies.
EARLY ANTHROPOIDS FROM AFRICA AND ASIA
By the middle Eocene, early anthropoids show a remarkably broad geographic
distribution, ranging from western Algeria to eastern China (Figure 2; Beard,
2002). However, even by this early date, important anatomical features distin-
guish African and Asian anthropoids. All of the African anthropoids described
until now from this interval—including Algeripithecus,Tabelia, and Biretia—
are documented solely by isolated teeth. Despite this meager fossil record, the
phylogenetic position of these animals is uncontroversial because they bear
Mammalian Biogeography and Anthropoid Origins 449
Figure 2. Map of Africa and Eurasia, showing the wide geographic distribution of
Paleogene anthropoids.
such typically anthropoid features as bunodont upper and lower molars, large
upper molar hypocones, and the loss or reduction of lower molar paraconids
(Bonis et al., 1988; Godinot and Mahboubi, 1992, 1994; Godinot, 1994).
In contrast, Asian middle Eocene anthropoids—typified by Eosimias—retain
numerous primitive features, including the absence of upper molar hypocones
and the presence of large, cuspidate paraconids on all lower molars. Accord-
ingly, although Asian eosimiids are documented by anatomically superior speci-
mens, their anthropoid status remains controversial (Gunnell and Miller, 2001;
Ciochon and Gunnell, 2002; Schwartz, 2003; Simons, 2003). Nevertheless,
comprehensive phylogenetic analyses indicate that eosimiids are basal anthro-
poids (Kay et al., 2004), a conclusion that is upheld by multiple derived charac-
ters in the eosimiid dentition, lower face, and ankle region (Beard et al., 1994,
1996; Jaeger et al., 1999; Gebo et al., 2000, 2001; Beard and Wang, 2004).
The anatomical disparity between African anthropoids such as Algeripithecus
and Asian anthropoids such as Eosimias suggests that cladogenesis between the
450 Primate Biogeography
two groups occurred substantially before the middle Eocene. At the same time,
three lines of evidence indicate that the earliest anthropoids arose in Asia, rather
than Africa. The first of these consists of the extremely basal phylogenetic po-
sition of Eosimias and its Asian relatives on the anthropoid family tree (Beard
et al., 1994, 1996; Gebo et al., 2000, 2001; Beard and Wang, 2004; Kay et al.,
2004). If anthropoids arose some place other than Asia, it is difficult to explain
why Asian eosimiids consistently show up near the base of anthropoid phylo-
genies (e.g., Kay et al., 2004; Seiffert et al., 2004). Indeed, this predicament is
exacerbated by a second factor supporting an Asian origin for anthropoids—the
fact that Tarsius and its fossil relatives are restricted to Asia (or to Laurasia, if
North American omomyids and European microchoerids are regarded as tar-
siiforms) (Beard, 1998b). A wide variety of anatomical, paleontological, and
molecular evidence indicates that tarsiers and their extinct relatives are the sis-
ter group of anthropoids (e.g., Martin, 1990; Kay et al., 2004; Schmitz and
Zischler, 2004). By definition, sister taxa originate at the same time and in
the same place (Beard, 1998a). The restricted geographic range of living and
fossil tarsiers therefore severely constrains the realm of possible locations where
anthropoids may have originated. The final line of support for an Asian origin
for anthropoids comes from paleontological and molecular evidence suggesting
that the initial diversification of primates into strepsirhines, tarsiiforms, and an-
thropoids occurred very rapidly (e.g., Beard and MacPhee, 1994; Yoder, 2003;
Eizirik et al., 2004). Given the overwhelming evidence that primates as a whole
originated in Asia, rapid cladogenesis of the order into its three major subdivi-
sions would have left little time for intercontinental dispersal to intervene and
complicate an otherwise simple biogeographic pattern.
The very early dichotomy between anthropoids and tarsiiforms that is implied
by available molecular and paleontological data explains how African and Asian
anthropoids were able to diverge so widely by the middle Eocene. Further cor-
roboration for the antiquity of the anthropoid clade comes from phylogenetic
analysis of the earliest known euprimate.
PHYLOGENETIC AND BIOGEOGRAPHIC
SIGNIFICANCE OF ALTIATLASIUS
For no other reason than its age, Altiatlasius from the late Paleocene of
Morocco figures prominently in any discussion of the phylogeny and biogeog-
raphy of early primates. Given the significance of Altiatlasius, it is unfortunate
Mammalian Biogeography and Anthropoid Origins 451
that we know so little about the anatomy of this creature. Altiatlasius is docu-
mented by approximately ten isolated teeth and one lower jaw fragment bearing
the germ of an unerupted M2(Sig´e et al., 1990). Not surprisingly, this meager
anatomical record has led to conflicting phylogenetic reconstructions. Altiat-
lasius was originally described as an “omomyid,” but the phylogenetic scheme
adopted by Sig´e et al. (1990, Figure 1) placed Altiatlasius as the sister group
of Simiiformes or Anthropoidea. Subsequent workers have generally supported
and elaborated upon this viewpoint (Godinot, 1994; Beard, 1998b; Seiffert
et al., 2004). Alternatively, Hooker et al. (1999) interpreted Altiatlasius as a
plesiadapiform on the basis of upper molar characters, including an elongated
and buccally oriented postmetacrista and a large parastyle, that they regarded
as being more primitive than those of any known euprimate. However, Beard
and Wang (2004) have recently demonstrated that these same features occur in
Eosimias, thereby enhancing the likelihood that Altiatlasius is a basal anthro-
poid.
The phylogenetic position of Altiatlasius is reexamined here in light of the
new information regarding upper molar anatomy in Eosimias published by
Beard and Wang (2004). An obvious impediment to this analysis is the problem
of missing data for Altiatlasius. Indeed, although Sig´e et al. (1990) ascribed
an isolated lower premolar to Altiatlasius, this attribution is not accepted here
because the tooth differs fundamentally from those of other early anthropoids,
omomyids, and adapiforms. Similar reservations were expressed by Rose et al.
(1994, p. 12). We therefore remain ignorant of such basic aspects of the denti-
tion of Altiatlasius as the dental formula, the size and orientation of the lower
incisors, and the anatomy of all upper and lower tooth crowns anterior to the
molars. Despite these obstacles, the upper and lower molar anatomy of Altiat-
lasius seemingly emits a strong phylogenetic signal. A branch-and-bound search
of 25 dental characters distributed across 11 taxa (Appendices 1 and 2) using
PAUP 4.0b10 (Swofford, 2002) yielded a single most parsimonious tree, which
is illustrated in Figure 3.
Perhaps the most intriguing result of the cladistic analysis performed here
is the support it offers for a close phylogenetic tie between Altiatlasius and
Eosimias. Given the dental characters under consideration, these taxa are most
parsimoniously interpreted as sister groups. Regardless of whether this putative
Altiatlasius +Eosimias clade withstands further scrutiny, both taxa appear to
be stem anthropoids, lying outside a clade including crown anthropoids such as
Saimiri and primitive Fayum anthropoids such as Arsinoea and Proteopithecus.
452 Primate Biogeography
Figure 3. The most parsimonious tree recovered from branch-and-bound search in
PAUP 4.0b10 (Swofford, 2002) of the character-taxon matrix given in Appendix 2. With
the exception of Character 12, all characters were treated as unordered (see Appendix 1).
Tree length =45; consistency index =0.689.
Anatomical support for regarding Altiatlasius as a basal anthropoid comes from
its peculiar upper and lower molar structure, which differs markedly from the
pattern common to other early euprimates (Figure 4). Several authors have
emphasized the remarkable similarity in the dentitions of basal adapiforms and
omomyids (Godinot, 1978; Rose and Bown, 1991; Rose et al., 1994). A very
different dental pattern characterizes Altiatlasius,Eosimias, and other basal
anthropoids. In contrast to those of early adapiforms and omomyids, the up-
per molars of Eosimias and Altiatlasius bear a complete lingual cingulum, an
enlarged parastyle, a well-developed and buccally oriented postmetacrista that
terminates in a weak metastyle, and a paracone and metacone that are situated
internally on the crown (away from the labial margin). Additionally, the upper
molars of Eosimias and Altiatlasius lack any trace of the postprotocingulum, a
structure that is present in basal adapiforms and omomyids. The lower molars of
Eosimias and Altiatlasius differ from those of basal adapiforms and omomyids
in having protoconids that are taller and more voluminous than their corre-
sponding metaconids, entoconids that are shifted mesially to lie near the base
of the postvallid, and hypoconulids that project distally beyond the remainder
of the postcristid. Finally, the paraconid and metaconid cusps on the lower mo-
lars of Eosimias and Altiatlasius do not become increasingly connate from front
Mammalian Biogeography and Anthropoid Origins 453
Figure 4. Schematic drawings of upper and lower second molars in some early eupri-
mates. From left to right, the taxa depicted are as follows: the early Eocene adapiform
Cantius, the early Eocene omomyid Teilhardina, the late Paleocene stem anthropoid
Altiatlasius, and the middle Eocene stem anthropoid Eosimias. Various phylogenetically
significant dental features are highlighted.
to back across the molar series as they do in basal adapiforms and omomyids.
Given how paltry our current knowledge of Altiatlasius is, this taxon shares
an extraordinary number of features in common with Eosimias. Although the
polarity of dental characters is not always easy to establish among basal eupri-
mates, a significant fraction of the features held in common by Eosimias and
Altiatlasius are likely to be derived.
454 Primate Biogeography
If the phylogenetic analysis performed here is accurate (or even roughly so),
Altiatlasius cannot be interpreted as a basal euprimate, despite its age. Its nested
phylogenetic position within the euprimate radiation, along with the absence
of potential primate sister taxa in Africa, indicates that Altiatlasius dispersed to
Africa from elsewhere, with the most obvious option being Asia.
BIOGEOGRAPHY AND ANTHROPOID ORIGINS:
THE SHORT FUSE EXPLODES IN AFRICA
Over the years, scientific attempts to illuminate anthropoid origins have
produced several hypotheses that bear upon the temporal, phylogenetic,
biogeographic, and adaptive contexts of this important macroevolutionary
transformation. Prior to the mid-1990s, most researchers assumed that an-
thropoids originated relatively late in the Paleogene, despite lingering disagree-
ments over the phylogenetic position of anthropoids with respect to other liv-
ing and fossil primates (e.g., Gingerich, 1980; Delson and Rosenberger, 1980;
Rasmussen and Simons, 1992; Rasmussen, 1994). Two main factors appear
to have contributed to the notion that anthropoids originated sometime near
the Eocene-Oligocene boundary. The first of these was a dearth of anthro-
poid fossils dating significantly before the end of the Eocene. The second was
a persistent—yet typically unacknowledged—influence from the Scala natu-
rae positing that, because early anthropoids were “more advanced” than their
prosimian relatives, they must have taken longer to evolve. Regardless of the
conflicting phylogenetic reconstructions of different researchers, we can conve-
niently refer to all hypotheses that advocate such late Paleogene dates as “long
fuse” versions of anthropoid origins (Figure 5). Given the dramatic climatic and
biotic events that transpired near the Eocene-Oligocene boundary, these “long
fuse” versions of anthropoid origins naturally set the stage for broader attempts
to decipher both the biogeographic and adaptive contexts of anthropoid origins
(e.g., Cachel, 1979; Rasmussen and Simons, 1992; Rasmussen, 1994; Holroyd
and Maas, 1994).
Recent discoveries of anthropoid fossils in North Africa and Asia dating to
the earlier part of the Paleogene allow us to reject these traditional “long fuse”
versions of anthropoid origins, for the simple reason that their chronology has
now been falsified. Biogeographic and adaptive hypotheses regarding anthro-
poid origins that are contingent upon such a long fuse can likewise be rejected.
Unless one accepts an inordinately early date for primate origins, we are left with
Mammalian Biogeography and Anthropoid Origins 455
Figure 5. Divergent models of anthropoid origins discussed in the text. Under both
models, the order Primates (abbreviated as “P”) originated in the Paleocene, when the
sister group of Primates (depicted here as Dermoptera) branched away from the ear-
liest members of the primate clade. Likewise, both models accept the monophyly of
Haplorhini (abbreviated as “H”), which originated sometime later in the Paleocene,
coinciding with cladogenesis between ancestral strepsirhines and ancestral haplorhines.
The models disagree on the timing of anthropoid origins, the definition of Anthro-
poidea (abbreviated as “A”), and the phylogenetic position of crown anthropoids and
their closest relatives. Under the short fuse model, Anthropoidea originates in the late
Paleocene, when the lineages culminating in modern tarsiiforms and anthropoids split.
Extinct taxa (including Altiatlasius, Eosimiidae, Amphipithecidae, Parapithecidae, and
Proteopithecidae) that are more closely related to crown anthropoids than to tarsi-
iforms are, by definition, stem anthropoids (abbreviated as “sa”). Under the long fuse
model, Anthropoidea originates in the late Eocene, when stem anthropoids are thought
to have crossed an arbitrary grade-level boundary separating them from their nearest
“prosimian” relatives. In the version of the long fuse model shown here, anthropoids
are depicted as being the descendants of adapiforms (abbreviated as “ad”). Other ver-
sions of the long fuse would regard anthropoids as having descended from omomyids or
some other haplorhine group, yet the chronology of anthropoid origins would remain
largely unaffected.
456 Primate Biogeography
“short fuse” models of anthropoid origins, whereby relatively little time elapsed
between the origin of the order Primates and the establishment of its three ma-
jor clades, Strepsirhine, Tarsiiformes, and Anthropoidea (Figure 5). Although
certain proponents of the molecular clock do indeed advocate surprisingly early
dates for primate origins (e.g., Eizirik et al., 2004), even these workers typically
agree with the “short fuse” prediction that the origin of anthropoids occurred
soon after the first primates evolved.
As we have seen, basic chronological frameworks such as the “short fuse”
model advocated here can impact biogeographic and adaptive hypotheses re-
garding anthropoid origins as well. Indeed, with the demise of adaptive hy-
potheses that sought to link anthropoid origins with the shifting global climate
and environments near the Eocene-Oligocene boundary, there is currently no
compelling explanation for how and why anthropoids achieved their modern
ecological dominance. Given this lack of understanding, recent advances in sev-
eral of the areas reviewed above—including enhanced resolution of mammalian
phylogeny, improvements in our knowledge of the early Cenozoic record of
Africa, and theoretical progress in understanding the interplay between phy-
logeny and biogeography—suggest the following alternative hypothesis.
Basal anthropoids originated in Asia, as did the earliest primates before
them. Molecular and paleontological estimates of the timing of the dichotomy
between anthropoids and tarsiiforms overwhelmingly support the “short fuse”
model, suggesting that the most recent common ancestor of these taxa lived
no later than the late Paleocene (Beard and MacPhee, 1994; Beard, 1998b;
Meireles et al., 2003; Eizirik et al., 2004). Soon after the anthropoid clade
was established in Asia, one or more lineages dispersed to Africa, where basal
anthropoids are documented by Altiatlasius by the late Paleocene. These basal
anthropoids were among the first Laurasian mammals (and the first primates)
to succeed in colonizing the ancestral homeland of the afrotheres. There,
they encountered minimal ecological competition and experienced a rapid
and expansive evolutionary radiation that remains poorly documented in the
African fossil record. Many, perhaps even most, of the diagnostic morphological
synapomorphies that distinguish modern anthropoids from tarsiiforms and
strepsirhines evolved during this early and explosive radiation of African
anthropoids. As a result, some ten million years after their initial colonization
of Africa, middle Eocene anthropoids on that continent were already equipped
with most of the features that distinguish modern anthropoids from their living
and fossil “prosimian” relatives. In contrast, contemporary Asian anthropoids
Mammalian Biogeography and Anthropoid Origins 457
such as Eosimias never experienced the opportunity to radiate in splendid
isolation in Africa. They retained numerous primitive features in common with
Altiatlasius as a result.
How believable is this account of anthropoid origins? Like most freshly
minted hypotheses, it requires further testing before it can be widely accepted.
Nevertheless, the “short fuse” model of anthropoid origins is far more consis-
tent with current knowledge of mammalian and primate phylogeny, the fossil
record, and the complicated ways that phylogeny and biogeography influence
one another than are any of its competitors. For example, even if we have yet
to reach any consensus on identifying the sister group of primates, we know
that primates are not afrotheres. Furthermore, even if we admit that the early
Cenozoic fossil record of Africa remains inadequately sampled, we must ac-
knowledge that most ordinal-level taxa of living placental mammals originated
in Laurasia (more specifically, Asia). The probability that both primates and
anthropoids originated in Asia is therefore extremely high, even if it is not
yet proven. Likewise, while it is obvious that better specimens of Altiatlasius
are necessary to render any final judgement on its phylogenetic position, the
dental similarities shared by it and Eosimias are remarkable, suggesting a close
phylogenetic relationship. Few would contest the fact that these similarities far
outweigh any resemblances between Altiatlasius and other basal euprimates.
Accordingly, until anatomical evidence emerges that would suggest otherwise,
we must assume that Altiatlasius marks the initial colonization of Africa by pri-
mates, rather than any deeper phylogenetic history of primates there. Judging
by the examples provided by Malagasy lemurs and South American platyrrhines,
the dispersal of early primates such as Altiatlasius to an isolated, tropical land-
mass populated by a largely endemic mammalian fauna must have triggered a
tremendous adaptive radiation. One product of this radiation may well have
been the modern anthropoid bauplan, having been molded from one sharing
much in common with primitive haplorhines. If so, chance and historical con-
tingency, rather than long-term adaptive trends and the Scala naturae, account
for this major macroevolutionary transformation among primates.
ACKNOWLEDGEMENTS
I thank John Fleagle for providing the opportunity to contribute to this vol-
ume. An earlier version of the manuscript was improved by comments made by
Erik Seiffert, John Fleagle, and two anonymous reviewers. Thanks also to the
458 Primate Biogeography
numerous colleagues with whom I have worked in the field in Asia in recent
years, including Yaowalak Chaimanee, Daniel L. Gebo, Jean-Jacques Jaeger,
Bernard Marandat, Laurent Marivaux, Ni Xijun, and Wang Yuanqing. Mark
Klingler skillfully prepared the figures. This research has been supported by
National Science Foundation grant BCS 0309800.
APPENDIX 1
Character descriptions
1. i1 orientation: procumbent (0); or relatively vertical (1).
2. i1 size: i1 <i2 (0); i1 =i2 (1); or i1 >i2, or clear evidence of i1 hypertrophy
if i2 absent (2).
3. p1: present (0); or absent (1).
4. p2 root configuration: double-rooted (0); or single-rooted (1).
5. p2 lingual cingulid: absent or incomplete (0); or complete (1).
6. p2 size: p2 significantly smaller than p3 (0); p2 equal to or larger than
p3 (1).
7. p3 exodaenodonty: absent (0); or present (1).
8. p3 lingual cingulid: absent or incomplete (0); or complete (1).
9. p3 mesial root location: directly mesial to distal root (0); mesiobuccal to
distal root (1); or fused with distal root (2).
10. p4 exodaenodonty: absent (0); or present (1).
11. p4 mesial root location: directly mesial to distal root (0); mesiobuccal to
distal root (1); or fused with distal root (2).
12. p4 metaconid: absent (0); present, located inferior and distal to protoconid
(1); or present, located higher on crown and lingual to protoconid (2)
(ordered).
13. m1-2 protoconid size: equal in height to metaconid (0); or taller and more
voluminous than metaconid (1).
14. m1-2 protoconid location: closely appressed with metaconid (0); or widely
spaced buccolingually from metaconid (1).
15. m1-2 entoconid location: at distolingual corner of talonid (0); or shifted
mesially near the base of the postvallid (1).
16. m1-2 hypoconulid development: indistinct (0); or prominent (1).
17. m1-2 hypoconulid location: central, being incorporated within postcristid
(0); distal, projecting beyond postcristid (1); or lingual, being “twinned”
with entoconid (2).
Mammalian Biogeography and Anthropoid Origins 459
18. m2-3 paraconid: more closely connate with metaconid than is the case on
m1 (0); similar in disposition relative to metaconid as on m1 (1); or absent
or highly reduced (2).
19. m3 hypoconulid: projects distally beyond level of hypoconid and ento-
conid, forming a “talonid heel” (0); or evinces weak distal projection, fail-
ing to form a “talonid heel” (1).
20. P3-4 protocone location: fully lingual (0); or mesial and buccal, away from
lingual margin of crown (1).
21. M1-2 lingual cingulum: absent or incomplete (0); or complete (1).
22. M1-2 postprotocingulum: absent (0); or present (1).
23. M1-2 parastyle: absent or only weakly developed (0); or distinct (1).
24. M1-2 conules: present (0); or absent or greatly reduced (1).
25. M1-2 postmetacrista and metastyle: absent or only weakly developed (0);
or present, strongly developed (1).
Taxon-character matrix used in parsimony analysis
Palenochtha 0211? 0??00 00000 00100 01100
Pronothodectes 02110 01001 00000 00000 01000
Altanius 0100? ?1001 01000 01000 01000
Cantius 00000 00100 01000 00000 01000
Teilhardina 02011 00000 01000 00000 01000
Altiatlasius ????? ????? ??111 111?? 10101
Eosimias 10111 01111 11111 11111 10111
Arsinoea 10111 11111 11111 1201? ?????
Proteopithecus 10111 11111 12000 12211 10010
Saimiri 10111 11121 22111 00211 10010
Tarsius 02111 01101 01100 00001 10000
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