Fossil Record of Miocene Hominoids
David R. Begun
Contents
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
What Is a Hominoid? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Origins of Hominidea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Proconsuloidea . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Proconsul . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Other Possible Proconsuloids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Early Hominoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Afropithecus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Morotopithecus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Eurasian Hominoid Origins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
East African Middle Miocene Thick-Enameled Hominoids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Summary of Middle Miocene Hominoid Evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Early Hominids . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Fossil Pongines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Sivapithecus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Ankarapithecus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Other Probable Fossil Pongines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The Earliest Fossil Hominines: The Dryopithecins 1 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Late Miocene European Hominines: The Dryopithecins 2 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Oreopithecus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Late Miocene East African Hominines? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Late Miocene Hominid Extinctions and Dispersals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Cross-References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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D.R. Begun (*)
Department of Anthropology, University of Toronto, Toronto, ON, Canada
e-mail: [email protected]
# Springer-Verlag Berlin Heidelberg 2015
W. Henke, I. Tattersall (eds.), Handbook of Paleoanthropology,
DOI 10.1007/978-3-642-39979-4_32
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Abstract
Hominoids, or taxa identified as hominoids, are known from much of Africa,
Asia, and Europe since the Late Oligocene. The earliest such taxa, from Africa,
resemble extant hominoids but share with them mainly primitive characters.
Middle and Late Miocene taxa are clearly hominoids, and by the end of the
Middle Miocene, most can be attributed to either the pongine (Pongo) or
hominine (African ape and human) clade. Interestingly, there is no definitive
fossil record of the hylobatid clade (gibbons and siamangs), though there have
been some proposed candidates. Miocene hominoids experienced a series of
dispersals among Africa, Europe, and Asia that mirror those experienced by
many other contemporaneous land mammals. These intercontinental movements
were made possible by the appearance of land bridges, changes in regional and
global climatic conditions, and evolutionary innovations. Most of the attributes
that define the hominids evolved in the expansive subtropical zone that was
much of Eurasia. Hominines and pongines diverge from each other in Eurasia,
and the final Miocene dispersal brings the hominine clade to Africa and the
pongine clade to Southeast Asia. Having moved south with the retreating
subtropics, hominines and pongines finally diverge in situ into their individual
extant lineages.
Introduction
Nonhuman fossil hominoids represent a highly diverse and successful radiation of
catarrhine primates known from many localities ranging geographically from
Namibia in the south, Germany in the north, Spain in the west, and Thailand in
the east, and temporally from Oligocene deposits in Kenya to the Pleistocene of
China (Fig. 1). More than 50 genera of nonhuman hominoids are known (Table 1),
probably a small percentage of the total number that have existed. Given the focus
of these volumes on ape and especially human evolution, this survey of the fossil
record of Miocene hominoids will concentrate on taxa that most or all researchers
agree are hominoid and in particular on taxa that are most informative on the pattern
and biogeography of modern hominoid origins.
What Is a Hominoid?
Most of the fossil taxa attributed to the Hominoidea or the Hominidea (new rank,
Table 2) in this chapter are known to share derived characters with living hominoids. Because the two living families of the Hominoidea, Hylobatidae and
Hominidae, share characters that are either absent or ambiguous in their development in Proconsul and other Early Miocene taxa, a new rank is proposed here to
express the monophyly of the Hominoidea and the monophyly of catarrhines more
closely related to extant hominoids than to any other catarrhine. The magnafamily
Hominidea (a rank proposed in a work on perissodactyl evolution; Schoch 1986)
Fossil Record of Miocene Hominoids
1263
Fig. 1 Map showing the location of the Miocene taxa discussed in this chapter. Namibia (southern
Africa), from which Otavipithecus was recovered, is not shown
unites Proconsuloidea with Hominoidea to the exclusion of other catarrhines. This
differs from Harrison’s use of the term proconsuloid that he sees as referring to the
sister taxon to cercopithecoids and hominoids (Harrison 2002).
A few taxa are included in this review if they are too poorly known to preserve
unambiguous hominoid synapomorphies but closely resemble other better-known
fossil hominoids. In general, fossil and living hominoids retain a primitive catarrhine dental morphology. This makes it difficult to assign many fossil taxa to the
Hominoidea since a large number are known only from teeth and small portions of
jaws. Dentally, the most primitive Hominidea differ only subtly from extinct
primitive catarrhines (propliopithecoids and pliopithecoids) (Fig. 2, node 1).
Propliopithecoids (Propliopithecus, Aegyptopithecus) are usually smaller and
have much more strongly developed molar cingula, higher cusped premolars, and
smaller incisors and canines (Begun et al. 1997; Rasmussen 2002; see chapter
“▶ Potential Hominoid Ancestors for Hominidae,” Vol. 3). Pliopithecoids
(Pliopithecus, Anapithecus) are also generally smaller and have molars with more
strongly expressed cingula, more mesial protoconids, and relatively small anterior
teeth (Begun 2002). However, the differences between Late Miocene hominids and
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
Age
Oligo.
Oligo.
Oligo.
eM
eM
eM
eM
eM
eM
eM
eM
eM
eM
eM
eM
eM
eM
eM
e-m M
e-m M
eM
Ma
28–29
25.2
25
21
?20–17.5
?20–17.5
19
19
19
19
19
19
19
18–19
19
19.5–17
17.5
17.5
17.5–15
17.5–15
17
Genera
Saadanius
Rukwapithecus
Kamoyapithecusc
“Proconsul meswae”d
Morotopithecus
Kogolepithecusc
Ugandapithecusd
Xenopithecusc
Proconsul
Limnopithecusc
Rangwapithecusc
Micropithecusc
Kalepithecusc
Dendropithecusc
Lomorupithecus
cf. Proconsule
Turkanapithecus
Afropithecus
Simiolus
Nyanzapithecus
Heliopithecus
Table 1 Genera of fossil ape or apelike taxaa
Important localities
Harrat Al Ujayfa
Rukwa Rift
Lothidok
Meswa Bridge
Moroto
Moroto
Napak/Songhor
Koru
Songhor/Koru
Koru/Songhor
Songhor
Napak/Koru
Songhor/Koru
Rusinga/Songhor/Napak/Koru
Napak
Rusinga/Mfangano
Kalodirr
Kalodirr
Kalodirr/Maboko
Rusinga/Maboko
Ad Dabtiyah
Country
Saudi Arabia
Tanzania
Kenya
Kenya
Uganda
Uganda
K/U
Kenya
Kenya
Kenya
Kenya
K/U
Kenya
K/U
Uganda
Kenya
Kenya
Kenya
Kenya
Kenya
S. Arabia
Materialb
Facial cranium
Mandibular fragment
Craniodental fragments
Craniodental fragments
Cranial, dental, postcrania
Dental
Cranial, dental, postcrania
Craniodental fragments
Cranial, dental, postcrania
Craniodental
Craniodental
Craniodental
Craniodental fragments
Cranial, dental, postcrania
Craniodental fragments
(Cranial, dental, postcrania)+
Cranial, dental, postcrania
Cranial, dental, postcrania
Cranial, dental, postcrania
Craniodental fragments
Dental
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22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41
42
43
eM
eM
mM
mM
mM
mM
mM
mM
mM
mM
m-l M
m-l M
lM
lM
lM
lM
lM
lM
lM
lM
lM
lM
16.5
16
15
15
15
13
13
12.5
12.5
12.5
12.5–7
?13.5–7
10
10–9
11–8?
10
9.5
10.25
9.85
9.5
9–8
9–8
cf. Griphopithecus
Griphopithecus
Equatorius
Mabokopithecus
Nacholapithecus
Kenyapithecus
Otavipithecus
Pierolapithecus
Dryopithecus
Anoiapithecus
Sivapithecus
Khoratpithecusf
Rudapithecus
Hispanopithecus
Neopithecusg
Ankarapithecus
Samburupithecus
Chororapithecus
Nakalipithecus
Ouranopithecus
Graecopithecus
Lufengpithecus
Engelswies
Paşalar/Çandır
Maboko/Kipsarimon
Maboko
Nachola
Fort Ternan
Otavi
Els Hostalets de Pierola
St. Gaudens, La Grive
Els Hostalets de Pierola
Potwar Plateau
Magaway (M), Khorat)/Ban Sa (Th.)
Rudabánya
Can Llobateres/Can Ponsic
Salmendingen
Sinap
Samburu
Chorora Fm
Nakali
Ravin de la Pluie
Pygros
Lufeng
Germany
Turkey
Kenya
Kenya
Kenya
Kenya
Namibia
Spain
France
Spain
Pakistan
Thailand/Myanmar
Hungary
Spain
Germany
Turkey
Kenya
Ethiopia
Kenya
Greece
Greece
China
(continued)
Dental
Cranial (dental)+, postcrania
(Cranial, dental, postcrania)+
Dental
Partial skeleton
Cranial, dental, postcrania
Craniodental, vertebra
Partial skeleton
Mandibles + teeth
Craniodental
(Cranial, dental, postcrania)+
Craniodental fragments
(Cranial, dental, postcrania)+
(Cranial, dental, postcrania)+
m3
Cranial, dental, postcrania
Craniodental fragments
Isolated teeth
Mandible and teeth
(Craniodental)+, 2 phalanges
Mandible
(Cranial, dental)+, postcrania
Fossil Record of Miocene Hominoids
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Ma
8–7
7
7–6
6.5
6
5.8–5.2
1–0.3
Genera
New taxon
Oreopithecus
Sahelanthropus
Indopithecus
Orrorin
“Ardipithecus”h
Gigantopithecus
Important localities
Çorakyerler
Baccinello/Monte Bamboli
Toros-Menalla
Potwar Plateau
Lukeino
Alayla (Middle Awash)
Liucheng
Country
Turkey
Italy
Chad
Pakistan
Kenya
Ethiopia
East Asia
Materialb
Mandible, maxilla
(Cranial, dental, postcrania)+
Craniodental
Mandible
Craniodental, postcrania
Craniodental, postcrania
Mandibles, teeth
Oligo. Oligocene, e M Early Miocene, e-m M early Middle Miocene, m M Middle Miocene, m-l M Middle-Late Miocene, l M Late Miocene, K/U Kenya and
Uganda, Pl. Pleistocene, M Myanmar (Burma), Th. Thailand
a
These 50 genera include taxa from the Oligocene and Early Miocene that share mainly primitive characters with the Hominoidea but that appear to be derived
relative to pliopithecoids and propliopithecoids. Please see text for further discussion
b
Material briefly described by part representation. Dental ¼ mainly isolated teeth; Dental, mandible, maxilla ¼ known only from these parts; Craniodental
fragments ¼ teeth and few cranial fragments; Craniodental ¼ larger samples of more informative cranial material; Cranial, dental, postcrania ¼ good
samples from each region; ( ) + ¼ very good representation of parts in parentheses
c
Unclear attribution to Hominoidea
d
Large taxon possibly distinct from Proconsul
e
Proconsul from the Rusinga and Mfangano localities in Kenya is likely to be distinct at the genus level from the Proconsul type material
f
Middle Miocene samples attributed to this taxon are more fragmentary and may not be congeneric
g
The Neopithecus brancoi type is an isolated M3 that some attribute to the Pliopithecoidea while other to Dryopithecus (Begun and Kordos 1993). I regard this
as a nomen dubium
h
“Ardipithecus kadabba.” The type of the genus, Ardipithecus ramidus, is younger and shares derived characters with australopithecines not present in
A. kadabba, making Ardipithecus in my opinion paraphyletic
44
45
46
47
48
49
50
Age
lM
lM
lM
lM
lM
lM
Pl.
Table 1 (continued)
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Fossil Record of Miocene Hominoids
Table 2 A taxonomy of
the Hominidea
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Cercopithecidea (Magnafamily, new rank)
Hominidea (Magnafamily, new rank)
Proconsuloidae
Crown hominoids of uncertain status
Proconsul
Kenyapithecus
cf. Proconsul
Oreopithecus
Samburupithecus
Family incertae sedis
Micropithecus
Afropithecus
Hominoidea
Morotopithecus
Hylobatidae
Heliopithecus
Hylobates
Griphopithecus
Hominidae
Equatorius
Nacholapithecus
Dryopithecusa
Otavipithecus
Hispanopithecus
Rudapithecus
Ouranopithecus
Superfamily incertae sedis
Graecopithecus
Rangwapithecus
Sivapithecus
Nyanzapithecus
Lufengpithecus
Mabokopithecus
Khoratpithecus
Turkanapithecus
Ankarapithecus
Magnafamily incertae sedis
Gigantopithecus
Kamoyapithecus
Indopithecus
Chororapithecus
Nakalipithecus
Sahelanthropus
Dendropithecus
Orrorin
Simiolus
Homo
Limnopithecus
Ardipithecusb
Kalepithecus
Praeanthropus
Australopithecus
Paraustralopithecus
Paranthropus
Pongo
Pan
Gorilla
a
Includes Pierolapithecus and Anoiapithecus
Includes two genera
b
Late Miocene pliopithecoids are more marked than between Early Miocene
Hominidea and pliopithecoids, making defining features less than clear-cut. Cranially Hominidea have a completely ossified tubular ectotympanic, which distinguishes them from both propliopithecoids and pliopithecoids but not from
cercopithecoids. Saadanius shares a completely ossified tubular ectotympanic
with crown catarrhines (Hominidea and Cercopithecidea). This has led some
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Fig. 2 Cladogram depicting the relations among most Miocene Hominidea discussed in this
chapter. The cladogram is resolved only at the level of the family in many cases, except within the
Hominidae, where most clades are resolved. Numbered nodes refer to characters or suites of
characters that serve to define clades. They are not intended as comprehensive lists of synapomorphies. For clarity, Hispanopithecus and Rudapithecus, together a sister clade to Dryopithecus,
are not shown. Node 1: reduced cingula, delayed life history (M1 emergence), incipient separation
of the trochlea and capitulum, increased hip and wrist mobility, powerful grasping, coccyx
(no tail). Node 2: thick enamel, increased premaxillary robusticity, further reduction in cingula,
Fossil Record of Miocene Hominoids
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researchers to conclude that Saadanius represents the common ancestor of crown
catarrhines and that its age (28–29 Ma) must be the oldest possible age of divergence of the Old World Monkeys and apes (Zalmout et al. 2010). This conclusion,
however, does not follow from the evidence. While Saadanius may preserve
characters that approximate or even duplicate those of the last common ancestor
of Old World Monkeys and apes, its geological age is irrelevant to the question of
the age of divergence of these two lineages Pozzi et al. 2011. We have no idea how
long Saadanius or its relatives lived before the 28–29 Ma specimens that were
discovered. The taxon could be millions of years older, and in fact, we have this
very problem with the pliopithecoids. Most if not all pliopithecoids are known from
Eurasia, and they range in age between about 18 and 9 Ma, but they lack synapomorphies of the crown catarrhini. Using the same logic applied to the interpretation of
Saadanius, the age of the pliopithecoids would indicate a divergence date of not more
than 18 Ma for Old World Monkeys and apes, or even 9 Ma, if the last appearance of
the Pliopithecoidea is taken as the divergence date. Clearly this lineage is millions of
years older than the age of the oldest fossils we have of the group, and these oldest
specimens remain to be discovered. Pliopithecoids represent what we call a ghost
lineage, with a huge gap between their origin and first appearance in the fossil record.
The same can be said of gibbons or for that matter, African apes. While we have
convincing evidence of the Pongo clade at 12 Ma or so and the human lineage at
7 Ma or so, there is no evidence of Pan or Gorilla at all, with the possible exception of
teeth attributed to Pan from a 500 Ka site in Kenya (McBrearty et al. 2005), many
millions of years after their divergence from humans. The same is very probably true
of Saadanius. When coupled with the convincing genetic data suggesting a divergence date of at least 30 Ma (Disotell et al. 2011), the claims of a more recent
divergence based on Saadanius do not hold up.
Unfortunately, few Miocene Hominidea fossils preserve the portion of the
temporal bone that includes the ectotympanic, so in many cases, we simply do
not know if this key crown catarrhine synapomorphy was present or not. In
addition, hylobatids, cranially the most primitive extant hominoid, share many
features found in short-faced Old and New World monkeys, again making it
difficult to tease out synapomorphies. Hominoids show a tendency to expand the
length and superoinferior thickness or robusticity of the premaxilla, with increasing
overlap with the palatine process of the maxilla over time, but once again this is not
present in hylobatids or in early well-preserved specimens of Proconsul, for
example (Begun 1994a). Only one specimen of Early Miocene Hominidea is
ä
Fig. 2 (continued) increase in P4 talonid height, possible increases in forelimb-dominated positional behaviors. Node 3: further “hominoidization” of the elbow. The position of Kenyapithecus is
extremely unclear. Without this taxon, node 3 features the numerous characters of the hominoid
trunk and limbs related to suspensory positional behavior. Node 4: Hominidae (see text). Node 5:
Homininae (see text). Lack of resolution of the hominini reflects continuing debate on relations
among Pliocene taxa that is beyond the scope of this chapter. Pierolapithecus may be a stem
hominid or stem hominine, as depicted here. Node 6: Ponginae (see text). Gigantopithecus is
probably a pongine but the relations to other pongines are unclear
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complete enough to say much about the brain, and there are no unambiguous
synapomorphies linking it to hominoids. The brain of Proconsul is similar relative
to body size to both hylobatids and papionins, the Old World monkeys with the
largest brains, and the sulcal pattern, while debatable, lacks most if not all hominoid
features (Falk 1983; Begun and Kordos 2004). Like hylobatids, most
cercopithecoids, and most mammals other than hominids, a portion of the brain
of Proconsul occupied a large the subarcuate fossa of the temporal bone. Cranial
and dental evidence also suggests that Proconsul was moderately delayed in terms
of life history, another similarity with extant hominoids (Kelley 1997, 2004).
Postcranially, Proconsul more clearly represents the ancestral hominoid
morphotype, though this too is the subject of debate. Proconsul fossils exhibit
hominoid attributes of the elbow, wrist, vertebral column, hip joint, and foot, though
in all cases these are subtle and disputed (Beard et al. 1986; Rose 1983, 1988, 1992,
1994, 1997; Ward et al. 1991; Ward 1993, 1997a; Begun et al. 1994; but see Harrison
2002, 1987). Proconsul has a suite of characters consistent with the hypothetical
ancestral morphotype of the hominoids, and it should not be surprising that these are
poorly developed at first, only to become more defined as hominoids evolve. In
comparison with the hominoid outgroup (cercopithecoids), we can expect the earliest
hominoids to show subtle indications of increased orthogrady, positional behaviors
with increased limb flexibility and enhanced grasping capabilities and no tail, generalized (primitive) dentition, encephalization at the high end of extant cercopithecoids
of comparable body mass, and life history variables closer to extant hominoids than
to extant cercopithecoids (see chapter “▶ Estimation of Basic Life History Data of
Fossil Hominoids,” Vol. 1). Proconsul has all of these attributes.
If these are the features that define the Hominidea, which taxa among Miocene
fossil catarrhines are not Hominidea? Even the earliest cercopithecoids (victoriapithecids) are easily distinguished from hominoids (Benefit and McCrossin 2002).
Pliopithecoids, often grouped with the “apes,” are even more distantly related. They
are clearly stem catarrhines lacking synapomorphies of all crown catarrhines
including Proconsul and Victoriapithecus (Begun 2002). The most informative
among these synapomorphies are the tubular ectotympanic and the entepicondylar
groove (often referred to as the absence of an entepicondylar foramen). In the
following sections, I will summarize current knowledge of the Miocene Hominidea,
focusing on well-known taxa that serve to illustrate important events in hominoid
evolutionary history (Fig. 2).
Origins of Hominidea
It is likely that hominoids originated in Africa from an ancestor that, if known,
would be grouped among the Pliopithecoidea. Pliopithecoids, currently known only
from Eurasia, share with all catarrhines the same dental formula and possibly with
crown catarrhines a reduction of the midface, subtle features of the molar dentition,
and a partial ossification of the ectotympanic tube (Begun 2002). The presence
of pliopithecoids in Africa is suggestive but remains to be demonstrated
Fossil Record of Miocene Hominoids
1271
(Andrews 1978; Begun 2002; Rossie and MacLatchy 2006). The oldest and most
primitive catarrhine that can lay claim to hominoid status however is African
(Table 1). Kamoyapithecus, from the Oligocene of Kenya, differs from other
Oligocene catarrhines (propliopithecoids) in being larger and having canines and
premolars that more closely resemble Miocene hominoids than Oligo-Miocene
non-hominoids (Leakey et al. 1995). Only craniodental material of Kamoyapithecus
has been described, and it is so primitive as to make attribution to the Hominoidea
difficult. Though it would fail to fall among the Hominoidea in a quantitative
cladistic analysis due to its fragmentary preservation and primitive morphology,
it makes in my view a good Hominidean precursor. Stevens et al. (2013) report on a
new taxon, Rukwapithecus, from 25.2 Ma sediments in Tanzania. The specimen
consists of a nicely preserved right mandible of a juvenile individual with the p4 to
m2 erupted and the m3 still in its crypt. Unfortunately, and this is frustratingly
common, no teeth can be directly compared between Kamoyapithecus and
Rukwapithecus, as the latter is known only from lower postcanine teeth, none of
which are known for Kamoyapithecus. We cannot rule out the possibility that
Rukwapithecus is a junior subjective synonym of Kamoyapithecus and only more
fossils will help to resolve this question. On the other hand, Stevens et al. (2013)
characterize Rukwapithecus as the oldest known fossil ape and tentatively classify it
among the nyanzapithecines, a poorly defined and possibly paraphyletic taxon that
includes Rangwapithecus and Nyanzapithecus. These taxa do have some unusual
features of the lower dentition, but given the tiny sample size, it is premature in my
opinion to consider the “nyanzapithecines” and Rukwapithecus in particular to be
more closely related to Middle Miocene and later hominoids than Proconsul, as
Stevens et al. (2013) suggest. Koufos (see chapter “▶ Potential Hominoid Ances
tors for Hominidae,” Vol. 3) covers some of the same fossils as covered here, with
some differences in interpretation. Senut (chapter “▶ The Miocene Hominoids and
the Earliest Putative Hominids,” Vol. 3) proposes some radically different interpretations of some of the material presented here, in addition to interpretations of
the latest Miocene and the Pliocene hominin fossil record that differ from any other
published interpretation of which I am aware. Both authors and Schwartz (chapter
“▶ Defining Hominidae,” Vol. 3) employ the term hominid to mean humans and
taxa more closely related to humans than to any other taxon. The vast majority of
researchers employ the term as it is used here, referring to great apes and humans
and all fossil taxa more closely related to these crown taxa than to hylobatids.
Proconsuloidea
Proconsul
The superfamily Proconsuloidea, as defined by Harrison (2002), includes many
mainly Early Miocene taxa. As noted, in this chapter, a number of taxa from this
group are interpreted to represent primitive Hominidea or hominoids. A hypothetical ancestral morphotype for the Hominidea is given in Fig. 2 (node 1). Node 1
1272
D.R. Begun
Plate 1 Proconsul from the
Tinderet localities of Songhor
and Koru. The two
P. africanus specimens to the
left are male as is the P. major
mandible to the right. From
left to right, M 14084
(P. africanus type), KNM-SO
1112, M 16648. Not to scale.
P. major is much larger
represents the bifurcation of Proconsul from hominoids with more apparent
synapomorphies to living hominoids. Proconsul as described here is based mainly
on the sample from Rusinga Island and Mfangano, two localities that are close
together on Lake Victoria, western Kenya. These sites are often referred to as the
Kisingiri Proconsul localities, as opposed to the Tinderet localities of Songhor,
Koru, Legetet, and Chamtwara, among others. The Kisingiri include the species
Proconsul heseloni (Walker et al. 1993) and Proconsul nyanzae (Le Gros Clark and
Leakey 1950). The type specimen of Proconsul africanus (Hopwood 1933) is from
Koru, and the type of Proconsul major (Le Gros Clark and Leakey 1950) is from
Songhor, both of which are Tinderet localities (Drake et al. 1988). Historically the
Tinderet localities have been considered to be older than the Kisingiri sites (Drake
et al. 1988), but this new evidence indicates that there is some overlap in ages
(Table 1) (McNulty personal communication). There is strong evidence that the
Kisingiri species of Proconsul that are the basis of the description here actually
belong to a different genus from the Tinderet types (see below). However, as this is
not the appropriate venue to name a new genus, I will follow convention and refer to
the Rusinga sample as Proconsul. In the end, both taxa traditionally attributed to
Proconsul are most likely to be sister taxa, so whether it is one genus or two is only
of interest to those who are working directly on this material, though when worked
out it will give us a much better idea of the actual specimen composition of each
taxon, which is the necessary precursor to any analysis of the paleobiology of fossil
taxa (Plates 1, 2, and 3).
Postcranial Morphology
Proconsul and other proconsuloids are defined by a large number of characters.
Proconsul is a generalized arboreal quadruped but is neither monkey-like nor
apelike (Rose 1983). The following summary is mainly from Rose (1997), Ward
(1997a), and Walker (1997). In addition to the characters noted that emphasized its
hominoid affinities, Proconsul has limbs of nearly equal length (though the forelimbs were probably slightly longer than the hindlimbs), with scapula positioned
laterally on the thorax and the ovoid and narrow glenoid positioned inferiorly, as in
Fossil Record of Miocene Hominoids
1273
Plate 2 “Proconsul”
heseloni from Rusinga.
KNM-RU 2036 on the left is
the type specimen and is
female, while the specimen to
the right (KNM-RU 2087) is a
male
Plate 3 “Proconsul”
nyanzae from Rusinga.
M16647 on the right is the
type specimen and male.
KNM-RU 7290 is a female
generalized quadrupeds. The thorax is transversely narrow and deep superoinferiorly, and the vertebral column is long and flexible, especially in the lumbar
region. The innominate is long with a narrow ilium and an elongated ischium. The
sacrum is narrow, and its distal end indicates that it articulated with a coccygeal and
not a caudal vertebra, in other words Proconsul had a coccyx and not a tail (Ward
et al. 1991).
In the details of limb morphology, Proconsul also combines aspects of monkey
and ape morphology. Proconsul forelimbs lack the characteristic elongation of ape
forelimbs, though this trend in ape evolution may be represented by some slight
forelimb elongation in Proconsul. The humeral head is oriented posteriorly relative
to the transverse plane, and the humeral shaft is convex anteriorly, both of which are
consistent with the position of the glenoid fossa and the shape of the thorax. The
distal end of the humerus lacks the enlargement of the capitulum and trochlea and
other details of the hominoid elbow, but it does have a narrow zona conoidea and a
mild trochlear notch. These are characters that are more strongly developed in
extant apes that are universally regarded as indications of suspensory positional
behavior. It is interesting that Proconsul shows incipient signs of apelike morphology in the elbow while lacking other more definitive indicators of orthogrady or
suspension. It is possible that these early, subtle changes in the elbow and in other
1274
D.R. Begun
areas of the postcranium of Proconsul are related to the positional demands of an
animal moving around in the trees without a tail (see below).
The medial epicondyle is more posteriorly oriented as in monkeys. The proximal
ends of the radius and ulna are consistent with the morphology of the distal
humerus. The radial head is small and ovoid, the ulnar trochlea is narrow and has
a poorly developed keel, and the radial notch is positioned anteriorly. The ulna also
has a large olecranon process. All of these features are consistent with generalized
pronograde (above branch) quadrupedalism as opposed to antipronograde (suspensory or below branch) (Ward 2007).
Distally, the radial carpal surface is flat and articulates mainly with the scaphoid.
The ulnar head is comparatively large with a long and prominent styloid process that
articulates directly with the pisiform and triquetrum, unlike living hominoids, which
have greatly reduced ulnar styloids and no contact with the carpals. However, the
nature of the contact between the ulnar styloid and the pisiform and triquetrum differs
from that of monkeys and does suggest a greater degree of mobility, or at least a
different pattern of mobility, than seen in Old World Monkeys (Beard et al. 1986). The
carpals are small transversely. The scaphoid is separate from the os centrale and the
midcarpal joint is narrow. The hamate hamulus is small, and the surface for the
triquetrum is flat and mainly medially oriented (Beard et al. 1986). However, the
manner in which the bones of the wrist come together in Proconsul shares attributes
with monkeys and apes, making it unique. Nevertheless, in my view, the Proconsul
wrist does provide evidence of an incipient transformation for a more stable
pronograde-dominated posture to more diverse habitual postures. The metacarpal
surfaces of the distal carpals are small and comparatively simple as are the
corresponding surfaces on the metacarpal bases. The metacarpals are short and straight
and their heads transversely narrow. The proximal ends of the proximal phalanges are
slightly dorsally positioned as in palmigrade quadrupeds. All the phalanges are short
and straight compared with apes, though secondary shaft features, in particular of the
proximal phalanges, suggest powerful grasping (Begun et al. 1994).
The hindlimbs of Proconsul are also dominated by monkey-like characters.
The long bones are long and slender. The femoral head is small compared to apes,
but its articulation with the acetabulum indicates more mobility compared to most
monkeys. The feet of Proconsul are monkey-like in their length-to-breadth ratio
(they are narrow compared to great ape feet). Proconsul tarsals are elongated
relative to breadth and the metatarsals long compared to the phalanges. Like those
of the hands, the foot phalanges of Proconsul are straighter and less curved than in
apes but with more strongly developed features related to grasping than in most
monkeys. The hallucial phalanges are relatively robust, suggestive of a powerfully grasping big toe. Body mass estimates for the species of Proconsul, based
mainly on postcranial evidence, range from about 10 to 50 kg (Ruff et al. 1989;
Rafferty et al. 1995). The lower estimate is based in part of juvenile specimens,
and it is probable that the smallest adult Proconsul weighed about 15 kg. In
addition to morphological evidence, the range of body mass estimates in Proconsul from Rusinga and Mfangano strongly suggest that at least two species are
represented.
Fossil Record of Miocene Hominoids
1275
Fig. 3 Midsagittal cross section of a number of Hominidea palates showing some of the features
described in the text. Proconsul has a small premaxilla and a fenestrated palate (large foramen and
no overlap between the maxilla and premaxilla). Nacholapithecus has a longer premaxilla with
some overlap. It is similar to Afropithecus and conceivably could be the primitive morphotype for
the Hominidae. Pongo and Sivapithecus have a similar configuration but with further elongation
and extensive overlap between the maxilla and premaxilla, producing a smooth subnasal floor.
Hominines have robust premaxillae that are generally shorter and less overlapping than in
Sivapithecus and Pongo. Dryopithecus is most similar to Gorilla, which may represent the
primitive condition for hominines. Pan and Australopithecus have further elongation and overlap,
but the configuration differs from Pongo. This morphology is suggested to be an important
synapomorphy of the Pan/Homo clade (Begun 1992b) (Modified from Begun 1994)
Craniodental Morphology
As noted, Proconsul has a moderate amount of encephalization (comparable to
hylobatids and papionins), a short face with a fenestrated palate (Fig. 3), a smoothly
rounded and somewhat airorhynchous face (Fig. 4), and a generalized dentition.
Morphologically, the dentition is consistent with a soft fruit diet, and microwear
analysis suggests the same (Kay and Ungar 1997; chapter “▶ Dental Adaptations of
African Apes,” Vol. 2). The somewhat enlarged brain of Proconsul implies a degree
of life history delay approaching the hominoid pattern (Kelley 1997, 2004; Kelley
and Smith 2003; Smith et al. 2003).
One aspect of the cranium of Proconsul that has received some attention is the
frontal sinus. Walker (1997) interprets the presence of a frontal sinus in Proconsul
to indicate its hominid status, citing the presence of large frontal sinuses in some
great apes. Other researchers have suggested that the frontal sinus is a primitive
character, as it is found in Aegyptopithecus and many New World monkeys
(Andrews 1992; Rossie et al. 2002). The confusion stems from the use of one
term to describe several different characters. As Cave and Haines (1940) noted long
1276
D.R. Begun
Fig. 4 Lateral views of some Hominidea crania showing possible changes through time. A mildly
airorynch Proconsul may be a good ancestral morphotype for hominoid craniofacial hafting, as a
similar degree of airorhynchy is also found in hylobatids (Shea 1988). Rudapithecus shares with
other hominines neurocranial elongation (though this also occurs in hylobatids), the development
of supraorbital tori, klinorhynchy, and, probably in association with the latter, a true
frontoethmoidal sinus (Modified from Kordos and Begun (2001))
ago, frontal sinuses in primates have various ontogenetic origins, and it is likely that
they are not homologous across the primates. New World monkeys have frontal
sinuses that are outgrowths from the sphenoid sinus, as is also the case for
hylobatids. On the other hand, Pongo, which occasionally has a frontal sinus,
derives it from the maxillary sinus (see chapter “▶ Defining Hominidae,” Vol. 3).
African apes and humans normally have large frontal sinuses derived from the
ethmoidal sinuses. “Frontal sinuses” then are actually three different characters,
frontosphenoidal sinuses, frontomaxillary sinuses, and frontoethmoidal sinuses.
While it is possible to establish the ontogenetic origin of a pneumatized frontal
bone in living primates, it is more difficult in fossil primates. However, the
placement and size of the frontal sinuses correlate very well with their ontogenetic
origin, offering a protocol for identifying the specific type of frontal sinus present in
a fossil (Begun 1994a). Frontosphenoidal sinuses invade large portions of the
frontal squama but not the supraorbital or interorbital regions. Frontomaxillary
sinuses are infrequent in Pongo, but when they occur, they are associated with
narrow canals or invaginations connecting the maxillary sinuses to a small
pneumatization of the frontal via the interorbital space. In African apes and
humans, the frontoethmoidal sinuses arise from a spreading of the ethmoidal air
cells in the vicinity of nasion, resulting in large pneumatizations from below nasion
into the supraorbital portion of the frontal. The actual amount of frontal
pneumatization is variable, while the presence of a large sinus around nasion is
Fossil Record of Miocene Hominoids
1277
constant. Therefore, while we cannot observe the development of frontal
pneumatization in fossil primates, and we do not have adequate ontogenetic series
to directly reconstruct this growth, we can infer the type of frontal pneumatization
from its position, extent, and connection to the source sinus. In Proconsul, as in
hylobatids, New World monkeys, and Aegyptopithecus, the frontal pneumatization
is extensive and occupies the frontal squama, consistent with a frontosphenoidal
sinus. Thus, the “frontal sinus” in Proconsul is a primitive character, as suggested
by Andrews (1992), but for different reasons. The frontal pneumatization of
Rudapithecus, on the other hand, conforms to the pattern seen exclusively in
African apes and humans (see below).
In summary, Proconsul was an above branch mid- to large-sized catarrhine with
a diet dominated by soft fruits and a somewhat slower life history than
cercopithecoids. Encephalization may imply other similarities to hominoid behavioral or social ecology, or it may simply be a consequence of relatively large body
mass and/or a slower life history (Kelley 2004; Russon and Begun 2004). The
slightly enhanced range of motion in Proconsul limbs may imply some degree of
orthogrady, it may be a consequence of the absence of a tail, of large body mass in
an arboreal milieu, or, most likely, some combination of all three (Beard et al. 1986;
Begun et al. 1994; Kelley 1997).
Other Possible Proconsuloids
A number of taxa are regarded by many researchers as having a probable close
relationship to Proconsul. The three with the best evidence for affinities to the
proconsuloids are Proconsul sensu stricto, Micropithecus, and Samburupithecus.
As noted, the type species of the genus Proconsul is P. africanus. P. africanus and
P. major, both from Tinderet sites, are never found together with Proconsul from
Rusinga and are also more primitive and lack synapomorphies shared by Proconsul
from Rusinga and other hominoids (see below). Other taxa listed in Table 2 are
either more likely to be hominoids given similarities to known hominoids
(Rangwapithecus, Nyanzapithecus, Mabokopithecus) or they are so primitive or
poorly known as to make unclear their magnafamily status.
Proconsul sensu stricto
The species of Proconsul sensu stricto from Songhor and Koru (P. africanus and
P. major) probably represent a different genus from P. heseloni and P. nyanzae, the
samples on which the descriptions of Proconsul presented here are based. A new
genus would replace P. heseloni and P. nyanzae, as P. africanus has priority.
Proconsul sensu stricto from Songhor and Koru has elongated postcanine teeth,
more strongly developed cingula, upper premolars with strong cusp heteromorphy,
and conical, individualized molar cusps, all of which suggest that the older species
are in fact more primitive. The two Tinderet species differ from each other mainly in
size. Postcrania attributed to Proconsul from the Tinderet Proconsul sensu stricto
localities are distinct from postcrania from the younger Proconsul localities such as
1278
D.R. Begun
Rusinga, in details that have been correlated to paleoecological differences (Andrews
et al. 1997). While sufficiently similar to the better-known younger Proconsul sample
to warrant placing both in the same superfamily, the more modern morphology of the
younger Proconsul sample will almost certainly require taxonomic recognition.
Ugandapithecus, based on the sample of P. major, adds to the confusion (Senut
et al. 2000). Ugandapithecus is not a useful nomen in that it mixes a number of
specimens from different localities, different sizes, and even different morphologies, and it has not been effectively compared with and distinguished from either
Proconsul sensu stricto or the Kisingiri sample. Therefore, the nomen is not
recognized here except as a junior subjective synonym of Proconsul. Nevertheless,
it turns out that Proconsul as traditionally defined probably does represent more
than one genus. Senut et al. (2000; see chapter “▶ The Miocene Hominoids and the
Earliest Putative Hominids,” Vol. 3) have suggested that large-bodied hominoids
from Moroto, in Uganda, that is, P. major, may also be attributed to
Ugandapithecus (hence the name, though the type is from Kenya), calling into
question the interpretation that hominoid cranial and postcranial fossils from
Moroto belong to one taxon (Morotopithecus). However, the evidence for more
than one large hominoid genus at Moroto is not strong (see below).
Micropithecus
Micropithecus (Fleagle and Simons 1978) is a small catarrhine with comparatively
broad incisors and long postcanine teeth with low cusps and rounded occlusal
crests. The cingula are less strongly developed than most other Early Miocene
catarrhines. Males and females exhibit marked size dimorphism. Comparisons with
living catarrhines suggest a body mass of about 3–5 kg (Harrison 2002). While
Harrison (2002, 2010) considers this taxon to be even more distantly related to the
Hominoidea than are the Proconsuloidea, the subtly more modern features of the
dentition suggest that it may belong to the Proconsuloidea. Fleagle and Simons
(1978) in fact attribute Micropithecus to the Hominoidea, although as noted the
features shared with hominoids are very subtle. If Micropithecus is a proconsuloid,
as preferred here, it would indicate that the proconsluoids were quite diverse in
body mass, as is the case in all catarrhine superfamilies.
Samburupithecus
Samburupithecus is another possible proconsuloid, known only from a large maxillary fragment from the Late Miocene of the Samburu region of Kenya (Ishida and
Pickford 1997). Ishida and Pickford (1997) have suggested that Samburupithecus is an
early member of the African ape and human clade, while others place it within the
hominoids, but without specific affinities to any living clade (e.g., Harrison 2010; see
chapter “▶ The Miocene Hominoids and the Earliest Putative Hominids,” Vol. 3).
However, Samburupithecus retains many primitive characters of the Proconsuloidea.
These include a low root of the zygomatic processes, a strongly inclined nasal aperture
edge, the retention of molar cingula, and thick enamel with high dentine relief (Begun
2001). Samburupithecus is most likely to be a late surviving proconsuloid. Its unusual
dental characters (e.g., large molars with individualized cusps separated by deep
Fossil Record of Miocene Hominoids
1279
Plate 4 Comparison
between Samburupithecus,
KNM-SH 8531 (left) and
“Proconsul” (KNM-RU
1677a). Note the strongly
developed molar cingula and
the small M1 relative to M2 in
both specimens. The molars
are similar in overall
morphology as well
narrow fissures) are reminiscent of morphological “extremes” found in terminal
lineages with long evolutionary histories. Oreopithecus, Gigantopithecus,
Paranthropus, Daubentonia, and Ekgmowechashala all share with Samburupithecus
exaggerated occlusal features compared with other members of their respective
clades. The size and occlusal morphology of Samburupithecus that superficially
resembles Gorilla (Ishida and Pickford 1997) may be related in part to the fact that
both are ends of long phylogenetic branches. In a pattern analogous to long branch
attraction in molecular systematics, there is a tendency for separate long isolated
lineages to converge in certain aspects of their morphology (Begun 2001). For
whatever the reason, in its details Samburupithecus is primitive and more likely to
belong to the proconsuloids than the hominoids (Plate 4).
Nyanzapithecines
In contrast to the phylogeny presented in Stevens et al. (2013), I consider
Rangwapithecus and Nyanzapithecus to be proconsuloids and not more closely related
to more modern apes. Harrison (2010) includes the nyanzapithecines among the
proconsuloids, and that is the view adopted here. Nyanzapithecines as defined by
Harrison (2002, 2010) include a diverse assemblage of fossil taxa ranging in dental
size from somewhat smaller that Proconsul to the size of Proconsul heseloni or
P. africanus. Several of these specimens are beautifully preserved, including the
holotypes of Rangwapithecus and Turkanapithecus. There is a nicely preserved
mandible of Nyanzapithecus as well. Yet, these taxa have proven extremely resistant
to classification. I am not convinced that the Nyanzapithecinae as constituted by
Harrison (2010) is a natural group. While there are superficial similarities in the
occlusal morphology of the molars of all three genera and Mabokopithecus as well,
these taxa are mostly distinguished from Proconsul by the complexity of their occlusal
1280
D.R. Begun
surfaces rather than being linked by morphological details. In many cases, these types
of molars with more complicated patterns of crests and taller cusps that tend to be
more isolated from one another occur in conjunction with selection for a more
folivorous diet. This may explain in part some of what I consider to be superficial
convergences in the morphology of the teeth of these taxa. In sum, I find the case for a
specific relationship between Mabokopithecus and Nyanzapithecus fairly convincing,
but I would not include Rangwapithecus or Turkanapithecus in the same subfamily.
All of these taxa are most likely to be proconsuloids with more folivorous adaptations
than other proconsuloids. As noted earlier, at this point it is premature to link the
25 Ma Rukwapithecus with the much younger sample of Rangwapithecus.
Early Hominoids
Afropithecus
A number of late Early Miocene and Middle Miocene taxa share characters with
extant Hominoids and are included here in the Hominoidea. Afropithecus (Leakey and
Leakey 1986) is known from several localities in northern Kenya dated to 17–17.5 Ma
(Leakey and Walker 1997). Afropithecus shares an increase in premaxillary
robusticity and length with most extant hominoids (Fig. 3). Like many Late Miocene
and Pliocene hominids, Afropithecus has very thick occlusal enamel as well (Smith
et al. 2003). On the other hand, similarities have been noted between Afropithecus
cranial morphology, particularly the morphology of the midface, and that of
Aegyptopithecus. Leakey and Walker (1997) have suggested that the unusual
primitive-looking face of Afropithecus may be related to a specialized scerocarp
seed predator adaptation. This is functionally consistent with the robust, prognathic
premaxilla; large, relatively horizontal incisors; large but relatively low-crowned
canines; expanded premolars; thick enamel; and powerful chewing muscles of
Afropithecus. A similar set of features is found in modern primate seed predators
such as pithecines. It may be that some of the primitive appearance of the
Afropithecus face is homoplastic with Aegyptopithecus. However, another possibility
is that the unusual morphology of the face of the single specimen of Afropithecus on
which this morphological characterization is based is the result of postmortem
deformation. My observations of the original specimen and other more fragmentary
specimens of Afropithecus lead me to conclude that the type is deformed and probably
resembled Proconsul more closely than Aegyptopithecus. Nevertheless, the characters
noted above related to the development of the premaxilla, the implantation of the
incisors, and the implantation and morphology of the canines are real differences from
Proconsul. Thus, as with Proconsul, Afropithecus has a mosaic of primitive and
derived characters (Leakey et al. 1991; Leakey and Walker 1997; Plate 5).
The large, albeit deformed, type specimen of Afropithecus reveals some information on neurocranial morphology. KNM-WK 16999 preserves a portion of the
braincase immediately behind the orbits. Postorbital constriction is very marked,
though I believe this is the result in part of postmortem deformation. However, there
Fossil Record of Miocene Hominoids
1281
Plate 5 The type specimen
of Afropithecus, KNM-WK
16999 (left) and a well
preserved mandible,
KNM-WK 17012 (right).
Note the lack of bone surfae
around the nasal aperture and
incisors and the exceptionally
large interorbital area,
indicative of deformation
is no doubt that the anterior temporal lines are very strongly developed. These
converge to form a pronounced and very anteriorly situated sagittal crest. The
small portion of the anterior cranial fossa preserved indicates a cerebrum that was
constricted rostrally, lacking the frontal lobe expansion typical of extant and fossil
great apes. The increased robusticity of the masticatory apparatus of Afropithecus in
comparison with Proconsul is undeniable, despite some caveats related to
preservational issues. The large mandibles, robust zygomatics, thickly enameled
teeth, and powerfully developed attachment sites for chewing muscles all indicate
that the dietary adaptations of Afropithecus differed significantly from those of
Proconsul, and more closely approach those of some later Miocene apes. These
differences from Proconsul are confirmed by more recently described specimens
(Rossie and MacLatchy 2013).
Afropithecus is similar in size to Proconsul nyanzae, based on cranial, dental,
and postcranial dimensions (Leakey and Walker 1997). Afropithecus postcrania are
very similar to those of Proconsul, so much so that Rose (1993) found them
essentially indistinguishable. However, Afropithecus postcrania are much less
well known than Proconsul, and it is conceivable that as more fossils of
Afropithecus are discovered, some differences from Proconsul will emerge. Nevertheless, given our current state of knowledge, the postcranial adaptation of
Afropithecus, in terms of body mass and positional behavior, is Proconsul-like,
while the craniodental anatomy is markedly distinct.
Another early hominoid taxon, Heliopithecus, is contemporaneous with
Afropithecus and morphologically very similar, though it is only known from a
fragmentary hemimaxilla and a few isolated teeth (Andrews and Martin 1987).
Both Heliopithecus and Afropithecus share characters that are found next in the fossil
record in Eurasia, which suggests that Heliopithecus and Afropithecus taxa may have
a closer relationship to late Early Miocene and Middle Miocene hominoids from
Europe than do proconsuloids. Certainly the most important piece of the puzzle of
ape evolution to be provided by Heliopithecus is its geography. Heliopithecus is from
the site of Ad Dabtiyah, in Saudi Arabia. While that sounds extraordinary, it is useful
1282
D.R. Begun
to recall that geologically the Saudi Arabian peninsula is part of the African plate, and
until fairly recently much of the fauna of Africa was present in the Arabian peninsula
as well. During the Early Miocene, the Arabian peninsula was much more humid than
today and supported large and diverse forest communities. Given my interpretation
that Afropithecus-like adaptations may have permitted hominoids to disperse into
Eurasia in the late Early Miocene (see below), the presence of a very similar taxon on
the road to Eurasia from East Africa is certainly telling.
Morotopithecus
Morotopithecus is a fossil hominoid from Uganda dated to about 21 Ma by some
and 17 Ma by others (Gebo et al. 1997; Pickford et al. 2003). It is best known from a
large cranial specimen including most of the palate (Pilbeam 1969). For many
years, this specimen was attributed to Proconsul major, but it is clear that it and
other specimens from Moroto are sufficiently different to justify a genus distinct
from Proconsul. Morotopithecus is similar in size to Proconsul major and larger
than Proconsul nyanzae and Afropithecus. It lacks the distinctive subnasal morphology of Afropithecus and has a Proconsul-like premaxilla that is short, gracile,
and does not overlap the palatine process of the maxilla, resulting in a large incisive
fenestration (Fig. 3). Morotopithecus has a broad palate; large anterior teeth,
especially the canines, which are tusklike; a piriform aperture broadest about
midway up; and an interorbital space that appears to be relatively narrow, though
it is damaged. However, the most important distinction of Morotopithecus is the
morphology of the postcrania, which are said to be modern hominoid-like. Newly
described specimens of Morotopithecus include the shoulder joint, hip joint, and
details of the vertebral column (MacLatchy 2004). Walker and Rose (1968)
described the vertebrae as hominoid-like, which has been confirmed by more recent
discoveries and analyses. The glenoid fossa of Morotopithecus suggests a more
mobile shoulder joint as does the morphology of the hip joint. However, it is the
hominoid-like position of the transverse processes of the vertebrae that represents
the strongest evidence for the hominid affinities of Morotopithecus. The roots of the
transverse processes of the lumbar vertebrae of Morotopithecus are positioned
posteriorly, as in extant great apes, suggesting a stiff lower back and an axial
skeleton like that of extant hominoids. However, this interpretation has not gone
unchallenged, and for the time being, I consider the degree to which
Morotopithecus was orthograde to be unresolved (Nakatsukasa 2008).
Eurasian Hominoid Origins
As noted, Heliopithecus and Afropithecus have more robust jaws and teeth than
Early Miocene proconsuloids, and this may represent a key adaptation that permitted the expansion of hominoids into Eurasia at about 17 Ma, when during a marine
low stand, a diversity of terrestrial mammals moved between Africa and Eurasia
Fossil Record of Miocene Hominoids
1283
(Made 1999; Begun 2001, 2009; Begun et al. 2003a, b, 2012; Nargolwalla 2009).
Toward the end of the Early Miocene, the movement of the southern landmasses
northward, combined with a number of other developments (the Alpine and Himalayan orogenies, the earliest appearance of the polar ice caps, and the Asian
monsoons), leads to a sequence of connections and barriers to terrestrial faunal
exchange (Rögl 1999a, b; Adams et al. 1999; MacLeod 1999; Hoorn et al. 2000;
Zhisheng et al. 2001; Guo et al. 2002; Liu and Yin 2002; Wilson et al. 2002;
Nargolwalla 2009). This period of global turbulence affected sea levels between
continents cyclically such that for the remainder of the Miocene, there would be
periodic connections (low stands) and disconnections (high stands) between the
continents. At about 17 Ma, a low stand that had permitted the exchange of
terrestrial faunas between Eurasia and Africa (the Proboscidean datum) was coming
to an end but not before hominoids possibly resembling Afropithecus and
Heliopithecus had dispersed from Africa into Eurasia (Heizmann and Begun
2001; Begun 2002, 2004; Begun et al. 2003a, b, 2012).
At the end of the Early Miocene, about 16.5 Ma, hominoids of more modern
dental aspect first appear in Eurasia. The oldest Eurasian hominoid is
cf. Griphopithecus, known from a molar fragment from Germany (Heizmann and
Begun 2001). Griphopithecus (Abel 1902) is known mainly from large samples
from Turkey of roughly the same age, while the type material is known from a
probably later (14–15 Ma) locality, Děvı́nská Nová Ves, in Slovakia (Heizmann
1992; Andrews et al. 1996; Heizmann and Begun 2001; Begun et al. 2003a, b).
cf. Griphopithecus from Engelswies in Germany is a tooth fragment that has the
more modern features of being thickly enameled with low dentine penetrance (tall
dentine horns did not project into the thick enamel cap as in Proconsul and probably
Afropithecus). cf. is the designation for a taxon that is similar enough to another
taxon for there to be a strong likelihood that they are the same, but with some
formally acknowledged uncertainty. Griphopithecus is better known from over
1,000 specimens, mostly isolated teeth, from two localities in Turkey (Çandır and
Paşalar). One species, Griphopithecus alpani (Tekkaya 1974), is known from both
localities, while a second somewhat more derived taxon is also found at Paşalar
(Alpagut et al. 1990; Martin and Andrews 1993; Kelley and Alpagut 1999; Ward
et al. 1999; Kelley et al. 2000; Kelley 2002; G€uleç and Begun 2003).1
1
Some researchers have suggested that the specimen from Engelsweis, which we all agree is at least
16.5 Ma, if not more than 17 Ma, is more likely to be an Afropithecus or a relative thereof, with no
relationship to Griphopithecus (Casanovas-Vilar et al. 2011). These researchers are in agreement
with Böhme et al. (2011) that Griphopithecus in Anatolia is later in time (ca. 13.5 Ma). My analysis
of the biostratigraphy of the Çandır locality indicates that it is likely to be at least 16 Ma (Begun
et al. 2003a). Until more research is concluded, there will remain uncertainty about the ages of the
Çandır and Paşalar localities, though at 13.5 Myr this makes them much younger than previously
thought. However, even if the Anatolian Griphopithecus sites are 3 Myr younger than Engelsweis,
that is no justification for the claim that the latter must have been the result of a separate dispersal
event as opposed to the simpler scenario in which hominoids with thickly enameled teeth enter
Europe at 17 Ma and evolve in situ. As noted earlier, the tooth from Engelsweis more closely
resembles those from Anatolia and Slovakia than it resembles Afropithecus.
1284
D.R. Begun
Plate 6 Top row,
Nacholapithecus palate. Left,
lateral view, right, palatal
view. Bottom row,
Nacholapithecus mandible
(left), Equatorius mandible
(right). The Nacholapithecus
specimens belong to the
partial skeleton KNM-BG
35250, and the Equatorius
mandible to the partial
skeleton KNM-TH 28860
Griphopithecus alpani has a robust mandible with strongly reinforced symphysis; broad, flat molars with thick enamel; and reduced cingulum development
compared with Proconsul. It retains primitive tooth proportions (small M1 relative
to M2), anterior tooth morphology, and postcanine occlusal outline shape. A few
fragments of the maxilla from Paşalar indicate a primitive morphology for the
anterior palate (Martin and Andrews 1993). The morphology of Griphopithecus
molars as well as their microwear indicates a diet allowing the exploitation of hard
or tough fruits, though it is not clear if this means simply that they could exploit
these resources when needed (a keystone resource) or if they were a favored source
of food. Two postcranial specimens, a humeral shaft and most of an ulna, from the
younger site of Klein-Hadersdorf, Austria, are also similar to Proconsul and
indicate that Griphopithecus was a large-bodied above-branch arboreal quadruped
similar in size and positional behavior to Proconsul nyanzae (Begun 1992a).
Phalanges from Paşalar are also said to be most similar to those of Proconsul and
extant arboreal quadrupeds (Ersoy et al. 2008) (Plates 6 and 7).
East African Middle Miocene Thick-Enameled Hominoids
Shortly after the appearance of Griphopithecus in western Eurasia (but see footnote 1),
dispersals between Eurasia and Africa were interrupted by the Langhian transgression
(Rögl 1999a). Following the Langhian, at about 15 Ma, dispersals resumed in
a number of mammal lineages, probably also including hominoids (Begun
et al. 2003a, b; Begun 2009; Nargolwalla 2009; Begun et al. 2012). Hominoids closely
similar to Griphopithecus in dental morphology appear in Kenya at this time.
Equatorius is known from 15 Ma localities in the Tugen Hills and at Maboko, both
in Kenya. This taxon, previously attributed to Kenyapithecus, is very similar
to Griphopithecus but has a distinctive incisor morphology and reduced cingula,
Fossil Record of Miocene Hominoids
1285
Plate 7 Kenyapithecus and Griphopithecus. Top row, Kenyapithecus wickeri (type specimen,
KNM-FT 46), lateral (left) and occlusal (center) views. Equatorius (type specimen, M16649)
occlusal (right). Bottom row, Griphopithecus alpani type mandible (MTA 2253) (left) and three
upper central incisors, from left to right, “Proconsul” (KNM-RU 1681), Equatorius (KNM-MB
104) and Kenyapithecus wickeri (KNM-FT 49)
probably warranting a distinct genus status (Ward et al. 1999; Kelley et al. 2000; Ward
and Duren 2002; contra Begun 2000, 2002; Benefit and McCrossin 2000). Equatorius
is also known from a good sample of postcrania, including most of the bones of the
forelimb, vertebral column, hindlimb long bones, and a few pedal elements
(McCrossin 1997; Ward and Duren 2002). Like Griphopithecus, which is much less
well known postcranially, Equatorius is similar to Proconsul nyanzae in postcranial
size and morphology.
Nacholapithecus (Ishida et al. 1999) is known from deposits of the same age as
Equatorius in the Samburu Basin of Kenya (Nakatsukasa et al. 1998). Like
Equatorius, Nacholapithecus is known from a relatively complete skeleton, more
complete in fact than the best specimen of Equatorius. From this exceptional
skeleton, we know that Nacholapithecus is similar to other Middle Miocene
hominoids in most aspects of the jaws and teeth but unique in aspects of limb
morphology. While they are not especially elongated, the forelimbs of
Nacholapithecus are more robust, that is, they are more strongly built, than are
the hindlimbs. In a fascinating comparison, Ishida et al. (2004) show that
Nacholapithecus has forelimb joints the size of a chimpanzee but hindlimb joints
closer in size to those of a baboon, of much smaller body mass. The forelimbs were
not elongated as in modern apes, but they were enlarged. This is difficult to
understand, but it probably has something to do with some increase in the degree
to which Nacholapithecus was loading its forelimbs relative to its hindlimbs, even
if it was not suspensory. Once again, we have a weird, unique fossil ape without a
modern counterpart. Kunimatsu et al. (2004) provide evidence that the anterior
portion of the palate of Nacholapithecus is more hominid-like in its length and
degree of overlap with the palatine process of the maxilla (Fig. 3). This morphology
1286
D.R. Begun
is the principal evidence for the hominoid status of this species. However, in its
details, the anterior palate of Nacholapithecus is unlike that of hominids (see
below). In my opinion, there is also evidence of some postmortem compression
that may contribute to the impression that the anterior portion of the palate of
Nacholapithecus is more modern looking than it actually was.
Otherwise, the postcranial skeleton of Nacholapithecus is similar to other
Middle Miocene hominoids in having the general signature of a generalized,
palmigrade, arboreal quadruped, but differs from Equatorius, also known from
fore and hindlimb, in the enlarged size and robusticity of its forelimb. While not
like extant nonhuman hominoids in forelimb length relative to the hindlimb,
Nacholapithecus forelimbs are large and powerful, indicating a form of positional
behavior emphasizing powerful forelimb grasping (Ishida et al. 2004). Interestingly, several wrist bones are well preserved in both Nacholapithecus and
Equatorius, and they are quite similar to each other and to Proconsul and
Afropithecus (personal observations).
Kenyapithecus (Leakey 1962) is the most derived of the Middle Miocene
African hominoids, and may be the earliest hominid (Table 2), although I should
add that it is the least well known. Kenyapithecus is known only from a small
sample from Fort Ternan in Kenya, though a second species may be present in
Turkey (see below). Like other Middle Miocene hominoids, Kenyapithecus has
large flat molars with broad cusps and thick enamel. The maxilla of Kenyapithecus,
however, is derived in having a high root of the zygomatic, a probable hominid
synapomorphy. While McCrossin and Benefit (1997) believe that Equatorius and
Kenyapithecus represent a single species, most researchers have concluded that two
genera are present and that Kenyapithecus is derived relative to Equatorius
(Harrison 1992; Ward et al. 1999), and that is the view adopted here. As noted, it
has been suggested that Kenyapithecus is also present at Paşalar. If so, and if
Kenyapithecus is indeed an early hominid, this would date the origin of the hominid
family to at least 16 Ma (but see footnote 1). However, there is a roughly 3 Ma gap
between possible Kenyapithecus at Paşalar and the type material from Fort Ternan.
One last Middle Miocene hominoid deserves mention here. Otavipithecus is the
only Miocene hominoid known from southern Africa, from the 13 Ma site of Berg
Aukas in Namibia (Conroy et al. 1992). Several specimens have been described,
including the type mandible, a frontal fragment, and a few postcrania (Conroy
et al. 1992; Pickford et al. 1997; Senut and Gommery 1997). It has been suggested
that Otavipithecus has affinities to hominids (Conroy et al. 1992; Ward and Duren
2002), but it preserves primitive proconsuloid characters such as a small M1
compared to M2, a long M3, parallel tooth rows, a small space for the mandibular
incisors, low P4 talonid, and tall, centralized molar cusps (Begun 1994b). Singleton
(2000) carried out the most comprehensive analysis of Otavipithecus and concluded
that it may be related to Afropithecus, which is broadly consistent with the placement of the taxon in Fig. 2. Like Heliopithecus, the most informative piece of
information from the sample of Otavipithecus comes from its biogeography.
Otavipithecus is a huge geographic outlier, suggesting that hominoids were widespread in equatorial and southern Africa but have yet to be found. Otavipithecus is
Fossil Record of Miocene Hominoids
1287
morphologically somewhat atypical of Early and Middle Miocene hominoids, and I
expect that when other taxa are found between Kenya and Namibia or elsewhere in
Africa, they will be equally surprising.
Summary of Middle Miocene Hominoid Evolution
The radiation of Middle Miocene hominoids in Africa was relatively short-lived
and less diverse than the Early Miocene radiation (see Table 1). Having apparently
dispersed from Eurasia by about 15 Ma, they are mostly extinct by 12.5–13
Ma. Aside from a few fragmentary specimens that most likely represent the end
of the Proconsul lineage (Hill and Ward 1988), hominoids would not appear again
in Africa until the Late Miocene. Given the rarity of hominoid localities in the early
Middle Miocene, the biogeographic hypothesis of the dispersal of Middle Miocene
hominoids presented here is debatable. It is certainly possible, for example, that
Early Miocene Griphopithecus-like fossils will be found in Africa that will show
that Equatorius, Nacholapithecus, and Kenyapithecus all evolved in situ in Africa
and that apparently earlier fossils from Eurasia are either misdated or are early
offshoots of this clade with no direct relationship to later hominids (Ward and
Duren 2002). In the end, perhaps the best way to think about Middle Miocene
hominoids is in terms of a group of closely related genera that occupied the circumMediterranean region and the contiguous regions north into Germany and south into
Kenya (with one known long distance dispersal into Namibia). Movements within
the geographic area of these taxa were probably very complex and numerous over
time, but from this melting pot of Middle Miocene thickly enameled hominoids, the
first true hominids appear.
Early Hominids
While Kenyapithecus shares a synapomorphy with the Hominidae (position of the
zygomatic root), the first clear-cut hominids are known from Eurasia and share
numerous cranial, dental, and postcranial synapomorphies with living hominids.
This is the most important body of data supporting the Eurasian origins hypothesis.
If that hypothesis is incorrect, we need to account for the absence of fossil hominids
in Africa (which could just be bad luck) and also the presence of apparent hominid
synapomorphies in both the Asian and European hominid fossil records.
The extant Hominidae is divided into two subfamilies, Ponginae and Homininae,
and the earliest representatives of both subfamilies are roughly contemporaneous.
The earliest hominines are represented by Dryopithecus and possibly
Pierolapithecus and Anoiapithecus (see below). Much better known and with
clearer hominine synapomorphies are Rudapithecus, Hispanopithecus, and
Ouranopithecus (see chapter “▶ Potential Hominoid Ancestors for Hominidae,”
Vol. 3). The earliest pongines are represented by Ankarapithecus, Sivapithecus, and
relatives. Miocene hominines are known from western Eurasia, while Miocene
1288
D.R. Begun
pongines are known from South and East Asia, reflecting the basic biogeographic
division of the two hominid subfamilies today [but see Kelley and Gao (2012)].
Fossil Pongines
The oldest sample of fossils widely interpreted as pongine is of Sivapithecus from
the middle Chinji formation in the Siwaliks of Pakistan (Raza et al. 1983; Rose
1984, 1989; Kappelman et al. 1991; Barry et al. 2002). Specimens referred
Sivapithecus indicus that are known to come from the middle Chinji formation
share characters with later Sivapithecus and other hominids including reduced or
absent molar cingula; relatively large M1; reduced premolar cusp heteromorphy;
long, buccolingually compressed canines; broad-based nasal aperture; elongated
and robust premaxilla partly overlapping the maxilla; and, as in Kenyapithecus, a
high position to the zygomatic root. They share specifically with later Sivapithecus
fewer clear-cut characters, such as probably strongly heteromorphic upper incisors
(known only from the roots), and broad, flat cusped molars with thick enamel,
though these characters are also found in most other Middle and many Late
Miocene hominoids. One specimen of Chinji Sivapithecus, GSP 16075, represents
a portion of the palate with the connection between the maxilla and premaxilla
partially preserved. The maxillary-premaxillary relationship is highly diagnostic of
Sivapithecus and the pongine clade, and the morphology of the Chinji specimen has
been interpreted to share characters of this complex (Raza et al. 1983; Ward 1997b;
Kelley 2002). However, while the specimen does have a relatively elongated,
horizontal, and robust premaxilla, the area of the incisive fossa and foramen is
not preserved. In the absence of this region, it is difficult to distinguish Chinji
Sivapithecus from later Sivapithecus, including later Sivapithecus indicus, to which
it is assigned, versus another pongine, Ankarapithecus. Ankarapithecus preserves a
morphology of the anterior palate that lacks the synapomorphies of Sivapithecus
and Pongo (Begun and G€uleç 1998), and this may also be the case for the Chinji
jaw. Resolution of this uncertainty would help to clarify the biogeography of
pongine origins (see below).
Sivapithecus
Sivapithecus Craniodental Evidence
Most of the Sivapithecus samples, including the best-known specimens with the
clearest evidence of pongine affinities, are from younger localities of the Siwaliks
of India and Pakistan, dated between 10.5 and 7.5 Ma (Barry et al. 2002). In the
following section, I discuss Sivapithecus in some detail because it is in many ways
critical to understanding Late Miocene hominoid evolution. Three species are
generally recognized in this sample, the best known of which is Sivapithecus
sivalensis (Lydekker 1879), from localities ranging in age from 9.5 to 8.5 Ma
(Kelley 2002). In addition to the characters outlined above, Sivapithecus sivalensis
Fossil Record of Miocene Hominoids
1289
Plate 8 GSP 15000, the best
preserved specimen of
Sivapithecus. To the right is a
lateral view of the face
without the mandible
(Courtesy of Milford
Wolpoff)
is known from a suite of cranial characters strongly indicative of pongine affinities
(Pilbeam 1982). These include unfused tympanic and articular portions of the
temporal bone; a posterosuperiorly directed zygomatic arch with deep temporal
and zygomatic processes; vertically oriented frontal squama; supraorbital costae or
rims; a narrow interorbital space; elongated nasal bones; tall, narrow orbits; wide,
anteriorly oriented zygoma; narrow, pear-shaped nasal aperture; externally rotated
canines; long, horizontally oriented nasoalveolar clivus that is curved along its
length but flat transversely; and a subnasal region with the posterior pole of the
premaxilla merging into the anterior edge of the maxillary palating process to form
a flat, nearly continuous subnasal floor (Fig. 3) and a strongly concave facial profile
from glabella to the base of the nasal aperture. Sivapithecus is also likely to have
been airorhynchous (having a dorsally deflected face), as in Pongo (Fig. 4). All of
these and other characters are described in more detail in Ward and Pilbeam (1983),
Ward and Kimbel (1983), Ward and Brown (1986), Brown and Ward (1988), and
Ward (1997b). Sivapithecus sivalensis is not identical to Pongo in cranial morphology, however, even if the similarities are striking and detailed. Sivapithecus
sivalensis is more robust than similarly sized (female) Pongo in features related
to the masticatory apparatus, including aspects of the zygomatic and temporal
bones, maxillary robusticity, and molar morphology. The molars in particular are
easily distinguished from those of Pongo in having thicker enamel and in lacking
the complex pattern of crenulations seen in unworn Pongo molars. However,
overall the number of derived characters shared with Pongo is impressive (Ward
1997; Kelley 2002) (Plates 8, 9, and 10).
Sivapithecus indicus (Pilgrim 1910) is the oldest species, and if the middle
Chinji fossils are included, it would range from 12.5 to 10.5 Ma (Kelley 2002). It
is the smallest species, at least in terms of dental size, and appears to have a slightly
shorter nasoalveolar clivus or premaxilla compared with Sivapithecus sivalensis
(see above). Sivapithecus parvada (Kelley 1988) is considerably larger than the
other species and is known from the Nagri formation locality Y311, about 10 Ma.
Sivapithecus parvada males are about the dental size of female gorillas. The upper
central incisors are especially long mesiodistally, the M3 is larger than the M2, the
premolars are relatively large, and the symphysis of the mandible is very deep
(Kelley 2002).
1290
D.R. Begun
Plate 9 Sivapithecus
palates. GSP 15000 to the left
and YPM 13799 (formerly
Ramapithecus) to the right
(Courtesy of Milford
Wolpoff)
Plate 10 Sivapithecus mandibles, showing substantial diversity in size and morphology. The two
specimens to the left courtesy of Milford Wolpoff. From left to right, GSP 15000, GSP 9564,
M. 15423
Sivapithecus Postcrania
Sivapithecus postcrania have been described in many publications (Pilbeam et al.
1980, 1990; Rose 1984, 1986, 1989; Spoor et al. 1991; Richmond and Whalen 2001;
Madar et al. 2002). They combine a mixture of characters, some suggesting more
palmigrade postures and others suggestive of more suspensory positional behavior
(see chapter “▶ Postcranial and Locomotor Adaptations of Hominoids,” Vol. 2).
Fossil Record of Miocene Hominoids
1291
This has been interpreted by some to indicate that Sivapithecus is more primitive
than any living hominoids, all of which, even humans, share numerous characters of
the shoulder and forelimbs related to suspensory behavior or an ancestry of suspensory behavior (Pilbeam 1996, 1997; Pilbeam and Young 2001, 2004). This view,
also shared by McCrossin and Benefit (1997), has dramatic implications for the
interpretation of the hominoid fossil record. All Late Miocene hominoids, including
Sivapithecus, share many characters of the cranium and dentition with living
hominoids. If Sivapithecus is more primitive than extant hominoids, given its
apparently primitive postcrania, then all the apparently derived hominid features
of Sivapithecus would have evolved in parallel in Sivapithecus, and as these authors
suggest, by extension in all Late Miocene hominoids (Oreopithecus, Dryopithecus,
Rudapithecus, Ouranopithecus, Lufengpithecus, etc.). These parallelisms include
not only craniodental morphology but also details of life history and, as it turns
out, many postcranial characters as well. In fact, the apparently primitive characters
of Sivapithecus postcrania are small in number compared with the large number of
clearly derived hominid characters from throughout the skeleton and known biology
of all Late Miocene hominids. Rather than rejecting the hominid status of
Sivapithecus and other Late Miocene hominids because not all of their postcranial
morphology is strictly hominid or even extant hominoid-like, it is much more likely
that these few characters reflect mosaic evolution of the hominid skeleton, uniquely
derived features of the anatomy of Sivapithecus, as well as some parallelism in
extant hominoids (Begun 1993; Begun et al. 1997; Begun and Kivell 2011;
see below).
Sivapithecus postcrania, though they have been the subject of more discussion
related to phylogeny, are actually less well known than those of Proconsul,
Equatorius, or Nacholapithecus. The following is summarized mainly from Rose
(1997), Richmond and Whalen (2001), and Madar et al. (2002). Much more
information is available from all the references cited earlier. Two species of
Sivapithecus are known from the humerus, which is unlike that of modern hominoids in the curvature of the shaft and the development of the deltopectoral plane.
The bicipital groove is also broad and flat and suggests a posteriorly oriented
humeral head, as in the Early and Middle Miocene Hominidea described earlier.
However, the humerus has such an unusual morphology that the orientation of the
head, which is already somewhat difficult to predict from bicipital groove position
(Larson 1996), cannot be reconstructed with great confidence. Nevertheless, the
morphology of the proximal humerus in Sivapithecus is suggestive of some form of
pronograde quadrupedalism as seen, for example, in extant cercopithecoids. If the
humeral head were oriented more posteriorly, it would also be consistent with a
scapula that is placed on the side of a compressed rib cage, as in typical mammalian
quadrupeds, and unlike extant hominoids (Rose 1989; Ward 1997a). No direct
evidence is available for the thorax or any part of the axial skeleton of Sivapithecus,
however, so this will also have to await further discoveries. The deltopectoral plane
and the curvature of the shaft of the humeri in Sivapithecus are quite strongly
developed compared with most cercopithecoids and indicate in my view a unique
form of positional behavior that is neither extant hominoid nor extant
1292
D.R. Begun
cercopithecoid-like (Madar, et al. 2002). The distal end of the humerus is in the
main hominoid-like, including a well-developed trochlea separated from the capitulum by a deep, well-defined groove (the zona conoidea), though in a few details of
the posterior surface, there are similarities to Proconsul and Kenyapithecus (Rose
1997). Overall, however, the functional morphology of the elbow of Sivapithecus is
most like the hominoid elbow in its ability to resist movements other than flexion
and extension at the elbow joint, a hallmark of the Hominoidea (Rose 1988).
The Sivapithecus forearm is poorly known, especially the proximal portions of the
ulna and radius, which would help to more fully understand the Sivapithecus elbow.
A juvenile radial shaft is known that is described as Proconsul-like, though as a
juvenile, it is not clear to what extent we might expect any hominoid-like characters,
such as curvature and the nature of the ligamentous/muscular insertions, would be
expressed. On the other hand, the few carpal bones that are known show a mixture of
hominoid and non-hominoid features. The capitate of Sivapithecus has a somewhat
expanded and rounded head, as in great apes, but overall is transversely narrow and
elongated proximodistally compared with great apes. The joint surface for the third
metacarpal is irregular as in great apes. The hamate is similar in length/breadth
proportions and has a less strongly projecting hammulus than do great ape hamates
(Spoor et al. 1991). The joint on the hamate for the triquetrum is oriented as in
gorillas and also most other non-hominoid anthropoids, and its shape suggests a
stabilizing function at the wrist, which differs fundamentally from the typical mobility of the ulnar side of the wrist in extant hominoids. The proximal end of a first
metacarpal is similar in morphology to hominids and Early Miocene Hominidea in
being saddle-shaped, a configuration considered to represent a good compromise
between mobility and stability in a wide variety of positions. The manual phalanges
are long and curved, with strongly developed ridges for the flexor muscles and their
sheaths. One complete phalanx has a relatively deep and somewhat dorsally positioned articular surface for the metacarpal head, which is more typical of palmigrade
quadrupeds. However, it is not completely clear if this is from a hand or a foot, and if
the latter is the case, a similar morphology exists in some hominoids as well.
Begun and Kivell (2011) undertook a reanalysis of the carpal bone of Sivapithecus
in light of recent discoveries of carpal bones of Rudapithecus (see below). They
concluded that there are a number of terrestrial and even knuckle-walking characteristics of the capitate and hamate of Sivapithecus, though the capitate and hamate of
Sivapithecus are nevertheless easily distinguished from those of African apes. The
authors suggest that if the Sivapithecus species to which these carpals belong
(S. sivalensis for the capitate and S. parvada for the hamate) did knuckle-walk,
they did so in a manner that was biomechanically different from extant African
apes (see chapters “▶ The Hunting Behavior and Carnivory of Wild Chimpanzees,”
Vol. 2, “▶ Great Ape Social Systems,” Vol. 2 and “▶ Origin of Bipedal
Locomotion,” Vol. 3). It is worth remembering of course that African apes today
are biomechanically distinct from one another in their knuckle-walking.
Whatever this means in terms of the big picture of hominoid evolution is unclear,
but one mystery that is potentially solved by this analysis is the biogeography of the
Miocene pongines (see below).
Fossil Record of Miocene Hominoids
1293
The hindlimb of Sivapithecus is less well known but generally more similar to
extant hominoids than the forelimb. The femur is known from proximal and distal
ends but not from the same individual (Rose 1986; Madar et al. 2002). The hip joint
as represented by the femoral head and neck was mobile in many directions, though
it has a well-developed fovea capitis, unlike Pongo, which is highly distinctive (but
not unique) in lacking a ligamentum teres of the femur and thus its attachment site
to the femur, the fovea capitis. The distal end of the femur preserves evidence of a
knee joint that is consistent with this interpretation, implying a knee joint loaded in
positions away from the sagittal plane. The knee also has a number of features
allowing for rotation of the leg and foot to adjust the lower extremity to a variety of
positions close to and further away from the center of mass (Madar et al. 2002). In
all of these features, the femur is more like that of hominoids than other
anthropoids.
Other hindlimb elements include several tarsal bones, phalanges, and a wellpreserved hallucial skeleton (Conroy and Rose 1983; Rose 1984, 1986, 1994). The
tarsals are perhaps more like those of great apes than any other part of the
postcranium of Sivapithecus (Rose 1984; Madar et al. 2002), indicating the presence of a broad foot, able to assume many positions but stable in all of them, and
supportive of body mass loading from many directions. The hallux or big toe is
strikingly robust, much more so than in Pongo, and indicates a strongly developed
grasping capability in the foot. The phalanges are also by and large hominoid-like,
with well-developed features related to powerful flexion of the toes, a critical
function in antipronograde activities (climbing as well as suspension).
Sivapithecus Phylogeny and Paleobiology
Overall, the morphology of Sivapithecus strongly supports a close phylogenetic
relationship to Pongo but an adaptation that differed from Pongo in important
aspects. Microwear suggests that Sivapithecus had a diet that was similar to that
of chimpanzees, while gnathic morphology suggests more of a hard-object diet
(Teaford and Walker 1984; Kay and Ungar 1997; chapter “▶ Dental Adaptations of
African Apes,” Vol. 2). Perhaps this reflects a capacity to exploit fallback or
“keystone” resources in times of scarcity. Most hominoids are known to practice
this strategy (Tutin and Fernandez 1993; Tutin et al. 1997). The case of gorillas may
be most relevant to the question of the diet of Sivapithecus. Most gorillas have diets
similar to chimpanzees but are able to exploit terrestrial herbaceous vegetation
(THV) in lean seasons when soft fruit is less available or in contexts in which they
are sympatric with chimpanzees (Tutin and Fernandez 1993; Tutin et al. 1997). The
microwear results may reflect the preferred and most common components of the
diet, while the morphology of the jaws and teeth may reflect a critical adaptation to
a keystone resource on which survival would depend during stressful periods
(see chapters “▶ Role of Environmental Stimuli in Hominid Origins,” Vol. 3 and
“▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments,” Vol. 1).
Postcranial evidence clearly indicates that Sivapithecus was not orang-like in its
positional behavior. In fact, it was unique; there are probably no living analogues.
Sivapithecus combines clear indications of pronograde forelimb postures and a
1294
D.R. Begun
palmigrade hand position with more antipronograde activities such as vertical
climbing and clambering implied by elbow joint stability over a wide range of
flexion/extension, powerful grasping hands and feet, an especially powerful hallux,
and hindlimbs capable of wider ranges of joint excursions than in extant pronograde
quadrupeds (Madar et al. 2002). It is difficult to imagine exactly what the positional
behavior of Sivapithecus might have been like.
One constant in the postcranial functional morphology of Sivapithecus is
arboreality. Perhaps Sivapithecus used its powerful limbs in climbing and bridging
or clambering activities, spreading the limbs across multiple supports to access
smaller branches. In a sense, it is orang-like without the suspension. While
Sivapithecus managed to distribute its considerable body mass across the tops of
several branches, orangs do the same but from below. In large animals, the
advantage to suspension is added stability on horizontal supports, since they
otherwise need to generate very high levels of torque to stay atop a branch
(Grand 1972, 1978; Cartmill 1985). Orang males are larger than Sivapithecus and
may be beyond the threshold where pronograde limb postures are possible in the
trees. The fact that the proximal half of the humerus of Sivapithecus, while similar
to that of a pronograde quadruped, is exceptionally robust, with extremely welldeveloped shoulder muscle attachments, may be an indication of a unique approach
to this problem.
Sivapithecus does share numerous postcranial features, especially of the elbow
and hindlimb, with extant hominoids and Dryopithecus. It is therefore possible that
the more monkey-like morphology of the proximal humerus and portions of the
hands and feet are actually homoplasies with cercopithecoids caused by the adoption of more pronograde postures in a hominoid that evolved from a more suspensory ancestor (Begun et al. 1997). This requires many fewer homoplasies than the
alternative hypothesis that all extant hominoid characters in all Late Miocene
hominoids are homoplasies (Pilbeam 1996, 1997; McCrossin and Benefit 1997;
Pilbeam and Young 2001, 2004). There is some evidence from the functional
morphology of Sivapithecus to support the hypothesis that its form of pronograde
arboreal quadrupedalism is actually superimposed on a suspensory hominoid
groundplan (see chapter “▶ Origin of Bipedal Locomotion,” Vol. 3).
The problem of angular momentum causing instability in a large mammal
standing on top of a branch is alleviated in part by spreading the limbs apart on a
wide support, or across several supports, which Sivapithecus seems to have been
capable of doing (Madar et al. 2002). It can also be all alleviated by placing the
center of mass closer to the support, which is suggested for Griphopithecus (Begun
1992a), and may have also occurred in Sivapithecus, as a consequence of its
habitually more laterally placed limbs (Madar et al. 2002). The positioning of the
limbs more laterally in hominoids is part of the suite of characters related to trunk
morphology and scapular position. It is not facilitated by monkey-like trunks and
scapular positions, which promote more parasagittal limb movements. Finally, an
important response to angular momentum is to increase the torque generated by the
limbs on the support, to prevent excessive excursions from a balanced position,
especially when a single support of only modest size is used, again suggested to be
Fossil Record of Miocene Hominoids
1295
an aspect of the positional behavior of Sivapithecus (Madar et al. 2002). Higher
torque results from more powerful gripping, also characteristic of Sivapithecus
(Madar et al. 2002), and may have been boosted by especially powerfully developed shoulder joint adduction and medial rotation, particularly if the shoulder is in a
relatively abducted position to begin with, as in hominoids.
The morphology of the proximal half of the humerus in Sivapithecus is consistent with very powerful adduction and medial rotation by deltoideus and pectoralis
major. These muscles left extremely prominent scars on the humerus of
Sivapithecus. If the arm of Sivapithecus were positioned as in extant hominoids,
laterally on a posteriorly positioned scapula, the adduction and medial rotation
capacities of deltoideus and pectoralis would be increased by increasing the relative
mass of the clavicular portion of deltoideus, which is unknown in Sivapithecus.
However, in addition to the need for powerful muscles, which existed in
Sivapithecus, these functions would also be enhanced by other attributes known
in Sivapithecus. The extension of the muscles along the shaft distally and the
possible decreased humeral neck torsion would increase the moment arm for
these muscles in adduction and reposition the insertions of these muscles medially,
possibly to make more of the deltoideus available for adduction and medial
rotation. The strong mediolateral curvature of the shaft may result from high
mediolateral bending stresses that would result from very powerful shoulder
adduction on a fixed limb. The proximal shaft is also very broad mediolaterally,
suggestive of strong mediolaterally directed stresses. While speculative, it is certainly conceivable that the upper part of the forelimb of Sivapithecus was less
monkey-like than generally perceived and may not imply that much of the trunk
was of the primitive anthropoid type. A small number of autapomorphies of the
shoulder of Sivapithecus may have allowed this taxon to practice a relatively
efficient form of arboreal pronograde quadrupedalism while maintaining the capacity for many of the antipronograde activities of hominoids, though probably not for
frequent upper limb below-branch suspension. This hypothesis is functionally
consistent with the morphology of the Sivapithecus postcranium in general and is
certainly more parsimonious than the hypothesis that would interpret all Late
Miocene hominoid characters as homoplasies (Begun and Kivell 2011).
Ankarapithecus
Aside from some material from Nepal attributed to Sivapithecus (Munthe
et al. 1983), Sivapithecus is known only from India and Pakistan. Specimens
from central Anatolia, Turkey, once attributed to Sivapithecus (Andrews and
Tekkaya 1980) are now assigned to Ankarapithecus, following the original conclusions of Ozansoy (1957, 1965). Ankarapithecus meteai is known from a male palate
and mandible from two different individuals and a female partial skull (mandible
and face) from a third locality, all close to each other in location and geological time
(Kappelman et al. 2003). Begun and G€uleç (1995, 1998) resurrected the nomen
Ankarapithecus based mainly on the morphology of the premaxilla and the
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D.R. Begun
Plate 11 Ankarapithecus
(MTA 2125)
relationship between this bone and the maxilla but concluded that Ankarapithecus
is nonetheless in the pongine clade. Alpagut et al. (1996) and Kappelman
et al. (2003) described newer and much more complete fossils of Ankarapithecus
and concluded that it is a stem hominid (sharing a common ancestor with both
pongines and hominines). The new fossils discovered and described by these
authors include the region around the orbits, which lacks some of the characters
of Sivapithecus. The interorbital region is intermediate in breadth between Pongo,
with the narrowest interorbitals, and African apes and the orbits themselves are
broad rather than tall and narrow. Alpagut et al. (1996) and Kappelman et al. (2003)
also interpret the supraorbital region as a supraorbital torus, characteristic of
African apes and humans and some European Late Miocene taxa, and they interpret
a frontal sinus in the cranium of Ankarapithecus as a frontoethmoidal sinus. These
authors see the mixture of hominine and pongine characters as an indication that
Ankarapithecus precedes their divergence (Plate 11).
Craniodental Evidence
The frontal sinuses in Ankarapithecus appear to be confined to the frontal squama and
do not invade the frontal supraorbital region from a broad expansion of the ethmoidal
sinuses. They are positioned and developed as in extant taxa with frontal
pneumatizations derived either from the sphenoidal or maxillary sinuses and are
unlike those derived from the ethmoid (see above discussion). The frontal
pneumatization in Ankarapithecus is unlikely to be a frontoethmoid sinus and thus
is not a synapomorphy of the hominines. The supraorbital region, while robust, is
morphologically similar to the robust supraorbital costae of large orangs or Cebus and
also unlike the bar-like supraorbital tori of African apes. Thus, the supraorbital region
of the Ankarapithecus cranium is more pongine than hominine-like and, like the
maxilla, probably represents the primitive morphology for the pongines (see below).
In Ankarapithecus, the premaxilla, the portion of the palate with the alveoli for
the incisors and the mesial half of the canines, is unlike that of Sivapithecus and
more like that of African apes. The premaxilla is long, but it does not overlap the
Fossil Record of Miocene Hominoids
1297
palatine process of the maxilla to fill the incisive fossa to the degree seen in
Sivapithecus. Instead, the subnasal fossa is stepped (there is a drop between the
base of the nasal aperture and the floor of the nasal cavity) into an incisive fossa that
is most like that of some chimpanzees, a relatively large depression opening into a
canal (the incisive canal that runs between the premaxilla and maxilla to exit on the
palatal side via the incisive foramen). Rudapithecus has a similar configuration of
the subnasal fossa, incisive canal, and incisive foramen, though the fossa is larger
and the canal is shorter in length and larger in caliber, as in some gorillas (Begun
1994a; Fig. 3). The premaxilla of Ankarapithecus is curved or convex anteroposteriorly as in Sivapithecus, African apes, and Rudapithecus, but it is also convex
transversely, as in African apes and Rudapithecus unlike Sivapithecus, which has a
transversely flatter premaxilla. In all of these features, Ankarapithecus expresses a
condition intermediate between pongines and hominines, which I consider primitive for the pongines (Begun and G€uleç 1998). Alpagut et al. (1996) and Kappelman
et al. (2003) have suggested that these characters indicate that Ankarapithecus
precedes the divergence of pongines and hominines and is thus a stem hominid.
Other features of the morphology of Ankarapithecus resemble pongines more
clearly, including canine implantation, zygoma size and orientation, orbital margin
morphology, nasal length, and dental morphology. Overall, Ankarapithecus most
closely resembles Sivapithecus and Pongo but retains a more primitive palatal
morphology that suggests it is at the base of the pongine clade.
Postcranial Evidence
Some postcrania of Ankarapithecus are known, including a well-preserved radius
and two phalanges (Kappelman et al. 2003). A femur tentatively identified as
primate is more likely in my opinion to be from a carnivore. The radius shares
characters with extant great apes including features of the radial head and a
comparatively long radial neck (Kappelman et al. 2003). Other hominoid-like
features described or figured in Kappelman et al. (2003) but not identified as
hominoid-like by these authors include a proximodistally compressed and more
circular radial head, a deep radial fovea, flat as opposed to concave shaft surface
along the anterior surface, a more distal origin of the interrosseous crest, and a
smooth distal dorsal surface. The specimen actually strikes me as quite hominoidlike with a few features more normally associated with large non-hominoid anthropoids, a pattern more or less in keeping with other Late Miocene hominoids. The
phalanges are said to be relatively straight and thus non-hominoid-like, but only
distal portions are preserved. They too strike me as more hominoid-like than
Kappelman et al. (2003) suggest, given its distal shaft robusticity, dorsopalmar
compression, and distopalmarly projected condyles. The curvature and ridges for
the flexor musculature are said to be poorly developed compared with hominoids,
but this may be related to many factors (preservation, age, digit attribution).
Overall, Ankarapithecus is characterized by many features found in other
pongines and is probably the most basal known member of that clade. Like
Sivapithecus, it was much more massive in the development of its masticatory
apparatus than Pongo, and its postcranium, though very poorly known, suggests
1298
D.R. Begun
arboreality and at least some features of hominoid-like antipronograde positional
behaviors, but probably lacking the degree of suspension seen in dryopithecins,
Oreopithecus, and extant hominoids (but see Kappelman et al. 2003).
Other Probable Fossil Pongines
Indopithecus-Gigantopithecus
Extremely large fossil hominoids, larger than any extant primate, have been known
from Asia since the early part of the twentieth century. Gigantopithecus blacki (von
Koenigswald 1935) is a Pleistocene taxon known from numerous isolated teeth and
a few mandibles. It is recent enough to be outside the purview of this review and has
been described many times elsewhere. Sivapithecus giganteus (Pilgrim 1915) is the
oldest nomen attributed to samples from the Late Miocene of South Asia that may
be related to Gigantopithecus. This sample, only known from a lower M3 from the
Late Miocene of the Siwaliks, is mainly distinguished from Sivapithecus by size.
When a mandible with teeth of similar size was found, a new species,
Gigantopithecus bilaspurensis, was named, but more recently most researchers
have combined the mandible with the type of Sivapithecus giganteus (the lower
molar), thus making the new combination Gigantopithecus giganteus (Kelley
2002). Von Koenigswald (1949) proposed the nomen Indopithecus for the M3. In
my view, the type of G. bilaspurensis is sufficiently distinct from Pleistocene
Gigantopithecus that I place both the mandible and the M3 in Indopithecus, making
the new combination Indopithecus giganteus. The jaws and teeth of Indopithecus
are larger than any Sivapithecus, and the only known mandible is distinctive in
having reduced anterior tooth crown heights and molarized or enlarged premolars.
G. blacki, on the other hand, is larger still and has highly complicated postcanine
occlusal morphology and relatively even larger mandibles and smaller anterior
teeth. Because I. giganteus and G. blacki share characters of the lower jaws and
teeth that appear commonly during the course of hominoid evolution (in fact, in
many other mammal lineages as well), the relationship between the two is uncertain. Jaws and teeth in general, and mandibles in particular, are magnets for
homoplasy in primate evolution (Begun 1994b, 2007), and this may be another
example. In the end, the morphology of the jaw and teeth of Indopithecus much
more closely resembles that of Sivapithecus, while certain dental proportions more
closely resemble Gigantopithecus. Given the age and morphological differences, I
prefer to recognize two genera, though I do recognize that they are closely related.
The most parsimonious hypothesis is that I. giganteus is a primitive member of the
Gigantopithecus clade and that the strong similarity to Sivapithecus in the molars,
apart from size, suggests that it is the sister clade to that taxon (Table 1, Plate 12).
Lufengpithecus
Thousands of fossils, mostly isolated teeth, are known from a number of localities
in Yunnan Province, southern China. These are attributed to the genus
Lufengpithecus (Wu 1987). Lufengpithecus is most commonly recognized as a
Fossil Record of Miocene Hominoids
1299
Plate 12 Two mandibles of
Gigantopithecus compared
with a modern human
mandible. Gigantopithecus
images courtesy of Milford
Wolpoff
pongine. Kelley tentatively recognizes three species of Lufengpithecus, distinguished mainly by size and geography (each is known from a single site).
Lufengpithecus shares a few cranial characters with other pongines including a
small, pear-shaped nasal fossa, aspects of the implantation of the canine roots in the
maxilla, a deep canine fossa, supraorbital costae, and anteriorly oriented zygoma
(Schwartz 1997 and personal observations). However, while it lacks many of the
detailed similarities of the face between Sivapithecus and Pongo, its teeth are much
more like those of Pongo than Sivapithecus in details of occlusal morphology,
including the unusual presence of highly complex wrinkling or crenulations (Kelley
2002). The face of Lufengpithecus is unlike those of Sivapithecus and Pongo in
having broad orbits, a broad interorbital space, a comparatively short premaxilla,
high crowned incisors and canines, and compressed and very tall crowned male
lower canines. Though very damaged, my impression is that the nasal floor is unlike
the smooth floor of Sivapithecus and Pongo but possibly more similar to the
morphology in Ankarapithecus. There are intriguing similarities between
Lufengpithecus and dryopiths, especially in the incisors and premaxilla, and Kelley
and I have independently reached the conclusion that they might be more closely
related to one another than Lufengpithecus is to pongines. This, however, is a
hypothesis that needs a lot more investigation, and for now I follow Kelley
(2002) in placing Lufengpithecus among the pongines (Plates 13 and 14).
L. lufengensis (Xu et al. 1978) from a site near Shihuiba, in Lufeng county, is the
best-known species of the genus and is also known from a number of postcranial
remains including fragments of a scapula, clavicle, radius, first metatarsal, and two
phalanges. None have been published in detail, but all of these specimens show
clear indications of modern hominid morphology associated with suspensory positional behaviors (personal observations). This is especially true of the phalanges,
which are strongly curved and bear the markings of powerful flexor tendons. The
metatarsal is similar to that of Sivapithecus in its relative robusticity.
Until the fossils attributed to Lufengpithecus are published in detail, it will be
impossible to be confident in assessing their taxonomic and phylogenetic relations.
At this point, it seems likely that Lufengpithecus is a pongine and probably a sister
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D.R. Begun
Plate 13 Female (upper left,
PA 586) and male (upper
right, PA 548) mandibles of
Lufengpithecus in occlusal
view, and, below, an anterior
view of the male. Note the
high crowned and narrow
anterior dentition
Plate 14 Two Lufengpithecus babies. To the left, from Yuanmou (YV 0999) and to the right,
from Shuitangba (ZT 299) (Courtesy of Jay Kelley)
taxon to the Pongo-Sivapithecus-Ankarapithecus clade. However, the generally
more Pongo-like morphology of the molar occlusal surfaces and the more clearly
hominoid-like morphology of the postcrania are enigmatic and suggest caution in
interpreting evolutionary relationships. Kelley and Gao (2012) describe a juvenile
specimen of Lufengpithecus from a different locality, Yuanmou, also in Yunnan
Province. The Yuanmou specimen is interpreted by these authors as having more
similarities with dryopithecins than previously supposed for Lufengpithecus, which
is consistent with my impressions of the adult specimens from Shuhuiba. However,
we both come short of concluding that there is definite evidence of a phyletic link
between Lufengpithecus and the dryopithecins. Interpreting the morphology of a
taxon from a juvenile specimen can be very tricky. More detailed comparisons
between the Yunnan Province Lufengpithecus samples and those of dryopithecins
Fossil Record of Miocene Hominoids
1301
from Europe are needed to determine if there really are phylogenetic connections
between the two groups of hominids independent of the Siwalik taxa. This, however, would represent a dramatic development in our understanding of Late Miocene ape biogeography and would falsify an observation I made some years ago
about the separation of the Asian and European samples (Begun 2005). Another
possibility of course is that the Yunnan samples represent another lineage of
hominid not specifically related to any living great ape (Ji et al. 2013). Only more
detailed comparisons among these samples will help to resolve this issue.
Khoratpithecus
Three samples of Southeast Asian Miocene hominoids have recently come to light.
Chaimanee et al. (2003) describe a Middle Miocene sample of hominoids from
Thailand they originally attributed to a species of Lufengpithecus. The age of the
locality is not completely certain, and it is possible that the fauna could be correlated
with a more recent magnetostratigraphic interval, but for now the sample is considered to date to the late Middle Miocene or early Late Miocene (13.5–10 Ma).
However, on the basis of more recently discovered Late Miocene hominoid fossils
from Thailand, Chaimanee et al. (2004) described a new genus, Khoratpithecus, and
revised their previous taxonomic conclusions to include the Middle Miocene taxon in
the newly named genus as well. The fossils, a sample of isolated teeth and a wellpreserved mandible, are very similar to Lufengpithecus but show a number of
differences in the anterior dentition and lower jaw (Chaimanee et al. 2004).
Chaimanee et al. (2004) interpret Khoratpithecus to be more closely related to
Pongo than is any other pongine, mainly based on the shared derived character of a
missing anterior digastric muscle. More fossils are needed to test this hypothesis more
fully. The greater significance of these discoveries is the location, in Thailand, and the
possibly early age, Middle Miocene. In 2011 the same research group described a
new species of Khoratpithecus from Myanmar (formerly Burma), to the northwest of
Thailand (i.e., in the direction of the Siwaliks of India and Pakistan) (Jaeger
et al. 2011). The three species of Khoratpithecus are represented only by a small
number of mandibles and isolated teeth, and it is not clear if three different species are
represented, but they do appear to be distinct from Sivapithecus and Lufengpithecus.
All four genera of Asian great apes described here range in age from possibly as
old as 13.5 Ma to possibly as young as 6 Ma. If the dates are correct, Khoratpithecus
ayeyarwadyensis, from Myanmar, is the oldest of this group and is roughly contemporary with Kenyapithecus from Fot Ternan, Kenya. Lufengpithecus
lufengensis from Shuhiba (Yunnan Province, China) and Indopithecus from the
Siwalik Hills are the youngest, at about 6–7 Ma, and are roughly contemporaneous
with Sahelanthropus, from Chad, the earliest known hominin.
The Earliest Fossil Hominines: The Dryopithecins 1
At about the same time that hominids appear in Asia, they make their first
appearance in Europe. As is the case with the earliest pongines, the earliest
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D.R. Begun
hominines lack a number of synapomorphies of living hominines (African apes and
humans) and are less distinct from related non-hominines than are more recently
evolved hominines. This has led naturally to differences of opinion regarding
the systematics of this group (see chapters “▶ Defining Hominidae,” Vol. 3 and
“▶ Hominoid Cranial Diversity and Adaptation,” Vol. 2). There are three main
interpretations of the evolutionary relations among the taxa included here in the
Homininae. As noted, some researchers conclude that no known Eurasian Late
Miocene taxon has a specific relationship to extant hominoids (Pilbeam 1996, 1997;
McCrossin and Benefit 1997; Pilbeam and Young 2001, 2004). Most researchers,
however, accept the hominid status of these fossil taxa but are divided as to their
interrelationships. Some researchers (Andrews 1992) have concluded that European
Late Miocene hominids are best viewed as stem hominids, preceding the divergence
of hominines and pongines. Others interpret most or all Eurasian hominines to be
members of the pongine clade (Moyà-Solà et al. 1995). Finally, some researchers
interpret most or all European hominids to be hominines, although there is disagreement among them as to the precise pattern of relations (Bonis and Koufos 1997; Begun
and Kordos 1997; see chapter “▶ Potential Hominoid Ancestors for Hominidae,”
Vol. 3). As my interpretation falls with the last group, this will be reflected in this
chapter. I will however attempt to outline the major arguments from each perspective.
Nomenclatural History
The taxonomic history of Dryopithecus and the dryopithecins is very complicated
(see Begun 2002 for a more complete history). At one time, most of the well-known
taxa described here were attributed to Dryopithecus (Proconsul, Sivapithecus,
Ouranopithecus, Ankarapithecus, Griphopithecus). More recently Dryopithecus
was restricted to the sample European great apes from Spain, France, Germany,
Austria, Hungary, and Georgia that all share features in common with African apes,
in particular thinly enameled teeth with less robust jaws than Sivapithecus or
Ouranopithecus. This was the consensus when the first version of this review was
published in 2007. Since then the concept of Dryopithecus has become even more
narrowly defined. As of this writing, Dryopithecus is restricted more or less to the
original sample from St. Gaudens, a mandible from Austria and a maxilla from
Spain. The important distinctions between Dryopithecus and most of the other
samples that have until recently been attributed to Dryopithecus are age and
morphology. All Dryopithecus, along with Pierolapithecus and Anoiapithecus,
are more primitive in dental morphology (persistent cingula, small first molars,
short premolars, robust canines) (Begun et al. 2012; Alba 2012). Postcranially,
Pierolapithecus is more primitive than the later-occurring Hispanopithecus and
Rudapithecus (see below). Dryopithecus, Pierolapithecus, and Anoiapithecus all
occur in the Middle Miocene. Later-occurring and more modern-looking
dryopithecins are all from the Late Miocene in Europe.
Specimens from the Middle Miocene of Spain have been attributed to
Dryopithecus but also to two new taxa, Pierolapithecus and Anoiapithecus.
The latter is known only from a distorted facial fragment, while the former is
known from many parts of a skeleton, though unfortunately the face is seriously
Fossil Record of Miocene Hominoids
1303
damaged. Because Dryopithecus sensu stricto is known only from male mandibles, it is extremely difficult to compare it with Pierolapithecus and
Anoiapithecus, both of which are known mainly from upper teeth and postcrania.
There is a mandibular fragment of Anoiapithecus that can be compared directly
with Dryopithecus, and in my opinion, the differences between the two samples
do not warrant a genus level distinction. Pierolapithecus is not known from
lower teeth or jaws, and it is impossible to compare this sample with
Dryopithecus. In addition, when they were first described, each of these taxa
was assigned to different hominid clades.
Pierolapithecus and Anoiapithecus were first described as stem hominids,
predating the divergence of pongines and hominines (Moyà-Solà et al. 2004,
2009a). Dryopithecus, when it was discovered at Hostalets, was first described as
a hominine and possibly a sister clade to Gorilla (Moyà-Solà et al. 2009b). In
addition, Hispanopithecus, also from the Vallès Penedès but from younger deposits
(see below), was first described as a pongine. This represents three separate
hominid clades present in a relatively restricted temporal and geographic span,
which I consider unlikely. The most current interpretation of all of these taxa places
them in the Ponginae (Alba 2012, Fig. 8, p. 265), though this author acknowledges
that other interpretations, including the alternatives that they are all hominines or
stem hominids, are possible. The practical difficulties in comparing
Pierolapithecus, Anoiapithecus, and Dryopithecus to each other, given the few
comparable parts preserved (see below), led me to be skeptical that three different
genera and possibly three different clades can be effectively identified from these
samples. The fact that all three Middle Miocene genera were found within a few
kilometers of one another from essentially the same time period and same geological formation made me even more skeptical that three different genera are
represented. All three are Middle Miocene and are more primitive than Late
Miocene apes including Hispanopithecus. However, this is not the place for a
taxonomic revision of these genera, so I will use the nomena originally proposed
by the describers while noting that they are probably all closely related and possibly
all Dryopithecus.
Dryopithecus fontani
Dryopithecus is the first-named taxon, and it is agreed by most researchers that this
taxon is Middle Miocene and more primitive than Late Miocene European great
apes. There is disagreement as to whether or not other early hominids taxa lived in
Western Europe during the same time as Dryopithecus. Dryopithecus was first
identified from St. Gaudens, on the northern slopes of the French Pyrenees (Lartet
1856). Dryopithecus sensu stricto, that is, D. fontani, is only known from three
mandibles, a few isolated associated teeth, and a humeral shaft, all from
St. Gaudens. Two isolated teeth from La Grive, also in France but in a geologically
completely different context (Alpine as opposed to Pyrenean), are also traditionally
attributed to Dryopithecus. These sites are considered to be Middle Miocene, based
exclusively on their fauna, and the apes from these sites are more primitive dentally
than apes that occur later on in Europe.
1304
D.R. Begun
Dryopithecus fontani is known from three male mandibles and a humerus, all
from the same locality in France, a female mandible from Austria, and a partial face
from Spain (Begun 2002; Begun et al. 2012; Moyà-Solà et al. 2009b). Two isolated
upper teeth from La Grive in France are also usually attributed to D. fontani. The
mandibles and their dentitions are typically hominid in being comparatively robust
with well-developed symphyseal tori, large incisors, compressed canines, elongated
postcanine teeth with peripheralized cusps and lacking cingula, P4 with trigonids
and talonids of nearly equal height, and molars of nearly equal size, especially M1
and M2. The teeth of all Dryopithecus are thinly enameled with dentine horns
penetrating well into the enamel caps. D. fontani is distinguished from other species
of Dryopithecus in having a mandible that shallows (becomes lower compared to
breath) distally, a high frequency of buccal notches on the lower molars, and
comparatively robust lower canines.
The more recently described material attributed to Dryopithecus from Catalonia
include a palate that cannot be directly compared with the fossils from France and
Austria but does allow a comparison with Anoiapithecus and Pierolapithecus. Alba
(2012) maintains that the morphological differences among these three samples are
sufficient to justify the recognition of three different genera, all of which he places
within the ponginae. In my view, the differences are minor and the samples, while
including well-preserved specimens, are small, making it very difficult to assess
ranges of variation within each group. This being the case, I think it is more likely
that a single genus is represented, and by the rule of taxonomic priority, that taxon
would be Dryopithecus (Begun et al. 2012).
Dryopithecus fontani is also known from a humeral shaft from the type locality
that has been described as chimpanzee-like (Pilbeam and Simons 1971; Begun
1992a). It is the only nearly complete humerus of the genus. It is comparatively long
and slender with poorly developed muscle insertion scars and a slight mediolateral
and anteroposterior curvature. Neither the proximal nor the distal epiphyses are
preserved, but the diaphysis preserved close to each epiphysis is hominoid-like.
Proximally, it is rounded in cross section with a bicipital groove position suggesting
some degree of humeral torsion (but see Rose 1997; Larson 1998). Distally, it is
mediolaterally broad and anteroposteriorly quite flat, with a large, broad, relatively
shallow olecranon fossa (Begun 1992a).
Finally, the proximal end of a femur has been tentatively attributed to
Dryopithecus (cf. Dryopithecus). This specimen has been described as less suspensory than Hispanopithecus, with indications of a more quadrupedal form of locomotion (Moyà-Solà et al. 2009b). If this is truly Dryopithecus, this interpretation is
somewhat at odds with the interpretation of suspensory locomotion based on the
humerus, but as we see very often in the fossil record, different anatomical regions
evolve somewhat independently, leading to morphological mosaics that have no
analogues among living taxa.
Pierolapithecus catalaunicus
The best-known Middle Miocene hominine genus is represented by the very nicely
preserved partial skeleton of Pierolapithecus (Moyà-Solà et al. 2004). The
Fossil Record of Miocene Hominoids
1305
specimen, from northern Spain, is dated to 11.93 Ma (Casanovas-Vilar et al. 2011).
The specimen includes most of a face which, though distorted, preserves nearly all
the teeth and many informative facial characters. It also includes a partial postcranial skeleton, the most informative parts of which are some lumbar vertebrae, ribs,
and a number of hand and foot bones. Moyà-Solà et al. (2004) interpret
Pierolapithecus as a basal or stem hominid. More recently, Alba (2012) prefers
the hypothesis that Pierolapithecus is a pongine. Moyà-Solà et al. (2004) cite the
lumbar vertebrae, which preserve evidence of a hominoid-like vertebral column
and by extension rib cage. This is indicated by the position of the lumbar transverse
processes, placed more posteriorly in hominoids to stiffen the lower back (Ward
1993). However, the morphology of the lumbar vertebrae in Pierolapithecus is
more hylobatid-like, extant hominids having even more posteriorly positioned
transverse processes. Other aspects of the postcranium that clearly support the
hominoid status of Pierolapithecus include ribs, indicative of a broad, anteroposteriorly compressed rib cage, robust clavicle, and a wrist morphology indicating no
direct contact between the carpus at the triquetrum and the ulna (Moyà-Solà
et al. 2004). These features are shared with all extant hominids. Hylobatids are
unique in their carpal/ulnar contact, having a large intervening articular meniscus
(Lewis 1989). The homologous surface of the triquetrum in Pierolapithecus indicates a great ape and not a hylobatid configuration.
The carpals in general are hominid-like in their overall morphology, including
relative size, robusticity, and general pattern of the orientation of the joint surfaces.
The lunate, triquetrum, and hamate in particular closely resemble small chimpanzees, but it is not clear if these are derived characters for hominines or hominids.
Moyà-Solà et al. (2004) describe the phalanges of Pierolapithecus as being relatively shorter, less curved, and with metacarpal joint surfaces facing more dorsally
than in Rudapithecus and Hispanopithecus, clearly suspensory hominines, which
they interpret to mean that Pierolapithecus had a palmigrade hand posture (see also
Alba et al. 2010). At the same time, the attributes of the thorax and hand suggest
antipronograde (suspensory) limb positions, which is somewhat contradictory.
They resolve this dilemma with the suggestion that Pierolapithecus was a powerful
vertical climber but not suspensory. This is similar to the suggestion made earlier
regarding Sivapithecus, though the morphology of the phalanges does not in fact
rule out suspension. The phalanges are curved compared with most arboreal
primates and have strongly developed flexor muscle attachments, even if these
are not so strongly expressed as in Hispanopithecus and Rudapithecus (Begun and
Ward 2005). Deane and Begun (2008) concluded that the phalanges of
Pierolapithecus were in the range of curvature seen in Hylobates, Pongo,
Rudapithecus, and Hispanopithecus. Based on phalangeal curvature, Deane and
Begun (2010) considered Pierolapithecus to be more suspensory than Old World
monkeys and African apes but less than in Asian apes.
Moyà-Solà et al. (2004) interpret various craniodental attributes of
Pierolapithecus to reflect its stem hominid status as well. The face is prognathic
with an enlarged premaxilla. The zygomatic root is high, the nasal aperture broad,
and the postcanine teeth have a typical hominid morphology (elongated, relatively
1306
D.R. Begun
large M1, absence of cingula, reduced premolar cusp heteromorphy, buccolingually
large incisors, compressed canines). The premaxilla is expanded compared with
early and exclusively Middle Miocene hominoids and appears to have an overlap
posteriorly with the maxilla, as in hominids. However, according to these authors, it
lacks the distinctive attributes of either the hominine of pongine clade.
Some of the distinctive attributes of Pierolapithecus are clearly related to
distortion. The glabella is unlikely to have been as posterior as it appears, the
midface is clearly badly damaged and was not as prognathic as in Afropithecus,
despite what the authors suggest, and the premaxilla is obviously displaced relative
to the palatine process of the maxilla (Begun and Ward 2005). In my view, the face
much more closely resembled Hispanopithecus, though it is still distinct enough to
justify a separate genus. The similarities with Afropithecus are probably related to a
similar pattern of distortion (see above).
All in all, Pierolapithecus closely resembles Dryopithecus, known from contemporaneous localities in France and Austria, and Hispanopithecus and
Rudapithecus, known from younger localities in Spain and Hungary. Based on
this level of similarity, a consensus is emerging that all of these taxa belong in the
tribe Dryopithecini (Begun et al. 2012; Alba 2012).
Attributes of the postcrania and dentition are more primitive in Pierolapithecus
and justify a separate genus from Late Miocene Hispanopithecus and Rudapithecus.
There is evidence to suggest that Pierolapithecus is a stem hominine and not as
Moyà-Solà et al. (2004) conclude, a stem hominid, or as Alba (2012) concludes, a
stem pongine (Begun and Ward 2005; Begun 2007, 2009; Begun et al. 2012). Details
of dental morphology are strikingly similar to other dryopithecins (Dryopithecus,
Rudapithecus, Hispanopithecus). Despite the unusually small M3 and elongated
upper canine, most of the teeth could easily be mistaken for those of other
dryopithecins and show features distinctive for that tribe, including relatively tall
crowned and mesiodistally narrow upper incisors, compressed canines, premolars
with prominent cusps separated by a broad deep basin, and molars with marginalized
or peripheralized, relatively sharp cusps. The contact between the premaxilla and the
maxilla appears to also have been very similar to Rudapithecus in being stepped with
only a modest degree of overlap between the two (Alba 2012; Begun 2007, 2009;
Begun et al. 2012). The supraorbital region, though described by Moyà-Solà
et al. (2004) as having thin supraorbital arches, actually closely resembles
Rudapithecus and Hispanopithecus specimens from Spain and Hungary, with subtle
tori emerging from a more prominent glabella. In my view, Pierolapithecus is close
to the common ancestor of the Hominidae but already shares a common ancestor with
the Homininae (Begun and Ward 2005; Begun 2009). Its postcranial morphology,
however, is probably very close to that of the hominid ancestral morphotype (Fig. 2).
Anoiapithecus
Anoiapithecus is the third genus of Middle Miocene hominine from Hostalets de
Pierola (Moyà-Solà et al. 2009a). As noted, it was originally interpreted to be a stem
hominid and more recently a stem pongine. The stem hominine attribution is largely
on the basis of its short face (hence the trivial name brevirostris). The dental
Fossil Record of Miocene Hominoids
1307
Plate 15 Rudapithecus. The two crania (RUD 77, left and RUD 200, right) include the most
complete brain cases of a European hominine. The RUD 200 image is a virtual reconstruction
superimposed on a chimpanzee skull (Courtesy of Philipp Gunz). RUD 12 (bottom left) is a female
left hemi-palate mirror imaged to make a complete palate. RUD 14 (bottom right) is juvenile male
mandible
morphology, which is the best preserved parts of Anoiapithecus, is very similar to
other dryopithecins, and without the facial portions, it would certainly be assigned
to Dryopithecus. The facial portions that are preserved are quite fragmentary, and I
am doubtful that a reliable reconstruction of the palate relative to the upper part of
the face can be achieved. When the most complete and well-preserved parts of the
Anoiapithecus specimen are considered, their similarity with Dryopithecus is undeniable. Whether or not the reconstruction provided in Moyà-Solà et al. 2009a holds
up will depend in my view on the recovery of a more completely preserved face.
Late Miocene European Hominines: The Dryopithecins 2
Hispanopithecus
Hispanopithecus crusafonti (Begun 1992c) is known from a sample of isolated teeth
and a palatal fragment from Can Ponsic and a well-preserved mandible from Teuleria
del Firal, both in northern Spain and both dated to between 10.4 and 10 Ma
(Casanovas-Vilar et al. 2011). H. crusafonti is dentally similar to other dryopithecins
but has distinctive upper central incisors, a more robust mandible lacking the distal
shallowing of Dryopithecus, upper molars of nearly the same size, and a number of
other subtle features of dental morphology (Begun 1992c) (Plates 15, 16, 17, and 18).
1308
D.R. Begun
Plate 16 RUD 44 in medial
view. Note the stepped
subnasal fossa (blue lines)
between the alveolar process
and the palatine process of the
maxilla (yellow lines)
Plate 17 Hispanopithecus
(IPS 18000). The frontal bone
in anterior view is mirror
imaged from the left side.
Black arrows, rudimentary
supraorbital tori; white
arrows, torus in lateral view;
yellow arrow, frontal sinus
penetrating into the
interorbital space; red arrow,
zygomatic portion of the
frontozygomatic suture
Hispanopithecus laietanus (Villalta and Crusafont 1944) is known from several
slightly younger sites in Spain. Dentally, it is smaller but similar to other
dryopithecins and lacks the unique dental characters of H. crusafonti. It is the
best-known species of the genus. Like H. crusafonti, H. laietanus has tall, relatively
narrow upper central incisors, though not to the degree seen in H. crusafonti. The
mandible is relatively robust. A partial cranium of H. laietanus displays numerous
hominid cranial characters (broad nasal aperture base, high zygomatic roots, shallow subarcuate fossa, and probable enlarged premaxilla with maxillary overlap,
although the specimen is damaged in that area). A few hominine characters are
found on this specimen as well (supraorbital tori connected to glabella,
frontoethmoidal sinus, inclined frontal squama, and thin enamel) (see Alba 2012
for a different interpretation).
The most significant specimen of H. laietanus is a partial skeleton, an exceptional and important specimen (Moyà-Solà and Köhler 1996). The most significant
features of the postcranial skeleton of H. laietanus are the numerous and unambiguous indications of both well-developed suspensory positional behavior and clear
hominid synapomorphies. These include elongated forelimb; large hands with
Fossil Record of Miocene Hominoids
1309
Plate 18 Hispanopithecus
reconstruction (left) and
Rudapithecus in three fourth
view (right)
powerful, curved, elongated digits; comparatively short and robust hindlimb; and a
hominid-like lumbar region. Other attributes interpreted to be present in this partial
skeleton, such as an elongated clavicle and limb proportions approaching those of
Pongo, are based on fragmentary evidence and are less reliable. The specimen has
some unusual features for a hominid such as short metacarpals, but overall it is quite
modern. The humerus, though fragmentary, is like that of D. fontani and unlike that
of Sivapithecus. While there is universal agreement that Hispanopithecus is orthograde and suspensory, there is disagreement on the degree to which it was suspensory (Almécija et al. 2007; Deane and Begun 2008, 2010; Alba et al. 2010).
Rudapithecus hungaricus
Rudapithecus hungaricus Kretzoi, 1969 was named based on the sample of
hominines from Rudabánya, Hungary (Begun and Kordos 1993). Most researchers
rejected to generic distinctiveness of Rudapithecus, preferring to include the
Rudabánya sample in Dryopithecus brancoi (Begun and Kordos 1993), myself
included. In the second half of the nineteenth century, shortly after the initial
discovery and description of Dryopithecus fontani, additional fossil hominoid
teeth began to turn up in Germany. These were eventually assembled to define
the new species, D. brancoi (Schlosser 1901), though not before considerable
taxonomic shuffling (see Begun 2002 for more historical details). D. brancoi is
based on an isolated M3 which, while not the ideal type specimen, can be effectively
distinguished from the other species. To help in species identification, the species
diagnosis was revised by Begun and Kordos (1993) based on the excellent sample
from Rudabánya, Hungary. This was the majority view through 2009. At that time,
researchers working on the Spanish and Hungarian samples had independently
come to the conclusion, as described earlier, that Dryopithecus as originally
described should include only Middle Miocene more primitive European
hominines, while the Late Miocene taxa traditionally attributed to Dryopithecus
should be reassigned to their original nomena (Rudapithecus and Hispanopithecus).
The nomenclatural history of these samples is described more fully in
Begun (2009).
1310
D.R. Begun
Table 3 Great ape and African ape craniodental character states of Rudapithecus
Great ape character states
Labiolingually thick incisors
Compressed canines
Elongated premolars and molars
M1 ¼ M2
No molar cingula
Reduced premolar cusp heteromorphy
High root of the zygomatic
Elongated midface
Broad nasal aperture below the orbits
Reduced midfacial prognathism
Elongated, robust premaxilla
Premaxilla-palatine overlap
Shallow subarcuate fossa
Enlarged semicircular canals
Large brain
High cranial base (Begun 2004)
African ape character states
Biconvex premaxilla
Stepped subnasal fossa
Patent incisive canals
Broad, flat nasal aperture base
Shallow canine fossa
Supraorbital torus
Inflated glabella
Frontal sinus above and below nasion
Projecting entoglenoid process
Fused articular and tympanic temporal
Broad temporal fossa
Deep glenoid fossa
Elongated neurocranium
Moderate alveolar prognathism
Klinorhynchy
Rudapithecus hungaricus is only known from Rudabánya (Hungary) and is dated
to about 10 Ma. Six other localities in Germany, Austria, and Georgia may also
contain Rudapithecus, but as the specimens are all isolated teeth, it is difficult to be
certain. Rudapithecus shares all the hominid characters already described for other
Late Miocene hominids, but the cranium is better preserved in this taxon than in any
other and provides additional details (Table 3).
Rudapithecus shares with other dryopithecins all the details of canine and
postcanine tooth morphology outlined above. It shares relatively narrow and
labiolingually thick upper central incisors with other dryopithecins, though not to
the degree seen in H. crusafonti. Rudapithecus preserves a few details of the face
and many details of the neurocranium and basicranium, with further evidence of its
hominid status. The zygoma are high, prominent, and oriented anterolaterally, as in
hominines, and the number and position of the zygomaticofacial foramina is
variable (this character has been proposed as one that could establish the pongine
affinities of Hispanopithecus, but the configuration in Rudapithecus is homininelike (Kordos and Begun 2001)) The neurocranium is large, with a reconstructed
cranial capacity in the range of extant chimpanzees (Rudapithecus is the only Late
Miocene hominid for which cranial capacity reconstruction is possible from direct
measurements of the brain case [in two individuals]) (Kordos and Begun 1998,
2001; Begun and Kordos 2004).
Among the hominine characters preserved in the cranial sample of Rudapithecus
are a relatively low and elongated neurocranium, with the inion displaced inferiorly
(Table 3). The interorbital and supraorbital regions have sinuses that are largest
above glabella. Glabella is prominent and continuous with small supraorbital tori
separated from the frontal squama by a mild supratoral sulcus (Begun 1994a).
Fossil Record of Miocene Hominoids
1311
The temporal bone, in addition to preserving evidence of a shallow subarcuate fossa
(a hominid character), suggests fusion of the articular and tympanic portions and
preserves details of the temporomandibular joint found only in hominines (Kordos
and Begun 1997). RUD 200 (also known as RUD 197-200), the best preserved
cranium of a dryopithecin, is the first to include a well-preserved neurocranial and
facial skeleton in connection and shows clearly that the cranium of Dryopithecus
was klinorhynch (having a ventrally deflected face), which it shares with African
apes among the hominoids (Kordos and Begun 2001; Fig. 4).
The nasoalveolar clivus or premaxilla is hominine like in its orientation, size,
surface anatomy, and relations (Fig. 3). It is biconvex, long compared to Early
Miocene Hominidea and hylobatids (proportionally equal in length to Gorilla), with
a posterior pole that is elevated relative to the nasal floor, giving a stepped
morphology to the subnasal fossa (Begun 1994a; Fig. 3). The resulting incisive
fossa of the subnasal floor is deep and well defined, the incisive canal is short and
large in caliber, and the incisive foramen on the palatal side is comparatively large.
This suite of characters is found in Gorilla as well, which suggests that this is the
ancestral morphology for hominines. Pan and Australopithecus share the
synapomorphic condition of a more elongated but still biconvex premaxilla,
which along with their spatulate upper central incisors and neurocranial morphology is among the most important morphological synapomorphies of the
chimpanzee-human clade (Begun 1992c).
Rudapithecus is well represented by postcrania, including a distal humerus that
is hominid-like in all details related to trochlear and capitular morphology as well as
having broad and shallow fossae for the processes of the radius and ulnae (see
above). The ulna is robust with a strongly developed trochlear keel and a radial
facet orientation that indicates forearm bones positioned for enhanced
antipronograde postures (Begun 1992a). The scaphoid is Pongo-like in morphology
and was not fused to the os centrale, as it is in African apes and humans (Begun
et al. 2003c). The capitate is large with a complex metacarpal articular surface, as in
African apes, but the head is comparatively narrow and the bone overall is elongated compared to African apes, again more like the condition in Pongo and
Sivapithecus. The triquetrum and pisiform provide evidence that the ulna did not
contact the medial carpals in any way, an important synapomorphy of the great apes
and humans. The phalanges are long, strongly curved, and marked by sharp ridges
for the flexor musculature, indicative of suspensory positional behavior (Begun
1993). The femora of are short, with a large head, long neck, and extremely robust
shaft, consistent with the hominoid pattern, and again especially similar to Pongo.
The foot is also apelike in its broad, flat talar body and mobile but large
entocuneiform and hallux.
Ouranopithecus
A large hominid sharing characters of Dryopithecus and Sivapithecus was first
described from northern Greece and attributed to the genus Dryopithecus (to which
Sivapithecus was also attributed at the time) (Bonis et al. 1975). Soon it became clear
that the sample from Greece was distinct from both Sivapithecus and Dryopithecus,
1312
D.R. Begun
Plate 19 Ouranopithecus and “Ouranopithecus” turkae. Top, palatal, anterior, lateral and medial
views of “Ouranopithecus” turkae (CO-205). Bottom, from left to right, RPL 128 and two views of
ZIR 1
and the new nomen Ouranopithecus (see chapter “▶ Potential Hominoid Ancestors
for Hominidae,” Vol. 3) was proposed (Bonis and Melentis 1977; Plate 19).
Ouranopithecus is a large hominid, the approximate size of a large male
chimpanzee or female gorilla, whose morphology is similar to that of other
dryopithecins but with a much more robust masticatory adaptation (Begun and
Kordos 1997). Ouranopithecus has a palate that is similar to other dryopithecins in
the degree and pattern of overlap of the maxilla and premaxilla (Bonis and Melentis
1987; Begun and Kordos 1997). The morphology of the nasoalveolar clivus is also
similar to dryopithecins and extant hominines. The nasal aperture is broad at its
base, the interorbital space is broad, and the orbits are rectangular. The zygomatic
roots arise relatively low and anteriorly on the maxilla, which is interpreted as a
homoplasy with Early Miocene taxa, as a similar condition is also found in robust
australopithecines that share with Ouranopithecus a very robust masticatory apparatus (Begun and Kordos 1997; Begun 2007). The glabella is projecting, and like
Hispanopithecus and Rudapithecus, it is continuous with subtle tori above each
orbit. The frontal squama is concave above glabella, as in Hispanopithecus, but this
is somewhat exaggerated by damage. Dentally, Ouranopithecus is similar to
dryopithecins and other hominids in tooth proportions and overall dental morphology. It differs from dryopithecins in having hyperthick occlusal enamel, molars
with broad cusps and flat basins, mesiodistally longer incisors, and relatively
low-crowned male upper canines. The mandibles are also more robust than in
Fossil Record of Miocene Hominoids
1313
other dryopithecins and have strongly reinforced symphyses. The female mandibles
tend to be more robust (or shallower) than the male mandibles. One mandible
preserves the condylar process, which is large and strongly convex anteroposteriorly. Ouranopithecus is also known from two unpublished phalanges.
In many publications, summarized in Bonis and Koufos (1997), it has been
argued that Ouranopithecus is a hominin (specifically related to humans), mainly
on the basis of canine reduction and masticatory robusticity. However, these
features occur repeatedly during hominoid evolution. Ouranopithecus is most
parsimoniously interpreted as a terminal member of the dryopithecin clade, with
a number of craniodental specializations related to an increase in masticatory
robusticity (Begun and Kordos 1997; Begun 2001, 2002, 2007, 2009). The large
jaws and teeth and hyperthick enamel, as well as microwear studies, suggest an
ability to exploit hard and/or tough fruits, nuts, and other dietary resources (Kay
1981; Ungar 1996; Bonis and Koufos 1997; Kay and Ungar 1997).
Graecopithecus
Another taxon, Graecopithecus (von Koenigswald 1972), is also known from
Greece but from a much younger locality over 200 km from the Ouranopithecus
localities. It is similar to Ouranopithecus, and some have suggested that the two
samples belong to the same genus, which would be called Graecopithecus, since
this nomen has priority (Martin and Andrews 1984). In my view, the generic
distinction is warranted. Graecopithecus, known only from a poorly preserved mandible with a fragmentary M1, a much worn M2, and root fragments, is similar to
Ouranopithecus in apparently having thick occlusal enamel. However, it is the overall
size of female Ouranopithecus but has an M2 bigger than some male Ouranopithecus,
and the M2 is actually broader than the mandibular corpus at the level of the M2. The
symphysis is more vertical and the M1 is relatively small (Begun 2002, 2009).
Graecopithecus is morphologically distinguishable from Ouranopithecus, much younger in age, and geographically distant from Ouranopithecus localities.
There are two other samples of Late Miocene hominines that have affinities with
Ouranopithecus. G€uleç et al. (2007) described a new species of Ouranopithecus,
O. turkae, based on a large maxilla recovered from the site of Çorakyerler, in
Central Anatolia. The site is unique for Eurasian Late Miocene apes in being an
open habitat and being young in age (about 8–8.5 Ma). Only Oreopithecus in
Europe and Lufengpithecus in Asia are younger. Having studied the maxilla from
Çorakyerler in detail, it is my view that it represents a new genus of hominine
(Sevim et al. 2001; Begun 2009; Begun et al. 2012). It is much larger than
Ouranopithecus, the maxilla fitting comfortably on the mandible of Indopithecus,
and the anterior dental morphology is quite distinct. However, until more recently
recovered specimens are described, I refrain from naming a new genus.
The other sample of Late Miocene hominine that may be attributed to
Ouranopithecus is the isolated P4 from the site of Azmaka, near Chirpan,
Bulgaria (Spassov et al. 2012). The site may be as late as 7 Ma, but only one P4
is known. The specimen is clearly a hominid, and more closely resembles thickly
enameled taxa, but its precise affinities remain to be determined.
1314
D.R. Begun
The greater significance of these two samples from Bulgaria and Turkey are not
their taxonomic or phylogenetic affinities, but their location in geographic and
temporal space. Both are much later than some have predicted for Miocene apes
in Europe, and both are associated with paleoecological settings that some have said
excludes the presence of apes (Bernor et al. 2004; Bernor 2007). There are many
problems with the naı̈ve preconception that hominines could not have dispersed
between Eurasia and Africa in the Late Miocene (see Begun et al. 2012 for a
detailed critique). We now know that Late Miocene hominines lived in much drier
conditions than previously supposed, and we also know that even without these
adaptations, ample evidence exists for forest corridors and refugia in southeastern
Europe and North Africa that could have allowed forest-adapted taxa to disperse
between the two continents (Begun et al. 2012) The presence of hominines from
Çorakyerler and Azmaka demonstrate that it is unwise to exclude a priori an
ecological association resulting from the wondrous and unpredictable interaction
of natural selection, anatomy, behavior, and ecology.
Paleobiology of the Dryopithecins
Most dryopithecins display dental morphological characters that are very similar to
extant Pan and suggest a soft fruit diet (Begun 1994a). Microwear analyses support
this assessment (Kay and Ungar 1997). The dryopithecin gnathic is gracile compared
to many other Late Miocene hominids (less robust mandibles, thinner occlusal
enamel, smaller attachment sites for the muscles of mastication), which is both
consistent with a soft fruit diet and more similar to extant African apes, Pan in
particular. Postcranially, Hispanopithecus and Rudapithecus are unambiguously
suspensory, but they do lack a few synapomorphies, particularly of the extremities,
which characterize all extant hominids. These have to do mainly with the robusticity
of the bones of the carpus and tarsus, which may be attributable to a “red queen”
phenomenon, as in the case of the progressive development of shearing quotients
during the course of hominoid evolution (Kay and Ungar 1997). In the fossil record of
many mammals, there is evidence of a shift toward a certain adaptation (folivory,
frugivory, suspension, climbing, bipedalism, etc.) that becomes increasingly refined
in individual lineages descended from the common ancestor initially expressing the
behavior. In order to remain competitive, the descendants must, in essence, run to
stay in the same place, as increasingly efficient versions of the same adaptation
appear independently (van Valen 1973). Rudapithecus and Hispanopithecus were
arboreal, suspensory, soft fruit frugivores with a dentition similar to Pan, living in
seasonal subtropical forests but probably capable of exploiting a variety of resources,
possibly including meat (Kordos and Begun 2002).
The exception to this general pattern among the dryopithecins is
Ouranopithecus, which was a hard/tough object feeder. While the postcrania have
not been described in Ouranopithecus, it has been suggested that it was probably
more terrestrial than other dryopithecins, given its diet and habitat, which was more
open country than any other dryopithecin (Bonis and Koufos 1994). However, a
definitive answer to the question of the positional behavior of Ouranopithecus must
await analysis of the phalanges.
Fossil Record of Miocene Hominoids
1315
Oreopithecus
The other European Miocene hominoid discovered and described during the nineteenth century is the highly unusual Oreopithecus (Gervais 1872). Over the years,
Oreopithecus has been called a pig, prosimian, monkey, and ape, the last being the
attribution most researchers agree on today (Harrison and Rook 1997; Moyà-Solà
and Köhler 1997; Begun 2002). Oreopithecus is younger than other Late Miocene
European hominoids and is known from about 6 to 7 Ma localities in Italy. At the
time, most of the Italian peninsula was separated from the rest of Europe by the sea,
as is today the Italian island of Sardinia, where one Oreopithecus locality is found.
In the Late Miocene, all Oreopithecus localities were insular, and the faunas
associated with them are unique and difficult to compare to continental European
faunas (Harrison and Rook 1997). Oreopithecus is a product of its insular environment as well and is characterized by many unique adaptations that make it difficult
to understand its relations to other hominoids.
In its craniodental morphology, Oreopithecus is similar to dryopithecins and African
apes in having apparently thin enamel, but otherwise the morphology of the teeth is quite
unique. Like other hominids, Oreopithecus has compressed canines, reduced premolar
cusp heteromorphy, and reduced or absent molar cingula. However, the incisors are
small and low crowned; the P4 has a primitive-looking low talonid compared to the
trigonid; the postcanine dentition has tall, isolated cusps; and the lower molars have a
unique occlusal morphology with a centroconid connected to the four principal cusps by
a well-developed system of crests. The upper molars are also strongly “cristodont,”
which makes them appear similar to the lower molars, superficially resembling the
condition of upper and lower molar bilophodonty in Old World monkeys.
The mandible is strongly built with some specimens being quite robust transversely and others deeper. The ramus is expansive to accommodate large temporalis
and masseter muscles, which is also evidenced by the prominent temporal crests and
pronounced postorbital constriction. The face is badly damaged but appears to have
had a short and relatively gracile premaxilla, which is consistent with the small
incisors. The brain case is also badly damaged but was clearly small, housing a
much smaller brain than great apes of comparable body mass (Harrison 1989; Begun
and Kordos 2004). Like Sivapithecus and non-hominids, the articular and temporal
portions of the temporal bone are not fused, but like hominids the subarcuate fossae
are small. The ectocranial crests are very strongly developed, while the frontal is
comparatively smooth, without tori, and the postorbital constriction is marked.
The most impressive aspect of Oreopithecus is its postcranium. A remarkably
complete but crushed skeleton along with many other isolated postcranial elements
is known from Oreopithecus. The axial skeleton (rib cage and trunk) is hominoidlike in its short lower back and broad thorax, and the pelvis is also comparatively
short and broad, as in hominids. The forelimbs are very elongated compared with
the hindlimbs, the glenoid fossa of the scapula is deep, and the elbow has all the
typical hominoid features described previously. The femur is short and robust with
a large head, and the knee joint indicates mobility in several planes. The hand is
long but narrow, and the foot is comparatively short, though in both the hand and
1316
D.R. Begun
foot, the digits are long and curved. The carpals and tarsals are primitive hominoidlike in being transversely gracile compared to their length. They more closely
resemble the carpal and tarsal bones of Proconsul than those of hominids.
Oreopithecus combines primitive and derived hominoid characters that ironically
make it extremely difficult to place phylogenetically, despite its relatively complete
preservation. Harrison and Rook (1997) consider Oreopithecus to be a stem hominid
closely related to the dryopithecins. Moyà-Solà and Köhler (1997); Moyà-Solà
et al. (1999) interpret both the dryopithecins and Oreopithecus to be stem pongines
(see chapter “▶ Defining Hominidae,” Vol. 3), and they have also concluded that
Oreopithecus was an arboreal biped with a well-developed precision grip. However,
these conclusions are based in part on an erroneous reconstruction of the hand of
Oreopithecus (Susman 2004 and personal observations) and a very unlikely reconstruction of the foot (Köhler and Moyà-Solà 1997 and personal observations). Rook
et al. (1999) interpret CT scans of the innominate of Oreopithecus to imply a
remodeling of bone consistent with bipedalism, but alternative interpretations are in
my view more likely (Wunderlich et al. 1999). Overall, the overwhelming signal
from the postcranium of Oreopithecus is of a suspensory arboreal adaptation. The
long, curved phalanges are unambiguous indicators of suspension and incompatible
with either bipedalism or a precision grip.
Though some have interpreted aspects of the cranial morphology of Oreopithecus to
have resulted from neoteny leading to a superficially primitive morphology (Moyà-Solà
et al. 1997; Alba et al. 2001), it is very difficult to identify heterochrony in fossil taxa
(Rice 1997), and the much more straightforward interpretation is that Oreopithecus
does in fact retain a number of primitive characters not found in other Late Miocene or
extant hominids (Harrison 1986; Harrison and Rook 1997; Begun 2002). These include
a short, gracile premaxilla, large incisive foramen, low position of the zygomatic root,
small brain, a number of features of the basicranium, and several postcranial characters
(gracile phalanges; transversely small carpals; short, relatively gracile tarsals; etc.). It is
very unlikely that a single growth process resulting from selection for bipedalism and an
omnivorous diet, as suggested by Alba et al. (2001), would have produced such a
diversity of consistently primitive characters throughout the skeleton.
The extraordinary morphology of the cranium and dentition of Oreopithecus are
probably related to a specialized folivorous adaptation. Oreopithecus molars have
the highest shearing quotients of any hominoid, which is consistent with a highfiber diet (Kay and Ungar 1997). The exceptionally developed chewing muscles of
Oreopithecus, its robust mandibles, and even the small size of its brain are all
consistent with a folivorous diet requiring high-bite forces but relatively little
planning or “extractive foraging” (Begun and Kordos 2004).
Late Miocene East African Hominines?
At the same time that Late Miocene apes are flourishing in Eurasia, two taxa, recognized
from small samples, are known from East Africa. Chororapithecus is recognized from a
small number of isolated teeth from Ethiopia dated to between about 10 and 10.5 Ma
Fossil Record of Miocene Hominoids
1317
(Suwa et al. 2007). They accept, based on molecular clock evidence, that the divergence
of Pongo and the African apes and humans occurred at about 20 Ma, that for Gorilla at
about 12 Ma, and that for Pan and humans at about 9 Ma. These divergence dates are of
course the subject of much discussion. These authors cautiously assign Chororapithecus
to the gorilla clade, suggesting that Chororapithecus represents an early gorilla. The
main line of evidence is a crest revealed by CT scans on the dentine surface of one of the
molars, which the authors suggest is an indication of an adaptation to shearing,
characteristic of gorillas. However, the ridge in question is only present on the dentine
surface and not the surface that would have been in contact with food. Therefore, even if
this dentine crest is homologous with a ridge on the teeth of gorillas, it is very doubtful
that it represents an adaptation to shearing, since it could never have encountered a
single fiber of food (being buried under the enamel cap). At best this crest, if found to be
homologous with a crest on the enamel surface of a gorilla tooth, would be considered
an exaptation and not evidence of selection for a gorilla-like mode of adaptation
suggested by Suwa et al. (2007).
The sample of Chororapithecus is fragmentary, and frankly, if found anywhere
outside of Ethiopia, it would be considered inadequate to support any particular
phylogenetic hypothesis. It is in the right place the right time, according to some
scenarios, but when examined in detail, it fails to demonstrate the presence of a
gorilla at 10 Ma, or even a hominine. The fragmentary nature of these specimens
does not allow for a definitive assignment of Chororapithecus to a hominid clade.
I would not exclude the possibility that it is a late surviving Proconsul.
Another collection of fossils from East Africa is Nakalipithecus, from Kenya, dated
to about 9.8 Ma (Kunimatsu et al. 2007). The sample consists of a fragmentary mandible
and some isolated teeth. Sadly, the teeth in the mandible are highly worn, making it
difficult to use this most complete specimen to assign this taxon to the sister clade to
Ouranopithecus, as suggested by the authors. There is, however, a female upper canine
that does bear a strong resemblance to Ouranopithecus (Kunimatsu et al. 2007). In my
view, Nakalipithecus is more likely to be a hominine and to be related to Eurasian apes
than Chororapithecus. Kunimatsu et al. (2007) suggest that Nakalipithecus, because its
known range is slightly older than the known range of Ouranopithecus, might be
ancestral to the Greek ape. The time difference between the two samples however is
minimal by paleontological standards (9.5 vs. 9.8). Nakalipithecus represents the best
connection in the Late Miocene between Europe and Africa, but there is no good
evidence that Nakalipithecus is ancestral to Ouranopithecus. Given the close ages of
both samples, it cannot be said which is ancestral to which. It remains true, however, that
the earliest hominines are at least 12.5 Ma from Europe, so that whatever the relationship is between Nakalipithecus and Ouranopithecus, the Eurasian taxa came first.
Late Miocene Hominid Extinctions and Dispersals
Hominids first appear in the Middle Miocene of Eurasia and quickly radiate, but
between about 10 and 9 Ma they begin to disappear. The view presented here is that
the hominids from western Eurasia are hominines, and those in the east are
1318
D.R. Begun
pongines (Begun 2004, although see above for an alternative interpretation).
Descendants of each subfamily eventually disperse south of the Tropic of Cancer
as other taxa become extinct in Eurasia (Begun et al. 1997, 2012; Begun 2001,
2004). This view has been supported by genetic evidence (Stewart and Disotell
1998) and criticized based on differing interpretations of the fossil record. For
example, it has been noted that Africa is a more likely place for the origin of the
Hominidae and the Homininae, presumably because African apes still live there and
because it is said to be poorly sampled, especially in the Late Miocene. The fossils
that would support this interpretation remain to be discovered. In fact, many Late
Miocene localities are known from Africa, a number with paleoecological indications
of forested settings (Begun 2001, 2004; Begun et al. 2012), yet no hominines have
ever been identified in Africa dating between Kenyapithecus and Sahelanthropus
apart from Chororapithecus and Nakalipithecus, which, as noted, may be hominines
but are much younger than the earliest European hominines. Samburupithecus is also
present in this time period, but it is even more primitive and less likely to be a
hominine than Chororapithecus and Nakalipithecus. Samburupithecus retains many
primitive dental and maxillary characters (Begun 2001). Isolated teeth from Ngorora
have been described as having affinities primarily with the Proconsuloidea or Middle
Miocene East African hominoids (e.g., Equatorius) (Hill and Ward 1988; Begun
2001; Hill 2002). Pickford and Senut (2005) have recently reported teeth from
Ngorora and Lukeino described as chimpanzee and gorilla-like, but in my view, the
older teeth cannot be distinguished from others with affinities to the Proconsuloidea,
and the younger teeth are probably from Orrorin (see chapter “▶ The Miocene
Hominoids and the Earliest Putative Hominids,” Vol. 3), known from the same
locality (Lukeino) (Senut et al. 2001). Most importantly, an African origin of the
hominines to the exclusion of the European taxa fails to explain the widespread
pattern, from Spain to Hungary, of morphology associating Eurasian apes with those
from Africa. To deny a European origin of the Homininae based on the evidence to
date is to evoke ad hoc hypotheses of convergence or homoplasy to explain away the
documented similarities between dryopithecins and crown hominines. One can
choose not to believe a hypothesis because of an a priori expectation that evidence
disproving it will eventually be found (e.g., Bernor 2007), but in my view, this is not
an acceptable approach to science.
Hominids appear to have moved south from Eurasia in response to global
climate changes that produced more seasonal conditions in Eurasia toward the
end of the Miocene (Quade et al. 1989; Leakey et al. 1996; Cerling et al. 1997;
Begun 2001, 2004, 2009; Fortelius et al. 2006; Agustı́ 2007; Agustı́ et al. 2003;
Nargolwalla 2009) (see Begun et al. (2012) for a comprehensive review of the
evidence of faunal dynamics and climate change in the Late Miocene). Much
evidence exists for climate change throughout much of Eurasia in the Late Miocene, which led to the development of more seasonal conditions. This culminates in
the Messinian Salinity Crisis that led to the desiccation of the Mediterranean basin
at the end of the Miocene (Hs€u et al. 1973; Clauzon et al. 1996; Krijgsman
et al. 1999). Other consequences include the development of Asian monsoons,
desertification in North Africa, the early phases of Neogene polar ice cap
Fossil Record of Miocene Hominoids
1319
expansion, and the expansion of North American grasslands (Garcés et al. 1997;
Hoorn et al. 2000; Zhisheng et al. 2001; Griffin 2002; Guo et al. 2002; Janis
et al. 2002; Liu and Yin 2002; Wilson et al. 2002). In both Europe and Asia,
subtropical forests retreat and are increasingly replaced by more open-country
grasslands and steppes (Bernor et al. 1979; Bernor 1983; Fortelius et al. 1996;
Cerling et al. 1997; Bonis et al. 1999; Magyar et al. 1999; Solounias et al. 1999;
Fortelius and Hokkanen 2001). In some places, forests persisted and elsewhere
more severe changes occurred, creating a number of refugia, some of which
continued to host hominids well into the period of climatic deterioration. This is
the case for the Oreopithecus localities of Tuscany and Sardinia (Harrison and
Rook 1997). Other well-known localities, such as Dorn-D€urkheim in Germany,
retain a strongly forested character, though they lack hominoids (Franzen 1997;
Franzen and Storch 1999).
There is a gradient of extinctions of forest forms from west to east corresponding
to the gradient of appearance of more open-country faunas from east to west
(Bernor et al. 1979; Fortelius et al. 1996, 2001; Begun 2001, 2004). Between
about 12 and 10 Ma, Dryopithecus disappears from localities in Europe, becoming
very rare by 9.5 Ma in Spain and Germany. This wave of extinctions ends coincident with an important faunal event in Western Europe known as the mid-vallesian
crisis, when a major turnover of terrestrial faunas leads to the widespread extinction
of local taxa generally attributed to the development of more open conditions
(Moyà-Solà and Agustı́ 1990; Fortelius et al. 1996). The youngest specimens
possibly attributable to Dryopithecus are the most easterly, currently assigned to
Udabnopithecus from the 8 to 8.5 Ma locality of Udabno in Georgia (Gabunia
et al. 2001).
In the eastern Mediterranean, hominids persist to the end of this time.
Ouranopithecus in Greece is mainly known from the end of the hominid presence
in Europe and may be a terminal taxon of the Dryopithecus clade (Begun and
Kordos 1997). In Anatolia, at the eastern edge of the faunal province that includes
Greece and the eastern Mediterranean (the Greco-Iranian province (de Bonis
et al. 1999)), a very large hominid resembling Ouranopithecus may be as young
as 7–8 Ma in age (Sevim et al. 2001). At this time, forest taxa are increasingly
replaced by more open-country forms. This is true of virtually all mammalian
orders. Among the primates, hominoids decline and cercopithecoids are on the
increase (Andrews et al. 1996). Grazing ungulates and grassland or dry ecologyadapted micromammals also become more common (Fortelius et al. 1996; Agustı́
et al. 1999; de Bonis et al. 1999; Solounias et al. 1999; Agustı́ 2007).
The dispersal of Late Miocene faunas between Eurasia and Africa is complex
and includes both open and more forest-adapted taxa. Among the more opencountry taxa, horses disperse from North America to the Old World, and modern
bovids and giraffids appear to have dispersed from Europe to Africa (Dawson 1999;
Made 1999; Solounias et al. 1999; Agustı́ et al. 2001). Among the more close
setting mammals, hippos move from Africa to Europe, and pigs of varying ecological preferences move from Asia to Europe and Africa (Fortelius et al. 1996; Made
1999). Small carnivores (mustelids, felids, and viverrids), larger carnivores (ursids,
1320
D.R. Begun
hyaenids) porcupines, rabbits, and chalicotheres, most of which also prefer more
closed settings, also disperse from Eurasia to Africa (Leakey et al. 1996; Ginsburg
1999; Heissig 1999; Made 1999; Winkler 2002).
Many of these dispersals involved forest or wetter ecology taxa (hippos, some
suids, primates, carnivores, rodents, and chalicotheres), which is consistent with the
evidence of climate change at that time. There is ample time between 10 and 7 Ma
for the dispersal of forest-adapted taxa between Eurasia and Africa before the onset
of the severe dry spell that culminates in the Messinian, including evidence of forest
corridors and refugia well into the Late Miocene in the Balkans and North Africa
(Pickford et al. 2006; Begun et al. 2012). Taxa disperse south into Africa as
conditions continue to deteriorate leading to the Messinian crisis, among them
probably the ancestors of the African apes and humans. This scenario has hominid
ancestors leave Africa in the Early Miocene and return as hominines in the Late
Miocene, but this is precisely what seems to have occurred in several mammalian
lineages, including those represented by Late Miocene African species of
Orycteropus (aardvark), several small carnivores, the hippo Hexaprotodon, and
possibly the proboscideans Anancus, Deinotherium, and Choerolophodon (Leakey
et al. 1996; Ginsburg 1999; Heissig 1999; Made 1999; Boisserie et al. 2003;
Werdelin 2003; Begun and Nargolwalla 2004).
Conclusion
The Miocene epoch witnesses several adaptive radiations of hominoids and
hominoid-like primates. It was indeed the golden age of the Hominoidea. Many
catarrhines appear in East Africa in the Early Miocene, some of which are surely
related to living hominoids. A few of the basic attributes of the Hominoidea appear
at this time, including the absence of a tail, somewhat extended life history, and a
hylobatid level of encephalization, and hints of powerful hand and foot grips and a
propensity for more vertical climbing. Among the diversity of Early Miocene
Hominidea, a group emerged that may have had an adaptation to a diet dependent
on more embedded resources, leading to a dispersal into Eurasia. Once there,
hominoids flourish and expand, splitting into eastern and western clades that led to
extant hominids (hominines in the west and pongines in the east) and an early
southern clade that becomes extinct. Early in the Late Miocene, the hominid
radiation in Eurasia began to dwindle, with the earliest extinctions occurring in the
west and progressing eastward. Hominids and many other mammals experienced
extinction events at this time, and many clades of Eurasian mammals also dispersed
south, probably as a result of major global climatic events. Western Eurasian
hominines dispersed into Africa, leading to the evolution of the African apes and
humans, and eastern pongines dispersed into Southeast Asia, leading to the appearance of the Pongo clade. Shortly after their dispersal into Africa, hominines diverged
into their respective clades, probably relatively quickly. Gorillas remain the most
conservative in many respects, though they achieve some of the largest body masses
in any primate and specialize in their ability to exploit high-fiber keystone resources.
Fossil Record of Miocene Hominoids
1321
Chimpanzees and humans diverged, possibly within a million years of the emergence of the gorilla clade, the chimp clade remaining relatively conservative and the
human clade experiencing much more rapid and dramatic evolutionary changes.
Human ancestors retain the imprint of their Eurasian and African ape ancestors and
were very probably similar to extant African apes, particularly chimpanzees, that is,
the fossil record of hominoid evolution suggests that humans evolved from a
knuckle-walking, forest-dwelling soft fruit frugivore/omnivore, not a chimpanzee
in the modern sense, but more chimp-like than anything else nonetheless. The details
of the evolutionary events leading to the origin of the individual lineages of the
Homininae remain to be worked out, a process hampered in part by a poor fossil
record that, for example, includes almost no fossil relative of gorillas or chimpanzees (but see McBrearty and Jablonski 2005).
Cross-References
▶ Defining Hominidae
▶ Dental Adaptations of African Apes
▶ Estimation of Basic Life History Data of Fossil Hominoids
▶ Great Ape Social Systems
▶ Hominoid Cranial Diversity and Adaptation
▶ Origin of Bipedal Locomotion
▶ Postcranial and Locomotor Adaptations of Hominoids
▶ Potential Hominoid Ancestors for Hominidae
▶ Role of Environmental Stimuli in Hominid Origins
▶ The Hunting Behavior and Carnivory of Wild Chimpanzees
▶ The Miocene Hominoids and the Earliest Putative Hominids
▶ The Paleoclimatic Record and Plio-Pleistocene Paleoenvironments
▶ Zoogeography: Primate and Early Hominin Distribution and Migration Patterns
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