Fossil apes and human evolution

Abstract

A distinctive ancestor
There has been much focus on the evolution of primates and especially where and how humans diverged in this process. It has often been suggested that the last common ancestor between humans and other apes, especially our closest relative, the chimpanzee, was ape- or chimp-like. Almécija et al. review this area and conclude that the morphology of fossil apes was varied and that it is likely that the last shared ape ancestor had its own set of traits, different from those of modern humans and modern apes, both of which have been undergoing separate suites of selection pressures.
Science , this issue p. eabb4363

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REVIEW SUMMARY
◥
PRIMATE EVOLUTION
Fossil apes and human evolution
Sergio Almécija*, Ashley S. Hammond, Nathan E. Thompson, Kelsey D. Pugh,
Salvador Moyà-Solà, David M. Alba
BACKGROUND: Ever since the writings of Darwin
and Huxley, humans’place in nature relative to
apes (nonhuman hominoids) and the geo-
graphic origins of the human lineage (hom-
inins) have been heavily debated. Humans
diverged from apes [specifically, the chim-
panzee lineage (Pan)] at some point between
~9.3 million and ~6.5 million years ago (Ma),
and habitual bipedalism evolved early in hom-
inins (accompanied by enhanced manipulation
and, later on, cognition). To understand the se-
lective pressures surrounding hominin origins,
it is necessary to reconstruct the morphology,
behavior, and environment of the Pan-Homo
last common ancestor (LCA). “Top-down”ap-
proaches have relied on living apes (especially
chimpanzees) to reconstruct hominin origins.
However, “bottom-up”perspectives from the
fossil record suggest that modern hominoids
represent a decimated and biased sample of a
larger ancient radiation and present alternative
possibilities for the morphology and geography
of the Pan-Homo LCA. Reconciling these two
views remains at the core of the human ori-
gins problem.
ADVANCES: There is no consensus on the
phylogenetic positions of the diverse and widely
distributed Miocene apes. Besides their frag-
mentary record, disagreements are due to the
complexity of interpreting fossil morphologies
that present mosaics of primitive and derived
features, likely because of parallel evolution
(i.e., homoplasy). This has led some authors to
exclude known Miocene apes from the mod-
ern hominoid radiation. However, most re-
searchers identify some fossil apes as either
stem or crown members of the hominid clade
[i.e., preceding the divergence between orang-
utans (pongines) and African great apes and
humans (hominines), or as a part of the modern
great ape radiation]. European Miocene apes
have prominently figured in discussions about
the geographic origin of hominines. “Kenyapith”
apes dispersed from Africa into Eurasia ~16 to
14 Ma, and some of them likely gave rise to
the European “dryopith”apes and the Asian
pongines before 12.5 Ma. Some authors inter-
pret dryopiths as stem hominines and support
their back-to-Africa di spersal in the latest
Miocene, subsequently evolving into modern
African apes and hominins. Others interpret
dryopiths as broadly ancestral to hominids or
an evolutionary dead end.
Increased habitat fragmentation during
the late Miocene in Africa might explain
the evolution of African ape knuckle walking
and hominin bipedalism from an orthograde
arboreal ancestor. Bipedalism might have al-
lowed humans to escape the great ape “special-
ization trap”—an adaptive feedback loop
between diet, specialized arboreal locomotion,
cognition, and life history. However, under-
standing the different selection pressures that
underlie knuckle walking and bipedalism is
hindered by locomotor uncertainties about
the Pan-Homo LCA and its Miocene forebears.
In turn, the functional interpretation of Mio-
cene ape mosaic morphologies is challenging
because it depends on the relevance of prim-
itive features. Furthermore, adaptive complexes
can be co-opted to perform new functions
during evolution. For instance, features that
are functionally related to quadrupedalism or
orthogrady can be misinterpreted as bipedal
adaptations. Miocene apes show that the
orthograde body plan, which predates below-
branch suspension, is likely an adaptation for
vertical climbing that was subsequently co-opted
for other orthograde behaviors, including habit-
ual bipedalism.
OUTLOOK: Future research efforts on hominin
origins should focus on (i) fieldwork in un-
explored areas where Miocene apes have yet
to be found, (ii) methodological advances in
morphology-based phylogenetics and pale-
oproteomics to retrieve molecular data beyond
ancient DNA limits, and (iii) modeling driven by
experimental data that integrates morphological
and biomechanical information, to test locomo-
tor inferences for extinct taxa. It is also impe-
rative to stop assigning a starring role to each
new fossil discovery to fit evolutionary scenar-
ios that are not based on testable hypotheses.
Early hominins likely originated in Africa
from a Miocene LCA that does not match any
living ape (e.g., it might not have been adapted
specifically for suspension or knuckle walk-
ing). Despite phylogenetic uncertainties, fossil
apes remain essential to reconstruct the “start-
ing point”from which humans and chimpan-
zees evolved. ▪
RESEARCH
Almécija et al., Science 372, 587 (2021) 7 May 2021 1of1
The list of author affiliations is available in the full article online.
*Corresponding author. Email: salmecija@amnh.org (S.A.)
Cite this article as S. Almécija et al., Science 372,eabb4363
(2021). DOI: 10.1126/science.abb4363
READ THE FULL ARTICLE AT
https://doi.org/10.1126/science.abb4363
0
5
10
15
20
Million years ago
25
Miocene
Catarrhines: Cercopithecoids and hominoids
Nakalipithecus
Ekembo
Hominids: Great apes and humans
Hominoids: Apes and humans
Hylobatids Pongo Gorilla Pan Homo
“Dryopith” apes
Sivapithecus
Ardipithecus
Nacholapithecus
Old World monkeys
Hominins: The human lineage
?? ??
Chimpanzee-human
last common ancestor
?
Plio-
Pleistocene
The evolutionary history of apes and humans is largely incomplete. Whereas the phylogenetic relationships
among living species can be retrieved using genetic data, the position of most extinct species remains
contentious. Surprisingly, complete-enough fossils that can be attributed to the gorilla and chimpanzee lineages
remain to be discovered. Assuming different positions of available fossil apes (or ignoring them owing to
uncertainty) markedly affects reconstructions of key ancestral nodes, such as that of the chimpanzee-human LCA.
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REVIEW
◥
PRIMATE EVOLUTION
Fossil apes and human evolution
Sergio Almécija
1,2,3
*, Ashley S. Hammond
1,2
, Nathan E. Thompson
4
, Kelsey D. Pugh
1,2
,
Salvador Moyà-Solà
3,5,6
, David M. Alba
3
Humans diverged from apes (chimpanzees, specifically) toward the end of the Miocene ~9.3 million to
6.5 million years ago. Understanding the origins of the human lineage (hominins) requires reconstructing
the morphology, behavior, and environment of the chimpanzee-human last common ancestor. Modern
hominoids (that is, humans and apes) share multiple features (for example, an orthograde body plan facilitating
upright positional behaviors). However, the fossil record indicates that living hominoids constitute narrow
representatives of an ancient radiation of more widely distributed, diverse species, none of which exhibit the
entire suite of locomotor adaptations present in the extant relatives. Hence, some modern ape similarities
might have evolved in parallel in response to similar selection pressures. Current evidence suggests that
hominins originated in Africa from Miocene ape ancestors unlike any living species.
In1871,Darwin(1)speculatedthathumans
originated in Africa based on the anatom-
ical similarities with African apes (gorillas
and chimpanzees) identified by Huxley
(2). However, Darwin urged caution until
more fossils became available—the European
Dryopithecus was the only recognized fossil
ape at the time (3). After 150 years of con-
tinuous discoveries, essential information about
human origins remains elusive owing to debates
surrounding the interpretation of fossil apes
(Figs. 1 and 2).
Genomic data indicate that humans and
chimpanzees are sister lineages (“hominins”
and “panins,”respectively; Box 1) that diverged
from a last common ancestor (LCA) toward the
end of the Miocene, at some point between
~9. 3 million and ~6.5 million years ago (Ma)
(4,5). All extant hominoids (apes and humans)
are characterized by the lack of an external tail,
high joint mobility (e.g., elbow, wrist, hip), and
the possession of an “orthograde”(upright)
body plan, as opposed to the more primitive,
“pronograde”body plan of other anthropoids
and most other mammals (Fig. 2). These body
plans are associated with two different types
of positional (postural and locomotor) behav-
iors: pronograde behaviors, taking place on
nearly horizontal supports with the trunk held
roughly horizontally; and orthograde (or “anti-
pronograde”) behaviors, with the torso posi-
tioned vertically (6,7). Extant ape features also
include enhanced joint mobility, long forelimbs
relative to hindlimbs, and (except gorillas) long
hands with high-to-very-high finger curvature
(8–10). The orthograde body plan is generally
interpreted as a suspensory adaptation (11,12),
or as an adaptation for vertical climbing sub-
sequently co-opted for suspension (13).
Based on similarities between chimpanzees
and gorillas, a prevalent evolutionary model
argues that African apes represent “living
fossils”and that knuckle-walking chimpanzees
closely reflect the morphology and behavior
of the Pan-Homo LCA—the “starting point”
of human evolution (14,15). This working
paradigm also postulates that modern African
apes occupy the same habitats as their ances-
tors (16) (Fig. 1). This assumption is based on a
classical scenario that situates hominin origins
in East Africa, owing to environmental changes
after the rifting of East African Rift Valley during
the Miocene (17). For some, a chimpanzee-like
Pan-Homo LCA could also imply that all extant
ape locomotor adaptations were inherited from
amodernape-likeancestor(18). However, the
fossil record denotes a more complex picture:
Miocene apes often display mosaic morphol-
ogies, and even those interpreted as crown
hominoids do not exhibit all the features
present in living apes (19) (Fig. 3).
The Pan-like LCA model builds on the “East
Side Story”of hominin origins (17), a seriously
challenged scenario. First, it is grounded in
the living-ape geographic distribution, which
may not match that at the time of the Pan-Homo
split (Fig. 1). Second, the model relies on an
outdated account of the fossil record (from
the 1980s), when the earliest known hominin
(Australopithecus afarensis) was recorded in
East Africa, and no possible fossil gorillas and
chimpanzees were known (17). Subsequent
fossil discoveries are incompatible with such
a narrative: Australopithecus remains from
Chad indicate that early hominins were living
~2500kmwestoftheEastAfricanRift~3.5Ma
(20). Furthermore, if Sahelanthropus is a hom-
inin, it would push back the human lineage
presence in north-central Africa to ~7 Ma (21).
Moreover, continued fieldwork efforts in less
explored areas have shown that hominoids
lived across Afro-Arabia during the Miocene
(22–25). In addition, remains of putative hom-
inines have been found in East Africa (26,27),
perhaps even in Europe (28,29). Finally, paleo-
environmental reconstructions for late Miocene
apes and hominins suggest that the Pan-Homo
LCA inhabited woodlands, not tropical rain-
forests (30–33).
Current debates about the transition from
an ape into a bipedal hominin are centered
on the morphological and locomotor recon-
struction of the Pan-Homo LCA, as well as its
paleobiogeography. Discrepancies are caused
by conflicting evolutionary signals among
living and fossil hominoids, indicating rampant
“homoplasy”(independent evolution causing
“false homology”), and are further complicated
by the highly incomplete and fragmentary
nature of the hominoid fossil record. This
review argues that, despite the limitations,
the information provided by fossil apes is
essential to inform evolutionary scenarios of
human origins.
Evidence as to humans’place in nature
Humans’inner primate
Since Linnaeus established modern taxonomy
in 1758 (34) and until the 1960s, morphological
similarity was the main basis for classifying
organisms. Linnaeus included modern humans
(Homo sapiens) within the order Primates, but
it was not until 1863 that Huxley provided
the first systematic review of differences and
similarities between humans and apes (2).
Imagining himself as a “scientific Saturnian,”
Huxley stated that, “The structural differences
between Man and the Man-like apes certainly
justify our regarding him as constituting a
family apart from them; though, inasmuch as
he differs less from them than they do from
other families of the same order, there can be
no justification for placing him in a distinct
order”[(2), p. 104]. Huxley’s work was moti-
vated by widespread claims (e.g., Cuvier, Owen)
that humans’“uniqueness”warranted their
placement in a separate order. Darwin con-
curred with Huxley that humans should be clas-
sified in their own family within primates (1).
We now know that most “human features”
are primitive traits inherited from primate
(e.g., trichromatic stereoscopic vision, manual
grasping) or earlier (e.g., five digits) ancestors
(35). Even humans’distinctively large brains
and delayed maturation are framed within a
primate trend of increased encephalization
and slower life history compared with other
RESEARCH
Almécija et al., Science 372, eabb4363 (2021) 7 May 2021 1of12
1
Division of Anthropology, American Museum of Natural
History (AMNH), New York, NY 10024, USA.
2
New York
Consortium in Evolutionary Primatology at AMNH, New York,
NY 10024, USA.
3
Institut Català de Paleontologia Miquel
Crusafont (ICP), Universitat Autònoma de Barcelona, 08193
Cerdanyola del Vallès, Barcelona, Spain.
4
Department of
Anatomy, New York Institute of Technology (NYIT) College of
Osteopathic Medicine, Old Westbury, NY 11568, USA.
5
Institució Catalana de Recerca i Estudis Avançats (ICREA),
08010 Barcelona, Spain.
6
Unitat d’Antropologia Biològica,
Departament de Biologia Animal, Biologia Vegetal i Ecologia,
Universitat Autònoma de Barcelona, 08193 Cerdanyola del
Vallès, Barcelona, Spain.
*Corresponding author. Email: salmecija@amnh.org
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mammals (35,36). Some differences in brain
size may partly reflect a neocortex enlarge-
ment related to enhanced visual and grasping
abilities (37). Like extant great apes, humans
displaylargerbodysize,larger relative brain
size, a slower life-history profile, and more
elaborate cognitive abilities than other prima-
tes (hylobatids included) (36). However, mod-
ern humans are extreme outliers in terms of
delayed maturation, encephalization, advanced
cognition, and manual dexterity, ultimately
leading to symbolic language and technol-
ogy (38).
Anatomically, only two adaptive complexes
represent synapomorphies present in all hom-
inins: the loss of the canine honing complex
and features related to habitual bipedalism
(33,39). Most anthropoids possess large and
sexually dimorphic canines coupled with body
size differences between males and females,
reflecting levels of agonistic behavior and
sociosexual structure (40). The fossil record
indicates that there was a reduction in canine
height, leading to the loss of the honing com-
plex in early hominins (41). Habitual bipedal-
ism is reflected in several traits across the body
(e.g., foramen magnum position and orienta-
tion; pelvic, lower-back, and lower-limb mor-
phology), present (or inferred) in the earliest
hominins (21,33,42).
Darwin linked the origin of bipedalism with
an adaptive complex related to freeing the
hands from locomotion to use and make tools
(replacing large canines), leading to a reciprocal
feedback loop involving brain size, cognition,
culture, and, eventually, civilization (1). Multi-
ple variants in the order of these events have
been advocated, with the freeing of the hands
alternatively linked to tools (43), food acquisi-
tion and carrying (15), or provisioning within a
monogamous social structure (44), to name a
few. There is general agreement that canine
reduction (including social structure changes),
enhanced manipulative capabilities, and biped-
alism were interrelated during human evolu-
tion. However, determining the order of events
and their causality requires reconstructing the
ape-human LCA from which hominins origi-
nated. Darwin also speculated that humans
and modern African ape ancestors originated
in Africa (1), based on the anatomical similar-
ities identified by Huxley and his own obser-
vations that many living mammals are closely
related to extinct species of the same region.
However, given the limited ape fossil record
at that time, he concluded that it was “useless
to speculate on this subject”[(1), p. 199]. Using
the French Dryopithecus to calibrate his “clock,”
Darwin concluded that humans likely diverged
as early as the Eocene and warned against “the
error of supposing that the early progenitor of
the whole Simian stock, including man, was
identical with, or even closely resembled, any
Almécija et al., Science 372, eabb4363 (2021) 7 May 2021 2of12
Gorilla gorilla
Gorilla beringei
Pan troglodytes
Pan paniscus
Pongo pygmaeus
Pongo abelii
Pongo tapanuliensis Hylobatidae
gorillas chimpanzees orangutans gibbons & siamangs
Miocene ape
region identified
Fig. 1. Extant and fossil ape distribution. Extant apes live in (or nearby)
densely forested areas around the equator in Africa and Southeast Asia. Except for the
recently recognized tapanuli orangutan (which may represent a subspecies of the
Sumatran orangutan), each of the three extant great ape genera presently has two
geographically separated species. The Congo River (highlighted in dark blue) acts as
the current barrier between common chimpanzees (Pan troglodytes) and bonobos
(Pan paniscus). Red stars indicate regions with Miocene sediments (spanning ~23 to
5.3 Ma) where fossil apes have been uncovered. (Some regions may contain more than
one site; contiguous regions are indicated with different stars if they extend over
more than one political zone.) It is possible that modern great ape habitats do not
represent the ancestral environments where the great ape and human clade evolved.
Paleontologically, the vast majority of Africa, west of the Rift Valley, remains highly
unexplored. Extant ape ranges were taken from the International Union for
Conservation of Nature (IUCN Red List). Background image sources: Esri, DigitalGlobe,
GeoEye, i-cubed, USDA FSA, USGS, AEX, Getmapping, Aerogrid, IGN, IGP,
swisstopo, and the GIS user community.
RESEARCH |REVIEW
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existing ape or monkey”[(1), p. 199]. These
ideas inaugurated a century of discussions
about human’s place in nature.
Reaching the “extant”consensus
Until the 1950s, the geographic origin of
hominins was disputed between Africa, Asia,
and Europe. After the publication of Darwin’s
On the Origin of Species (45), Haeckel predicted
that the “missing link”(dubbed “Pithecanthropus,”
the “ape-man”)wouldbefoundinAsia
(46). This idea led to Dubois’1891 discovery of
Homo erectus in Indonesia (47). In 1925, Dart
published the discovery of Australopithecus
africanus,“the man-ape from South Africa”
(48). However, the scientific community still
focused on Europe because of the Piltdown
“fossils,”until they were exposed as a hoax (49).
Asia remained a “mother continent”contender
owing to the “man-like ape”Ramapithecus,
discovered in the Indian Siwaliks (50).
During this time, the relationships of humans
to other primates were highly contentious.
Most authors advocated an ancient divergence
of humans from apes (51,52) or favored a
closer relationship to the great apes than to
the lesser apes (53,54). A few proposed that
Almécija et al., Science 372, eabb4363 (2021) 7 May 2021 3of12
pronogradeorthograde
thorax and lumbar vertebra
(cranial view)
A
Pan
Homo
Gorilla
Pongo
hylobatid
Ardipithecus
~4.4 Ma
Oreopithecus
~7 Ma
Hispanopithecus
~9.6 Ma
Pierolapithecus
~12 Ma
Nacholapithecus
~15 Ma
fossil hominoids
extant hominoids
B
Fig. 2. Pronograde versus orthograde body plan. (A) Macaque (above)
and chimpanzee (below) in typical postures, showing general differences
between pronograde and orthograde body plan characteristics. In comparison
to a pronograde monkey, the modern hominoid orthograde body plan is
characterized by the lack of an external tail (the coccyx being its vestigial
remnant), a ribcage that is mediolaterally broad and dorsoventrally shallow,
dorsally placed scapulae that are cranially elevated and oriented, a shorter
lower back, and long iliac blades. Modern hominoids have higher ranges
of joint mobility, such as the full elbow extension shown here, facilitated by a
short ulnar olecranon process. The inset further shows differences in lumbar
vertebral anatomy, including more dorsally situated and oriented transverse
processes in orthograde hominoids. (B) Representatives of each extant
hominoid lineage (left column) show different postural variations associated
with an orthograde body plan. The orthograde body plan facilitates bipedal
walking in modern humans and different combinations of arboreal climbing
and below-branch suspension in apes. Knuckle walking in highly terrestrial
African apes is seen as a compromise positional behavior superimposed onto
an orthograde ape with long forelimbs relative to the hindlimbs. Associated
skeletons of fossil hominoids (right column) show that an orthograde body
can be disassociated from specific adaptions for suspension (e.g.,
Pierolapithecus exhibits shorter and less curved digits than Hispanopithecus).
Other fossil apes exhibit primitive “monkey-like”pronograde body plans
with somewhat more modern ape-like forelimbs (e.g., Nacholapithecus).
Approximate age in millions of years ago is given to representative fossils
of each extinct genus: Ardipithecus (ARA-VP-6/500), Nacholapithecus
(KNM-BG35250), Pierolapithecus (IPS21350), Hispanopithecus (IPS18800),
and Oreopithecus (IGF 11778). Silhouettes of extant and fossil skeletons are
shownataboutthesamescale.
RESEARCH |REVIEW
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humans were more closely related to one or
both of the African apes (55,56), although
these views were not widely accepted (57).
These alternative phylogenetic hypotheses
heavily affected reconstructions of the LCA.
Some (e.g., Schultz, Straus) advocated for a
“generalized”ape ancestor (52), whereas others
relied on extant hominoid models. Notably,
Keith developed a scenario in which a “hylobatian”
brachiating stage preceded an African ape-
like creature: a knuckle-walking “troglodytian”
phase immediately preceding bipedalism (11).
Focused on Keith’s“hylobatian”stage, Morton
proposed that the “vertically suspended pos-
ture”of a small-bodied hylobatid-like an-
cestor caused the erect posture of human
bipedalism (12). Gregory, another prominent
“brachiationist,”supported similar views (53).
Morton argued that knuckle walking did not
represent an intermediate stage preceding
bipedalism but rather a reversion toward
quadrupedalism in large-bodied apes specialized
for brachiation. At that time, “brachiation”was
used for any locomotion in which the body was
suspended by the hands. Now, it refers to the
pendulum-like arm-swinging locomotion of
hylobatids (6).
By the 1960s, the Leakeys’discoveries in
Tanzania [e.g., Paranthropus boisei (58), Homo
habilis (59)] reinforced the relevance of Africa
in human evolution, which became firmly es-
tablished as the “mother continent”with the
A. afarensis discoveries during the 1970 s (60,61).
LCA models still centered on the available fossil
apes (mostly represented by jaw fragments and
isolated teeth) accumulated after decades of
paleontological fieldwork in Africa and Eurasia.
In 1965, Simons and Pilbeam (62)revised
and organized available Miocene apes in three
genera: Dryopithecus,Gigantopithecus,and
Ramapithecus. The genus Sivapithecus was
included in Dryopithecus,consideredthean-
cestor of African apes, whereas Ramapithecus
was considered ancestral to humans based on
its short face (and inferred small canines) (63).
Leakey (64) and others agreed with Simons
and Pilbeam that humans belong to their own
family (Hominidae, or “hominids”), whereas
great apes would belong to a distinct family
(Pongidae, or “pongids”). He also agreed that
Ramapithecus was an Asian early human an-
cestor. However, Leakey proposed reserving
the genus Sivapithecus for the “Asian dryopith-
ecines”and claimed that the human lineage
couldbetracedbackto,atleast,themiddle
Miocene of Africa with Kenyapithecus wickeri
(~14 Ma).
Two major “revolutions”in the study of
evolutionary relationships started in the 1960s.
First, a series of studies jump-started the field
of molecular anthropology: Blood protein com-
parisons by Zuckerkandl et al.(65) and Good-
man (66)foundthatsomegreatapes—gorillas
and chimpanzees—were more closely related to
humans than to orangutans. Sarich and Wilson
developed an “immunological molecular clock”
and concluded that African apes and humans
share a common ancestor as recent as ~5 Ma
(67). These results led to decades-long debates
regarding the African ape–human split. For
example, Washburn resurrected extant Afri-
can apes as ancestral models in human evolu-
tion, proposing knuckle walking as the precursor
of terrestrial bipedalism (68). By contrast, pale-
ontologists argued that the molecular clock was
inaccurate because of the much older age of the
purported human ancestors Kenyapithecus and
Ramapithecus (69). Second, Hennigian cladistics
(“phylogenetic systematics”), which only rec-
ognizes “synapomorphies”(shared derived
features) as informative for reconstructing
phylogeny (70), became slowly implemented
in anthropology by the mid-1970s (71).
In the 1970s and 1980s, the relationships
among gorillas, chimpanzees, and humans were
still disputed. Chromosomal comparisons (72),
DNA hybridization (73), and hemoglobin se-
quencing (74) supported a closer relationship
between chimpanzees and humans, whereas
morphology-based cladistics recovered gorilla-
chimpanzee as monophyletic (75). In the late
1980s, the first single-locus DNA sequencing
studies (76), followed in the 1990s with multiple
loci analyses, finally resolved the “trichotomy”
(77). Current genomic evidence indicates that
humans are more closely related to chimpan-
zees (5), having diverged at some time between
~9.3and~6.5Ma(4). Ever since “the molecular
revolution,”the perceived relevance of fossil
apesinhumanevolutionhasbeeninjeopardy.
African apes as time machines?
Extant African apes have been considered
ancestral models since Keith’s“troglodytian”
stage in the 1920s (11), and especially since
the 1960s, with updated hypotheses inspired
by the “molecular revolution”(68,78)andfield
discoveriesonchimpanzeebehaviorbyGoodall
(79). Leakey played a central role in promoting
Goodall’s pioneering research (subsequently
fostering Fossey’s research in gorillas and
Galdikas’s research in orangutans). Now, a
prominent paradigm proposes that chimpan-
zees represent “living fossils”that closely de-
pict the Pan-Homo LCA (14,16). This model
combines molecular data with the anachro-
nistic view that Gorilla and Pan are morpho-
logically similar (75). Under these assumptions,
knuckle walking, once used to defend African
ape monophyly (80), is used to argue that
African apes are morphologically “conservative”
and only display size-related differences (14).
This model contends that gorillas are allomet-
rically enlarged chimps and that chimpanzees
[or bonobos (78)] constitute a suitable model for
the Pan-Homo LCA, perhaps even the hominine
or hominid LCAs (14). This narrative also in-
corporates the paleobiogeographic assumption
Almécija et al., Science 372, eabb4363 (2021) 7 May 2021 4of12
Box 1. Simplified taxonomy of extant primates. The adjectives “lesser”and “great”refer to the
smaller size of the former relative to great apes and human group, not to old evolutionary notions based
on the Scala Naturae. Given that some apes are more closely related to humans than to other
apes, the word “ape”is a gradistic term used here informally to refer to all nonhominin hominoids.
Finally, the taxonomic convention used (the most common), does not reflect that panins and
hominins are monophyletic [although some do; e.g., (169)].
Order Primates
Suborder Strepsirrhini (non-tarsier “prosimians”: lemurs, galagos and lorises)
Suborder Haplorrhini (tarsiers and simians)
Infraorder Tarsiiformes (tarsiers)
Infraorder Simiiformes (or Anthropoidea: simians or anthropoids)
Parvorder Platyrrhini (New World monkeys)
Parvorder Catarrhini (Old World simians)
Superfamily Cercopithecoidea (Old World monkeys)
Superfamily Hominoidea (apes and humans)
Family Hylobatidae (“lesser apes”: gibbons and siamangs)
Family Hominidae (“great apes”and humans)
Subfamily Ponginae (the orangutan lineage)
Genus Pongo (orangutans)
Subfamily Homininae (the African ape and human lineage)
Tribe Gorillini (the gorilla lineage)
Genus Gorilla (gorillas)
Tribe Panini (the chimpanzee lineage)
Genus Pan (common chimpanzees and bonobos)
Tribe Hominini (the human lineage)
Genus Homo (humans)
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that African apes likely occupy the same hab-
itats as their ancestors: Without new selection
pressures, there was no need for evolution.
If hominins originated from a chimpanzee-
like LCA, human bipedalism must have evolved
from knuckle walking (15), a functional com-
promise enabling terrestrial travel while retain-
ing climbing adaptations (80). Under this view,
bipedal hominins originated from an ancestor
that was already terrestrial while traveling.
Theseconclusionsarelogicalfroma“top-down”
perspective, based on the evidence provided by
extant hominoids and early hominins. However,
a fully informed theory of hominin origins must
also apply a “bottom-up”approach (81,82), from
the perspective of extinct apes preceding the
Pan-Homo split. It is also essential to clarify
whether chimpanzees represent a good ances-
tral model for the Pan-Homo LCA. Unfortu-
nately, the view from the bottom is blurry.
The tangled branches of ape evolution
The fossil ape dilemma: Homoplasy and
mosaic evolution
With more than 50 hominoid genera and a
broad geographic distribution (Fig. 1), the
Miocene has been dubbed “the real planet of
the apes”(83). Besides their fragmentary
nature, a persistent challenge is understand-
ing the phylogenetic relationships among fossil
apes, which exhibit mosaics of primitive and
Almécija et al., Science 372, eabb4363 (2021) 7 May 2021 5of12
Fig. 3. Phylogenetic relation-
ships among living hominoids
and chronostratigraphic
ranges of fossil hominoids. A
time-calibrated phylogenetic tree
of living hominoids is depicted
next to the spatiotemporal ranges
of the fossil hominoids mentioned
in the text. Fossil taxa are color
coded based on possible phyloge-
netic hypotheses. The vertical
green dashed line indicates that
there is a continuity in the African
fossil ape record. However,
currently, it is sparse between
~14 and 10 Ma. Robust and lasting
phylogenetic inferences of apes
are difficult, in part, because of
the fragmentary nature of the
fossil record and probable high
levels of homoplasy. Many
Miocene ape taxa are represented
only by fragmentary dentognathic
fossils, and the utility of mandibles
and molars for inferring phylogeny
in apes has been questioned.
Another area of uncertainty
relates to the position of many
early and middle Miocene African
apes relative to the crown
hominoid node. The discovery or
recognition of more complete
early Miocene fossil hylobatids
would help resolve their position
and, thus, what really defines the
great ape and human family.
Splitting times are based on the
molecular clock estimates of
Springer et al.(168) (hominoids
and hominids) and Moorjani et al.
(4), which are more updated for
hominines and Pan-Homo.
Silhouettes are not to scale.
Shaded boxes represent geo-
graphic distributions (green is
Africa, gold is Europe, and purple
is Asia).
05 Million years ago101520
Miocene
Pleistocene
Pliocene
Pan–Homo
LCA
stem
hominoids
stem hominids
stem hominines
crown hominines
crown hominids
crown hominoids
stem hominoids
or stem hominids
stem hominoids
stem hominids
or stem pongines
or stem hominines
hominins
hominins
or other hominines
incertae sedis
ponginesstem hominines
Morotopithecus
Kenyapithecus
Equatorius
Nacholapithecus
Chororapithecus
Dryopithecus
Pierolapithecus
Hispanopithecus
Rudapithecus
Nakalipithecus
Graecopithecus
Sivapithecus
Ankarapithecus
Lufengpithecus
Gigantopithecus
Oreopithecus
Sahelanthropus
Orrorin
Ardipithecus
Pongo
Australopithecus
Ournaopithecus
Griphopithecus
Homo
Pan
Gorilla
Hylobatidae
Ekembo
Samburupithecus
Danuvius
Otavipithecus
“dryopiths”
Khoratpithecus
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derived features with no modern analogs. The
Asian Miocene ape Sivapithecus best exempli-
fies this complexity. Discoveries during the
1970s and 1980s, including a facial skeleton
(84), clarified that Ramapithecus is a junior
synonym of Sivapithecus, which is likely related
to orangutans (85). However, two Sivapithecus
humeri show a primitive (pronograde-related)
morphology, calling into question the close
phylogenetic link with Pongo that had been
inferred from facial similarities (86).
The root of this “Sivapithecus dilemma”
(18)isidentifyingwhere“phylogenetic signal”
is best captured in hominoids: the postcranium
or the cranium? The former implies that a
Pongo-like face evolved independently twice;
the latter entails that some postcranial sim-
ilarities among living apes evolved more than
once. Both hypotheses highlight the phyloge-
netic noise that homoplasy introduces in
phylogenetic inference. Indeed, several studies
have found that homoplasy similarly affects
both anatomical areas (87). The conclusion
that Sivapithecus is not a pongine relies on
the assumption that suspensory adaptations
and other orthograde-related features present
in living hominoids were inherited from their
LCA (18). However, this is contradicted by
differences among living apes [e.g., forelimb
andhandanatomy,degreeoflimbelongation,
hip abduction capability (8,9,19,80,88–91)].
These studies concluded that apparent sim-
ilarities could represent independently evolved
biomechanical solutions to similar locomotor
selection pressures. For instance, hand length
“similarities”among living apes result from
different combinations of metacarpal and/or
phalangeal elongation in each extant genus (9).
Parallel evolution—homoplasy among closely
related taxa due to shared genetic and devel-
opmental pathways—could explain some post-
cranial similarities related to suspensory
behaviors among extant apes (80). Compared
with convergences among distantly related
taxa, parallelisms are more subtle and difficult
to detect and they readily evolve when similar
selection pressures appear. Within extant pri-
mates, suspensory adaptions evolved indepen-
dently in atelines and between hylobatids and
great apes (8,80,88,91,92). When the hom-
inoid fossil record is added, independent evo-
lution of suspensory adaptations has been
inferred, too, for orangutans, chimpanzees,
and some extinct lineages (9,89,93,94).
Knuckle walking has also been proposed to
have different origins in gorillas and chimpan-
zees (80,93,95). As for suspension, the pre-
existenceofanorthogradebodyplan,vertical
climbing, and general arboreal heritage could
have facilitated the independent evolution of
knuckle walking to circumvent similar bio-
mechanical demands during terrestrial quad-
rupedalism while preserving a powerful grasping
hand suitable for arboreal locomotion (9).
The possibility of parallelisms indicates that
ancestral nodes in the hominoid evolutionary
tree, including the Pan-Homo LCA, cannot be
readily inferred without incorporating fossils.
In addition, fossils from “known”evolutionary
lineagesarecommonlyusedtocalibratemole-
cular clocks despite being subject to consid-
erable uncertainty (4). Even worse, relatively
complete fossil apes undisputedly assigned
to early members of the gorilla and chim-
panzee lineages remain to be found.
Counting crowns: The case of the European
Miocene apes
Sivapithecus and other fossil Asian great apes
(e.g., Khoratpithecus,Ankarapithecus,Lufeng-
pithecus) are generally considered pongines
(Fig. 3) based on derived craniodental traits
shared with Pongo (94,96–98), although
alternative views exist, particularly for Lufeng-
pithecus (99). By contrast, the phylogenetic
positions of apes from the African early (e.g.,
Ekembo,Morotopithecus) and middle Miocene
(Kenyapithecus, Nacholapithecus,Equatorius)
remain very controversial. Like Sivapithecus,
they exhibit only some modern hominoid fea-
tures superimposed onto a primitive-looking
pronograde (“monkey-like”) body plan (Fig. 2).
Some authors interpret this mosaicism as
indicating that most Miocene apes do not
belong within the crown hominoid radiation
and, thus, are irrelevant to reconstructions
of the Pan-Homo LCA (14). This is likely the
case for early Miocene African taxa. However,
the vertebrae of Morotopithecus [~20 Ma (100)
or ~17 Ma (101)] display orthogrady-related
features absent from other stem hominoids,
indicating either a closer relationship with
crown hominoids or an independent evolution
of orthogrady (102). In turn, Kenyapithecus and
Nacholapithecus arecommonlyregardedas
preceding the pongine-hominine split owing
to the possession of some modern hominid
craniodental synapomorphies combined with
a more primitive postcranium than that of
living great apes (94,103). This raises the
question: Can some Miocene apes belong to
the crown hominid clade despite lacking many
of the features shared by extant great apes?
The large-bodied apes from the middle-to-
late Miocene of Europe are at the center of
discussions about great ape and human evolu-
tion (19,28,94,104,105). Named after Dryopi-
thecus (3), they are generally distinguished as a
subfamily (Dryopithecinae) (94) or tribe (Dry-
opithecini) (28). However, it is unclear if they
constitute a monophyletic group or a para-
phyletic assemblage of stem and crown hom-
inoids (94). Thus, we refer to them informally
as “dryopiths.”These apes are dentally con-
servative, but each genus exhibits different
cranial and postcranial morphology. The dry-
opith fossil record includes the oldest skeletons
that consistently exhibit postcranial features of
living hominoids (orthograde body plan and/
or long and more curved digits). Dryopithecus
(~12 to 11 Ma) is known from craniodental
remains and isolated postcranials that are too
scarce to reconstruct its overall anatomy (106).
By contrast, Pierolapithecus (~12 Ma) is re-
presented by a cranium with an associated
partial skeleton (19). Cranially a great ape, its
rib, clavicle, lumbar, and wrist morphologies
are unambiguous evidence of an orthograde
body plan. Yet, unlike chimpanzees and orangu-
tans (but similar to gorillas), Pierolapithecus
lacks specialized below-branch suspensory adap-
tations [see discussion in (10)]. The recently
described Danuvius (~11.6 Ma, Germany), and
the slightly younger (~10 to 9 Ma) Hispanopi-
thecus (Spain) (105)andRudapithecus (Hungary)
(28) represent the oldest record of specialized
below-branch suspensory adaptations (e.g., long
and strongly curved phalanges; Fig. 2). Danuvius
has also been argued to show adaptations to
habitual bipedalism (but see below).
The different mosaic morphology exhibited
by each dryopith genus is a major challenge
for deciphering their phylogenetic relation-
ships (Fig. 3). Current competing phyloge-
netic hypotheses consider dryopiths as stem
hominoids (107,108), stem hominids (94,96,109),
or crown hominids closer to either pongines
(105), hominines (28), or even hominins (29,110).
However, recent phylogenetic analyses of apes
recovered dryopiths as stem hominids (97,109),
perhaps except Ouranopithecus (~9 to 8 Ma)
and Graecopithecus (~7 Ma) (97). Ouranopi-
thecus has been interpreted by some as a stem
hominine, or even as a crown member more
closely related to the gorilla or human lineages
(110). Graecopithecus has also been advocated
as a hominin (29), although the fragmentary
available material hinders evaluation of this
hypothesis. Such contrasting views about
dryopiths stem from their incomplete and
fragmentary fossil record coupled with per-
vasive homoplasy. However, because these
factors are equal for all researchers, their
differentconclusionsmustalsorelatetoana-
lytical differences (e.g., taxonomy, sampling,
polymorphic and continuous trait treatment).
Therootoftheconflictistheremarkabledif-
ferences in subjective definition and scoring of
complex morphologies (e.g., “incipient supra-
orbital torus”).
Paleobiogeography of the African ape and
human clade
One hundred fifty years after Darwin specu-
lated that modern African ape and human
ancestors originated in Africa, possible hom-
inins have been found as far back as the latest
Miocene of Africa (21,33,111): Sahelanthropus
(~7 Ma), Orrorin (~6 Ma), and Ardipithecus
kadabba (~5.8 to 5.2 Ma). However, others
question the feasibility of identifying the ear-
liest hominins among the diverse Miocene apes
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(96,112). Puzzlingly, despite some claims based
on scarce remains (113–115), ancient represen-
tatives of the gorilla and chimpanzee lineages
remain elusive. Some apes from the African late
Miocene—Chororapithecus (26), Nakalipithecus
(27), and Samburupithecus (116)—have been
interpreted as hominines, but the available
fragmentary remains preclude a conclusive as-
sessment. Furthermore, Samburupithecus is
likely a late-occurring stem hominoid (97,117).
During the middle Miocene (~16.5 to 14 Ma),
apes are first found “out of Africa.”These
are the genera Kenyapithecus (Turkey) and
Griphopithecus (Turkey and central Europe).
We informally refer to them as the “kenyapiths”
because there is no consensus on their rela-
tionships (28,94,118). Kenyapiths indicate
that putative stem hominids are first recorded
in Eurasia and Africa before the earliest record
of both European dryopiths and Asian pon-
gines at ~12.5 Ma (94). Paleobiogeographical
and paleontological data suggest that kenya-
piths dispersed from Africa into Eurasia as
one of the multiple catarrhine intercontinental
dispersal events occurred during the Miocene
(e.g., hylobatids, pliopithecoids) (83,94). Al-
though some competing evolutionary scenarios
agree that kenyapiths gave rise to dryopiths in
Europe, the phylogenetic and geographic origin
of hominines remains contentious (28,94).
If dryopiths are stem hominids, they could
either be close to the crown group or con-
stitute an evolutionary dead end, an indepen-
dent “experiment”not directly related to either
pongines or hominines. Alternatively, dryo-
piths might be crown hominids more closely
related to one of these groups. If dryopiths
are hominines, this implies that the latter
could have originated in Europe and subse-
quently dispersed “back to Africa”during the
late Miocene (28,29,83). This would coincide
with vegetation structure changes caused by
a trend of increased cooling and seasonality
(32) that ultimately drove European apes to
extinction [or back to Africa (28)]. In this
scenario, hominines and pongines would be
vicariant groups that originally evolved in
Europe and Asia, respectively, from early kenya-
pith ancestors. Given the suspensory specializa-
tions of late Miocene dryopiths (Hispanopithecus
and Rudapithecus), if modern African apes
originated from these forms, this scenario im-
plies that the hominine ancestor could have
been more reliant on suspension than living
chimpanzees or gorillas. The claim that homi-
nines originated outside of Africa may be
justified by cladistic analyses recovering dry-
opiths as stem hominines but may not be
based on the lack of late Miocene great apes
in Africa because fossils from this critical time
period have been discovered (~13 to 7 Ma)
(Fig. 3). Both molecular and paleontological
evidence (e.g., Sivapithecus) situate the pongine-
hominine divergence within the middle Mio-
cene. Hence, the debate cannot be settled with-
out more conclusively resolving the phylogenetic
relationships of middle Miocene dryopiths.
An alternative scenario proposes a vicariant
divergence for hominines and pongines from
kenyapith ancestors but favors the origin of
hominines in Africa (94,119). It argues for a
second vicariant event between European
dryopiths and Asian pongines soon after the
kenyapith dispersal into Eurasia. Cladistically,
dryopiths would be pongines but would share
none of the currently recognized pongine auta-
pomorphies, evolved after the second vicariant
event. This scenario is difficult to test, but it
would be consistent with the apparent absence
of clear pongine synapomorphies in Lufengpi-
thecus (99) and the more derived nasoalveolar
morphology of Nacholapithecus (103) com-
pared with some dryopiths (106). However, it
would imply even higher levels of homoplasy,
including the independent acquisition of an
orthograde body plan in Africa and Eurasia
from pronograde kenyapith ancestors.
A third possibility is that none of the taxa
discussed above are closely related to the African
ape and human clade (107). Under this view,
bona fide extinct nonhominin hominines have
yet to be found in largely unexplored regions
of Africa, explaining the virtual lack of a gorilla
and chimpanzee fossil record. According to
Pilbeam, paleoanthropologists could be “like
the drunk looking for his keys under the
lamppost where it was light rather than where
he had dropped them, working with what we
had rather than asking whether or not that
was adequate”[(108), pp. 155–156]. Africa is
a huge continent, and most paleontological
discoveries are concentrated in a small portion
of it. The greatest challenge is finding hominoid-
bearing Mio-Pliocene sites outside East and
South Africa, even though we know they exist
(20–22).Besidesinsufficientsamplingef-
fort, this is hindered by numerous impedi-
ments to fieldwork in most of Africa, including
geopolitical conflicts, restricted land use devel-
opment, lack of suitable outcrops (due to
extensive vegetation cover), and taphonomic
factors [tropical forests do not favor fossil
preservation (120)].
A Miocene view of (Miocene) hominin origins
Evolution in motion
The decades-long feud regarding arboreality
and bipedalism in A. afarensis exemplifies the
complexity of inferring function from anat-
omy. “Totalist”functional morphologists rely
on a species’“total morphological pattern”(121)
to infer its locomotor repertoire. Totalists see a
bipedalearlyhomininwithsomeape-likereten-
tions (e.g., curved fingers) pointing to con-
tinued use of the trees and consider that certain
not-yet-human-like features (e.g., hip) indicate
a different type of bipedalism (122). Instead,
“directionalists”—for whom functional infer-
ences are only possible for derived traits
evolved for a specific function—focus exclu-
sively on bipedal adaptations (123). Totalist
and directionalist interpretations of the fossil
record differ in the “adaptive significance”at-
tributed to primitive features, which result in
different behavioral reconstructions. Two other
related factors further complicate locomotor
inferences in extinct species: First, different
positional behaviors have similar mechanical
demands [e.g., bipedalism, quadrupedalism and
some types of climbing (39)]. Second, preexisting
morphofunctional complexes originally selected
to fulfill a particular function (adaptations)
can be subsequently co-opted for a new role
(exaptations).
The mosaic nature of hominoid morpho-
logical evolution makes the functional recon-
struction of fossil apes especially challenging,
as recently exemplified by Danuvius (104): It
was described as possessing long and curved
fingers, a long and flexible vertebral column,
hip and knee joints indicative of extended
postures, and an ankle configuration align-
ing the foot perpendicular to the long axis of
the tibia. Such a combination of features was
functionally interpreted as indicating below-
branch suspension combined with above-branch
bipedalism.However,acritiquetotheoriginal
study concluded that the morphological affin-
ities of Danuvius with modern great apes support
a positional repertoire that includes orthogrady
and suspension, but not bipedalism (124). Part of
the “problem”with the original interpretation is
that it infers a derived locomotor behavior—
bipedalism—from primitive features that are
also functionally related to quadrupedalism.
For instance, the inferred “long-back”morphol-
ogy of Danuvius is characteristic of most quadru-
pedal monkeys and other Miocene apes (125),
denoting the lack of trunk specialization seen
in extant great apes. The Danuvius femoral
head joint, being (primitively) posterosuper-
iorly expanded (126), is consistent with flexed
quadrupedal hip postures that are not used
during human-like bipedalism. In addition,
the distal tibia configuration of Danuvius is
shared with Ekembo and cercopithecoids (104),
thus being likely plesiomorphic and not unique
to bipeds. When the primitive and derived
features of Danuvius are considered, a totalist
would argue that it combined high degrees of
plesiomorphic quadrupedal locomotion with
novel (suspensory) behaviors, whereas a direc-
tionalist would downplay the primitive fea-
tures in favor of the newly derived adaptive
traits (i.e., suspension).
The late Miocene Oreopithecus (~7 Ma, Italy)
is another example of conflicting phylogenetic
and functional signals. Phylogenetic interpre-
tations of Oreopithecus include cercopithecoid,
stem hominoid, and hominid (even hominin)
status (127). However, current phylogenetic anal-
yses suggest that Oreopithecus could represent
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a late-occurring stem hominoid (97,128), with
postcranial adaptations to alternative types of
orthogrady, such as forelimb-dominated behav-
iors (129) and terrestrial bipedalism (130).
Even if not directly related to hominins (or
modern hominoids), the locomotor adapta-
tions of Oreopithecus, and other Miocene apes,
are worthy of further research to understand
the selection pressures that led to the (inde-
pendent) emergence of modern hominoid posi-
tional behaviors.
To distinguish true locomotor adaptations
from exaptations, current research efforts focus
on plastic “ecophenotypic”traits, potentially
denoting how fossil hominoids were actually
moving. Bone is a living tissue, and growth is
expected to occur in predictable ways that
reflect loading patterns throughout life (131).
Thus, cross-sectional and trabecular bone prop-
erties and their links to behavior are widely
investigated (132,133). Yet, experimental studies
indicate that internal bone morphology does not
necessarily match stereotypical loading patterns
(134). Ample evidence suggests that irregular
loading, even in low magnitude, can be more
osteogenically potent than stereotypical load-
ing (135). This may bias interpretations of
individual fossils with a species-atypical load-
ing pattern during life (e.g., because of an
injury). Bone (re)modeling also does not con-
sistently occur in response to changes in load-
ing pattern: It can occur in ways that detract
from, rather than enhance, function (136)
and may manifest differentially across the
skeleton (137). Incongruence also exists be-
tween actual bone performance and expecta-
tions based on aspects of internal morphology
(138). Finally, there is a strong genetic com-
ponent to the responsiveness of bone (re)model-
ing to loading (136), which is largely unknown
for most species. The confidence with which
internal bone structures can be used to retrodict
behavior in fossil species remains a work in
progress.
Before bipedalism
Competing hypotheses about the locomotor
behavior immediately preceding hominin
bipedalism include terrestrial knuckle walking
(15), palmigrade quadrupedalism (93), and dif-
ferent types of arboreal (orthograde) behaviors
such as climbing and suspension (7), vertical
climbing (139), or arboreal bipedalism and
suspension (104,140). Miocene great apes can
enlighten this question by helping to identify
the polarity of evolutionary change preceding
the Pan-Homo divergence (81,82). For in-
stance, if Pierolapithecus is interpreted as an
orthograde ape without specific suspensory
adaptations but retaining quadrupedal adap-
tations [see alternatives in (10)], then the ortho-
gradebodyplanandulnocarpalcontactloss
could be interpreted as an adaptation to verti-
cal climbing, subsequently co-opted for suspen-
sion (19). Similarly, habitual bipedalism might
have directly evolved from other orthograde
behaviors without an intermediate stage of
advanced suspension or specialized knuckle
walking. Hence, Pierolapithecus complements
previous hypotheses that biomechanical aspects
of the lower limb during quadrupedalism and
vertical climbing could be functionally “pre-
adaptive”for bipedalism (39,139).
A holistic view indicates that the Pan-Homo
LCA was a Miocene ape with extant great ape–
like cognitive abilities, likely possessing a
complex social structure and tool traditions
(36,38,141). This ape would exhibit some
degree of body size and canine sexual dimor-
phism (with large honing male canines) (15),
indicating a polygynous sociosexual system (40).
BasedonMioceneapesandearliesthominins,
it is also likely that the Pan-Homo LCA was
orthograde and proficient at vertical climb-
ing [see alternative interpretation based on
Ardipithecus (33,93)], but not necessarily
adapted specifically for below-branch suspen-
sion or knuckle walking (9,33). Chimpanzees
seem to retain the Pan-Homo LCA plesio-
morph ic condition in some regards [e.g., brain
and body size (38), vertebral counts (125), foot
morphology (142)]. However, in others [e.g.,
interlimb (93), hand (9), pelvis (143) length
proportions; femur morphology (89)], early
hominins are more similar to generalized Mio-
cene apes. These results further reinforce the
idea that functional aspects of other locomo-
tor types were co-opted for bipedalism during
hominin origins.
The “East Side Story”scenario links the
divergence of chimpanzees and humans to
the rifting of East Africa, which would have
triggered a vicariant speciation event from the
ancestral Pan-Homo LCA (17). Chimpanzees
would have remained “frozen in time”in their
ancestral tropical forest environment, whereas
humans would be the descendants of the
group “left behind”ontheeastsideoftheRift.
Major climate and landscape changes would
have then forced the earliest hominins to adapt
to more open (grassland savanna) environ-
ments by acquiring bipedalism—and the rest
is history. Several decades after the proposal
of this scenario, where do we stand?
The landscape of East Africa has dramati-
cally changed during the past 10 million years
because of tectonic events leading to specific
climatic conditions and associated changes
in vegetation structure, from mixed tropical
forest to more heterogeneous and arid envi-
ronments than elsewhere in tropical Africa
(144,145). The trend of progressive aridifica-
tion did not culminate in the predominance of
savanna environments until ~2.0 Ma—roughly
coinciding with hominin brain size increase
and the appearance of H. erectus—and was
punctuated by alternating episodes of extreme
humidity and aridity, resulting in a fluctuating
extension of forests through time (144,145).
Despite ongoing discussions about early hom-
inin paleoenvironments (woodland with forest
patches versus wooded savanna) (146), evi-
dence from Miocene apes (30,31) supports
that the Pan-Homo LCA inhabited some kind
ofwoodland.Therefore,ithasbeensuggested
that the Pan-Homo LCA was probably more
omnivorous than chimpanzees (ripe fruit spe-
cialists) and likely fed both in trees and on the
ground (33), in agreement with isotopic analy-
ses for Ardipithecus ramidus (41).
Bipedalism would have emerged because of
the selection pressures created by the progres-
sive fragmentation of forested habitats and
the need for terrestrial travel from one feeding
patch to the next. Data on extant ape positional
behaviors (Fig. 4) suggest that hominin terres-
trial bipedalism originated as a posture rather
than a means of travel on the ground (147)or
in trees (140). Rose (39) proposed a long process
of increasing commitment to bipedality in the
transition to more complex open habitats
throughout the Plio-Pleistocene, and Potts (148)
argued that key stages in hominin evolution
mayrelatetoadaptiveresponsestocopewith
highly variable environments. The fossil and
archaeological records provide a new twist
to the order of evolutionary events in early
hominin evolution. The remains of Orrorin
and Ar. ramidus indicate that habitual terres-
trial bipedalism, enhanced precision grasping,
and loss of canine honing evolved at the dawn
of the human lineage well before brain enlarge-
ment (9,33,89,93). It was not until later in
time [maybe starting with Australopithecus
(149) and continuing with Homo], that some
preexisting hand attributes were co-opted for
purposive and systematic stone toolmaking
in more encephalized hominins with more
advanced cognitive abilities (38,150).
The specialization trap
That hominins continuously evolved since
the Pan-Homo LCA is universally accepted,
but the possibility that all living hominoids
(including chimpanzees) experienced their
own evolutionary histories is sometimes dis-
regarded. Potts (151) suggested that the greater
cognitive abilities of great apes originated to
continue exploiting fruit supplies from densely
forested environments in front of strong envi-
ronmental variability. Coupled with locomotor
adaptations (e.g., vertical climbing, suspension)
enabling an efficient navigation through the
canopy, this “cognitive trap”would consist of
an adaptive feedback loop between diet, loco-
motion, cognition, and life history. Although
hominids originated approximately during
the “Mid-Miocene Climatic Optimum”(~17 to
15 Ma), their subsequent radiation from ~14 Ma
onward paralleled a trend of climatic “deterio-
ration”during the rest of the Miocene (152).
Great apes might have initially thrived by
Almécija et al., Science 372, eabb4363 (2021) 7 May 2021 8of12
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evolving particular adaptations to more ef-
ficiently exploit their habitats, thereby occupy-
ing new adaptive peaks without abandoning
the same area of the adaptive landscape
broadly occupied by earlier stem hominoids.
Nevertheless, this evolutionary strategy would
become unsustainable once a particular paleo-
environmental threshold was surpassed. This
could explain the fate of European dryopiths,
which survived for some time under sub-
optimal conditions (despite the progressive
trend of cooling and increased seasonality)
until they vanished (94).
The dietary, locomotor, and cognitive spe-
cializations of late Miocene great apes would
have hindered their shift into new adaptive
peaks suitable for the more open environ-
ments toward the latest Miocene (153). The
Miocene planet of the apes gave way to the time
of the more generalist Old World monkeys,
enabling their survival in a wider variety of
seasonal habitats (30,92,154).Thesamespe-
cialization trap can explain the delayed retreat
of pongines (and hylobatids) to southeastern
Asia throughout the Plio-Pleistocene. The high-
ly specialized orangutans remain extant, but
not for long because their habitat continues to
shrink. African apes could have partially over-
come the specialization trap by evolving (per-
haps in parallel) semiterrestrial adaptations—
knuckle walking. Gorillas also expanded their
dietary range (more folivorous) and enlarged
their body size. Contrary to the view that go-
rillas are “enlarged”chimpanzees, morphomet-
ric analyses indicate that gorillas underwent
their own evolutionary history, resulting in
different ontogenetic trajectories (155,156)
and postcranial differences that cannot be ex-
plained by size-scaling effects (9,143). Why,
when, and how many times knuckle walking
evolved is more difficult to explain than the
origin of hominin bipedalism. Habitat frag-
mentation coupled with a higher reliance on
arboreal feeding might be invoked (i.e., knuckle
walking serves both terrestrial and arboreal
locomotion). This idea is difficult to reconcile
with the premise that continuous-canopy forests
covered the tropical belt of central and west-
ern Africa since the Miocene, unless gorillas
and chimpanzees evolved in less densely for-
ested habitats (30,31,114) and retreated to
tropical forests when outcompeted by homi-
nins and/or cercopithecoids. Ironically, the same
specializations that allowed great apes to survive
despite major environmental challenges since
thelateMiocenemightultimatelydoomthem
to extinction.
Hominins might have escaped the great-ape
specialization trap by evolving novel and
more radical adaptations: bipedalism (another
specialized orthograde locomotion), concomi-
tant freeing of the hands, and subsequent en-
hanced manual dexterity, brain configuration,
sociosexual behavior, and culturally mediated
technology. Human evolution also reflects the
progressive adaptation (biological first, cultural
later) to ever-changing environments (39,148).
Some essential changes (upright posture, en-
hanced cognition) are just the continuation
of a trend started in Miocene hominoids
(19,36,151). While escaping from the great
ape specialization trap, humans might have
fallen into another evolutionary cul-de-sac,
with current human activities and overpopu-
lation leading the biosphere to a point beyond
return (157). Will humans escape their own
specialization trap?
Conclusions and perspectives
Fossils uniquely inform deep-time evolution-
ary studies, which is essential to plan for the
future (158). However, we must be aware of the
many existing limitations and the gaps in our
knowledge. For example, we need more fossils
becausewearelikelymissingvastlymorethan
what we have. More fieldwork is necessary to
find fossil apes close to the gorilla or chimpanzee
lineages, and it is essential to extend such efforts
to unexplored or undersampled areas (Fig. 1).
It is also essential to continue developing tools
of phylogenetic inference. Bayesian approaches
are promising, but uncertainty remains about
their applicability to morphological data (159).
Improvements in the treatment of continuous
characters and recent methodological advances
for analyzing three-dimensional geometric mor-
phometric data within a cladistic framework
(in combination with traditional characters)
are promising for reconstructing fossil homi-
noid phylogeny (160). The oldest (recently
retrieved) ancient DNA is ~1 Ma (161). Paleo-
proteomics could be a complementary solu-
tion because it has enabled sampling further
back in time up to ~2 Ma, recently confirming
Almécija et al., Science 372, eabb4363 (2021) 7 May 2021 9of12
hylobatids Pongo GorillaPan
Homo
terrestrial
cercopithecoids
??
comparable data
not available
extant models
chimpanzee–human
last common ancestor
quadrupedalism
suspension
leaping
vertical climbing
bipedal standing
bipedal walking
0
5
10
15
20
25
30
% total positional repertoire
Fig. 4. The positional repertoire preceding human bipedalism. Although one particular behavior can
dominate the locomotor repertoire of a given species, the full positional repertoire (postural and locomotor
behaviors) of living primates is diverse, complex, and not fully understood. For example, some locomotor
behaviors are not totally comparable (e.g., monkey quadrupedalism versus African ape knuckle walking).
Furthermore, comprehensive data are not yet available for some extant hominoids (e.g., Gorilla). Bipedalism
did not appear de novo in hominins; it existed as a posture or locomotion within a broader Miocene
ape positional repertoire. The combined evidence of Miocene apes and early hominins indicate that the
locomotor repertoire of the Pan-Homo LCA likely included a combination of positional behaviors not
represented among living primates. Over time, bipedal behaviors became the predominant activity within the
repertoire of early hominins (and knuckle walking in the chimpanzee lineage). Locomotor behaviors (plus
bipedal standing) in each taxon represent percentages of total positional behavior repertoire. (The full
repertoire is not shown; hence, these do not add to 100%.) Data were taken from (92). Quadrupedalism
includes Hunt’s categories “quadrupedal walk”and “quadrupedal run,”suspension includes “suspensory,”
“brachiate,”“clamber,”and “transfer.”The locomotor repertoire compositions of the LCA and modern humans
(Homo) are conjectural, for illustrative purposes.
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the pongine status of Gigantopithecus (162).
Future technological advances in paleoproteo-
mics could potentially help to answer key
questions by retrieving paleoproteomes from
Miocene apes.
Locomotor reconstructions of the Pan-Homo
LCA and other fossil hominoids are seriously
hampered by the lack of current analogs.
Washburn spotted the fundamental limitation:
“It is not possible to bring the past into the
laboratory. No one can see a walking Austra-
lopithecus”[(163), p. 67]. Such inferences rely
on morphofunctional assumptions of bone,
joint, or muscle function, but experimentally
derived biomechanical data are required to
test these assumptions and provide reliable
inferences from fossils. Technological advances
now facilitate noninvasive kinematic data col-
lection from animals in their natural envi-
ronments (164). In turn, experimental and
morphological information should be integrated
to better predict the locomotion of fossil
hominoids. Forward dynamic simulations offer
a powerful pathway for predicting de novo
movements in fossil species while iterating pos-
sible effects of morphology and soft tissue (165).
Humans are storytellers: Theories of human
evolution often resemble “anthropogenic nar-
ratives”that borrow the structure of a hero’s
journey to explain essential aspects such as the
origins of erect posture, the freeing of the
hands, or brain enlargement (166). Intrigu-
ingly, such narratives have not drastically
changed since Darwin (166). We must be aware
of confirmation biases and ad hoc interpreta-
tions by researchers aiming to confer their new
fossil the starring role within a preexisting
narrative. Evolutionary scenarios are appeal-
ing because they provide plausible explana-
tions based on current knowledge, but unless
grounded in testable hypotheses, they are no
more than “just-so stories”(167).
Many uncertainties persist about fossil apes,
and the day in which the paleobiology of
extinct species can be undisputedly recon-
structed is still far away. However, current dis-
agreements regarding ape and human evolution
would be much more informed if, together
with early hominins and living apes, Miocene
apes were also included in the equation. This
approach will allow us to better discern primi-
tive and derived traits, the common from the
specific, or the unique. This is the role of fossil
apes in human evolution.
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ACKNO WLEDG MENTS
We thank the many colleagues that motivated and shaped this
review through their own work on the “Miocene ape-hominin
transition.”In particular, we highlight the decades-long work of
P. Andrews, D. Begun, B. Benefit, T. Harrison, B. Jungers, J. Kelley,
O. Lovejoy, L. MacLatchy, M. Nakatsukasa, M. McCrossin,
M. Pickford, D. Pilbeam, B. Senut, J. Stern, C. Ward, and T. White.
E. Delson and S. Catalano provided constructive criticisms on an
earlier version of the manuscript. K. Younkin assisted by making
Fig. 2. Funding: This research has been funded by the Agencia
Estatal de Investigación (CGL2016-76431-P and CGL2017-82654-P,
AEI/FEDER EU) and the Generalitat de Catalunya (CERCA
Programme and consolidated research groups 2017 SGR 86 and
2017 SGR 116 GRC). Competing interests: The authors declare no
competing interests.
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Fossil apes and human evolution
Sergio Almécija, Ashley S. Hammond, Nathan E. Thompson, Kelsey D. Pugh, Salvador Moyà-Solà and David M. Alba
DOI: 10.1126/science.abb4363
(6542), eabb4363.372Science
, this issue p. eabb4363Science
selection pressures.
different from those of modern humans and modern apes, both of which have been undergoing separate suites of
morphology of fossil apes was varied and that it is likely that the last shared ape ancestor had its own set of traits,
review this area and conclude that theet al.closest relative, the chimpanzee, was ape- or chimp-like. Almécija
process. It has often been suggested that the last common ancestor between humans and other apes, especially our
There has been much focus on the evolution of primates and especially where and how humans diverged in this
A distinctive ancestor
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