ArticlePDF Available

Fossil hominin shoulders support an African ape-like last common ancestor of humans and chimpanzees

Authors:

Abstract and Figures

Reconstructing the behavioral shifts that drove hominin evolution requires knowledge of the timing, magnitude, and direction of anatomical changes over the past ∼6–7 million years. These reconstructions depend on assumptions regarding the morphotype of the Homo–Pan last common ancestor (LCA). However, there is little consensus for the LCA, with proposed models ranging from African ape to orangutan or generalized Miocene ape-like. The ancestral state of the shoulder is of particular interest because it is functionally associated with important behavioral shifts in hominins, such as reduced arboreality, high-speed throwing, and tool use. However, previous morphometric analyses of both living and fossil taxa have yielded contradictory results. Here, we generated a 3D morphospace of ape and human scapular shape to plot evolutionary trajectories, predict ancestral morphologies, and directly test alternative evolutionary hypotheses using the hominin fossil evidence. We show that the most parsimonious model for the evolution of hominin shoulder shape starts with an African ape-like ancestral state. We propose that the shoulder evolved gradually along a single morphocline, achieving modern human-like configuration and function within the genus Homo. These data are consistent with a slow, progressive loss of arboreality and increased tool use throughout human evolution.
Content may be subject to copyright.
Fossil hominin shoulders support an African ape-like
last common ancestor of humans and chimpanzees
Nathan M. Young
a,1
, Terence D. Capellini
b,c
, Neil T. Roach
b,d
, and Zeresenay Alemseged
e
a
Department of Orthopaedic Surgery, University of California, San Francisco, CA 94110;
b
Department of Human Evolutionary Biology, Harvard University,
Cambridge, MA 02138;
c
Broad Institute of MIT and Harvard University, Cambridge, MA 02142;
d
Division of Anthropology, American Museum of Natural
History, New York, NY 10024; and
e
Department of Anthropology, California Academy of Sciences, San Francisco, CA 94118
Edited by Richard G. Klein, Stanford University, Stanford, CA, and approved August 12, 2015 (received for review June 9, 2015)
Reconstructing the behavioral shifts that drove hominin evolution
requires knowledge of the timing, magnitude, and direction of
anatomical changes over the past 67 million years. These re-
constructions depend on assumptions regarding the morphotype
of the HomoPan last common ancestor (LCA). However, there is
little consensus for the LCA, with proposed models ranging from
African ape to orangutan or generalized Miocene ape-like. The
ancestral state of the shoulder is of particular interest because it
is functionally associated with important behavioral shifts in hom-
inins, such as reduced arboreality, high-speed throwing, and tool
use. However, previous morphometric analyses of both living and
fossil taxa have yielded contradictory results. Here, we generated
a 3D morphospace of ape and human scapular shape to plot evo-
lutionary trajectories, predict ancestral morphologies, and directly
test alternative evolutionary hypotheses using the hominin fossil
evidence. We show that the most parsimonious model for the
evolution of hominin shoulder shape starts with an African ape-
like ancestral state. We propose that the shoulder evolved gradu-
ally along a single morphocline, achieving modern human-like con-
figuration and function within the genus Homo. These data are
consistent with a slow, progressive loss of arboreality and in-
creased tool use throughout human evolution.
geometric morphometrics
|
developmental simulation
|
phylomorphospace
|
scapula
|
rotator cuff
The human shoulder exhibits a unique combination of traits
for a primate, a fact that has complicated previous attempts
to reconstruct both its functional and evolutionary history. No-
tably, humans are most closely related to knuckle-walking/sus-
pensory chimpanzees and bonobos (Pan or panins) (1, 2), yet
morphometric analyses suggest that our shoulders are most
similar in shape to that of the highly arboreal, quadrumanous
orangutan (Pongo)(35). The hominin fossil record is similarly
complicated. Scapular remains attributed to Australopithecus
afarensis are described as similar to Gorilla (68) whereas the
more recent Australopithecus sediba (MH2) displays morphom-
etric affinities to both African apes (gorillas, chimpanzees, and
bonobos) and Pongo (9). This mix of character states raises the
question of whether modern human morphology reflects evolu-
tion from a more derived African ape morphology or retention of
primitive traits from an earlier ape ancestor.
A critical piece of evidence for solving this puzzle is the
morphotype of the homininpanin last common ancestor (LCA)
(67 Mya). Although the fossil record near the hypothesized
divergence time with Pan is the most direct means of addressing
what the anatomy of the LCA shoulder was like, both hominin
and African ape fossils from this time period are rare, frag-
mentary, and poorly understood (10, 11). Despite these diffi-
culties, competing hypotheses about the LCA make explicit and
mutually exclusive predictions of the direction, magnitude, and
ordering of character transformations that we should observe in
the fossil record. Moreover, the likelihood of these alternative
hypotheses can be directly tested using the better characterized
later hominin fossil record. Specifically, given alternative ancestral
conditions, one can model the associated evolutionary trajectories
and intermediate states connecting them to the descendant pop-
ulations and test how well these predictions fit the available
fossil evidence.
Two hypotheses of the LCA postcranial morphotype have
been proposed, both requiring different selection pressures and
levels of homoplasy. In the first scenario, a number of anatomical
and locomotor traits shared among closely related African apes
are thought to be homologous (1214) and represent the an-
cestral state of the LCA from which early hominins evolved
[an African ape(AA) model] (15). In particular, panins are
thought to be phenotypically conservative and thus a useful, if
imperfect, proxy for the anatomy and positional behavior of our
shared LCA (1) (Fig. 1A). In the second scenario, the mosaicism
that characterizes the known fossil ape record (e.g., refs. 1619)
supports the argument that many living ape similarities are not
homologies (20); thus the ancestral morphotype for both apes
and humans [i.e., the Miocene ape ancestor(MAA)] would
reflect a more primitive, generalized postcranial morphotype and
positional behavior [an ape convergence(AC) model]. For
example, some have argued from differences in African ape wrist
morphology that knuckle walking behaviors evolved in parallel
(21, 22), in which case the LCA must be more primitive. Thorpe
et al. (23, 24) used similar reasoning to assert that hominins did
not evolve from a knuckle-walking LCA, but rather one that
practiced the hand-assisted, arboreal bipedality observed in liv-
ing orangutans (Fig. 1B). Lovejoy et al. (25) noted that many
features of the early hominin Ardipithecus ramidus do not re-
semble African apes and argued that this difference was evidence
Significance
Knowing the direction and pace of evolutionary change is
critical to understanding what selective forces shaped our an-
cestors. Unfortunately, the human fossil record is sparse, and
little is known about the earliest members of our lineage. This
unresolved ancestor complicates reconstructions of what be-
havioral shifts drove major speciation events. Using 3D shape
measurements of the shoulder, we tested competing evolu-
tionary models of the last common ancestor against the fossil
record. We found that a sustained shift in scapular shape oc-
curred during hominin evolution from an African ape-like an-
cestor to a modern human-like form, first present in our genus,
Homo. These data suggest a long, gradual shift out of the trees
and increased reliance on tools as our ancestors became more
terrestrial.
Author contributions: N.M.Y., T.D.C., and N.T.R. designed research; N.M.Y., T.D.C., N.T.R.,
and Z.A. performed research; Z.A. contributed new reagents/analytic tools; N.M.Y. ana-
lyzed data; and N.M.Y., T.D.C., N.T.R., and Z.A. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
1
To whom correspondence should be addressed. Email: nathan.m.young@gmail.com.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1511220112/-/DCSupplemental.
www.pnas.org/cgi/doi/10.1073/pnas.1511220112 PNAS Early Edition
|
1of6
ANTHROPOLOGY
of a cautious, above-branch, arboreal LCA, more similar to early
quadrupedal Miocene apes like Proconsul than the orthograde
and suspensory crown taxa (26) (Fig. 1C).
To test these alternative evolutionary models of the HomoPan
LCA, we used Procrustes-based geometric morphometrics methods
to summarize the major sources of 3D variation and covariation in
the shape of one structural component of the shoulder, the scapula.
When combined with a phylogenetic hypothesis (Fig. 1D), the
resulting phylomorphospaceprovides explicit predictions about
the evolutionary trajectories connecting hypothesized ancestral and
descendant populations, associated character state transformations,
and proposed ancestral conditions (27), which we tested against the
hominin fossil record. Our results demonstrate that many seemingly
contradictory results from previous analyses are both predictable
outcomes of how scapula morphospace is occupied and consistent
with our understanding of how scapular shape is linked to function.
Moreover, they suggest explicit alternative development hypotheses
that provide a basis for future attempts to validate phylogenetic
models in human evolution.
Results
We first performed a principal components analysis (PCA) of
scapula shape and found that the majority of hominoid variation
(75%) is partitioned along three axes that discriminate taxa,
have biological/functional relevance, and are meaningful above
random error (Fig. 2 ADand Fig. S1). The first axis (PC1) is
associated with the angle of the scapular spine and glenoid rel-
ative to the vertebral border of the blade, which is near per-
pendicular in MAA proxies and Pongo but has a more cranial
orientation in African apes and hylobatids. More perpendicular
spines tend to be longer and the blade wider, accounting for
almost all of their covariation (Fig. S2). The second axis (PC2)
distinguishes the superiorly projecting vertebral and superior
borders and relatively large supraspinous fossa in African apes
from a superior border parallel to the spine and a smaller
supraspinous in the MAA proxies, Pongo, and hylobatids. As in
previous analyses (3, 4), Homo does not significantly overlap with
any primate but instead resides in a unique position that combines
primitive quadrupedalcharacteristics like a long, robust scapular
spine that is perpendicular to the vertebral border (similar to
Nasalis,Lagothrix,andPongo, but further lateralized) with a blade
shape more typical of African apes. The third axis primarily dis-
tinguishes Gorilla and Pongo from all other taxa and is associated
with a scapular blade that is medio-laterally wider than accounted
for by PC1 alone (Fig. S3).
We next reconstructed the predicted ancestral states by
mapping the trees for each alternative phylogenetic scenario in
the comparative morphospace (Fig. 2 Eand Fand Fig. S1 Aand
B). Both the AA and AC trees locate the basal hominoid node,
reflecting the common ancestral morphotype of apes, in a region
consistent with hypothesized MAA proxies (Nasalis and Lago-
thrix) and similar to Pongo. Only close sister taxa overlap in the
first two axes of this morphospace, confirming that hominoids do
not share a common suspensoryshoulder morphology (20, 28).
However, these trees otherwise differ in the magnitude and lo-
cation of homoplasy required.
In the AA model, a direct path from Pan to Homo predicts
changes in the apportionment of the fossae and associated blade
width as orientation of the spine became more perpendicular
relative to the vertebral border and the glenoid more inferiorly
positioned (Fig. S1Aand Movie S1). Interestingly, this vector
passes through a Gorilla-like morphospace and the inferred
African ape LCA along PC1. This arrangement predicts that
ancestral hominins shared the common African ape blade shape
and spine angle with Gorilla but lacked the further expansion of
the vertebral border and supraspinous found in this large African
ape. The phylomorphospace reconstruction is largely concordant
with this vector, predicting that the common ancestor of African
apes and humans was similar to Pan in blade shape, but with a
less angulated spine and wider blade as in Gorilla. This tree
therefore requires one instance of homoplasy to explain simi-
larities between Pan and gibbons in glenoid/spine angulation
whereas Gorilla exhibits an independent expansion of the
supraspinous from a generalized African ape morphotype. In this
Pongo
Gorilla
Pan
Australo
MAA
Hylo
Homo
A
Arboreal, Suspensory?
Brachiator
Quadrumanous
“African ape”
Terrestrial Biped
Wrangham & Pilbeam (2001) Thorpe & Crompton (2007)
Pongo
Gorilla
Pan
Australo
MAA
Hylo
Homo
Arboreal, Quadruped (AQ)
Brachiator
Arboreal Biped, Cautious Climber
Knuckle-walker
Terrestrial Biped
BLovejoy et al. (2009)
Pongo
Gorilla
Pan
Ardi
???
Hylo
Homo
Brachiator
Quadrumanous
Knuckle-walker
Terrestrial Biped
C
DAfrican Ape (”AA”)
Symphalangus
Pongo
P. paniscus
Au. sediba
MAA
Hylobates
Ho. neander.
Ho. ergaster
Au. afarensis
Gorilla
P. troglodytes
Ho. sapiens
Ape Convergence (”AC”)
Symphalangus
Pongo
P. paniscus
Au. sediba
MAA
Hylobates
Ho. neander.
Ho. ergaster
Au. afarensis
Gorilla
P. troglodytes
Ho. sapiens
E
Symphalangus
Pongo
P. paniscus
Au. sediba
MAA
Hylobates
Ho. neander.
Ho. ergaster
Au. afarensis
Gorilla
P. troglodytes
Ho. sapiens
AQ, “Multigrade”?
Fig. 1. Alternative models of the homininpanin last common ancestor (LCA). The branching pattern of living apes as inferred from genomic data is agreed
upon; however, reconstruction of ancestral nodes differs among researchers. (A) In the African ape (AA) model, hominins derive from a knuckle-walking
African ape-like LCA, typically conceived of as chimpanzee-like. (Band C) Ape convergence (AC) models hypothesize that the LCA is either a more generalized
great ape or an unknown primitive ancestral Miocene ape. AQ, arboreal quadrupedalism. (Dand E) Phylogenetic trees used to model these differences, with
evolution from a common morphotype represented by a polytomy. Hominin phylogeny based on ref. 58.
2of6
|
www.pnas.org/cgi/doi/10.1073/pnas.1511220112 Young et al.
scenario, both Pongo and hylobatids retain the primitive blade
shape in which the superior border more closely parallels the spine,
with the gibbons independently evolving a more cranial spine and
glenoid position with associated narrowing of the blade.
In contrast, the evolutionary vector reconstructed from either an
MAA proxy or a Pongo-like LCA to humans predicts that hominins
would be convergent on African apes in blade shape whereas the
more inferior orientation of the spine and glenoid is derived from a
similar condition in the MAA (Fig. S1Band Movie S2). The phy-
lomorphospace analysis reconstructs a different path in which the
basal hominoid node is intermediate in both blade shape and spine
angulation relative to all extant apes. In this case, the AC model
requires three independent episodes of convergence between hu-
mans, panins, and Gorilla in blade shape and two independent
events to explain convergence between Pongo and hylobatids, as
well as the previously mentioned convergence in spine angulation
predicted by the AA model for panins and hylobatids.
Consistent with the AA model, we found that, when fossil taxa
were included in the analysis (Fig. 2B), australopithecines are
intermediate between panins and Homo whereas all hominins
are arranged in a roughly temporal/phylogenetic gradient from
older and more primitive species (A. afarensis) to younger
(A. sediba) and/or more derived species (Homo ergaster,Homo
neanderthalensis)(Fig. S4). Developmental simulations under a
range of hypothetical ontogenetic vectors on average growthe
juvenile A. afarensis in the direction of a more African ape-like
blade shape along PC2 (Fig. 2 CE). These data suggest that
some of the resemblance of the A. afarensis juvenile to Pongo and
MAA blade shape is attributable to the fact that, in all anthro-
poids, younger individuals tend to be wider and have less
developed fossae (29), consistent with PC2. As measured by
Procrustes distance, A. afarensis simulations are most similar in
shape to Gorilla and Nasalis (Table S1 and Fig. S5), the former
of which is consistent with previous analyses (6, 8). However, the
evolutionary vector from Pan to australopithecines and humans
passes underneathand not throughthe space occupied by
Gorilla in the second and third axes of the PCA and canonical
variates analysis (CVA). This simple, linear trajectory is consis-
tent with evolution from either a more Pan-like LCA or a gen-
eralized African ape, both consistent with the AA model. Both
H. ergaster and H. neanderthalensis are located in a hyper-human
location in morphospace, which is due to both a spine angle that
is lateralized (PC1), and the cranial orientation of the vertebral
border above the suprascapular notch (PC2). This difference
may reflect natural variability because both H. ergaster and
H. neanderthalensis are located within the 90% frequency ellipses
of the modern human sample (Fig. S2D). Alternatively, modern
humans have subsequently experienced changes in supraspinous
size and spine angulation due to selection, random drift, or a
combination of both.
Discussion
By calculating evolutionary vectors through scapula shape mor-
phospace and testing these models against a better characterized
fossil record, we found that the course of hominin shoulder evolu-
tion is consistent with the AA model predictions. Specifically, fossil
Hylobates Pongo Pan Gorilla Ho. sapiens
Au. afarensis
DIK 1-1 (r)
Ho. ergaster
KNM -
WT15000 (r)
Fossil Hominin
Ho.neander.
Kebara 2 (r)
Au. sediba
MH2 (r)
a.m. Ho.sapiens
Qafzeh 9 (r)
DIK 1-1 •
Pongo
DIK 1-1 •
Pan
DIK 1-1 •
MAA (Nasalis)
DIK 1-1 •
Gorilla
HomoAustralopithecus
Extant
E
Principal Component 1 (47.3% Variation)
Principal Component 2 (18.8% Variation)
-0.10 0.00 0.10 0.20
-0.10 0.00 0.10
Au. afarensis
Au. sediba
Ho.ergaster
Gorilla
Bonobo
Chimp
Siamang
Gibbon
Orang
Lagothrix
Nasalis
Human
D
Ho.neander.
C
F
Au.afarensis
Au.sediba
H.ergaster
African
Apes
Gibbons
MAA
Orang Human
H.neander.
ROOT
Au.afarensis
Au.sediba
H.ergaster
African
Apes
Gibbons
MAA
Orang
Human
H.neander.
ROOT
B
A
Fig. 2. Comparative and evolutionary scapula shape morphospace. (Aand B) Representative hominoid scapulae and fossil hominins, shown scaled to
identical vertebral border length. (C) Developmental simulations of DIK 1-1 (A. afarensis) using growth vectors from alternate proposed LCA morphotypes.
(Top) Simulations. (Bottom) Simulations with DIK 1-1 scapula overlay (transparent blue), scaled to the same size to highlight shape differences. (D) PC1 and -2
morphospace with mean specimen warped along each axis to show associated shape changes. PC1 describes orientation of the spine relative to the blade
whereas PC2 describes differences in the borders of the supraspinous fossa. Dashed arrows show the direct evolutionary vector from hypothetical an-
cestral states (AA, African ape mean; AC, MAA mean) to modern humans. Points, individual specimens; dark ellipses, 90% confidence interval (CI) of the
mean; light ellipses, 90% CI of the sample; red points, DIK 1-1 developmental simulations. (Eand F) Phylogenetic reconstruction for the AA (tree length =
0.085, P<0.0001) and AC (tree length =0.100, P<0.0001) models illustrates alternative predictions for branching patterns and ancestral states within the
morphospace.
Young et al. PNAS Early Edition
|
3of6
ANTHROPOLOGY
hominins occupy a region of scapula morphospace that is in-
termediate between African apes and modern humans and are
arranged in a temporal gradient consistent with their inferred
phylogenetic position (Fig. S4 AD). These data strongly support
a model in which the modern human shoulder evolved from an
African ape-like LCA via long-term, directional selection on a
single but integrated trait: a longer and more lateralized config-
uration of the spine and glenoid mapped onto a shared African
ape blade shape (Fig. 3). This result implies that previously noted
similarities of the human shoulder to quadrupedal apes and Pongo
are convergent. This interpretation is not only more parsimonious
than evolution from a generalized, quadrupedal LCA morphotype,
but is also consistent with functional explanations for the evolution
of this suite of traits in the hominin lineage and our current un-
derstanding of scapular morphogenesis and development.
These conclusions assume that reconstructed morphospaces
accurately capture potential variation and that ancestral states
can be reasonably estimated by phylogenetic reconstruction
within them. In the former, the concordance of our results with
previous analyses (e.g., ref. 29) suggests that the major contrib-
utors to primate scapula shape are contained within a few in-
tegrated variables, and therefore fossil primates are unlikely to
deviate markedly from this pattern. In the latter, there is no a
priori reason to believe that species evolve along the most direct
path between states. But in either case, these assumptions are
testable, particularly because homoplasy would be reflected by
species occupying a similar morphospace that their common an-
cestor did not. In this regard, both the AA and AC models infer that
homoplasy has occurred in the living ape shoulder but differ in
when and where convergence occurred.
The most evolutionarily labile trait in the scapula is the angle of
the spine and glenoid relative to the vertebral border, with Pan and
hylobatids at one extreme and humans at the other. In both trees,
the reconstruction of ancestral states suggests that spine angulation
is a highly evolvable trait prone to convergence. The arrangement of
hominins in a temporal sequence along this axis further corrobo-
rates that spine angle can evolve in a continuous manner in-
dependently of other scapular anatomy, consistent with what is
known of spine development (see below). In contrast, blade shape
better reflects phylogenetic relationships because humans are sim-
ilar to African apes, which together differ from the inferred prim-
itive pattern found in hylobatids, Pongo, and the MAA proxies. The
AA model reconstructs a single event to evolve African ape blade
morphology whereas the AC model predicts an intermediate an-
cestor to all apes that subsequently radiated into the living hominoid
lineages. In the case of African apes and humans, if there is no
functional association with the supraspinous shape, it is not obvious
what selective forces drove this convergence. The supraspinous
morphology of African apes, and particularly Gorilla, is thought to
be a compromise that enables stabilization of the shoulder joint
against shear forces generated during quadrupedal knuckle walking
while retaining the dorsal position that enhances climbing (30). If
this functional interpretation were correct, then any argument for
homoplasy among African apes and hominins in this trait would
imply that all three independently evolved knuckle walking.
Although the AA model is more parsimonious than the AC
model, ancestral state reconstruction of the African ape node does
not overlap either extant species. This result leaves open the
question of whether australopiths are similar to Gorilla because they
approximate the ancestral African ape morphotype or whether they
reevolvedthis generalized condition from a more Pan-like
shoulder. Although the ancestral state reconstruction supports a
generalized African ape ancestor, there are reasons to prefer a
more Pan-like condition. Notably, many morphological differences
between Pan and Gorilla are associated with body size (13, 31, 32),
and early hominin body size is comparable with the chimpanzee
(33). Body size is also strongly linked to social structure; thus, any
reconstruction invoking a Gorilla-like body size would also have
additional implications beyond the skeletal phenotype (e.g., multi-
male, multifemale in Pan troglodytes vs. a single male, multifemale
group in Gorilla) (15). Regardless, if the LCA was more Pan-like,
then early hominins reevolved a Gorilla-like spine/glenoid angle, but
if more Gorilla-like, then the more cranial angle in Pan is a later
evolutionary event convergent on some hylobatids, perhaps due to
increased arborealism relative to the ancestral African ape. Absent
fossil representatives of either Pan or Gorilla lineages, it is not
possible to discriminate these alternatives.
The correspondence of the current hominin fossil record to
both the AA evolutionary vector and the phylomorphospace, as
well as the magnitude of the phenotypic shift and the relatively
short timeframe over which it occurred, are all strong circum-
stantial evidence that these changes were predominantly driven
by sustained directional selection and not genetic drift. This in-
ference is consistent with its functional association because the
angle of the spine is directly tied to the predominant direction of
forelimb actions (e.g., overhead vs. lateralized). In particular,
selection on the relative positions of the blade and spine is as-
sociated with the cranio-caudal orientation of the glenoid (Fig.
3). This gradual shift in spine and glenoid angle affects the fiber
orientation of the pectoral and scapular muscles, altering the
position of the upper limb where force production is optimized
(34). The reduced, caudally shifted angle in Homo is consistent
with both a decreased reliance on use of the upper limb for
overhead actions, such as climbing, and the increased use of
Nacholapithecus
Sivapithecus
Siamang
Gibbon
Gorilla
Bonobo
Chimpanzee
Human
Ho.ergaster
Au.afarensis
Au.sediba
Proconsul
Ho.neander.
Orangutan
a
t0
t1
t2
t3
t4
t5
Fig. 3. Model of shoulder shape evolution. Scapula morphospace is recon-
structed at individual time horizons (t
n
) for the phylogeny shown. The an-
cestral hominoid condition is reconstructed to be similar in shape and
configuration to Pongo (t
0
). Pongo shares with Lagothrix a penchant for
slow, cautious movements through high forest canopy, including frequent
bouts of pronograde suspensory locomotion (5961). This similarity suggests
that derived suspensorypostcranial characteristics of Pongo shared with
other apes are partially convergent, consistent with evidence from Sivapithecus
(16). In this model, hylobatids evolved a more cranially oriented spine and
glenoid from this morphotype, which is predicted to fall in the intermediate
space (t
12
). African apes evolved a unique blade shape with cranial spine (t
1
),
subsequently diversifying into Pan and Gorilla lineages (t
2
). Hominins retained
the ancestral African ape blade shape, but the angle of the spine relative to the
vertebral border gradually shifted (t
34
), consistent with realignment of the
shoulder musculature due to selection associated with more lateralized activities
and/or reduced reliance on overhead activities (e.g., climbing).
4of6
|
www.pnas.org/cgi/doi/10.1073/pnas.1511220112 Young et al.
lateralized behaviors, such as tool use and throwing. The slow,
sustained pace over which these changes took place suggests that,
whereas they conferred a selective advantage for lateralized actions
in the hominin lineage, they may have been balanced by a tradeoff
with other factors, such as continued use in arboreal contexts. The
early appearance of a moderate caudal shift in spine and glenoid,
dating to Australopithecus, is consistent with new evidence suggest-
ing that tool use extends well past the origins of Homo (3537).
Interestingly, the later A. sediba has a more human-like shoulder
compared with earlier A. afarensis, suggesting that the ancestor of
A. sediba and Homo shared the more derived configuration. That
said, it is not until the emergence of later Homo that a modern
scapular configuration was largely in place (38, 39). This final
shift toward a fully lateralized spine and glenoid was likely
costly to climbing efficiency and/or arm hanging (40), while also
increasing shear stress at the shoulder and elevating the risk of
rotator cuff injury (41, 42). Given the fitness value of efficient
climbing for accessing food and avoiding predators, we speculate
that the selective forces driving this shift must also have been
significant.
Both models posit a series of changes to both the position of the
spine and the shape of the blade in multiple lineages. Later post-
natal growth has a relatively limited and similar effect on blade
shape across lineages whereas spine angle does not change with age
(29). These facts suggest that genetic regulation of the early posi-
tioning of muscles, spine, and acromion are critical to establishing
species differences rather than later growth or functional remod-
eling. Identifying the genetic and molecular mechanisms that con-
trol variation in scapular morphogenesis may provide a novel
approach to directly test among alternative evolutionary models.
For example, each model makes predictions about the timing and
history of selection on cis-regulatory elements that control de-
velopmental traits (e.g., the spine in Fig. S4A). If variation in either
regulatory or downstream sequence is the proximate target of se-
lection, then timing the signature of selection could serve as a direct
test of these hypotheses. In the AA model, one would predict there
would be evidence for concerted evolutionary sequence change
(and/or key functional base pair changes) within regulatory regions
for genes that only influence the interaction of spine and blade. In
contrast, the AC model would predict sequence evolution in regu-
latory regions for genes influencing blade and spine, and such
changes should be step-wise chronologically. In either case, changes
should date to particularly informative periods as supported by the
fossil record. Identification of the cis-regulatory architecture that
underlies the specific traits in question will be highly informative for
understanding their variation potential, testing competing evolu-
tionary scenarios, and ultimately providing the opportunity to per-
form experimentalpaleontology, by altering sequence data in
model species (43).
Materials and Methods
Data. We collected 3D landmark data from scapulae of museum specimens
from the following extant hominoid species: Homo sapiens (modern humans,
n=31), Pan troglodytes (chimpanzee, n=56), Pan paniscus (bonobo, n=
36), Gorilla gorilla (lowland gorilla, n=72), Pongo pygmaeus (Bornean
orangutan, n=48), Symphalangus syndactylus (siamang, n=41), and
Hylobates sp. (gibbon, n=35). Use of anonymized human data was ap-
proved by the University of California, San Francisco Committee on Human
Research (no. 10-01599). As proxies of the primitive Miocene ape ancestral
morphotype (MAA), we use the cercopithecoid colobine Nasalis larvatus
(proboscis monkey, n=19) and the ceboid ateline Lagothrix lagotricha
(wooly monkey, n=11), consistent with reconstructions of both Early and
Middle Miocene apes (e.g., Proconsul,Nacholapithecus) and hypothesized
functional and morphological similarity (18, 44, 45). We used adult wild-
caught males and females, one scapula per indi vidual, principally t he right.
Specimens were chosen from similar geographic localities and/or within
subspecies to minimize the effect of population heterogeneity. Missing,
broken, damaged, or pathological individuals were excluded. Three-dimensional
landmark coordinate data (x,y,z) were recorded using a Microscribe-3Dx digitizer
(Immersion Corporation) as previously described (32, 46). We obtained
3D computed-tomography (CT) data from the original specimens of DIK 1-1
(A. afarensis, right side) (13), MH2 (A. sediba, right side) (16), Kebara 2
(H. neanderthalensis, right side), and Qafzeh 9 (anatomically modern H. sapiens,
right side) and generated a 3D object in Amira 5.4 (Visage Imaging, Inc.). For
KNM WT15000 (H. ergaster, right side) and La Ferassie I (H. neanderthalensis,
right side), we used high quality casts. All 3D objects were landmarked in
Landmark Editor 3.5 (University of California, Davis). We applied a series of
landmarks to each specimen (n=13) (29, 45), excluding those not found in
all fossils (Fig. S6).
Shape Analysis. We performed a Procrustes superimposition to remove the
effects of scale, rotation, and alignment, and to reflect right and left scap-
ulae. We removed the effect of size heterogeneity by performing a multi-
variate regression of shape on log centroid size (LCS) within species. We used
the residuals of the group-centered means in all subsequent analyses. We first
performed a principal components analysis (PCA) to assess shape variation,
and two further analyses to take into account group information and assess
the effect of sample size differences among species: (i) a canonical variates
analysis (CVA) using species as the grouping variables and the overall pooled
covariance matrix as the measure of within-group variability, and (ii) a be-
tween-group PCA (bgPCA) using PC axes estimated from averages of each
species (47). We performed a within-configuration partial least squares (PLS)
analysis within each species and centering on the group mean to compare
covariation between variation in the spine and blade landmarks, with sig-
nificance tested by permutation (1,000 replicates). We calculated Procrustes
distances among species and tested for significance using a permutation test
for pairwise distances (10,000 iterations). From these distances, we per-
formed a cluster analysis, using the unweighted pair group with arithmetical
mean (UPGMA) method, and generated a phenetic tree using the neighbor-
joining (NJ) method (Nasalis/Lagothrix =root) in the software NTSYS-pc
(v.2.1) (48). Eigenanalysis and visualizations were performed in MorphoJ
v1.06d (49), Landmark Editor (v.3.0) (50), and the geomorph package (51)
implemented in R(v.3.2.1) (52).
Developmental Simulation. To compare DIK 1-1 to the adult morphospace, we
performed a developmental simulation using allometric estimates under
different assumptions of growth (Pan,Gorilla,Pongo, and Nasalis) (32). To do
this analysis, we performed a Procrustes superimposition including the four
extant species and DIK 1-1 so that all individuals and ontogenetic vectors
were in the identical shape space. We next performed a multivariate re-
gression of shape on log centroid size for each species age series alone and
calculated the associated species-specific ontogenetic vector (Fig. S7). We
next estimated adult shape by adding the product of each ontogenetic
vector times LCS (=0.75, the difference in LCS between juvenile and adult)
to the DIK 1-1 Procrustes coordinates (53). Simulations were visualized by
transforming the DIK1-1 specimen to the target adult landmark configura-
tion in Landmark Editor (v.3.5) (Fig. 2C).
Phylogenetic Morphospace. We implemented squared-change parsimony (54)
to (i) map alternative phylogenetic trees (Fig. 1 Band C) onto the continuous
shape space defined by PCA, bgPCA, and CVA, (ii) reconstruct alternative
ancestral morphotypes (i.e., nodes), and (iii ) infer evolutionary trajectories
(30, 55, 56). Squared-change parsimony is a generalization of maximum
likelihood-based methods where all branch lengths are 1.We justify this
simplification by the fact that, with the exception of H. neanderthalensis,
branch lengths are unknown for hominin fossil taxa. All trees reflect the
currently accepted branching pattern as inferred from genomic datasets and
calibrated from the fossil record (2) (Fig. 1 Dand Eand Table S2), but the AC
trees differ in that a shared ancestral morphotype is represented by a si-
multaneous origin modeled as a hard polytomy (branch length of 0) (Fig.
1E). In both cases, the MAA state corresponds to Nasalis and Lagothrix,
which are also used to root the tree. Trees were generated in Mesquite
v.3.01 (57). For each tree, we calculated the total branch length and tested
the hypothesis of no phylogenetic signal using a permutation design (10,000
replicates) as implemented in MorphoJ v.1.06c (49).
ACKNOWLEDGMENTS. The Peabody Museum, Museum of Comparative
Zoology, American Museum of Natural History, National Museum of Natural
History, Field Museum of Natural History, Cleveland Museum of Natural
History, University of Zürich-Irchel, Zooligische Staatssammlung, Musée Royale
de lAfrique Centrale, Powell-Cotton Museum, Kyoto University Primate Re-
search Institute, and Japan Monkey Center provided access to specimens.
T. Nalley assisted with segmentation of DIK1-1. K. Carlson provided computed
tomography (CT) data for MH2. S. Mellilo kindly provided a subset of the adult
human landmark data. B. Feeley provided additional human imaging data
Young et al. PNAS Early Edition
|
5of6
ANTHROPOLOGY
(CHR no. 10-01599). J. Camacho assisted in the CT scanning of La Ferassie I. I.
Hershkovitz provided CT data for Kebara 2 and Qafzeh 9. Funding was pro-
vided through grants from the National Science Foundation (Grant BCS-
1518596 to T.D.C., N.M.Y., and N.T.R.) and the generosity of Margaret and
William Hearst (Z.A.). N.M.Y. acknowledges funding from National Institutes
of Health Grants R01DE019638 and R01DE021708 and the ongoing support
of the University of California, San Francisco OrthopaedicTrauma Institute,
T. Miclau, R. Marcucio, and the Laboratory for Skeletal Regeneration.
1. Ruvolo M (1997) Molecular phylogeny of the hominoids: Inferences from multiple
independent DNA sequence data sets. Mol Biol Evol 14(3):248265.
2. Steiper ME, Young NM (2006) Primate molecular divergence dates. Mol Phylogenet
Evol 41(2):384394.
3. Oxnard CE (1967) The functional morphology of the primate shoulder as revealed by
comparative anatomical, osteometric and discriminant function techniques. Am J
Phys Anth 26(2):219240.
4. Oxnard CE (1977) Morphometric affinities of the human shoulder. Am J Phys
Anthropol 46(2):367374.
5. Bello-Hellegouarch G, et al. (2013) A comparison of qualitative and quantitative
methodological approaches to characterizing the dorsal side of the scapula in Hom-
inoidea and its relationship to locomotion. Int J Primatol 34:315336.
6. Alemseged Z, et al. (2006) A juvenile early hominin skeleton from Dikika, Ethiopia.
Nature 443(7109):296301.
7. Haile-Selassie Y, et al. (2010) An early Australopithecus afarensis postcranium from
Woranso-Mille, Ethiopia. Proc Natl Acad Sci USA 107(27):1212112126.
8. Green DJ, Alemseged Z (2012) Australopithecus afarensis scapular ontogeny, func-
tion, and the role of climbing in human evolution. Science 338(6106):514517.
9. Churchill SE, et al. (2013) The upper limb of Australopithecus sediba.Science
340(6129):1233477.
10. Pilbeam D (1996) Genetic and morphological records of the Hominoidea and hominid
origins: A synthesis. Mol Phylogenet Evol 5(1):155168.
11. Harrison T (2010) Apes among the tangled branches of human origins. Science
327(5965):532534.
12. Zihlman AL, Cronin JE, Cramer DL, Sarich VM (1978) Pygmy chimpanzee as a possible
prototype for the common ancestor of humans, chimpanzees and gorillas. Nature
275(5682):744746.
13. Groves CP (1988) The evolutionary ecology of the Hominoidea. Anu Psicol 39:8798.
14. Gebo DL (1996) Climbing, brachiation, and terrestrial quadrupedalism: Historical
precursors of hominid bipedalism. Am J Phys Anthropol 101(1):5592.
15. Wrangham R, Pilbeam D (2001) African Apes as Time Machines. All Apes Great and
Small, eds Galdikas BMF, Briggs NE, Sheeran LK, Shapiro GL, Goodall J (Springer,
Berlin), Vol 1, pp 517.
16. Pilbeam D, Rose MD, Barry JC, Shah SM (1990) New Sivapithecus humeri from Pakistan
and the relationship of Sivapithecus and Pongo.Nature 348(6298):237239.
17. Moyà-Solà S, Köhler M, Alba DM, Casanovas-Vilar I, Galindo J (2004) Pierolapithecus
catalaunicus, a new Middle Miocene great ape from Spain. Science 306(5700):
13391344.
18. Nakatsukasa M, Kunimatsu Y (2009) Nacholapithecus and its importance for un-
derstanding hominoid evolution. Evol Anth 18:103119.
19. Alba DM, Almécija S, Casanovas-Vilar I, Méndez JM, Moyà-Solà S (2012) A partial
skeleton of the fossil great ape Hispanopithecus laietanus from Can Feu and the
mosaic evolution of crown-hominoid positional behaviors. PLoS One 7(6):e39617.
20. Larson SG (1998) Parallel evolution in the hominoid trunk and forelimb. Evol Anth 6:
8799.
21. Dainton M, Macho GA (1999) Did knuckle walking evolve twice? J Hum Evol 36(2):
171194.
22. Kivell TL, Schmitt D (2009) Independent evolution of knuckle-walking in African apes
shows that humans did not evolve from a knuckle-walking ancestor. Proc Natl Acad
Sci USA 106(34):1424114246.
23. Thorpe SKS, Holder RL, Crompton RH (2007) Origin of human bipedalism as an ad-
aptation for locomotion on flexible branches. Science 316(5829):13281331.
24. Thorpe SKS, McClymont JM, Crompton RH (2014) The arboreal origins of human bi-
pedalism. Antiquity 88:906926.
25. Lovejoy CO, Suwa G, Simpson SW, Matternes JH, White TD (2009) The great divides:
Ardipithecus ramidus reveals the postcrania of our last common ancestors with Af-
rican apes. Science 326(5949):100106.
26. White TD, Lovejoy CO, Asfaw B, Carlson JP, Suwa G (2015) Neither chimpanzee nor
human, Ardipithecus reveals the surprising ancestry of both. Proc Natl Acad Sci USA
112(16):48774884.
27. Sidlauskas B (2008) Continuous and arrested morphological diversification in sister
clades of characiform fishes: A phylomorphospace approach. Evolution 62(12):
31353156.
28. Young NM (2003) A reassessment of living hominoid postcranial variability: Implica-
tions for ape evolution. J Hum Evol 45(6):441464.
29. Young NM (2008) A comparison of the ontogeny of shape variation in the anthropoid
scapula: Functional and phylogenetic signal. Am J Phys Anthropol 136(3):247264.
30. Larson SG (2015) Rotator cuff muscle size and the interpretation of scapular shape in
primates. J Hum Evol 80:96106.
31. Hartwig-Scherer S (1993) Allometry in hominoids: A comparative study of skeletal
growth trends. PhD dissertation (University of Zurich, Zurich).
32. Pilbeam D, Young N (2004) Hominoid evolution: Synthesizing disparate data. CR
Palevol 3:305321.
33. Grabowski M, Hatala KG, Jungers WL, Richmond BG (2015) Body mass estimates of
hominin fossils and the evolution of human body size. J Hum Evol 85:7593.
34. Roach NT, Venkadesan M, Rainbow MJ, Lieberman DE (2013) Elastic energy storage in
the shoulder and the evolution of high-speed throwing in Homo.Nature 498(7455):
483486.
35. Skinner MM, et al. (2015) Human-like hand use in Australopithecus africanus. Science
347(6220):395399.
36. McPherron SP, et al. (2010) Evidence for stone-tool-assisted consumption of animal
tissues before 3.39 million years ago at Dikika, Ethiopia. Nature 466(7308):857860.
37. Harmand S, et al. (2015) 3.3-million-year-old stone tools from Lomekwi 3, West Tur-
kana, Kenya. Nature 521(7552):310315.
38. Larson SG (2007) Evolutionary transformation of the hominin shoulder. Evol Anth 16:
172187.
39. Larson SG (2009) Evolution of the hominin shoulder: Early Homo.The First Humans:
Origins of the Genus Homo, eds Grine FE, Leakey RE (Springer, New York).
40. Hunt KD (1991) Positional behavior in the Hominoidea. Int J Primatol 12:95118.
41. Apreleva M, Parsons IM, 4th, Warner JJ, Fu FH, Woo SL (2000) Experimental in-
vestigation of reaction forces at the glenohumeral joint during active abduction.
J Shoulder Elbow Surg 9(5):409417.
42. Parsons IM, Apreleva M, Fu FH, Woo SL (2002) The effect of rotator cuff tears on
reaction forces at the glenohumeral joint. J Orthop Res 20(3):439446.
43. Pieretti J, et al. (2015) Organogenesis in deep time: A problem in genomics, devel-
opment, and paleontology. Proc Natl Acad Sci USA 112(16):48714876.
44. Rose MD (1983) Miocene hominoid postcranial morphology: Monkey-like, ape like,
neither, or both? New Interpretations of Ape and Human Ancestry, eds Ciochon RS,
Corruccini RS (Plenum, New York), pp 405417.
45. Rose MD (1993) Locomotor anatomy of Miocene hominoids. Postcranial Adapta-
tion in Nonhuman Primates, ed Gebo DL (Northern Illinois Univ Press, DeKalb, IL),
pp 252272.
46. Young NM (2006) Function, ontogeny and canalization of shape variance in the
primate scapula. J Anat 209(5):623636.
47. Mitteroecker P, Bookstein F (2011) Linear discrimination, ordination, and the visual-
ization of selection gradients in modern morphometrics. Evol Biol 38:100114.
48. Rohlf FJ (2000) NTSYS-PC, Numerical Taxonomy System for the PC Exeter Software
(Applied Biostatistics Inc., Setauket, NY), Version 2.1.
49. Klingenberg CP (2011) MorphoJ: An integrated software package for geometric
morphometrics. Mol Ecol Resour 11(2):353357.
50. Wiley DF, et al. (2005) Evolutionary morphing. Visualization 2005 (IEEE, Washington,
DC), pp 431-438.
51. Adams DC, Otárola-Castillo E (2013) geomorph:AnRpackage for the collection and
analysis of geometric morphometric shape data. Methods Ecol Evol 4:393399.
52. R Core Team (2015) R: A Language and Environment for Statistical Computing (R
Foundation for Statistical Computing, Vienna). Available at www.R-project.org/.
53. Zelditch ML, Swiderski DL, Sheets HD (2012) Geometric Morphometrics for Biologists:
A Primer (Academic, London), 2nd Ed.
54. Maddison WP (1991) Squared-change parsimony reconstructions of ancestral states
for continuous-valued characters on a phylogenetic tree. Syst Zool 40:304314.
55. Adams DC, Collyer ML (2009) A general framework for the analysis of phenotypic
trajectories in evolutionary studies. Evolution 63(5):11431154.
56. Klingenberg CP, Gidaszewski NA (2010) Testing and quantifying phylogenetic signals
and homoplasy in morphometric data. Syst Biol 59(3):245261.
57. Maddison WP, Maddison DR (2015) Mesquite: A Modular System for Evolutionary
Analysis. Version 3.03. Available at mesquiteproject.org. Accessed June 1, 2015.
58. Dembo M, Matzke NJ, Mooers AØ, Collard M (2015) Bayesian analysis of a morpho-
logical supermatrix sheds light on controversial fossil hominin relationships. Proc Biol
Sci 282(1812):20150943.
59. Thorpe SKS, Crompton RH (2005) Locomotor ecology of wild orangutans (Pongo
pygmaeus abelii) in the Gunung Leuser Ecosystem, Sumatra, Indonesia: A multivari-
ate analysis using log-linear modelling. Am J Phys Anthropol 127(1):5878.
60. Thorpe SKS, Crompton RH (2006) Orangutan positional behavior and the nature of
arboreal locomotion in Hominoidea. Am J Phys Anthropol 131(3):384401.
61. Cant JGH, Youlatos D, Rose MD (2003) Suspensory locomotion of Lagothrix lago-
thricha and Ateles belzebuth in Yasuní National Park, Ecuador. J Hum Evol 44(6):
685699.
6of6
|
www.pnas.org/cgi/doi/10.1073/pnas.1511220112 Young et al.
Supporting Information
Young et al. 10.1073/pnas.1511220112
AA
AC
Au. afarensis
Au. sediba
Ho. ergaster
African
Apes
Gibbons
MAA
Human
Au. afarensis
Au. sediba
African
Apes
Gibbons
MAA
Human
Canonical Axis 1 (47% Variation)
Canonical Axis 2 (23% Variation)
6
3
0
-3
-6
-6 3 0 3 6 9
CD
Au. afarensis
Au. sediba
Ho. ergaster
Gorilla
Bonobo
Chimp
Siamang
Gibbon
Orangutan
Lagothrix
Nasalis
Human
bgPC 1 (46.8% Shape Variation)
bgPC 2 (20.1% Shape Variation)
Au. afarensis
Au. sediba
Ho. ergaster
Gorilla
Bonobo
Chimp
Siamang
Gibbon
Human
-0.20 -0.10 0.00 0.10 0.20 0.30
-0.20 -0.10 0.00 0.10 0.20
EF
AA
AC
Au. afarensis
Au. sediba
Ho. ergaster
Gorilla
Bonobo
Chimp
Siamang
Gibbon
Orangutan
Human
Nasalis
Lagothrix
Ho. neander.
Ho. neander.
Ho. ergaster
Ho. neander.
Ho. neander.
Nasalis
Orangutan
O
Lagothrix amHs
amHs
Ho. neander.
Au. afarensis
Au. sediba
Ho. ergaster
Gorilla
Bonobo
Chimp
Siamang
Gibbon
Orangutan
Human
Nasalis
Lagothrix
Ho. neander.
ROOT
ROOT
Pongo
Pongo
0.20
0.10
0.00
-0.10
-0.20
-0.20
-0.10 0.00 0.10 0.20 0.30
0.20
0.10
0.00
-0.10
-0.20
-0.20
-0.10 0.00 0.10 0.20 0.30
A
B
Principal Component 1 (45.4% Variation)
Principal Component 2 (19.1% Variation)
Principal Component 1 (45.4% Variation)
Principal Component 2 (19.1% Variation)
Gorilla
Bonobo
Chimp
Siamang
Gibbon
Pongo
Lagothrix
Nasalis
Human
Gorilla
Bonobo
Chimp
Siamang
Gibbon
Pongo
Lagothrix
Nasalis
Human
AA
AC
ROOT
ROOT
AA
AC
AA
AC
Fig. S1. Extended shape analyses. (Aand B) Principal components analysis (PCA) using only the extant species. Phylogenetic reconstructions are shown as branching patterns, with ancestral nodes at branch joints. Dashed lines show the most direct
evolutionary path between hypothesized ancestral and descendant states. AA, African ape model; AC, ape convergence model. (C) Canonical variates analysis (CVA) showing the first two axes. Distribution of species and associated shape vectors are
similar to those identified in the PCA (Fig. 2) but show greater separation due to the methodology. (D) Phylogenetic reconstructions within the CVA morphospace using a method of squared-change parsimony on the CV1 and -2 axes while using
alternative tree hypotheses (Fig. 1 Dand E). Results show that a simple morphocline separates Pan and Homo in CV1 for the AA model, and a two-step process in CV1 and -2 for the AC model. (E) Results of the between-group principal components
analysis (bgPCA) are largely identical to the PCA and CVA although there is reduced discrimination of African apes, suggesting that Pan and Gorilla may be even more similar when sample size effects are taken into account. (F) The phylogenetic
reconstruction within the bgPCA morphospace is also concordant with other ordination results. Color coding is the same as in Fig. 2D. Red dots represent different developmental simulations of DIK 1-1 (A. afarensis).
Young et al. www.pnas.org/cgi/content/short/1511220112 1of7
% Total Squared Covariance
PLS Axis
100
80
60
40
20
0
BLADE PLS1
0.15
0.10
0.05
0.00
-0.05
-0.10
-0.15
-0.20
SPINE PLS1
0.150.100.050.00-0.05-0.10-0.15-0.20
Au.sediba
Ho. ergaster
Au.afarensis
Rv=0.633
p<0.0001
AB
C
Fig. S2. Partial least squares (PLS) results. (A) Distribution of covariation between blade and spine shows that the majority of shape variation is associated with
the first axis. (B) Plot of PLS1 axes for blade and spine variation shows a highly significant association of shape variation covariation (R
v
=0.633, P<0.0001).
(C) Associated PLS shape vector direction and magnitudes for positive (+0.10) and negative (0.15) shown on the mean configuration (red, blade landmarks;
blue, spine landmarks).
Young et al. www.pnas.org/cgi/content/short/1511220112 2of7
-0.20 -0.10 0.00 0.10 0.20 0.30
0.20 0.10 0.00 - 0.10 - 0.20
Principal Component 1 (47.3% Shape Variation)
Principal Component 3 (9.3% Shape Variation)
Au. afarensis
Au. sediba
Ho. ergaster
Gorilla
Bonobo
Chimp
Siamang
Gibbon
Orangutan
Lagothrix
Nasalis
Human
A
D
Au. afarensis
Au. sediba
Ho. ergaster
Gorilla
Bonobo
Chimp
Siamang
Gibbon
Orangutan
Lagothrix Nasalis
Human
AA Model AC Model
PC1 (47.3% Variation)
PC2 (18.8% Variation)
PC3 (9.3% Variation)
0.25
0.20
0.15
0.10
0.05
0.00
-0.05
-0.10
0.04
0.02
0.00
-0.02
-0.04
-0.06
-0.08
-0.05
0.05
0.00
Pongo
Nasalis
Ho.neandertal.
Ho.ergaster
Au.sediba
Ho.sapiens
P.pansiscus
P.troglodytes
Gorilla
Symphalangus
Hylobates
Lagothrix
AA
AC
Au.afarensis
BC
ROOT
Ho. neander.
Au. afarensis
Au. sediba
Ho. ergaster
Gorilla
Bonobo
Chimp
Siamang
Gibbon
Orangutan
Lagothrix Nasalis
Human
ROOT
Ho. neander.
Ho. neander.
Fig. S3. Extended PCA results. (A) Visualization of PC3 shape changes from positive (Top) to negative (Bottom). Gorilla and Pongo differ from all other taxa in having moderately wider scapula beyond those identified in PC1. (B) Three-dimensional scatterplot of PC1, PC2, and PC3.
Dashed lines show approximate direct evolutionary vectors connecting hypothesized ancestral and descendant species for the AA and AC models. (C) Two-dimensional scatterplot of PC1 vs. PC3 with examples of Gorilla and Pongo shown. (D) Reconstructed phylogenetic trees from
the PC1 and PC3 morphospace from Fig. 2. Note that the PC3 axis is reversed in Aand Brelative to the trees shown in Cand D.
Young et al. www.pnas.org/cgi/content/short/1511220112 3of7
y = -188.29x + 9.4688
R = 0.74475
-1.000
4.000
9.000
14.000
19.000
24.000
29.000
34.000
39.000
-0.15 -0.10 -0.05 0.00 0.05 0.10
Millions of Years Ago (mya)
PC2 Score
y = -93.821x + 21.273
R = 0.35565
-1.000
4.000
9.000
14.000
19.000
24.000
29.000
34.000
39.000
0.00 0.05 0.10 0.15 0.20 0.25 0.30
Millions of Years Ago (mya)
PC1 Score
y = 17.992x + 2.0509
R = 0.00916
-1.000
1.000
3.000
5.000
7.000
9.000
11.000
-0.02 0.00 0.02 0.04 0.06 0.08 0.10 0.12
Millions of Years Ago (mya)
PC2 Score
y = -24.886x + 5.6978
R = 0.86158
-1.000
1.000
3.000
5.000
7.000
9.000
11.000
-0.20 -0.10 0.00 0.10 0.20 0.30
Millions of Years Ago (mya)
PC1 Score
AA Model
AC Model
PC1 : Spine Angle PC2 : Blade Shape
A
B
C
D
Fig. S4. PC scores versus time. (AD) Regressions of PC1 shape scores on both estimated divergence time (ancestral nodes) and geologic age (fossils) illustrate
alternative predictions for the timing and strength of selection in the hominin lineage on spine and glenoid orientation.
UPGMA Neighbor JoiningAB
Au. afarensis
Pan paniscus
Pan trroglodytes
Hylobates sp.
Sy. syndactylus
Gorilla gorilla
Ho. ergaster
Homo sapiens
Au. sediba
Lagothrix lagotricha
Nasalis larvatus
Pongo pygmaeus
Ho. neanderthalensi
s
Procrustes Distance
0.00 0.05 0.10 0.16 0.21
Au. afarensis
Pan paniscus
Pan trroglodytes
Hylobates sp.
Sy. syndactylus
Gorilla gorilla
Ho. ergaster
Homo sapiens
Au. sediba
Lagothrix lagotricha
Nasalis larvatus
Pongo pygmaeus
Ho. neanderthalensis
Procrustes Distance
0.05 0.10 0.15 0.20 0.26
Fig. S5. Procrustes distance trees. (A) Tree generated using the unweighted pair group method with arithmetic mean (UPGMA) method. (B) Tree generated
using the neighbor joining (NJ) method. In both cases, A. afarensis is associated with Gorilla whereas either H. ergaster or H. neanderthalensis is associated with
H. sapiens. Procrustes distances and significance values are found in Table S1.
Young et al. www.pnas.org/cgi/content/short/1511220112 4of7
9
10
11
12
13
7
5
1
2
3
4
5
6
7
8
10
9
LANDMARKS
1: Suprascapular notch
2: Superior point on vertebral border
3: Intersection of spine with vertebral border
4: Inferior point on vertebral border
5: Superior lateral point of teres major fossa
6: Lateral most extent of spine
7: Glenoid neck
8: Root of spine
9: Inferior extent of glenoid
10: Dorsal side of glenoid
11: Ventral extent of glenoid
12: Superior extent of glenoid
13: Shallowest extent of glenoid
DORSAL GLENOID
Fig. S6. Scapula landmarks. Descriptions and locations of the 3D landmarks used in this study are shown on a representative P. troglodytes scapula (Left)
shown in dorsal and medial view.
0.12
0.09
0.06
0.03
0.00
-0.03
-0.06
-0.09
-0.12
3.6 3.9 4.2 4.5 4.8 5.1 5.4 5.7 6.0
Shape Score
Log Centroid Size
Au. afarensis (N=1)
Go. gorilla (N=167)
Pa. troglodytes (N=146)
Po. pygmaeus (N=53)
Na. larvatus (N=56)
Fig. S7. Growth vectors used for developmental simulation. Multivariate regression of group shape on log centroid size for the taxa shown. Individual growth
vectors were generated by performing the same multivariate regression analysis using the Procrustes coordinates from the group superimposition but per-
formed on each species alone. The Procrustes coordinates of A. afarensis (DIK 1-1) were simulated at an adult size corresponding to an increase of log centroid
size of 0.75, consistent with achieving an adult outcome (dashed ellipses) in each of the taxa used.
Young et al. www.pnas.org/cgi/content/short/1511220112 5of7
Table S1. Procrustes distances between species pairs below the diagonal and Pvalues (10,000 permutations) above
the diagonal
Species A. afa A. sed G. gor H. erg H. nea H. sap Hy. sp. L. lag N. lar P. pan P. tro P. pyg S. syn
A. afarensis 0.141 *** 0.039 0.037 *** *** 0.000 *** *** *** *** ***
A. sediba 0.132 0.014 n/a 0.333 0.164 0.023 0.019 0.050 0.016 0.017 0.018 0.003
G. gorilla 0.128 0.206 0.012 0.000 *** *** *** *** *** *** *** ***
H. ergaster 0.199 0.153 0.275 n/a 0.176 0.014 0.080 0.026 0.011 0.010 0.021 0.008
H. neander. 0.215 0.175 0.286 0.089 0.025 0.001 0.002 0.001 0.001 0.001 0.001 0.000
H. sapiens 0.159 0.130 0.229 0.132 0.111 *** *** *** *** *** *** ***
Hy. sp. 0.200 0.265 0.190 0.374 0.382 0.311 *** *** *** *** *** ***
L. lagotricha 0.155 0.197 0.213 0.263 0.268 0.204 0.197 *** *** *** *** ***
N. larvatus 0.121 0.134 0.181 0.206 0.216 0.162 0.216 0.113 *** *** *** ***
P. paniscus 0.170 0.223 0.133 0.330 0.346 0.284 0.130 0.233 0.198 *** *** ***
P. troglodytes 0.152 0.208 0.118 0.314 0.326 0.260 0.124 0.214 0.188 0.046 *** ***
P. pygmaeus 0.163 0.195 0.188 0.260 0.246 0.179 0.208 0.150 0.136 0.221 0.200 ***
S. syndactylus 0.207 0.267 0.186 0.379 0.388 0.321 0.059 0.232 0.239 0.112 0.106 0.228
A. afarensis (A. afa), Australopithecus afarensis;A. sediba (A. sed), Australopithecus sediba;G. gorilla (G. gor), Gorilla gorilla;
H. ergaster (H. erg), Homo ergaster;H. neander.(H. nea), Homo neanderthalensis;H. sapiens (H. sap), Homo sapiens;Hy.sp.,Hylobates
sp.; L. lagotricha (L. lag), Lagothrix lagotricha;N. larvatus (N. lar), Nasalis larvatus;P. paniscus (P. pan), Pan paniscus;P. troglodytes (P. tro),
Pan troglodytes;P. Pygmaeus (P. pyg), Pongo pygmaeus;S. Syndactylus (S. syn), Symphalangus syndactylus.***P0.001.
Table S2. Average PC1 scores, geologic ages, and estimated
divergence times
Species/node
PC1 Age, Mya
Mean SD Estimate Low High
H. sapiens 0.195 0.027 0.000 ——
AMHs 0.189 0.106 0.097 0.116
H. neander. 0.251 0.019 0.063 0.058 0.068
H. ergaster 0.228 1.550 1.500 1.600
A. sediba 0.117 1.977 1.974 1.980
A. afarensis 0.063 0.013 3.330 3.310 3.350
Panins 0.067 0.030 6.600 6.000 7.000
African apes 0.036 0.044 8.600 7.700 9.200
P. pygmaeus 0.091 0.037 18.300 16.300 20.800
MAA 0.086 0.031 30.500 26.900 36.400
Dashes indicate the diagonal, for which there is no value. AMHs, anatom-
ically modern H. sapiens.
Young et al. www.pnas.org/cgi/content/short/1511220112 6of7
Movie S1. PanHomo evolutionary transformation. Example of a thin-plate spline (TPS) deformation between representative P. troglodytes and H. sapiens
scapulae in which landmark configurations have been scaled to the same size and aligned to the vertebral border. Shape differences are primarily associated
with the orientation of the spine and glenoid angle, which become more inferiorly oriented. Note that blade shape remains largely unchanged.
Movie S1
Movie S2. PongoHomo evolutionary transformation. Thin-plate spline (TPS) deformation between representative P. pygmaeus and H. sapiens scapulae in
which landmark configurations have been scaled to the same size and aligned to the vertebral border. Shape transformations into the human state consist of
both a more inferior orientation of the spine and glenoid angle, and changes to the shape of the supraspinous fossa, particularly the cranial orientation of the
superior border.
Movie S2
Young et al. www.pnas.org/cgi/content/short/1511220112 7of7
... The completeness and the ca. 3.67 Ma date of the StW 573 skeleton offer an opportunity to add to the debate on the form of the pectoral girdle in crown hominins (e.g., Larson, 2007;Young et al., 2015;Green et al., 2016;Melillo, 2016), which in turn provides an opportunity to assess changing roles of the upper limb as the positional behavior repertoire shifted over the course of early human evolution. African middle Miocene apes are represented by three scapulae and one clavicle attributed to Nacholapithecus (ca. ...
... In the present study, scapular form of australopiths tended to fall along CV1 between humans on the one hand and African apes on the other hand when considering the 18-variable analysis (Fig. 10), or mostly between humans and chimpanzees and broadly overlap with gorillas when considering the 11-variable analysis (Fig. 11). An intermediate position of stem homininans between these extant groups also was noted by Young et al. (2015) in their analysis of scapular 3D morphospace and underscores the unique australopith scapular configuration in comparison to that of extant hominoids. In our 18-variable CVA, StW 573 aligned with African apes in scapular form to an arguably greater degree than other Australopithecus scapulae (KSD-VP-1/1, MH2, and both DIK-1-1 scapulae), whereas in the 11-variable CVA, KSD-VP-1/1 exhibited this distinction. ...
... Recent evaluations have pointed toward African ape-like scapular form, particularly gorilla-like form, as the most parsimonious model for crown hominin LCA form (Young et al., 2015;Green et al., 2016). The absence of much of the supraspinous fossa in KSD-VP-1/1 is notable in our comparisons. ...
Article
The ca. 3.67 Ma adult skeleton known as ‘Little Foot’ (StW 573), recovered from Sterkfontein Member 2 breccia in the Silberberg Grotto, is remarkable for its morphology and completeness. Preservation of clavicles and scapulae, including essentially complete right-side elements, offers opportunities to assess morphological and functional aspects of a nearly complete Australopithecus pectoral girdle. Here we describe the StW 573 pectoral girdle and offer quantitative comparisons to those of extant hominoids and selected homininans. The StW 573 pectoral girdle combines features intermediate between those of humans and other apes: a long and curved clavicle, suggesting a relatively dorsally positioned scapula; an enlarged and uniquely proportioned supraspinous fossa; a relatively cranially oriented glenoid fossa; and ape-like reinforcement of the axillary margin by a stout ventral bar. StW 573 scapulae are as follows: smaller than those of some homininans (i.e., KSD-VP-1/1 and KNM-ER 47000A), larger than others (i.e., A.L. 288-1, Sts 7, and MH2), and most similar in size to another australopith from Sterkfontein, StW 431. Moreover, StW 573 and StW 431 exhibit similar structural features along their axillary margins and inferior angles. As the StW 573 pectoral girdle (e.g., scapular configuration) has a greater affinity to that of apes—Gorilla in particular—rather than modern humans, we suggest that the StW 573 morphological pattern appears to reflect adaptations to arboreal behaviors, especially those with the hand positioned above the head, more than human-like manipulatory capabilities. When compared with less complete pectoral girdles from middle/late Miocene apes and that of the penecontemporaneous KSD-VP-1/1 (Australopithecus afarensis), and mindful of consensus views on the adaptiveness of arboreal positional behaviors soliciting abducted glenohumeral joints in early Pliocene taxa, we propose that the StW 573 pectoral girdle is a reasonable model for hypothesizing pectoral girdle configuration of the crown hominin last common ancestor.
... Piecing together scant archaeological and climatic evidence, it is commonly held that the last common ancestor (LCA) of Pan and hominins repeatedly migrated from a forest to a savannah environment from approximately 6-7 Mya (million years ago) (Young et al., 2015). Hominins are thought to have responded to the savannah by developing bipedalism, which was potentially advantageous for numerous reasons, such as longer sightlines, movement efficiency, and social communication. ...
... Mya), Australopithecus possessed similar encephalisation to Pan, and presumably similar social and intellectual sophistication. With the arrival of H. erectus (1.8 Mya), shoulder physiology and loss of body hair support the likelihood of a progressively drier savannah environment; where bipedalism and body heat removal were key advantages in finding calories for a larger brain (Isbell & Young, 1996;Tomasello et al., 2012;Young et al., 2015). A doubling in brain volume from H. habilis (2.1-1.5 Mya) to the later H. erectus, possessing 1100 cm 3 (500 kya), demonstrates exponential encephalisation that at least 300 kya ago ended with H. sapiens' 1200 cm 3 (Hublin et al., 2017;Richter et al., 2017). ...
Article
Full-text available
A perennial challenge of evolutionary psychology is explaining prosocial traits such as a preference for fairness rather than inequality, compassion towards suffering, and an instinctive ability to coordinate within small teams. Considering recent fossil evidence and a novel logical test, we deem present explanations insufficiently explanatory of the divergence of hominins. In answering this question, we focus on the divergence of hominins from the last common ancestor (LCA) shared with Pan. We consider recent fossil discoveries that indicate the LCA was bipedal, which reduces the cogency of this explanation for hominin development. We also review evolutionary theory that claims to explain how hominins developed into modern humans, however it is found that no mechanism differentiates hominins from other primates. Either the mechanism was available to the last common ancestor (LCA) (with P. troglodytes as its proxy), or because early hominins had insufficient cognition to utilise the mechanism. A novel mechanism, sub-group level selection (sGLS) is hypothesised by triangulating two pieces of data rarely considered by evolutionary biologists. These are behavioural dimorphism of Pan (chimpanzees and bonobos) that remain identifiable in modern humans, and the social behaviour of primate troops in a savannah ecology. We then contend that sGLS supplied an exponential effect which was available to LCA who left the forest, but was not sufficiently available to any other primates. In conclusion, while only indirectly supported by various evidence, sGLS is found to be singularly and persuasively explanatory of human's unique evolutionary story.
... Although there is no direct evidence, it is commonly held that the last common ancestor (LCA) of Pan and Homo repeatedly migrated from a forest to a savannah environment from approximately 6-7 Mya (million years ago) (Young, Capellini, Roach, & Alemseged, 2015). ...
... sGLS proposes that since MMU are generally more egalitarian, junior OMU members would demonstrate preferential migration to MMU subgroups (Young et al., 2015). MMU might have also enticed female migration by offering greater choice of sexual partner, which Pan females certainly seek. ...
Thesis
Full-text available
As a thesis by publication, the candidate presents his published or submitted first-author research papers that develop a model to explain the innate capacity of humans to collaborate in egalitarian teams. Group dynamics are comprised of the minutiae of member perceptions and reactions that cohere a group. This research addresses the lack of a compelling (comprehensive, accurate and detailed) model of group dynamics. The word model describes a simplified representation of reality, that may encapsulate multiple theories. By contrast, theory is singular and suggests only partial representation of reality. A model may therefore offer a more complete representation and may achieve the consilience of numerous theories. This thesis formulates the PILAR model and evaluates each of its five Pillars (Prospects, Involved, Liked, Agency, Respect) and 20 interconnecting forces for their collective capacity to characterise a small group. Various empirical and conceptual evaluations allow the candidate to recommend PILAR as a consilience model that credibly integrates numerous theories while representing an extensive assortment of group dynamics. Chapter one Reviews current group dynamics literature; including concepts, models, perspectives, and methodologies. Reasons are proposed for why social and organisational psychology has (arguably) failed to converge upon a compelling baseline model that is consistent with anthropological hominin groups. To demonstrate a potential application of such a model, I examine a practitioner method of organisational devolution, Appreciative Inquiry (AI). The chapter then presents a novel, iterative, method for developing a baseline model of group dynamics that has been adopted by the candidate. Chapter two (published) Proposes PILAR as a baseline model of group dynamics encapsulating a significant proportion of social and group psychology (SGP) theory. PILAR postulates five ostensive constructs (Pillars) that each member is unconsciously influenced by, when moderating their level of effort, or engagement. These five Pillars then prompt various participant behaviours, including both visible actions such as expressing an opinion or aiding another member, and hidden actions such as thought processes, which may only be evident in body language (if at all). Chapters three, four and five (all published) These three chapters examine whether group members use the five Pillars to assess one another’s contribution to a team. A member observing a colleague’s low Pillars may deduce their poor engagement, while higher Pillars suggest significant effort. A member might also collectively evaluate colleagues’ Pillars to assess a group’s overall engagement, either to match this level, or strategically vary from it, for instance to demonstrate leadership (discussed further in §8.3.3). Chapter three considers whether peer assessment data is indicative of a student team’s collective engagement, and therefore team grade. However only a weak correlation between team grade and team engagement is found. Empirical investigation reveals that half of the respondents answered the survey insincerely, as demonstrated by a lack of variance between responses. Recommendations are made for an improved, and shorter, peer assessment instrument to encourage sincere responses. Using an Exploratory Factor Analysis, Chapter four tests whether respondents aligned their item responses in accordance with the five Pillars. Results were as hypothesised, which prompts the candidate to assess whether the five Pillars were present in a popular online peer assessment tool, the Comprehensive Assessment of Team Member Effectiveness (CATME). It is found that CATME’s originating methodology had excluded two Pillars from consideration. High inter-correlations between CATME’s dimensions may have been the result of redundancy as three Pillars were extended over five dimensions. Chapter five reports the design of a brief peer assessment instrument informed by the Pillars, called Pillar-PP, that assesses a respondent’s peer’s perceptions. The chapter concludes with a recommendation to validate Pillar-PP, while also attempting to identify inter-rater bias between respondents. Chapter six (published) To investigate the universality of PILAR, Chapter six attempts unification of two divergent literatures, one positivist and one constructivist. Regarding the positivist literature, it was postulated that should PILAR accurately represent the small group, its Pillars may be able to categorise industrial and organisational psychology (IOP) constructs, since organisations are constituted by (albeit, hierarchical) teams. Regarding the constructivist literature, AI is action research that facilitates the formation of egalitarian team to undertake ad hoc projects. Chapters seven (published) and eight (submitted) These two chapters develop an evolutionary story behind a postulated baseline model. Chapter seven contends that sub-group level selection (sGLS) selected for pre-verbal anthropological prosociality. Chapter eight extends sGLS by considering how hominins and modern humans moderate their engagement as hierarchy steepness varies. Chapter nine (submitted) Assesses to extent to which Pillars are represented within a systematically selected set of constructs used for group research. It is found that approximately 80% of constructs conceptually align with one Pillar, which suggests that PILAR constitutes a baseline model. Chapter ten (published) Applies PILAR to two growing societal problems, mental health and precarious employment. I develop a model that connects the five Pillars with wellbeing via constructs associated with positive psychology. Each Pillar is postulated as only being reliably achievable when a member possesses the respective dimension of psychological capital (PsyCap). Furthermore, that participation in the team delivers the member each of five basic psychological needs (BPN). When examined in the context of low-status, precarious, employment, a novel public policy for increasing population wellbeing is presented. Chapter eleven The conclusion summarises the sequence of postulates developed through the course of the thesis. Policy and theory implications were then explored, followed by chapter-specific limitations that are potentially significant in aggregation. The thesis ends with a contention that a unique methodology allows deeper insights than ordinarily possible in a dynamically complex problem space.
... Functionally, knuckle walking reduces external moments at the MCP joints despite the retention of (36). The suspensory hand of Ar. ramidus, its terrestrial plantigrade foot posture (5), and the retention of knuckle-walking features in the wrists of early hominins (1), as well as other African ape-like regions of the skeleton (53)(54)(55), provide indirect support for the knuckle-walking hypothesis. Our evolutionary modeling analyses and ancestral estimations strongly support a more Pan-like, rather than monkey-like, hand morphology for the Homo-Pan LCA, which raises the critical question of which hand posture the LCA would have used if it was not a knuckle walker. ...
... Therefore, suspension, vertical climbing, and knuckle walking are naturally linked from both functional and evolutionary perspectives. Ultimately, the definitive resolution of the knuckle-walking hypothesis relies on the recovery of direct fossil evidence of chimpanzee and gorilla postcranial evolutionary history, but we interpret the preponderance of the available fossil and comparative evidence to support hypotheses of a large-bodied, semiterrestrial, knuckle-walking LCA with adaptations to climbing, suspension, and heel-strike plantigrady (1,5,40,(53)(54)(55)81). ...
Article
Full-text available
The morphology and positional behavior of the last common ancestor of humans and chimpanzees are critical for understanding the evolution of bipedalism. Early 20th century anatomical research supported the view that humans evolved from a suspensory ancestor bearing some resemblance to apes. However, the hand of the 4.4-million-year-old hominin Ardipithecus ramidus purportedly provides evidence that the hominin hand was derived from a more generalized form. Here, we use morphometric and phylogenetic comparative methods to show that Ardipithecus retains suspensory adapted hand morphologies shared with chimpanzees and bonobos. We identify an evolutionary shift in hand morphology between Ardipithecus and Australopithecus that renews questions about the coevolution of hominin manipulative capabilities and obligate bipedalism initially proposed by Darwin. Overall, our results suggest that early hominins evolved from an ancestor with a varied positional repertoire including suspension and vertical climbing, directly affecting the viable range of hypotheses for the origin of our lineage.
... Green and Alemseged suggested that the DIK-1-1 scapulae were most similar to those of Gorilla juveniles 38 , and when considered alongside other adult australopith scapulae (e.g., KSD-VP-1/1 and A.L. 288-1), the growth of the A. afarensis shoulder may have followed an ape-like trajectory, which was supported by its dental development 36,39 . Analysis of another A. afarensis scapula from Woranso-Mille, Ethiopia (KSD-VP-1/1) 40 , a potential large male individual dated around 3.6 Ma 41 , did not present such an apelike model of the adult australopith shoulder blade 38,[42][43][44] . The KSD-VP-1/1 scapula preserves more derived features relative to DIK-1-1, though differences between them do not appear to exceed the magnitude of ontogenetic variation that may exist within a living species (and across sexes) 42,43 . ...
... Specifically, the KSD-VP-1/1 scapula is different from that of African apes in having a less cranial orientation of the spine as well as features linked with a manipulatory function of the upper limb, such as the infraspinous fossa expansion. Further research on the Dikika specimen hypothesized its adult morphology using different ontogenetic primate trajectories and suggested an ape-like adult shape for it, in contrast to what was found in the KSD-VP-1/1 scapula 44 . In this context, "ape-like" refers to a mediolaterally narrow scapula with a cranially oriented glenoid and acromion, hypothesized as the plesiomorphic condition. ...
Article
Full-text available
Two well-preserved, subadult 800 ky scapulae from Gran Dolina belonging to Homo antecessor, provide a unique opportunity to investigate the ontogeny of shoulder morphology in Lower Pleistocene humans. We compared the H. antecessor scapulae with a sample of 98 P. troglodytes and 108 H. sapiens representatives covering seven growth stages, as well as with the DIK-1-1 (Dikika; Australopithecus afarensis), KNM-WT 15000 (Nariokotome; H. ergaster), and MH2 (Malapa; A. sediba) specimens. We quantified 15 landmarks on each scapula and performed geometric morphometric analyses. H. sapiens scapulae are mediolaterally broader with laterally oriented glenoid fossae relative to Pan and Dikika shoulder blades. Accordingly, H. antecessor scapulae shared more morphological affinities with modern humans, KNM-WT 15000, and even MH2. Both H. antecessor and modern Homo showed significantly more positive scapular growth trajectories than Pan (slopes: P. troglodytes = 0.0012; H. sapiens = 0.0018; H. antecessor = 0.0020). Similarities in ontogenetic trajectories between the H. antecessor and modern human data suggest that Lower Pleistocene hominin scapular development was already modern human-like. At the same time, several morphological features distinguish H. antecessor scapulae from modern humans along the entire trajectory. Future studies should include additional Australopithecus specimens for further comparative assessment of scapular growth trends.
... By showing that a logical prerequisite for free hand percussion, free hand hitting, can already be part of the natural developing behavioral repertoire of one of our closest relatives, gorillas, our study helps to shed light on the likely range of requirements and potential sources for the emergence of such stone tool production and use during human evolution. Particularly, even though throughout human evolution tool use behavior may have increased alongside a gradual evolution of human-like morphology 71 , our current knowledge on extant non-human primates underlines that species with very different skeletal morphologies and locomotor patterns (e.g. arboreal capuchins and semi-terrestrial western gorillas) have the biomechanical and morphofunctional capacity to knock two rocks together. ...
Article
Full-text available
The earliest stone tool types, sharp flakes knapped from stone cores, are assumed to have played a crucial role in human cognitive evolution. Flaked stone tools have been observed to be accidentally produced when wild monkeys use handheld stones as tools. Holding a stone core in hand and hitting it with another in the absence of flaking, free hand hitting, has been considered a requirement for producing sharp stone flakes by hitting stone on stone, free hand percussion. We report on five observations of free hand hitting behavior in two wild western gorillas, using stone-like objects (pieces of termite mound). Gorillas are therefore the second non-human lineage primate showing free-hand hitting behavior in the wild, and ours is the first report for free hand hitting behavior in wild apes. This study helps to shed light on the morphofunctional and cognitive requirements for the emergence of stone tool production as it shows that a prerequisite for free hand percussion (namely, free hand hitting) is part of the spontaneous behavioral repertoire of one of humans’ closest relatives (gorillas). However, the ability to combine free hand hitting with the force, precision, and accuracy needed to facilitate conchoidal fracture in free hand percussion may still have been a critical watershed for hominin evolution.
... Kuhn, 2015;Roach et al., 2013;Roach & Richmond, 2015). Young et al. (2015) and Feuerriegel et al. (2017) argue that this adaptation came at the expense of a reduced ability to use arboreal niches, meeting the criteria proposed by Wood and Strait (2004) to support compelling morphological evidence of evolution toward carnivorous stenotopy. ...
Article
The human trophic level (HTL) during the Pleistocene and its degree of variability serve, explicitly or tacitly, as the basis of many explanations for human evolution, behavior, and culture. Previous attempts to reconstruct the HTL have relied heavily on an analogy with recent hunter‐gatherer groups' diets. In addition to technological differences, recent findings of substantial ecological differences between the Pleistocene and the Anthropocene cast doubt regarding that analogy's validity. Surprisingly little systematic evolution‐guided evidence served to reconstruct HTL. Here, we reconstruct the HTL during the Pleistocene by reviewing evidence for the impact of the HTL on the biological, ecological, and behavioral systems derived from various existing studies. We adapt a paleobiological and paleoecological approach, including evidence from human physiology and genetics, archaeology, paleontology, and zoology, and identified 25 sources of evidence in total. The evidence shows that the trophic level of the Homo lineage that most probably led to modern humans evolved from a low base to a high, carnivorous position during the Pleistocene, beginning with Homo habilis and peaking in Homo erectus. A reversal of that trend appears in the Upper Paleolithic, strengthening in the Mesolithic/Epipaleolithic and Neolithic, and culminating with the advent of agriculture. We conclude that it is possible to reach a credible reconstruction of the HTL without relying on a simple analogy with recent hunter‐gatherers' diets. The memory of an adaptation to a trophic level that is embedded in modern humans' biology in the form of genetics, metabolism, and morphology is a fruitful line of investigation of past HTLs, whose potential we have only started to explore.
Chapter
Schimpansen leben in einem polygynandrienen Paarungssystem, in dem sich Weibchen mit mehreren Männchen und Männchen mit mehreren Weibchen paaren. Vermutlich haben sich Menschen nach dem pan-homo Split vor ca. 7 Millionen Jahren von einem polygynandrienen zu einem polygynen (Harem) und dann zu einem überwiegend monogamen Paarungssystem entwickelt. Die Sexualität des Jetzt-Menschen zeigt zugleich Merkmale des älteren polygynen und des neueren monogamen Paarungssystems. In diesem Kapitel werden zahlreiche Beispiele von Anpassungen an das ältere und an das jüngere Paarungssystem des Menschen erläutert. Im Ergebnis bedeutet es, dass wir Menschen ein sexuelles Mischwesen sind. Daraus können sich Probleme in unserer Sexualität und Partnerschaft ergeben. Die Kenntnis dieser sehr verschiedenen sexuellen Strategien des Jetzt-Menschen hilft, die eigene Sexualität und insbesondere die des Gegengeschlechts besser zu verstehen und eine gute Sexualtherapie zu machen.
Article
Objectives: One of the most contentious issues in paleoanthropology is the nature of the last common ancestor of humans and our closest living relatives, chimpanzees and bonobos (panins). The numerical composition of the vertebral column has featured prominently, with multiple models predicting distinct patterns of evolution and contexts from which bipedalism evolved. Here, we study total numbers of vertebrae from a large sample of hominoids to quantify variation in and patterns of regional and total numbers of vertebrae in hominoids. Materials and methods: We compile and study a large sample (N = 893) of hominoid vertebral formulae (numbers of cervical, thoracic, lumbar, sacral, caudal segments in each specimen) and analyze full vertebral formulae, total numbers of vertebrae, and super-regional numbers of vertebrae: presacral (cervical, thoracic, lumbar) vertebrae and sacrococcygeal vertebrae. We quantify within- and between-taxon variation using heterogeneity and similarity measures derived from population genetics. Results: We find that humans are most similar to African apes in total and super-regional numbers of vertebrae. Additionally, our analyses demonstrate that selection for bipedalism reduced variation in numbers of vertebrae relative to other hominoids. Discussion: The only proposed ancestral vertebral configuration for the last common ancestor of hominins and panins that is consistent with our results is the modal formula demonstrated by chimpanzees and bonobos (7 cervical-13 thoracic-4 lumbar-6 sacral-3 coccygeal). Hox gene expression boundaries suggest that a rostral shift in Hox10/Hox11-mediated complexes could produce the human modal formula from the proposal ancestral and panin modal formula.
Article
Full-text available
This philosophical study focuses on the possibility, inference, and theoretical position of scientific knowledge with a critique of Popperian and Lakatosian ideas in regards to the scientific procedure, after a comprehensive investigation of the fundamental skeptical arguments of philosophy having the potential to undermine the establishment of scientific knowledge along with a threat to human knowledge altogether. Albeit the Agrippan Problem, at first, seems to threaten the possibility of not only scientific knowledge, but human knowledge entirely, it can be solved in concur with the examination of Cartesian skepticism through the constitution of an ontological ground upon which reality is constructed; this allows to set basic beliefs—human knowledge is possible. Subsequently, espousing realist and materialist scheme of reality, in parallel with basic beliefs posed by the scheme, renders the survey of scientific knowledge possible, by virtue of the reliance upon sensory experience. Nevertheless, the attack of inductive skepticism against the scientific methodology by repudiating inductive inferences in science casts a shadow over the possibility and inference of scientific knowledge. Yet, the existence of certain, verified, and irrefutable hypotheses evidently shows the possibility of and by the use induction to some extent, revealing the impossibility of falsifiability and applying deductive reasoning demonstrate the inference of scientific knowledge. Furthermore, within a theoretical framework wherein verified hypotheses —scientific knowledge— are positioned in the hardcore and updatable hypotheses are located in the protective belt, more systematic and comprehensive inferences and more accurate predictions can be made.
Article
Full-text available
Almost a century and a half ago, Charles Darwin in The Descent of Man (1871: 141) highlighted the evolution of bipedalism as one of the key features of the human lineage, freeing the hands for carrying and for using and making tools. But how did it arise? The famous footprints from Laetoli in Tanzania show that hominin ancestors were walking upright by at least 3.65 million years ago. Recent work, however, suggests a much earlier origin for bipedalism, in a Miocene primate ancestor that was still predominantly tree-dwelling. Here Susannah Thorpe, Juliet McClymont and Robin Crompton set out the evidence for that hypothesis and reject the notion that the common ancestor of great apes and humans was a knuckle-walking terrestrial species, as are gorillas and chimpanzees today. The article is followed by a series of comments, rounded off by a reply from the authors.
Article
Full-text available
The oldest direct evidence of stone tool manufacture comes from Gona (Ethiopia) and dates to between 2.6 and 2.5 million years (Myr) ago 1 . At the nearby Bouri site several cut-marked bones also show stone tool use approximately 2.5 Myr ago 2 . Here we report stone-tool-inflicted marks on bones found during recent survey work in Dikika, Ethiopia, a research area close to Gona and Bouri. On the basis of low-power microscopic and environmental scanning electron microscope observations, these bones show unambiguous stone-tool cut marks for flesh removal and percussion marks for marrow access. The bones derive from the Sidi Hakoma Member of the Hadar Formation. Established 40 Ar– 39 Ar dates on the tuffs that bracket this member constrain the finds to between 3.42 and 3.24 Myrago, and stratigraphic scaling between these units and other geological evidence indicate that they are older than 3.39 Myr ago. Our discovery extends by approximately 800,000 years the antiquity of stone tools and of stone-tool-assisted consumption of ungulates by hominins; furthermore, this behaviour can now be attributed to Australopithecus afarensis.
Article
Full-text available
The phylogenetic relationships of several hominin species remain controversial. Two methodological issues contribute to the uncertainty-use of partial, inconsistent datasets and reliance on phylogenetic methods that are ill-suited to testing competing hypotheses. Here, we report a study designed to overcome these issues. We first compiled a supermatrix of craniodental characters for all widely accepted hominin species. We then took advantage of recently developed Bayesian methods for building trees of serially sampled tips to test among hypotheses that have been put forward in three of the most important current debates in hominin phylogenetics-the relationship between Australopithecus sediba and Homo, the taxonomic status of the Dmanisi hominins, and the place of the so-called hobbit fossils from Flores, Indonesia, in the hominin tree. Based on our results, several published hypotheses can be statistically rejected. For example, the data do not support the claim that Dmanisi hominins and all other early Homo specimens represent a single species, nor that the hobbit fossils are the remains of small-bodied modern humans, one of whom had Down syndrome. More broadly, our study provides a new baseline dataset for future work on hominin phylogeny and illustrates the promise of Bayesian approaches for understanding hominin phylogenetic relationships. © 2015 The Author(s).
Article
Full-text available
Human evolutionary scholars have long supposed that the earliest stone tools were made by the genus Homo and that this technological development was directly linked to climate change and the spread of savannah grasslands. New fieldwork in West Turkana, Kenya, has identified evidence of much earlier hominin technological behaviour. We report the discovery of Lomekwi 3, a 3.3-million-year-old archaeological site where in situ stone artefacts occur in spatiotemporal association with Pliocene hominin fossils in a wooded palaeoenvironment. The Lomekwi 3 knappers, with a developing understanding of stone’s fracture properties, combined core reduction with battering activities. Given the implications of the Lomekwi 3 assemblage for models aiming to converge environmental change, hominin evolution and technological origins, we propose for it the name ‘Lomekwian’, which predates the Oldowan by 700,000 years and marks a new beginning to the known archaeological record.
Article
Full-text available
The fossil record is a unique repository of information on major morphological transitions. Increasingly, developmental, embryological, and functional genomic approaches have also conspired to reveal evolutionary trajectory of phenotypic shifts. Here, we use the vertebrate appendage to demonstrate how these disciplines can mutually reinforce each other to facilitate the generation and testing of hypotheses of morphological evolution. We discuss classical theories on the origins of paired fins, recent data on regulatory modulations of fish fins and tetrapod limbs, and case studies exploring the mechanisms of digit loss in tetrapods. We envision an era of research in which the deep history of morphological evolution can be revealed by integrating fossils of transitional forms with direct experimentation in the laboratory via genome manipulation, thereby shedding light on the relationship between genes, developmental processes, and the evolving phenotype.
Article
Full-text available
Australopithecus fossils were regularly interpreted during the late 20th century in a framework that used living African apes, especially chimpanzees, as proxies for the immediate ancestors of the human clade. Such projection is now largely nullified by the discovery of Ardipithecus. In the context of accumulating evidence from genetics, developmental biology, anatomy, ecology, biogeography, and geology, Ardipithecus alters perspectives on how our earliest hominid ancestors--and our closest living relatives--evolved.
Chapter
It is not the purpose of this chapter to provide definitive answers to any of the questions asked in its title, even though various aspects of these questions have formed a large part of the lively debate that has been conducted in recent years concerning Miocene hominoid postcrania. The material available for investigation has been increased significantly recently by new specimens from the early Miocene of East Africa [KNM-RU 2036C and KNM-RU 5872 specimens (Walker and Pickford, this volume, Chapter 12)], the later Miocene of Rudabánya, Hungary [Rud specimens (Morbeck, this volume, Chapter 14)], and the Potwar Plateau of Pakistan [most GSP specimens (Pilbeam et al., 1980)]. The main purpose of this chapter is to make some general comments on functional features of the morphology of some Miocene hominoid postcrania and on possible positional capabilities consistent with those features. Similarities to and differences from features of Miocene species evident in the postcrania of groups of living higher primates will be made purely in terms of function. Attention will be directed toward the larger bodied Miocene hominoids. Original specimens of all the East African and Asian material have been examined. The European material has been examined in cast form.