Science-2015-Alba- (1)
RESEARCH ARTICLE SUMMARY
tral morphotype from which extant hominoids (apes and humans)evolved is complicated by the mosaic nature of ape evolution,the con-founding effects of independently evolved features (homoplasy),and the virtual lack of hylobatids (gibbons and siamangs)in the Miocene fossil record.For several decades,small-bodied an-thropoid
primates from Africa and Eurasia have not played an important role in this de-bate,because they generally lack the shared derived features of extant catarrhines (homi-noids and Old World monkeys)and are thus considered to precede their divergence.Even some small-bodied catarrhines from Africa (dendropithecids),considered to be stem hom-inoids by some authors,are viewed as more
Proconsul .This has led to the assumption that hylobatids are a dwarfed lineage that evolved from a larger-bodied and more great ape –like common ancestor with hominids (great apes and humans).
RATIONALE:Here we describe a new genus of
small-bodied (4to 5kg)ape from the Miocene (11.6Ma),discovered in the Abocador de Can Mata stratigraphic series (Vallès-Penedès Ba-sin,northeast Iberian Peninsula),that chal-lenges current views on the last common ancestor of extant hominoids.This genus is based on a partial skeleton that enables a reliable reconstruction of cranial morphol-ogy and a detailed assessment of elbow and
wrist anatomy.It exhibits a mosaic of primi-tive (stem catarrhine –like)and derived (extant hominoid –like)features that forces us to re-evaluate the role played by small-bodied catar-rhines in ape evolution.
RESULTS:The new genus retains some fea-
tures that are suggestive of generalized above-branch quadrupedalism,but it possesses more extensive hominoid-like postcranial features (mostly related to enhanced forearm rotation and ulnar deviation capabilities)than those convergently displayed by atelids.Its overall body plan is more compatible with an empha-sis on cautious and eclectic climbing,combined with some degree of below-branch forelimb-dominated suspension (although less acro-batic than in extant gibbons).Its relative brain
size implies a monkey-like
degree of encephalization (similar to that of hylo-batids but below that of great apes),and dental microwear indicates a fru-givorous diet.From aphylo-genetic viewpoint,the new genus combines craniodental and postcranial primitive features (similar to those of dendropithecids)with mul-tiple derived cranial and postcranial features shared with extant hominoids.Some cranial similarities with gibbons would support a closer phylogenetic link between the new genus and hylobatids.However,this possibility is not sup-ported by the total evidence.A cladistic analysis based on more than 300craniodental and postcranial features reveals that the new genus is a stem hominoid (preceding the divergence between hylobatids and hominids),although more derived than previously known small catarrhines and Proconsul .
CONCLUSION:As the first known Miocene
small-bodied catarrhine to share abundant derived features with extant hominoids,the new genus indicates a greater morphological diversity than previously recognized among this heterogeneous group,and it provides key insight into the last common ancestor of hy-lobatids and hominids.Our cladistic results,coupled with the chronology and location of the new genus,suggest that it represents a late-surviving offshoot of a small African stem hominoid that is more closely related to crown hominoids than Proconsul is.These results sug-gest that,at least in size and cranial morphology,the last common ancestor of extant hominoids might have been more gibbon-like (less great ape –like)than generally assumed.
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The list of author affiliations is available in the full article online.*Corresponding author.E-mail:david.alba@icp.cat
Cite this article as D.M.Alba et al .,Science 350,aab2625(2015).DOI:10.1126/science.aab2625
Cranial reconstruction and life appearance.Artist ’s representation of the cranial recon-struction (in frontal view)and of the life appearance (in lateral oblique view)of the new genus of small-bodied ape from the Iberian Miocene.[Artwork by M.Palmero]Read the full article
at http://dx.doi.
org/10.1126/science.aab2625..................................................
o n D e c e m b e r 12, 2015
w w w .s c i e n c e m a g .o r g D o w n l o a d e d f r o m
RESEARCH ARTICLE
Old World monkeys(cercopithecoids)by
the Oligocene[≥25million years ago(Ma)]
(1,2)and subsequently diversified in both
Africa and Eurasia during the Miocene (23to~5Ma)(3).They are currently represented by crown hominoids(4)—i.e.,the small-bodied hylobatids(gibbons and siamangs)and the larger-bodied hominids(great apes and humans),which diverged from one another by the early Miocene (~17Ma)(1).Reconstructing the ancestral morpho-type from which extant apes and humans evolved is a challenging task(5–7),given the mosaic nature of evolution(8),the confounding effects of inde-pendently evolved features(homoplasy)(5,9),the conflicting evidence provided by Miocene great apes(6,9),and the incomplete and fragmentary nature of the hominoid fossil record[in particular, the virtual lack of fossil gibbons until at least the latest Miocene(10,11)].Thus,although extant hominoids share numerous derived features,par-ticularly in the trunk and forelimb,it is uncertain to what extent these characteristics were inherited from their last common ancestor,whose morpho-type is still under discussion(5,6,11,12).
The earliest hypotheses postulated a small-bodied gibbon-like ancestor(13),and for many primates from Africa and Eurasia)were consid-
ered to be broadly ancestral to gibbons(14,15).
Today,hylobatids are generally considered to be
a specialized and probably dwarfed lineage,
evolved from a larger and more great ape–like last
common ancestor with hominids(6,16).This is
because known small-bodied extinct catarrhines,
such as the African dendropithecids(including at
least Dendropithecus,Simiolus,and Micropithecus)
and the Eurasian pliopithecoids(Pliopithecus,
Epipliopithecus,and allied genera),lack most of
the synapomorphies(shared derived features)of
crown catarrhines(17–21).Even dendropithecids,
which are more derived than pliopithecoids and
are currently interpreted by some authors as stem
hominoids(preceding the hylobatid-hominid di-
vergence)(3,8,22),are considered to be more
basal than the stem ape Proconsul(8,21–23).Here
we describe a new Miocene small-bodied ape from
Spain,Pliobates cataloniae gen.et sp.nov.(24).
In some primitive features,this new primate re-
sembles previously known small-bodied catarrhines
such as dendropithecids,but it differs from them
and from Proconsul by displaying multiple crown-
hominoid derived features.This mosaic provides
key insight into ape evolution by forcing us to re-
evaluate the role played by small-bodied catarrhines
in the emergence of crown hominoids.
Provenance
The new taxon is described on the basis of a par-
tial skeleton(IPS58443;table S1)that is perma-
nently housed in the collections of the Institut
Catalàde Paleontologia Miquel Crusafont(ICP)in
Sabadell,Spain.The main cranial fragments were
initially discovered on3January2011by a team
of paleontologists from the company FOSSILIA
Serveis Paleontològics i Geològics,directed by
one of the authors(J.M.R.),while overseeing the
excavation works performed by digging machines
at the Can Mata landfill(els Hostalets de Pierola,
Catalonia,Spain).In the following days,post-
cranial elements were found at the field during
excavation of the same stratigraphic level,and
the remaining postcranial small bones and other
small fragments were subsequently recovered by
screen-washing the excavated sediments.All the
fossils therefore come from a single horizon,which
was labeled ACM/C8-A4(Abocador de Can Mata,
Cell8,sector A,locality4).
The ACM local stratigraphic composite series
(25–27)is located in the Vallès-Penedès Basin
(northeast Iberian Peninsula),a half-graben trend-
ing north-northeast–south-southwest and limited
by the Catalan Coastal Ranges;this structure was
generated by the rifting of the northwest Medi-
terranean during the Neogene(28,29).The basin
infill mostly consists of marginal alluvial fan sed-
iments that have provided a rich fossil record of
Miocene terrestrial vertebrates(30).The area of
els Hostalets de Pierola has thick middle to late
Miocene sequences that were deposited in distal-
to-marginal inter-fan zones of coalescing alluvial
fan systems(27).The ACM composite series,about
250m in thickness,includes more than200for-
mally defined localities that can be accurately
dated based on lithostratigraphic,magnetostrati-
graphic,and biostratigraphic correlation(26,27,31).
The whole series is late Aragonian,and,based on
updated chron boundaries(32),it spans from~12.6
to11.5Ma.Locality ACM/C8-A4is correlated to
chron C5r.2n(11.657to11.592Ma)with an in-
terpolated age of11.628Ma,which is close to the
middle/late Miocene boundary,as defined by the
base of the Tortonian and currently dated to
11.625Ma(32).
Methods
Cranial reconstruction
The cranium was preserved in a main piece
(IPS58443.1)with parts of the neurocranium,
basicranium,muzzle,and right maxilla(Fig.1,A
to C);a medium-sized fragment with the left max-
illa(IPS58443.2);and other smaller fragments
that were found in close spatial association or re-
covered by screen-washing the surrounding sedi-
ments.These other fragments include part of the
occipital and right parietal(IPS58443.3),the right
glenoid region(IPS58443.4),the right occipital
condyle(IPS58443.5),a fragment of the right orbit-
al margin(IPS58443.6),the left orbital margin and
temporal process of the zygomatic(IPS58443.12),a
parietal fragment(IPS58443.11),and several other
minor fragments whose location cannot be de-
termined(IPS58443.7to IPS58443.10,IPS58443.13,
and IPS58443.37).The mandible was not pre-
served,except for a fragment of the right ramus
with the condyle(IPS58443.14).The main frag-
ment(IPS58443.1)is composed of several bone
fragments that are crushed against each other
and somewhat displaced from their anatomical
position,but(like the remaining specimens)not
plastically distorted.
Several bone fragments of IPS58443.1were in-
dividualized through careful mechanical prepara-
tion,but for many other bone fragments,their
1Institut Catalàde Paleontologia Miquel Crusafont(ICP), Universitat Autònoma de Barcelona(UAB),Edifici ICTA-ICP, Carrer de les Columnes sense número,Campus de la UAB, 08193Cerdanyola del Vallès,Barcelona,Spain.2Center for the Advanced Study of Human Paleobiology,Department of Anthropology,The George Washington University, Washington,DC20052,USA.3FOSSILIA Serveis Paleontològics i Geològics,Jaume I87,5è1a,08470Sant Celoni,Barcelona,Spain.4InstitucióCatalana de Recerca i Estudis Avan?ats at ICP and Unitat d’Antropologia Biològica (Department de Biologia Animal,de Biologia Vegetal i
d'Ecologia),Universitat Autònoma de Barcelona,Edifici ICTA-ICP,Carrer de les Columnes sense número,Campus de la UAB,08193Cerdanyola del Vallès,Barcelona,Spain.
*Corresponding author.E-mail:david.alba@icp.cat
fragility and state of preservation precluded a complete isolation from each other and/or from the embedding matrix.Therefore,for conserva-tional reasons,no complete preparation of the specimen was performed,and a virtual three-dimensional (3D)reconstruction was undertaken instead.The larger specimens (IPS58443.1and IPS58443.2)were scanned at the American Mu-seum of Natural History (New York)with a high-resolution computed tomograph (CT)system (Phoenix v|tome|x s180,General Electric Mea-surement &Control Solutions,Hanover,Germany),using a nanofocus x-ray tube.Different protocols were used for these two cranial fragments:160kV voltage,1.4mA current,0.2mm Cu filter,and magnification of 2.10013075,obtaining 1600slices (virtual cross-sectional images)of 0.2mm in thickness and a pixel size of 0.09523217mm (IPS58443.1);and 145kV voltage,1.3mA current,0.1mm Cu filter,and a magnification of 2.93159482,obtaining 1500slices of 0.2mm in thickness and a pixel size
of 0.06822225mm (IPS58443.2).Raw CT data were imported into VGStudio Max 2.1and exported (as a stack of TIFF files)to Avizo 7.0and Geomagic 2012for segmentation,reposition-ing,mirroring,and/or visualization.CT-scanned bone fragments were segmented slice by slice by digitally removing the matrix with the aid of dif-ferential bone and sediment densities,using the semiautomatic thresholding tools of Avizo 7.0.Ad-ditional small isolated bone fragments not sur-rounded by matrix were scanned with a 3D desktop laser scanner (NextEngine)at high definition and with a dimensional accuracy of 0.13mm (Macro Mode);the resulting 3D models were exported to Geomagic 2012to align and repair the meshes.The preserved bone fragments generally had clean fractures that allowed them to be easily matched with other fragments.Up to 393D virtual models of bone fragments,including pieces of the pre-maxillae and maxillae with teeth,lacrimals,zygo-matics,frontal,parietals,temporals,occipital,and pterygoids,were thus digitally assembled and re-positioned using Avizo 7.0and Geomagic 2012on
the basis of preserved morphology,fracture con-gruence,and bilateral symmetry.Once the pre-served fragments were adequately positioned,areas preserved only in one side of the cranium were mirrored.The individual models were then merged to obtain the definitive 3D virtual model,which was also 3D-printed with a ZPrinter 450at the Universitat Autònoma de Barcelona for visuali-zation and comparative purposes.
To reconstruct the muzzle area,we primarily relied on IPS58443.1,in which the right premaxilla (with the alveoli for I1to C1)and the maxilla (with P3to M3,the lower portion of the nasal aperture,most of the palatine process,and the in-termaxillary suture)are almost completely pre-served.The left maxillary specimen (IPS58443.2)is less complete and only includes the M2to M3series and a smaller portion of the intermaxillary suture,as well as the zygomatic root.Palate width and shape were thus reconstructed by mirroring the right fragment onto the left one,then further adjusting it based on the fit onto the left portion of the intermaxillary suture and the alignment with the left molars.With regard to the orbital area,although the orbits are not completely pre-served on either side,their profile can be re-constructed with reasonable accuracy based on the available fragments:IPS58443.1includes,in several fragments,most of the interorbital area of the frontal and the superior orbital rims,the maxillary portion of the right inferior orbital rim,a zygomatic portion of the right lateral orbital rim,and both lacrimals;IPS58443.12includes a larger lateral portion of the left orbit that en-compasses part of the temporal process of the zygomatic arch and the frontomaxillary suture.Although the zygomaticomaxillary suture is not preserved on either side,the missing portion of the zygomatic process of the maxilla on the left side is minimal.Therefore,it is possible to situate the left orbit relative to the muzzle,on the basis of the orientation between the zygomatic process of IPS58443.12and the zygomatic root preserved in IPS58443.2.Similarly,although the frontozy-gomatic suture is not preserved at the end of the left zygomatic process of IPS58443.1,only a very small portion is missing;thus,the preservation of the suture in the zygomatic portion of the lateral orbital rim in IPS58443.12enables a reliable re-construction of the superolateral aspect of the orbit,based on the curvature of these two frag-ments.The inferior orbital rim can be also re-constructed using its right maxillary portion,which is preserved in IPS58443.1,by mirroring onto the left side.Moreover,the preservation of both su-perior orbital rims in the frontal fragments of IPS58443.1further allows the right orbit to be positioned relative to the muzzle,in spite of the fact that the right zygomaticomaxillary suture is not preserved.Overall,although the missing fragments of the orbital rims introduce some de-gree of uncertainty,the curvature of the various preserved portions enables a confident reconstruc-tion of orbital size and shape.The preserved portions of the zygomatic and maxilla further enable reliable positioning of the orbits relative to the muzzle.Because the missing portions
Fig.1.Cranium and dentition.(A to C )Cranium of the holotype (IPS58443)of Pliobates cataloniae gen.et sp.nov.The main cranial fragments,including the basicranium and the right palate,are shown in basal view (A);details of the right palatal fragment are shown in left-lateral (B)and right-lateral (C)views.(D )Detail of the right postcanine teeth,in occlusal view (mesial is to the right).
RESEARCH |RESEARCH ARTICLE
are very small,other possible reconstructions do not differ substantially from the one provided here.
To reconstruct the neurocranium,we relied on the relative spatial position of the braincase frag-ments in the crushed main specimen(IPS58443.1). Because these fragments are not plastically de-formed,they show the original curvature of the braincase,which considerably facilitated the re-construction of its overall shape.The frontals are preserved in six fragments that enable the re-construction of most of the braincase morphology (including the whole supraorbital area and the connection with the parietals on the left side).The parietals are preserved in19fragments,which have well-preserved sutures and neat fractures. The latter fact,together with the spatial associ-ation among the various fragments,enables the reconstruction of the posterior contour of the cra-nial https://www.wendangku.net/doc/9b19080077.html,rge portions of both temporals,in-cluding the tympanic bullae,are also preserved in IPS58443.1.The right temporal is more com-pletely preserved than the left one;it includes not only the glenoid fossa and the temporal process of the zygomatic arch,but also the suture with the parietal.These preserved pieces,mirrored onto the left side,enabled the reconstruction of the lateral aspects of the neurocranium.The occipi-tals are less completely preserved,being restricted to three basioccipital fragments and one occipital fragment,which include the occipital condyles and enable a reliable orientation of the preserved profile of the foramen magnum.One of these fragments connects with the left temporal,thereby enabling the reconstruction of the basicranium. Only minor displacements,caused by diagenesis, had to be corrected;these included displacements between the left bulla and the left occipital con-dyle and basioccipital,and the artifactual separa-tion of the occipital-temporal suture.Once these elements were slightly repositioned into their cor-rect anatomical place,they fit congruently with the surrounding https://www.wendangku.net/doc/9b19080077.html,st,the pterygoid wings are also preserved on the right side,attached to the palatine but slightly crushed,so that some realignment of this bone was necessary.The con-nection of the braincase with the superior portion of the face is possible through the frontal frag-ments,which on the left side are continuous with the parietal fragments.The connection between the braincase and the lower portion of the face is possible,not only because of the preservation of the superior orbital rims in the frontal and of a maxillary portion of the right inferior orbital rim, but also because part of the right pterygoid wing (anatomically adjacent to the palatine)was pre-served in its original anatomical position,attached to one of the bone fragments of IPS58443.1(which includes a large portion of the basicranium and temporal).This pterygoid fragment enables a re-liable reconstruction of the relative position of the muzzle and the neurocranium via the basicranium, and it further confirms the correctness of the re-construction of orbital shape and position.The position of the muzzle was further tested on the basis of the congruent alignment on the right side between the temporal process of the zygomatic in IPS58443.12and the zygomatic process of the
temporal in IPS58443.4.
Dental measurements and body
mass estimation
Standard dental measurements of mesiodistal
length(MD)and maximum buccolingual breadth
(BL)were taken(in millimeters)to assess dental
size and proportions by means of comparative
bivariate plots of log-transformed BL versus MD
for each of the upper molars.Data for extant and
extinct small-bodied catarrhines were taken from
the literature(17,33–46)or measured by one of
the authors(D.M.A.).Based on MD and BL mea-
surements,tooth square area(A,in square mil-
limeters)was computed for postcanine teeth to
estimate the body mass(BM,in kilograms)of
Pliobates,using allometric equations of BM versus
A(47).BM of Pliobates and,for comparative pur-
poses,of Epipliopithecus vindobonensis was also
estimated based on allometric equations,using
postcranial estimators(48)separately for samples
of hominoids and catarrhines(i.e.,hominoids
plus cercopithecoids),based on sex-species mean
data.Six postcranial BM estimators were used
(49),including three surface areas(for the tibia,
humerus,and radius)and three linear measure-
ments(for the humerus and radius;tables S2
and S3).
Humeral torsion and arm angle
Humeral torsion,or the orientation of the hu-
meral head relative to the mediolateral axis of
the distal humerus(50),cannot be directly com-
puted in the described skeleton because the
humeral head is missing.Accordingly,humeral
torsion was kindly estimated by https://www.wendangku.net/doc/9b19080077.html,rson,fol-
lowing her methodology(50)for incomplete hu-
meri lacking the proximal end(based on the
bisector of the bicipital groove,indicating the ori-
entation of the humeral head),as well as using the
posterior buttress for the humeral head(as a ref-
erence for the head axis).Measurements were
obtained from a cast of the two humeral di-
aphyseal fragments of the holotype specimen.This
humerus was originally preserved as a single spe-
cimen,with a crack filled with sediment at about
midshaft level,the two fragments being slightly
crushed against each other in the proximodistal
direction.After manual separation of the matrix,
the original shape of the diaphysis was recon-
structed by correctly aligning casts of the two
fragments.
The arm angle(or carrying angle at the elbow
joint),which is the angle between the long axes
of the humerus and ulna(arm angles<0°imply
medial deviation of the ulna)(51),was computed
from a photograph of the rearticulated original
specimens.
Postcranial proportions
The degree of elongation of the forearm,the arm,
and the forelimb as a whole were assessed by
means of allometric regressions of radius,humerus,
and radius-plus-humerus length(in millimeters),
respectively,relative to BM(in kilograms).Allo-
metric equations(table S4)were derived based
on data taken from the literature(48,52–54)or
kindly provided by E.Sarmiento to S.M.S.Regres-
sions for anthropoid primates were based on
n=54sex-species means,corresponding to31
species from17genera;hylobatids,orangutans,
Ateles,and Brachyteles were excluded from the
regressions because they are clear outliers.Allo-
metric residuals were computed for the studied
sample as well as for Pliobates and Epipliopithecus;
humeral length in the former,given the lack of
the humeral head,was estimated by taking in-
to account the proportions of the humerus of
Epipliopithecus.
To assess the size of the triquetrum relative to
the hamate,the size of each bone was computed
as the geometric mean of three measurements
representing their maximum dimensions:maxi-
mum mediolateral breadth,dorsopalmar height,
and proximodistal length for the triquetrum;
and maximum proximodistal length,dorsopalmar
height,and mediolateral breadth for the hamate.
Comparative data were kindly provided by T.Kivell;
her metrics and sample(including28anthropoid
species from16genera)are described in the lit-
erature(55,56).
Cranial capacity and encephalization
For preservational reasons,it was not possible to
compute cranial capacity(CC,in cubic centi-
meters)from the virtual endocast.Therefore,CC
was estimated using published allometric equations
based on various external neurocranial measure-
ments(57):maximum width of the braincase base
(CW,in millimeters);vertical height of braincase
(CH,in millimeters);chord of the midline suture
through occipitals,parietals,and frontals(CL,in
millimeters);modulus of the above-mentioned
linear measurements(CO,in millimeters),com-
puted as CO=CW+CH+CL;the product of the
above-mentioned linear dimensions(PR,in cubic
millimeters),computed as PR=CW×CH×CL;
and foramen magnum area(FMA,in square cen-
timeters),computed as FMA=(p/4)×FMW×
FML,where FMW is foramen magnum width,
and FML is foramen magnum length(both in
millimeters).To assess encephalization,we relied
on lower taxonomic–level metrics of relative brain
size,which are significantly correlated with gen-
eral domain cognitive abilities in primates(58,59).
Encephalization residuals(ER)were computed
as ER=ln CC observed–ln CC predicted,by using the
ordinary least-squares cercopithecoid allometric
regression(ln CC=0.4778ln BM+3.457),whereas
encephalization constants(EC)were computed as
EC=CC/BM0.28(58,59).Sex-species mean data
for extant species were taken from the literature
(58).In addition to the estimates derived for
Pliobates in this study,published data for various
extinct catarrhines(female Aegyptopithecus zeuxis,
male Victoriapithecus macinnesi,female Proconsul
nyanzae,male Oreopithecus bambolii,and female
Hispanopithecus hungaricus)were also included
in the analyses(37,58,60–62).
Dental microwear
Paleodietary reconstruction was based on dental
microwear analysis(63).The M1of Pliobates was
RESEARCH|RESEARCH ARTICLE
selected,because it exhibits clearer and larger
phase II crushing and grinding facets than the re-
maining molars.Occlusal surfaces were examined
through an environmental scanning electron mi-
croscope at×500magnification in secondary emis-
sions mode and at20kV,following established
procedures(63).An area of standardized size,cor-
responding to0.02mm2on the original facet(64),
was analyzed using the custom software package
Microware4.02(65).Three microscopic varia-
bles were measured:percentage of pits,breadth
of striations,and breadth of pits.Striations and
pits were categorized by following an arbitrarily
set length-to-width ratio of4:1(63,66–68).We
compared our results with those previously de-
rived for a sample of11extant anthropoids with
well-known diets(63,69,70),partitioned into
three distinct dietary categories(66),as well as
with those reported for extinct catarrhines
(64,66–68,71),including both pliopithecoids
and hominoids.Microwear data were analyzed
by means of canonical variates analysis,using
SPSS Statistics19software.
Phylogenetic analysis
A cladistic analysis based on maximum parsimony
was performed with PAUP*(Phylogenetic Anal-
ysis Using Parsimony)version4.0for Unix(72),
with the search command“branch-and-bound,”
based on a taxon-character data matrix of319
characters and20taxa(tables S5and S6).This
matrix was coded anew by the authors,although
it was partially based on character statements
taken from the literature(8,22,73–76).All but10
characters were treated as unordered,whereas in-
applicable characters were treated as missing data.
Clade robusticity was assessed by means of boot-
strap analysis(10,000replicates)and Bremer support
indices.For the most-parsimonious cladograms,
the following metrics were computed:consistency
index(excluding uninformative characters),reten-
tion index,and rescaled consistency index.Char-
acter polarity was determined using the outgroup
method,with the stem catarrhine Aegyptopithecus
being used as such.Ingroup taxa include the stem
catarrhine Saadanius,two cercopithecoids(the
extant Macaca and the extinct Victoriapithecus),
extant hylobatids,extant(Pongo,Gorilla,and Pan)
and extinct(Pierolapithecus and Hispanopithecus)
great apes,and a wide representation of small-bodied
fossil catarrhines from Africa[two dendropithecids,
including Micropithecus and Dendropithecus-plus-Simiolus(coded simultaneously)]and Eurasia(six pliopithecoids,including Pliopithecus,Epipliopithecus, Dionysopithecus,Barberapithecus,Anapithecus,and Plesiopliopithecus).The phylogenetic placement of Saadanius,Micropithecus,and most pliopithecoids (except Epipliopithecus)should be considered with
caution,because they have a large proportion of
missing data.For this reason,the analysis was also
performed with these taxa removed. Systematic paleontology
Order Primates Linnaeus,1758.Suborder Hap-
lorrhini Pocock,1918.Infraorder Anthropoidea
Mivart,1864.Parvorder Catarrhinié.Geoffroy
Saint-Hilaire,1812.Superfamily Hominoidea Gray,1821.Family Pliobatidae fam.nov.Type genus:
Pliobates gen.nov.,whose diagnosis is as for its
type(and only)species,described below.
Pliobates cataloniae gen.et sp.nov.
Holotype:IPS58443,a partial skeleton with an as-
sociated skull(Fig.1and movie S1),housed at the
ICP.It is composed of70bones and bone frag-
ments(table S1)found in close spatial association,
which,given the lack of repeated elements,are
attributed to a single adult female individual
(based on the small canine alveolus),with an
estimated body mass of4to5kg(tables S7and
S8).It includes large portions of the cranium
with postcanine maxillary teeth(Table1),a man-
dibular fragment,a partial left forelimb(nearly
complete humerus,radius,partial ulna,carpals,
and bones of the manual rays),more fragmentary
elements of the right forelimb,and bones from
the hind limb.
Type locality:ACM/C8-A4(els Hostalets de
Pierola,Catalonia,Spain),in the ACM stratigraphic
series(Vallès-Penedès Basin,northeast Iberian
Peninsula).
Age,stratigraphic position,and distribution:
Only known from the type locality,which has an
estimated age of11.6Ma(middle/late Miocene
boundary)and is thus somewhat younger than all
other ACM hominoid-and pliopithecoid-bearing
localities(9,31,33,77,78),the latter of which
have been dated to11.7to11.9Ma[updated from
(77,78)].
Etymology:Genus name from the Latin plio-
(itself from the Greek,meaning“greater in ex-
tent”)and from the Greek bates(meaning“the
one that walks or haunts”).The name is a con-
traction of the genus names Pliopithecus(“more
ape”)and Hylobates(“the one that walks in the
woods or in the trees”),in allusion to the small
body size and the mosaic of primitive(stem
catarrhine–like)and derived(crown hominoid)
features displayed by the new taxon.The species
epithet is the genitive of the female substantive
“Catalonia,”the Latin name of Catalunya(in which
the type locality is situated).
Diagnosis
Small-bodied catarrhine primate(estimated fe-
Female upper canines moderately compressed.
Upper cheek teeth low-crowned and with sub-
pyramidal,moderately peripheral,and inflated
cusps.Upper premolars relatively broad and ovoid,
P4smaller than P3,both with heteromorphic
cusps,a markedly convex lingual contour and a
distinct lingual cingulum(more developed in the
P4),a distinct transverse crest separating the re-
stricted mesial fovea from the extensive trigon
basin,and the postparacrista forming an abrupt
angle with the distal marginal ridge.Upper molars
only moderately broader than long,with markedly
convex lingual profiles;buccal cusps quite pe-
ripheral and buccal cingula discontinuous;lin-
gual cingula relatively well developed,shelf-like,
and C-shaped,but not surrounding the hypocone
(which is distinct and more peripheral than the
protocone);mesial fovea restricted,with an oblique-
ly directed preprotocrista,and trigon basin ex-
tensive,being separated by a continuous crista
obliqua from the slightly smaller distal fovea,
which displays no hypocone-metacone crest.M2
slightly larger than the M1,and M3shorter and
trapezoidal(due to the oblique buccal margin,
with a centrally situated metacone and a rudi-
mentary hypocone).
Face small but with a distinct snout,the an-
terior portion of the nasals being almost parallel
to the palate.Maxillary sinus large and frontal
sinus present but small.Nasal aperture narrow.
Nasoalveolar clivus short,with an open palatine
fenestra.Anteriorly slightly narrow palate with
somewhat convergent upper tooth rows.Zygo-
matic root moderately high.Orbits subcircular,
large,and frontated,with telescopic orbital rims
located over the P4.Estimated cranial capacity
(69to75cm3)indicating a monkey-like degree of
encephalization.External auditory meatus tubu-
lar but short and not completely ossified,with a
V-shaped end and its anterior portion fused with
the postglenoid process.Carotid foramen perfo-
rating the bulla posterodistally,and carotid canal
horizontally and anteriorly oriented.Spinosum
and postglenoid foramina absent.Jugular fora-
men large and ventrally visible.
Humerus without entepicondylar foramen and
capitular tail,with a well-developed capitulum,
and a narrow and deep zona conoidea.Radial head
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beveled surface for articulation with the humeral zona conoidea,the articular surface for the ulnar radial notch extending along a large portion of the radial head,and a laterally facing bicipital tuberosity.Distal radioulnar joint fully diarthro-dial,with an expanded and two-faceted semilunar articulation on the ulnar head,and a partially developed ulnar fovea.Ulnar styloid process with reduced girth and not articulating with the short pisiform.Triquetrum small and with a reduced articular surface for the ulnar styloid process. Hamate relatively long proximodistally,with a steep triquetrum facet,a relatively large head and a distally projecting hamulus.Capitate with a relatively small and oblong head and a di-vided facet for the second metacarpal on its radial side.
Differential diagnosis
The new taxon differs from pliopithecoids and dendropithecids in its lack of a humeral capitular tail,its hominoid-like proximal radial morphol-ogy,its expanded ulnar head with a two-faceted semilunar articulation,and its partially developed ulnar fovea.It further differs from these taxa and proconsulids in its more hominoid-like carpal morphology(including the lack of a pisiform facet for the styloid process,a capitate facet for the second metacarpal divided by a deep ligamen-tary notch,and a distally projecting hamulus in the hamate),and particularly from pliopithecoids in its overall larger muzzle,more horizontal nasals anteriorly,some details of the upper molars,and (at least compared with Epipliopithecus)the lack of an entepicondylar foramen in the humerus.It also differs from all of the above-mentioned taxa in its fused ectotympanic and postglenoid proc-ess,and from these taxa and hominids in its hor-izontal and anteriorly oriented carotid https://www.wendangku.net/doc/9b19080077.html,st, it differs from crown hominoids(hylobatids and hominids)in its incompletely ossified ectotym-panic and in its more primitive dentition and forelimb morphology(particularly in the humer-oulnar articulation).
Description,comparisons,and paleobiology Dental morphology and diet
Although the lack of lower dentition precludes comparisons with some taxa,the upper cheek teeth of Pliobates(Fig.1D and Table1)generally resemble those of other small-bodied Miocene catarrhines in both occlusal morphology and pro-portions(figs.S1and S2).In contrast,they display a more primitive morphology than those of extant hominoids,including the similarly sized gibbons. Hylobatids possess more elongated cheek teeth with more peripheralized cusps,less developed cingula,and a much more extensive central fovea. Compared with Miocene small-bodied catarrhines from Eurasia and Africa(fig.S1),the upper molars of Pliobates more closely resemble those of the dendropithecid Micropithecus(21,34,35,79)in several features,such as the markedly convex lingual profiles and moderately developed buccal cingula(albeit to a lesser extent than in Micro-pithecus),the C-shaped lingual cingulum that is mostly restricted to the protocone(not surround-ing the hypocone),the well-developed and lingual-
ly situated hypocone,and the relatively narrow M1
and M2.Nevertheless,Pliobates differs in several
features from Micropithecus,which has more re-
stricted buccal cingula,a hypocone-metacone
crest,and a relatively longer and less trapezoidal
M3.The dentition of Pliobates more clearly dif-
fers from Epipliopithecus and other pliopithecoids
(fig.S1),including from Barberapithecus[also
recorded at the Vallès-Penedès Basin(36)]and
Pliopithecus[previously recorded at ACM(33)]in
several features,such as the more convex lingual
profile,the more peripheral buccal cusps,the less
developed cingula of the molars,the narrower M1
and M2,and the M3occlusal morphology and
proportions(fig.S2).
With regard to microwear features,the M1
displays a pitting percentage of30.0%,a pit
breadth of5.67m m,and a striation breadth of
1.98m m.Based on pitting incidence(Fig.2,A and
B),which is the most useful metric for distinguishing
among
dietary categories(70),Pliobates closely
resembles extant frugivores(Pan troglodytes)and
eclectic feeders(Papio cynocephalus)that largely
rely on ripe fruit.In contrast,the pitting incidence
of Pliobates is higher than in extant folivores and
much lower than in extant hard-object feeders
(including orangutans).Compared with other ex-
tinct catarrhines from Western Europe,the pitting
percentage of Pliobates is somewhat lower than
in most pliopithecoids and hominoids,for which
some degree of sclerocarpy has been inferred
(66,68).This low pitting incidence is consistent
with the pit-and striation-breadth measure-
ments(which show no sign of extreme folivory
or specialized hard-object feeding)and most
closely approaches that of the fossil hominoids
Anoiapithecus brevirostris and Hispanopithecus
laietanus,previously interpreted as soft frugivores
(68).These results are confirmed by a multivariate
analysis that simultaneously examined the three
microwear variables(Fig.2C and tables S9to S11),
in which Pliobates falls closer to the extant
frugivorous–mixed-feeder centroid for the first
Fig.2.Results of the dental microwear analyses.(A)Pitting incidence(%)of Pliobates,the extant comparative sample,and pliopithecoids and extinct hominoids from Europe and T urkey.(B)Bivariate plot of striation breadth versus pitting incidence.(C)Bivariate plot of the first two canonical axes delivered by the canonical variates analysis,based on three distinct,broad dietary groups:folivores, mixed feeders and frugivores,and hard-object feeders.Colored polygons in(B)and ellipses in(C)illustrate the variability of extant dietary categories.Small black symbols denote the comparative sample of extant anthropoids,whereas large black symbols represent the centroids of each dietary category.Different symbols are employed to distinguish the various extinct species;results for Iberian hominoids and pliopithecoids are shown in red and blue,respectively,whereas those from other localities are shown in yellow and green,respectively.
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and second canonical axes and is classified as a
frugivore.Dental microwear analyses therefore
indicate a mainly frugivorous diet for Pliobates,
compatible with a high consumption of ripe fruit
and a low sclerocarpic component.
Body mass
Dental BM estimates for the female holotype of Pliobates(table S7)range from2.9to4.8kg,with an average BM estimate of3.9kg and an un-
certainty degree(based on the combined95%
confidence intervals for each dental locus)of2.5
to5.7kg.Postcranial BM estimates(table S8)are
on average4.8kg(range:4.0to5.6kg),based on
catarrhine regressions,and4.3kg(range:2.6to
6.3kg),based on hominoid regressions(estimates
for each postcranial estimator and their confi-
dence intervals are given in table S8).Given that
the size of Pliobates is in the lower range for extant
hominoids,the catarrhine regressions probably
yield more accurate estimates,although the
hominoid-based estimates are closer to the den-
tal ones.Overall,the body mass of the holotype of Pliobates cataloniae can be estimated at~4to5kg (much lower than that estimated for Epipliopi-thecus vindobonensis,~11to12kg;table S8). Cranial morphology and encephalization A3D virtual reconstruction of the cranium,based
on the preserved specimens,is shown in fig.S3,
whereas the final reconstruction(including mir-
rored portions)is shown in Fig.3and movie S1.
Based on this reconstruction,the cranium of Pliobates differs from the primitive catarrhine con-dition(22,37,60)by being short,wide,and high.
However,the tubular ectotympanic is short and
incompletely ossified—i.e.,less developed than in Saadanius and extant crown catarrhines(20–22). The maxillary sinus is extensive,as in stem cat-
arrhines and hominoids(22,80),and there is
also a small frontal sinus,as in stem hominoids
but unlike in stem catarrhines,cercopithecoids,
hylobatids,and pongines(22,37,80).The face is
short and displays anteriorly situated orbits,as in
hylobatids,colobines,and some extinct small-bodied
catarrhines such as Epipliopithecus,Micropithecus,
and Lomorupithecus(19,21,38,76,79).However, Pliobates differs from these taxa(and more close-ly resembles hylobatids)by displaying a more
well-defined muzzle(especially compared with Epipliopithecus)with long and more horizontal nasals,a higher zygomatic root(moderately high
as in hylobatids,but less so than in hominids),an
interorbital pillar nearly orthogonal to the frontal
squama(as in hylobatids and chimpanzees),a
high degree of orbital convergence and fronta-
tion(as in all extant hominoids),and thin and
anteriorly projecting(telescopic)orbital rims[to
a greater extent than in Epipliopithecus(38),and
thus most closely resembling hylobatids and,as
far as it can be ascertained with incomplete pre-
servation,Micropithecus(79)].Pliobates also dis-
plays derived hominoid features in the basicranium
(Fig.4A),including the absence of a postglenoid
foramen with a large and ventrally visible jugular
foramen(as in all extant hominoids),the foramen
ovale situated anteriorly and laterally to the Eusta-chian aperture(as in hylobatids and African
apes),the fusion between the auditory meatus
and the
postglenoid process(as in hylobatids
and African apes),and the horizontal and an-
teriorly directed carotid canal in the petrosal bone
(as in hylobatids).
Fig.4.Basicranial morphology.(A)Drawing of the left basicranium of the holotype(IPS58443)of Pliobates cataloniae gen.et sp.nov.,as preserved in ventral view.The jugular foramen appears artifactually larger because of the displacement of the temporal and occipital portions along the occipitotemporal suture(corrected in the reconstruction in Fig.3).The course of the carotid canal is shown with a dashed line,based on CT images.AE,articular eminence;CAF,carotid foramen;COF,condylar fossa;EA,Eustachian aperture;EAM,external auditory meatus;EP,Eustachian process;ET,ectotympanic;FM,foramen magnum; FO,foramen ovale;GF,glenoid fossa;JF,jugular foramen;OC,occipital condyle;OTS,occipitotemporal suture;PGP,postglenoid process.(B to D)Drawings of comparable views(not to scale)in Hylobates sp.
(B),Proconsul heseloni KNM RU2036[(C),reversed],and Victoriapithecus macinnesi KNM MB29100a (D)(KNM,Kenyon National Museums;RU,Rusinga;MB,Maboko).Arrows denote the V-shaped,incompletely ossified ventral terminal tip of the tubular ectotympanic in the extinct taxa.[Artwork by M.Palmero] Fig.3.Cranial reconstruction.Virtual reconstruction of the holotype(IPS58443)cranium of Pliobates cataloniae gen.et sp.nov.,including mirrored fragments,in frontal(A),lateral(B),posterior(C),basal (D),and superior(E)views.Further details are given in fig.S3and the methods in the text.
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Braincase measurements yield an average cra-nial capacity estimate of69.0cm3(range:41.4to 110.7cm3;table S12),which is close to the es-timates of60.1and65.3cm3delivered by the two most reliable estimators(57)and only slightly lower than the estimate of75.1cm3obtained from foramen magnum area(table S12).According to our estimates of body mass(4.5kg)and cranial capacity[72cm3(average of cranial and foramen magnum estimates)],Pliobates would display a monkey-like degree of encephalization extensively overlapping with extant cercopithecoids(fig.S4 and table S13),being much more encephalized than the stem catarrhine Aegyptopithecus,slightly more so than the stem cercopithecoid Victoriapithecus, and only slightly less so than hylobatids and the extinct hominoids Proconsul and Oreopithecus.All these taxa,like cercopithecoids,are less encephal-ized than the extinct hominoid Hispanopithecus (Rudapithecus)and the extant great apes.Although humans are outliers in brain size–body size allo-metric regressions,great apes further display an allometric grade shift compared with hylobatids (and Pliobates),which are only slightly more en-cephalized on average than cercopithecoids(58). Postcranial morphology and locomotion The humerus(Fig.5)resembles that of extant crown catarrhines,proconsulids,and dendropithecids by lacking(unlike Epipliopithecus)an entepicondylar foramen(17,20,21,38,79,81,82).Pliobates more closely resembles extant hominoids in the laterally facing bicipital tuberosity in the radius(81,83) (Fig.5),as well as in the configuration of the humeroradial articulation(81,82,84)(Fig.6), including:in the humerus,the lack of capitular tail[present in Epipliopithecus,dendropithecids, and cercopithecoids(84)]and the moderately globulous(although not posterolaterally expanded) capitulum with a well-developed zona conoidea [lacking in Epipliopithecus and dendropithecids (81–84)];and,in the radius,the only slightly tilted and almost circular radial head with a small and flat area,a reduced lateral lip,and a beveled surface for the humeral zona conoidea.Pliobates also has a hominoid-like diarthrodial distal radio-ulnar joint(85–87),with a two-faceted expanded semilunar articulation in the ulnar head(Fig.6). In this regard,Pliobates departs from Epiplio-pithecus,dendropithecids,and cercopithecoids (17,38,82)and more closely resembles Proconsul (88),although the ulnar head is less extensive than in extant hominoids.In contrast with these derived features,the humeral shaft and humer-oulnar joint are plesiomorphic:The former(Fig.5) is anteriorly straight and somewhat proximally retroflexed;the latter(Fig.6)lacks the stabilizing features of extant hominoids(83,89),as shown by the narrow ulnar trochlear notch without a median keel(in agreement with the absence of spooling and the poorly defined trochlear lateral keel in the humerus of Pliobates).
Humeral torsion in Pliobates is estimated at 101°,irrespective of the method employed(based on the posterior buttress for the humeral head or the bisector of the bicipital groove),with a con-fidence interval spanning95.7°to106.3°[based on the prediction error(5.23%)for the bicipital
groove method(50)].This degree of torsion is
moderate,higher than that estimated for Pro-
consul heseloni(92°),but comparable to estimates
for Dryopithecus fontani(102°)and Dendropithecus
macinnesi(103.5°),and only slightly below the
value estimated for Epipliopithecus vindobonensis
(109°).The humeral torsion of Pliobates is thus
most comparable to that of non-atelid platyrrhines
and lower than that of Ateles and extant homi-
noids,especially African great apes and humans
[although the high degree of humeral torsion of
extant hominoids is related to increased mobility
at the glenohumeral joint,the higher values of
great apes and humans appear related to knuckle-
walking and enhanced manipulation,respectively,
rather than suspensory behaviors(50)].In con-
trast to the moderate humeral torsion,the fore-
limb of Pliobates appears somewhat elongated
relative to its body size(fig.S5).Allometric com-
putations of relative forelimb length in fossils
(residuals are given in table S14)must be con-
sidered with caution,because they are dependent
on the accuracy of body-size estimates.However,
the forelimb of Pliobates(based on our BM esti-
mate of4.5kg)appears more elongated than that
of Epipliopithecus(based on our estimate of
11.5kg).The latter taxon,contrary to previous
assertions(81,83),has the generalized propor-
tions of
quadrupedal monkeys.Pliobates,in con-
trast,has a forelimb elongation similar to that of
female orangutans and Brachyteles,although it
is less extreme than in Ateles and especially than
in hylobatids.The same pattern holds when the
humerus and radius are analyzed separately,
although in Pliobates,relative length is some-
what higher for the radius than for the humerus.
Pliobates further displays a high arm angle(8°),
which is considerably greater than the average in
most anthropoids,except Hylobates(9.8°),Pongo
(6.3°),and Ateles(6.5°)(51).
The ulnocarpal articulation of Pliobates is
completely different from that of Epipliopithe-
cus and dendropithecids(17,38,90),including a
partially developed ulnar fovea(Fig.6),which,in
extant hominoids,is the attachment area of the
triangular disc ligament and the intra-articular
meniscus(85–87).The ulnar styloid process is
relatively long and slender,with no discernible
articular surfaces for the pisiform or triquetrum.
This agrees with the lack of an articular facet for
the styloid process on the pisiform,like extant
hominoids but unlike monkeys and Proconsul
(91).However,in contrast to Pierolapithecus(92),
the triquetrum of Pliobates shows a proximal
articular facet,which is more developed than
that present in hylobatids and sometimes Pan
(51,87)but less developed than in monkeys.
This suggests that ulnotriquetral contact might
have been reduced by some kind of intra-articular
Fig.5.Forelimb long bones.Shown are the humerus,radius,and ulna of the holotype(IPS58443) of Pliobates cataloniae gen.et sp.nov.(A to E)Partial left humerus in medial(A),posterior(B),lateral (C),anterior(D),and distal(E)views.(F to K)Left radius in medial(F),posterior(G),lateral(H),anterior (I),proximal(J),and distal(K)views.(L to O)Proximal half of the left ulna in medial(L),posterior(M),lateral (N),and anterior(O)views.(P to T)Distal fragment of the left ulna in medial(P),posterior(Q),lateral (R),anterior(S),and distal(T)views.
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tissue,similarly to some Ateles species(93).More-
over,as in apes,the triquetrum of Pliobates is
small relative to hamate size(fig.S6),indicat-
ing a reduced loading on the ulnar side of the
wrist.However,as in monkeys and Proconsul,
the triquetrum of Pliobates differs from that of
extant apes and Pierolapithecus(92)by possess-
ing a proximally protruding beak-like process
(Fig.7).The hamate of Pliobates is“Miocene ape–
like”(91,92),although it more closely resembles
that of hylobatids by possessing a dorsopalmarly
narrow and proximodistally long triquetral ar-
ticular surface that is proximally globular,as well
as a distally projecting hamulus(Fig.7).Pliobates
further resembles hylobatids and Ateles by having
an oblong and mediolaterally narrow capitate
head that,like the facet for the hamate,is prox-
imodistally aligned.This morphology contrasts
with the more globulous,wider,and ulnarly in-
clined capitate head of other catarrhines,including Proconsul(88,91)and Pierolapithecus(92);in Pliobates,though,it is not radially inclined,as it is in hylobatids.Moreover,the capitate facet for
the second metacarpal is divided by a deep liga-
mentary notch(Fig.7),as in extant hominoids
and Pierolapithecus(92)but not in other catar-
rhines(including Proconsul),in which the facet
for the second metacarpal is dorsopalmarly con-
tinuous and occupies the whole lateral aspect
of the capitate(Fig.7)(91).Pliobates has a com-
plex articulation between the third metacarpal
and capitate,as in extant apes but not in Proconsul
(91);however,as in Pierolapithecus(92),the capi-
tate of Pliobates lacks a hook-like process.
Regarding positional behaviors,although the
primitive morphology of the proximal humerus
of Pliobates is suggestive of generalized above-
branch quadrupedalism(94),its overall post-
cranial body plan is more compatible with a
locomotor repertoire that includes a large amount
of cautious and eclectic climbing(87,95).This
inference is supported by the emphasis on pro-
nation and supination capabilities,the reduced
compressive forces transferred across the ulnar
side of the wrist,and the important ulnar deviation
and rotatory capabilities.It agrees with previous
hypotheses on the original locomotor adaptations
of hominoids(95,96)and with recent interpreta-
tions of Proconsul that similarly depict this taxon
as an arboreal quadruped with adaptations for
cautious climbing and clambering(12,88),in-
cluding an incipient distal radioulnar diarthrosis
that(unlike in Pliobates)is still associated to a
nonretreated ulnar styloid process(88).The re-
duced ulnocarpal articulation of Pliobates thus
more closely foreshadows the condition of extant
hominoids,although to a lesser extent than in
the stem great ape Pierolapithecus(92),indicat-
ing a decreased emphasis on forearm use under
weight-bearing conditions relative to Proconsul
(88).Several characteristics of Pliobates(partic-
ularly the elongated forearm,the high arm angle,
and the laterally facing bicipital tuberosity)fur-
ther suggest some degree of below-branch forelimb-
dominated suspensory behaviors(51).However,
the lack of hominoid-like elbow-stabilizing features
in the humeroulnar joint(83,89),the generalized metacarpophalangeal proportions,and the lack
of marked phalangeal curvature suggest that
Pliobates was not specifically adapted to perform
the acrobatic suspensory behaviors(ricochetal
brachiation)displayed by extant gibbons.
Phylogeny and evolutionary implications
Our cladistic analysis,based on both cranioden-
tal and postcranial characters,recovers a single
most-parsimonious tree(Fig.8and table S15),
indicating that Pliobates is more closely related
to crown hominoids than other Miocene small-
bodied catarrhines and Proconsul are.With mod-
erate support(bootstrap71%,Bremer index3),
our results contradict the view of some authors
that all of these taxa are stem catarrhines(pre-
ceding the divergence between hominoids and
Old World monkeys)(17,21)and concur instead
with some previous cladistic analyses indicating
a hominoid status for both Proconsul(2,8,22)
and,at least,dendropithecids(8,22).Our analysis
is inconsistent with the current consensus that
Epipliopithecus is a pliopithecoid(20,66,76,78);
however,the internal phylogeny of pliopithecoids
and dendropithecids is not settled by our results(it is
recovered by the most-parsimonious tree but not by
the bootstrap50%-majority-rule consensus).Simi-
larly,the phylogenetic relationships between the
analyzed dryopithecines(Hispanopithecus and
Pierolapithecus)are not well resolved(the closer
link between Pierolapithecus and crown homi-
nids has a Bremer index of1and bootstrap sup-
port of56%).In contrast,our analysis recovers,
with very high support(bootstrap93to100%,
Bremer indices7to11),both the molecular phylo-
geny of extant hominoids(1,6)and the stem
hominid status of Pierolapithecus and Hispa-
nopithecus(9,92).The position of Pliobates as a
stem hominoid more derived than Proconsul is
relatively well supported(bootstrap78%,Bremer
index2).When the analysis is repeated excluding
all fossil taxa with large amounts of missing data
(fig.S7),the position of Pliobates as a stem hom-
inoid more derived than Proconsul is much better
Fig.6.Elbow and wrist
morphology.The most
diagnostic features of the
elbow and wrist joints of
Pliobates cataloniae gen.
et sp.nov.(IPS58443),
denoted by arrows in
drawings of the distal
humerus,proximal
radius,and distal ulna,
are shown with those of
selected extant and
extinct anthropoids for
comparison.(A to D)
Anterior(top)and distal
(bottom)views of the
distal humerus in P.cata-
loniae(A),Epipliopithecus
vindobonensis Individual I
[(B),reversed],Dendro-
pithecus?sp.KNM
MO17022A(C)(MO,
Moruorot),and Hylobates
moloch(D).(E to H)
Views perpendicular
to the radial tuberosity
(top)and proximal view
(bottom)of the proximal
radius in P.cataloniae
(E),E.vindobonensis
Individual I(F),Simiolus
enjiessi KNM MO63
[(G),reversed)],and
H.moloch(H).(I to M)
Medial(top)and distal
(bottom)views of the
distal ulna in P.cataloniae
(I),E.vindobonensis Indi-
vidual I(J),H.moloch(K),
Ateles paniscus(L),and Cercopithecus aethiops(M).1,absence of entepicondylar foramen;2,absence of capitular tail;3,lack of spool-shaped trochlea;4,well-developed beveled surface for the zona conoidea;5, small and flat area in the radial head;6,ulnar fovea;7,two-faceted,expanded semilunar articular surface in the ulnar head.Specimens are shown as if from the left side and are not to scale.[Artwork by M.Palmero]
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supported (bootstrap 100%,Bremer index 20);it is even more robust than the monophyly of crown hominoids (bootstrap 98%,Bremer index 11)and than the great-ape status of Pierolapithecus and Hispanopithecus (bootstrap 100%,Bremer index 13).
Given that our analyses support Pliobates as a stem hominoid more derived than Proconsul ,the mosaic of primitive and derived features displayed by the former taxon is of utmost relevance for in-terpreting the evolution of several key features among catarrhine primates.Many authors agree that homoplasy has played an important role in hominoid postcranial evolution (5,9,12,92),but Pliobates shows a mosaic of primitive and derived features both in the cranium and the postcra-nium.For the cranium,this is best illustrated by the short tubular (but incompletely ossified)exter-nal auditory meatus with a V-shaped end,which would imply the independent acquisition of a more completely ossified ectotympanic in cercopithecoids and hominoids.This has previously been posited by some authors (20),and it is suggested to some ex-tent by the stem catarrhine Saadanius (22),the stem Old World monkey Victoriapithecus (60),and the stem ape Proconsul (97);in these taxa,the ectotympanic,albeit slightly more developed,is still short,does not laterally exceed the post-glenoid process,and lacks a completely closed terminal ventral tip (Fig.4).In contrast,several other cranial features of Pliobates are derived toward the crown-hominoid condition,gener-ally more closely resembling hylobatids than hominids.Some of the similarities with gib-bons (e.g.,short face with a distinct muzzle and anteriorly situated telescopic orbits)may be size-related to a large extent (98),but others (horizontal and anteriorly directed carotid canal)are otherwise only known in hylobatids.Coupled with the fact that Pliobates chrono-logically fits within the long ghost lineage of hylobatids,from their divergence from homi-nids at ~17Ma (1)until their putative oldest record (Yuanmoupithecus )at 8to 7Ma (10,39),these similarities raise the possibility that Pliobates might be a stem hylobatid.This hypothesis is not favored by our total (craniodental plus postcranial)evidence –based cladistic analyses,which support instead a stem hominoid status for Pliobates ,mostly because of the lack of various crown-hominoid postcranial synapomorphies.However,its hylobatid cranial features and small body size suggest that,at least in some respects,the last common ancestor of crown hominoids might have been more gibbon-like (or less great ape –like)than generally assumed (6,16).
Furthermore,Pliobates supports the view that some small-bodied catarrhines played a more important role in the emergence of crown hom-inoids than has generally been assumed over the past decades.The postcranial evidence provided by Miocene great apes such as Pierolapithecus and Sivapithecus (9,92,99)indicates that the last common ancestor of crown hominoids must have been postcranially more primitive than it would be inferred to be exclusively on the basis of extant forms.This supports some degree of parallel
Fig.8.Results of the cladistic analysis.Single most-parsimonious tree of 645steps,based on
a taxon-character data matrix of 319characters and 20taxa (tables S5and S6).Consistency index =
0.5912(excluding uninformative characters);retention index =0.6897;Rescaled consistency index =0.4213.Numbers below nodes are Bremer
indices,and numbers above nodes are bootstrap support
percentages (only shown when ≥50%).Node numbers refer to clades in the list of apomorphies in table S15.
Fig.7.Carpal bones.Line drawings of carpal bones in Pliobates cata-loniae gen.et sp.nov.(IPS58443)are shown with those of selected anthropoid genera for comparison.(A to E )Left capitate,in radial (top)and proximal
(bottom)views,of Cer-copithecus aethiops (A),Ateles paniscus (B),Pierolapithecus cat-alaunicus (C),Hylobates lar (D),and P.cataloniae (E);gray shading
denotes articular areas for the second metacar-
pals,and cross-hatching denotes those for the third metacarpal.(F to J )Left hamate,in radial (top)and ulnar
(bottom)views,of C.aethiops (F),A.paniscus (G),Pi.catalaunicus (H),https://www.wendangku.net/doc/9b19080077.html,r (I),and P.catalo-niae (J).(K to O )Left triquetrum,in proximo-medial (top)and distal (bottom)views,of C.aethiops (K),A.paniscus (L),Pi.catalaunicus (M),https://www.wendangku.net/doc/9b19080077.html,r (N),and P.cataloniae (O).Drawings are not to scale.
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evolution in the postcranium between extant hylobatids and hominids(5),although not to such a great extent as if Pliobates was interpreted as a crown hominoid.As a stem ape,Pliobates cannot resolve whether many of the postcranial derived features shared by extant hylobatids and homi-nids are homologous(6)or homoplastic(5),al-though Pliobates does suggest that a suite of features in the humeroradial and wrist joints might be homolgous.In these anatomical re-gions,Pliobates displays much more extensive postcranial synapomorphies of crown hominoids than those convergently displayed by atelids,in-cluding a diarthrodial radioulnar joint,an expanded ulnar head,an incipient ulnar fovea,a long and thin styloid process with reduced contact with the rel-atively small triquetrum,and a distally projecting hamulus on the hamate.Pliobates also displays incipient suspensory adaptations,although,based on currently available evidence,it is not possible to conclusively ascertain whether these were inherited by the last common ancestor of crown hominoids(and later secondarily lost in some fos-sil great apes such as Sivapithecus and Pierolapi-thecus)or whether they merely represent an independent acquisition of Pliobates’s. Conclusions
Pliobates provides the first evidence of crown-hominoid postcranial synapomorphies in a Mio-cene small-bodied catarrhine,thus demonstrating a greater diversity in postcranial morphology and positional behaviors than previously recognized among this paraphyletic assemblage of taxa.Three decades ago,the degree of parallel evolution re-quired to evolve hylobatids from small-bodied catarrhines such as dendropithecids,albeit con-ceivable,was considered unlikely in light of the available evidence(18),because of the numerous parallelisms that would be required in crown-hominoid(and even crown-catarrhine)features between hylobatids and hominids.Although the evidence provided by Pliobates reduces this morphological gap,this taxon still falls short of being supported as a hylobatid by our cladistic analyses,which strongly favor instead the mo-nophyly of extant hominoids with all fossil small-bodied catarrhines excluded.However,unlike dendropithecids,which are currently interpreted as stem catarrhines(21)or hominoids more basal than Proconsul(22),Pliobates is unambiguously interpreted as more closely related to crown hom-inoids.Given its chronology and geographic location,as well as the retention of plesiomorphic dental and some postcranial features that re-semble those of small-bodied catarrhines such as dendropithecids,Pliobates is likely to be a late-surviving offshoot of a small African stem hom-inoid more closely related to crown hominoids than Proconsul is.This has important implications for reconstructing the ancestral morphotype from which extant hominoids evolved:It suggests that some small-bodied catarrhines could have played a much more remarkable role in ape evolution than previously thought,and that the last com-mon ancestor of crown hominoids was not nec-essarily great ape–like.REFERENCES AND NOTES
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