RESEARCH ARTICLES◥
PRIMATE EVOLUTION
Oligocene primates from China revealdivergence between African andAsian primate evolutionXijun Ni,1,2* Qiang Li,1,2 Lüzhou Li,1 K. Christopher Beard3,4
Profound environmental and faunal changes are associated with climatic deteriorationduring the Eocene-Oligocene transition (EOT) roughly 34 million years ago. Reconstructinghow Asian primates responded to the EOT has been hindered by a sparse record ofOligocene primates on that continent. Here, we report the discovery of a diverse primatefauna from the early Oligocene of southern China. In marked contrast to Afro-ArabianOligocene primate faunas, this Asian fauna is dominated by strepsirhines.There appears tobe a strong break between Paleogene and Neogene Asian anthropoid assemblages. Asianand Afro-Arabian primate faunas responded differently to EOT climatic deterioration,indicating that the EOT functioned as a critical evolutionary filter constraining thesubsequent course of primate evolution across the Old World.
Primates are among the most thermophilicand hence environmentally sensitive of allmammals. As a result, both the geographicdistribution and macroevolutionary pat-terns shown by fossil primates are strongly
mediated by shifting climatic conditions duringthe Cenozoic. Dramatic range expansions, suchas the dispersal of the earliest primates fromtheir Asian birthplace into North America andEurope during the Paleocene-Eocene ThermalMaximum, coincided with intervals of extremeglobal warmth (1, 2). In contrast, episodes ofcooler, drier climatic conditions such as thatcharacterizing the Eocene-Oligocene transition(EOT) resulted in continental-scale extinction ofprimates on landmasses that lacked direct geo-graphic access to low-latitude refugia (3). Pri-mateswere extirpated at or near the EOT inNorthAmerica and Europe, but Afro-Arabian primatefaunas dominated by anthropoids continued toradiate during the Oligocene and Neogene (4–7).In northern China and Mongolia, mammalianfaunal turnover across the EOT was pervasiveenough to be comparedwith theEuropeanGrandeCoupure, and this abrupt change in Asian mam-mal faunas has been designated the MongolianRemodeling (8, 9). However, assessing the im-pact of EOT climatic deterioration on early Asian
primates has been hindered by geographic andtemporal biases in the Asian fossil record. Eoceneprimates have been sporadically reported fromnorthern China andMongolia (10–12), but Eoceneprimates aremore diverse and abundant in south-ern Asia, where the Oligocene record is generallyabsent (13, 14). With the sole exception of the lateearly Oligocene Paali Nala locality in the BugtiHills of Pakistan (15–17), Oligocene primates areunknown in Asia. This very limited record ofAsian Oligocene primates hasmade it difficult toassess the impact of EOT environmental changeson Asian primate evolution. Here, we describe adiverse assemblage of fossil primates from theearly Oligocene of Yunnan Province in southernChina that helps to fill this gap in the record ofAsian primate evolution.We collected the primate fossils reported here
via careful excavation and screen-washing at theLijiawa fossil site in Yunnan, which has yieldedmore than 10mammal taxa that indicate an earlyOligocene age (supplementary materials) (18).Primates Linnaeus, 1758; Strepsirhini Geoffroy,
1812; Adapiformes Hoffstetter, 1977; Sivaladapi-dae Thomas and Verma, 1979; Yunnanadapisgen. nov.Type species:Yunnanadapis folivorussp. nov. Included species: The type species andYunnanadapis imperator sp. nov. Diagnosis:Differs from Paukkaungia, Hoanghonius, andRencunius in having more nearly molariform P4and P4 (P4 remains unknown in Paukkaungia).Lower molars further differ from those of Pauk-kaungia,Hoanghonius, andRencunius in havingless cuspidate paraconids and more angular hy-poconids that are relatively mesial in position,so that the cristid obliqua is shorter than thepostcristid. Upper molars further differ fromthose of Hoanghonius and (especially) Rencu-nius in lacking distinct conules. Lower molars
differ from those ofWailekia and Kyitchaungiain having lingually open trigonids with proto-conid andmetaconidmore closely approximatedand talonids bearing more trenchant cristids.Uppermolars differ from those ofGuangxilemurin having more prominent parastyles and pre-and postprotocristae joining the bases of theparacone and metacone, respectively, rather thanmerging with the pre- and postcingula. Uppermolars with weaker buccal cingulum and incom-plete mesostyle, in contrast to Guangxilemurtongi. Lower molars differ from those of Guang-xilemur singsilai in having lingually open trig-onids and deeper, more extensive valley separatingentoconid and hypoconulid. Differs from Miocenesivaladapids in lacking fully molariform P4 and P4
and having upper molars with distinct periconeand hypocone cusps and pre- and postprotocris-tae joining bases of paracone and metacone.Etymology: Generic name recognizes the geo-graphic provenance of this taxon and its adapi-form affinities.Yunnanadapis folivorus sp. nov. Holotype:
IVPP V22702, left dentary fragment preservingthe crowns of C1-M3 (Fig. 1A and supplementarymaterials). Horizon and locality: Early Oligo-cene Lijiawa fossil site, upper part of CaijiachongFormation, YuezhouBasin, YunnanProvince, China.Diagnosis: Smaller than Yunnanadapis impera-tor. P3 without buccal cingulid, in contrast to Y.imperator. P4 differs from that of Y. imperator inhaving much weaker buccal cingulid and hypo-conid and cristid obliqua more lingual in position,yielding deeper hypoflexid and narrower talonidbasin. Etymology: Trivial name reflects the likelydietary adaptations of this species.Yunnanadapis imperator sp. nov. Holotype:
IVPP V22706, right P4 (Fig. 1B and supplemen-tary materials). Horizon and locality: EarlyOligocene Lijiawa fossil site, upper part of Cai-jiachong Formation, Yuezhou Basin, YunnanProvince, China. Diagnosis: Larger than Yun-nanadapis folivorus. P3 with strong buccal cin-gulid, in contrast to Y. folivorus. P4 differs fromthat of Y. folivorus in having much strongerbuccal cingulid and hypoconid and cristid obli-qua more buccal in position, yielding shallowerhypoflexid and wider talonid basin.Etymology:Latin “imperator” (commander), in allusion tothe large size of this species.Laomaki yunnanensis gen. et sp. nov. Holo-
type: IVPP V22708, right maxilla fragment pre-servingM1-3 (Fig. 1C and supplementarymaterials).Horizon and locality: Early Oligocene Lijiawafossil site, upper part of Caijiachong Formation,Yuezhou Basin, Yunnan Province, China. Diag-nosis: Differs from all sivaladapids aside fromRencunius in having strongly developed conuleson upper molars. P4 and P4 lack substantial mo-larization, in contrast to Yunnanadapis andMio-cene sivaladapids. Upper and lower molars differfrom those of Rencunius and Paukkaungia inhaving highly crenulated enamel, taller and morepyramidal cusps/cuspids, and more trenchantcrests/cristids. Uppermolars aremore transversethan those of Rencunius, and upper molar con-ules are pyramidal rather than bulbous. P4 bears
RESEARCH
SCIENCE sciencemag.org 6 MAY 2016 • VOL 352 ISSUE 6286 673
1Key Laboratory of Vertebrate Evolution and Human Origins,Institute of Vertebrate Paleontology and Paleoanthropology(IVPP), Chinese Academy of Sciences, 142 Xi Zhi Men WaiStreet, Beijing, 100044, China. 2Chinese Academy ofSciences (CAS) Center for Excellence in Tibetan PlateauEarth Sciences, Beijing, 100101, China. 3Biodiversity Institute,University of Kansas, 1345 Jayhawk Boulevard, Lawrence, KS66045-7561, USA. 4Department of Ecology and EvolutionaryBiology, University of Kansas, 1345 Jayhawk Boulevard,Lawrence, KS 66045-7561, USA.*Corresponding author. Email: [email protected]
on July 16, 2020
http://science.sciencemag.org/
Dow
nloaded from
a tiny hypocone, in contrast to that ofRencunius.Etymology: Generic name derives from theMandarin “lao” (old) and the Malagasy “maky”(lemur). Trivial name reflects the geographic prov-enance of this species.Ekgmowechashalidae Szalay, 1976; Gatanthro-
pusmicros gen. et sp. nov.Holotype: IVPP V22717,isolated left M1 (Fig. 1D and supplementarymaterials). Horizon and locality: Early Oligo-cene Lijiawa fossil site, upper part of CaijiachongFormation, Yuezhou Basin, Yunnan Province,China.Diagnosis: Differs from other ekgmowe-chashalid primate genera (including Bugtilemur,Muangthanhinius, and Ekgmowechashala) in hav-ing simpler, more nearly premolariform P4 withhypconid and cristid obliqua located near themidline of the talonid, rather than buccally as inBugtilemur and Muangthanhinius. P4 withoutneomorphic buccal cingular cuspid, in contrastto Ekgmowechashala. M1-2 lack prominent devel-opment of metastylids, in contrast to Ekgmowe-chashala. Protoconid, protocristid, and metaconidof lowermolar are transversely aligned, in contrast
to those of Bugtilemur andMuangthanhinius, inwhich these structures are obliquely oriented sothat metaconid is located distolingual to proto-conid.Uppermolarsdiffer fromthoseofBugtilemurin having more inflated (rather than buccolinguallycompressed) paracone and metacone, broaderbuccal cingulum, and stronger and more exten-sive postprotocingulum. Etymology: In allusionto the ekgmowechashalid affinities of this taxon,its generic name derives from the Greek “gata”(cat) and “anthropus” (man), and its trivial namederives from the Greek “micros” (small). Ekgmo-wechashala signifies “little cat man” in the Lakotalanguage, which lacks a term for nonhumanprimates.Haplorhini Pocock, 1918; Tarsiiformes Gregory,
1915; Tarsiidae Gray, 1825;Oligotarsius rarus gen.et sp. nov. Holotype: IVPP V22727, isolated leftM1 (Fig. 1E and supplementary materials). Hori-zon and locality: Early Oligocene Lijiawa fossilsite, upper part of Caijiachong Formation, Yuez-hou Basin, Yunnan Province, China. Diagnosis:Smaller than other living and fossil tarsiers, aside
from Eocene Tarsius eocaenus and modern Tar-sius pumilus. Differs from extant tarsiids andMioceneHesperotarsius in havingwell-developedconules and distobuccally oriented postmetacristaon M1. Postprotocrista of M1 continuous withpostmetaconule crista, rather than merging withhypometacrista to form distal margin of trigon, asin extant tarsiids. M1 differs from that of EoceneXanthorhysis in being relatively shorter, broader,and higher-crowned, with entoconid located far-ther mesially. Lacks hypoparacrista and hypome-tacrista. Etymology: Generic name reflects theage of this taxon. Trivial name reflects the sparsedocumentation of Tarsiidae in the fossil recordgenerally, as well as the meager representation ofthis species in the Caijiachong early Oligocenefauna.Anthropoidea Mivart, 1864; Eosimiidae Beard
et al., 1994; Bahinia Jaeger et al., 1999; Bahiniabanyueae sp. nov. Holotype: IVPP V22730, iso-lated right M1 (Fig. 1F and supplementary ma-terials, comments regarding possible additionalelements pertaining to the holotype). Horizon
674 6 MAY 2016 • VOL 352 ISSUE 6286 sciencemag.org SCIENCE
Fig. 1. Diverse primates from the early Oligocene of Yunnan Province, China.(A) Yunnanadapis folivorus gen. et sp. nov., left dentary fragment preserving C1-M3
(holotype, IVPP V22702), and composite upper dentition including right dP4 (IVPPV22703), reversed left P4 (IVPP V22704), and right maxillary fragment preservingM1-3 (IVPP V22705). (B) Yunnanadapis imperator gen. et sp. nov., left P3 (IVPPV22707), and reversed right P4 (holotype, IVPP V22706). (C) Laomaki yunnanensisgen. et sp. nov., right maxillary fragment preserving M1-3 (holotype, IVPP V22708);reversed left P3, P4, andM1 (IVPPV22714,V22715, and V22716, respectively); reversedright dentary fragment preserving P3, P4, M1, M2, and M3 (IVPP V22709,V22710, V22711, V22712, and V22713, respectively). (D) Gatanthropus microsgen. et sp. nov., left C1 (IVPP V22718); reversed right P2, P3, P4 (IVPP V22719,
V22720, and V22721, respectively); left M1 (holotype, IVPP V22717); left M2
and M3 (IVPP V22722 and V22723, respectively); right M1, M2, and M3 (IVPPV22724, V22725, and V22726, respectively). (E) Oligotarsius rarus gen. et sp.nov., reversed left C1 and M1 (IVPP V22728 and V22729, respectively), and leftM1 (holotype, IVPP V22727). (F) Bahinia banyueae sp. nov., reversed left P2
and P3 (IVPP V22731 and V22732, respectively), right P4 (IVPP V22733), rightM1 (holotype, IVPP V22730), right M2 missing metacone lobe (IVPP V22734)juxtaposed with a right M2 fragment preserving metacone lobe only (IVPPV22735), right M3 (IVPP V22736), left P3 and left trigonid of M1 (IVPP V22737and V22738, respectively), reversed right M2 trigonid and talonid (IVPPV22739 and V22740, respectively). Scale bars, 2 mm.
RESEARCH | RESEARCH ARTICLESon July 16, 2020
http://science.sciencemag.org/
Dow
nloaded from
and locality: Early Oligocene Lijiawa fossil site,upper part of Caijiachong Formation, YuezhouBasin, Yunnan Province, China. Diagnosis: Up-per molars with weaker buccal and lingualcingula than in Bahinia pondaungensis. AlthoughP2 < P3 < P4 as inB. pondaungensis, inB. banyueaeP2 is larger and P3 is smaller in relation to P4
than is the case in B. pondaungensis. Etymol-ogy: Trivial name honors the pioneering workon the Caijiachong mammal faunas of YunnanProvince made by our friend and colleagueBanyue Wang.Despite the dramatic faunal turnover during
the EOT observed across Europe, North America,and northern Asia (8, 9), the early Oligocene pri-mate fauna from Yunnan reported here and thelate early Oligocene primate fauna fromPakistan(15–17) show that multiple primate lineages suc-cessfully weathered the EOT climatic deteriora-tion in tropical regions of Asia (Fig. 2). Indeed,most of the Asian primate clades that succeeded
in traversing the EOT were able to persist therefor tens of millions of years, showing that theEOT functioned as a critical filtering episodeduring the evolutionary history of Asian primates.Comparing the composition of the early Oligoceneprimate faunas from Yunnan and Pakistan withlater Eocene Asian primate faunas known fromChina, Myanmar, and Thailand reveals that sur-viving this Eocene-Oligocene evolutionary filterentailed a high degree of taxonomic and ecologicalselectivity. Later Eocene primate assemblagesin China, Myanmar, and Thailand tend to bedominated, both in terms of taxonomic richnessand numerical abundance, by stem anthropoidsbelonging to the families Eosimiidae andAmphi-pithecidae (13, 14, 19, 20). In stark contrast, onlyone of the six primates known from the earlyOligocene of Yunnan is an anthropoid. Threeof five primate species documented from thelate early Oligocene of Pakistan are anthropoids,but even in this case, the anthropoid taxa known
from Pakistan differ from their contemporaryAfrican relatives in being relatively small-bodied.Phylogenetic analysis (Fig. 3) shows that Yunna-nadapis folivorus, Y. imperator, and Laomakiyunnanensis belong to the Sivaladapidae, a cladethat persisted in southern and southeastern Asiauntil the lateMiocene (21,22). Likewise, the affinitiesof Gatanthropus micros lie withMuangthanhinius,Bugtilemur, and the enigmatic North Americangenus Ekgmowechashala, which together com-prise the strepsirhine clade Ekgmowechashalidae(23). Late Eocene–early Oligocene primates fromAfro-Arabia show a very different pattern oftaxonomic selectivity in response to the EOT.There, very few strepsirhines (none of which werelarge) survived the EOT, whereas anthropoidsdiversified both taxonomically and ecologically(Fig. 2) (6).On the basis of the current record of early
Oligocene primates from Yunnan, taxonomic se-lectivity across the EOT in southern Asia strongly
SCIENCE sciencemag.org 6 MAY 2016 • VOL 352 ISSUE 6286 675
Olig
otar
sius
rar
us
Afr
asia
djij
idae
Tar
siifo
rm
Kra
bia
min
uta
Phi
leos
imia
s br
ahui
orum
Phi
leos
imia
s ka
mal
i
Bah
inia
pon
daun
gens
isB
ahin
ia b
anyu
eae
Bug
tipith
ecus
inex
pect
ans
Mya
nmar
pith
ecus
yar
shen
sis
Gan
lea
meg
acan
ina
Pon
daun
gia
min
uta
Pon
daun
gia
cotte
riS
iam
opith
ecus
eoc
aenu
s
Bug
tilem
ur m
athe
soni
Gat
anth
ropu
s sp
.M
uang
than
hini
us s
iam
iG
atan
thro
pus
mic
ros
Pau
kkau
ngia
par
vaLa
omak
i yun
nane
nsis
K
yitc
haun
gia
taka
ii W
aile
kia
orie
ntal
e
Gua
ngxi
lem
ur s
ings
ilai
Yun
nana
dapi
s fo
livor
us
Yun
nana
dapi
s im
pera
tor
Gua
ngxi
lem
ur to
ngi
40
39
38
37
36
35
34
33
32
31
30
"Anc
hom
omys
" m
iller
iW
adile
mur
ele
gans
Sah
arag
alag
o m
isre
nsis
Kar
anis
ia a
renu
laK
aran
isia
cla
rki
Ple
siop
ithec
us te
ras
Nos
mip
s ae
nigm
atic
us
Afr
amon
ius
diei
des
Afr
adap
is lo
ngic
rista
tus
Om
anod
on m
inor
Shi
zaro
don
dhof
aren
sis
Afr
otar
sius
liby
cus
Bire
tia fa
yum
ensi
s
Tal
ahpi
thec
us p
arvu
sQ
atra
nia
basi
odon
tos
Bire
tia p
ivet
eaui
Bire
tia m
egal
opsi
s
Ars
inoe
a ka
llim
os
Pro
teop
ithec
us s
ylvi
aeS
erap
ia e
ocae
na
Cat
opith
ecus
bro
wni
Afr
otar
sius
cha
trat
hi
Uni
dent
ified
olig
opith
ecid
Qat
rani
a w
ingi
Qat
rani
a fle
agle
i
Api
dium
bow
niA
pidi
um z
uetin
aA
pidi
um m
oust
afai
Olig
opith
ecus
rog
eri
Olig
opith
ecus
sav
agei
Api
dium
phi
omen
se
Par
apith
ecus
fraa
siS
imon
sius
gra
nger
i
Moe
ripith
ecus
mar
kgra
fi
Pro
plio
pith
ecus
hae
ckel
i
Moe
ripith
ecus
mar
kgra
fi T
aqah
Pro
plio
pith
ecus
chi
roba
tes
Pro
plio
pith
ecus
ank
eli
Aeg
ypto
pith
ecus
zeu
xis
Ma
2
1
EOB
Afro-Arabian strepsirhines Afro-Arabian haplorhines Asian haplorhines Asian strepsirhines
Fig. 2. Divergent taxonomic composition of fossil primates across theEocene-Oligocene boundary (EOB) in Afro-Arabia and southernAsia.Grayarea indicates haplorhines. Pale red area indicates strepsirhines. The phylo-genetic affinities of Nosmips are uncertain (26).The width of the shaded areasdirectly reflects taxonomic diversity. Solid red and gray lines designate gen-erally accepted monophyletic groups (Fig. 3) (6). Dashed lines indicate hy-pothetical range extensions in earlier strata.White arrows indicate that lineages
persist to later intervals. Dashed line with arrowhead 1 indicates interconti-nental dispersal of early anthropoids from Asia to Afro-Arabia (6, 27). Dashedline with arrowhead 2 indicates a second dispersal episode of anthropoidsbetween Afro-Arabia and Asia during the early Oligocene, as suggested by ourphylogenetic analysis that Phileosimias and Bugtipithecus are more closelyrelated to Afro-Arabian anthropoids than to Asian anthropoids (supplementarymaterials). Ma, million years ago.
RESEARCH | RESEARCH ARTICLESon July 16, 2020
http://science.sciencemag.org/
Dow
nloaded from
favored strepsirhines over haplorhines. Ecologi-cally, strepsirhines were the only Asian primatesto occupy those niches available to primates ofrelatively large body mass because medium andlarge haplorhine taxa such as amphipithecidswere eradicated across the EOT in Asia. Thispattern of turnover across the EOT amongAsian primates differs radically from thatwhich has been observed in Afro-Arabia. There,only small strepsirhines survived the EOT,whereasanthropoid haplorhines diversified to occupy arange of body sizes that was nearly an order ofmagnitude larger than their previous distribu-tion (Fig. 4). The divergent responses shown byAfro-Arabian andAsian primates across the EOTset the stage for subsequent macroevolutionarypatterns within this group. Africa became thegeographic nexus of anthropoid evolution,whereasAsia continued to harbor sivaladapid strepsirhinesand tarsiid haplorhines. Dynamic changes tothe Asian physical environment during the in-terval spanning the EOT included progressiveretreat of the Paratethys Sea from central Asia,continueduplift of the Tibetan-Himalayan orogen,and opening of the South China Sea (24). Africawas not immune to global climatic changesacross the EOT, but it did not experience thedramatic tectonic and paleogeographic alter-ations that characterized Asia at this time. It istempting to attribute the different patterns ofturnover in Asian and African primate faunasacross the EOT to local changes in vegetationand paleoenvironment (25), but current evi-dence is not sufficient to rule out the possibilitythat stochastic processes also played a substan-tial role.
676 6 MAY 2016 • VOL 352 ISSUE 6286 sciencemag.org SCIENCE
Fig. 3. Summary phylo-geny of 196 mammals.Parsimony analysis isbased on a data matrixthat includes 1227 mor-phological charactersand 663 molecularcharacters of long andshort interspersednuclear elements scoredfor 149 fossil and 47living taxa. The topologyof extant treeshrews,flying lemurs, and pri-mates used as abackbone constraint or“molecular scaffold” isbased on a gene super-matrix (supplementarymaterials).
Afrasia djijidae
Phenacopithecus spp.
Gatanthropus micros
Eosimias sinensis
Guangxilemur spp.
Tarsius syrichta
Periconodon pygmaeus
Oligotarsius rarus
Eosimias centennicus
Necrolemur spp.Altanius orlovi
Rencunius spp.
Microchoerus erinaceus
13 tree shrews
Ekgmowechashala philotau
Laomaki yunnanensis
Eosimiid Nyaungpinle
Sivaladapis nagrii
Protoadapis curvicuspidens
Bahinia banyueae
Xanthorhysis tabrumi
Pseudoloris parvulus
Bugtilemur mathesoni
Outgroup
Afrotarsius chatrathi
Vectipithex raabi
Sinoadapis shihuibaensis
Hoanghonius stehlini
Afrotarsius libycus
Yunnanadapis spp.Paukkaungia parva
Bahinia pondaungensis
Muangthanhinius siami
98
ha
plo
rhin
es
34 crown anthropoids
29 plesiadapiformsand flying lemurs
15 lemuriforms
25 adapids
Ekg
mo
we
-cha
sha
lids
Siva
lad
ap
ids
Ta
rsiids
44
tarsiifo
rms
Eo
simiid
s
20
stem
an
thro
po
ids
54
strep
sirhin
es
Afr
asia
djij
idae
Tar
siifo
rmK
rabi
a m
inut
aB
ahin
ia p
onda
unge
nsis
Gat
anth
ropu
s sp
.M
uang
than
hini
us s
iam
iP
aukk
aung
ia p
arva
Kyi
tcha
ungi
a ta
kaii
Mya
nmar
pith
ecus
yar
shen
sis
Wai
leki
a or
ient
ale
Gan
lea
meg
acan
ina
Gua
ngxi
lem
ur to
ngi
Pon
daun
gia
min
uta
Pon
daun
gia
cotte
riS
iam
opith
ecus
eoc
aenu
s
Olig
otar
sius
rar
us
Bug
tilem
ur m
athe
soni
Phi
leos
imia
s br
ahui
orum
Phi
leos
imia
s ka
mal
iG
atan
thro
pus
mic
ros
Bah
inia
ban
yuea
e B
ugtip
ithec
us in
expe
ctan
sLa
omak
i yun
nane
nsis
G
uang
xile
mur
sin
gsila
iY
unna
nada
pis
foliv
orus
Y
unna
nada
pis
impe
rato
r
"Anc
hom
omys
" m
iller
iW
adile
mur
ele
gans
Sah
arag
alag
o m
isre
nsis
Kar
anis
ia a
renu
laA
frot
arsi
us li
bycu
sK
aran
isia
cla
rki
Bire
tia fa
yum
ensi
sTa
lahp
ithec
us p
arvu
sQ
atra
nia
basi
odon
tos
Bire
tia p
ivet
eaui
Bire
tia m
egal
opsi
sA
rsin
oea
kalli
mos
Ple
siop
ithec
us te
ras
Pro
teop
ithec
us s
ylvi
aeS
erap
ia e
ocae
naC
atop
ithec
us b
row
niN
osm
ips
aeni
gmat
icus
Afr
amon
ius
diei
des
Afr
adap
is lo
ngic
rista
tus
Afr
otar
sius
cha
trat
hiO
man
odon
min
orU
nide
ntifi
ed o
ligop
ithec
idS
hiza
rodo
n dh
ofar
ensi
sQ
atra
nia
win
giQ
atra
nia
fleag
lei
Api
dium
bow
niA
pidi
um z
uetin
aA
pidi
um m
oust
afai
Olig
opith
ecus
rog
eri
Olig
opith
ecus
sav
agei
Api
dium
phi
omen
seP
arap
ithec
us fr
aasi
Sim
onsi
us g
rang
eri
Pro
plio
pith
ecus
hae
ckel
iM
oerip
ithec
us m
arkg
rafi
Moe
ripith
ecus
mar
kgra
fi Ta
qah
Pro
plio
pith
ecus
chi
roba
tes
Pro
plio
pith
ecus
ank
eli
Aeg
ypto
pith
ecus
zeu
xis
0
2000
4000
6000
0
2000
4000
6000
EOB
Afro-Arabian late Eocene primates Afro-Arabian early Oligocene primates
Asian late Eocene primates Asian early Oligocene primates
g
g
Fig. 4. Body-mass spectrum of fossil primatesacross the EOB in Afro-Arabia and southernAsia.Gray bars represent haplorhines. Pale red barsrepresent strepsirhines. Nosmips is uncertain (26).Later Eocene Afro-Arabian anthropoids occupy themiddle of the spectrum. Later EoceneAfro-Arabianstrepsirhines dominate the two extremes. EarlyOligocene Afro-Arabian strepsirhines are restrictedto the small end of the body-size distribution. EarlyOligocene Afro-Arabian anthropoids span most ofthe body-mass range. Later Eocene Asian strep-sirhines occupy the middle part of the body-massspectrum. Later EoceneAsiananthropoidsdominatethe small and large body-mass areas. Early Oligo-cene Asian anthropoids are restricted to the smallbody-mass area. Early Oligocene Asian strepsirhinescontinue to occupy a broad range of bodymasses.Data are listed in table S2.
RESEARCH | RESEARCH ARTICLESon July 16, 2020
http://science.sciencemag.org/
Dow
nloaded from
REFERENCES AND NOTES
1. X. Ni, Y. Hu, Y. Wang, C. Li, Anthropol. Sci. 113, 3–9 (2005).2. K. C. Beard, Proc. Natl. Acad. Sci. U.S.A. 105, 3815–3818
(2008).3. M. Köhler, S. Moyà-Solà, Proc. Natl. Acad. Sci. U.S.A. 96,
14664–14667 (1999).4. E. R. Seiffert, Folia Primatol. (Basel) 78, 314–327 (2007).5. I. S. Zalmout et al., Nature 466, 360–364 (2010).6. E. R. Seiffert, Evol. Anthropol. 21, 239–253 (2012).7. N. J. Stevens et al., Nature 497, 611–614 (2013).8. J. Meng, M. C. McKenna, Nature 394, 364–367 (1998).9. J. Sun et al., Sci. Rep. 4, 7463 (2014).10. X. Ni, K. C. Beard, J. Meng, Y. Wang, D. L. Gebo, Am. Mus.
Novit. 3571, 1–11 (2007).11. B. Wang, Vertebrata PalAsiatica 46, 81–89 (2008).12. X. Ni et al., Proc. R. Soc. B Biol. Sci. 277, 247–256 (2010).13. K. C. Beard, T. Qi, M. R. Dawson, B. Wang, C. Li, Nature 368,
604–609 (1994).14. K. C. Beard et al., Proc. R. Soc. B Biol. Sci. 276, 3285–3294
(2009).15. L. Marivaux et al., Science 294, 587–591 (2001).16. L. Marivaux, J. L. Welcomme, S. Ducrocq, J. J. Jaeger, J. Hum.
Evol. 42, 379–388 (2002).
17. L. Marivaux et al., Proc. Natl. Acad. Sci. U.S.A. 102, 8436–8441(2005).
18. O. Maridet, X. Ni, J. Vertebr. Paleontol. 33, 185–194 (2013).19. J. Jaeger et al., Science 286, 528–530 (1999).20. K. C. Beard, J. Wang, J. Hum. Evol. 46, 401–432 (2004).21. P. D. Gingerich, A. Sahni, Nature 279, 415–416 (1979).22. X. Ni, in Palaeovertebrata Sinica. Volume III. Basal Synapsids
and Mammals. Fascicle 3 (Serial no. 16). Eulipotyphlans,Proteutheres, Chiropterans, Euarchontans, and Anagalids, C. Li,Z. Qiu, Eds. (Science Press, 2015), pp. 284–389.
23. J. X. Samuels, L. B. Albright, T. J. Fremd, Am. J. Phys.Anthropol. 158, 43–54 (2015).
24. A. Licht et al., Nature 513, 501–506 (2014).25. R. J. Morley, in Tropical Rainforest Responses to Climatic
Change, M. Bush, J. Flenley, W. Gosling, Eds. (Springer-Verlag,ed. 2, 2011), chap. 1, pp. 1–34.
26. E. R. Seiffert et al., Proc. Natl. Acad. Sci. U.S.A. 107, 9712–9717 (2010).27. Y. Chaimanee et al., Proc. Natl. Acad. Sci. U.S.A. 109,
10293–10297 (2012).
ACKNOWLEDGMENTS
This project has been supported by the Strategic Priority ResearchProgram of CAS (CAS, XDB03020501), the National Basic
Research Program of China (2012CB821904), the CAS 100-talentProgram, the National Natural Science Foundation of China(41472025), and the U.S. National Science Foundation (BCS0820602, BCS 1441585, and EAR 1543684). We thank Z. Yan,G. Wang, R. Li, and G. Li for their assistance in the field. Thephylogenetic data used in the paper are archived in thesupplementary materials.
SUPPLEMENTARY MATERIALS
www.sciencemag.org/content/352/6286/673/suppl/DC1Materials and MethodsSystematic PaleontologyMeasurementsBody Mass EstimationPhylogenetic AnalysisFigs. S1 to S10Tables S1 and S2References (28–63)Databases S1 and S2
7 January 2016; accepted 24 March 201610.1126/science.aaf2107
ASTROPARTICLE PHYSICS
Observation of the 60Fenucleosynthesis-clock isotope ingalactic cosmic raysW. R. Binns,1* M. H. Israel,1* E. R. Christian,2 A. C. Cummings,3 G. A. de Nolfo,2
K. A. Lave,1 R. A. Leske,3 R. A. Mewaldt,3 E. C. Stone,3
T. T. von Rosenvinge,2 M. E. Wiedenbeck4
Iron-60 (60Fe) is a radioactive isotope in cosmic rays that serves as a clock to infer an upperlimit on the time between nucleosynthesis and acceleration.We have used the ACE-CRISinstrument to collect 3.55 × 105 iron nuclei,with energies ~195 to ~500mega–electron volts pernucleon, of which we identify 15 60Fe nuclei.The 60Fe/56Fe source ratio is (7.5 ± 2.9) × 10−5.The detection of supernova-produced 60Fe in cosmic rays implies that the time required foracceleration and transport to Earth does not greatly exceed the 60Fe half-life of 2.6million yearsand that the 60Fe source distance does not greatly exceed the distance cosmic rays can diffuseover this time, ⪍1 kiloparsec. A natural place for 60Fe origin is in nearby clusters of massive stars.
Signature of recent nucleosynthesisThe radioactive isotope 60Fe [whichdecays byb–decaywith a half-life of 2.62 × 106 years (1)]is expected to be synthesized and ejected intospace by supernovae, and thus could be
present in galactic cosmic rays (GCRs) near Earth,depending upon the time elapsed since nucleo-synthesis and the distance of the supernovae.60Fe is believed to be produced primarily incore-collapse supernovae of massive stars withmass M > ~10 solar masses (M⊙), which occurmostly in associations of massive stars (OBassociations). It is the only primary radioactiveisotope with atomic number Z ≤ 30 [with the
exception of 59Ni, for which only an upper limitis available (2)] produced with a half-life longenough to potentially survive the time intervalbetween nucleosynthesis and detection at Earth.(Primary cosmic rays are those that are synthe-sized at the GCR source, as opposed to secondarycosmic rays, which are produced by nuclear in-teractions in the interstellar medium.) 60Fe is dif-ficult to measure with present-day instrumentsbecause of its expected extreme rarity, based onnucleosynthesis calculations for supernovae(3, 4). The detection of 60Fe in cosmic rays wouldbe a clear sign of recent, nearby nucleosynthe-sis. The long period of data collection (17 years)achieved by the Cosmic Ray Isotope Spectrometer(CRIS) aboard NASA’s Advanced CompositionExplorer (ACE) (5), the excellentmass and chargeresolution of the CRIS instrument, and its capa-bility for background rejection have enabled usto detect 60Fe.
60Fe has been detected in other samples ofmatter. Measurements of diffuse g-rays from the
interstellar medium (ISM) by the spectrometeron the International Gamma-Ray AstrophysicsLaboratory (INTEGRAL) spacecraft have revealedline emission at 1173 and 1333 keV from 60Co, thedaughter product of 60Fe decay, clear evidencethat “nucleosynthesis is ongoing in the galaxy”(6). As expected, this emission is diffuse insteadof point-like, since the 60Fe lifetime is sufficientlylong to allow it to diffuse over distances that arelarge compared to the size of a supernova rem-nant. This is one of many strong connectionsbetween g-ray astronomy and direct cosmic-raystudies (7).Deep-sea manganese crusts from two differ-
ent locations have also been found to harborelevated 60Fe levels (8, 9). Analysis of crust layersusing accelerator mass spectrometry showedsignificant increases in the 60Fe/Fe ratio 2.8million years (My) ago, “compatible with depo-sition of supernova ejecta at a distance of a fewtens of pc” (9). The measurement was verifiedby an independent analysis (10), although theseinvestigators did not find a corresponding in-crease in a marine-sediment sample [see (10, 11)for discussion]. We note that the manganesecrust studies (8–10) used outdated half-lives for60Fe and 10Be—1.49 and 1.51 My , respectively—instead of the currently accepted 2.62 and 1.387My(1). Using these recent lifetimes, it has been esti-mated that the peak in the 60Fe/Fe ratio (9) as afunction of depth corresponds to an age of 2.2 My(11). Lunar surface samples also show elevated60Fe/Fe ratios consistent with supernova debrisarriving on the Moon ~2 My ago (12, 13). Thesedeep-sea manganese crust and lunar surfaceobservations were compared with expectationsfrom possible stellar sources (11) and found tobe consistent with an origin in core-collapsesupernovae, but inconsistent with Type Ia su-pernovae, which produce orders of magnitudeless 60Fe.
Cosmic-ray 60Fe detection
The CRIS instrument was launched on ACE in1997 and has operated continuously since that
SCIENCE sciencemag.org 6 MAY 2016 • VOL 352 ISSUE 6286 677
1Washington University, St. Louis, MO 63130, USA.2NASA/Goddard Space Flight Center, Greenbelt, MD 20771,USA. 3California Institute of Technology, Pasadena, CA91125, USA. 4Jet Propulsion Laboratory, California Instituteof Technology, Pasadena, CA 91109, USA.*Corresponding author: Email: [email protected] (W.R.B.);[email protected] (M.H.I.)
RESEARCH | RESEARCH ARTICLESon July 16, 2020
http://science.sciencemag.org/
Dow
nloaded from
evolutionOligocene primates from China reveal divergence between African and Asian primate
Xijun Ni, Qiang Li, Lüzhou Li and K. Christopher Beard
DOI: 10.1126/science.aaf2107 (6286), 673-677.352Science
, this issue p. 673Sciencestill unknown whether this difference was due to the environment or chance.that primates took a different path in Asia. Instead of anthropoids, strepsirrhine (lemur-like) primates were dominant. It is
describe 10 previously unknown primates found in Yunnan Province in China that showet al.reestablishment in Asia. Ni transition, anthropoid primates were dominant in Afro-Arabian regions, but little has been known about primatespecies are particularly susceptible to cold, this change in climate drove a retraction of primates globally. After this
The transition between the Eocene and Oligocene periods was marked by distinct cooling. Because primateClimate filters dominant species
ARTICLE TOOLS http://science.sciencemag.org/content/352/6286/673
MATERIALSSUPPLEMENTARY http://science.sciencemag.org/content/suppl/2016/05/04/352.6286.673.DC1
REFERENCES
http://science.sciencemag.org/content/352/6286/673#BIBLThis article cites 57 articles, 8 of which you can access for free
PERMISSIONS http://www.sciencemag.org/help/reprints-and-permissions
Terms of ServiceUse of this article is subject to the
is a registered trademark of AAAS.ScienceScience, 1200 New York Avenue NW, Washington, DC 20005. The title (print ISSN 0036-8075; online ISSN 1095-9203) is published by the American Association for the Advancement ofScience
Copyright © 2016, American Association for the Advancement of Science
on July 16, 2020
http://science.sciencemag.org/
Dow
nloaded from
