Earth and Planetary Science Letters 617 (2023) 118246

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Earth and Planetary Science Letters

journal homepage: www.elsevier.com/locate/epsl

Temporal framework for the Yanliao Biota and timing of the origin of
crown mammals
Zhiqiang Yu a,b , Haibing Wang b,∗ , Chi Zhang b , Liping Dong b , Magdalena H. Huyskens c,1 ,
Zexian Cui d , Paige Cary c , Yankun Di c , Yuri Amelin c,2 , Gang Li e , Qiuli Li a , Xiao-Ping Xia d ,
Chenglong Deng a , Yuanqing Wang b,f , Huaiyu He a , Qing-Zhu Yin c
a
State Key Laboratory of Lithospheric Evolution, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing 100029, China
b
Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Beijing
100044, China
c
Department of Earth and Planetary Sciences, University of California at Davis, Davis, CA 95616, USA
d
State Key Laboratory of Isotope Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China
e
State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Paleontology, Chinese Academy of Sciences, Nanjing 210008, China
f
College of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing 100049, China

a r t i c l e i n f o a b s t r a c t

Article history: Establishing the temporal sequence of the Middle-Late Jurassic Yanliao Biota is essential as it anchors the
Received 22 May 2022 timing of many key evolutionary innovations in vertebrates. Lack of sufficiently reliable high-precision
Received in revised form 16 May 2023 ages of fossil-bearing horizons hinders our ability to reconstruct the tempo and mode of vertebrate
Accepted 24 May 2023
evolution. Here, we frame a temporal sequence of Yanliao Biota with precise age constraints for iconic
Available online xxxx
vertebrates, proposing that the major vertebrate-bearing strata span from 164 Ma to 157 Ma in age. The
Editor: F. Moynier
increasing ecological diversity of mammaliaforms is well illustrated by the Middle-Late Jurassic Yanliao
Keywords: Biota and Early Cretaceous Jehol Biota. Incorporation of the updated temporal frameworks in Bayesian
Yanliao Biota tip-dated mammaliaform phylogeny reveals that Triassic haramiyidans are separate from Jurassic taxa and
U-Pb geochronology unrelated to crown Mammalia. Tip-dated phylogeny supports a long-fuse model for mammal evolution,
Jurassic featured by a Late Triassic root and Middle-Late Jurassic interordinal diversification of crown Mammalia,
Bayesian tip-dating analysis showing consistency with molecular-based timetrees in divergence timing.
evolution
© 2023 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND
Mammalia
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction gids (Theropoda, Pennaraptora), the earliest known eutherian

The late Mesozoic is an important period for the evolution
of mammals, dinosaurs, and birds. Fascinating phenotypic evo-
lution occurred during the Jurassic and Cretaceous, such as the
dinosaur-to-bird transformation, the evolution of flight, and eco-
morphological diversification of mammaliaforms. The Middle-Late
Jurassic Yanliao Biota and Early Cretaceous Jehol Biota in north-
east China are among the most spectacular terrestrial Lagerstät-
ten that have documented these significant evolutionary innova-
tions through their well-preserved fossils, including bizarre di-
nosaurs, transitional pterosaurs, membrane-winged scansorioptery-
*
Corresponding author.
E-mail address: wanghaibing@ivpp.ac.cn (H. Wang).
1
Current address: Norges geologiske undersøkelse (NGU), Leiv Eirikssons vei 39,
7040, Trondheim, Norway.
2
Current address: Korea Basic Science Institute, Building 202, 162 YeonGu DanJi-
ro, Ochang, Cheongwon, Cheongju, Chungbuk 28119, Republic of Korea.
mammal, and the earliest known representatives of Cryptobranchi-
dae of Urodela (salamanders) (Luo, 2007; Meng, 2014; Wang et
al., 2019a; Zhou et al., 2010, 2021). Fossil discoveries in the Yan-
liao and Jehol biotas provide a rare opportunity to probe into the
origins and early evolution of many Mesozoic organisms. These
discoveries have instigated extensive research and provided un-
precedented evidence for phenotypic innovations in vertebrate
evolution (Han et al., 2017; Luo et al., 2011, 2015b, 2017; Meng et
al., 2017; Wang et al., 2021, 2019a; Xu et al., 2015; Zhang et al.,
2008).
Despite the increasing number of important fossil discoveries in
the Yanliao Biota, the temporal distribution of this biota remains
unclear due to the lack of sufficiently reliable and precise dat-
ing results. Without a temporal framework of these biotas, there
is significant uncertainty regarding the mode and tempo of ma-
jor evolutionary transitions. To date, geochronological constraints
on the fossiliferous layers of the Yanliao Biota mainly focused on
the late stage represented by the Linglongta Biota (younger part

https://doi.org/10.1016/j.epsl.2023.118246
0012-821X/© 2023 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
Z. Yu, H. Wang, C. Zhang et al.
of Yanliao Biota) with the flourishing time being ca. 160 Ma at
the Daxishan, Bawanggou, and Yaolugou sections (e.g., Chu et al.,
2016; Yu et al., 2021). Systematic geochronological investigations
of tuffs/bentonites stratigraphically associated with vertebrate fos-
sil horizons in the Yanliao Biota are still lacking, particularly in the
Daohugou Biota (conventionally regarded as the early stage of the
Yanliao Biota, but see Sullivan et al., 2014). Whether the age of the
Nanshimen section is Middle Jurassic (temporally close to the Dao-
hugou Biota, see Huang, 2015) or Late Jurassic (temporally close to
the Linglongta Biota, see Jia and Gao (2016) and Xu et al. (2015)) is
still under debate based on biostratigraphic and lithostratigraphic
evidence. Without sufficient temporal constraints for these impor-
tant fossil discoveries, it is difficult to accurately evaluate the deep
evolutionary history of Mesozoic organisms.
Here, we report a set of zircon U-Pb dates with tuffs strati-
graphically correlated to the vertebrate bearing horizons at four
localities/sections of the Yanliao Biota. The stratigraphic correla-
tion between the fossil-bearing layers and the intercalated tuff
beds is well documented, thus allowing us to precisely determine
the ages of the strata and associated vertebrate fossils. Using the
resulting stringent temporal constraints on main vertebrate fossil
layers, we build a temporal framework of fossil mammals to con-
duct quantitative analysis of tempo and mode of the evolution of
mammaliaforms.
Well-preserved fossils from the Lagerstätten Yanliao and Jehol
biotas represent the best-known specimens in many basal clades
and comprise a sizable proportion of ingroup taxa in morpholog-
ical matrices for mammaliaform phylogeny, e.g., 17% (21/123) in
the present dataset (see Supplementary Material, character ma-
trix files), laying the fundamental groundwork for comprehensive
reconstruction of mammaliaform phylogeny. However, competing
hypotheses on mammaliaform evolution exist with a focus on the
affinity and phylogenetic placement of allotherians, a group pro-
posed by some to comprise haramiyidans, multituberculates, and
gondwanatherians (Bi et al., 2014; Han et al., 2017; Huttenlocker
et al., 2018; Krause et al., 2020, 2014; Meng et al., 2017; Wang
et al., 2019b; Zheng et al., 2013; Zhou et al., 2013), although the
placement of haramiyidans is disputed (Zhou et al., 2013; Luo et
al., 2015a; Meng et al., 2017; Huttenlocker et al., 2018). Under-
standing the timing and composition of crown mammals is funda-
mental in the evolutionary biology of vertebrates. However, based
on the fossil record alone, both a Late Triassic origin of mammals
before their Jurassic diversification (the long-fuse model) or a Mid-
dle Jurassic origin followed by a rapid diversification (the explosive
model) are permissible (Cifelli and Davis, 2013; Zheng et al., 2013;
Zhou et al., 2013).
Recently, explorations of deep divergence in mammaliaforms
encountered incongruence between phylogeny and stratigraphy,
particularly in regard to previously poorly known haramiyidans.
Specifically, splitting haramiyidans and multituberculates chal-
lenges the monophyly of allotherians but fits well with the stratig-
raphy (Huttenlocker et al., 2018; Luo et al., 2015a, 2017; Meng
et al., 2017; Zhou et al., 2013). In this interpretation, substantial
similarities in skull, dentition, and ear bones are interpreted as
adaptive convergence between the stem clade haramiyidans and
the crown clade multituberculates (Huttenlocker et al., 2018; Luo
et al., 2015a, 2017; Meng et al., 2017; Zhou et al., 2013). Alterna-
tively, these two groups may nest in the monophyletic allotherian
clade (Bi et al., 2014; Han et al., 2017; Wang et al., 2019b, 2021;
Zheng et al., 2013), but the resulting placement of allotherians
(particularly Late Triassic taxa) inside Mammalia (crown mammals)
in the phylogeny is not congruent with stratigraphy, an evolution-
ary scenario not commonly expected (Cifelli and Davis, 2013).
Compared to parsimony and Bayesian non-clock analyses with-
out exploiting ages of taxa, the tip-dating methods in Bayesian
inference, which incorporate both the morphological data matrix
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Earth and Planetary Science Letters 617 (2023) 118246
and the fossil ages, open a window to further test the hypotheses
on the incongruence between phylogeny and stratigraphy. There
have been intense discussions on mammaliaform phylogeny (e.g.,
Close et al., 2015; Hoffmann et al., 2020; King and Beck, 2020),
and the observed apparent incongruence was recently attributed
to a novel tree topology that displayed a complete split of Tri-
assic haraimiyidans, Jurassic haramiyidans, and multituberculates
based on modified phylogenetic matrices that removed all Ceno-
zoic mammals (King and Beck, 2020).
Here we combine absolute radiometric clocks (U-Pb and Ar-Ar)
with the rock clock (sedimentary) and evolutionary clock (phy-
logeny), in order to establish a firm chronological framework of
the Yanliao Biota based on a series of high-precision dating results
for the sediments bearing evolutionarily important fossils. With
the incorporation of the updated temporal framework of mam-
maliaforms from the Yanliao and Jehol biotas under the Bayesian
tip-dating framework, we compile new datasets to test the existing
incongruence between phylogeny and stratigraphy, focusing in par-
ticular on the affinity of allotherians and the evolutionary model of
crown Mammalia. Our findings reveal the basal phylogenetic place-
ment of Triassic haramiyidans. The tip-dated phylogeny provides
new insights into the evolutionary model for crown Mammalia.
2. Geologic setting and sampling
The terrestrial rift basins in the North China Craton contain
a nearly complete sedimentary succession of Jurassic and Cre-
taceous strata (Zhu et al., 2012; Meng et al., 2022). The Late
Mesozoic terrestrial strata of this area, in ascending order, are
represented by the Middle Jurassic Jiulongshan/Haifanggou Forma-
tion and the Upper Jurassic Tiaojishan/Lanqi Formation, the Upper
Jurassic-Lower Cretaceous Tuchengzi Formation, the Lower Creta-
ceous Yixian and Jiufotang formations. These strata contain two
well preserved terrestrial biotas, the Yanliao and Jehol biotas. Both
the Jiulongshan/Haifanggou and Tiaojishan formations yield fossils
of the Yanliao Biota. The fossils of the Jehol Biota occur within the
Lower Cretaceous Huajiying Formation (equivalent to sense strito
Dabeigou and Dadianzi formations in Luanping Basin, Yu et al.,
2022), Yixian Formation and Jiufotang Formation.
The Daohugou locality (41◦ 19 13 N, 119◦ 14 15 E) (Figs. 1,
S1) is one of the most important Yanliao Biota’s fossil sites in
East Asia because of its renowned fossil discoveries, including
pterosaurs Jeholopterus ningchengensis and Liaodactylus primus, the
feathered dinosaurs Pedopenna daohugouensis, Epidexipteryx hui, and
Epidendrosaurus ningchengensis (suggested to be a junior synonym
of Scansoriopteryx), salamanders Jeholotriton paradoxus, Chuner-
peton tianyiense, Neimengtriton daohugouensis (originally Liaoxitriton
daohugouensis), mammaliaforms Castorocauda lutrasimilis, Volati-
cotherium antiquus and Megaconus mammaliaformis, insects Lich-
nomesopsyche gloriae, Strashila daohugouensis, and Hadropsylla sinica
(the complete list of taxa and references see Tabs. S1-2 in Sup-
plementary Material). Tuff samples, DHG20-1 and DHG20-2, which
came from a new artificially exposed cave with ∼7.7 m exposed
strata, were collected for SIMS and CA-ID-IRMS zircon U-Pb dating,
respectively (Fig. S1). Those represent the closest physical proxim-
ity to the fossil-bearing layer that yields pterosaurs and mammals
(Fig. S1). The lithology of this artificially exposed cave is composed
of mainly lacustrine sedimentary deposits.
The Wubaiding section (41◦ 22 9 N, 119◦ 23 38 E) (Figs. 1, S1)
is located in the northeast of the Reshuitang Town, Lingyuan City,
western Liaoning Province. The exposed strata of this section are
about 10 meters thick and pertain to the Haifanggou Formation.
The lithology consists predominantly of volcano-sedimentary de-
posits that can be subdivided into three parts: the lower part is
composed of thick volcanic conglomerate; the middle part, ap-
proximately 7 m thick fossil-bearing shales; and the upper part,
Z. Yu, H. Wang, C. Zhang et al.
Fig. 1. Temporal-spatial distribution of the Yanliao Biota. (A) Schematic map showing the location of the study area in eastern Asia. (B) Geographic distribution of major
fossil localities of the Yanliao Biota. (C) Chronostratigraphy of the study area (Huang, 2019; Yu et al., 2021). Sampling localities for geochronology reported in this study are
marked by red numbers in parentheses on both panels B and C.
thick volcanic conglomerate. Two tuff samples collected for SIMS
zircon U-Pb dating, WBD17-1 and WBD17-2, are from two layers
(Fig. S1) bracketing the fossil layer that yields a variety of verte-
brate fossils, including scansoriopterygid Ambopteryx longibrachium
and salamanders Pangerpeton sinensis and Chunerpeton (the com-
plete list of taxa and references see Tab. S1). Sample WBD17-1 is
from a horizon 6 m below sample WBD17-2.
The Nanshimen section (40◦ 31 52 N, 119◦ 29 11 E) (Figs. 1,
S1) is located to the north of the small village of Nanshimenzi,
Qinglong County, Hebei Province. The Nanshimen section is about
56.6 m in thickness, mainly consisting of gray sandstones and silt-
stones. The fossil-bearing beds cropping out at the locality per-
tain to the Upper Jurassic Tiaojishan Formation based on previous
biostratigraphy, lithostratigraphy, and our field observations. One
tuff sample, GG16-4, was sampled for U-Pb dating in 2016 (Fig.
S1). The tuff sample is from a horizon that contains a variety of
plants Coniopteris hymenophylloides and Czekanowskia sp., conchos-
tracans, bivalves, Arguniella sp. and Ferganoconcha sp., and verte-
brate fossils, including a docodontan, Docofossor brachydactylus, two
haramiyidan mammals, Vilevolodon diplomylos and Arboroharamiya
allinhopsoni, a salamander Qinglongtriton Nanshimenensis, a choris-
toderan Coeruleodraco jurassicus, and a bony-crested dinosaur, Cai-
hong juji (the complete list of taxa and references see Tab. S1-2).
The holotype section of the Haifanggou Formation was first es-
tablished in the Yujiagou section (called Haifenggou section in this
study), near Haifenggou and Yujiagou villages, Beipiao City, west-
ern Liaoning Province (GPS: 41◦ 50 52.82 N, 120◦ 47 7.57 E) of the
Beipiao Basin (Huang, 2015) (Figs. 1, S2). This section outcropped
the upper Beipiao Formation, Haifanggou Formation, Tiaojishan
Formation, and lower Tuchengzi Formation. The upper Beipiao For-
mation is dominated by coal bearing clastic rocks, interpreted to
have been deposited in lacustrine and marsh environments. The
Haifanggou Formation is dominated by conglomerate interlayered
with sandstone, siltstone, and mudstone, and is considered to have
been deposited in fluvial environments. The Tiaojishan Formation
is dominated by intermediate volcanic rocks. The Tuchengzi For-
mation is composed of clastic rocks deposited in fluvial to la-
custrine environments. The samples HFG17-4 and HFG20-1 (GPS:
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Earth and Planetary Science Letters 617 (2023) 118246
41◦ 50 52.82 N, 120◦ 47 7.57 E) were collected from the Haifeng-
gou section, Beipiao City, western Liaoning. The former sample is
near the boundary of the Haifanggou and Tiaojishan formations.
The sampling horizon of sample HFG20-1 represents closest phys-
ical proximity to the vertebrate-bearing layer (the complete list of
taxa and references see Tabs. S1-2).
3. Analytical methods
3.1. SIMS U-Pb zircon geochronology analytical methods
Zircon grains, together with zircon standards Plešovice and
Qinghu were mounted in epoxy mounts which were then polished
to expose the center of the crystals. Cathodoluminescence (CL) im-
ages (Fig. S3), transmitted and reflected light micrographs were
obtained prior to SIMS analyses, at the Institute of Geology and
Geophysics, Chinese Academy of Sciences.
Uranium, Th and Pb were measured in zircon in two SIMS lab-
oratories following standard procedures, similar to those described
by previous works (Q.L. Li et al., 2010; X.H. Li et al., 2009). Tuff
samples WBD17-1, WBD17-2, and HFG20-1 were measured using
the CAMECA IMS-1280-HR SIMS at the Institute of Geology and
Geophysics, Chinese Academy of Sciences, and samples HFG17-4
and DHG20-1 were measured using the CAMECA IMS-1280-HR at
the State Key Laboratory of Isotope Geochemistry, the Guangzhou
Institute of Geochemistry, Chinese Academy of Sciences. Calibra-
tion of Pb/U ratios was performed relative to the reference material
Plešovice (337.13 ± 0.37 Ma, Sláma et al., 2008), which was ana-
lyzed between every five unknowns. A long-term uncertainty of
1.5% (1RSD) for 206 Pb/238 U measurements of the reference mate-
rial was propagated to the uncertainty of single analytical spots,
despite that of 206 Pb/238 U error during the course of this study
is commonly around 1% or less. Measured compositions were cor-
rected for common Pb using non-radiogenic 204 Pb. To monitor the
reliability of the whole procedure, an in-house reference zircon
Qinghu was analyzed as unknown together with other samples,
giving a mean 206 Pb/238 U age of 159.1 ± 1.0 Ma (MSWD = 0.59,
n = 31), consistent with the recommended value (159.5 ± 0.2 Ma,
Z. Yu, H. Wang, C. Zhang et al.
2SD) (see Li et al. (2013)). Data reduction was carried out using
Isoplot 4.15 (Ludwig, 2012).
3.2. CA-ID-IRMS U-Pb zircon geochronology
The chemical abrasion procedure is modified from (Mattinson,
2005). Zircon grains were annealed at 900 ◦ C and subsequently
analyzed by laser ablation ICPMS (inductively coupled plasma
mass spectrometry) for U-Pb geochronology. These were performed
to identify any detrital or inherited components and to select
the youngest population of zircons for the CA-ID-IRMS (chemical
abrasion-isotope dilution isotope ratio mass spectrometry) at the
University of California, Davis. These analyses confirmed a single
age population. Subsequently, selected grains were leached for 15
h at 190 ◦ C, and a 202 Pb-205 Pb-233 U-236 U tracer (Huyskens et al.,
2016) was added to the chemically abraded zircons prior to dis-
solution. Pb and U were separated from the matrix elements by
standard HCl ion exchange chemistry and Pb was loaded onto zone
refined Re filaments with a silica gel activator (Huyskens et al.,
2012). Pb was analyzed on a Triton Plus TIMS. Samples below ∼10
pg of radiogenic Pb were measured in peak jumping mode on a
secondary electron multiplier. For larger samples, in addition to at
least a few cycles in peak jumping mode, Pb was also measured
with 204 Pb in the axial SEM, while all other isotopes (202 Pb, 205 Pb,
206
Pb, 207 Pb, and 208 Pb) were collected simultaneously in Faraday
cups coupled with 1013  resistor amplifier boards. U isotope dilu-
tion measurements were performed on a Neptune Plus MC-ICP-MS
using an ESI APEX introduction system. More details on the ana-
lytical methods can be found in Liao et al. (2020). Together with
the samples, two Temora zircon standards were processed and a
206
Pb/238 U age of 417.32 ± 0.14 Ma (MSWD = 0.7) was obtained.
3.3. Phylogenetic analysis
The morphological character matrix used in the study was ex-
panded from a published matrix (Wang et al., 2019b) with addition
of newly reported Middle Jurassic multituberculates and Creta-
ceous haramiyidans. The new character matrix is composed of 123
taxa and 505 characters. The parsimony analysis was conducted in
TNT (Tree analysis using New Technology) version 1.5 using the
new technology search method with sectorial search, ratchet, drift,
and tree fusing (Goloboff et al., 2008). Bayesian non-clock analyses
were conducted in MrBayes 3.2.8 (Ronquist et al., 2012). To detect
how stratigraphic information and morphological evolution inter-
plays, we inferred the timetrees from the Bayesian tip-dating anal-
yses in MrBayes 3.2.8 (Ronquist et al., 2012) which incorporated
both the morphological data matrix and the fossil ages (details in
Supplementary Material).
4. Results
4.1. Assessment and reported criteria for age data
Numerous attempts have been made to constrain the age and
duration of the Yanliao Biota using a variety of chronometers,
e.g., U-Pb and Ar-Ar. However, an ∼1% age bias exists between
40
Ar/39 Ar and U/Pb methods. To better compare previous 40 Ar/39 Ar
ages and our U-Pb ages and address the age bias between Ar-
Ar and U-Pb chronometers, the 40 Ar/39 Ar ages of previous studies
were recalculated based on the same updated decay constant and
the ages of the standards that have been calibrated against U-Pb
ages (Tab. S3). Here we focused the previous geochronologic data
that were obtained from the tuffs/bentonites stratigraphically asso-
ciated with the fossiliferous layers of the Yanliao and Jehol biotas
(Chu et al., 2016; Yu et al., 2021) (Tab. S2). Unless otherwise noted,
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Earth and Planetary Science Letters 617 (2023) 118246
previously reported 40 Ar/39 Ar ages mentioned in this study are re-
ported as ± Y/Z, where Y is the originally reported uncertainty,
and Z includes Y plus decay constant uncertainties.
4.2. Samples
Seven samples were collected from the intercalated tuff layers
in the volcano-sedimentary sequences of the Haifanggou and Tiao-
jishan formations in the Yanliao area (Fig. 1). All of the samples
were collected from excavation sites of the Daohugou locality, or
from outcrops at the Wubaiding, Nanshimen, and Haifenggou sec-
tions (Figs. 1 and S1-S2). The stratigraphic correlation between the
fossil-bearing layers and the intercalated tuff beds is well docu-
mented, thus allowing us to precisely determine the ages of the
strata and associated vertebrate fossils.
All the tuffs are mainly composed of crystal fragments, vitro-
clastics, lithic fragments, and fine volcanic ashes (Fig. S4). The
pyrogenic crystal fragments are distributed sporadically and are
dominated by angular to sub-angular quartz and feldspars. Vitro-
clastics are of bow, arc or chicken bone morphology with elon-
gated, bent, and rounded in the size range of ∼30 μm (with the
exception of DHG20-1 which contains vitro-clastics, the rest are
mainly altered to clay), indicating these volcanic horizons are pri-
marily ash falls with minimal sedimentary transportation.
Zircon grains from the dated samples are mostly euhedral to
subhedral, transparent and colorless. Most analyzed zircon grains
exhibited oscillatory zoning patterns, indicating an igneous origin.
A minor population with inherited cores, easily recognizable from
the cathodoluminescence (CL) images, is not analyzed (Fig. S3).
4.3. U-Pb zircon geochronology
The SIMS and CA-ID-IRMS U-Pb zircon geochronological results
are listed in Figs. 2-3 and Tabs. S4-5. For SIMS zircon U-Pb ages,
we report two levels of uncertainty: Age ± X/Y, where X rep-
resents the analytical error, the error Y represents the analytical
error plus external reproducibility (2SD; 1%). For CA-ID-IRMS re-
sults, weighted mean ages of multiple grains with uncertainties are
given in the ± X/Y/Z format, where X is the 2σ analytical error ex-
clusive of all external sources of uncertainty, Y includes X and the
additional tracer calibration and/or calibration standard error, and
Z incorporates the U decay constant uncertainties (see detailed in-
formation on the dated samples and data sets in Supplementary
Material).
In total, 129 zircon grains of five tuff samples were analyzed
by SIMS U-Pb zircon dating method. Twenty-seven zircon grains
were analyzed from sample DHG20-1. All 27 analyses yield a Con-
cordia U-Pb age at 163.7 ± 1.1 Ma, a weighted mean 206 Pb/238 U
age of 163.7 ± 1.1/2.0 Ma, with a mean square of weighted devi-
ate (MSWD) = 1.1 (Fig. 2A). Thirty-five zircon grains were analyzed
from sample WBD17-1. Twelve zircons are likely to have experi-
enced Pb-loss or 204 Pb contamination of cracks, one analysis (spot
23) yields an older age, indicative of xenocryst (Tab. S4), and the
other 22 analyses yield a Concordia U-Pb age at 163.4 ± 1.2 Ma,
a weighted mean 206 Pb/238 U age of 163.4 ± 1.2/2.0 Ma (MSWD
= 0.71) (Fig. 2B). Twenty-two zircon grains were analyzed for
WBD17-2. Except for one analysis (spot 22) yields slightly younger
age, probably due to Pb loss (Tab. S4). The remaining twenty-one
analyses yield a Concordia U-Pb age at 162.8 ± 1.2 Ma, a weighted
mean 206 Pb/238 U age is 162.8 ± 1.2/2.0 Ma (MSWD = 1.5) (Fig. 2C).
Twenty-four spot analyses were conducted on 24 zircon grains for
HFG17-4. Apart from four analyses are discordant due to the high
common Pb, one analysis (spot 24) yields an older age, indicative
of xenocryst (Tab. S4), the remaining 19 of these analyses yield a
Z. Yu, H. Wang, C. Zhang et al.
Fig. 2. Zircon U-Pb geochronology. SIMS (A-E) and CA-ID-IRMS (F-I) zircon dates from samples obtained from the Daohugou (A, F-G), Wubaiding (B-C), Haifenggou (D-E),
and Nanshimen (G-H) sections, respectively. Ages in here represent the weighted mean 238 U/206 Pb ages of dated samples. See Figs. 1 and S1 for sections and stratigraphic
positions of the samples.
Concordia age of 162.1 ± 1.8 Ma, a weighted mean 206 Pb/238 U age
of 162.3 ± 1.3/2.1 Ma (MSWD = 0.58) (Fig. 2D). Twenty-one spot
analyses were conducted on 21 zircon grains for HFG20-1. All 21
analyses yield a Concordia U-Pb age at 163.9 ± 1.3 Ma, a weighted
mean 206 Pb/238 U age of 163.9 ± 1.3/2.1 Ma (MSWD = 1.5) (Fig. 2E).
In addition, high-precision U-Pb geochronology of GG16-4 and
DHG20-2 were performed for the Nanshimen and Daohugou sec-
tions, respectively. 10 zircon grains from sample DHG20-2 were
analyzed by CA-ID-IRMS, one grain yields an older age of 320.98
Ma, suggesting a xeno- or antecrystic origin, and one discordant
outlier with larger uncertainty. The remaining eight analyses yield
a weighted-mean 206 Pb/238 U age of 163.337 ± 0.058/0.077/0.35
Ma (n = 8, MSWD = 1.5) (Fig. 2F-2G). Nine zircon grains from sam-
ple GG16-4 were analyzed by CA-ID-IRMS. Out of nine analyses,
five are concordant, overlap within error and yield a weighted-
mean 206 Pb/238 U age of 158.58 ± 0.17/0.18/0.38 Ma (n = 5,
MSWD = 1.4) (Figs. 2H-2I). One analysis was discordant, one
yielded a slightly younger age, potentially caused by Pb loss and
two were older detrital origin (Tab. S5).
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Earth and Planetary Science Letters 617 (2023) 118246
4.4. Phylogenetic results
Bayesian tip-dating analyses revealed a different tree topol-
ogy particularly regarding the affinity of haramiyidans (Fig. 4),
leading to a different hypothesis on the timing of crown Mam-
malia’s origin. The tip-dated tree displays that Middle-Late Juras-
sic euharamiyidans forms the sister group of multituberculates
within crown Mammalia, while Triassic haramiyidan Thomasia and
Haramiyavia, and Early Cretaceous haramiyidan Cifelliodon are sep-
arate from euharamiyidans and outside crown Mammalia (Fig. 4).
The tip-dated mammaliaform phylogeny is quite distinct in topol-
ogy from the Bayesian undated phylogeny and also different from
the strict consensus of parsimony analysis, in which close affinity
between haramiyidans and multituberculates is supported consis-
tently in the monophyletic allotherian clade within Mammalia (see
strict consensus of parsimony analysis and majority consensus of
Bayesian non-clock analysis in Supplementary Material). It suggests
an old origin for crown Mammalia in Triassic (207.98 Ma, median
value of estimated age for the node).
Z. Yu, H. Wang, C. Zhang et al.
Fig. 3. Stratigraphy and geochronology of the composite stratigraphic log (modified after Huang, 2019). Bawanggou section (A) in northern Hebei Province; (B) the Daxishan
section in western Liaoning Province; (C) the Daohugou section in southeastern Inner Mongolia Autonomous Region; (D) the Wubaiding section in western Liaoning Province;
and, (E) the Nanshimen section in northern Hebei Province. Sample positions and ages are indicated: (1) Guancaishan locality, western Liaoning, Liu et al., 2006; (2)
Haifenggou section, western Liaoning, Chang et al., 2009; (3) Haifenggou section, western Liaoning, Chang et al., 2014; (4) Yu et al., 2021; (5) Wang et al., 2013; (6) Chu et
al., 2016; (7) He et al., 2004; (8) Chen et al., 2004; (9) Yang and Li, 2008.
5. Discussion
5.1. Temporal constraints on the main vertebrate fossils of the Yanliao
Biota
Pristine volcanic crystal morphology indicates minimal trans-
portation or reworking of zircon in a sedimentary environment.
The consistency between the obtained ages from the tuff samples
and the stratigraphic sequences also indicates that the crystalliza-
tion ages of zircons represent the depositional ages of the sampling
horizons. The weighted mean 206 Pb/238 U age of 162.3 ± 1.3/2.1 Ma
(sample HFG17-4) for the Haifenggou section, the holostratotype
section of the Haifanggou Formation, provides age constraints on
the boundary between the early and late stages of Yanliao Biota
in the area. The weighted mean 206 Pb/238 U age of 163.9 ± 1.3/2.1
Ma (sample HFG20-1) provides age constraints on the vertebrate
fossils bearing layers in this section.
Our results from the Daohugou, Wubaiding, and the lower part
of the Haifenggou sections provide the new age constraints on the
Daohugou Biota and on the lower age limit of vertebrates in the
Yanliao Biota (Fig. 3). The late phase of the Yanliao Biota present
in the Tiaojishan Formation in western Liaoning has been dated
at 157 Ma based on the U-Pb ages of the volcanic ash samples
above the fossil-bearing shale layer of interbeds in the Tiaojis-
han Formation at the Guancaishan section (Liu et al., 2006). Taking
aforementioned radiometric age data together, we propose that the
main vertebrate fossil layers of the Yanliao Biota range in age from
164 to 157 Ma (Fig. 3).
5.2. Temporal constraints on early divergence of Caudata
Numerous exceptionally well preserved specimens of six sala-
mander species have been discovered so far from the Yanliao Biota
6
Earth and Planetary Science Letters 617 (2023) 118246
(Gao and Shubin, 2003, 2012; Jia et al., 2021; Jia and Gao, 2016;
Wang, 2000, 2004; Wang and Evans, 2006). Among them, Chuner-
peton (Gao and Shubin, 2003; but also see Rong et al., 2021) and
Neimengtriton (Jia et al., 2021) from Daohugou section had been
thought to be earliest members of Cryptobranchoidea, whereas
Beiyanerpeton (Guancaishan; Gao and Shubin, 2012) and Qing-
longtriton (Nanshimen; Jia and Gao, 2016) had been regarded as
the earliest representatives of Salamandroidea. Although the exact
phylogenetic positions of these taxa are still highly controversial
(Jia et al., 2021; Rong et al., 2021; Jones et al., 2022), the sala-
manders from Yanliao Biota certainly represent one of the earliest
radiations of the Caudata, after the appearance of the lineage in
Middle/Late Triassic (Schoch et al., 2020). Our new chronology pro-
vides precise time constraint (164 Ma) for the beginning of this
first known salamander radiation in the Mesozoic.
5.3. Temporal constraints on scansoriopterygid dinosaurs
The membrane-winged scansoriopterygid dinosaurs Epiden-
drosaurus ningchengensis (Zhang et al., 2002) and Epidexipteryx hui
(Zhang et al., 2008) from the Daohugou section, Yi Qi from the
Bawanggou section (Xu et al., 2015), and Ambopteryx longibrachium
from the Wubaiding section (Wang et al., 2019a) were exclusively
from the Yanliao Biota (Fig. 3). The weighted mean 206 Pb/238 U
ages of 163.7 ± 1.1/2.0 Ma (sample DHG20-1) and 163.337 ±
0.058/0.077/0.35 Ma (sample DHG20-2) are from the Daohugou
locality (Figs. 1, 2A, 3, and S1); the 163.4 ± 1.2/1.5 Ma (sample
WBD17-1) and 162.8 ± 1.2/1.7 Ma (sample WBD17-2) are from
the Wubaiding section (Figs. 1, 2B, 2C, 3, and S1), and our pre-
vious published ages of 159.0–159.8 Ma are from the Bawanggou
section (Yu et al., 2021) from three tuff or bentonite samples. Note
that two tuff samples from the Wubaiding section yield indistin-
guishable although reversed ages under the precision of the SIMS
Z. Yu, H. Wang, C. Zhang et al.
U-Pb dating method (Schaltegger et al., 2015). Thus, the age of
the dinosaur-bearing layer at the Wubaiding section was set to
ca. 163 Ma. In summary, our findings suggest that the sedimen-
tary layers bearing membrane-winged dinosaurs were deposited
between 164–160 Ma; therefore, the temporal distribution of the
membrane-winged dinosaurs is constrained to 164–160 Ma. This
helps to further refine the story of flight development in theropod
dinosaurs of which scansoriopterygids are the earliest branching
gliding flyers (Pei et al., 2020).
5.4. Temporal constraints on mammaliaforms of Yanliao Biota
To date, the fossil-bearing layers of the Yanliao Biota have been
discovered in the Daohugou, Nanshimen, Bawanggou, and Dax-
ishan sections. Previous high-precision chemical abrasion isotope
dilution thermal ionization mass spectrometry (CA-ID-TIMS) ages
range from 160.25 ± 0.087 (Y)/0.19 (Z) Ma to 160.89 ± 0.11
(Y)/0.21 (Z) Ma for the mammal-fossil-bearing layers of the Dax-
ishan section (Chu et al., 2016). The weighted mean 206 Pb/238 U
ages of 163.7 ± 1.1/2.0 Ma (sample DHG20-1) and 163.337 ±
0.058/0.077/0.35 Ma (sample DHG20-2) for the Daohugou local-
ity and of 158.58 ± 0.17/0.18/0.38 Ma (sample GG16-4) for the
Nanshimen section suggest that the fossil-bearing layers were de-
posited in this time interval. Notably, our high precision CA-ID-
IRMS U-Pb zircon dates at the Daohugou and Nanshimen sections
provide the age range of the mammal-fossil-bearing layers of the
Yanliao Biota. On the basis of the new chronology presented here
and previous radiometric dating results (see details in Supplemen-
tary Material) from mammal horizons in the Yanliao Biota, the
sedimentary sequence bearing euharamiyidans fossils is now con-
strained to 163.337–158.58 Ma (Fig. 3, Tabs. S2-S3).
5.5. Mammaliaform evolution
Recent debate on haramiyidan affinities concerns the mono-
phyly of allotherians (whether haramiyidans are closely related to
multituberculates), the monophyly of haramiyidans (whether the
Triassic taxa are closely related to the Jurassic and Cretaceous
taxa), and the phylogenetic placement of haramiyidans (within
or outside crown Mammalia). Our Bayesian tip-dated phylogeny
suggests that Triassic Haramiyavia and Thomasia and Cretaceous
Cifelliodon are not closely related to the Middle-Late Jurassic eu-
haramiyidans and positioned outside crown Mammalia (Fig. 4),
similar to the recently dated phylogenies for mammaliaforms that
challenge the monophyly of taxonomic unit Haramiyida (Hoff-
mann et al., 2020; King and Beck, 2020). It demonstrates that the
incorporation of stratigraphic information in morphological data
has implications for tree topologies that show significant changes
from phylogenies of the non-clock analyses using parsimony and
Bayesian non-clock methods. Stratigraphic information is one of
the most dominant factors postulated against the morphological
evidence in this case (King, 2021). Incorporation of stratigraphic
data in Bayesian tip-dating analyses reveals that Triassic haramiyi-
dans, one of the earliest mammaliaform clades, are not closely
related to crown mammals as previously suggested (Huttenlocker
et al., 2018; Krause et al., 2020; Luo et al., 2015a, 2017; Meng et
al., 2017; Zhou et al., 2013). Morphological evidence in the dataset
appears not strong enough to support the temporally inconsistent
placement of Triassic haramiyidans within Mammalia (Fig. 4). Con-
versely, Cretaceous Cifelliodon holds its basal phylogenetic position
as sister to Triassic haramiyidans in the dated tree (Fig. 4).
Split between Triassic and later haramiyidans does not sup-
port the monophyly of allotherians in the current dated phylogeny,
but euharamiyidans are clustered closely with multituberculates in
crown Mammalia, contrary to the hypothesis on the basal phyloge-
netic placement of all haramiyidans (Huttenlocker et al., 2018; Luo
7
Earth and Planetary Science Letters 617 (2023) 118246
et al., 2015a, 2017; Meng et al., 2017; Zhou et al., 2013). Character
choice and scoring may contribute to such competing tree topolo-
gies in phylogenetic reconstructions. Compared with different in-
terpretations of phenotypic evolution of particular morphological
structures that could vary dramatically among the practitioners
(see recent review by Wang et al. (2021)), stratigraphic data based
on high-precision dating not only provide a time scale for the oc-
currence of fossils but are also crucial to independently assess the
quality of morphological matrix, particularly when discussing vital
evolutionary events based on morphology-only datasets.
The divergence timing of Mammalia is debated in both com-
peting morphology-based undated phylogenies (i.e., parsimony
and Bayesian undated trees) (e.g., Bi et al., 2014; Luo et al.,
2015a; Zheng et al., 2013; Zhou et al., 2013), and in morphology-
and molecular-based datasets (e.g., Alvarez-Carretero et al., 2022;
O’Leary et al., 2013; Springer et al., 2019; Upham et al., 2019).
The minimum age of Mammalia suggested by the fossil record
is inconsistent between morphology-based studies (e.g., Bi et al.,
2014; Zheng et al., 2013; Zhou et al., 2013) and both a long-fused
model and explosive model in mammalian evolution has been
proposed (Cifelli and Davis, 2013). In our analysis, incorporating
fossil ages into Bayesian tip-dating methods, places the estimated
age of the Mammalia node at approximately 208 Ma with 95%
highest posterior density intervals of age estimations ranging from
217.63–199.27 Ma (median age of 207.98 Ma) (Fig. 4). This is close
to the age estimates proposed by some researchers previously
(Close et al., 2015; Hoffmann et al., 2020; King and Beck, 2020;
Mao et al., 2021; Wang et al., 2021). Notably, the credible interval
for age estimates extends through the Late Triassic Norian to Early
Jurassic Sinemurian and the median age for the node of crown
Mammalia lies in the Late Triassic Rhaetian, dramatically older
than Middle Jurassic as suggested by the fossil record alone. The
deep root of crown Mammalia in dated trees reduces the discrep-
ancy in age estimation between morphology and molecular-based
datasets, such as an age estimation of 215–165 Ma for Mammalia
in a recent Bayesian molecular-clock dated tree of mammals by
integrating phylogenomic data (Alvarez-Carretero et al., 2022). Our
results indicate that stratigraphic data in model-based phylogenetic
analyses help merge the gap between the morphological-clock and
molecular-clock with respect to the divergence timing of crown
Mammalia.
The evolutionary pace of mammals is featured as the long-fuse
and explosive models, depending on the time elapsed between
their origin and significant diversification (Cifelli and Davis, 2013;
Springer et al., 2019). In contrast to the explosive model, cur-
rent dated phylogeny supports the long-fuse model with the root
of Mammalia laying deep in Late Triassic. However, the substan-
tial interordinal and intraordinal diversification of crown mammals
occurred in Middle-Late Jurassic and Late Cretaceous (Fig. 5), rep-
resenting a delayed early burst model (Close et al., 2015), imply-
ing the existence of enormous ghost lineages of crown mammals
in the Early Jurassic. The ecological diversity of mammaliaforms
displayed a burst led primarily by stem groups in Early Jurassic,
increased during Middle-Late Jurassic and maintained in Early Cre-
taceous (Close et al., 2015; Grossnickle and Polly, 2013; Grossnickle
et al., 2019), as spectacularly illustrated by the Yanliao and Je-
hol biotas. This pattern may have been influenced by the breakup
of Pangea and the key anatomical or physiological innovations in
mammal lineages as they responded to changing environments
(Close et al., 2015). Our results imply that the Early Jurassic is
a crucial time in mammaliaform evolution, during which signifi-
cant evolutionary innovations were acquired leading to subsequent
ecological evolutionary experiments in Middle-Late Jurassic mam-
maliaforms (Luo, 2007). For instance, how the multi-cusped cheek
teeth (e.g., in haramiyidans, multituberculates, and gondwanathe-
rians) evolved from the ancestral triconodont-like morphotype is
Z. Yu, H. Wang, C. Zhang et al. Earth and Planetary Science Letters 617 (2023) 118246

Fig. 4. Bayesian tip-dated tree using new datasets (50% majority-rule consensus). Blue bars for each node denote the credible interval age estimate. The number from
1-9 denotes the majority of phylogenetic clades over mammaliaforms. The conventional allotherians are marked in purple, blue and green shading in the dated phylogeny,
showing the separation of Triassic Haramiyavia, Thomasia and Cretaceous Cifelliodon from euharamiyidans and multituberculates. Fossils of Yanliao and Jehol biotas, with
respective localities and precise age constraints, are indicated by solid rectangles and circles in colors on the tree, respectively.

8
Z. Yu, H. Wang, C. Zhang et al.
Fig. 5. Ecological diversity of mammaliaforms in the Mesozoic. The distribution of fossil occurrence of Jurassic and Cretaceous mammaliaforms plotted in the upper and
lower global maps with blue and green rectangles marking the fossil sites in the Middle-Late Jurassic Yanliao Biota (A) and the Early Cretaceous Jehol Biota (B). Curve
of ecological diversity in (C) is modified from previous study (Grossnickle et al., 2019) (data source from Paleobiology Database; vertebrate silhouettes are from http://
phylopic.org).
still controversial (e.g., Meng, 2014; Luo et al., 2015a; Sulej et al.,
2020). Future fossil discoveries from the Late Triassic and Early
Jurassic are expected to further reduce the stratigraphic and mor-
phological gaps in the evolution of mammaliaforms and are clearly
crucial to further resolve the question of the timing of mammal
origins.
6. Conclusions
Taking the published radiometric age data and our new chronol-
ogy together, we propose that the main vertebrate fossil layers
of the Yanliao Biota range in age from ∼164 to 157 Ma. New
SIMS and CA-ID-IRMS zircon U-Pb geochronology of the Daohugou,
Wubaiding, and Nanshimen sections, show ages of 163.337 Ma,
∼163 Ma, and 158.58 Ma, respectively, which constrain the age
of the Yanliao Biota of those sections. These dates have provided
a stringent age range for the membrane-winged (scansorioptery-
gid) dinosaurs and the beginning of the first known salamander
radiation in the Mesozoic. Our Bayesian tip-dated phylogeny of
mammaliaforms using the updated temporal framework based on
radiometric ages supports the hypothesis that Triassic haramiyi-
dans are not closely related to the Jurassic euharamiyidans. It
favors the long-fuse model for the evolution of crown mammals
with the root of Mammalia lying deep in the Late Triassic.
CRediT authorship contribution statement
H.H. and Y.W. designed the research; Z.Y., H.W., H.H., Y.W., and
G.L. conducted field investigations and collected samples. Z.Y., H.H.,
H.W., and C.Z. performed research; Z.Y., H.H., H.W., C.Z., X.X., Q.L.,
9
Earth and Planetary Science Letters 617 (2023) 118246
P. C., M. H., Y.K.D., Y.A., and Q.-Z. Y. performed experiments and
analyzed data; Z.Y., H.W., C.Z., D.C., and D.L. drafted the manuscript
with contributions from all authors.
Declaration of competing interest
The authors declare that they have no known competing finan-
cial interests or personal relationships that could have appeared to
influence the work reported in this paper.
Data availability
Data will be made available on request.
Acknowledgements
We are grateful to the journal Editors Frederic Moynier and
Bosewell Wing for editorial handling, Dr Elsa Panciroli for her
insightful and constructive comments. The authors thank Prof.
Zhonghe Zhou for providing insights on discussion of biological
evolution. We benefit from discussions with David Grossnickle,
Fan Jin, Qigao Jiangzuo, and Congyu Yu. We thank Youjuan Li and
Shunxing Jiang for field work. We thank Yu Liu, Guoqiang Tang,
Xiaoxiao Ling, Xinxin Zhang, and Jiao Li for their support and ad-
vice during the SIMS zircon U-Pb analysis. This work is funded
by the National Natural Science Foundation of China (42288201,
42272017, 42203024, and 41802005); the Strategic Priority Re-
search Program of the Chinese Academy of Sciences (XDB26000000
and XDB18000000); the Youth Innovation Promotion Association,
CAS (2021068).
Z. Yu, H. Wang, C. Zhang et al.
Appendix A. Supplementary material
Supplementary material related to this article can be found on-
line at https://doi.org/10.1016/j.epsl.2023.118246.
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