The Yana RHS site: Humans in the Arctic before the Last Glacial Maximum

Abstract

A newly discovered Paleolithic site on the Yana River, Siberia, at 71 degrees N, lies well above the Arctic circle and dates to 27,000 radiocarbon years before present, during glacial times. This age is twice that of other known human occupations in any Arctic region. Artifacts at the site include a rare rhinoceros foreshaft, other mammoth foreshafts, and a wide variety of tools and flakes. This site shows that people adapted to this harsh, high-latitude, Late Pleistocene environment much earlier than previously thought.

Full text

The Yana RHS Site: Humans in
the Arctic Before the Last
Glacial Maximum
V. V. Pitulko,
1
* P. A. Nikolsky,
2
E. Yu. Girya,
1
A. E. Basilyan,
2
V. E. Tumskoy,
3
S. A. Koulakov,
1
S. N. Astakhov,
1
E. Yu. Pavlova,
4
M. A. Anisimov
4
A newly discovered Paleolithic site on the Yana River, Siberia, at 71°N, lies well
above the Arctic circle and dates to 27,000 radiocarbon years before present,
during glacial times. This age is twice that of other known human occupations
in any Arctic region. Artifacts at the site include a rare rhinoceros foreshaft,
other mammoth foreshafts, and a wide variety of tools and flakes. This site
shows that people adapted to this harsh, high-latitude, Late Pleistocene envi-
ronment much earlier than previously thought.
The Berelekh site, at 70°N, dating to
⬃13,000 to 14,000 years ago (1), has long
been accepted as the earliest evidence of
humans anywhere in the Arctic (2, 3). Other
Paleolithic sites in northeast Asia, including
those in the Aldan River valley, lie far south
of the Arctic Circle. Moreover, the dates for
the oldest Aldan sites, ⬃32,000 to 33,000
years ago, as reported in the mid-1970s (4),
are not universally accepted.
East Siberia was thus thought to have
been colonized no earlier than 20,000 to
22,000 years ago. Some researchers believe
the harsh glacial environment prevented hu-
man occupation of western Beringia until
after the Last Glacial Maximum (LGM),
about 18,000 years ago (5–7). Here, we de-
scribe a newly discovered, Paleolithic site on
the Yana River, Siberia, at 71°N, that dates to
27,000
14
C years before present (
14
C yr B.P.)
[about 30,000 calendar years (cal yr) ago] and
discuss the implications for the peopling of
this and adjacent regions.
The Yana River (Fig. 1) flows north for
879 km, first through sub-Arctic, then Arctic,
regions, and empties into the Laptev Sea at
72°N. It is one of northeast Asia’s largest
rivers, with a basin of 238,000 km
2
. Much of
that basin lies within the Arctic Circle. In
1974, Scherbakova located nine Holocene
sites between Verkhoyansk and the Yana-
Adycha junction along the Yana River (8). A
decade later, nearly 70 Late Holocene sites
had been found (9). However, several hun-
dred kilometers of the Yana Valley, from the
Yana-Adycha junction to the Arctic Ocean,
remained largely unknown archaeologically.
Little industrial activity occurred here.
The Yana RHS. In 1993, Mikhail
Dashtzeren found a carefully worked fore-
shaft, with bevel ends (Fig. 2), made from the
horn of a wooly rhinoceros (Coelodonta an-
tiquitatis) in the Yana Valley. It bears a strik-
ing resemblance to Clovis foreshafts from
North America (10–12). Surviving Clovis
foreshafts are made from ivory. Rhinoceros
horn, more flexible and less rigid, may have
been more suitable than ivory. But rhinocer-
oses became extinct in Siberia about 14,000
to 15,000 radiocarbon years ago (13) and are
not believed to have reached the New World.
Presumably, Siberian hunters brought the
technology of foreshafts with them when they
entered the New World. Foreshafts permitted
hunters to replace broken points quickly, then
hurl the spear again—a great advantage when
facing big game. Guided by Dashtzeren, we
found a Paleolithic site in situ and named it
Yana RHS. It occupies an ancient terrace on
the river’s left bank, at 70°43⬘N, 135°25⬘E
(Figs. 1 and 3), about 100 km south of the
current mouth (Fig. 1). At the site, ice-
complex alluvial deposits form two terraces
of different ages (14).
The higher terrace, formed by frozen silt
with syngenetic ice wedges 4 to 5 m wide,
rises to 40 m above the water line (a.w.l.).
Because erosion is occurring at the top of the
terrace, we use the water level as a baseline
for all measurements. Radiocarbon dates
place the age of this terrace at ⬃30,000 to
35,000
14
C yr B.P. Pleistocene bone remains
collected in situ in the upper third of the
exposure date to ⬎45,000
14
C yr B.P. (GIN
11697, bison; and GIN 11696, horse). Simi-
larly, plant remains (peat) from 18 and 32 m
a.w.l. date to ⬎32,000 (LE 6027) and
⬎29,000
14
C yr B.P. (LE 6002), respectively.
The lower terrace, which is frozen, rises to
16 to 18 m a.w.l. Its active horizon is no
deeper than 0.7 to 0.8 m. The bottom layer is
bedded sandy loam. At 12 m a.w.l., silt re-
places loam. Terrace deposits include synge-
netic ice wedges up to 2 m wide that form a
polygonal grid. Polygons are relatively small,
with a width on each side of 5 to 7 m. Here
and there, second-generation ice wedges ap-
pear with widths reaching 0.5 m. The alluvial
deposits contain numerous filiform rootlets
and residues of twigs (or roots), plus isolated
inclusions of allochthonous peat (Figs. 3 and
4). The upper part of the lower terrace also
has a few lenses of Holocene lacustrial sedi-
ments 4 to 5 m thick that contain branches
and tree fragments. Radiocarbon dates from
these plant and tree remains vary from 3000
to 6700
14
C yr B.P. (Fig. 3).
The river now erodes this lower terrace.
During our survey in 2001, we found four mod-
ern beaches with high concentrations of artifacts
and broken and burnt bones along about 800 m
of the river. The artifacts were most abundant on
the roughly level inner edges of the beaches up
1
Institute for the History of Material Culture, Russian
Academy of Sciences, 18 Dvortsovaya nab., St. Peters-
burg 191186, Russia.
2
Geological Institute, Russian
Academy of Sciences, 7 Pyzhevsky pereulok, Moscow
119017, Russia.
3
Geological Research Laboratory of
the North, Faculty of Geography, Moscow State Uni-
versity, Leninskie Gory, Moscow 119992, Russia.
4
Arc-
tic and Antarctic Research Institute, 38 Bering Street,
St. Petersburg 199397, Russia.
*To whom correspondence should be addressed. E-
mail: archeo@archeo.ru, pitulko.volodya@nmnh.si.edu
Fig. 1. Location map of the Yana RHS site.
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to 1.5 m a.w.l. In several places, cultural mate-
rial appeared in talus just above the beaches
with the highest abundance of bones and arti-
facts. Most of the beach material was covered
slightly with sediment (Fig. 3).
On the modern floodplain, we found the
remains of several collapsed frozen blocks of
sediment. Some of these blocks evidently
descended intact, holding units full of arti-
facts, diverse-sized flakes, and fragmented
bones. Four radiocarbon dates were obtained
from these bone fragments, excavated from a
depth of 0.5 m in the floodplain (table S1).
Returning in 2002, we found at 7 to 8 m
a.w.l. deposits of unevenly distributed arti-
facts and animal bones (including mammoth,
bison, and horse), representing an in situ
cultural layer within the lower terrace
(TUMS1) (Fig. 4; figs. S1 to S3 and S5). We
identified this same cultural layer (under the
same geological conditions and at the same
elevation) at three other exposures: TUMS2,
AMA, and in a trench (Trench A) (figs. S4,
S6, and S7). In that trench, the vertical dis-
tribution of the cultural material could be
traced from concentrated surface finds at zero
level, up the slope to 7.5 m a.w.l. No artifact
lay at a higher level.
Geochronology. A horse mandible, asso-
ciated with small bone fragments and stone
flakes of varied size (fig. S8), was found in situ
in a river bank cut at TUMS1. It lay at 7.5 m
a.w.l. and dated 27,300 ⫾ 270
14
C yr B.P. (Beta
173067). These and other finds clearly marked
an occupation level of 27,000 radiocarbon yr
B.P., at 7 to 7.5 m a.w.l.: stratigraphically
sealed within regular bedded silt accumulation,
and retaining primary cryo texture.
The age of the occupation level was sup-
ported by a sequence of additional radiocar-
bon dates (standard radiometric), obtained
from different elevations (Fig. 4, table S1).
Elevations are given in meters above water
level, from bottom to top, within the exposed
area of TUMS1. At 6.75 m a.w.l., plant ma-
terial (filiform rootlets) dated 26,500 ⫾ 600
14
C yr B.P. (LE 6443). At 7.5 m a.w.l., plant
remains dated 25,900 ⫾ 750
14
C yr B.P. (LE
6444). At 8.3 m a.w.l., twigs dated 18,100 ⫾
340
14
C yr B.P. (LE 6445). At 9.6 m a.w.l.,
plant remains (filiform rootlets) dated
22,400 ⫾ 300
14
C yr B.P. (LE 6446).
All dates, except at 8.3 m, agree with their
stratigraphic position. Inversion at 8.3 m
a.w.l. is less important than the consistency
of the other dates. Plant material samples
(filiform rootlets, water-screened with fil-
tered water) produce either average ages or
ones slightly younger than the level from
which they were collected. The two most
important dates (6.75 m and 7.5 m a.w.l.)
overlap with the horse mandible date at a 2␴
level of confidence.
Eight additional
14
C dates link the cultural
layer, blocks excavated on the modern flood-
plain, and surface finds. Six relate directly to
the cultural material (table S1). Four of these
(15, 16) came from the eroded cultural layer
near the western limit of the elongated am-
phitheater, formed on the banks by thermo
erosion (Fig. 3). Two came from foreshafts.
Two others are dates on bones of a brown
bear and Pleistocene lion. Bone collagen was
used in both the radiometric and accelerator
mass spectrometry dating.
Four standard radiometric dates were ob-
tained from bones found on the floodplain
(Secondary Context). The youngest is 25,800
⫾ 600
14
C yr B.P. (GIN 11465). Three others
are 27,800 ⫾ 500
14
C yr B.P. (GIN 11464),
27,400 ⫾ 600
14
C yr B.P. (GIN 11466), and
27,600 ⫾ 500
14
C yr B.P. (GIN 11467). GIN
11465 was run on a partly burnt piece of
mammoth ivory. Sample GIN 11467 is a
horse bone containing an embedded flake,
together with a patch of gray silt, the parent
material of the cultural layer. The material,
used for the two other GIN dates, as well as
all bone fragments that were radiocarbon dat-
ed, bore clear utilization, butchering, or cook-
ing marks (table S1).
The rhinoceros foreshaft, one of two ivory
foreshafts, and a horse mandible were dated
by accelerator mass spectrometry. The rhi-
noceros foreshaft dates 27,440 ⫾ 210
14
Cyr
B.P. (Beta 162233). One of the two ivory
foreshafts dates 28,250 ⫾ 170
14
C yr B.P.
(Beta 173064). Both dates come from surface
finds, as do dates from the Pleistocene lion
and brown bear.
The date for the horse mandible lies be-
tween that of the Pleistocene lion, 26,050 ⫾
240
14
C yr B.P. (Beta 173066), and that of the
brown bear, 28,280 ⫾ 300
14
C yr B.P. (Beta
173065). This helps to estimate the age of the
Fig. 2. Wooly rhinoceros foreshaft found by
Dashtzeren in 1993.
Fig. 3. Stratigraphy of the Yana River left bank bearing cultural deposits: (1)
loamy sand; (2) silty loam; (3) organic partings–silty–sandy loam alternation
strata; (4) contemporary slope and proluvum-alluvium deposits; (5) ice-
wedges; (6) clear contact line; (7) gradational contact; (8) suggested presence
of the cultural level; (9) observed position of the cultural level at 7 to 7.5 m
a.w.l.; (10) direction of transportation of archaeological material eroded from
the cultural layer, and concentrations of it; (11) artifacts; (12) broken bones;
(13) dated bone material; (14) dated plant, wood, and peat material.
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surface bone collection (17 ). The date of the
horse mandible alone links that collection to
cultural level.
No contradiction occurs between the
14
C
dates of the cultural layer, secondary context,
and surface finds. Four dates fall within 400
years of each other and overlap at a 1␴ level
of confidence. Almost all overlap at a 2␴
level of confidence. The coherency and con-
sistency of dates suggest the site was occu-
pied ⬃27,000 radiocarbon yr B.P. (about
30,000 cal yr ago).
Stone industry. During 2001 and 2002,
we collected 376 artifacts of flinty slate, 1
object of granite, and 6 of quartz. Slate and
granite occur in the riverbed. The quartz ev-
idently came from elsewhere. More than 90%
of these artifacts were on the beach as rede-
posited “surface finds,” although some were
covered by sediment. Flake scars on all flinty
slate artifacts are well preserved. No object
bears traces of rolling or river erosion.
We have not yet found any formal tool
from the cultural layer. However, the cultural
layer in the TUMS1 profile (Fig. 4) yielded
flakes (n ⫽ 73) and bone fragments (n ⫽ 47),
differing in size, the smallest being 2 to 3
mm. Small pieces of red ocher were also
found. The flakes, bone fragments, and ocher
were recovered by water screening (figs. S8
and S9). Clearly, material in the cultural layer
remained unsorted, in situ, as originally de-
posited some 27,000 years ago. No other
cultural material along the riverbank, for a
distance of 1.5 km, appears to be mixed. This
suggests that Yana RHS is a single compo-
nent site, representing a single, Upper Paleo-
lithic stone industry.
The Yana RHS stone industry comprises
unifacial and bifacial flaking of pebbles (si-
liceous slate) and nonpebble rocks (quartz
crystal) (Fig. 5). Included are core-tools and
flake-tools, with flakes (67%) as by-products
of tool production. Some flakes were worked
unifacially, many with ventral retouching.
The remainder of the collection (33%, n ⫽
125 pieces) was identified as tools. Major
tool types include cores (n ⫽ 27); chopper
and chopping tools (n ⫽ 15); bifacial and
unifacial tools (n ⫽ 36), including pointed
pieces; side and angle-scrapers (n ⫽ 35);
end-scrapers (n ⫽ 2); chisel-like tools (n ⫽
2); retouched flakes (n ⫽ 7); and a single
hammer stone.
Berelekh, Dyuktai, and other sites of the
Dyuktai culture do not relate to the Yana
RHS industry and date considerably later (1,
4). No evidence of prismatic blades or
wedge-shaped cores was found at Yana RHS.
However, both Yana RHS and Berelekh site
have vast quantities of Pleistocene bones,
especially mammoth bones. Both adjoin river
crossings where big game could be trapped or
often drowned when ice gave way.
Organic artifacts. The rhinoceros fore-
shaft measures 478 mm long (Figs. 2 and
6A). Its mid-diameter is 15 mm. It tapers
slightly toward each end to 12 and 14 mm in
diameter. Both ends are beveled on one side.
This gives each end a half-round cross sec-
tion. The angle of each bevel is asymmetri-
cally offset with respect to the center line of
the shaft.
At present, this foreshaft is slightly
curved, probably due to the residual imprint
of the parent material. During manufacture, it
may have been straightened with a shaft
wrench, combined with soaking, steaming,
and/or heating. Morphologically similar
specimens, but made from mammoth or
mastodon ivory, are known from a handful of
early sites in North America (10–12).
Two foreshafts of mammoth ivory, one
complete, one fragmentary, were also recov-
ered. Both were associated with stone tools and
broken bones. Each is shorter than the rhinoc-
eros foreshaft, but has the same shape, diame-
ter, and width, in addition to the beveled ends.
What appears to be a punch or an awl, made
from a wolf (Canis lupus L.) metatarsal (Fig.
6B), was also found. Its distal end was not
recovered, but what remains is 89 mm long,
indicating a large animal, but within the range
of modern wolves. Deliberate cuts on the bone
may have kept a wrap in place, while the wrap,
over time, burnished the bone.
Fig. 4. Stratigraphy observed from TUMS1 pro-
file: (1) permanently frozen cultural level; (2)
dated horse mandible found in situ in associa-
tion with flakes and small bone fragments (pri-
mary context); (3) radiocarbon dates obtained
for the profile.
Fig. 5. Stone artifacts from Yana RHS: (A) a side scraper with bifacially retouched working edge; (B)
worked piece of quartz crystal; (C) end scraper; (D) pointed tool; (E) a side scraper with bifacially
retouched working edge. (A), (C), and (D), siliceous slate; (B), quartz crystal; (E), chert.
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Faunal remains. Nearly 800 bones and
bone fragments were collected at the Yana RHS
and along the riverbank (18). These included
both identifiable and unidentifiable bones.
About a third of those identified can be associ-
ated with the exposed cultural layer. Bones
identified by element (n ⫽ 28), as well as small
water-screened fragments (n ⫽ 47 ), were ex-
cavated from the cultural layer, together with
the artifacts. The others were simply gathered
along the riverbank, both upstream and down-
stream from the site, for 1500 m.
On the basis of their potential relation to the
cultural layer, these materials are grouped as
follows: (i) bones and bone fragments discov-
ered in the cultural layer; (ii) bones and bone
fragments from the talus and floodplain terrace
below the cultural layer; (iii) concentrations
found on the beach downstream of the exposed
cultural layer; and (iv) bones and bone frag-
ments with no relation to the cultural layer, or
with very low probability of such a relation.
The primary context, or Context One, the
cultural layer, contained mammoth (Mam-
muthus primigenius Blumenbach) bones collect-
ed directly from the cultural layer (from 7 to
7.5 m a.w.l.). These include a small skull frag-
ment, small fragments of ivory (split pieces), a
fragment of thoracic vertebra of a young animal,
and fragments of long mammoth bones. A horse
(Equus caballus L.) mandible fragment with
teeth was also recovered and dated. They also
include reindeer (Rangifer tarandus L.) mandi-
ble fragments with teeth, isolated teeth, as well
as fragments of radii, calcanei, and vertebrae;
two bison (Bison priscus Bojanus) phalanges
and a scapulae fragment; and Pleistocene hare
(Lepus tanaiticus Gureev) vertebra and metacar-
pal, plus fragments of scapula, humerus, and
mandible. There is also a wooly rhinoceros
(Coelodonta antiquitatis Blumenbach) tooth
fragment, plus several dozen (n ⫽ 47) small,
unidentified bone fragments from the same cul-
tural level. All large bones, and almost all small
fragmented bones, show traces of scraping.
Bones and bone fragments were collected
from the talus, floodplain, and beach. All
these areas lay below and adjacent to the
cultural layer. Presumably, many came from
there, as evidenced by the following: (i) large
accumulations of bones appeared only in lo-
cations where this cultural layer was exposed
or was recently exposed; (ii) one bone, sent
for dating, contained a small stone flake; (iii)
stone artifacts accumulated in these same lo-
cales; (iv) some of the bones bore traces of
scraping; (v) intact, cracked, or slightly frag-
mented bones would normally be found in
these regions, whereas the overwhelming ma-
jority were broken into small fragments, yet
bore no evidence of “rolling”; (vi) the same
accumulations contained burnt bone frag-
ments; and (vii) radiocarbon dates from these
bones are close to those from the cultural
layer (see above). In addition to the bones of
mammoth, wooly rhinoceros, reindeer, horse,
bison, and Pleistocene hare, we identified
bones from six other species: musk-ox (Ovi-
bos moschatus Zimmerman), wolf (Canis lu-
pus L.), polar fox (Alopex lagopus L), brown
bear (Ursus arctos L.), the Pleistocene lion
[Panthera spelaea (Goldfuss)], and a wolver-
ine (Gulo gulo L.).
Context Two. About 260 bones and bone
fragments (excluding numerous, unidentified,
small and tiny bone fragments) were found
under conditions where their relation to the
cultural layer was evident. These represented
11 mammalian species (18), plus unidentified
birds. Mammals included mammoth, rhinoc-
eros, Pleistocene bison, horse, reindeer,
musk-ox, wolf, polar fox, Pleistocene lion,
brown bear, and wolverine. Only the reindeer
and wolf still inhabit this area. Wolverine and
bear are occasionally reported along the
coastal lowland. The others (mammoth, rhi-
noceros, bison, lion) became extinct in Sibe-
ria or no longer reside there (musk-ox, horse).
The Arctic hare replaced the Pleistocene hare.
Contexts Three and Four are hard to dis-
tinguish. Over 540 bones were found on the
beach, upstream and downstream from the
exposed cultural layer. Presumably, some be-
longed to this cultural layer, but we cannot
link them unequivocally. The number of in-
tact bones in this collection is much greater
than that in the cultural layer. The composi-
tion of species remains the same. These in-
clude also the musk-ox (Ovibos moschatus
Zimmerman), wolf (Canis lupus L.), polar fox
(Alopex lagopus L.), brown bear (Ursus arc-
tos L.), and a wolverine (Gulo gulo L.). Only
one species, the Pleistocene lion [Panthera
spelaea (Goldfuss)], is not present in the cul-
tural layer. A single lion shoulder bone was
found after the water dropped in late Septem-
ber, not too far from where Dashtzeren found
the rhinoceros shaft. This bone dates to
26,050 ⫾ 240
14
C yr B.P. (Beta 173066).
Conceivably, this species inhabited the area
contemporaneously with the site occupancy.
Bones from the site, and from the surround-
ing area, appear typical of the Late Pleistocene
in this area. Mammoth bones are relatively
common, possibly from human activity. Rein-
deer is the most common species directly in the
cultural site and presumably served as the major
game animal. Bird bones also were found only
at the site. Those who camped here evidently
hunted reindeer, horses, and birds.
Implications. For more than 100 years,
archaeologists have speculated about human
residents in the Arctic during Pleistocene times,
but lacked confirming evidence. The Yana
RHS provides that evidence. The record of
Arctic sites is fragmented: Yana RHS at 27,000
14
C yr B.P., Berelekh at 13,000
14
C yr B.P. (1,
4), and Zhokhov at 8000
14
C yr B.P. (19).
These time gaps need to be filled for a more
complete understanding.
Formation of the cultural layer at Yana
RHS coincides with the boundary between
Kuranakh-Sala warming [the terminal stage
of Karginsk/Middle Wisconsin (MW) Inter-
val] and the Mus-Khaya cooling of Sartan/
Late Wisconsin Glacial. The environment of
the Yana delta then shifted from open, flood-
plain meadows to tundra. This part of Asia
was never covered with large ice sheets. Av-
erage temperatures, reconstructed from pol-
len records, were colder than are those of
today (20, 21). During Karginsk times, both
landscape and climate varied in western Ber-
ingia (22). However, the environment re-
mained favorable for large herbivores.
The extensive Bering Land Bridge formed
during the Early Wisconsin Glacial (50,000
Fig. 6. Organic artifacts from Yana RHS: (A) the rhino horn foreshaft (proximal end); (B) wolf
metatarsal bone (a broken awl?) with multiple cut marks; (C) cut marks (enlarged).
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to 70,000 cal yr B.P.). It remained partly
emergent during the warm Karginsk/MW In-
terval (23,000 to 50,000 cal yr B.P.). Paleo
valleys of several major rivers (Lena, Yana,
and others) can be traced on the Arctic shelf
to a depth of 50 m at this time (23).
Yana RHS offers bifacial technology with
no sign of blade making. By contrast, the
Dyuktai culture combines bifaces with a
blade industry based on wedge-shaped cores
(3). Its earliest appearance in the Bering Land
Bridge region dates to about 12,000 to 11,000
cal yr B.P. (24 ). Yana is 27,000 radiocarbon
yr B.P. In theory, the Yana people may have
crossed over the land bridge toward the end
of Karginsk Interval.
It is difficult to assess similarities between
Yana RHS and Clovis foreshafts. Thousands of
kilometers and roughly 16,000 years separate
them. Their similarity is intriguing, and they
both have bifacial industries. Although a direct
connection remains tenuous, the Yana RHS site
indicates that humans extended deep into the
Arctic during colder Pleistocene times.
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12. J. Dunbar, S. Webb, D. Cring, in Bone Modification,R.
Bonnichsen, M. Sorg, Eds. (CSFA Publications, Oregon
Univ. Press, 1989), pp. 473–497.
13. L. Sulerzhitsky, F. Romanenko, Cryosphera Earth 1,27
(1997).
14. Apparently, these terraces present Terrace 3 (the
higher one, 35 to 40 m a.w.l.) and Terrace 2 (lower
terrace, 16 to 18 m a.w.l.). Terrace 1 is not presented
within the bluff. Presumably, it is totally eroded here.
The floodplain terrace, or Terrace 0, exists here in the
form of small sections.
15. First
14
C dates for the site obtained by L. D. Suler-
zhitsky (Geological Institute, Russian Academy of
Sciences, Moscow).
16. Species identification for
14
C samples provided by
E. A. Vanghenheim (Geological Institute, Russian
Academy of Sciences, Moscow).
17. The Yana RHS bone collection offers the full range of
carnivore species present at the end of the Karginsk
Interval. Carnivore bones, especially those of the
large species, rarely appear in natural exposures. The
appearance of so many bones in one place suggests
human activity in the past.
18. Species identification provided by P. A. Nikolsky
(Geological Institute, Russian Academy of Sciences,
Moscow).
19. V. Pitulko, Quat. Sci. Rev. 20, 267 (2001).
20. T. N. Kaplina, A. V. Lozhkin, Izv. Akad. Nauk SSSR Ser.
Geogr. 2, 84 (1982) [in Russian].
21. G. G. Kartashova, Vestn. Mosk. Univ. Geogr. 6,37
(1983) [in Russian].
22. P. M. Anderson, A. V. Lozhkin, Quat. Sci. Rev. 20,99
(2001).
23. Yu. A. Pavlidis, Shelf Mirovogo Okeana v pozdnechet-
vertichnoe vremya (Nauka, Moscow, 1992) [in Rus-
sian].
24. T. Goebel, M. R. Waters, M. Dikova, Science 301, 502
(2003).
25. The Zhokhov-Yana Project, a long-term Russian-
American effort, is directed by V. Pitulko and fi-
nanced by a private foundation in New York. Unlim-
ited thanks to M. Dashtzeren, who guided us to Yana
RHS; to the Lena-Delta Wildlife Reserve, Tiksi; to E.
Savchenko, VICAAR (Victory Arctic & Antarctic Re-
search, Ltd., St. Petersburg), for logistic skills; and to
L. Sulerzhitsky (Geological Institute, Moscow), who
provided
14
C dates when we were in the field. Un-
limited thanks to the 28 people who, to date, worked
at the Yana site.
Supporting Online Material
www.sciencemag.org/cgi/content/full/303/5654/52/
DC1
Figs. S1 to S9
Table S1
2 April 2003; accepted 14 November 2003
Foxg1 Suppresses Early Cortical
Cell Fate
Carina Hanashima,
1,2
Suzanne C. Li,
2
* Lijian Shen,
3
Eseng Lai,
2
†‡
Gord Fishell
1
‡
During mammalian cerebral corticogenesis, progenitor cells become progres-
sively restricted in the types of neurons they can produce. The molecular
mechanism that determines earlier versus later born neuron fate is unknown.
We demonstrate here that the generation of the earliest born neurons, the
Cajal-Retzius cells, is suppressed by the telencephalic transcription factor
Foxg1. In Foxg1 null mutants, we observed an excess of Cajal-Retzius neuron
production in the cortex. By conditionally inactivating Foxg1 in cortical pro-
genitors that normally produce deep-layer cortical neurons, we demonstrate
that Foxg1 is constitutively required to suppress Cajal-Retzius cell fate. Hence,
the competence to generate the earliest born neurons during later cortical
development is actively suppressed but not lost.
In both invertebrate (1, 2) and vertebrate (3, 4)
central nervous system development, neuronal
progenitors produce specific cell types in a
characteristic temporal order. Analysis in the
mammalian brain (5–7) and retina (8–10) sug-
gests a general rule governing this process:
Neural progenitors can produce cells character-
istic of later but not earlier points in develop-
ment. The mechanism behind this progressive
restriction in progenitor potential is not under-
stood. The laminar cell fate in the mammalian
cortex provides an excellent model for studying
these changes in progenitor potential. The
mammalian cerebral cortex comprises six lay-
ers of neurons that are generated in an orderly
sequence during development (11, 12). With
the exception of the Cajal-Retzius (CR) cells,
which reside in layer 1, the cerebral cortex is
produced in an inside-out manner. The deeper
layer cells exit the ventricular zone (VZ) first,
followed by more superficial cells at later peri-
ods. Hence, the birthdate of a cortical neuron is
predictive of its fate (13–15). Furthermore, cell
transplantation studies suggest that early-born
classes of neurons can adopt later cell fates but
not the converse (5–7). Thus, during cortical
development, there appears to be a ratcheting
mechanism by which the potential of early pro-
genitors is progressively restricted.
The first restriction in the neuronal cell types
that cortical progenitors can generate is the tran-
sition from the production of CR cells to the
production of deep-layer neurons. CR cells, in
addition to being the first postmitotic popula-
tion, are of particular importance for the devel-
opment of a properly organized cerebral cortex
(16, 17). CR cells reside in the subpial region of
layer 1 and secrete the extracellular glycoprotein
Reelin (18, 19), which provides a critical signal
for the guidance of later born cells that populate
the cortical laminae. One of the few genes
known to affect this early phase of cortical
development is Foxg1, which encodes a winged
helix transcriptional repressor (20–22). Foxg1
controls the number of cells produced in the
cortex and the loss of this gene results in hyp-
1
Developmental Genetics Program and the Depart-
ment of Cell Biology, The Skirball Institute of Biomo-
lecular Medicine, New York University Medical Cen-
ter, 540 First Avenue, New York, NY 10016, USA.
2
Cell Biology Program, Memorial Sloan-Kettering
Cancer Center, 1275 York Avenue, New York, NY
10021, USA.
3
Department of Physiology and Biophys-
ics, Weill Medical College of Cornell University, New
York, NY 10021, USA.
*Present address: Hackensack University Medical Center,
30 Prospect Avenue, Hackensack, NJ 07601, USA.
†Present address: Clinical Pharmacology, Merck Re-
search Labs, RY34-A-428, 126 East Lincoln Avenue,
Rahway, NJ 07065– 0900, USA.
‡To whom correspondence should be addressed. E-
mail: fishell@saturn.med.nyu.edu (G.F.); eseng _lai@
merck.com (E.L.)
R ESEARCH A RTICLES
2 JANUARY 2004 VOL 303 SCIENCE www.sciencemag.org56