Wheo the WorIds FopuIatioo Iook II.

Ihe 8priogboard oI the NeoIithic

eographic Iraositioo
)ean-Pierre 8ocquet-Appel
uurng the econonc transton fron foragng to farnng, the sgnal of a na|or denographc shft can be
observed n cenetery data of World archaeologcal sequences. Ihs sgnal s characterted by an abrupt
ncrease n the proporton of |uvenle skeletons and s nterpreted as the sgnature of a na|or denographc
shft n hunan hstory, knoWn as the Neolthc uenographc Iranston (NuI. Ihs expresses an ncrease
n the nput nto the age pyrands of the correspondng lvng populatons Wth an estnated ncrease
n the total fertlty rate of tWo brths per Wonan. Ihe unprecedented denographc nasses that the NuI
rapdly brought nto play nake ths one of the fundanental structural processes of hunan hstory.
A
Iter the members oI the genus Homo had
been living as Ioragers Ior at least 2.4 mil-
lion years, agriculture began to emerge in
seven or eight regions across the world, almost
simultaneously at the beginning oI the Holocene:
in the Levant, in North and South China, in New
Guinea and Ethiopia, and in eastern North Amer-
ica, Mesoamerica, and South America, all during
the chronological window Irom 11,500 to 3500
years ago (1). In world archaeological sequences,
the emergence oI agriculture coincides with a con-
siderable increase in arteIact remains, which was
long interpretedas indicatinga spurt in demographic
growth. The worlds population on the eve oI the
emergence oI agriculture is estimated to have been
around 6 million (2) individuals as against almost
7 billion today, multiplying by 1200 in just 11,000
years. The shiIt Irom Iorager to producer societies
is known as The Neolithic Revolution (3). The ma-
jor change that arose Irom this revolution was, in
evolutionary time, the number oI potential mouths
it was possible to Ieed per km
2
, i.e., the weight oI
the population, 0.05 people per km
2
with the
Ioraging system as against 54 today and, perhaps,
70 to 80 by 2050. The archaeological data, such
as the increasing density oI settlement sites during
the transition, are too imprecise to express the de-
mographic shiIt. Cemetery data provide a more
direct reIlection oI demographic processes, and it
is Irom cemeteries that the signal oI a major demo-
graphic shiIt can be observed in world archaeo-
logical sequences in the Northern Hemisphere
(Fig. 1). This signal is characterized by a relatively
abrupt increase in the proportion oI 5- to 19-year-old
juveniles in cemeteries during the economic tran-
sition Irom Ioraging to Iarming. This proportion
(called
15
p
5
in demographic notation) leveled
oII 1000 years aIter the advent oI the Iarming
system locally (dt 1000 years). This expresses
an increase in the input into the age pyramids oI
the corresponding living populations (4, 5),with
an estimated increase in total Iertility rate oI
two births per woman.
What, in the agricultural economy, had an im-
pact on human biology that ultimately determined
the growth oI the population? The increase in
natural maternal Iertility, through a reduction in
the birth interval, is mainly determined by the
energy balance and the relative metabolic load
(6). It implies a positive return oI the postpartum
energy balance, which occurred earlier in Iarming
than in Ioraging societies due to the energy gain
Irom the high-calorie Iood oI sedentary Iarmers
(wheat, lentils, peas, maize, rice, and millet) com-
pared to the low-calorie Iood oI mobile Ioragers
(mainly game), coupled with a decrease in the
energy expenditure oI carrying inIants. This signal
is interpreted as the signature oI a major demo-
CN8S (Natluual Ceuter ur Scleutllc 8esearch, ul82l47 aud
LlhL (lractlcal Schuul u hlqh Studles, 44, rue de l'Aulcal
\uuche, larls 750l4, lrauce. L-uall: |eau-plerre.bucquet-
appelQevulhuu.curs.r

d (years)
1
5

5
llg. 1. Ihe proporton of 5- to 19-
year-old skeletons (to all skeletons 5
or nore years old (vertcal axs:
15

n 133 ceneteres across the North-

ern hensphere durng the transton
fron foragng to farnng (hortontal
axs: dr. Ihe hortontal axs dr repre-
sents the tne that elapsed betWeen
the advent of farnng at that partc-
ular locaton, algned at dr = 0 |fron
(25|. (8eIow Ihe populaton explo-
son of the Neolthc uenographc Iran-
ston, detectable n ceneteres, Was
unprecedented n the hstory of homo
salens. Neolthc gallery grave of La
Chaussee Irancourt, lrance (~4500
years before the present.
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22 SCIENCE www.sciencemag.org
graphic shiIt in human history and is known as
the Neolithic Demographic Transition (NDT) (7)
or, synonymously, the Agricultural Demographic
Transition. These demographic shiIts can be seen
in the west oI southwestern Asia (8), mainland
Southern Asia, Europe and North AIrica, and the
north and southwest oI North America (9, 10).
The NDT is detectable Irom a signal represent-
ing a shiIt toward higher Iertility values, but the
mortality part oI the signal is missing and must be
inIerred. The universal density-dependent (also
called Malthusian, or homeostatic) demographic
model is used here. Unless we assume a demo-
graphic growth rate that would rapidly reach a
cosmic number, the most likely scenario is that
an increase in the birth rate was closely Iollowed
in time by an increase in mortality, producing the
historical growth rate typical oI pre-industrial Iarm-
ing populations (0.2 to 0.1 per year), with their
high birth and mortality rates.
What might have been the causes oI the in-
creased mortality rate? Old and new pathogens
would have contributed. With the appearance oI
sedentary village liIe and the corresponding growth
in local population density, mortality rates inherited
Irom the Ioragers rose rapidly, particularly in chil-
dren under 5 years oI age. Causes oI increased
inIant mortality include a lack oI clean drinking
water, contamination by Ieces and the absence oI
latrines, and reduced breastIeeding as maternal
Iertility increased. Candidate inIectious diseases,
by epidemiological inIerence Irom current pre-
industrialized areas, include those associated with
diarrhea (Rotavirus and Coronavirus) as the main
killers oI children under 5 years oI age. Zoonoses
could have had an impact on the population with
the introduction oI animal domestication, whether
at the same time as plant domestication |pigs, wa-
ter buIIalo, and probably chickens in China; guin-
ea pigs, llamas, and alpacas (11) in the Andean
highlands| or later |goats, sheep, and subsequent-
ly cattle and pigs in the Levant (12)|.
When compared with the Contemporary De-
mographic Transition (CDT) as described Ior
Western industrialized societies, the NDTwas its
mirror image. In the CDT, the decline in mortality
was Iollowed by a decline in Iertility, but in the
NDT, increased Iertility was Iollowed by increased
mortality. The CDT is slowing the growth oI the
world population, but the NDT was its spring-
board. In both cases, however, the time lag between
the two stages produced an interval in which Iertility
exceeded mortality and resulted in a rapid increase
in the population. As demographic density in-
creased appreciably in the centers oI these zones, the
NDT triggered a major geographical redistribu-
tion oI the population, with colonization or invasion
by early Iarmers with their technologies, liIe-
styles, and languages that in some cases reached
the continental scale, supporting what RenIrew
and Bellwood have called the Iarming/language
dispersal hypothesis (13). Simultaneously, the
NDT was accompanied by increasing social strat-
iIication and complexity, the advent oI market
economies, and the ensuing emergence oI states.
The demographic limit at which a hamlet be-
comes a village can be deIined by the cognitive
limit oI integration by the human brain oI numbers
oI interpersonal relationships, i.e., 150 people (14).
Although villages were established by sedentary
Ioragers, in geographically Iixed zones with dense
Iood resources (wild grasses, shellIish, Ireshwater
Iish, various nuts) in several points on the planet
and in the same chronological windowas the NDT,
these Iorager villages were marginal exceptions.
Their economic system was constrained by the
limits oI nature, which leIt little margin Ior demo-
graphic growth. World archaeological sequences
show that the Iirst sedentary villagers emerged in
large numbers Irom the NDT. They were Iaced
with entirely new social, economic, and ecological
challenges. NDT villagers are discussed in the vol-
ume edited by Bandy and Fox (15). In comparison
with nearly 2.5 million years oI a Iorager culture,
the NDT, in just a Iew hundred years, or two or
three millennia at most, caused humans to domes-
ticate themselves in villages. In these primitive vil-
lage societies oI Iarmers, say these two authors,
liIe was improvised, provisional, and innovative.
Do these early villages represent evolutionary re-
sponses Irom the Iirst human Iarmers to a set oI
new, recurrent, and comparable socioecological
conditions? II so, what were the major Iactors that
shaped developments oI these early villages? With
the demographic concentration emerged political
institutions, Iromvillage to proto-city, Irombig man
to chieIdom. In world archaeological sequences,
what are the similarities and dissimilarities with the
tempo oI demographic concentration (16)? At the
peak oI the NDT, there were children everywhere
and the average age oI the population was about
18 years old. What evidence or impacts oI this ex-
ceptionally youthIul population can be recognized
in the patterns oI cultural production oI the Iirst
agricultural societies, Irom ceramics to statuary
and images?
Theoretically, the NDTwas accompanied by the
Iirst epidemiological transition (17). Coronavirus
and Rotavirus are hypervariables, and their taxa
are not speciIically dated (18, 19). Among extant
taxa, do those endemic to prehistoric Ioragers and
responsible Ior childhood diarrhea in the NDT
still exist? The phylogenetic analyses oI three
important present-day inIectious diseases either
do not coincide with the timing oI the NDT |mea-
sles: 1100 CE (20); severe IormoI smallpox: 350
to 1550 CE (21)| or suggest a zoonosis scenario,
which is the reverse oI what is intuitively expected:
Tuberculosis (Mycobacterium tuberculosis com-
plex) was transmitted by humans to bovines dur-
ing their domestication in Mesopotamia 10,000
years ago (22). These epidemiological results are
mixed and require closer investigation. The NDT
implies RenIrew and Bellwoods Iarming/language
dispersal hypothesis and Ammerman and Cavalli-
SIorzas model oI demic expansion (23). In mo-
lecular skeleton data, one must thus expect a
phylogeny oI pioneer Iarmers derived Irom pop-
ulations oI ancestral source regions oI expansion,
as shown, Ior example, by Haak et al. (24) on the
expansion oI pioneer Linearbandkeramik (LBK)
Iarmers in central and northern Europe. But what
emerges Ior other regions oI agricultural inven-
tion? Because oI the unprecedented demographic
masses it rapidly brought into play, the NDT,
which is nowending with the CDTand the collapse
in Iertility, is one oI the Iundamental structural
processes oI human history; its multidimensional
consequences are just beginning to be explored in
terms oI sociopolitics and ideology, epidemiology,
and population genetics.
keferences and Notes
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. l. ucquet-Appel, 0. ar-Yuse, Lds. (Sprluqer,
0urdrecht, Netherlauds, 2008, pp. 5780.
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|/ans|||on and ||s conseaences, . l. ucquet-Appel,
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l0. !. A. Kuhler, \. 0. varleu, lu 8ecom|n l|||ae/s. |ne
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l2. . 0. vlque, lu |ne heo|||n|c uemo/an|c |/ans|||on and ||s
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l8. \. l. \. de Sllva e| a|., j. Ved. l|/o|. 83, 357 (20ll.
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2l. Y. Ll e| a|., |/oc. ha||. 4cad. 5c|. J.5.4. 104, l5787 (2007.
22. !. wlrth e| a|., ||o5 |a|no. 4, el000l60 (2008.
23. A. . Auueruau, L. L. Cavalll-Sura, Van (|ond. 6, 674
(l97l.
24. w. haal e| a|., ||o5 8|o|. 8, el000536 (20l0.
25. . l. ucquet-Appel, 2008. lu |ne heo|||n|c uemo/an|c
|/ans|||on and ||s conseaences, . l. ucquet-Appel,
0. ar-Yuse, Lds. (Sprluqer, 0urdrecht, Netherlauds,
2008, pp. 3556.
AcknoWledgments: !hls Wurl Was suppurted b, the
lreuch Natluual 8esearch Aqeuc, uuder reereuce
uuuber AN8-09-CLl-004-0l/08LS0C.
l0.ll26/scleuce.l208880
2012 Population Compilation Booklet
www.sciencemag.org SCIENCE 23