AMERICAN JOURNAL.

OF PHYSICAL ANTHROPOLOGY 96109-132 (1995)

Indo-European Origins: A Computer-Simulation Test of

Five Hypotheses
GUIDO BARBUJANI, ROBERT R. S O W , AND NEAL L. ODEN
Dipartimento di Scienze Statistiche, Universita di Bologna, I-40126
Bologna, Italy (G.B.); Department of Ecology and Evolution, State
University of New York, Stony Brook, New York 11 794-5245 (R.R.S.,
G.B.); The EMMES Corporation, Potomac, Maryland 20854 (N.L.O.)

KEY WORDS Genetic variation, Demic diffusion, Language,

Computer simulation

ABSTRACT Allele frequency distributions were generated by computer

simulation of five models of microevolution in European populations. Genetic
distances calculated from these distributions were compared with observed
genetic distances among Indo-European speakers. The simulated models dif-
fer in complexity, but all incorporate random genetic drift and short-range
gene flow (isolation by distance). The best correlations between observed and
simulated data were obtained for two models where dispersal of Neolithic
farmers from the Near East depends only on population growth. More com-
plex models, where the timing of the farmers expansion is constrained by
archaeological time data, fail to account for a larger fraction of the observed
genetic variation; this is also the case for a model including late Neolithic
migrations from the Pontic steppes. The genetic structure of current popula-
tions speaking Indo-European languages seems therefore to largely reflect a
Neolithic expansion. This is consistent with the hypothesis of a parallel
spread of farming technologies and a proto-Indo-European language in the
Neolithic. Allele-frequencygradients among Indo-European speakers may be
due either to incomplete admixture between dispersing farmers, who presum-
ably spoke proto-Indo-European, and pre-existing hunters and gatherers (as
in the traditional demic diffusion hypothesis), or to founder effects during the
farmers dispersal. By contrast, successive migrational waves from the East, if
any, do not seem to have had genetic consequences detectable by the present
comparison of observed and simulated allele frequencies.
0 1995 Wiley-Liss, Inc.

Wide allele-frequency clines exist a t sev- gies of Mesolithic and Neolithic settlements
eral loci in Europe (Menozzi et al., 1978; indicate a westward spread of farming tech-
Sokal and Menozzi, 1982; Sokal et al., nologies from the Near East, starting ap-
1989a). Their extent is such that simple proximately 8,000 BC (Ammerman and Cav-
models of isolation by distance are unlikely alli-Sforza, 1984; Renfrew, 1987). The
to explain them. It is generally agreed that observed gene-frequency gradients can then
they result from a population expansion be explained by attributing the propagation
starting in Anatolia approximately 10,000 of farming t o the dispersal of early farmers,
years ago (Menozzi et al., 1978; Sokal and
Menozzi, 1982; Renfrew, 1987, 1991, 1992;
Cavalli-Sforza, 1988; Sokal et al., 1991),
Received January 25,1994; accepted August 7,1994
most likely associated with the development
Address reprint requests to Robert R. Sokal, Department of
of technologies for food production (Hassan, Ecology and Evolution, State University of New York, Stony
1973; Zeven, 1980). Radiocarbon chronolo- Brook, NY 11794-5245.

0 1995 WILEY-LISS, INC.

110 G . BARBUJANI ET AL.
who interbred only sparingly with the bands
of hunters and gatherers whom they met in
the process, and who had already colonized
most of Europe (Ammerman and Cavalli-
Sforza, 1984). Such a combination of demo-
graphic growth, range expansion, and lim-
ited admixture has been termed demic
diffusion (Menozzi et al., 1978). Its expected
consequences include correlations between
allele frequencies and the dates of onset of
agriculture (Sgaramella-Zonta and Cavalli-
Sforza, 1973), which have actually been ob-
served (Sokal et al., 1991).
The European regions where early (Neo-
lithic) agriculturalists expanded correspond
approximately to the current western range
of Indo-European languages. This raises the
question whether the cultural process of
Indo-European diffusion was also deter-
mined by the demographic processes accom-
panying the spread of farming (Renfrew,
1987). The traditional view holds, on the
contrary, that proto-Indo-European entered
Europe not earlier than 4500 BC, through
three migrational waves also coming from
the East, namely from the Pontic steppes
(Gimbutas, 1979, 1986). Although directed
westwards, like demic diffusion, these
waves were not associated with population
increases comparable to those caused by the
introduction of farming and animal breed-
ing. Therefore, diffusion of Indo-European
in the late Neolithic would imply that lan-
guages spread more through cultural con-
tacts (Zvelebil and Zvelebil, 1988) than by
demographic processes (see Renfrew, 1989).
As a corollary t o this, association between
patterns of genetic and linguistic variation
should be limited and occasional among con-
temporary Indo-European speakers.
Support for the view linking the spread of
proto-Indo-European in Europe with demic
diffusion comes from studies showing that
patterns of linguistic and genetic diversity
correspond in many European populations
(Sokal, 1988; Cavalli-Sforza et al., 1988,
1992; Harding and Sokal, 1988; Barbujani
and Sokal, 1990, 1991; Bertranpetit and
Cavalli-Sforza, 1991). The exceptions in-
clude Basques (Piazza et al., 1988; Bertran-
petit and Cavalli-Sforza, 19911, Hungarians
(Barbujani et al., 1990), and Uralic-speakers
(Guglielmino et al., 19901, that is to say,
groups whose current languages do not be-
long to the Indo-European phylum.
Recent years have seen both a refinement
of the hypotheses on Indo-European origins,
and the emergence of contradictory data.
Based on archaeological and linguistic evi-
dence, Cavalli-Sforza (1988) and Renfrew
(1991, 1992) argued that the common ele-
ments recognized within the so-called Nos-
tratic linguistic macrofamily (Kaiser and
Shevoroshkin, 19881, including Indo-Euro-
pean, Altaic, Afro-Asiatic, and Elamo-Dra-
vidian, derive from a common biological ori-
gin of most of their current speakers. It is
then possible to interpret the current distri-
bution of most Nostratic, and not only Indo-
European, languages as a consequence of a
multidirectional spread of agriculture. Re-
cent genetic analyses agree with this view
(Cavalli-Sforza et al., 1993; Barbujani and
Pilastro, 1993). On the other hand, a model
incorporating the effects of the origin of agri-
culture and/or specifically the hypotheses of
Renfrew and Gimbutas failed to explain a
larger fraction of the correlations between
genetic and linguistic distances than is ex-
plained by the simple effects of geographic
distances (Sokal et al., 1992).
Further evidence in favor of either hy-
pothesis may be obtained by simulating
their genetic consequences, and then com-
paring them with the patterns of genetic
variation observed in the field. In the only
simulation study available so far, present-
time genetic variation was demonstrated to
be compatible both with a Neolithic origin of
Indo-European speakers, and with later im-
migration from the Pontic steppes (Rendine
et al., 1986). However, the two hypotheses
were not contrasted in that study, but com-
bined. A relationship between current gene-
frequency gradients and dispersal from the
east was evident, and seems undisputable.
However, when exactly, and by what type of
process, proto-Indo-Europeans spread has
not been convincingly ascertained. We are
particularly interested in establishing if the
demic diffusion of early farmers can, at least
in principle, explain a large share of current
genetic diversity among Indo-European
speakers, or if additional processes must be
included in the model to obtain a better fit
with real data. Among these additional pro-
 INDO-EUROPEAN ORIGINS
cesses, we gave a special emphasis to the
migratory waves postulated by Gimbutas.
In this study, we simulated microevolu-
tionary scenarios of increasing complexity,
from an unrealistically simple one to models
including several archaeologically docu-
mented migrations. We then calculated cor-
relation coefficients between the simulated
and real gene frequencies (or, more pre-
cisely, between matrices of genetic distances
calculated from each of them). We expected
to observe an increasing agreement between
real and simulated data as the models get
more and more realistic. When an increase
in the complexity of the model is not
matched by an increase in the correlations,
we conclude that the new factors included in
that model do not improve our understand-
ing of the phenomenon, and should there-
fore be considered unnecessary. This does
not automatically imply that these factors
played no evolutionary role at all. But, if
they did, evidence of their effects should be
sought in data other than the currently
available allele frequencies. A large data-
base of European allele frequencies (see
Sokal et al., 1989a) was analyzed for this
purpose.
METHODS AND DATA
Overview of the simulations
We carried out a series of computer simu-
lations of five microevolutionary models. All
models were based on a stepping-stone pop-
ulation structure, consisting of a 60 X 37
regular lattice, superimposed onto the map
of Europe. Each node of the lattice rep-
resents a l-degree square quadrat. Of the
2,220 nodes of the lattice, 1,512 are land
areas supporting a human population. Each
node (population) is characterized by its ef-
fective size (N,) and by the frequency of one
allele (p).At each generation p undergoes
random variation, representing the effects
of genetic drift, which is a function of N,.
Migration is allowed only between adjacent
populations. The numbers of individuals mi-
grating at each generation depend on popu-
lation sizes, and on factors of resistance to
migration, which are zero across plains, but
greater than zero across mountain chains
and seas. The differences among the five
111
models lie in parameters other than those
described so far.
Each simulation experiment consisted of
440 iterations (representing generations) of
a series of population processes. In this way,
assuming a 25-year generation interval and
non-overlapping generations, each experi-
ment spans 11,000 years. The simulated al-
lele frequencies were printed at generation
440, representing present time, for the local-
ities corresponding to those for which allele-
frequency data are available in a database of
European allele frequencies (Sokal et al.,
1989a), from which non-Indo-European
speakers had been discarded. Matrices of
Prevostis genetic distances (Prevosti et al.,
1975) were calculated on both real and sim-
ulated allele frequencies, and their degree of
resemblance was evaluated by Mantel
(1967) tests of matrix correlation.
Five FORTRAN programs were written,
each corresponding to one of five models for
the origins of Indo-Europeans described in
the following section, and incorporating sub-
routines developed by Press et al. (1986)and
Manly (1991).
An outline of the models
IBD: Isolation by distance
The first, clearly oversimplified, hypothe-
sis, is that Indo-European-speaking popula-
tions evolved under conditions of isolation
by distance (IBD model). Current patterns
of genetic variation would then simply re-
sult from the interaction between random
fluctuations of allele frequencies in time,
i.e., genetic drift, and dispersal of individu-
als. Under isolation by distance, variations
in population size affect only the impact of
genetic drift-the larger the population, the
smaller the allele-frequency fluctuations.
Population growth, which occurs after gen-
eration 40, does not prompt migratory move-
ments. Thus, the IBD model neglects all
gene flow processes other than those in
which movements of individuals from their
birthplaces are local and random (i.e.,
equally likely in all directions except for mi-
gration resistance factors, see below).
Under the IBD model, the demographic
increase that occurred in the Neolithic (and
is detailed in the section Population Growth
112 G. BARBUJANI ET A L

Among Farmers) was simulated without OAC: Isolation by distance, plus effects
separating hunting-gathering and farming of the origin of agriculture, and cultural
populations, i.e., as if all hunter-gatherers transmission
turned to agriculture a t 8,000BC.
Cultural transmission from farmers to
hunter-gatherers may be built into the
model, yielding what we call OAC; C stands
OAG: Isolation by distance plus effectsof for culture. Under this model, at all locali-
the origin of agriculture ties some hunter-gatherers learn how to
produce food, and therefore their alleles are
Isolation by distance is the null hypothe-
transmitted across generations with greater
sis for human microevolution (Wijsman and
efficiency. From the genetic standpoint, this
Cavalli-Sforza, 1984). Therefore, all models
is equivalent to a certain degree of admix-
that follow are not alternative to IBD.
ture, whereby some genes of the hunter-
Rather, they incorporate it as a necessary, if
not sufficient process, for determining the gatherers contribute to the gene pool of the
farmers. As a consequence, these genes
currently observed patterns of genetic varia-
spread at once with the genes of the farmers,
tion. OAG, the simplest such model, is one
and are thus carried into new localities. This
which combines IBD with the likely effects
is the Neolithic demic diffusion model, as
of the demographic processes following the
originally proposed (Menozzi et al., 1978;
origin of agriculture. Under this model, pop-
Renfrew, 1987).
ulations of hunter-gatherers initially occupy
Europe and evolve under isolation by dis-
tance. At a specific moment in time (8,000
BC, chosen on the basis of archaeological in-
ATC: Isolation by distance, plus effects
formation), a few populations in southern of the origin of agriculture, cultural
Anatolia turn to farming. This starts a local transmission, and archaeological
process of population growth in the areas time constraints
where farming is being practiced, followed
by dispersal outwards when local population Under OAC, the spread of farmers from
densities have reached a certain threshold. Anatolia into Europe is driven by their in-
In this way, migratory movements between crease in numbers at each locality, which
farming communities are not necessarily causes dispersal towards areas of lower pop-
symmetrical, as is reasonable to assume in ulation density. Therefore, in the OAC
many evolutionary scenarios (Rogers and model, the farming technologies spread a t
Jorde, 1987). The rate of spread of farmers is an approximately constant rate through
driven by their intrinsic growth rate; it is space (as in Ammerman and Cavalli-Sforza,
constrained only by geographical factors 1971). This is known to be an approximation
such as mountain chains or bodies of water. (Barker, 1985).A further refinement of OAC
No cultural transmission is simulated be- considers archaeological time constraints
tween the hunter-gatherers and the farmers (ATC). Under ATC, we use archaeological
who immigrate into their regions. Only the information about the likely date at which
farmers allele frequencies are eventually farming reached each specific site in Europe
compared with observed matrices of genetic (see Sokal et al., 1991). In this way, the
distances. In this way, the genetic conse- arrival of farmers into a new locality re-
quences of this model are those that would flects archaeologically documented cultural
be expected if hunter-gatherers were re- transformations; farmers spread at an irreg-
placed without admixture, i.e., became ex- ular rate, corresponding to the actual pro-
tinct. The only microevolutionary role they cess as inferred from archaeological evi-
play is to serve as a source population at the dence. Incorporation of hunter-gatherers
beginning of the Neolithic, for that small into each farming population occurs at the
fraction in Anatolia of the total population same rates and through the same processes
that develops the new farming technologies. as in OAC.
 INDO-EUROPEAN ORIGINS
GIM: Isolation by distance, plus effects of
the origin of agriculture, cultural
transmission, archaeological time
constraints, and late Neolithic
migmtions
In the OAG, OAC, and ATC models, the
first farmers are also considered the first
speakers of proto-Indo-European. The alter-
native hypothesis considers them as the Ne-
olithic inhabitants of areas that were later
invaded by the first proto-Indo-European
speakers, the Kurgan people (Gimbutas,
1979, 1986). The three migrational waves
postulated by Gimbutas are added to ATC in
the GIM model, by simulating long-distance
migratory movements between 4,250 BC and
2,900 BC. A number of successive population
movements are added as well; presumably,
they were independent from the spread of
Indo-European, but are considered by Gim-
butas (personal communication) relevant to
an accurate description of human evolution
in Europe.
Details on the simulation parameters
and algorithms
The data matrix
In all simulation cycles, a matrix of 60
columns by 37 rows was defined, each ele-
ment in the matrix representing a square of
edge length 1 degree in a Mercator projec-
tion of Europe. The data matrix covers the
area between 10 degrees of longitude West
and 50 degrees East, and between 72 and 35
degrees of latitude North. Iceland is not in-
cluded in this simulation.
Geography
Each of the 2,220 elements (= nodes or
pixels or localities) of the data matrix con-
tained an integer value, L, which was 1 for
plains, 2 for mountains, 3 for seas, and 4 for
the Black Sea. A local population was as-
signed to each of the 1,512 land pixels.
Initial allele frequencies
Under all the models tested, for each land
pixel a variable PHG was defined, represent-
113
ing the frequency of an allele at a polymor-
phic locus in the hunting-gathering popula-
tion, i.e., in the only type of population
existing at the beginning of the simulation.
From a mathematical standpoint, it does not
make a difference if this locus is regarded as
biallelic, or if it is considered multiallelic,
since the fate of only one of its alleles is
simulated in the followingphases. Allele fre-
quencies were drawn from a gamma distri-
bution truncated at one (Nei, 19871, whose
mean was fixed either a t 0.33 or at 0.50.
Initial population sizes
Estimates of population densities among
current hunting-gathering tribes suggested
to Rendine et al. (1986) that the effective
size NHG of the hunting-gathering popula-
tions of Europe should be approximately 300
in each of the 840 elementary areas of their
simulation. To have the same population
density in the 2,220 pixels of this simula-
tion, NHG was fixed at 114. This corresponds
to a population density of 0.04 individuals
per square km,within the estimated range
of population densities for hunter-gatherers
in temperate climates (Hassan, 1981). In
Rendine et al.s (1986) model, the individu-
als were considered as haploid, whereas
here they are diploid. This may have caused
a certain degree of divergence between the
two models, as the drift variances are af-
fected by the levels of ploidy of a population.
Genetic drift among hunter-gatherers
Non-overlapping generations were simu-
lated. At each generation, a new allele fre-
quency was drawn, for each locality, from a
normal distribution whose mean was the al-
lele frequencyp of the same population a t
the previous generation, and whose vari-
ance w a s p 0 - p), divided by twice the effec-
tive population size NHG (Nei, 1987). This
represented the effect of sampling of alleles
from one generation to the following, i.e.,
random genetic drift.
Dispersal of hunter-gatherers
Symmetrical dispersal occurred between
adjacent pixels, once every generation fol-
114 G. BARBUJANI ET AL.
TABLE 1. Factors of resistance to migration (RTW
And an adjacent Between a pixel in the-
pixel in t h e Plains Mountains Sea Black Sea
Plains 0.00
Mountains 0.25 0.50
Sea 0.45 0.70 0.90
Black Sea 1.00 1.00 1.00 1.00
lowing drift; population sizes of the two lo-
calities exchanging individuals did not
change as a result of dispersal. Therefore,
this study assumed a stepping-stone model
(Kimura and Weiss, 19641,whose properties
are discussed by Jorde (1980). We chose a
dispersal rate m of 0.065 (as in Rendine et
al., 1986), which means that at each genera-
tion, after reproduction, 6.5%of the resident
individuals could be replaced by immigrants
from the adjacent pixels. However, physical
obstacles in the pixels between which dis-
persal occurred could reduce the number of
migrants. Physical obstacles t o migration
were expressed by a factor of resistance to
migration, RTM, detailed in Table 1. The
average value of RTM, calculated between
all suitable pairs of pixels, was 0.300. This
means that, on the average, only 70% of the
potentially dispersing individuals actually
moved from their birthplace to an adjacent
locality. To compensate for this, the dis-
persal rate m was replaced by m' = 0.0651
0.700 = 0.0928. In other words, 9.28%of the
individuals in a locality were potentially
subject to migration elsewhere, and 6.5%ac-
tually migrated, on the average. The num-
ber N(AB) of individual hunter-gatherers
moving from locality A t o B (and vice versa,
from B to A) was
N(AB) = NHGm' (1 - RTM(AB)) (1)
4
~
where the denominator refers to the number
of adjacent populations in a stepping-stone
model, and RTM(AB) depends on the envi-
ronmental features a t localities A and B (Ta-
ble 1).WhenNHGwas fixed at 114, each pair
of adjacent localities exchanged 2 effective
individuals per generation. However, under
the IBD model the hunting-gathering popu-
lations increase in size, starting at genera-
tion 40; in this case, the number of migrants
per generation increased accordingly. When,
by contrast, hunter-gatherers decreased in
numbers owing to the expansion of farmers,
NAB) decreased as well until it reached
zero. Because of the RTM factor, two locali-
ties in the plains exchanged freely one-
fourth of the migrants allowed at each gen-
eration, whereas dispersal was reduced
between populations separated by moun-
tains or bodies of water, and for populations
a t the extremes of the simulated area. No
dispersal was allowed across the Black Sea,
to more carefully represent the population
processes in the surrounding area (e.g., the
migrations of Kurgan people), which oc-
curred mostly by land movements.
The allele frequency after migration,
pfHG, was then calculated as
-
P'HG = P N G [ ( ~- m') (1 - RTMI
+ rn'PHGin (2)
where RTM is the average resistance to mi-
gration between the pixel of interest and the
nA adjacent pixels (1 < nA < 41, and pHGin
is
Inception of farming in the nuclear zone
Under all models except IBD, the spread
of farming starts with the splitting of some
populations into two groups, one practicing
agriculture, and the other still living in a
hunting-gathering economy. At generation
40 (i.e., 10,000 years ago), 20 individuals
turn to farming at each of six pixels in Ana-
tolia, around the village of Catal Humk,
where the oldest archaeological evidence of
farming activities is situated (Redrew,
1991). Each group of 20 individuals repre-
sents a random sample of the pre-existing
hunting-gathering population at the same
site; therefore, initially they have the same
allele frequency: pF = PHG. However, from
generation 41 they evolve in reproductive
isolation, so that there will be two distinct
populations of hunter-gatherers and farm-
ers, HG and F, at those localities, with dis-
tinct allele frequencies. In the absence of
 INDO-EUROPEAN ORIGINS 115
cultural transmission between groups, i.e., pansion towards localities a t the same
under the OAG model, the two groups coex- latitude (i.e., with the same type of climate)
ist without any genetic exchange, at all lo- was presumably more common than dis-
calities where farming communities have persal northwards, towards more rigorous
been established. climates. This led us to subdivide the history
of our simulated farming populations into
Population growth among farmers four successive phases. Phase 1: Initially,
the population is scarce, and simply tends to
The farming populations have access to a increase logistically, without sending emi-
wider range of resources, and tend to in- grants, but receiving immigrants from other
crease in numbers (Hassan, 1973); 50-fold farming populations a t higher density, if
increases have been estimated by Ammer- any. Phase 2: When NF reaches a first
man and Cavalli-Sforza (1984). We simu- threshold, T1, a few individuals begin to dis-
lated a logistic increase, whose key parame- perse longitudinally; this often entails colo-
ter, the growth rate, generally referred to as nization of a new site on the west, whereas
r (Feller, 1940; Eisen, 1979; Keyfitz, 1977), gene flow is asymmetrical with the eastern
was here called a,following Rendine et al. neighbors, whose density is still higher.
(1986). In the absence of reliable informa- Phase 3: As the population size approaches
tion on growth rates among early farmers, the carrying capacity of 7,560, a second
we tried a preliminary set of values, and threshold, T2 is reached, and gene flow oc-
chose a = 0.5, which gave us a rate of popu- curs also northwards and southwards, once
lation increase compatible with the known again giving rise to a new population of
rates of spread of farming in Europe, 1 km farmers if the adjacent pixel to the north or
every year, on the average (Ammerman and south has not been colonized yet. The
Cavalli-Sforza, 1971). That value was em- thresholds had to be fixed in a somewhat
ployed in all the simulations presented here. arbitrary manner. It seemed realistic to al-
The equation calculating, at generation t low for the first westwards dispersal two to
and for each locality, the effective size NF of three generations after inception of the
the farming population is farming economy, so as to roughly match the
archaeologically documented rates of
1) x (1 + a (1 - spread. T1 was fixed at 24 (corresponding to
a census size of 72 individuals), whereas for
T2 we chose 50% of the carrying capacity,
where NF(t - 1)is the population size a t the i.e., 3,780. Phase 4: Finally, when adjacent
former generation, and 7,560 is the carrying populations have reached their equilibrium
capacity of the area, chosen for reasons anal- size of 7,560 effective individuals, the migra-
ogous to those that led us to choose tory exchanges become symmetrical. The
NHG= 114. Since the effective population general equation, expressing the number of
size is approximately one-third of the cen- farmers moving, say, from locality A to adja-
sus size (Wright, 19691, this corresponds cent locality B, N(AB),is
roughly to a farming population of 23,000
dwelling on a 1-degree-square quadrat of
land, and to 20,000 farmers in each elemen-
tary area of Rendine et al.s (1986) simula-
tion. for NF(A) greater than the appropriate
threshold, i.e., T1 for latitudinal and T2 for
Dispersal of farmers and origin of longitudinal movements, respectively. All
farming outside the nuclear zone relevant quantities have been defined for
Equation 1. Since N,(A) is variable across
Under the OAG and OAC models, the generations, N(AB) varies too.
growth of farming populations prompts mi- In this way, the input and output of genes,
gratory movements into neighboring locali- from and to the adjacent pixels of the map,
ties where farming has not yet started. Ex- could be different a t different times during
116
the simulations. If the number of immi-
grants from each locality is taken into ac-
count in the calculation of the allele fre-
quency of the immigrants, which we called
pHGinin Equation 2 and which will be called
pFinfor farmers, a n analogous formula gives
the allele frequency after gene flow among
farmers:
p'F = p F [ ( l - m ' ) (1 - RTM)I
+ rn'PFin (5) Pixels in the sea
Figure 1 is an example of allele frequencies
generated under the OAG and OAC models.
Allele frequencies of specific localities were,
of course, different in different realizations
of the same process, and between OAG and
OAC. What was constant, however, was the
pattern of occupation of land areas by ex-
panding farmers, because it depended only
on population growth and dispersal parame-
ters, which were kept constant across real-
izations.
For the ATC and GIM models, by contrast,
the spread of farming followed the pattern
that can be inferred from archaeological evi-
dence. Once a farming community exists at
a certain locality, the exchange of genes with
neighboring farming communities occurred
in the same manner as described for the
OAG and OAC models (Eq. 5). The differ-
ence is in the establishment of new farming
populations, which under ATC and GIM was
controlled by a matrix of dates of origin of
agriculture at each land pixel of the map
(details on how archaeological information
was processed for this purpose are in Sokal
et al. (1991)). Therefore, when colonization
of a new locality by the first farmers had
to be simulated, eight effective founding
individuals were sampled with replace-
ment from the closest suitable locality. In a
few cases, this required input of immigrants
from localities that were not directly adja-
cent to the one in which farming was start-
ing. This was the only violation that we
tolerated of the assumptions of the step-
ping-stone model. Figure 2 is an example
of allele frequencies generated under the
ATC and GIM models. It shows that the
spread of farmers is initially slower than
simulated under the OAG and OAC models,
especially along the northern shores of
the Mediterranean Sea. By genera-
G . BARBUJANI ET AL.
tion 200, however, the four models yield a
similar pattern of land occupation. The only
major exception is an area of north-western
Alps, where archaeological evidence shows a
delayed onset of farming activities (Sokal et
al., 1991). Of course, such a delay was not
predicted by the mechanism of farming
expansion underlying our OAG and OAC
models.
A stepping-stone model does not allow for
long-distance population movements, i.e.,
those associated with sailing, which are con-
sidered important in the colonization of Eu-
rope, and in the successive phases of agricul-
tural dispersal (Renfrew, 1987). To simulate
the effects of the movement of a few individ-
uals across the seas, we chose to assign a
pseudopopulation to each pixel located in
the sea. Pseudopopulations did not undergo
random fluctuation of allele frequencies,
and did not increase in numbers. They in-
cluded only the individuals dispersing from
neighboring pixels (their number was deter-
mined according to Equation 1)) whose de-
scendants had the same allele frequencies,
and a t each generation proceeded one step
forward in the dispersal process. In this
way, the movement of a few individuals
across the sea was simulated. This had little
importance for the allele frequencies of
Fig. 1. Spread of farmers under the OAG and OAC
models. The localities where farming is being practiced
are indicated by letters representingallele frequency in
farmers, at generations 100 (6500 BC), 200 (4000 BC), and
240 (3000 BC). Eight allele-frequencyclasses are defined,
from a to h, each corresponding to an interval equal to
0.125 (a, p F < 0.125; b, 0.125 <p,0.250; c, 0.250
< p F < 0.375; etc.). Hyphens represent areas inhabited
only by hunter-gatherers.The nuclear zone is delimited
by a solid square. While the pattern of land occupation
shown was constant for all the realizations of the mod-
els, the allele frequencies depicted are those of a single
run of OAC.
Fig. 2. Spread of farmers under the ATC and GIM
models. The localities where farming is being practiced,
based on archaeological information, are indicated by
figures representing allele frequency of farmers, at gen-
erations 100 (6500 BC), 200 (4000 BC), and 240 (3000 BC).
Allele-frequencyclasses are as in Figure 1. The pattern
ofland occupationwas again the same in all realizations
of ATC and GIM, but the allele frequency shown is that
of a single realization ofATC.
 1
t
118 G. BARBUJANI ET AL.

hunter-gatherers and for those of farmers
once the spread of farming through Europe
was completed; however, it had an effect on
the establishment of farming communities
under the OAG and OAC models, as a few
individuals could quickly reach distant lo-
calities by sea. The resulting pattern of occu-
pation of coastal regions corresponds well
with the archaeological evidence (see Figs. 1
and 2).
Cultural contacts and admixture
Rendine et al. (1986), the value of y was
adjusted so that resultant values of S had
approximately the same magnitude as in
Equation 6. However, we found, over a
range of test conditions, that the results
were only trivially affected. Therefore, we
report results for Expression 6 without redo-
ing the analysis for every test condition.
Disappearance of hunting-gathering
populations

Under the OAC, ATC, and GIM models, at In the IBD model, hunter-gatherers adopt
each generation a certain number of hunter- farming at generation 40, and thus all genes
gatherers adopted farming, if a farming of Indo-European speakers come from the
community already existed a t the locality genetic pool of the hunting-gathering com-
where they lived. The likelihood of this cul- munities. In the OAG model, conversely, the
tural shift depended on the probability of hunter-gatherers go extinct, and thus all
contacts between farmers and hunter-gath- genes of Indo-European speakers derive
erers, and on a coefficient of acculturation from the genes of the few first farmers of
which was called y by Rendine et al. (1986). Southern Anatolia. These are the two ex-
The number S of individuals shifting to treme models, as far as the origins of Indo-
farming at each generation is related to the Europeans are concerned. Under the other
probability of contacts between farmers and models, a certain degree of admixture is sim-
hunter-gatherers. If farmers are NF at a ulated between the two communities at each
given locality and a t a given moment in locality, reflecting a widespread view of hu-
time, their probability of meeting one of the man evolution in Europe (Cavalli-Sforza
NHG hunter-gatherers will represent a frac- and Piazza, 1993).
tion equal to 2(NF x NHG) of all the Under the OAC, ATC, and GIM models,
(NF+ NHG)' possible contacts. The proba- the hunters and gatherers are considered to
bility y that such a contact will result in disappear from a certain locality when their
acculturation has been estimated at 0.00024 number is such that S is less than 1. Be-
(Rendine et al., 1986). Therefore, at each cause acculturation starts after a phase of
generation, the NF farmers will transmit population buildup for farmers, the extinc-
their technologies t o a number S of the tion of the hunting-gathering communities
hunter-gatherers estimated as also proceeds as a wave, from southeast to
northwest, spreading in parallel with the
farming economy, but several generations
later.
Long-range migratory movements
where all parameters have already been de- In the GIM model, three major migratory
fined. waves of Kurgan people are supposed to
It can be argued that the change in a par-
have introduced Indo-European languages
ticular quadrat of the number of hunter- into Europe, around 4,250 BC, 3,400 BC, and
gatherers per generation might better be 2,900 BC, respectively (Gimbutas, 1979,
modelled as proportional to the product of 1986).
the number of hunter-gatherers and the In Gimbutas' (1979) view, the westward
number of farmers, that is migrations of Kurgan people in Europe in-
S = YNHGNF (7) troduced a new patriarchal culture, charac-
terized by horse-riding and new warfare
where y = 1.56250 x In this expres- techniques. These cultural changes were not
sion, closely resembling a formula used by associated with major innovations of the
 INDO-EUROPEAN ORIGINS 119
subsistence techniques. Most of the popula- parameters being constant. Gene flow is re-
tions of Europe by then were farmers. It is duced at generation 265, i.e., 3,375 years
therefore highly unlikely that concomitant ago, by which time all suitable regions had
population growth could occur. We chose to been colonized by early agriculturalists. The
represent these waves as a flow of genes parameters of the simulation are summa-
from the purported source area, north of the rized in Table 2.
Black Sea and west of the Caspian Sea. For
the sake of simplicity, these movements
were concentrated in one generations time Gene-frequency data
(at generations 190,224, and 244), although The simulated sets of allele frequencies
each of them probably lasted two centuries were compared with a database of allele fre-
(Gimbutas, 1979). For each movement, we quencies, which had been analyzed in vari-
simulated replacement of 20% of the genes ous studies on Europe (Sokal et al., 1988,
in the target area, with genes coming from 1989a,b, 1990, 1991, 1992; Harding and
the source area. Probably this overempha- Sokal, 1988; Barbujani and Sokal, 1990;
sizes the genetic consequences of the simu- Sokal, 19911, and had been continuously up-
lated migratory movements. dated. The data corresponding to popula-
The invading Kurgan people were not the tions speaking languages other than Indo-
entire population of the area between the European (Basque, Finnish, Estonian, Lapp,
Black and Caspian sea moving en masse; Hungarian, Turkish: Ruhlen, 1987)were dis-
rather, they were groups of individuals be- carded.
longing to semi-nomadic tribes (Gimbutas, Twenty-six genetic systems were consid-
1979). Accordingly, we chose to simulate ered. Most of them corresponded to indepen-
their contribution to the genetic pool of thedent loci; exceptions are ABO, MN, and Rh,
invaded populations as if they were com- for which two (or three, for Rh) systems were
ing from several populations in the appro- independently considered, each resulting
priate zone. The location of four such popu- from typing of alleles by different sets of an-
lations was chosen a t random, and then held tisera. This convention has long been fol-
lowed in studies on human variation (e.g.,
constant in all 2,600 simulation cycles of the
GIM model. The allele frequencies of the re-see Lewontin, 1972). Each system is indi-
cipient populations (Fig. 3) were then recal-
cated by a letter code, preceded by a number
culated as if 20% of the pre-existing indi- referring to Mourants coding system (Mou-
viduals had been replaced by immigrant Kur- rant et al., 1976), except for 100HLA-A,
gan people. 101/2HLA-B, 200GM, and 201Kh4, whose
In addition, Gimbutas (personal commu- numerical codes were assigned in our lab-
nication) pointed out to us 12 other direc- oratory. Overall, 3,481 records, and 93 alle-
tional and potentially migratory processes les or haplotypes were considered.
that may have been important in determin- The number of samples available for the
ing the current linguistic population struc-26 systems varied widely, ranging from a
ture of Europe. These processes are summa- minimum of 27 (for 5-1 LUTHERAN), to a
rized in Figure 4, and were incorporated in maximum of 762 (for 1-1ABO).Genetic dif-
the GIM model. Once again, for each of them ferences between localities were summa-
we simulated replacement of 20% of the in- rized by 26 matrices of Prevostis distances
dividuals of the target area by individuals
(Prevosti et al., 19751, separately calculated
whose allele frequency was the average al- for each system. We shall refer to these ma-
lele frequency in the sourcearea. trices as observed distance matrices, as op-
posed to the simulated ones, generated by
Decrease of population mobility after the computer under one of the five models
establishment of a farming economy tested. To properly compare the two sets of
Once farming populations have reached data, prior to calculating genetic distances
the maximum size allowed by the programs, we pooled the observed frequencies of all al-
a reduction of mobility is simulated by sim- leles except the one whose average fre-
ply halving the migration rate m, all other quency was closest to 0.5.
120 G. BARBUJANI ET AL.
Fig. 3. Migratory movements simulated under the
GIM model. The four localities whose allele frequencies
are averaged, to represent the allele frequencies of the
migrating population, are marked by asterisks. The re-
gions affected by the three migratory waves proposed by
Hypothesis testing
For every one of the 26 genetic systems,
each of the five simulation programs was
run 100 times, yielding 13,000 simulation
cycles (or realizations) in all, 2,600 for each
model. Every realization resulted from de-
terministic movements of individuals across
the map of Europe, and random allele-fre-
quency fluctuations occurring during ini-
tialization and from genetic drift each gen-
eration. The latter were dictated by a
random number generator, and gave rise to
the various replicates at generation 440. A
particular realization of the OAG process
Gimbutas are surrounded by solid lines; the zone where
Basque is currently spoken is not supposed to have been
affected by these migratory episodes. Figures refer to
the generation at which each migratory wave was simu-
lated.
adds OAG movements to those already re-
quired by the IBD model, but random allele-
frequency fluctuations are the same. This is
also true for the other models, each incorpo-
rating the previous ones. For all models,
then, random change in allele frequencies
was the same, for each pixel and each gener-
ation, under all five models. It was not the
same, however, for the hunting-gathering
and for the farming populations of the same
pixel. Thus, the 500 cycles of simulation for
each locus fall naturally into 100 groups,
each with five matched runs, in ascending
model order. Because of the matching, we
 INDO-EUROPEAN ORIGINS 121

Fig. 4. Twelve potentially important migratory processes considered by Gimbutas (personal commu-
nication) to have been relevant in European ethnohistory, each one represented by an arrow from a
sourceregion to a targetregion. Figures refer to the generation at which each population movement
was simulated.

could use paired statistical tests to compare
models. This provided a considerable in-
crease in statistical power over unpaired
comparisons.
After 440 generations in each computer
cycle, simulated allele frequencies were
sampled from localities chosen so as to
match the locations of the samples of the
observed allele-frequency database. Matri-
ces of Prevostis distances were computed
from the simulated data, so as to obtain 100
simulated matrices for each matrix of ob-
served genetic distances (Prevosti et al.,
1975). This measure of genetic distance was
chosen for consistency with previous studies
(Sokal, 1988; Sokal et al., 1993).
Simulated and observed matrices were
then compared pairwise by means of Man-
tels test of matrix association (Mantel,
1967; Smouse et al., 1986). This test com-
putes the equivalent of a correlation coeffi-
cient between matrices, and evaluates its
significance by constructing a null distribu-
tion of the test statistic. A Monte Carlo pro-
cedure is employed for this purpose; rows
and columns of one matrix are repeatedly
permuted at random, while the other matrix
is kept constant, and the test statistic is re-
122 G. BARBUJANI ET AL.

TABLE 2. Parameters defined in the simulation

L Environment: 1 = plains; 2 = mountains; 3 = seas; 4 = Black Sea
NHG Effective population size of hunter-gatherers (114in all models but IBD, where it is allowed to
increase up to 7560. In the OAC, ATC, and GIM models it is then reduced as an effect of the
cultural transmission of farming technologies)
NF Effective population size of farmers (Initially equal to 0, then allowed to increase up to 7560 in all
models but IBD)
PHG Frequency of one allele among hunter-gatherers (initially sampled from a gamma distribution)
PF Frequency of one allele among farmers for all models except IBD (Initially undefined. For the six
pixels of the nuclear zone, pF = pHG a t generation 40. In the other pixels, the initial p F value
reflects the proportion of immigrating farmers and of hunter-gatherers who were incorporated into
the farming population, under the different models)
a Intrinsic growth rate of the farming populations
Y Acculturation rate, i.e., rate of assimilation of hunter-gatherers by farmers
m Migration rate
RTMAB)
Resistance to migration between localities A and B (see Table 1)
RTM Average resistance to migration between one pixel and its adjoining pixels

calculated each time, so a s to yield the de-
sired null distribution.
Because each observed matrix was com-
pared with 100 simulated matrices for each
model tested, a procedure was needed to
combine all this information. We chose to
compute average Mantel correlation coeffi-
cients, and to calculate Fishers combined
probabilities (Sokal and Rohlf, 1995) from
the 100 individual probabilities for each
model.
Since we are looking for positive associa-
tion of observed and simulated data, and a
negative correlation would have no biologi-
cal meaning, all tests of significance were
one-tailed. However, a s a further control, we
also counted the number of occurrences of
negative correlations that would be signifi-
cant if the test had been two-tailed. This
allowed us to identify the models generating
allele-frequency distributions departing
widely from the observed distributions.
The main purpose of this study was to
compare competing hypotheses on the origin
of Indo-Europeans. Because the hypotheses
can be ranked, by increasing complexity,
from IBD through OAG, OAC, ATC, and
GIM, four painvise tests of goodness of fit
were carried out, OAG versus IBD, OAC ver-
sus OAG, ATC versus OAC, and GIM versus
ATC. This was done taking advantage of the
paired design based on the same random
seeds in the simulations. We employed two
different procedures: 1) a paired-compari-
sons t-test, where the test statistic was the
difference between the average Mantel cor-
relation coefficients, and only positive dif-
ferences (indicating a n improvement of the
fit for the more complex hypothesis) were
considered significant; 2) Wilcoxons signed
rank test (Sokal and Rohlf, 19951, a nonpa-
rametric paired-comparisons test, once
again considering significant only the cases
in which the fit improved for the more com-
plex hypothesis.
RESULTS
The average Mantel correlations for each
genetic system (Table 3) yield numerous sig-
nificant agreements between observed and
simulated matrices of genetic distances, for
all models, although fewest with IBD. The
number of significant ( P < 0.05) positive av-
erage correlations is maximal for the ATC
model (20/26), but it is not substantially
lower for OAG, OAC, and GIM (respectively,
18, 17, and 16 systems). For IBD it is only
10/26. The numerical values of the correla-
tions are low despite their high level of sta-
tistical significance. This is characteristic
for genetic distances and is because the
Mantel correlations were constrained to be
linear.
Next we examine the number of cases in
which individual simulation realizations
gave genetic distance matrices that would
appear negatively associated (P s 0.05)
with the observed one, if the test had been
two-tailed. A substantial number of dis-
agreements, between observed and simu-
lated data is evident for IBD (6 at system
4-13 RHESUS), for ATC (8 in the 1-1 ABO
 INDO-EUROPEAN ORIGINS 123
TABLE 3. A) Average Mantel correlations of observed with simulated genetic distances and B) significance levels based
on ont-tailed probabilities for positive correlation combined by Fisher's method'
System IBD OAG OAC ~
An: GIM
A. Mantel correlations
1-1-mo 0.01294 0.14800 0.15233 0.13137 0.01887
1-2x30 0.05699 0.10831 0.09718 0.00411 0.03532
2-5-MN 0.00324 -0.05627 -0.05352 -0.04100 -0.03231
2-7-MN -0.02886 -0.02236 -0.02091 -0.03127 -0.03912
3-1-P -0.03558 -0.04556 -0.03411 0.02409 0.01112
4-1RHESU 0.01311 -0.01457 -0.01428 0.00674 0.03130
4-13RHES -0.02547 0.06920 0.06120 0.03431 0.02375
4-19RHES -0.04258 -0.03158 -0.02899 -0.01635 -0.08314
5-1LUTH -0.00590 -0.05392 -0.04768 0.00777 0.02033
6-1-KELL 0.01789 0.07960 0.08378 0.03392 0.03330
6-3-KELL -0.04254 0.06145 0.01510 -0.01550 -0.06665
7-1ABHSE 0.01781 0.01064 0.02805 0.05623 0.05420
8-1DUFFY 0.00290 0.04017 0.05362 0.01197 -0.01077
36-1-HP 0,11991 0.15415 0.17941 0.07459 0.08002
37-1-TF 0.00592 0.08658 0.09142 0.08117 0.00461
38-1-GC -0.01547 -0.05739 -0.05843 -0.01637 0.05178
50-1-1AP -0.00965 0.12963 0.11903 0.10520 0.06548
52-PGD 0.04775 -0.03417 -0.03457 -0.04371 0.01603
53-PGM1 -0.00845 0.13174 0.14000 0.10789 0.06152
56-AK -0.00696 0.06676 0.10858 0.05081 -0.01301
63-ADA 0.00667 0.27423 0.26493 0.07537 0.03099
65-TASTE 0.02802 0.17960 0.16922 0.07373 0.04040
100HLA-A 0.01417 0.13654 0.15443 .0.08977 0.01311
101-102 -0.00854 0.24013 0.22784 0.12228 0.09136
200-GM 0.01455 0.34928 0.33330 0.14102 0.03480
201-KM -0.02816 0.07813 0.09279 0.05959 -0.03732
B. Significance levels
1-1-ABO 0.00000 0.00000 0.00000 0.00000 0.00000
1-2-ABO 0.00000 0.00000 0.00000 0.00489 0.00000
2-5-MN 0.00339 1.00000 1.00000 1.00000 1.00000
2-7-MN 1.00000 1.ooooo 1.00000 1.00000 1.00000
3-14' 1.00000 1.Ooooo 1.00000 0.o0000 0.00003
4-1RHESU 0.00000 1.00000 1.00000 0.00198 0.00000
4-13RHES 0.99975 0.00000 0.00000 0.00000 0.00000
4-19RHES 0.99996 0.99980 0.99913 0.00001 1.00000
5-1-LUTH 0.52240 1.00000 1.00000 0.22014 0.04162
6-1-KELL 0.47350 0.0oooo o.ooooo 0.00001 0.00385
6-3-KELL 1.00000 0.00000 0.09492 0.94677 1.00000
7-1ABHSE 0.00942 0.03488 0.00002 0.00000 0.00000
8-1DWFY 0.94188 0.00000 0.00000 0.01885 0.99931
36-1-HP 0.00000 0.00000 0.00000 0.00000 0.00000
37-1-TF 0.82795 0.00000 0.00000 0.00000 0.79836
38-1-GC 0.98856 1.00000 1.00000 0.51374 0.00000
50-1-1AP 0.94062 0.00000 0.00000 0.00000 0.00000
52-PGD 0.00554 1.00000 1.00000 0.99974 0.68047
53-PGM1 0.99819 0.00000 0.00000 0.00000 0.00000
56-AK 0.97077 0.00000 0.00000 0.00000 0.99442
63-ADA 0.05673 0.00000 0.00000 0.00000 0.00132
65-TASTE 0.00000 0.00000 0.00000 0.00000 0.00000
100HLA-A 0.00107 0.00000 0.00000 0.00000 0.06326
101-102 0.97945 0.0oooo o.ooooo 0.0oooo 0.00000
200-GM 0.04825 0.00000 0.00000 0.00000 0.00115
201-KM 0.99886 0.00000 0.00000 0.00000 0.99918
Overall probability 0.00000 0.00000 0.00000 0.00000 0.00000
'Values below 0.05 show significant positive correlation between simulated and observed genetic distances

and 11 in the 2-5 MN systems), and for GIM
(26 in the 1-1 ABO, and 8 in the 4-19
RHESUS systems).
The painvise comparisons by t-tests and
by Wilcoxon's signed ranks test agree in
their means and significances that the most
significant increase in the resemblance of
observed and simulated genetic distances
occurs between IBD and OAG. In the t-tests
shown in Table 4 , 1 7 systems show a signifi-
cant increase of correlation,whereas in only
7 cases does the similarity decrease. These
124 G. BARBUJANI ET AL

TABLE 4. Results of paired comparisons t-tests for differences between 5 Indo-European simulation hypotheses:
P ( H I ) - P (H2)
~ ~

System OAG - IBD OAC - OAG ATC - OAC GIM - ATC

1-1-ABO 0.13506*** 0.00432 -0.02095 -0.11250

1-2-ABO 0.05133*** -0.01113 - 0.09307 0.03121***
2-5-MN -0.05951 0.00275*** 0.01252** 0.00869*
2-7-MN 0.00650 0.00145 -0.01037 -0.00785
3-1-P -0.00998 0.01145*** 0.05819*** -0.01296
4-1RHESU -0.02767 0.00029 0.02102*** 0.02456***
4-13RHES 0.09467*** -0.00800 -0.02689 -0.01056
4-19RHES 0,01099 0.00259 0.01265 -0.06679
5-1-LUTH -0.04802 0.00624 0.05545*** 0.01256
6-1-KELL 0.06171*** 0.00419 -0.04987 -0.00061
6-3-KELL 0.10399*** -0.04634 - 0.03060 -0.05115
7-1ABHSE -0.00717 0.01741*** 0.02818* -0.00203
8-1DUFFY 0.03727*** 0.01345*** -0.04164 -0.02275
36-1-HP 0.03425** 0.02525** - 0.10482 0.00543
37-1-TF 0.08065*** 0.00484 -0.01026 -0.07655
38-1-GC -0.04192 -0.00104 0.04206*** 0.06816***
50-1-1AP 0.13928*** -0.01061 -0.01383 -0.03972
52-PGD -0.08192 -0.00040 -0.00914 0.05974***
53-PGM1 0.14019*** 0.00826 -0.03212 -0.04637
56-AK 0.07372*** 0.04182*** -0.05777 -0.06382
63-ADA 0.26756*** -0.00930 -0.18956 -0.04438
65-TASTE 0.15158*** -0.01038 -0.09549 -0,03333
100HLA-A 0.12237*** 0.01789*** -0.06466 -0.07666
101-102 0.24867*** -0.01229 -0.10556 -0.03092
200-GM 0.33473*** -0.01597 -0.19229 -0.10622
201-KM 0.10630*** 0.01466 -0.03320 -0.09691
Mean difference 0.07402 0.00198 -0.03662 -0.02660
Asterisks indicate significant positive differences as follows: *0.05 3 P 2 0.01,**0.01P P > 0.001,***0.001 P.

figures compare with 7 systems showing sig- although ATC shows a significant positive
nificantly improved correspondence and 10 correlation for the largest number of sys-
showing decreased correspondence for OAC tems, on the average, correlations between
versus OAG, 6 and 19, and 5 and 19, respec- observed and simulated genetic distance are
tively, for ATC versus OAC, and GIM versus higher for OAC and OAG.
ATC. These results are reflected in the To test the plausibility of our simulations
mean differences shown at the bottom of Ta- we also calculated FsTvalues (Wright,
ble 4. 1978) for both our observed gene-frequency
Using Wilcoxons criterion, the results do surfaces and the simulated surfaces. The
not change much, so we do not feature them median results over all genetic systems are
as a separate table. The numbers of systems 0.011780 for the observed surfaces, and
showing significance increased and any de- 0.098273, 0.10399, 0.096562, 0.056609, and
creased resemblance between observed and 0.003211, respectively, for the simulated
simulated data are, respectively, 17 and 7 surfaces of models IBD, OAG, OAC, ATC,
for OAG versus IBD; 10 and 9 for OAC ver- and GIM. Although the FsTvalues of the
sus OAG; 5 and 19 for ATC versus OAC; and observed surfaces overlapped only slightly
5 and 18 for GIM versus ATC. those of the simulated surfaces, the median
We conclude, as a result of all the tests, of the observed data falls within the bound-
that similarity between observed and simu- aries of the medians described by the mod-
lated genetic distances increases from IBD els. The latter fall into 3 groups by magni-
to OAG, and, to a lesser extent, from OAG to tude of FsT.These are 1)IBD, OAG, OAC; 2)
OAC. On the contrary, it decreases as mod- ATC; and 3) GIM. Thus, the clear superior-
els are tested in which the spread of farmers ity of OAG and OAC over IBD cannot be
is constrained by archaeological time data shown by FST since various patterns of local-
(ATC), or demographic processes occurring ity differentiation can yield the same F,,
in the late Neolithic are added (GIM). Thus value.
 INDO-EUROPEAN ORIGINS
DISCUSSION
Which model matches observed
data best?
The IBD model assumes that, in the Neo-
lithic, groups of hunter-gatherers and farm-
ers were not separated. The former gradu-
ally turned to farming, so that there was a
genetic continuity between pre- and post-
Neolithic populations in Europe, and Indo-
European languages spread only by cultural
transmission. Allele frequency patterns gen-
erated under this model resemble poorly the
patterns of genetic variation observed in
contemporary populations, showing that
this evolutionary hypothesis does not fit
with the available genetic evidence.
Resemblance between observed and simu-
lated patterns is much greater for the other
four models, in which farmers evolve sepa-
rately from hunter-gatherers, and processes
of population expansion are important. The
levels of resemblance, however, do not differ
much among these four models. For in-
stance, the GIM model, including several
population processes occurring in the last
5,000 years, does not give higher correla-
tions, or significant correlations at a higher
number of loci, than the OAG model, where
the demographic changes prompted by the
origin of agriculture are simulated in a
much rougher manner.
Actually, various results of this simula-
tion study indicate that the fit of simple
models, such OAG and OAC, is better than
that of more complex models. The Mantel
correlations between observed and simu-
lated genetic distances would be negative
and significant in only 21 of the 2,600 cases
for OAG, and in 14 cases for OAG, had tests
been two-tailed. These figures compare with
89 and 105 negative significant correlations
for ATC and GIM, respectively. It seems,
therefore, that nothing is added to our un-
derstanding of the phenomena, if we add ar-
chaeological time data to constrain the
spread of Neolithic farmers, and even less so
if we simulate population movements in the
late Neolithic. The models where farmers
disperse into new areas simply because of
their numbers, which increase logistically,
yield patterns showing a better agreement
with the observed data.
125
Similarly, the pairwise comparison of
models show a substantial increase of fit of
the OAG over the IBD model (Table 41,
whereas the elements included in the ATC
and GIM simulations cause a slight but evi-
dent departure from the patterns observed,
making them poorer fits than OAG.
A first conclusion one may draw from the
results of this simulation study is that two
models account best for many aspects of the
contemporary genetic structure of Indo-
European-speaking populations of Europe.
One is the demic diffusion model, as origi-
nally put forward by Menozzi et al. (1978),
and associated with linguistic evidence by
Renfrew (1987). Under this model, here
called OAC, the two forces driving microevo-
lution in Europe were population growth de-
termined by farming, and dispersal accom-
panied by limited population admixture
between early agriculturalists (possibly pro-
to-Indo-European speakers) and preexisting
hunters and gatherers. The other model,
OAG, is a simplified version of the demic
diffusion model, in which dispersal of farm-
ers does not lead to any degree of admixture
with hunter-gatherers.
How plausible is the OAG model?
While the OAC model has already re-
ceived support from studies focussing on its
genetic (Sokal et al., 1991; Cavalli-Sforza et
al., 19931, as well as linguistic and archaeo-
logical, aspects (reviewed in Renfrew, 1992),
what we called OAG here has not been ana-
lyzed in detail so far. An apparent problem
with it is, how can a model not involving
admixture account for the continent-wide
clines observed in Europe?
Inspection of gene-frequency maps gener-
ated in this study, at various moments in
time, shows that founder effects are common
while farmers disperse. Founder effects are
due to the limited numbers of individuals
who start the farming communities in new
localities. In the OAG model as we simu-
lated it, most farming communities start
with 8 effective individuals; but even if this
number were larger, the probability for the
allele in question to be lost or fixed would be
substantial. Loss of genetic variation
through repeated founder effects has been
invoked as the likely cause of clines in sev-
126 G. BARBUJANI ET AL.
era1 studies on natural populations of toads
in Australia (Easteal, 1988) and aquatic in-
vertebrates in Canada (Boileau et al., 1992).
Theoretical work on the genetic effects of
colonization of previously unoccupied locali-
ties (Wade and McCauley, 1988) agrees with
this view.
An additional factor, increasing the likeli-
hood of clines even in the absence of admix-
ture between farmers and hunter-gatherers,
is the Black Sea. Archaeological evidence
(e.g., see Renfrew, 1991) indicates that two
waves of early farmers dispersed westwards
and northwards from the Near East, with
the Black Sea separating them (this is why
we did not allow movement of individuals
through it, but only along its coasts). The
two waves later converged in eastern Eu-
rope, after a period of independent evolu-
tion. If the same allele had been lost, or
fixed, in both groups of farmers, no particu-
lar pattern would result; but if founder ef-
fects had had opposite consequences in the
two groups, the successive admixture would
initially determine a steep cline, and succes-
sive gene flow would smooth it, resulting in
a wide gradient (Endler, 1977).
Even under OAG, therefore, a certain role
of admixture is important. But admixture,
under OAG, is between different groups of
farmers, who were geographically separated
in part of their evolutionary history, rather
than between farmers and hunter-gatherers
of the same area. This interpretation em-
phasizes the role both of geographical fac-
tors, such as distance between regions, and
of cultural barriers between sympatric com-
munities of farmers and hunters-gatherers.
Indeed, physical barriers are often associ-
ated with genetic and linguistic change,
even between Indo-European speakers (Bar-
bujani and Sokal, 1990, 1991), although
other evolutionary mechanisms may also ac-
count for that association (Barbujani, 1991).
Genetics and Kurgan waves
Introducing the three migratory waves
postulated by Gimbutas (GIM model) into
the simulation, not only does not increase
the correlations, but somewhat reduces
them. This means that the current patterns
of allele frequencies among Indo-Europeans
can be explained without resorting to the
migrations of Kurgan people. This study
cannot establish whether or not these mi-
gration events really occurred, but, if they
occurred, they did not leave a significant
mark on the allele frequencies of current
populations.
Renfrew (1987) argued that the cultural
transformations that led Gimbutas to hy-
pothesize late-Neolithic migration waves
could be due to cultural contacts instead,
and equated the first Indo-Europeans with
the first farmers. The extensive changes in
ceramics, architecture, and metallurgy oc-
curring in the late Neolithic are then attrib-
uted to trading and imitation; long-distance
migratory movements, if any, may have
been marginal. Although not proved by our
simulation, this view is fully compatible
with it.
This study, therefore, agrees with the
main views expressed by Menozzi et al.
(19781, Rendine et al. (19861, Piazza (19931,
and Cavalli-Sforza et al. (1993). By contrast,
the emphasis laid by the same authors on
late Neolithic migrations from the Pontic
steppes (Cavalli-Sforza et al., 1993) does not
find support in our simulations. Among the
possible causes of this discrepancy, it may be
that Mantel's correlations are not sensitive
enough to recognize the effects of minor pro-
cesses of gene flow, such as those presum-
ably occurring in the late Neolithic. Alterna-
tively, however, or in addition, one should
consider the possibility that principal com-
ponents associated with low eigenvalues re-
flect, at least in part, artificial gradients due
to data interpolation. This may be the case
for areas where population samples are
sparse, such as most of eastern Europe. For
example, the Caucasus seems to show clinal
variation in the first and third principal
components of Cavalli-Sforza et al. (1993),
but a detailed genetic study shows that
clines are very uncommon there (Barbujani
et al., 1994).
Our evaluation of the Gimbutas model
should be revised if evidence could be pro-
vided that the spread of the Kurgan people
was accompanied by an increase in popula-
tion sizes larger than that simulated by us.
A certain level of ambiguity exists about
this, as the movement of people from the
Pontic steppes that Gimbutas (1979) hy-
 INDO-EUROPEAN ORIGINS
pothesized is called a population expan-
sion by Cavalli-Sforza et al. (1993). These
authors seem to suggest that, because of the
warfare technologies associated with it,
larger populations could be supported in the
regions affected. This aspect remains to be
explored, and we do not have evidence for or
against this view. However, even if this had
been the case, the increases in population
sizes prompted by the beginning of food pro-
duction seem to have been much larger than
those associated with new war technologies
(see Ammerman and Cavalli-Sforza, 1984).
Unless European populations increased dra-
matically in size between 6,000 and 5,000
years ago, as they did with the arrival of the
new farming technologies, we conclude that
the long-distance migrations postulated by
Gimbutas remain an unnecessary element
in the evolution of Indo-European-speaking
populations, as reconstructed from the com-
parison of theoretical models and gene-fre-
quency data.
Besides, early farmers expanded into ar-
eas of low population density, where few im-
migrants could substantially modify the ge-
netic build up of local populations; but this
was not the case for late Neolithic groups,
who invaded regions already occupied by
large farming communities. Simulations of
genetic processes based on the coalescent
approach (see Hudson, 1990) show that pat-
terns of genetic variation do not tend to
change much after a demographic expansion
(Harpending, 1994; Rogers and Jorde,
1995). Successive population movements
can smooth out the gradients and blur some
patterns, but are unlikely to leave a signifi-
cant mark on allele frequencies.
Are parasites responsible for clines?
Recent evolutionary models (reviewed in
Ladle, 1992) indicate that new genotypes
entering an area could be resistant to the
parasites that are already adapted to the
common resident genotypes. The new geno-
types would then increase in frequency, un-
til the parasites adapt to them. A selective
mechanism of this type, combined with gene
flow, might have been important in deter-
mining the European clines of allele fre-
quencies; models may be envisaged whereby
a form of frequency-dependent selection,
127
rather than limited admixture or founder
effects, leads to clinal variation of gene fre-
quencies (e.g., see Hedrick, 1986). It is in-
triguing to note that the hypothesis of demic
diffusion from the Near East was initially
developed to account for clines a t the histo-
compatibility loci, HLA-A and HLA-B
(Menozzi et al., 1978; Sokal and Menozzi,
19821, and that the most significant evi-
dence for clines spanning Eurasia has been
found at the glyoxalase locus (Barbujani,
19871, which is linked with HLA on chromo-
some 6, in a region of extensive linkage dise-
quilibrium (Hedrick et al., 1986).
However, this view, although compatible
with the gradients existing a t the HLA and
linked loci, can hardly account for the pat-
terns of variation observed among Indo-Eu-
ropean speakers at other, independently in-
herited, loci. Had the resistance to parasites
been the main cause of clines in Europe, one
would expect isolation by distance patterns
at most loci not involved in tissue recogni-
tion, which is not the case (Sokal et al.,
1989a; and this study). On the contrary, the
nearly parallel gradients observed for many
independent alleles suggest that an evolu-
tionary pressure affecting the entire genome
and not merely part of it, i.e., gene flow,
played a major evolutionary role (Slatkin,
1985,1987).
Relation to other work
Diakonov (1984; cited in Redrew, 1987)
listed what he called the essential questions
concerning the origins of Indo-European
speakers: Who migrated? Why? How many
of them were there? Was it actually a migra-
tion of people, or rather the transfer of a
language from one population to another?
The present study may contribute to an-
swering some of these questions. Our results
show that migrations in the late Neolithic,
which have been inferred from changes in
the material culture of eastern and central
Europe (Gimbutas, 19791, are not reflected
in the current genetic structure of Indo-Eu-
ropean-speaking populations. Conversely,
the correlations of observed and simulated
data are positive and significant only if we
simulate dispersal of farmers from the Le-
vant by demic diffusion. The results of this
study are, therefore, compatible with the
128 G. BARBUJANI ET AL.
view of identifying proto-Indo-European
speakers with the first Neolithic farmers
(Renfrew, 1987).
These findings appear at first glance to
contradict the results of Sokal et al. (1992)
who use the same genetic dataset. These au-
thors concluded that geographic proximity
explained a substantial amount of the ob-
served correlation between genetic and Indo-
European linguistic distances. However,
after allowing for geographic distances, sta-
tistically significant partial correlations re-
main, which are not explained by distances
describing the origin of agriculture by demic
diffusion, Renfrews hypothesis (as de-
scribed by his postulated transitions subse-
quent to the origin of agriculture), or Gim-
butas hypothesis. But note that the study
by Sokal et al. (1992) was based on the spa-
tial pattern of correlations between genetic
and linguistic distances, whereas this study
examines genetic variation patterns only.
The simulations reported here do not con-
sider the patterns of linguistic diversity ob-
served in Europe today. Our findings are
therefore compatible as well with a simpler
model in which the observed genetic pat-
terns reflect the process of demic diffusion
accompanying the origin and spread of agri-
culture in Europe, but these populations are
not the proto-Indo-Europeans. Note that the
new findings provide further support for the
demic diffusion hypothesis of Ammerman
and Cavalli-Sforza (1984). Statistical tests
of this hypothesis were carried out by Sokal
et al. (1991) using origin-of-agriculture dis-
tances constructed from observed dates of
the onset of the Neolithic. In the present
study these distances were constructed from
the simulation results using simple models
or the spread of farming populations. It is
reassuring that these models yield results in
agreement with observed genetic patterns
as had already been noted by Rendine et al.
(1986).
Our work also offers an answer to Dia-
konovs second question; presumably, proto-
Indo-European speakers dispersed because
their increase in numbers forced them to
look for new suitable land. A study of genetic
variation such as this cannot provide reli-
able estimates of population sizes in the re-
mote past, and even less so of numbers of
migrants. However, even a very small num-
ber of dispersing individuals may yield pat-
terns that correlate with the observed ones,
as seen for the OAG model. The results of
this study are compatible both with a com-
plete replacement of pre-existing hunter-
gatherers by Near Eastern farmers (the
OAG model), and with the more conven-
tional view that this replacement was only
partial, and that hunter-gatherers contrib-
uted to some extent to the genetic pool of
Indo-European speaking populations (the
OAC model). But the view whereby lan-
guage replacement was largely independent
of population movements (Zvelebil and
Zvelebil, 1988) fails to account for the large-
scale clinal patterns matching the direction
of the spread of agriculture observed in Eu-
rope, and therefore does not seem easy to
reconcile with the available genetic evi-
dence.
In principle, one could also envisage a sce-
nario whereby expanding farmers deter-
mined the main genetic characteristics of
European populations, whereas Indo-Euro-
pean languages spread in a later moment,
and mainly by a cultural process. Although
this cannot be ruled out, it does not seem the
best explanation available for the current
patterns of genetic and linguistic variation.
The model of Neolithic demic diffusion pro-
posed by Renfrew (1991) predicts the exist-
ence of clines in three linguistic groups
which are supposed to have expanded to-
gether with Indo-European. Many such
clines have actually been observed among
speakers of Altaic and Elamo-Dravidian
languages (Barbujani and Pilastro, 1993;
Barbujani et al., 1994). Moreover, some of
these clines disappear if different linguistic
groups are jointly analyzed (Barbujani and
Pilastro, 1993). Although not a proof, these
findings suggest that linguistic affiliation is
the key to deciphering gene-frequency pat-
terns in much of Eurasia. In the areas where
Indo-European, Elamo-Dravidian, and Al-
taic languages are spoken, linguistic, ge-
netic, and archaeological evidence can
jointly be accounted for by a demic expan-
sion from the Near East. Clearly, some lan-
guages may also have changed by cultural
 INDO-EUROPEAN ORIGINS 129
contact (some examples are well docu- among Indo-European speakers. These
mented: Renfrew, 1991); however, the over- models are not mutually exclusive, and it
lap between large clines and linguistic areas may well be that both phenomena were im-
suggests that cultural transmission had a portant, a t different localities. Conversely,
lesser impact than demographic expansions. there is no evidence for a major evolutionary
role of migratory phenomena occurring in
the late Neolithic. These phenomena may
CONCLUSIONS AND FUTURE STUDIES have affected population sizes and allele fre-
The replacement of a food-collectingecon- quencies on a local scale, but the large-scale
omy by one of food production has been a structure of Indo-European speaking popu-
complex process. In the Mediterranean area, lations seems basically to reflect Neolithic
for instance, farming replaced hunting- demic diffusion.
gathering very rapidly in certain regions, New archaeological evidence will cer-
but gradually in other regions where the two tainly be valuable for describing in detail
economies coexisted for centuries (Barker, times and modes of Neolithic expansions, on
1988). However, this does not seem to have which our ideas are certainly simplistic at
deeply affected gene-frequency patterns, the moment. On the genetic side, new allele
since the ATC model, where farmers spread frequency data on previously neglected pop-
at an irregular rate, did not result in a ulations are unlikely to substantially alter
greater correspondence of observed and sim- the picture, since, for most loci, the data sets
ulated genetic distances than OAG and already include hundreds of samples.
OAC. This may mean that the variable rate Rather, collection and analysis of mtDNA
of spread of Neolithic agriculture depended may offer a new perspective on human evo-
on factors in the physical environment. Once lution in Europe, as it has already done for
these factors are incorporated in the model other areas, including Oceania (Stoneking
(OAG or OAC), simulated and observed al- et al., 1990) and the Americas (Ward et al.,
lele frequency patterns resemble each other. 1991,1993; Torroni et al., 1992; Wallace and
At any rate, the models put forward and Torroni, 1992).
tested in our study should doubtless be re-
garded as approximate. Archaeological, lin-
guistic, and genetic studies of individual ACKNOWLEDGMENTS
populations will certainly add details to our This is contribution No. 913 in Ecology
reconstruction of European history; complex and Evolution from the State University of
models of the Indo-European expansion, New York a t Stony Brook. We thank Prof.
such as the one outlined by Sherratt (1988), Marija Gimbutas and Lord Renfrew for their
may be reformulated in such a way as to collegial cooperation in this work. We are
become comparable with genetic data. Nev- indebted to Barbara A. Thomson for techni-
ertheless, this study indicates that not all cal assistance. Jeff Walker computed the
hypotheses on the origins of Indo-Europeans 3-statistics and Donna DiGiovanni word-
account equally well for the available ge- processed the manuscript. Part of the com-
netic evidence. putation was carried out on the Cornell
The hypotheses whereby Indo-Europeans National Supercomputer Facility. This
entered Europe as the first farmers show research was supported by National Science
the best fit. There seems to be no cogent Foundation grant BNS 9117350. This paper
reason to think that the farmers spread was was prepared while Robert R. Sokal was a
due to factors other than their tendency to Fellow at the Center for Advanced Study in
grow in numbers, thanks to the increased the Behavioral Sciences at Stanford, Cali-
resources available. Both incomplete admix- fornia. He is grateful for financial support
ture with hunter-gatherers, and founder ef- provided by the National Science Founda-
fects occurring in the expansion of farmers, tion grant SES-9022192, and by sabbatical
seem to account satisfactorily for the ob- funds from his home institution. Guido Bar-
served patterns of genetic differentiation bujani wishes to acknowledge fruitful dis-
130 G.BARBUJANI ET AL.

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