Expected Regional Patterns of Mesolithic-Neolithic Human fopulation Admixture in Europe based on Archaeolo gical Evidence

Chapter I

Expected Regional Patterns of Mesolithic-NeolithicHuman fopulation Admixture in Europe based on

Archaeolo gical Evidence

Marta Miraz6nLahr, Robert A. Foley & Ron Pinhasi

IMile it is generally accepted that farming sprend into Europe from the Nesr East, the

extent to which this occu'.rred through population moaements or cultural diffusion or a

combination of the two remains uncirtain. One of the primary conditions for determining

the role of dispersals aersus cultural spread is the scale of the European Mesolithic

populcttionr. Hrrc rue use conclusions dlawn from an archaeological dnta base analysis

(pinhnsi et aI. Chapter 5) to generate a popul.ation density based model for determining

the expected degree of admiiture or replacement that occurred across the Mesolithic-

Neolithic transtion in r,urope. Fiae regional patterns sre desribed: 1) areas raith aery

sparse Mesolithic populations and dens"e Neoli'.thic, where the Neolithic would haae had a

major genetic impact on the succeeding gene pool (Anatolia, Bttlkans); 2) aress with

sparse"or modera'.te Mesolithic populationi and moderately dense -Neolithic settlement,

where there zuould be minor genetic contribution from the Mesolithic populations (Cen-

tral Europe, North EuropeaiPlains, northern ltaly); 3) areas where both Mesolithic snd

Neolithic populations were at lenst moderately dense, and so where there zuould be

expected an equal contribution from the two populations (southern Italy, zuestern Conti-

nental Europe); 4) areas wher-e the Neolithic wns relatiaely sparse and the Mesolithic

populations significant, and so a greater contributio.n f'rom the lst.ter.y.ould be expected

(Britain, Scnndinaaia); and ,rrrr-*hrre the Neolithic would haae had little or no impact

(Alpil. This model of regional aariation emphasizes the dynamic and geographically

sp ecific"natire of pr ehistoric human population distributions.

Recent work in molecular genetics has rekindled 7987;7998), while still controversial, certainly sup-

interest in the question of the extent to which the port the view that the spread of farming was a major

spread. of farming into Europe involved demic re- de-ogtaphic event' but have not contributed sig-

placement, cultural diffusion, or a mixture of the niflcantly to the question of the extent of genetic

;;; t;".";res. The genetic data have provided con- change' Morphological evidence has also not proven

flicting evidence, with some analysls suggesting to be concluiive, partly because the crucial remains

major genetic replacement (Ammeiman & Cavallil in terms of spatiil and temporal provenance have

Sfona7977;7973;1984;BarbujanietaLTggl;Sokalef not been studied in an appropriate comparative

al.7991),and others showing greater levels of conti- framework, and partly because the recent common

nuity (Richa rd,s et aL lg96).bit ".

lines- of evidence, ancestry of all European and adjacent populations'

principally the relationship bet.tee't tt "

,pr"ua oi together with signifiiant Palaeolithic gene flow' have

Ind.o-European languages and agriculture 1R".tfr"* reiulted in coriparatively small levels of morpho-

81

Marta Miraz6n Lahr et aL

logical diversity within the continent (Lahr 1996).Pinhasi c/ a1. (Chapter 5) have shown that the

quantitative use of archaeological data can show re-gional patterns of population history during theHolocene. This confirms the work of Houslev ef a/.(1997) and Dennell (1985) that the Early Hoiocenehuman population history of Europe is dynamic,and involves expansions and contractions of Meso-lithic populations as much as of those of Neolithicfarmers. In particular, it is clear that the demop;raphiclandscape on to which farming expanded was by nomeans uniform. In some areas, hunter-gatherers weredense and had been present for considerable time; inothers populations were sparse; in yet others theirexpansions occurred at the same time as the Neolithicin other regions of Europe, while in some regionshunter-gatherers seem to have disappeared prior tothe appearance of farming.

This complex pattern of Mesolithic occupationhas major implications for understanding the ge-netic contribution of any Neolithic populations thatmay have spread into Europe. Where there were nohunter-p;atherers, there could be no admixture. Wherethe Mesolithic populations were dense, there was agreater potential. In this chapter we develop a modelof potential interactions between hunter-gatherersand farmers based on relative population density,and then explore regional variation across Europe.The aim of the chapter is to provide molecular ge-neticists with a more realistic set of demographicexpectations for estimating the variable patterns ofadmixture and replacement that occurred with thespread of farming into Europe.

A demographic model for population replacementand genetic admixture in European EarlyHolocene history

The key insight derived from the archaeological database is that the distribution of populations acrossEurope during the Early Holocene is highly dynamic,and that this dynamism is not simply related to theappearance of the Neolithic. In population terms,

Neoli thic demography

Sparse

Table 8.1. Predictiae model for Mesolithic/Ncolithic population interqctiotr.

the major inference is that when farming appearedin Europe, it met a number of very different demo-graphic conditions, which may underlie the differ-ences in the scale, as well as timing, of Neolithicsettlements throughout the continent.

In order to try and produce testable modelsconcerning the levels of admixture among succes-sive populations, a general demographic model isnecessary. This general model uses the spatio-tem-poral patterns emerging from the archaeological database described in Pinhasi ct nl. (Chapter 6) to predictgenetic admixture between local hunter-gatherersand incoming farmers. As a simple set of init ial as-sumptions, it can be argued that the probability ofadmixture wil l be influenced by the relative sizes ofthe populations involved. More precisely, our abil-ity to detect admixture wil l be related to the prob-abil ity of each of the two populations inter-breeding,which in turn wil l be at least partly dependent uponrelative population size. From this simple assump-tion we can posit a number of theoretical possibil i-t ies (Table 8.1). First, that in regions where there wasa very sparse Mesolithic occupation and a very denseEarly Neolithic one, the Neolithic population wouldlargely carry the expanding Middle Eastern farmers'genes. Second, that in those regions where theMesolithic occupation was dense and the Neolithicone sparse, the resulting agricultural populationwould have been largely composed genetically oflocal foragers. And third, that in those areas wherethere was a dense Mesolithic occupation, followedby a dense Neolithic one, the agricultural popula-tion would have had more equal levels of geneticcontribution from the indigenous groups. The possi-ble interactions are shown in Table 8.1.

Regional ttarintiorr in Mesolithic nnd Neolithicpopulntiorts in EuropeThe basic regional demography according to sub-sistence economy and period is shown in Table 8.2.The information is derived from the available ar-chaeological data for the major regions of Europe,categorizing the level of human population density

Mesoli thic demography

lP:n',

Absent

Replacement / No admixture

Replacement / No admixture

Sparse

Minimal ad mixture (outcomedependent upon relat ivepopulat ion growth rates)

Low levels of admixture

Dense

High levels of admixture,resulting in genetic continuitv

Either replacement or admixture

82

Mesolithic-Neolithic Human PoPulation Admixture EutoPe

':,ili:ro:;il,i:;:,'J;::',:t'i#:,i:;",,P ctttern derit'ed t'rontthe different arens of

Pinhttst el

EuroPeTable 8.2. Demogrnythic prot'iles by

)i.1 Cr,op t u O' Tjt ick p e r t ic aI I i ne speriod and

indicnte the

betneen 70-5 KYn'

- No da ta

Area uninhabited'

V".y sParse occuPahonpockets of denser occuPatrons

t - - l

wI

;;;"*i".."oation with occasional

ModerateiY dense occuPation

Dense occuPation

of foragers and agriculturalists during different pe-

riods. This table ctearly identifies a nlmfer of sce-

nnrios of populatron ie'-'sity across the transition'

, " f - t i . f - ' tnd" ' i i " the genet ic lu t t : * " ' . , . - . ,From these data the following regional patterns

can be discerned'

1. Those parts of Europe where th::r1 was only a

verv sparse U"'oiitt-t'it and Late Palaeolithic oc-

ffi ;il;iJ:*:""'*J':::)","lill':X,:i"*'""were moderatetYfollowed uy u

""'f dense occupationby farmers

and no ""t'it"ttpf

hunter-gath"t"1t 'PI 5000 ep'

This is the case iol i"utJria an'd' the Balkans'

where the lmputt' ioth d"*ogtaph15 a1d genetic'

of the Neolithic';;;Jt is ihus likelv to have

been verY significant'

2. The second scenario describes-three cases' ln

which the genetrc"i'riputi of th" Neolithic would

have been *uiot)f""ti" which small amounts o{

admixture with local foragers would-h1;e been

expected.rhese:i'"'-u.::;'::.*?:Bi[::li.l.lXi!'i:fr;':J,r-," il;;tlth'c and Late Palaeorithic

ffitu,lon, -"'" ""'Y'P"'";: c;["11:ffti.'tl

dense Pockets' and

AHi'.":+:'tff +ig"=l;'.ltil:J,:1r",:.'il*:; lfl l; iT "?.# :-"# n'J^",il f: 1**ll:increased slightlY in

ment of farming l'-t tn"'" ut"us' This is the'case of

Central Europe, th" il;;h European plains and

northern ltalY'

3. The third scenario describes those areas of Eu-

rope where the genetJcontribution of immigrant

f aimers and the rtt"Jft4"ttf ithic- p opulation w ould

have been 'i-itu'' ihl' would have been the case

whete a moderatel;^;;"t" foraging population is

followed ny u *oi'"*iely dense agricultural one'

Earlv, Middle & Late Neolithic

9-5 KYaEarlv, Middle & Late Mesolithic

10-5 KYaLate Palaeolithic

Southern Italv

Northern ItalY

Central EuroPe

Northeast PIains

Western EuroPe

lberian Peninsula

r4----

83

Marta Miraz6n Lahr et al

Early Mesolithic Middle Mesolithic

/Early Neolithic

Late Mesolithic

/DIid-Late

Neolithic

Major

Genetic

Impaa of

Neolithic:very sparse --' "z*"moderate --+ Dense

Anatolia

Balkans

4.

5 .

without the survivorship ofa hunter-gatherer way of life.This is the case of southernItaly, and western Europe.The fourth case describesthose areas where the con-tribution of the local Meso-lithic groups to the resultingpopulation would have beengreater than those of the im-migrant Neolithic farmers.In these areas, the foragingpopulations increase afterthe appearance of farming,while the latter establish amoderately dense occupa-tion in some areas. This isthe case of the Brit ish Islesand Scandinavia.Finally, there are those areasof Europe where the impactof the Neolithic was virtu-ally none. This is the case ofthe Alps, where in the pe-riod between 7000 and 5000s r t he number o f f o rag ingsites increased, while therei s no ev idence fo r f a rm ingcommunities at all.

ImTtl i cat i ons fo r gerr e t i c s t u d ie sFigure 8.6 shows a map of Eu-rope which summarizes the re-gional patterns and expectationsdiscussed above. The darker theshading, the greater the ex-pected Neolithic genetic contri-bution if the archaeologicallyderived demographic model iscorrect.

Over two decades agcr ,Menozzi and colleagues (1978)introduced a series of maps ofgene f requencies of c lass ical ge-net ic systems across Europe.The map based on the loadingson the first principal componentin their statistical analysis dis-played a southeast to northwestcline which is compatible withthe model of the spread of farm-ing into Europe from the NearEast. Since then, similar results

Figure 8.'I,. Pnttern for a major Neolithic gertetic conrytonent.

Figure 8.2. Pottern for a major I 'Jeolithic genetic component rtt ith a mhrorMesol ith ic cort t r ib tLt io rt

Earlv Mesolithic Middle Mesolithic

/Earlv Neolithic

Late Mesolithic

Mid-Late Neolithic

Major

Genetic

Impact of

Neolithic,

wilh very

minor

Mesolithic

admixlure

verysparse --'' verysparse ---> sparse

tsparse

C. Europe

dense pockets ---) very sparse v.:ry sparse--}..-.,

' r 'ra

dense

N. European Plains

very sparse -"'7 very sparse very sparse

sparse

N. haly

Early Mesolithic Middle Mesolithic

/Earlv Neolithic

Late Mesolithic

/IVIid-Late Neolithic

Equal

genetic

contribution

of Mesolithic

and

Neolbhic

moderate ----,1,' .... very sparse-..*:::r

moai;;6--> dense

S. Italy

very sparse or

dense pockets ---; moderate --> J.::::...

moderate

W. Europe

S. France

Figure 8.3. Pattern for an equal Mesolithic nnd Neolithic gerrctic comporrcrft.

Mesolithic-Neolithic Human Population Admixture in Europe

have been obtained by Sokaland colleagues (1991) in theirs tudy of 26 genet ic systemsfrom 3373 localit ies in Europe,using spat ia l autocorre lat ionstatistics, by Semino and col-leagues (1qgb) in the frequenciesof two distinct Y-chromosomemarkers, and by Chikhi and col-leagues (1998) based on nuclearDNA variations.

The existence of a clinefrom southeast to northwestEurope was originally inter-preted as beinp; the outcome ofthe'demic diffusion' of farmersfrom the Near East, who wouldhave abso rbed a iong the i rmigration route, many of thelocal Mesolithic hunter-gathererbands (Cavall i-Sforza et al.7993;Cavalli-Sforz a 7996). The natureof these studies, drawing theirin ferences f rom the pat ternfound in the l iving populationof Europe, precluded the estab-lishment of the routes and tim-ing of the proposed Neolithicdiffusion across the continent.These genetic studies also didnot include in their assessment of the impact of sucha demic diffusion the varying population densitiesof the local Mesolithic population, either prior, dur-ing or after the'wave of advance'.

Barbujani and colleagues (1995) took a moretheoretical approach to the study of the spread offarming into Europe. They conducted a simulationstudy that compared five models of microevolutionin European populations. The simulations were basedon a combination of possible factors explaining theobserved clinal distribution of genetic systems acrossthe continent. Their f irst model was based on theassumption that European populations evolved un-der conditions of isolation by distance (IBD). Undersuch a model, current differentiation in allele fre-quencies among European populations would be sim-ply the outcome of random factors such as geneticdrift, dispersal and isolation. Their second model(OAC - isolation by distance plus effects of theorigins of agriculture) assumed that local hunter-gatherer populations were replaced without admix-ture by the incoming Neolithic farmers. The thirdmodel (OAC - isolation by distance plus the effects

Figure 8.4. Pattern for a greater genetic contribution from the Mesolithicpopulnt ions.

Figure 8.5. Pattern for rrc gerrctic impact for thc Neolithic.

of the origins of agriculture and cultural transmis-sion) adds the hypothetical effects of cultural trans-mission between the local hunter-gatherer bands andthe Neolithic farmers. The underlying assumptionin this case is that in certain regions, local hunter-gatherers adopted farming, and thus some of theirgenes would have contributed to the gene pool ofthe Neolithic population. This is equivalent to the'demic diffusion' model described above. The fourthmodel (ATC - as above plus archaeological t imeconstraints) added the effects of archaeological t imeconstraints by incorporating a temporal sequence ofwhen farmers arrived in the various localit ies in Eu-rope. The fifth and last model (GIM - as above pluseffects of later Neolithic migrations) adds to theformer ones the effect of Late Neolithic migrationsof the proto-Indo-European people. Barbujani andcolleagues (1995) found that the fit of the classicalg;enetic data to simpler models, such as OAG andOAC, is better than to the more complex ones. Thus,in their view, the addition of archaeological data(radiocarbon dates) and Late Neolithic populationmovements added nothing to the understanding of

Early Mesolithic Middle Mesolithic

/Early Neolithic

Late Mesolithic

/lVIid-Late Neolithic

Greater

genetic

contribution

of Mesolithic

very sparse sparse ---> moderate

Ftmoderate

Britain

densepockets ---| densepockets--+ moderate

4- t ery spirse

Scqndinavia

Early Mesolithic Middle Mesolithic

/Early Neolithic

Late Mesolithic

/IVIid-Late

Neolithic

No Genetic

Impoct of

Neolilhicdensepockets---) ---) verysparse

Alps

*-_

85

Marta Miraz6n Lahr et al

Figure 8.6. Stunmary mop of EuroTte showing the erpected genetic contributions of Neolithic and Mesolithicpopulntiorts hnsed ort thc demogrophic model snd srchneological etridence .

the pattern of genetic differences in Europe today.The OAC model, which is consistent with the'demicdiffusion' model of Ammerman & Cavall i-Sforza(7971; D8\, and the OAG model, that argues for noadmixture with local populations, show similar con-gruence with actual genetic data. Barbujani and col-leagues (1995) conclude that this may be explainedby the fact that a series of successive founder effectsand admixture between geographically separatedfarming groups would have af fected the c l ina ldistribution of genes in a similar manner had admix-ture between expanding farmers and local hunter-gatherers taken p lace.

In contrast, Richards et al. (7996) have usedmtDNA data to construct a somewhat differentmodel. The mtDNA network analyses suggest a muchless spatially structured pattern of European geneticvariation, with less evidence for a geographical gra-dient from the southwest to the northeast. Further-more, their analyses suggest that there is l i tt leevidence for a coalescence of mitochondrial lineagesat the time of Neolithic expansions across Europe,and that the existing Mesolithic and Palaeolithicpopulations made significant contributions to the

extant gene pool.The analyses of archaeologically inferred popu-

lation densities presented here suggest that neitherextreme is likely to be correct, but that regional vari-ation should be expected. The impact of the Neolithicis dependent upon three factors. The first is the den-sity of the Mesolithic populations. Significant contri-butions from Mesolithic populations can only occurwhere there were sufficient numbers of such peo-ples, regardless of the size of any incoming farmers.It is this regional demographic variation in Mesolithicpopulations that has not been taken into account inmost previous work. Pinhasi et uI. (Chapter 6), andthe models developed here indicate that it was onlythe north and northwestern parts of the continentand in parts of southern/western France and south-ern Italy that such dense populations existed. Else-where, the dynamics of the Mesolithic populationsduring the earlier parts of the Holocene make a sig-nificant contribution of Mesolithic genes to thepresent gene pool less likely.

The second factor is the scale of the Neolithicexpansion. Large and rapid expansions should leadto a genetic signature that is distinctive. This would

86

Mesolithic-Neolithic Human Population Admixture in Europe

be expected primarily in the Balkans and Anatolia,and to a lesser extent across Central Europe, particu-larly the Danube basin. lf the genetic data do showcontinuity, then this would imply that any incomingpopulation was already closely related to the popu-lations of Europe, and thus perhaps show evidencefor a common Later Pleistocene population in theEastern parts of the Mediterrarlean, with continuousgene flow leading to older estimated coalescence ages.

The final factor is the nature of any interactionbetween Mesolithic and Neolithic populations. Thesewould ult imately be dependent upon social and eco-logical factors, which have not been considered here.Two considerations are essential. One of these iswhether any interactions are competitive or co-op-erative. In either case this may lead to admixture,either through exchange of women in particular be-tween groups, or through the absorption of indi-viduals from displaced groups into the farmingcommunities. The other is that ethnographic experi-ence suggests that female mobility between suchgroups is l ikely to be higher than that of males (Foley& Lahr in press). This differential sex bias might bethe primary cause of the differences between theevidence derived from mtDNA and that from othergene systems. In the end it may be that Mesolithicwomen are better represented in the modern popu-lations of Europe than Mesolithic men.

Finally, it is worth stressing that this modeltakes no account of subsequent movements of popu-lations in Europe. We know from both historical andarchaeological evidence that there have been sub-stantial population movements over the last five mil-lennia, and thus there is a question mark to be placedover any assumptions about the geographical stabil-ity of populations derived from Neolithic expan-sions.

Conclusions

In this chapter we have argued that the nature ofgenetic continuity between Mesolithic and Neolithicpopulations of Europe depends upon demographicconditions prevail ing at the time. The archaeologicalrecord, as discussed by Pinhasi cf a/. (Chapter 6) canprovide information about these conditions. Thearchaeological evidence shows that the Mesolithicpopulat ions were very sparse in some par ts ofEurope, and considerably more densely packed inothers. Any arriving farmers would thus have metvery different competitive and interactive conditions,with divergent potential for gene flow. Furthermoreit is clear from the archaeological record that the

Neolithic expansion also occurred at very different

population densities. Farmers, whatever their ge-

netic affinities, were much denser in the Balkans and

Anatol ia, and parts of Central Europe, but were

never, during the Neolithic, verv abundant to the

north and west. These archaeologically derived mod-

els can be used to provide better expectations for the

nature of any replacement or admixture that may

have occurred at the time of the first farming econo-

mies in Europe.

References

Ammerman, A.J. & L.L. Cavall i -Sforza, 7977. Measuringthe rate of spread of early farming in Europe. Mari(N.S.) 6, 674 88.

Ammerman, A.J. & L.L. Cavall i -Sforza, 1.973. A popula-tion model for the diffusion of earlv farming in Eu-rope, in Thc Explnnntion of Culture Chnrtgc, ed. C.Renfrew. London: Duckworth, 343-57.

Ammerman, A.J. & L.L. Cavall i -Sforza, 1984. Tlrc Neoli thicTrnnsit ion arul the Cettet ics of Populnt ions iu Europte .Princeton (NJ): Princeton University Press.

Barbujani, C., R.R. Sokal & N.L. Oden, 1995. Indo-Euro-pean origins: a computer-simulat ion test of f ive hy-potlreses. Anrcricnn lcnLrrrnl oJ' Physicnl Anthropologv96,709-32.

Cavall i -Sforza, L.L., 1996. The spread of agriculture andnomadic pastoralism: insights from genetics, linguis-tics, and archaeology, in Tha Origitts nntl Sprend ofAgriculturc and Pnstoral ism in Eurasin, ed. D. Harris.London: University College London, 51-69.

Cavall i -Sforz a, L.L., P. Menozzi & A. Piazza, 1993. Demicexpansions and human evolution. Sciancc 259,63946.

Chikhi, L., G. Destro-Bisol, V. Pascal l , V. Baravel l i , M.Dobosz & C. Barbujani, 1998. Cl inal variat ion in thenuclear DNA of Europeans. Hurnnrt Biology 70,643-57.

Dennell , R.W., 1985. European Ecortontic Prehistort l : n Nett,Altltronclt. London: Academic Press.

Foley, R.A. & M.M. Lahr, in press. Anthropological andecological parameters for modell ing human genet-ics, in Cerrcs, Fossi ls nrrd Beltnzt iour, ed. P. Donnelly &R.A. Foley. Brussels: NATO Advanced Seminar Pub-l icat ions.

Housley, R.A., C.S. Gamble, M. Street & P. Pett i t t , 1997.Radiocarbon evidence for the Late Glacial humanrecolorrisation of northern Europe. Proccedirtgs of thcPrehistoric SocictV 63,25 54.

Lahr, M.M., 7996. Thc Eoolutiorr of Modarrt Hwnnn Di-oer-sify. Cambridge: Cambridge University Press.

Menozzi, P., A. Prazza & L.L. Cavaili-Sforza, 1978. Syn-thetic maps of human gene frequencies in Europe-ans. Scicnce 201, 786-92.

Renfrew, C.,7987. Archaeology nnd LnngtLage: the Puzzle ofthe Itrdo-EuroTtcarr Origirts. London: Penguin Books.

Renfrew, C.,7998. World l inguist ic diversity and farmingdispersals, in Archncology atd Langtrase, vol. 7: Theo-

€s.#:i

4---

87

Marta Miraz6n Lahr et aI.

retical and Methodological Orientatiotts, eds. R. Blench

& M. Spriggs. London: Routledge, 82-90.

Richards, M., H. COrte-Real, P. Forster, V. Macaulay, H.

Wilkinson-Herbots, A. Demaine, S. Papiha, R.

Hedges, H-J. Bandelt & B. Sykes, 1996. Paleolithic

and Neolithic lineages in the European mitochon-

drial gene pool. American lournal of Hunnn Cenetics

s9(1) ,185-203.

Semino, O., G. Passarino, A. Brega, M. Fel lous & A.S'

Santachiara-Benerecetti, 1996. A view of the Neolithic

demic diffusion in Europe through two Y chromo-

some-specific markers. American lournal of Human

Genetics 59(4),964-8.Sokal, R.R., N.L. Oden & C. Wilson, 1991. Genetic evi-

dence for the spread of agriculture in Europe by

demic diffusi on. N atur e 351, 143-4.

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