The Neolithic

Alan R. Rogers

March 7, 2018

Spread of farming across Europe

(Grahame Clark, 1965, Proc. Prehist. Soc.)

Major axis of genetic variation in Europe

95 genes (Cavalli-Sforza, 1994, p. 292)

Movement of people or of technology?

Local hunter-gatherers contributed less than 30% in theoriginal settlements. This finding leads us to reject apredominantly cultural transmission of agriculture.

(Lounes Chikhi et al. 2002)

Both mitochondrial DNA and Y chromosome analyses haveindicated a contribution of Neolithic Near Eastern lineages to thegene pool of modern Europeans of around a quarter or less. Thissuggests that dispersals bringing the Neolithic to Europe may havebeen demographically minor.

(Martin Richards 2003)

24 ky old burial from Mal’ta, Siberia

(Raghavan et al. 2013)

24 ky old burial from Mal’ta, Siberia

(Raghavan et al. 2013)

I 1/3 of ancestry sharedwith Native Americansand Europeans

I European mitochondrialDNA

Y haplogroup R1b1b2 most common in Ireland:

Mesolithic origin?

Microsatellite loci

I Microsatellite: a short DNA sequence repeated severaltimes, adjacent on chromosomeExample:ATTC ATTC ATTC ATTC (4 copies)ATTC ATTC ATTC ATTC ATTC ATTC (6 copies)

I High mutation rate.

I Variance among chromosomes increases with time.

Microsatellitevariationmeasures age

I Rows aredifferentmicrosatellites

I CG haplotype isold

I TA haplotype isyounger: about10,000 years

(Coelho et al 2005)

On Y haplogroup R1b1b2, microsatellite variation

is greatest in Turkey

Microsatellite variance vs. earliest Neolithic dates The Blatterhohle site in Germany

Skeletal remains fromMesolithic and Neolithicoccupations.

mitochondrial DNA

isotopic data (tells aboutdiet)

Bolingino et al (2013)

Isotopes (axes) and mtDNA (colors)

(Bollongino et al, Oct 2013)

Nuclear genes of Neolithic farmers and foragers

(Skoglund et al, 2012)

During Neolithic, farmer DNA like modern Sardinians.Forager DNA like modern Finns.

Neolithic farmers and foragers had different DNA

(Skoglund et al, 2012)

Large survey of Neolithic DNA

180 genomes fromEuropeanNeolithic andChalcolithic

From Hungary,Spain, Germany.

Lipson et al.(2017)

Mesolithic ancestry increases with time

Farmers andforagers co-existedand interbred overmillennia.

4 admixturegreatest inGermany

Lipson et al.(2017)

Eastern farmers interbred with eastern foragers

Principal components plot again

Modern Europeans

Anatolian Neolithic

Westernhunter-gatherers

Germany

Spain and Portugal

Neolithic populationsvaried in level ofMesolithic admixture.

Neolithic Britain

Neolithic arrives in NW Europe ∼7000 years ago.

Doesn’t make it to Britain for another 1000 years.

What happened then? A story unlike that of early NeolithicEurope.

Study of Brace et al (2018)

Genome-wide datafrom 6 Mesolithicand 67 NeolithicBrits, dating from10.5–4.5 kya.

Mesolithic admixture in Neolithic Britain

WHG fractiondoesn’t increasewith time.

Neolithic Britsdidn’t interbreedwith foragers.

Outline

◦ The European Neolithic: a movement of peoples or oftechnology?

I Linkage disequilibrium (LD)

I How LD responds to changes in population size.

I The history of European population size.

Linkage disequilibrium (LD) is one of those unfortunate termsthat does not reveal its meaning. As every instructor ofpopulation genetics knows, the term is a barrier not an aid tounderstanding. . . Detecting LD does not ensure either linkageor a lack of equilibrium.

(Montgomery Slatkin, 2008)

Gamete types at two genetic loci

A BA b

a B

a b

One locus has alleles A and a.

The other has alleles B and b.

There are four possible typesof gamete.

Gametes that carry A are“A-gametes.”

Linkage Equilibrium ⇐⇒ shaded fractions equal

A-gametes

b

B

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a-gametes

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LE: Knowledge aboutone locus tellsnothing about other.

Here, B is equallycommon amongA-gametes anda-gametes.

LD ⇐⇒ shaded fractions unequal

A-gametes

b

B

a-gametes

b

B

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...

LD: Knowledge aboutone locus helpspredict the other.

Here, B is morecommon amongA-gametes thana-gametes.

You can see LD in sequence data

(Garrigan et al 2004)

I Dots: identical tochimp sequence.

I Sites notindependent.

I A at site 1343predicts G at 1951

I This is linkagedisequilibrium (LD).

Cross-overs shuffle DNA

I occur duringreproduction.

I shuffle parentalchromosomes.

I sites far apartshuffled more.

I destroys LD

Why population size affects LD

I Small populations have short genealogies.

I Little time for recombination to happen.

I Lots of LD.

σ2d is a measure of LD

I Insensitive to sequencing error.

I Sensitive to ancient history.

European LD curve for chromosome 1

0.0

0.1

0.2

0.3

σ2d

0.0 0.1 0.2 0.3

Distance Between Sites (cM)

circles estimated σ2d

dashes 95% moving-blocks bootstrap◦

◦

◦◦◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦

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............. ............. ............. ............. ............. ............. ............. ............. ............. ............. ............. ............. ............. ............. ............. .............

Outline

◦ The European Neolithic: a movement of peoples or oftechnology?

◦ Linkage disequilibrium (LD)

I How LD responds to changes in population size.

I The history of European population size.

What does population growth do to the LD curve?

103

106

2N

tGenerations before present

Assumed history...................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................................

t generations ago, the population (2N) grew from 103 to 106.

Population growth makes LD curve steep

0.0 0.1 0.2 0.3

Distance Between Sites (cM)

t =∞1500

1000

500

t = 0

σ2d

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◦◦◦◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦

European LD curve is steep

0.0

0.1

0.2

0.3

σ2d

0.0 0.1 0.2 0.3

Distance Between Sites (cM)

◦

◦

◦◦◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦

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Observed σ2d minus best-fitting equilibrium curve

−0.01

0.00

0.01

0.02

0.03

0.0 0.1 0.2 0.3

Distance Between Sites (cM)

◦

◦

◦

◦◦◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦

◦ ◦ ◦

Differences positive on left;negative on right.

Observed curve is steeper thanany equilibrium curve.

Implies population growth.

Estimates from simulation of expanded population

102

104

106

108

2N

0 300

Generations Ago

Expansion at t = 300

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× × × × × × ×

× × ×

Shows same estimates as time path.

Estimates from European chromosomes (1000-Genomes Prj)

102

104

106

108

2N

Chr 1

............. ............. ............. ............. ....................................... ............. .......

.................................................................................................................................................................................................................................

............. ............. ............. ............. .................................................... ............. ....

Chr 2

............. ............. ............. ............. ....................................... ............. ....

...............................................................................................................................................................................................................................

............. ............. ............. ............. .................................................... .............

Chr 3

............. ............. ............. ............. ............. ............. .............

.......................................................................................................................................................................................................................

............. ............. ............. ............. ....................................... ............. .............

102

104

106

108

2N

0 200 400

Chr 4

............. ............. ............. ............. ............. ............. .............

.................................................................................................................................................................................................................

............. ............. ............. ............. ....................................... ............. .............

0 200 400

Chr 5

............. ............. ............. ............. ....................................... ............. ......

...............................................................................................................................................................................................................................

............. ............. ............. ............. .................................................... .............

0 200 400

Chr 6

............. ............. ............. ............. ............. ............. ................................................................................................................................................................................................ ............. ............. ............. ............. ............. ...........

Estimates from European chromosomes (1000-Genomes Prj)

102

104

106

108

2N

Chr 7

............. ............. ............. ....................................... ............. .......

...................................................................................................................................................................................................

............. ............. ............. ............. ....................................... ............. ..

Chr 8

............. ............. ............. ............. ............. ............. .............

........................................................................................................................................................................

............. ............. ............. ....................................... ............. .............

Chr 9

............. ............. ............. ............. ....................................... .............

........................................................................................................................................................................................................................

............. ............. ............. ............. .................................................... .............

102

104

106

108

2N

0 200 400

Chr 10

............. ............. ............. ............. ....................................... ............. ..

..........................................................................................................................................................................................................................

............. ............. ............. ............. .................................................... .............

0 200 400

Chr 11

............. ............. ............. ............. .......................... ............. .......

...........................................................................................................................................................................................................

............. ............. ............. ............. .................................................... .....

0 200 400

Chr 12

............. ............. ....................................... ............. ............. ............

...........................................................................................................................................................................................................

............. ............. ............. .................................................... ............. .

Estimates from European chromosomes (1000-Genomes Prj)

102

104

106

108

2N

Chr 13

............. ............. ............. ............. ....................................... ............. ..

.........................................................................................................................................................................................................................

............. ............. ............. ............. .................................................... .............

Chr 14

............. ............. ............. ............. ....................................... .............

..........................................................................................................................................................................................................................

............. ............. ............. ............. .................................................... .............

Chr 15

............. ............. ............. ............. ....................................... ............. .......

...............................................................................................................................................................................................................................

............. ............. ............. ............. .................................................... ............. .

102

104

106

108

2N

0 200 400

Chr 16

............. ............. ............. ............. .......................... ............. ....

....................................................................................................................................................................................................

............. ............. ............. ............. ....................................................

0 200 400

Chr 17

............. ............. ............. ............. ............. ............. ................................................................................................................................................................................................ ............. ............. ............. ............. ............. ...........

0 200 400

Chr 18

............. ............. ............. ....................................... ............. ............. ..

...........................................................................................................................................................................................................................

............. ............. ............. ............. .................................................... .............

Estimates from European chromosomes (1000-Genomes Prj)

102

104

106

108

2N

Chr 19

............. ............. ............. ..........................

............. .............

.............................................................................................................................................................................................

............. ............. ............. ............. ............. .......................................

0 200 400

Chr 20

............. ............. ............. ....................................... ............. ............

............................................................................................................................................................................................................

............. ............. ............. .................................................... ............. .....

0 200 400

Chr 21

............. ............. ............. ............. .......................... ............. .............

....................................................................................................................................................................................................................

............. ............. ............. ............. .................................................... .............

102

104

106

108

2N

0 200 400

Chr 22

............. ............. ............. ............. ....................................... .............

....................................................................................................................................................................................................................

............. ............. ............. ............. .................................................................

LD documents an expansion in European population size 300generations ago.

Or roughly 8000 y ago.

LD documents an expansion in European population size 300generations ago.

Or roughly 8000 y ago.

Neolithic radiocarbon dates

(Gkiasta et al, 2003)

Summary

I LD documents a Neolithic expansion of the Europeanpopulation.

I There was a movement of people during the Neolithic.