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Correlation of annual precipitation with human Y-chromsome diversity and emergence of Neolithic agricultural and pastoral economies in the Fertile Crescent

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Examining the beginnings of agriculture in the 'Fertile Crescent', this research team has compared the distribution of rainfall with the distribution of Y-chromosome haplogroups. The extended families signalled by J1 and J2 haplogroups seem to have had different destinies in the era of agro-pastoralist experiment: J2 were the agricultural innovators who followed the rainfall, while J1 remained largely with their flocks. Acknowledging the fuzzy edges of such mapping, the authors nevertheless escort us into new realms of the possible for the early history of peoples.
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Research
Correlation of annual precipitation with
human Y-chromosome diversity and the
emergence of Neolithic agricultural and
pastoral economies in the Fertile
Crescent
Jacques Chiaroni1, Roy J. King2& Peter A. Underhill3
Examining the beginnings of agriculture in the ‘Fertile Crescent’, this research team has compared
the distribution of rainfall with the distribution of Y-chromosome haplogroups. The extended
families signalled by J1 and J2 haplogroups seem to have had different destinies in the era
of agro-pastoralist experiment: J2 were the agricultural innovators who followed the rainfall,
while J1 remained largely with their flocks. Acknowledging the fuzzy edges of such mapping,
the authors nevertheless escort us into new realms of the possible for the early history of
peoples.
Keywords: Neolithic, Fertile Crescent, agriculture, pastoralism, annual precipitation,
Y-chromosome haplogroups, phylogeography
Introduction
The emergence of agriculture in the Fertile Crescent, while a complex and patchy event, was
facilitated by the presence of a Mediterranean climate characterised by wet winters and dry
summers. Such habitats were conducive to natural stands of cereals and legumes gathered
by pre-existing sedentary forager populations who were already in place at the onset of the
Holocene. Ice ages play an important role in shaping the genetic history of humans (Hewitt
2000; Torroni et al. 1998). The post-glacial warming trend was subsequently interrupted
by the colder, arid Younger Dryas episode, 11 000-10 300 BP (Bar-Yosef 1998; Bellwood
2005). This climatic fluctuation induced a reduction in the geographic distribution of
wild vegetative resources and likely catalysed cultural change (Twiss 2007) especially under
conditions of demographic pressure (Bar-Yosef 1998).
1French Blood Establishment of Alpes Mediterran´
ee (EFSAM), 149 Boulevard Baille, 13005 Marseille, France and
UMR6578 (CNRS/Faculty of Medicine of Marseille) Biological and Cultural Adaptability, Faculty of Medicine,
Marseille, France
2Department of Psychiatry and Behavioral Sciences, 401 Quarry Road, Stanford University, Stanford, CA 94305-
5722, USA
3Department of Genetics, Stanford University School of Medicine, 300 Pasteur Drive, Stanford, CA 94305-5120,
USA
Received: 20 August 2007; Accepted: 10 October 2007; Revised: 23 October 2007
antiquity 82 (2008): 281–289
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Correlation of annual precipitation with human Y-chromosome diversity
Figure 1. Position of haplogroup J and its major relevant
sub-clades shown within the context of the global Y-
chromosome binary phylogeny.
Genetic patterns in populations are
shaped by both locus specific forces
(natural selection) and population
level forces (drift). The latter include
migration, founder effect, neutral in
situ differentiation, non-random mating
and population size fluctuation (Cavalli-
Sforza et al. 1994). Y-chromosome
phylogeography most likely reflects the
effects of drift. The topology of the
major architectural branching structures
of human Y-chromosome diversity
in the global binary phylogeny is
an example of common descent
with modification (Figure 1).
Considerable progress in deter-
mining the global phylogenetic framework of the non-recombining
haploid mtDNA genome and Y-chromosome gene trees has propelled
the use of these elegant phylogenetic systems to characterise
population structure and reconstruct population histories (Underhill &
Kivisild 2007). Like climatic and archaeological evidence, such alternative molecular
genetic data also inform the multi-disciplinary conversation regarding the transition to
agriculture. In the case of the Y-chromosome, each molecular innovation (i.e. a nucleotide
substitution, insertion or deletion event) that creates a new branch (haplogroup) in the binary
gene tree traces to a unique common male molecular ancestor in whom the mutation event
first arose. This fact explains, to a large degree, the observation that the spatial patterning of
Y-chromosome diversity often has a particularly strong correlation with geography
(Underhill et al. 2001). One of the major varieties of Y-chromosomes that occur frequently
in the Fertile Crescent are those belonging to haplogroup J, whose representatives all
exclusively share a common single derived nucleotide base substitution that lies at the root of
this haplogroup and defines group membership. Haplogroup J manifests its highest global
frequency (50 per cent) in the western sector of the Fertile Crescent (Di Giacomo et al.
2004; Semino et al. 2004) with a spread zone spanning from north-west Africa (Arredi et al.
2004) to India (Sengupta et al. 2006). The origin of haplogroup J predates the Holocene era
and represents a persistent and widespread deep substrate of ancient common genetic heritage
(Cinniolu et al. 2004; Semino et al. 2004). Haplogroup J bifurcates into J1 and J2 varieties
(Figure 1). The results of several Y-chromosome population surveys involving haplogroup
J have been reported in populations located within the general region of the Fertile
Crescent.
Lifestyle differences exist between agriculturalists and pastoralists (Khazanov 1984).
Sedentary agriculturalists and semi-nomadic herders often occupy different ecological niches
(Cauvin 2000; Zarins 1990). Dry farming without irrigation is confined to regions of
250-400mm of annual precipitation (Bar-Yosef 1998; Buccellati 1992), while pastoral
nomadism is an adaptation to regional semi-aridity (Bellwood 2005; Zarins 1990). It has
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Jacques Chiaroni, Roy J. King & Peter A. Underhill
been shown that the spatial variation of rainfall is important in dictating the structure of
endemic flora (Kadmon & Danin 1999). Since the focus of our study is the Neolithic
transition, we restrict our analysis of Y-chromosomes and rainfall to the approximate Fertile
Crescent ‘homeland’ region implicated in the shift to an agro-pastoralist economy. We
analysed the differential phylogeography of the two offsetting sister clades of Y-chromosome
haplogroup J to demonstrate the concept of the co-evolution of genes and the phased origins
of early Neolithic cultivation and herding. Using annual precipitation to demarcate arable
(250mm) and semi-arid landscapes we evaluate corresponding extant Y-chromosome data
as a predictive metric to distinguish between the settled farming and the domesticated
animal herding lifestyles.
Methods
Twenty-two sets of Haplogroup J frequency data located within the Fertile Crescent area
were analysed from these current geopolitically defined populations: Turkey (Cinniolu et al.
2004); Egypt and Oman (Luis et al. 2004); Iraq (Semino et al. 2004); Jordan (Flores
2005), Syria and United Arab Emirates (Di Giacomo et al. 2004); Iran (Regueiro et al.
2006); Israeli Bedouins and ethnic Assyrians from Iran, Turkey and Iraq (unpublished
results). Ethnic and linguistic affiliations for some of these data are available in the original
publications.
Annual precipitation data were retrieved from The Times Atlas of the World (1989)
and the following web resource: http://www.globalbioclimatics.org/form/web.htm. Spatial
surfaces of binary haplogroup frequency and annual precipitation distributions were
computed using the MapViewer (version 7, Golden Software, Inc.). A cubic regression
analysis using Excel software was performed in which annual precipitation was the
independent variable used to predict the frequency of Y haplogroups J1-M267, J2a-
M410 and J2b-M12. The cubic regression analysis was chosen in order to detect
maximal, minimal and inflectional points in the data set. In addition Spearman ranked
correlations were calculated to test significance of the relationships between precipitation
and each Y-chromosome haplogroup frequency using the SPSS 11.0 computational statistics
application.
Results
As predicted, both haplogroups J1 and J2a correlated significantly with annual precipitation.
The Spearman correlation tests gave the following results for each haplogroup: J1
r=−0.45, p <0.05; J2a r =0.56, p <0.01; and J2b r =0.00, p (not significant).
The cubic regression for haplogroups J1 and J2a were also significant, F(3,18) =8.47
p<0.001 and F(3,18) =8.22, p <0.0012 respectively. Figure 2 illustrates the cubic
fit of haplogroups J1 and J2a versus annual precipitation. As shown, haplogroup J1
frequency increases as precipitation level reduces below the 400mm per year threshold,
typical of semi-arid climates. In contrast, haplogroup J2a frequency reaches a maximum at
700mm per year within the Mediterranean woodland and open parkland zone (Bar-Yosef
1998). Figure 3 displays the sample sites, precipitation contours and the interpolated
283
Correlation of annual precipitation with human Y-chromosome diversity
Figure 2. Panel A. Mean annual precipitation vs. haplogroup J2a-M410 frequency for 22 populations. Triangles indicate
data points. Curve is the best cubic fit. Panel B. Mean annual precipitation vs. haplogroup J1-M267 frequency for 22
populations. Triangles indicate data points. Curve is the best cubic fit.
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Jacques Chiaroni, Roy J. King & Peter A. Underhill
haplogroup frequency contours in the geographic regions analysed. Again, haplogroup
J2a frequency closely tracks the higher rainfall regions, while haplogroup J1 distributes in
the semi-arid and desert regions.
Discussion
Climatic fluctuation can spur movements of humans and also act as a mechanism
triggering social change (Kuper & Kr¨
opelin 2006). Development of Neolithic agro-pastoral
economies enhanced the opportunity for more rapid cultural divergence. It is plausible
that pastoral nomadism was an adaptation to the general semi-aridity of the region that
allowed peoples to extend their territorial range (Cauvin 2000). Although seasonality affects
both agriculturalists and pastoralists, its influence differs through the cultivation cycle
versus the mobility cycle, respectively. The study of Neolithic nomads is difficult since it
leaves fewer indications in the archaeological record. Nonetheless, some evidence of early
(8000-7600 BP) nomadic herding preserved by sandstorms has been reported in semi-arid
zones in the southern Levant (Cauvin 2000; Zarins 1990).
Previously it was shown that the cline of haplogroup J2 frequency predicted with over
80 per cent accuracy the distributions of both Neolithic pottery and figurines in the
Near East and south-eastern Europe (King & Underhill 2002). This analysis provides
another example of the correlation of Y-chromosomes and the Neolithic from a lifestyle
perspective. The genetic memory retained in the extant distributions of Y-chromosome
haplogroups J1-M267 and J2a-M410 within the Fertile Crescent significantly correlates with
regional levels of annual precipitation in a reciprocal manner. The statistically significant
correlations of Y-chromosome haplogroups, precipitation levels and domestic lifestyle are
pronounced. The spatial frequency distribution of haplogroup J2a coincides closely with
regions characterised by 400mm of annual precipitation capable of supporting settled
agriculture, while haplogroup J1-M267 distributions correlate inversely with semi-arid
regions characteristically used by pastoralists.
The frequency distributions for both haplogroups overlap when annual precipitation
approximates 250mm (Figure 2). This climatic transition zone (Buccellati 1992) underscores
the importance of not directly conflating haplogroup type with ethnicity. While the
respective haplogroup distributions are not mutually exclusive, in general, the respective
differentials in the opposing lifestyle and precipitation zones is undeniable. Prior work on
the geographic origin and the estimated dates for the temporal expansion of lineages J1-
M267 and J2a-M410 suggest a common origin near the Upper Euphrates in the foothills of
the Taurus mountains dating to the Late Glacial Maximum (LGM) (Cinniolu et al. 2004;
Semino et al. 2004). A probable scenario is that after the onset of the Holocene during the
PPNB period both J1-M267 and J2a-M410 participated in the shift to an agro-pastoral
economy with some J1-M267 lineages occupying the semi-arid regions in the Arabian
peninsula adjacent to the Fertile Crescent. At that time, an increase in frequency of J1-
M267 among semi-nomadic population was likely a random fluctuation in gene frequencies.
However, continued social-cultural barriers to population flow such as endogamy and
patrilocality could have led to the observed current differential geographic frequencies
between the J2a-M410 and J1-M267 haplogroups. The preference for intermediate annual
285
Correlation of annual precipitation with human Y-chromosome diversity
Figure 3. For caption see facing page.
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Jacques Chiaroni, Roy J. King & Peter A. Underhill
Figure 3. Panel A. Red symbols indicate the geographic locations of the 22 populations analysed. Panel B. Interpolated
spatial contours of annual precipitation (mm) distribution. Panels C and D. Interpolated spatial frequency distributions of
Y-chromosome haplogroups J2a-M410 and J1-M267 respectively in the Near East. Frequency scales are fractional.
287
Correlation of annual precipitation with human Y-chromosome diversity
rainfall levels (400-800mm) among Early Neolithic settlements may have also extended to
Thessaly in Greece (Perl`
es 2001) where J2a-M410 has been observed at high frequency (Di
Giacomo et al. 2003).
This study also provides a framework for the analysis of the maternally inherited
mitochondrial DNA genome (mtDNA) and rainfall in the Fertile Crescent. The mtDNA
genome is sensitive to both natural selection (Kivisild et al. 2006) and sex-specific forces at
the population level and may provide insights into possible sex-bias (Underhill & Kivisild
2007).
We acknowledge that our simple dichotomous model does not record that early
Neolithic societies were complex entities often characterised by broad spectrum and nuanced
subsistence strategies (Twiss 2007) that are not necessarily recorded in the genes. Complexity
in paternal heritage exists in most populations beyond just one haplogroup variety of
Y-chromosomes participating in a range expansion by agro-pastoralists. Nevertheless the
pattern of J1 and J2 haplogroup mapping provides a suggestive signal of dispersion.
Acknowledgements
The authors wish to thank Professors L. Luca Cavalli-Sfzora and Aaron Brody for their valuable comments as
well as comments by two anonymous referees. We thank Francesca Lattanzi, Mahnoosh Nik-Ahd and Jabeen
Ahmad for the Assyrian data.
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