Balinese Y-Chromosome Perspective on the Peopling of
Indonesia: Genetic Contributions from Pre-Neolithic Hunter-
Gatherers, Austronesian Farmers, and Indian Traders
TATIANA M. KARAFET,1J. S. LANSING,2,3ALAN J. REDD,1JOSEPH C. WATKINS,4S. P. K.
SURATA,5W. A. ARTHAWIGUNA,6LAURA MAYER,1MICHAEL BAMSHAD,7LYNN B.
JORDE,7AND MICHAEL F. HAMMER1,2
islands in the Indonesian archipelago, which served as a stepping-stone for
early migrations of hunter-gatherers to Melanesia and Australia and for more
recent migrations of Austronesian farmers from mainland Southeast Asia to
the Pacific. Bali is the only Indonesian island with a population that currently
practices the Hindu religion and preserves various other Indian cultural, lin-
guistic, and artistic traditions (Lansing 1983). Here, we examine genetic
variation on the Y chromosomes of 551 Balinese men to investigate the
relative contributions of Austronesian farmers and pre-Neolithic hunter-gath-
erers to the contemporary Balinese paternal gene pool and to test the hypoth-
esis of recent paternal gene flow from the Indian subcontinent. Seventy-one
Y-chromosome binary polymorphisms (single nucleotide polymorphisms,
SNPs) and 10 Y-chromosome-linked short tandem repeats (STRs) were ge-
notyped on a sample of 1,989 Y chromosomes from 20 populations repre-
senting Indonesia (including Bali), southern China, Southeast Asia, South
Asia, the Near East, and Oceania. SNP genotyping revealed 22 Balinese
lineages, 3 of which (O-M95, O-M119, and O-M122) account for nearly
83.7% of Balinese Y chromosomes. Phylogeographic analyses suggest that
all three major Y-chromosome haplogroups migrated to Bali with the arrival
of Austronesian speakers; however, STR diversity patterns associated with
these haplogroups are complex and may be explained by multiple waves of
Austronesian expansion to Indonesia by different routes. Approximately
2.2% of contemporary Balinese Y chromosomes (i.e., K-M9*, K-M230, and
The island of Bali lies near the center of the southern chain of
1Division of Biotechnology, Biosciences West, University of Arizona, Tucson, AZ 85721.
2Anthropology Department, University of Arizona, Tucson, AZ 85721.
3Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87521.
4Mathematics Department, University of Arizona, Tucson, AZ 85721.
5Maharaswati University, Tabanan, Bali, Indonesia.
6Balai Penelitian dan Pengkajian Teknologi Pertanian, Denpasar, Bali, Indonesia.
7Department of Human Genetics, University of Utah, Salt Lake City, UT.
Human Biology, February 2005, v. 77, no. 1, pp. 93–113
Copyright ? 2005 Wayne State University Press, Detroit, Michigan 48201-1309
KEY WORDS: BALI, INDONESIA, Y CHROMOSOME, AUSTRONESIAN EXPANSION, INDIAN
TRADERS, PRE-NEOLITHIC HUNTER-GATHERERS, VIETNAMESE, MALAYSIANS, PHILIPPINOS, TAI-
WANESE ABORIGINALS, SOUTHERN CHINESE, INDIANS, SRI LANKANS, SYRIANS, SAUDI ARABI-
ANS, MELANESIA, MICRONESIA, POLYNESIA, PAPUA NEW GUINEA, OCEANIA.
$CH8 01-04-05 13:56:03PS
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M lineages) may represent the pre-Neolithic component of the Indonesian
paternal gene pool. In contrast, eight other haplogroups (H, J, L, and R)
making up approximately 12% of the Balinese paternal gene pool appear to
have migrated to Bali from India. These results indicate that the Austronesian
expansion had a profound effect on the composition of the Balinese paternal
gene pool and that cultural transmission from India to Bali was accompanied
by substantial levels of gene flow.
Bali is one of the stepping-stones in the land bridge that once connected the
islands of Indonesia to the Asian mainland. Archeological and fossil evidence
suggests that the earliest inhabitants of Australia and Papua New Guinea crossed
this bridge 40,000 to 60,000 years ago (Thorne et al. 1999; Bowler et al. 2003).
Nineteenth-century Dutch archeologists envisaged continuous human occupation
in Bali stretching back into the Pleistocene (Lansing 1995). More recent archeo-
logical evidence indicates that Austronesian-speaking peoples settled on the coast
of Indonesia (including Bali), Malaysia, southern Vietnam, and the Philippines
before colonizing most of the inhabitable islands of the Pacific (Bellwood 1997).
This has led to the consensus view among archeologists that Austronesian-speak-
ing peoples migrated to Indonesia between 4,500 and 3,000 years ago from
southern China and Taiwan and displaced an aboriginal population of hunter-
gatherers. This view implies a southern Chinese or Taiwanese origin of Balinese
genes. Rapid eastward migrations resulted in the spread of both the Austronesian
language family and associated culture to coastal Melanesia and throughout Poly-
nesia between 3,000 b.c. and a.d. 400 (Bellwood 1997).
An alternative view posits an indigenous origin of Austronesian languages
in Melanesia or Southeast Asia (Dyen 1962; Oppenheimer 1998) with much less
population replacement by Neolithic farmers. Under this model substantial ge-
netic contributions from pre-Neolithic hunter-gatherers may be expected in con-
temporary Balinese. Genetic data from both mitochondrial DNA and the Y
chromosome have recently contributed to this controversy. By mainly focusing
on Polynesian populations, some researchers favor the rapid migration or ‘‘ex-
press train’’ (Diamond 1988) model (Sykes et al. 1995; Redd et al. 1995; Melton
et al. 1998; Su, Jin et al. 2000), and others favor a major contribution to the
Polynesian gene pool from eastern Indonesia and Melanesia (M. Richards et al.
1998; Capelli et al. 2001; Kayser et al. 2001; Hurles et al. 2002). Until now,
there has been no analysis focusing on the genetic composition of the island of
A second set of questions pertains to the more recent history of Indonesia.
Between the 3rd and 13th centuries a.d. dozens of Indic kingdoms appeared
across Southeast Asia, from the plains of Cambodia and central Java to remote
corners of Borneo and highland Burma (Lansing 1983). Bali became as deeply
‘‘Indianized’’ as any Southeast Asian society—worshipping Hindu and Buddhist
deities, celebrating the great Hindu and Buddhist myths, and measuring social
behavior against the standards of a caste system. Classical Indic civilization sur-
vived on Bali until the 20th century, long after the destruction of the other Indic
Y-Chromosome DNA in Bali / 95
states. But the question of how Indian culture came to Bali has never been fully
Two competing hypotheses concern the degree of demic versus cultural
diffusion. Although there is no evidence that Bali was initially populated by
Indians, archeological excavations provide evidence of Indian trade contacts
going back about 2,000 years (Ardika and Bellwood 1991). Majumdar (1963)
postulated wholesale colonization by Indian exiles, whereas van Leur (1955) ar-
gued that Indianization was wholly initiated by Southeast Asians who summoned
Brahmins to visit their courts, creating merely a ‘‘thin and flaking glaze’’ of Indic
language and customs. Although the spread of Islam was much more recent than
that of Indian religions, it was also more successful: Islam became the dominant
religion of Malaysia and Indonesia. Therefore, apart from Indianization, the pos-
sible influence of Persians and Arab Muslims has to be taken into account.
In the past three years the publication of a robust Y-chromosome haplo-
group tree defined by more than 250 binary polymorphisms (Y Chromosome
Consortium 2002; Jobling and Tyler-Smith 2003) has provided an opportunity to
understand paternal population origins, relationships, and dispersals with more
phylogenetic and geographic resolution than was previously possible. The addi-
tion of microsatellite data facilitates the estimation of haplogroup ages and popu-
lation divergence times, both of which can be used to infer the chronology of
recent human dispersal events. Indeed, the combination of these two kinds of
data provides a valuable source of information for more precise identification of
ancestral relationships, patterns of gene flow, and the effects of various demo-
graphic processes. Here, we present the first large-scale survey of Balinese pater-
nal diversity using a battery of 71 binary polymorphisms (mainly single
nucleotide polymorphisms, or SNPs) and 10 microsatellites on a sample of 551
Balinese Y chromosomes. Through comparisons of variation at the same markers
in a large Asian sample we assess the relative contributions of Austronesian farm-
ers, pre-Neolithic hunter-gatherers, and Indian traders to the contemporary Bal-
inese paternal gene pool. The results of these analyses reveal a complex history
of genetic contributions from different source populations.
Subjects and Methods
We analyzed 71 SNPs and 10 short tandem repeats (STRs) in a
sample of 1,989 Y chromosomes from 20 populations. Our Indonesian samples
included 551 Balinese Y chromosomes and 76 Y chromosomes from western
(n?21) and eastern (n?55) Indonesia. Also included in this survey were 1,187
Y chromosomes from 13 populations representing other Southeast Asians (Viet-
namese, Malaysians, Philippinos, and Taiwanese aboriginals), Southern Chinese
(Han, Miao, She, Tujians, and Yao), South Asians (southern Indians and Sri
Lankans), and Near Easterners (Syrians and Saudi Arabians) and 175 Y chromo-
somes from Melanesia, Micronesia, Polynesia, and Papua New Guinea (collec-
tively referred to as Oceania) (Table 1; Figure 1). Many of the non-Balinese
96 / karafet et al.
Frequencies of Major Y-Chromosome Lineages in Bali and 19 Additional Population
(M69) I (P19)
a. Downstream markers typed but not shown. See ‘‘Subjects and Methods’’ section and Figure 1 for a complete list of markers
b. O-P31* and O-SRY465.
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Y-Chromosome DNA in Bali / 97
Approximate geographic positions of 18 populations sampled in this study (see Table 1
and text for names and sizes of population samples). The populations are grouped into
four major geographic areas (dotted circles). Near Eastern populations (19 and 20) are
samples analyzed here have been described in previous studies (Bamshad et al.
2001; Hammer et al. 2001; Karafet et al. 2001; Redd, Roberts-Thomson et al.
2002). The Chinese Han sample was composed of individuals from the Guang-
dong and Shaanxi provinces and of individuals from different parts of Taiwan
(Karafet et al. 2001).
Buccal swabs were collected in 2001–2002 from 551 Balinese volunteers,
who gave informed consent. All sampling protocols were procedures approved
by the University of Arizona Human Subjects Committee and Balai Pengkajian
Teknologi Pertanian (Bali). Buccal cell DNA was isolated according to the
method of B. Richards et al. (1993).
previously published binary Y-chromosome markers (Karafet et al. 2002) and
the following eight polymorphisms: M69, M70, M110, M111, M214, and M230
(Underhill et al. 2000; Kayser et al. 2003), Apt (Pandya et al. 1998), and P34.
This is the first report describing PCR conditions for P34, a polymorphism re-
cently discovered in a panel of 92 globally distributed Y chromosomes (Hammer
et al. 2003). The Apt and M230 markers were genotyped as reported by Pandya
et al. (1998) and Kayser et al. (2003), respectively. We designed allele-specific
The polymorphic sites in our survey included a set of 63
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PCR reactions to type M69, M70, M110, M111, and M214 (conditions available
on request from T. Karafet).
A GVA mutation (referred to as P34) at position 956 of the DYS190
locus was genotyped by allele-specific PCR. The following primers were used to
amplify the 399-base pair (bp) control band and the 170-bp band that was allele
specific for mutant chromosomes: P34U (5?-CCTGGAAAAGTCAAATCATCG-
3?), P34L (5?-CGTGGCATCTTGTCATGTCT-3?), and P34A (5?-CTGTGTCTT-
TGTCTGTGTGTA-3?). The cycling conditions were 94?C for 3 min, followed
by 35 cycles at 94?C, 64?C, 72?C for 30 s, with a final extension step at 72?C for
2 min. Reactions were run in a final volume of 15 ?L containing 10 ng of geno-
mic DNA, 0.2 mM each dNTP, 1 mM each primer, 0.046 mM of TaqStart Anti-
body (Clontech), 0.0016 mM of Taq DNA polymerase (Eppendorf), 1.5 mM
MgCl2, 75 mM KCl, and 10 mM Tris-HCl (pH 8.3). The P36 marker was typed
as previously reported by Karafet et al. (2002), with the exception that substitu-
tion was incorrectly described as GVA instead of GVT.
For the microsatellite analysis 10 STRs (DYS19, DYS388, DYS389I,
DYS389II, DYS390, DYS391, DYS392, DYS393, DYS426, and DYS439) were
typed in two multiplex PCR reactions. Primer sequences were published by
Kayser et al. (1997) and Redd, Roberts-Thomson et al. (2002), and PCR condi-
tions were given by Redd, Agellon et al. (2002). PCR products were electropho-
resed on a 3100 Genetic Analyzer (Applied Biosystems) using a 36-cm array
and filter set D. The data were analyzed with Genescan, version 3.7 (Applied
Biosystems), and Genotyper, version 1.1 (Applied Biosystems). For all statistical
analyses DYS389I was subtracted from DYS389II because the DYS389II PCR
product also contains DYS389I. SNP and STR frequency data are available on
request from T. Karafet.
some Consortium (2002) for naming Y-chromosome lineages. Capital letters
A–R identify the 18 major Y-chromosome clades or haplogroups. We use the
shorthand mutation-based naming system, which retains the major haplogroup
information (i.e., 19 capital letters) followed by the name of the terminal muta-
tion that defines a given haplogroup. Lineages not defined on the basis of a de-
rived character state represent interior nodes of the tree (paragroups) and are
distinguished from terminal haplogroups defined by the derived state at a particu-
lar marker by an asterisk. The term haplogroup rather than paragroup (Y Chro-
mosome Consortium 2002) is often used to refer to these internal nodes. When
no farther downstream markers in the latest version of the Y-chromosome tree
(Jobling and Tyler-Smith 2003) were typed for this study, we considered the most
derived typed marker to represent a haplogroup. As suggested by de Knijff
(2000), distinct Y chromosomes identified by STRs are designated as haplotypes.
We follow the conventions recommended by the Y Chromo-
ber, and three population pairwise genetic distances—absolute size difference
Y-chromosome STR diversity, variance in repeat num-
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Y-Chromosome DNA in Bali / 99
(Dad), Goldstein’s (1995) (??)2(Ddm), and distance based on shared alleles
(Dps)—were calculated using the software package Microsat 1.5d (Minch et al.
1997). Haplotypic distance matrices were used to reconstruct neighbor-joining
trees using the software package PHYLIP (Felsenstein 1995). Median-joining
networks (Bandelt et al. 1999) were constructed using the Network 2.0c program.
For network calculations STRs were weighted according to their repeat number
variances such that higher weights were assigned to the least variable loci. The
reduced median output was used as input for the median-joining network. This
procedure reduces the chances of obtaining large reticulations within the network
(Hurles et al. 2002). Two different coefficients of admixture, mC(Chakraborty et
al. 1992) and mR, a least-squares estimator (Roberts and Hiorns 1965), were
estimated by means of Admixture 1.0 (Bertorelle and Excoffier 1998).
In the Bali population we estimated the time to the most recent common
ancestors of particular lineages by means of the YMRCA program (Stumpf and
Goldstein 2001). For all STRs we used the mutation rate estimate 2.8?10?3
proposed by Kayser, Roewer et al. (2000) and its 95% confidence interval
(1.72?10?3to 4.27?10?3) with a generation time of 25 years.
To avoid complications arising from the analysis of paragroups, we com-
bined all descendant lineages of a given marker when comparing STR diversity
levels among populations. Occasionally, when the geographic distribution of de-
scendant haplogroups differed markedly from that of the ancestral paragroup, we
also calculated STR diversity on those lineages associated with the paragroup
only. This facilitated comparisons of ancestral variation among populations with
the assumption that there were no missing SNPs marking the included lineages.
In the case of median-joining networks, there is often a problem in visualizing
the results when many STRs and samples are included in the analysis. Therefore
in some analyses we present the results of networks for the paragroup only.
Results and Discussion
Table 1 reports the frequencies of 23 of the 44 lineages found in our survey
that were defined on the basis of 71 binary markers typed in 1,989 Y chromo-
somes from 20 populations, including 551 males from different parts of the
island of Bali. Figure 2 shows the evolutionary relationships among 55 haplogro-
ups resulting from typing 57 of the 71 markers used in this survey. Three lineages
within haplogroup O (O-M95, O-M122, and O-M119) account for 83.7% of the
Y chromosomes in our Balinese sample. Surprisingly, most of the remaining Y
chromosomes (accounting for 11.8% of the total) are members of clades H, J, L,
and R. These haplogroups are absent or present at low frequencies in southern
China, Southeast Asia, and Oceania (Table 1). In our survey, these haplogroups
are limited almost entirely to South Asia and/or the Near East. In the following
sections we present the results of phylogeographic analyses of these Balinese Y-
chromosome haplogroups and discuss implications of these results for hypothe-
ses on the peopling of Bali and the Indonesian region.
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Evolutionary tree for the 55 Y-chromosome lineages defined by 57 of the 71 markers
used in this survey. The names of the markers are shown along the branches of the tree,
and lineage names are shown on the right-hand side. Lineage names with an asterisk
refer to internal nodes of the tree, or paragroups (see ‘‘Subjects and Methods’’ section).
Haplogroups found in Bali are shown in boldface.
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Y-Chromosome DNA in Bali / 101
Austronesian Roots of the Balinese Population.
groups, O-M122 and O-M119, are widely distributed in Asia and are likely of
Asian origin. Several researchers have suggested that the distribution of these
haplogroups provides evidence for an Austronesian expansion from eastern Asia
into island Southeast Asia, Melanesia, and Polynesia (Su, Jin et al. 2000; Kayser,
Brauer et al. 2000; Kayser et al. 2001, 2003; Capelli et al. 2001; Hurles et al.
2002). Although there is general agreement that haplogroups O-M122 and O-
M119 trace the spread of agricultural technology, different source populations
for these lineages have been proposed by different investigators. Su and col-
leagues (Su et al. 1999; Su, Jin et al. 2000) postulated that southern Chinese
populations were the source of two independent migrations, one toward Taiwan
and the other toward Polynesia through insular Southeast Asia. In contrast, Ca-
pelli et al. (2001) and Hurles et al. (2002) found little support for an Austronesian
expansion originating in southeast China and Taiwan. They suggested that most
of present-day Austronesian speakers trace their paternal origins to Pleistocene
hunter-gatherers and that the dispersal of the Austronesian languages was mainly
a cultural process. Kayser and colleagues (Kayser, Brauer et al. 2000; Kayser et
al. 2001, 2003) support an intermediate scenario—that Polynesian ancestors did
indeed originate in mainland Asia and Taiwan. However, they argue that the
colonization of the Pacific was preceded by extensive admixture with indigenous
In our sample, 6.9% of Balinese men have Y chromosomes that are mem-
bers of haplogroup O-M122, which contains the subclades O-M134 and O-LINE
(Figure 2). The data presented here and elsewhere indicate that O-M122 is a
major Southeast Asian and Oceanian lineage that is absent or nearly absent in
the Near East and South Asia (Table 1) as well as in Central and North Asia
(Karafet et al. 2001). Here, we note that the distribution of O-M122* chromo-
somes (i.e., paragroup O-M122*) is also more widespread than chromosomes
with the derived state at the M134 and LINE-1 mutations (i.e., haplogroups O-
M134 and O-LINE-1). Haplogroups O-LINE1 and O-M134 are prevalent in
China (Su et al. 1999; Su, Jin et al. 2000; Su, Xiao et al. 2000; Santos et al. 2000;
Karafet et al. 2001), making up almost 50% of all sampled chromosomes. These
two haplogroups probably originated in China and subsequently migrated into
surrounding regions (Su, Xiao et al. 2000; Santos et al. 2000). Paragroup O-
M122* is found in East and Southeast Asia and in Oceania (Kayser, Brauer et
al. 2000; Kayser et al. 2001, 2003; Santos et al. 2000; Capelli et al. 2001). The
highest average STR heterozygosity on the O-M122 haplogroup (and O-M122*
paragroup) background is found in Southeast Asia, followed by southern China,
with lower diversity in Oceania (Table 2).
In our Balinese sample, 38 O-M122 individuals have 17 different STR
haplotypes. Within O-M122*, Y-chromosome STR sharing is observed mainly
within populations; however, the Balinese have one haplotype that is widely dis-
tributed among Austronesian speakers from other parts of Indonesia, the Philip-
pines, Taiwan, and parts of Oceania. There are too many O-M122 haplotypes to
Two Y-chromosome haplo-
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STR Diversity Associated with Y-Chromosome Haplogroup/Paragroup Lineages
Papua New Guineans
a. Not including Balinese samples.
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Y-Chromosome DNA in Bali / 103
construct a readable reduced median-joining network, so phylogenetic relation-
ships among O-M122* STR haplotypes are reconstructed in a neighbor-joining
tree based on absolute allele size distances (Figure 3). Three distinct clusters
were observed: Two clusters contain ‘‘Austronesian’’ Y chromosomes mainly
from island Southeast Asia (e.g., Malaysia, the Philippines, and aboriginal Tai-
wan) and Oceania, whereas the third cluster is distinguished by a preponderance
of haplotypes from mainland China and Vietnam. Most Balinese O-M122 Y
chromosomes (23 out of 32) and haplotypes (9 out of 13) are associated with the
first and second clusters. All three genetic distance methods reveal the closest
relationship between O-M122 haplotypes from Bali and the Philippines (data not
shown). The most plausible explanation for the combined data is that O-M122
lineages migrated to Indonesia and Bali from Southeast Asia through the Philip-
pines. Alternatively, our data could be viewed as a spread of Y chromosomes out
of Southeast Asia to Oceania and the Philippines by way of Indonesia.
Haplogroup O-M119, which has a similar geographic distribution as O-
M122 (Table 1), is another haplogroup that may have been brought to Bali by
migrating Austronesian speakers. This haplogroup is observed in 100 Balinese
individuals (18.1%) with 38 different STR haplotypes. The M119 marker has
drawn particular interest because chromosomes with the derived state are most
frequent among Taiwanese aboriginal groups (Su et al. 1999; Su, Jin et al. 2000;
Kayser, Brauer et al. 2000; Kayser et al. 2001, 2003; Santos et al. 2000; Capelli
et al. 2001; Karafet et al. 2001). Caution is advised in interpreting this to indicate
a Taiwanese origin for this mutation because genetic drift resulting from extreme
isolation and/or a founder effect may have increased the frequency of this haplo-
group in aboriginal Taiwanese. Evidence in support of this hypothesis comes
from the slightly reduced STR diversity associated with O-M119 chromosomes
in aboriginal Taiwanese compared with other populations (Table 2), despite their
high frequency (70.8%) in this population (Table 1). For example, Bali exhibits
the second highest frequency of O-M119 chromosomes (17.8%) in our survey;
however, the average variance in STR allele size on Balinese O-M119 chromo-
somes is almost twice as high at that on aboriginal Taiwanese O-M119 chromo-
somes (Table 2).
In contrast to the O-M122* haplogroup, a neighbor-joining tree for O-
M119* STR haplotypes (Figure 4) shows little if any geographic structure. O-
M119* chromosomes from Bali, China, and Indonesia are distributed throughout
the tree, although Taiwanese aboriginal chromosomes exhibit some clustering.
The absence of geographic structure may suggest a more ancient dispersal, sev-
eral migrations from different source populations, and/or continued gene flow
from Southeast Asia after an initial expansion of O-M119* lineages into this
region. O-M119* chromosomes might also represent a heterogeneous group of
not-yet-identified haplogroups. Additional markers within this lineage may allow
further resolution of the O-M119* network.
Interestingly, the O-M110 haplogroup (a descendant of O-M119; see Fig-
ure 2) is not found in China. In our survey its geographic distribution is restricted
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Phylogenetic relationships among O-M122* STR haplotypes. The neighbor-joining tree
was constructed using the PHYLIP program on the basis of absolute allele size distances
calculated with the computer program Microsat. The geographic origins of each individ-
ual with respect to the four major groupings in Figure 1 are indicated. SEAS, Southeast
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Y-Chromosome DNA in Bali / 105
Phylogenetic relationships among O-M119* STR haplotypes. The geographic origins of
each individual with respect to the four major groupings in Figure 1 are indicated.
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106 / karafet et al.
to Austronesian speakers of Taiwan, the Philippines, Indonesia, Bali, and Mel-
anesia. Su and colleagues (Su et al. 1999; Su, Jin et al. 2000) also found this
haplogroup in Southeast Asia and Micronesia. An STR-based age for chromo-
somes carrying the M110 mutation is approximately 3,420 years (95%
CI?2,245–5,570). This pattern raises the possibility that O-M110 chromo-
somes could have been brought to Bali along with O-M122* chromosomes by
way of the Philippines.
Gene Flow from the Indian Subcontinent.
within the H, J, L, and R clades are observed in Bali (see Figure 2). Altogether
these four major lineages account for 12% of Balinese Y chromosomes. Interest-
ingly, the H-M69*, H-M52, H-Apt, J-p12f*, J-M12, L-M20, R-M207*, and R-
M17 lineages are virtually absent in southern China, Southeast Asia, and Oceania
and are almost entirely restricted to the Indian subcontinent and the Near East
(Table 1). Two of these lineages, H-Apt and H-M69*, have been previously re-
ported to be limited to Indian populations (Pandya et al. 1998; Kivisild et al.
2003), whereas H-M52 and R-M207* have also been found in Central Asia,
albeit at low frequencies (Semino et al. 2000; Karafet et al. 2001; Wells et al.
Although the combined results of these surveys strongly support the hy-
pothesis of an Indian origin for these four lineages, it is more difficult to infer
the source(s) for the Balinese J-p12f*, J-M12, L-M20, and R-M17 lineages. In
our survey these chromosomes are found in both Indian and Near Eastern popula-
tions at relatively high frequencies. The most common L-M20 microsatellite hap-
lotype in Bali is also the most frequent haplotype among Indian L-M20
chromosomes, suggesting that these Balinese chromosomes may be of recent
Indian origin. Interestingly, the Balinese do not share identical J-p12f*, and R-
M17 STR haplotypes with either Indians or Near Easterners.
To assess whether Balinese J-p12f* and R-M17 chromosomes are more
likely to have originated in India or in the Near East, we compared modal haplo-
types for our samples from these regions. The Balinese modal J-p12f* haplotype
exhibits a difference of two steps from the Indian modal haplotype and seven
differences from the Near Eastern modal haplotype. With respect to R-M17, the
Balinese modal haplotype differs by one step from the Indian modal haplotype,
whereas two steps differentiate the Balinese and Near Eastern modal haplotypes.
We also calculated genetic distances and constructed phylogenetic trees
based on our Y-chromosome STR data. All three trees give broadly consistent
results: smaller genetic distances and closer genetic relationships among Balinese
and Indians than among Balinese and populations from the Near East (Figure 5).
It is also possible that some Balinese R-M17 chromosomes are of recent Euro-
pean origin, because this haplogroup is found at low frequencies in Western Eu-
rope (Hammer et al. 2001).
Eight different haplogroups
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Neighbor-joining networks depicting relationships among haplogroups (a) J, (b) L, and
(c) R-M17 in Balinese, South Asian (SAS), and Near Eastern (NEA) populations based
on absolute allele size distances estimated from 10 STR loci.
What Is the Origin of the Most Common Balinese Y-Chromosome Haplo-
Most Balinese males (58.6%) carry haplogroup O-M95. This haplo-
group shows a geographic distribution that is different from haplogroups O-
M122 and O-M119, and so its presence in Bali may not be explained solely on
the basis of Austronesian expansions. O-M95 is found at higher frequencies in
Southeast Asia (13.1%) than in southern China (11.7%) and so far has been
found in only two individuals from Oceania (see Table 1) (Su, Jin et al. 2000;
Capelli et al. 2001; Hurles et al. 2002; Kayser et al. 2003). The presence of O-
M95 was reported in Indian caste and tribal populations at low frequencies (Wells
et al. 2001); however, Ramana et al. (2001) recently found this haplogroup at
high frequencies in three tribal populations from South India (17–48%). In the
present survey we also find a relatively high frequency (22.4%) of this haplo-
group among tribal populations from southern India and an average frequency of
7.9% in our combined South Asian sample. There is a narrow range of average
STR heterozygosity values associated with the O-M95 haplogroup, with the high-
est value (0.392?0.024) in Southeast Asia and slightly lower values in southern
China and South Asia (0.367?0.015 and 0.332?0.021, respectively) (see
Table 2). Thus our data provide weak support for Kayser et al.’s (2003) hypothe-
sis that Southeast Asia was the original homeland of the O-M95 haplogroup,
because both the highest frequency of O-M95 and the greatest STR diversity are
found in Southeast Asia.
Given that the O-M95 haplogroup is present in both Southeast Asia and
the Indian subcontinent and considering that our data provide evidence of gene
flow from India to Bali, we can envisage three scenarios for how this haplogroup
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108 / karafet et al.
migrated to Bali. The most plausible explanation is that O-M95 was brought to
Bali by Austronesian speakers from Southeast Asia or the Philippines along with
O-M122 and/or O-M119. This scenario fits well with the estimated age of the
M95 mutation of 8,800 years (Kayser et al. 2003), the geographic distribution of
O-M95, and the inferred route of the Austronesian expansion. However, the vir-
tual absence of O-M95 chromosomes in Oceania may reflect a later entry of
haplogroup O-M95 to Indonesia and Bali from Southeast Asia (i.e., after the
initial colonization of the Pacific by Austronesian farmers). Alternatively, Indians
might have carried O-M95 chromosomes together with H, J, L, and R lineages.
This model seems less likely because of the high frequency of O-M95 on Bali,
the relatively high frequency of O-M95 chromosomes throughout Southeast
Asia, and their patchy distribution in India (i.e., concentrated in few tribal popu-
lations). Finally, O-M95 chromosomes may have arrived in Bali through separate
migrations from Southeast Asia and India.
We addressed these hypotheses by examining patterns of STR diversity
associated with our sample of O-M95 chromosomes. A reduced median-joining
network depicts geographic clustering of the southern Chinese haplotypes, with
an absence of similar structure for O-M95 haplotypes from Bali, India, Malaysia,
Vietnam, and other parts of Indonesia (data not shown). To explore the genetic
relationships among O-M95 chromosomes from Bali, Southeast Asia, and India,
we calculated genetic distances based on STR data and analyzed modal haplo-
types among different populations. Modal haplotypes for the Balinese and for
the combined Southeast Asian sample are identical, whereas there are two muta-
tional step differences from the Indian modal haplotype. Genetic distance estima-
tions reveal that the divergence between Balinese and Indian O-M95 haplotypes
is at least twice as great as the divergence between Balinese and Southeast Asian
chromosomes. Surprisingly, the Balinese share 10 O-M95 haplotypes with Indi-
ans, but only 4 haplotypes are shared between the Balinese and Southeast Asians.
These conflicting results may indicate that most O-M95 chromosomes sampled
from Bali derive from a Southeast Asian ancestor and that a few others descend
from recent migrants arriving in Bali from the Indian subcontinent (i.e., a two-
Traces of an Aboriginal Population of Balinese Hunter-Gatherers?
Haplogroup M was previously recognized as a predominant haplogroup in Mel-
anesia and New Guinea (Hammer et al. 2001; Kayser et al. 2001, 2003), with
some presence in eastern Indonesia, Polynesia, and Malaysia (Su, Jin et al. 2000;
Capelli et al. 2001; Karafet et al. 2001; Hurles et al. 2002). In the present survey,
haplogroup M chromosomes are also mainly restricted to eastern Indonesia and
Oceania, with a low frequency in Southeast Asia and Bali (Table 1). An STR-
based estimate of the coalescence time of M-M4 chromosomes is approximately
8,200 years (Kayser et al. 2003), whereas an approach based on SNPs yields an
age of the M4 mutation of approximately 12,700?7,200 years (Hammer and
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Y-Chromosome DNA in Bali / 109
Based on its higher haplotype diversity in Melanesia, Kayser et al. (2003)
proposed a Melanesian rather than an eastern Indonesian origin of the M4 muta-
tion before the Austronesian expansion. Haplogroup M-P34, defined by a newly
discovered polymorphism reported here, is also mainly an Oceanian haplogroup
(Table 1). It turns out that all the M chromosomes in Bali (0.7%) and eastern
Indonesia (12.7%) are haplogroup M-P34. Papua New Guineans exhibit the high-
est STR diversity and contain haplotypes that link M-P34 and M-M4 SNP haplo-
groups in median-joining networks (data not shown). Thus our data support the
hypothesis of a Papua New Guinean origin of the P34 mutation. An STR-based
estimate of the coalescence time for chromosomes carrying the P34 mutation is
approximately 5,350 years (95% CI?3,500–8,720). The presence of haplo-
group M-P34 in Bali and Indonesia may reflect a contribution from early Pleisto-
cene settlers before the Austronesian expansion, and/or relatively recent gene
flow from Papua New Guinea.
Three other lineages that may represent pre-Neolithic Balinese Y chromo-
somes are haplogroups C, K-M230, and K-M9*. Haplogroup K-M230 is the
major Y-chromosome lineage in Melanesia and New Guinea, and it also occurs
in other parts of Indonesia (Kayser et al. 2003) (see Table 1). Kayser et al. (2003)
proposed a Melanesian rather than an eastern Indonesian origin of this haplo-
group and suggested that the K-M230 mutation arose before the Austronesian
expansion about 8,200 years ago.
Chromosomes carrying the M9-G mutation are widely distributed across
Asia; however, chromosomes carrying the ancestral state at seven of the eight
downstream SNPs that mark immediate descendant lineages from M9 (K-M9*)
on the most recent Y-chromosome tree (Jobling and Tyler-Smith 2003) are found
at relatively high frequencies only in the Philippines, Indonesia, Melanesia,
Papua New Guinea, and Micronesia. Capelli et al. (2001) hypothesized that all
Y chromosomes carrying the M9-G marker initially expanded out of Melanesia.
If this is the case, the small proportion of K-M9* chromosomes (1.1%) in Bali
may be a signature of pre-Neolithic settlements. In contrast to M-P34 and
K-M230, the distribution of K-M9* chromosomes is not restricted to Oceania.
They are also present in Malaysia and the Near East, albeit at low frequencies.
To test the possibility that Balinese K-M9* chromosomes were carried by
people from the Near East and/or Southeast Asia, we constructed a Y-chromo-
some STR network for this paragroup (data not shown). Three haplotypes ob-
served in Bali form a tight cluster that is closely affiliated with chromosomes
from Indonesia, Melanesia, Micronesia, and Papua New Guinea. The lowest ge-
netic distances are found between the Balinese and Papua New Guineans. Similar
to haplogroups M-P34 and K-M230, K-M9* chromosomes in Bali and Indonesia
most likely represent a pre-Neolithic contribution before the Austronesian expan-
Contrary to the situation for the K-M9*, K-M230, and M-P34 haplogroups,
three STR haplotypes associated with C* chromosomes in Bali form a tight clus-
ter that is connected to neighboring haplotypes from western Indonesia and East
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110 / karafet et al.
Asia. Compared with other haplogroups analyzed, C* has a low diversity in Bali.
The occurrence of C* chromosomes in Bali most probably reflects recent gene
flow to Bali.
The observed frequencies of K-M9*, K-M230, and M-P34 on Bali suggest
that 2.2% of the pre-Neolithic gene pool survived the invasion of Austronesian
Y chromosomes. Interestingly, a similar extent of replacement is evident in Java
(3.8%), and a slightly higher proportion of pre-Neolithic Y chromosomes is ob-
served in Borneo (15.0%) (Kayser et al. 2003). A similar analysis of our sample
of eastern Indonesians indicates major pre-Neolithic (78.2%) and minor Aus-
tronesian (21.8%) components of their paternal gene pool (Table 1).
This study was intended to compare the composition of the Balinese pater-
nal gene pool with those of its Asian neighbors to infer the relative contributions
of pre-Neolithic hunter-gatherer and Austronesian farmer Y chromosomes and to
test the hypothesis of recent gene flow from India. At least two paternal lineages
(O-M122 and O-M119) seem to trace the Austronesian expansion to Bali. Our
estimate of the coalescence times of these haplogroups on Bali—4,400 years
(95% CI?2,900–7,200) and 5,630 years (95% CI?3,700–9,170), respec-
tively—are older than archeological dates. This is not surprising, because both
haplogroups arose outside Bali, and early migrants to Bali most likely carried
diverse Y chromosomes within these haplogroups. Time estimates of these haplo-
groups have overlapping confidence intervals, suggesting that both O-M122 and
O-M119 chromosomes may represent a Y-chromosome signal of the earliest
Austronesian expansion. However, our data based on median-joining networks,
neighbor-joining trees, and genetic distances suggest that several expansion
waves of Austronesian groups may have reached Bali by different routes. Al-
though haplogroup O-M95 was probably brought by one of the Austronesian
migration waves, the data suggest that a subset of these chromosomes may have
entered Bali more recently from the Indian subcontinent. The influence of the
Austronesian expansion on the preexisting hunter-gatherer gene pool appears to
be substantial. The spread of these three haplogroups to Bali has nearly erased
the signature of the ancestral Y-chromosome pool.
We also assessed the possible influence of three more recent historical
events on the composition of the Balinese gene pool: a period of Indianization
characterized by the spread of the Hindu religion and culture to Bali, the expan-
sion of Islam to Indonesia, and the persistence of the Dutch empire on Bali for
almost 100 years. Although we do not find evidence for a significant West Asian
or Dutch contribution to the Balinese paternal gene pool, solid evidence for an
Indian contribution comes from the presence of multiple Indian-specific haplo-
groups on Bali. An estimate of the Balinese frequency of these Indian haplo-
groups (about 12%) provides a direct measure of the Indian contribution, whereas
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Y-Chromosome DNA in Bali / 111
admixture methods suggest that the total contribution of Indian Y chromosomes
to the Balinese gene pool might be as high as 19% (data not shown). Although
we cannot define how long Indian haplogroups have persisted on Bali, it is worth
noting that three of these lineages (J-12f*, R-M17, and R-M207*) reveal rela-
tively high average STR diversity (i.e., h?0.308, 0.279, and 0.281, respec-
tively), comparable with that seen in the major Balinese haplogroup, O-M95.
Coalescence time estimates of the Indian haplogroups on Bali vary from
2,600 to 3,100 years. As expected, these dates are older than the archeological
evidence for the earliest Balinese Indicized kingdoms (late first millennium a.d.);
however, they are consistent with archeological evidence for the earliest trade
contacts with India (Ardika and Bellwood 1991). Supporting evidence for 2,000-
year-old contact with India comes from an analysis of ancient mtDNA (Lansing
et al. 2004). Although there is no evidence of Indian Y chromosomes in our
eastern Indonesian sample, it is possible that a small number of Indian Y chromo-
somes are present in other Indonesian populations. However, it is not possible to
confirm this until larger sample sizes (Table 1) and/or appropriate markers are
typed (Kayser et al. 2003).
The discovery that about 12% of Balinese haplogroups are of relatively
recent Indian origin and that these haplogroups are rare or absent in neighboring
Indonesian islands should prompt a thorough re-examination of the archeological
evidence for contact between India and Bali. The genetic evidence we have pre-
sented suggests that the magnitude of such trade and other cultural contacts be-
tween India and Bali was much greater than has hitherto been imagined (Lansing
Biocomplexity Program (through grant BCS 0083524 awarded to J. S. Lansing and M. F.
Hammer) and by the National Science Foundation (through grants SBR-9514733, SBR-
9512178, and SBR-9818215 awarded to L. B. Jorde). Research in Indonesia was carried
out under the auspices of the Balai Pengkajian Teknologi Pertanian, Denpasar, Bali, with
the kind support and assistance of its director, Dr. Suprapto. We wish to express our
gratitude to Wayan Ardika of Udayana University; to the staff of the Balai Purbakala,
Bali, and its director, Ayu Kusumawati; and to the Lembaga Ilmu Pengetahuan Indonesia.
We thank Svetlana Reznikova, Christine Ponder, Rupesh Amin, Amit Indap, Jennifer Gul-
ick, and Veronica Contreras for excellent technical assistance.
This research was supported by the National Science Foundation’s
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