Genome Res. 13:1600-1606, 2003
©2003 by Cold Spring Harbor Laboratory Press; ISSN 1088-9051/03 $5.00
Letter
Mitochondrial Genome Variation and Evolutionary History of Australian and New Guinean Aborigines
Max Ingman1 and
Ulf Gyllensten
Department of Genetics and Pathology, Section of Medical Genetics,
Rudbeck Laboratory, University of Uppsala, S-751 85 Uppsala, Sweden
 |
ABSTRACT
|
|---|
To study the evolutionary history of the Australian and New Guinean
indigenous peoples, we analyzed 101 complete mitochondrial genomes including
populations from Australia and New Guinea as well as from Africa, India,
Europe, Asia, Melanesia, and Polynesia. The genetic diversity of the
Australian mitochondrial sequences is remarkably high and is similar to that
found across Asia. This is in contrast to the pattern seen in previously
described Y-chromosome data where an Australia-specific haplotype was found at
high frequency. The mitochondrial genome data indicate that Australia was
colonized between 40 and 70 thousand years ago, either by a single migration
from a heterogeneous source population or by multiple movements of smaller
groups occurring over a period of time. Some Australian and New Guinea
sequences form clades, suggesting the possibility of a joint colonization
and/or admixture between the two regions.
The continent of Australia has been separate from Asia since the late
Cretaceous, approximately 70 million years ago. However, lower sea levels
during the upper Pleistocene merged the Malay Peninsula with Sumatra, Java,
Borneo, and Bali to form what is generally known as "Sunda Land".
At the same time, mainland Australia, Tasmania, and New Guinea were joined
into a single landmass, called "Sahul Land"
(Fig. 1). Although Sunda and
Sahul have remained separate during the period of modern human evolution and
migration, sea distances connecting them would have been reduced to several
island hops of between 30 and 90 km (Klein
1989 ). Because Australia and New Guinea were joined from before
the time of human colonization until about 8000 years ago
(Bellwood 1978a), it is
possible that the indigenous peoples of these regions result from the same
migration. A date for initial human settlement of the Australian continent of
10,000 years ago was defendable as recently as the mid-1960s
(Klein 1989). Through the
re-dating of the Lake Mungo skeletal remains
(Thorne et al. 1999;
Bowler et al. 2003) and as a
result of several other studies (Roberts et al.
1990,
1994,
2001), a date of
40,000–60,000 years ago is now generally accepted. The only estimate of
a genetic coalescent for Australian Aborigines with individuals from outside
Australia is based on mitochondrial HVS1 sequences and ranges from
60,000–119,000 years ago, depending on which substitution rate is used
(van Holst Pellekaan et al.
1998). In addition, an expansion date of 51,000–85,000 years
ago for Australian Aborigines was estimated from mitochondrial D-loop
sequences (Redd and Stoneking
1999). Mitochondrial DNA has proven to be a useful tool in
studying the evolutionary history of human populations through key
characteristics such as high copy number, lack of recombination
(Olivio et al. 1983;
Ingman et al. 2000), high
substitution rate (Brown et al.
1979), and maternal mode of inheritance
(Giles et al. 1980). Although
the mitochondrial D-loop offers a convenient source of polymorphic data, it
also has a high incidence of parallel mutations
(Tamura and Nei 1993;
Ingman and Gyllensten 2001)
and mutation "hotspots"
(Wakeley 1993). Previous
studies of sequence variation in the coding region of the mitochondrial
genomes of Australian Aborigines have been restricted to Restriction Fragment
Length Polymorphism (RFLP) data (Cann et
al. 1987; Stoneking et al.
1990; Huoponen et al.
2001). Analyses based on the information content of the entire
mitochondrial genome sequence may provide novel insight into the evolutionary
history of Australia.
View larger version (23K):
[in this window]
[in a new window]
|
Figure 1 Map of Southeast Asia, Australia, and Melanesia. The predicted extent of
late Pleistocene coastline is indicated in light grey. 1, New Ireland; 2, New
Britain; 3, Bougainville (Solomon chain); 4, Fiji; 5, Samoa; 6, Tonga; 7, Cook
Islands; 8, Hawaiian Islands; 9, New Zealand; 10, Easter Island ( 3,000 km
to the east).
|
|
|
RESULTS
|
|---|
Sequence Data
To study the evolutionary history of the Australian and New Guinean
indigenous peoples, we analyzed a total of 101 complete mitochondrial genomes
from various populations including Australian Aborigines (n = 20 from
Northern Territory populations of Darwin, Alice Springs, Katherine, Tennant
Creek, Groote Eylandte) and New Guinean aborigines (n = 10 from
coastal, n = 11 from highland), as well as from the peoples of
Africa, India, Europe, Asia, Melanesia, and Polynesia (n = 60). The
Australian samples were selected to represent a broad range of locations
within the Northern Territory. The New Guinea samples were selected on the
basis of previous mitochondrial typing to represent a wide range of genetic
variation within highland and coastal populations. All 101 complete mtDNA
sequences are unique and vary in length from 16,557–16,575 bp. The 101
complete sequences contain 940 variable sites (741 in the coding region; 199
in the D-loop) of which 438 are parsimony-informative (321 in the coding
region; 117 in the D-loop). The mean pairwise distance between complete human
mtDNA genomes is 3.18x10-3 substitutions per site.
Phylogenetic Analysis
Because the pattern of nucleotide substitution in the mitochondrial D-loop
is characterized by a high frequency of homoplasy
(Ingman and Gyllensten 2001),
we first compared the topology of a neighbor joining (NJ) tree
(Saitou and Nei 1987)
reconstructed from the 101 complete mitochondrial sequences (tree not shown)
with a tree reconstructed using just the coding region sequences
(Fig. 2). Although the
topologies of the two trees were essentially the same, the tree of sequences
with the D-loop removed showed generally higher bootstrap values. For this
reason, in studying the phylogenetic relationships among the mitochondrial
lineages, we focused solely on the coding region. In the NJ tree, non-African
sequences are present on two major branches
(Fig. 2, labeled
"1" and "2"). Branch 1 and branch 2 are delineated by
the nucleotide positions 8701, 9540, 10398, 10400, 10873, 14783, 15043, and
15301 relative to the Cambridge reference sequence (CRS;
Anderson et al. 1981),
consistent with what are sometimes referred to as haplogroups N (branch 1) and
M (branch 2). All but one of the Australian sequences are found on branch 1,
together with all European sequences, more than half of the New Guinean
sequences, all of the Polynesian sequences, and several Asian sequences. On
branch 1 there are several examples where sequences that come from the same
geographic region form monophyletic groups, such as a group of sequences
predominantly from the New Guinea highlands
(Fig. 2, labeled
"1b") and another group comprising the European sequences.
Additionally, of the sequences on this branch from the New Guinea coast, all
but one cluster with the Polynesian sequences
(Fig. 2, labeled
"1a"). Of the 20 Australian sequences, the 19 that are found on
branch 1 are represented on 10 separate subbranches.
Based on an estimated substitution rate for the mitochondrial coding region
of 1.7x10-8 substitutions per site per year
(Ingman et al. 2000) and the
deepest genetic divergence within branch 1, the sequences on branch 1 coalesce
71,000±12,000 years ago. The coalescence time for sequences on branch 2
is 78,000±12,000 years ago.
Mitochondrial Diversity
Notably, Australia and New Guinea have high nucleotide diversity across the
complete mitochondrial genome ( = 2.26x10-3 and
2.42x10-3 respectively) and mean pairwise sequence difference
(MPSD) (k = 37.4 and 40.0 respectively), similar to that found across Asia
( = 2.36x10-3, k = 39.0). The variation in the Australian
and New Guinean coding region sequences shows a comparable pattern but with
nucleotide diversity a little lower than that found across Asia
(Table 1). The frequency
distribution of pairwise differences for the Australian mtDNA coding region
sequences shows a bell-shaped rather than ragged pattern
(Fig. 3A), indicating that
coalescence events for these sequences occur in a relatively restricted time
range which is often associated with population growth
(Slatkin and Hudson 1991;
Rogers and Harpending 1992).
This is a deviation from previously reported mismatch distributions based on
D-loop sequences from other hunter gatherer populations, that tend to show a
ragged pattern consistent with constant population size
(Watson et al. 1996). The
pairwise mismatch distribution for the New Guinean sequences shows a more
ragged pattern (Fig. 3B). The
bimodal distribution could be due to the sequences from the New Guinean
population evenly split on branch 1 and branch 2. In this case, the frequency
distribution will reflect that about half of the sequences are separated by
the maximum time possible for non-African sequences
(Slatkin and Hudson 1991).
Tests of selective neutrality based on the number of segregating sites and
nucleotide diversity can be used to test whether population sizes have
remained stable or have experienced a period of growth
(Fu and Li 1989;
Tajima 1989). The Australian
coding region sequences show evidence of a period of population expansion
(Tajima's D = -2.23, P < 0.01; Fu and Li's D = -2.91, P
< 0.02), whereas no indication of population expansion is seen among the
sequences from New Guinea (Tajima's D = -1.42, P > 0.1; Fu and
Li's D = -2.11, P > 0.05). Sequences from only the New Guinea
coast (Tajima's D = -0.52, P > 0.1; Fu and Li's D = -1.02,
P > 0.1) and from only the New Guinea highlands (Tajima's D =
-1.12, P > 0.1; Fu and Li's D = -1.10, P > 0.1) also
show no evidence of expansion.
View this table:
[in this window]
[in a new window]
|
Table 1. Numbers of Sequences (n), Segregating Sites (S), Nucleotide Diversity
(), and Average Number of Nucleotide Differences (k) for Various Subsets
of Complete Mitochondrial Sequences (Including the D-Loop) and the Coding
Region Alone
|
|
View larger version (18K):
[in this window]
[in a new window]
|
Figure 3 Pairwise mismatch distribution (bars) and the distribution expected under
constant population size (line) for Australian coding region sequences
(A) and New Guinean coding region sequences (B).
|
|
New Guinea and Polynesia
The New Guinean sequences are found in three major clades and share two
minor clades with Australian Aboriginal sequences. Two of these major clades
are present on branch 1 (labeled "1a" and "1b") and
are more closely related to the majority of Australian sequences than they are
to the New Guinean sequences in the third major clade
(Fig. 2, labeled
"2a"). Group 1a (Fig.
2) contains sequences from the New Guinea coast and the Polynesian
islands of Samoa, Cook Islands, and Tonga. Based on coalescence calculations,
these sequences are estimated to have a common ancestor 11,000±4000
years ago. In addition to branching support (bootstrap = 98), all sequences in
group 1a carry a 9-bp deletion. This deletion is also present in the Korean
sequence with which the lineages in this group share their evolutionary
history. Located in the intergenic region between the COII gene and the Lysine
tRNA gene, this deletion has been previously associated with Polynesian and
Southeast Asian populations (Redd et al.
1995). Another well supported clade is formed by sequences from
both coastal and highland New Guinea and one Nasioi from the Melanesian island
of Bougainville (bootstrap = 98; Fig.
2, labeled "2a"). The sequences on this clade coalesce
45,000±9000 years ago, calculated from the deepest genetic split.
Finally, group 1b (Fig. 2)
consists of sequences from both coastal and highland regions of New Guinea,
and this group has a coalescence time of 36,000±8000 years ago.
Colonization of Sahul
Most lineages in Australia and New Guinea do not show a relationship
indicative of co-colonization or gene flow, but two clades on branch 1, both
of three sequences, contain sequences from both Australia and New Guinea
(Fig. 2, marked
"1c" and "1d"). These groups of sequences last shared
common ancestors approximately 46,000±9000 ("1c") and
31,000±8000 ("1d") years ago. Interestingly, in both cases
the New Guinean sequences derive from individuals sampled from the highland
areas.
Although the number of individuals studied from each location is limited,
we also estimated the population divergence in the mitochondrial coding
region. The average number of nucleotide differences between populations
(dxy) indicates that on average the sequences from New Guinea are
somewhat more closely related to those from Australia (dxy =
0.00175±0.00015) than either of these populations are to the Asian
sequences (dxy = 0.00183±0.00014, P < 0.01) and
dxy = 0.00189±0.00015, P < 0.01, respectively).
Also, the sequences from the New Guinea highlands are on average more closely
related to the Australian sequences than those from the New Guinea coast
(dxy = 0.00170±0.00018 and dxy =
0.00181±0.00022, respectively P < 0.01).
|
DISCUSSION
|
|---|
High Mitochondrial Genome Diversity
Our study of complete mitochondrial genomes reveals high diversity within
Australian and New Guinean populations. This is consistent with analyses that
previously reported on diversity in the mitochondrial D-loop of Australian
Aborigine and New Guinea highland populations. A study of HVS1 found that
Australian Aborigines from a riverine population tend to have higher MPSD than
that of the African! Kung population (van
Holst Pellekaan et al. 1998). Another analysis of mitochondrial
D-loop sequences also reported high nucleotide diversity in Australia, but
lower than the values found in Asian and New Guinea highland populations
(Redd and Stoneking 1999).
High nucleotide diversity, paraphyletic tree topology, and a bell-shaped
mismatch distribution are indicators of a large number of singleton-nucleotide
differences between sequences, which is often attributed to exponential
population growth in a panmictic population
(Slatkin and Hudson 1991). The
time at which the populations expanded can be estimated from the data. An
estimate of Tau ( = 20.849) for the Australian sequences corresponds to a
population expansion about 40,000 years ago. However, if the sequences to be
compared are drawn from unrelated populations, the distribution of pairwise
differences can mimic the expected distribution under population expansion.
Consequently, the pattern of sequence differences among the Australian
mitochondrial lineages could also reflect that they have been subdivided into
a number of groups. This may be the result of isolation before, or soon after,
their arrival in Sahul. Genetic isolation of tribal groups corroborates a
conclusion based on analyses of mitochondrial DNA variation in an Aboriginal
Australian population from the Northern Territory
(Huoponen et al. 2001).
Effective population size of the Australian Aboriginal population may have
been reduced by an imbalanced male/female ratio ranging from 1.3–2.6
(Birdsell 1993). With a small
effective population size, genetic drift would be of substantial influence
within the tribe. Also, the great majority of marriages were contracted within
the tribe, making the tribe an essentially endogamous genetic unit
(Birdsell 1993). The proposed
genetic separation among Aboriginal populations could have occurred after a
single large population movement to Australia or as the result of multiple
migrations over the course of generations from a heterogeneous source
population.
Contrasting History of Australian Mitochondrial DNA and
Y-Chromosomes
Our analysis shows a striking difference between the genetic history of
females and the reported history of males in the Australian Aboriginal
population. As noted previously, the mitochondrial diversity in Australia is
relatively high. The pattern seen in the Y-chromosome is different in that an
Australia-specific haplotype (DYS390.1del/RPS4Y711T) is found in about 50% of
males in Australia (Kayser et al.
2001; Redd et al.
2002). Relatively high genetic diversity for the mitochondrial
genome can be attributed to a high substitution rate
(Brown et al. 1979) and to the
predominance of patrilocality in human populations
(Burton et al. 1996;
Seielstad et al. 1998;
Oota et al. 2001). In
addition, although polygyny was not the norm in Australian aborigines, around
15% of males in the desert areas, and a higher percentage on Australia's
northern coast, have been reported to have multiple wives
(Birdsell 1993), further
reducing the number of Y-chromosomes in the population. However, the smaller
effective population size among females would allow genetic drift to act
strongly within tribes, homogenizing the tribal mitochondrial gene pool.
Therefore, the high mitochondrial diversity noted in the present study could
be due to our sampling across subpopulations rather than within a single
tribe. Kayser et al. (2001)
proposed that the high frequency of a unique haplotype in Australia is the
result of a population expansion that started from a few hundred individuals.
In this case, the predominance of a unique Y-chromosome haplotype in Australia
would be the result of a founder effect. However, there does not appear to be
a corresponding loss of genetic diversity resulting from a bottleneck seen
among mitochondrial lineages.
Polynesian and Melanesian Lineages
The number of individuals included in this study from Polynesian and
Melanesian populations is not sufficient to address the genetic history of
these populations in any detail. However, the position of certain lineages or
groups in the phylogenetic tree is interesting in relation to previous
propositions regarding these populations. For instance, we note that group 1a
contains sequences from the New Guinea coast as well as from the Polynesian
islands of Samoa, Cook Islands, and Tonga. About 6000 years ago, an expansion
among Neolithic farmers in southern China and Taiwan brought the Austronesian
group of languages south and east to New Guinea. During the last
3000–4000 years, these Austronesian speakers have subsequently dispersed
throughout the Pacific; first to Fiji, then to Tonga and Samoa, and finally to
the Hawaiian Islands, Easter Island, and New Zealand
(Fig. 1; Bellwood
1978a,
1991). The timeframe for this
colonization has been dated from the spread of Lapita pottery from Melanesia
to Polynesia (Bellwood 1978b;
Diamond 1988). We note that
the sequence composition of group 1a and the estimated time to its common
ancestor roughly fits with both the timeframe and population history of this
migration.
Relationship Between Australian and New Guinean Mitochondrial
Lineages
Because genetic divergence precedes population divergence, the coalescence
date for branch 1 indicates that modern humans must have arrived on the
Australian continent less than 70,000 years ago. Also, we would expect that
Australia was colonized prior to the time of the expansion of Australian
lineages at 40,000 years ago. Although these time estimates are approximate,
we note that they are in general agreement with thermoluminescence dates of
50,000–60,000 years ago from two human occupation sites in northern
Australia (Roberts et al.
1990,
1994) and one in the
southeastern region of Australia (Thorne
et al. 1999; Bowler et al.
2003), and by animal extinctions across the continent about 46,000
years ago (Roberts et al.
2001).
Archaeological evidence indicates that humans were present in New Guinea at
least 40,000 years ago (Groube et al.
1986), at which time it was still joined with Australia. Our data
show that some Australian sequences do share a closer ancestry with some New
Guinean sequences than they do with other sequences on branch 1. In addition,
dxy distances indicate that New Guinean and Australian sequences
are more closely related to each other than either are to the Asian sequences.
This may suggest that Australia and New Guinea were colonized jointly or that,
if not, these populations have admixed since colonization. Previous studies
have yielded differing results with respect to the question of a common
genetic origin of these populations. Joint colonization is suggested by a
study of mitochondrial D-loop sequence variation
(van Holst Pellekaan et al.
1998), mitochondrial RFLP data
(Huoponen et al. 2001), and an
analysis of  -globulin haplotypes
(Roberts-Thomson et al. 1996).
Other analyses of mitochondrial D-loop sequences
(Redd and Stoneking 1999),
mitochondrial RFLPdata (Stoneking et al.
1990), and Y-chromosome data
(Kayser et al. 2001) have
suggested separate origins for the Australian and New Guinean indigenous
peoples. Our mitochondrial data imply that some lineages from the populations
of Australia and New Guinea have shared a common history since the initial
colonization of Sahul. This is compatible with alternative scenarios involving
either a common colonization of both areas from a heterogeneous source
population or independent colonization events and subsequent gene flow. The
comparison between the mitochondrial and Y-chromosome data in some of the
other populations examined is also of interest. The possibility of multiple
migrations to New Guinea, as indicated by the mitochondrial data, may also
explain the presence of Y-chromosome haplotypes in Melanesian populations that
are absent in Australia (Kayser et al.
2001). The lack of a common Y-chromosome haplotype found both in
Australia and in the New Guinea highlands (or in any other Melanesian
population) argues against the concept that the New Guinean and Australian
populations are derived from the same migration event
(Kayser et al. 2001). However,
the Australia-specific Y-chromosome haplotype could have arisen after the
colonization of Sahul and therefore is absent in other populations.
The overall distant relationship between mitochondrial sequences
contributes to the difficulty in decisively resolving the evolutionary history
of the Australian and New Guinean highland populations. The observed
contemporary genetic differences between the Australian and New Guinean
populations may also be compounded by the action of a combination of genetic
drift, selection, and complex population movements. An extended investigation
of mitochondrial genome diversity in other regions of Australia as well as
other populations in the region, based on a larger number of individuals, may
provide a better understanding of the genetic history of these populations.
For instance, a genetic similarity has been noted between Australian
Aborigines and individuals from the Indian Subcontinent based on Y-chromosome
(Redd et al. 2002),
mitochondrial D-loop (Redd and Stoneking
1999), and phenotypic (Birdsell
1993) data. Our mitochondrial data show no clear similarity
between Australian Aborigines and the three southern Indian sequences
examined, although a detailed examination of this hypothesis would require the
analysis of additional individuals from the Indian Subcontinent. Nevertheless,
mitochondrial DNA only provides information on the genetic history of females,
and given the contrast between the mitochondrial DNA and the Y-chromosome
patterns, it appears that additional studies of autosomal loci are also
necessary to obtain a balanced view of the evolutionary history of the peoples
in this region.
|
METHODS
|
|---|
PCR Primers and Sequencing
The primers used for PCR amplification were as described
(Rieder et al. 1998).
Sequencing was performed on the PCR products directly using BigDye Primer
(Applied Biosystems) chemistry. Separation of sequencing ladders was performed
on an ABI 3700 instrument. Both forward and reverse strands were sequenced.
Sequence analysis was performed using Sequencing Analysis 3.6.1 (Applied
Biosystems), and sequence alignment was made with Sequencher 4.1.2 (Gene
Codes). For a detailed description of complete mitochondrial genome sequencing
methods, see Ingman and Gyllensten
(2001).
Genetic Analysis
Genetic distances between sequences were calculated by MEGA version 2.1
(Kumar et al. 2001) using the
Kimura two-parameter model for nucleotide substitution
(Kimura 1980). Phylogenetic
trees were reconstructed with Paup4.0b10 (Sinauer Associates). Estimations of
genetic diversity and tests for selective neutrality were performed with DnaSP
version 3.53 (Rozas and Rozas
1999). Estimations of mean genetic distance between populations
were made by DnaSP version 3.53 (Rozas and
Rozas 1999) using Jukes and Cantor's substitution model
(Jukes and Cantor 1969). To
compare the between-population distances, we employed a Mann-Whitney test to
analyze pairwise distance data obtained using Paup4.0b10 using the Kimura
two-parameter model for nucleotide substitution.
Accession Numbers
The chimpanzee sequence (Accession no. D38113
[GenBank]
) we used as an outgroup was
obtained from GenBank, as were 49 complete human mitochondrial sequences
generated for one of our previous studies
(Ingman et al. 2000; Accession
nos. AF346963
[GenBank]
–AF346983, AF346985
[GenBank]
–AF347000,
AF347002
[GenBank]
–AF347011, AF347014
[GenBank]
–AF347015). The remaining 52 sequences
were sequenced for this study and are deposited in GenBank (Accession nos.
AY289051
[GenBank]
–AY289102). All sequences are also available at
http://www.genpat.uu.se/mtDB.
|
Acknowledgements
|
|---|
We thank M. Stoneking and J. Kuhl for DNA samples, and M. Stoneking and J.
Kijas for valuable comments on an earlier version of this manuscript. This
research was supported by a grant from the Swedish Natural Sciences Research
Council.
The publication costs of this article were defrayed in part by payment of
page charges. This article must therefore be hereby marked
"advertisement" in accordance with 18 USC section 1734 solely to
indicate this fact.
|
Footnotes
|
|---|
Article and publication are at
http://www.genome.org/cgi/doi/10.1101/gr.686603.
1 Corresponding author.
E-MAIL
max.ingman{at}genpat.uu.se;
FAX 46 (18) 471-4931. 
[The sequence data from this study have been submitted to GenBank under
accession nos. AY289051
[GenBank]
–AY289102. The following individuals kindly
provided reagents, samples, or unpublished information as indicated in the
paper: M. Stoneking and J. Kuhl.]
|
REFERENCES
|
|---|
Anderson, S., Bankier, A.T., Barrell, B.G., de Bruijn, M.H.,
Coulson, A.R., Drouin, J., Eperon, I.C., Nierlich, D.P., Roe, B.A., Sanger,
F., et al. 1981. Sequence and organization of the human
mitochondrial genome. Nature
290:
457-465.[CrossRef][Medline]
Bellwood, P. 1978a. Man's conquest of the
Pacific: The prehistory of Southeast Asia and Oceania. Oxford
University Press, New York.
Bellwood, P. 1978b. The Polynesians:
Prehistory of an island people. Thames and Hudson Ltd.,
London.
Bellwood, P. 1991. The Austronesian dispersal and the
origin of languages. Sci. Am.
265: 70-75.
Birdsell, J.B. 1993. Microevolutionary
patterns in Aboriginal Australia: A gradient analysis of clines.
Oxford University Press, New York.
Bowler, J.M., Johnston, H., Olley, J.M., Prescott, J.R., Roberts,
R.G., Shawcross, W., and Spooner, N.A. 2003. New ages for human
occupation and climatic change at Lake Mungo, Australia.
Nature 421:
837-840.
Brown, W.M., George Jr., M., and Wilson, A.C. 1979.
Rapid evolution of animal mitochondrial DNA. Proc. Natl. Acad.
Sci. 76:
1967-1971.[Abstract/Free Full Text]
Burton, M.L., Moore, C.C., Whiting, J.W.M., and Romney, A.K.
1996. Regions based on social structure. Curr.
Anthropol. 37:
87-123.[CrossRef]
Cann, R.L., Stoneking, M., and Wilson, A.C. 1987.
Mitochondrial DNA and human evolution. Nature
325: 31-36.
Diamond, J. 1988. Express train to Polynesia.
Nature 336:
307-308.[CrossRef]
Fu, Y.X. and Li, W.H. 1989. Statistical tests of
neutrality of mutations. Genetics
133:
693-709.
Giles, R.E., Blanc, H., Cann, H.M., and Wallace, D.C.
1980. Maternal inheritance of human mitochondrial DNA.
Proc. Natl. Acad. Sci.
77:
6715-6719.[Abstract/Free Full Text]
Groube, L., Chappell, J., Muke, J., and Price, D.
1986. A 40,000 year-old human occupation site at Huon Peninsula,
Papua New Guinea. Nature
324:
453-455.[CrossRef][Medline]
Huoponen, K., Schurr, T.G., Chen, Y., and Wallace, D.C.
2001. Mitochondrial DNA variation in an aboriginal Australian
population: Evidence for genetic isolation and regional differentiation.
Hum. Immunol. 62:
954-969.[CrossRef][Medline]
Ingman, M. and Gyllensten, U. 2001. Analysis of the
complete human mtDNA genome: Methodology and inferences for human evolution.
J. Hered. 92:
454-461.[Abstract/Free Full Text]
Ingman, M., Kaessmann, H., Paabo, S., and Gyllensten, U.
2000. Mitochondrial genome variation and the origin of modern
humans. Nature 408:
708-713.[CrossRef][Medline]
Jukes, T.H. and Cantor, C.R. 1969. Evolution of
protein molecules. In Mammalian protein metabolism
(ed. H.N. Munro). Academic Press, New York.
Kayser, M., Brauer, S., Weiss, G., Schiefenhovel, W., Underhill,
P.A., and Stoneking, M. 2001. Independent histories of human Y
chromosomes from Melanesia and Australia. Am. J. Hum.
Genet. 68:
173-190.[CrossRef][Medline]
Kimura, M. 1980. A simple method for estimating
evolutionary rates of base substitutions through comparative studies of
nucleotide sequences. J. Mol. Evol.
16:
111-120.[CrossRef][Medline]
Klein, R.G. 1989. The human career: Human
biological and cultural origins. University of Chicago Press,
Chicago.
Kumar, S., Tamura, K., Jakobsen, I.B., and Nei, M.
2001. MEGA2: Molecular evolutionary genetics analysis software.
Arizona State University, Tempe, AZ.
Olivio, P.D., Van de Walle, M.J., Laipis, P.J., and Hauswirth, W.W.
1983. Nucleotide sequence evidence for rapid genotypic shifts in
the bovine mitochondrial DNA D-loop. Nature
306:
400-402.[CrossRef][Medline]
Oota, H., Settheetham-Ishida, W., Tiwawech, D., Ishida, T., and
Stoneking, M. 2001. Human mtDNA and Y-chromosome variation is
correlated with matrilocal versus patrilocal residence. Nat.
Genet. 29:
20-21.[CrossRef][Medline]
Redd, A.J. and Stoneking, M. 1999. Peopling of Sahul:
mtDNA variation in aboriginal Australian and Papua New Guinean populations.
Am. J. Hum. Genet. 65:
808-828.[CrossRef][Medline]
Redd, A.J., Takezaki, N., Sherry, S.T., McGarvey, S.T., Sofro,
A.S., and Stoneking, M. 1995. Evolutionary history of the
COII/tRNALys intergenic 9 base pair deletion in human mitochondrial DNAs from
the Pacific. Mol. Biol. Evol.
12:
604-615.[Abstract]
Redd, A.J., Roberts-Thomson, J., Karafet, T., Bamshad, M., Jorde,
L.B., Naidu, J.M., Walsh, B., and Hammer, M.F. 2002. Gene flow
from the Indian subcontinent to Australia: Evidence from the Y chromosome.
Curr. Biol. 12:
673-677.[CrossRef][Medline]
Rieder, M.J., Taylor, S.L., Tobe, V.O., and Nickerson, D.A.
1998. Automating the identification of DNA variations using
quality-based fluorescence resequencing: Analysis of the human mitochondrial
genome. Nucleic Acids Res.
26:
967-973.[Abstract/Free Full Text]
Roberts, R.G., Jones, R., and Smith, M.A. 1990.
Thermoluminescence dating of a 50,000-year old human occupation site in
northern Australia. Nature
345:
153-156.[CrossRef]
Roberts, R.G., Jones, R., Spooner, N.A., Head, M.J., Murray, A.S.,
and Smith. M.A. 1994. The human colonization of Australia:
Optical dates of 53,000 and 60,000 years bracket human arrival at Deaf Adder
Gorge, Northern Territory. Quaternary Sci. Rev.
13:
575-586.[CrossRef]
Roberts, R.G., Flannery, T.F., Ayliffe, L.K., Yoshida, H., Olley,
J.M., Prideaux, G.J., Laslett, G.M., Baynes, A., Smith, M.A., Jones, R., et
al. 2001. New ages for the last Australian megafauna:
Continent-wide extinction about 46,000 years ago.
Science 292:
1888-1892.[Abstract/Free Full Text]
Roberts-Thomson, J.M., Martinson, J.J., Norwich, J.T., Harding,
R.M., Clegg, J.B., and Boettcher, B. 1996. An ancient common
origin of aboriginal Australians and New Guinea highlanders is supported by
-globin haplotype analysis. Am. J. Hum. Genet.
58:
1017-1024.[Medline]
Rogers, A.R. and Harpending, H. 1992. Population
growth makes waves in the distribution of pairwise genetic differences.
Mol. Biol. Evol. 9:
552-569.[Abstract]
Rozas, J. and Rozas, R. 1999. DnaSP version 3: An
integrated program for molecular population genetics and molecular evolution
analysis. Bioinformatics
15:
174-175.[Abstract/Free Full Text]
Saitou, N. and Nei, M. 1987. The neighbor-joining
method: A new method for reconstructing phylogenetic trees. Mol.
Biol. Evol. 4:
406-425.[Abstract]
Seielstad, M.T., Minch, E., and Cavalli-Sforza, L.L.
1998. Genetic evidence for a higher female migration rate in
humans. Nat. Genet. 20:
278-280.[CrossRef][Medline]
Slatkin, M. and Hudson, R.R. 1991. Pairwise
comparisons of mitochondrial DNA sequences in stable and exponentially growing
populations. Genetics
129:
555-562.[Abstract]
Stoneking, M., Jorde, L.B., Bhatia, K., and Wilson, A.C.
1990. Geographic variation in human mitochondrial DNA from Papua
New Guinea. Genetics
124:
717-733.[Abstract]
Tajima, F. 1989. Statistical method for testing the
neutral mutation hypothesis by DNA polymorphism.
Genetics 123:
585-595.[Abstract/Free Full Text]
Tamura, K. and Nei, M. 1993. Estimation of the number
of nucleotide substitutions in the D-loop of mitochondrial DNA in humans and
chimpanzees. Mol. Biol. Evol.
10:
512-526.[Abstract]
Thorne, A., Grun, R., Mortimer, G., Spooner, N.A., Simpson, J.J.,
McCulloch, M., Taylor, L., and Curnoe, D. 1999. Australia's
oldest human remains: Age of the Lake Mungo 3 skeleton. J. Hum.
Evol. 36:
591-612.[CrossRef][Medline]
van Holst Pellekaan, S., Frommer, M., Sved, J., and Boettcher, B.
1998. Mitochondrial control-region sequence variation in
aboriginal Australians. Am. J. Hum. Genet.
62:
435-449.[CrossRef][Medline]
Wakeley, J. 1993. Substitution rate variation among
sites in hypervariable region 1 of human mitochondrial DNA. J. Mol.
Evol. 37:
613-623.[Medline]
Watson, E., Bauer, K., Aman, R., Weiss, G., von Haeseler, A., and
Paabo, S. 1996. mtDNA sequence diversity in Africa.
Am. J. Hum. Genet. 59:
437-444.[Medline]
Received August 2, 2002;
accepted in revised format April 23, 2003.
 CiteULike  Connotea  Del.icio.us  Digg  Reddit  Technorati What's this?
This article has been cited by other articles:
|
|
|
|
 
P. Soares, J. A. Trejaut, J.-H. Loo, C. Hill, M. Mormina, C.-L. Lee, Y.-M. Chen, G. Hudjashov, P. Forster, V. Macaulay, et al.
Climate Change and Postglacial Human Dispersals in Southeast Asia
Mol. Biol. Evol.,
June 1, 2008;
25(6):
1209 - 1218.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Q. D. Atkinson, R. D. Gray, and A. J. Drummond
mtDNA Variation Predicts Population Size in Humans and Reveals a Major Southern Asian Chapter in Human Prehistory
Mol. Biol. Evol.,
February 1, 2008;
25(2):
468 - 474.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Meyer, U. Stenzel, S. Myles, K. Prufer, and M. Hofreiter
Targeted high-throughput sequencing of tagged nucleic acid samples
Nucleic Acids Res.,
August 1, 2007;
(2007)
gkm566v1.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. W. Carter
Mitochondrial diversity within modern human populations
Nucleic Acids Res.,
May 25, 2007;
35(9):
3039 - 3045.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. Hudjashov, T. Kivisild, P. A. Underhill, P. Endicott, J. J. Sanchez, A. A. Lin, P. Shen, P. Oefner, C. Renfrew, R. Villems, et al.
Revealing the prehistoric settlement of Australia by Y chromosome and mtDNA analysis
PNAS,
May 22, 2007;
104(21):
8726 - 8730.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. K. Gonder, H. M. Mortensen, F. A. Reed, A. de Sousa, and S. A. Tishkoff
Whole-mtDNA Genome Sequence Analysis of Ancient African Lineages
Mol. Biol. Evol.,
March 1, 2007;
24(3):
757 - 768.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. J. Pierson, R. Martinez-Arias, B. R. Holland, N. J. Gemmell, M. E. Hurles, and D. Penny
Deciphering Past Human Population Movements in Oceania: Provably Optimal Trees of 127 mtDNA Genomes
Mol. Biol. Evol.,
October 1, 2006;
23(10):
1966 - 1975.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
L. Scheinfeldt, F. Friedlaender, J. Friedlaender, K. Latham, G. Koki, T. Karafet, M. Hammer, and J. Lorenz
Unexpected NRY Chromosome Variation in Northern Island Melanesia
Mol. Biol. Evol.,
August 1, 2006;
23(8):
1628 - 1641.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Q.-P. Kong, H.-J. Bandelt, C. Sun, Y.-G. Yao, A. Salas, A. Achilli, C.-Y. Wang, L. Zhong, C.-L. Zhu, S.-F. Wu, et al.
Updating the East Asian mtDNA phylogeny: a prerequisite for the identification of pathogenic mutations
Hum. Mol. Genet.,
July 1, 2006;
15(13):
2076 - 2086.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. Sun, Q.-P. Kong, M. g. Palanichamy, S. Agrawal, H.-J. Bandelt, Y.-G. Yao, F. Khan, C.-L. Zhu, T. K. Chaudhuri, and Y.-P. Zhang
The Dazzling Array of Basal Branches in the mtDNA Macrohaplogroup M from India as Inferred from Complete Genomes
Mol. Biol. Evol.,
March 1, 2006;
23(3):
683 - 690.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. Galtier, D. Enard, Y. Radondy, E. Bazin, and K. Belkhir
Mutation hot spots in mammalian mitochondrial DNA
Genome Res.,
February 1, 2006;
16(2):
215 - 222.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Kivisild, P. Shen, D. P. Wall, B. Do, R. Sung, K. Davis, G. Passarino, P. A. Underhill, C. Scharfe, A. Torroni, et al.
The Role of Selection in the Evolution of Human Mitochondrial Genomes
Genetics,
January 1, 2006;
172(1):
373 - 387.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Friedlaender, T. Schurr, F. Gentz, G. Koki, F. Friedlaender, G. Horvat, P. Babb, S. Cerchio, F. Kaestle, M. Schanfield, et al.
Expanding Southwest Pacific Mitochondrial Haplogroups P and Q
Mol. Biol. Evol.,
June 1, 2005;
22(6):
1506 - 1517.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. Macaulay, C. Hill, A. Achilli, C. Rengo, D. Clarke, W. Meehan, J. Blackburn, O. Semino, R. Scozzari, F. Cruciani, et al.
Single, Rapid Coastal Settlement of Asia Revealed by Analysis of Complete Mitochondrial Genomes
Science,
May 13, 2005;
308(5724):
1034 - 1036.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Pavesi
Utility of JC polyomavirus in tracing the pattern of human migrations dating to prehistoric times
J. Gen. Virol.,
May 1, 2005;
86(5):
1315 - 1326.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Tanaka, V. M. Cabrera, A. M. Gonzalez, J. M. Larruga, T. Takeyasu, N. Fuku, L.-J. Guo, R. Hirose, Y. Fujita, M. Kurata, et al.
Mitochondrial Genome Variation in Eastern Asia and the Peopling of Japan
Genome Res.,
October 1, 2004;
14(10a):
1832 - 1850.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
![[Feedback]](/icons/banner/feedbackACT.gif){kind=icon}
![[For Subscribers]](/icons/banner/subscriberACT.gif){kind=icon}
![[Archive]](/icons/banner/archiveACT.gif){kind=icon}
![[Search]](/icons/banner/searchACT.gif){kind=icon}
![[Contents]](/icons/banner/tocACT.gif){kind=icon}
Top
ABSTRACT
RESULTS