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ARTICLE
Human genetics of the Kula Ring: Y-chromosome
and mitochondrial DNA variation in the Massim
of Papua New Guinea
Mannis van Oven1, Silke Brauer2,5, Ying Choi1, Joe Ensing3, Wulf Schiefenho
¨vel4, Mark Stoneking*,2
and Manfred Kayser*,1
The island region at the southeastern-most tip of New Guinea and its inhabitants known as Massim are well known for a unique
traditional inter-island trading system, called Kula or Kula Ring. To characterize the Massim genetically, and to evaluate the
influence of the Kula Ring on patterns of human genetic variation, we analyzed paternally inherited Y-chromosome (NRY) and
maternally inherited mitochondrial (mt) DNA polymorphisms in 4400 individuals from this region. We found that the nearly
exclusively Austronesian-speaking Massim people harbor genetic ancestry components of both Asian (AS) and Near Oceanian
(NO) origin, with a proportionally larger NO NRY component versus a larger AS mtDNA component. This is similar to previous
observations in other Austronesian-speaking populations from Near and Remote Oceania and suggests sex-biased genetic
admixture between Asians and Near Oceanians before the occupation of Remote Oceania, in line with the Slow Boat from Asia
hypothesis on the expansion of Austronesians into the Pacific. Contrary to linguistic expectations, Rossel Islanders, the only
Papuan speakers of the Massim, showed a lower amount of NO genetic ancestry than their Austronesian-speaking Massim
neighbors. For the islands traditionally involved in the Kula Ring, a significant correlation between inter-island travelling
distances and genetic distances was observed for mtDNA, but not for NRY, suggesting more male- than female-mediated gene
flow. As traditionally only males take part in the Kula voyages, this finding may indicate a genetic signature of the Kula Ring,
serving as another example of how cultural tradition has shaped human genetic diversity.
European Journal of Human Genetics (2014) 22, 1393–1403; doi:10.1038/ejhg.2014.38; published online 12 March 2014
INTRODUCTION
Oceania represents a vast geographic area with a complex human
settlement history.1,2 Previous studies have addressed human genetic
variation in Oceania, particularly Polynesia,3–8 mainland New
Guinea9–13 and Island Melanesia.14–18 One area of Near Oceania
(NO) yet understudied from a human genetic perspective is the island
region off the southeastern tip of New Guinea (Figure 1). Adminis-
tratively designated the Milne Bay Province of Papua New Guinea
(PNG), this area encompasses the D’Entrecasteaux Islands (ie,
Normanby, Fergusson, Dobu and Goodenough), the Trobriand
Islands, the Woodlark group (ie, Gawa, Woodlark and the Laughlan
Islands), the Louisiade Archipelago (ie, Misima, Sudest, Rossel and
the islands of the Calvados chain), as well as a portion of the nearby
PNG mainland. The inhabitants of this region have been designated
as Massim,19–21 a term that has since been used to refer not only to
the people but also to the geocultural region inhabited by them.22
From the many islands of the Massim, only the Trobriand Islands
were included in previous human genetic studies4,7,11,16,23 Hence, a
human genetic description of the Massim is lacking so far, despite the
major attention they have received in the cultural anthropology
literature, in particular with respect to the Kula, a traditional
inter-island trading system described in more detail below.
Human settlement of mainland New Guinea goes back at least
40–50 thousand years: the Ivane Valley in eastern PNG was occupied
43–49 thousand years ago (kya).24 The Solomon Islands (ie, the
archipelago east of the Milne Bay area) were occupied by at least
28 kya.25 Archeological findings in the Massim are scant26 and there is
currently no evidence of long-term human occupation before
2kya.
27,28 Given the lower sea levels during the Pleistocene, many
of the current Massim islands may have been connected by land
bridges,29 potentially facilitating human migration between them. The
languages spoken in the Massim belong to the Papuan Tip cluster
within the Western Oceanic branch of the Austronesian language
family,30 with the exception of Rossel Island, the easternmost island of
the Louisiade Archipelago, where a non-Austronesian (Papuan)
language is spoken.31
Among a number of the islands in the Milne Bay Province an
extensive trading system, referred to as Kula or Ku la Ri ng has
traditionally developed.32–37 This Kula exchange system was
extensively described by anthropologist Bronislaw Malinowski in his
1Department of Forensic Molecular Biology, Erasmus MC University Medical Center Rotterdam, Rotterdam, The Netherlands; 2Department of Evolutionary Genetics, Max Planck
Institute for Evolutionary Anthropology, Leipzig, Germany; 3Missionaries of the Sacred Heart (MSC), St. Paul’s Pastoral Centre, Hagita, Alotau, Papua New Guinea; 4Human
Ethology Group, Max Planck Institute for Ornithology, Andechs, Germany
*Correspondence: Professor M Kayser, Department of Forensic Molecular Biology, Erasmus MC University Medical Center Rotterdam, 3000 CA Rotterdam, The Netherlands.
Tel : þ31 10 7038073; Fax: þ31 10 7044575; E-mail: m.kayser@erasmusmc.nl
or Professor M Stoneking, Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, D-04103 Leipzig, Germany. Tel: þ49 341 3550502;
Fax: þ49 341 3550555; E-mail: stoneking@eva.mpg.de
5Current address: Netherlands Forensic Institute, The Hague, The Netherlands.
Received 1 November 2013; revised 6 February 2014; accepted 13 February 2014; published online 12 March 2014
European Journal of Human Genetics (2014) 22, 1393–1403
&
2014 Macmillan Publishers Limited All rights reserved 1018-4813/14
www.nature.com/ejhg
classic work ‘Argonauts of the western Pacific’33 and has since become
an oft-cited anthropological example of balanced reciprocity. This
particular trading system assures that items only available on some
islands, for instance, because of unequal geographic distribution of
natural resources, but vitally needed on other islands, are shared
among people from different islands. The Kula is centered around the
exchange of two valuables in a ring-like manner: necklaces, called
soulava, are moved in clockwise direction through the island world,
whereas armshells, called mwali,dosointheoppositedirection
(Figure 1). Notably, only men participate in the Kula; they sail to fixed
trading partners on other Kula islands and it is not uncommon for
them to stay away from home for several months. The islands of the
southeastern Massim are not extensively involved in the Kula. Only
Misima is sometimes mentioned as a Kula partner, but trading with
Misima is probably much less intense as compared with the northern
and western Massim.35,38
The presence of the Kula trading system, involving regular
migrations between islands with lengthy stays away from home, raises
the question whether besides the economic exchange also genetic
exchange takes place. If the male-specific migration of the Kula indeed
left detectable signatures in the genomes of the contemporary
populations from the region, this should be evident by studying the
paternally inherited non-recombining portion of the Y-chromosome
(NRY), in comparison with the maternally inherited mitochondrial
(mt) DNA. If true, the Kula would serve as another example of the
impact of human culture on genetic variation as has been observed
before, for example, for residence patterns39 and social stratification.40
Furthermore, it is of interest to investigate to what extent
the inhabitants of Rossel Island, given that they are the only
non-Austronesian (ie, Papuan) speakers of the Massim, differ
genetically from the other, Austronesian-speaking people of the
Massim, in particular their direct neighbors from Sudest. Although
human contacts between Rossel and Sudest certainly existed—
geographic distance between the two islands is small and sea-crossing
from one to the other is feasible—the Rossel society has been
described as endogamous,41 suggesting limited or no genetic
exchange with Sudest, a situation that could have promoted genetic
divergence between the two populations.
With these questions in mind, we analyzed NRY and mtDNA
polymorphisms in individuals from across the Massim area
(Figure 1). In reconstructing the demographic history of Oceania,
our results not only fill an important gap between previous genetic
studies on the mainland of New Guinea in the west,9–13 the Bismarck
Archipelago in the north14–16 and the Solomon Islands in the east,17,18
but also provide further insights into how human culture impacts on
human genetics.
MATERIALS AND METHODS
Samples
The sampling consisted of over 400 individuals from various locations within
the Milne Bay Province, PNG, as well as from two nearby coastal communities
from Collingwood Bay, Oro Province, PNG (Figure 1). Samples were collected
in 2001 (by MK, JE and WS) under approval of the Medical Board of PNG and
with support from the Diocese of Alotau, PNG (Missionaries of the Sacred
Heart, MSC), particularly then Bishop Desmond Moore MSC. Volunteers,
with individual written informed consent, provided a saliva sample and were
asked to give information regarding the origins of their parents and grand-
parents. Genetic work carried out within this study was additionally approved
Figure 1 Map of the Massim area within Oceania depicting the locations of the 14 groups studied. Groups that participate in the Kula traditional trading
system are indicated with filled black dots, whereas groups that do not are indicated with open dots; groups marginally involved in the Kula are indicated
with half-filled dots. Arrows indicate trading interactions between Kula partners with approximate travelling distances given in km.
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by the Ethics Commission of the University of Leipzig Medical Faculty and the
Medical Ethics Committee of the Erasmus MC University Medical Center
Rotterdam.
Each sample was assigned to one of the following 14 population groups
according to their matrilineal (maternal grandmother’s or mother’s) geographic
origin for mtDNA analyses, and male samples according to their patrilineal
(paternal grandfather’s or father’s) geographic origin for NRY analyses:
(1) Trobriand Islands; (2) Gawa; (3) Woodlark (also known as Muyuw);
(4) Laughlan Islands (also known as Budibudi Islands); (5) Fergusson (also
known as Moratau), including a few individuals from nearby Dobu (also
known as Watoa) and Goodenough (also known as Nidula); (6) Normanby
(also known as Duau); (7) Milne Bay mainland eastern tip; (8) Misima,
including some individuals from nearby Paneati, Panapompom and Kimuta;
(9) western Calvados Chain (including: Motorina, Bagaman, Utian or Brooker
Island, and Panaumala) ; (10) eastern Calvados Chain (including: Dadahai,
Kuanak or Abaga Gaheia Island, Nimoa, Panatinane or Joannet Island,
Panawina, Sabarl, and Wanim or Grass Island); (11) Sudest (also known as
Vanatinai or Tagula); (12) Rossel (also known as Yela); (13) Wanigela and
nearby settlements; and (14) Airara and nearby settlements. In case two
sampled individuals were closely related in the male and/or female line (by
sharing the same father/paternal grandfather and/or mother/maternal grand-
mother), one of them was excluded from the NRY and/or mtDNA data set,
respectively. The Trobriand Islands group was supplemented with the Trobriand
samples described in previous studies.7,16,18 The final Massim set comprised 389
individuals for NRY analyses and 432 individuals for mtDNA analyses.
For comparisons in a wider geographic context, we included previously
described population data from East Asia, Island Southeast Asia, and Near and
Remote Oceania, using a minimal sample size of 20 individuals per population
for both NRY and mtDNA7,10,16,18,42,43 (for an overview, see Supplementary
Table S1).
Genotyping
DNA was extracted from cheek swabs via a previously described salting-out
protocol.44 Haplogroup-defining single-nucleotide polymorphisms on the
non-recombining part of the Y-chromosome (Y-SNPs) were typed by
multiplex genotyping assays (details available in Supplementary Table S2)
based on the single-base primer extension principle (SNaPshot; Applied
Biosystems, Foster City, CA, USA). NRY short tandem repeats (Y-STRs) were
genotyped with the AmpFlSTR Yfiler Kit (Applied Biosystems) following the
manufacturer’s recommendations. The first hypervariable segment (HVS-I;
sequence range: nps 16024–16392) of the mtDNA genome was sequenced
as described previously.7Presence of the mtDNA 9-bp deletion
(m.8281_8289del), characteristic for haplogroup B, was determined by PCR
as described elsewhere.7Samples for which the mtDNA haplogroup could not
be unambiguously deduced from combined HVS-I and 9-bp deletion
data, were SNaPshot genotyped for additional, haplogroup-defining
mtDNA polymorphisms by applying the multiplex SNP assays described in
Ballantyne et al.45 The 432 HVS-I sequences of the Massim samples reported in
this study have been deposited in NCBI GenBank under accession numbers
KF034102–KF034533.
Data analysis
NRY haplogroups were assigned based on the classification tree provided in
Supplementary Table S3, following Karafet et al.46 (with the exception of
the placement of marker M83). MtDNA haplogroups were inferred according
to the classification tree provided in Supplementary Table S4, following Build
15 of the mtDNA phylogeny available at http://www.phylotree.org.47 For
analyses at the mtDNA HVS-I level, nps 16180–16183 were disregarded
because A to C transversions at these positions are dependent on the presence
of m.16189T4C. For analyses at the Y-STR level, the following 10 loci were
used: DYS19, DYS389I, DYS390, DYS391, DYS392, DYS393, DYS437, DYS438,
DYS448 and Y-GATA-H4, following van Oven et al.43 Measures of genetic
diversity, genetic distance (FST/RST/FST), analysis of molecular variance
(AMOVA) and Mantel tests were calculated using Arlequin version 3.5
(Excoffier and Lischer48). Multidimensional scaling (MDS) plots were
generated using the PROXSCAL algorithm49 implemented in SPSS version
20 (IBM, Armonk, NY, USA). Median-joining haplotype networks50 were
constructed using the software Network version 4.6.1.0 (Fluxus Technology
Ltd, Clare, Suffolk, UK), applying equal weighting for mtDNA sites and the
following weighting scheme for Y-STR loci: DYS19 (3), DYS389I (3), DYS390
(3), DYS391 (3), DYS392 (6), DYS393 (4), DYS437 (4), DYS438 (6), DYS448
(4) and Y-GATA-H4 (3).
Table 1 Observed NRY haplogroup frequencies (%) in the Massim area
Population n C-RPS4Y*aC-M208*aK-M9*aM-M4*aM-P34*aM-M104*aM-P117aS-M230*aS-M254*aO-M119*bO-M110bO-M122*bO-M324*b
Collingwood Bay
WAN 21 9.5 90.5
AIR 32 3.1 28.1 28.1 12.5 21.9 3.1 3.1
Western Massim
FER 35 17.1 37.1 17.1 2.9 2.9 17.1 5.7
NOR 27 3.7 40.7 22.2 14.8 7.4 11.1
MET 24 4.2 41.7 25.0 4.2 4.2 4.2 16.7
Northern Massim
TRO 60 10.0 25.0 1.7 26.7 11.7 16.7 8.3
GAW 10 20.0 2 0.0 10.0 10.0 40.0
WOO 13 7.7 38.5 7.7 30.8 15.4
LAU 5 20.0 40.0 20.0 20.0
Southeastern Massim
MIS 1 4 14.3 64.3 14.3 7.1
WCA 19 26.3 42.1 5.3 5.3 10.5 10.5
ECA 11 36.4 36.4 18.2 9. 1
SUD 38 36.8 39.5 2.6 15.8 2.6 2.6
ROS 80 33.8 6.3 30.0 1.3 28.8
Abbreviations: AIR, Airara; ECA, eastern Calvados; FER, Fergusson; GAW, Gawa; LAU, Laughlan Islands; MET, mainland eastern tip; MIS, Misima; NOR, Normanby; ROS, Rossel; SUD, Sudest;
TRO, Trobriand Islands; WAN, Wanigela; WCA, western Calvados; WOO, Woodlark.
aAssigned a Near Oceanian origin following Kayser M2and Kayser et al.7,16
bAssigned an Asian origin following Kayser M2and Kayser et al.7,16
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RESULTS AND DISCUSSION
NRY and mtDNA haplogroups in the Massim
In total, 13 NRY haplo-/paragroups were detected, all falling within
the major clades C, M, S, O and K* (Table 1). In particular, seven
haplo-/paragroups encompass the bulk (97.7%) of NRY diversity
(Figure 2a). Y-haplogroups O-M119*(xM110), O-M110 and
O-M324*(xM7,M134) are of Asian/Austronesian (AS) origin, whereas
haplogroups C-M208*(xP33,P54), M-P34*(xM83) and S-M254*(xM226)
Figure 2 Geographic distribution of (a) the seven major Y-chromosome haplogroups and (b) the nine major mtDNA haplogroups observed in the Massim area
(see Tables 1 and 2 for complete haplogroup frequency data). For comparison, the gross frequencies of these haplogroups as observed in other regions of
Asia/Oceania, pooled from different population samples, are included as well using previously published data.7,10,16,18,42 For practical reasons, the PNG
Highlands group includes Kapuna, a Papuan-speaking group from the Gulf Province of PNG with an assumed origin in the highlands, while the PNG Coast
group includes Bereina, an Austronesian-speaking group from the southern coastal area of PNG.
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are of NO origin, as previously described.7,16 The K-M9*
(xP79,M4,M353,P117,M214,M74,M230) paragroup is particularly
frequent in the Massim (overall: 33.4%) and probably includes
several yet undefined sublineages of K-M9. A Y-STR haplotype
network analysis for K-M9* (Supplementary Figure S1) indeed
showed that its haplotypes are quite diverse. Given that K-M9*
was not found in East Asia and only sporadically in Southeast Asia
in our data set, whereas it is rather frequent in parts of NO such as
in the Admiralty Islands (27.0%), a NO origin for the Massim
K-M9* Y-chromosomes observed here seems most likely. NRY
haplogroups were not homogeneously distributed throughout the
Massim (Figure 2a). The NO haplogroup M-P34* and the AS
haplogroup O-M324* were more prominent in the northern and
western Massim, whereas the NO haplogroup S-M254* was more
frequent in the southeastern Massim. Furthermore, Rossel stood
out from its local neighbors because of its high frequency of AS
haplogroup O-M110 and complete absence of NO haplogroup
C-M208*. The Wanigela group from the Collingwood Bay showed
a remarkably low haplogroup diversity (Supplementary Table S5)
with over 90% belonging to M-P34*.
We distinguished 12 different mtDNA haplo-/paragroups in the
Massim, all falling within the mtDNA clades P, Q, E, B4, B5, F and
R23 (Table 2). In particular, nine haplo-/paragroups accounted
for 96.5% of the mtDNA pool (Figure 2b). Haplogroups F1a,
B4-16261*(xB4a1a1a) and B4a1a1a (also known as the ‘Polynesian
motif’) are of (ultimate) AS origin,51,52 although B4a1a1a may also
have originated in descendants of East Asians residing in Nusa
Te n g g ar a 53–55 or in the Bismarck Archipelago.8Haplogroups
E*(xE2) and E2 are likely of Taiwanese/Island Southeast AS origin56
(here also classified as AS), whereas haplogroups P*(xP1), P1, Q1 and
Q2 have a NO origin.57 Like the NRY haplogroups, also the mtDNA
haplogroups were not homogeneously distributed throughout the
Massim (Figure 2b). NO haplogroup P1 was much more frequent in
the southeastern Massim, while AS haplogroup B4-16261* was almost
absent there, and NO haplogroups Q1 and Q2 were almost only
found in the western Massim. Rossel again stood out from its local
neighbors, because of its major component of AS haplogroup E* and
low frequency of NO haplogroup P*. Interestingly, Sudest showed a
relatively high frequency of the AS haplogroup F1a, which was
otherwise only detected sporadically (single individuals) in the eastern
Calvados and in Gawa but not in any of the other Massim groups
studied. The presence of haplogroup R23 in a single individual from
the western Calvados was unexpected, as this haplogroup has so far
only been observed much more westward in Nusa Tenggara58 and
among Cham from Vietnam.59
AS versus NO genetic ancestry in the Massim
To quantify the relative contributions of NO versus AS paternal and
maternal ancestors to the gene pool of the Massim people, we
assigned, based on previous knowledge, the most probable ancestral
origin to each of the observed NRY and mtDNA haplogroups
(Table 3). Overall, the proportion of AS mtDNA haplogroups in
the Massim (52.3%) was more than two times higher than that of AS
NRY haplogroups (23.9%). Such an excess of AS mtDNAs compared
with AS Y-chromosomes was previously also observed in Admiralty
Islanders north of the PNG mainland (60.7% AS mtDNA versus
18.2% AS NRY),16 in Solomon Islanders (excluding Polynesian
outliers; 77.7% AS mtDNA versus 27.5% AS NRY)18 and in
Polynesians from Remote Oceania (96.4% AS mtDNA versus 34.6%
AS NRY).7,16 This pattern is consistent with a historical admixture
scenario that involved mainly AS women and mainly NO men in NO,
perhaps the Bismarck Archipelago, before the occupation of Remote
Oceania, in line with the previously suggested Slow Boat from Asia
hypothesis of Polynesian origin in particular and the Austronesian
origin in general.4,7,16,60 Within the Massim, the people from the
northern islands carried the highest amount of AS ancestry, while
relatively low amounts of AS ancestry were seen in the southeastern
Massim. However, the non-Austronesian-speaking Rossel Islanders
Table 2 Observed mtDNA haplogroup frequencies (%) in the Massim area
Population n Q*aQ1aQ2aP*aP1aB4*bB4-16261*bB4a1a1abB5bbF1abE*bE2bR23b
Collingwood Bay
Wanigela 23 4.3 34.8 8.7 26.1 4.3 21.7
Airara 25 4.0 24.0 32.0 24.0 4.0 12.0
Western Massim
Fergusson 45 6.7 6.7 20.0 6.7 4.4 8.9 37.8 2.2 2.2 4.4
Normanby 22 4.5 27.3 4.5 63.6
Mainland eastern tip 31 3.2 19.4 3.2 9.7 9.7 12.9 29.0 3.2 9.7
Northern Massim
Trobriand Islands 47 6.4 2.1 23.4 4.3 25.5 27.7 10.6
Gawa 16 37.5 37.5 12.5 6.3 6.3
Woodlark 19 10.5 36.8 26.3 26.3
Laughlan Islands 6 16.7 16.7 16.7 16.7 33.3
Southeastern Massim
Misima 18 27.8 55.6 16.7
Western Calvados 14 28.6 35.7 28.6 7.1
Eastern Calvados 17 58.8 29.4 5.9 5.9
Sudest 39 48.7 12.8 7.7 2.6 28.2
Rossel 110 5.5 35.5 6.4 46.4 6.4
aAssigned a Near Oceanian origin following Kayser M2and Friedlaender et al.57
bAssigned an Asian origin following Kayser M2; Friedlaender et al 51; Trejaut et al52; Soares et al 56;Hillet al 58 and Peng et al.59
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formed an exception, showing a larger AS proportion both for NRY
and mtDNA than their direct Austronesian-speaking neighbors, a
finding that contradicts the expectation based on linguistics (for more
details on Rossel see below).
Massim genetic population substructure and the Kula
Genetic distances between the Massim groups calculated from NRY
and mtDNA haplogroup/haplotype data (Supplementary Table S6)
were visualized in MDS plots (Figure 3). Wanigela appears as a strong
outlier in both NRY-based plots, which can be explained by its
exceptionally high frequency of haplogroup M-P34* and the complete
lack of AS NRY haplogroups. Airara takes an outlier position only in
the Y-STR-based plot, but not in the NRY-haplogroup-based plot,
which can be explained by the fact that Airara’s K-M9* Y-STR
haplotypes are quite distinct from the K-M9* haplotypes in other
Massim groups (Supplementary Figure S1). In contrast, neither
Wanigela nor Airara are outliers in the mtDNA-based plots. Both
groups come from the coast of mainland PNG (Collingwood Bay), on
the border with the Massim area, and were included in this study
because Goodenough, one of the islands in the western Massim, is
visible from Collingwood Bay, and therefore people from Wanigela
and Airara may be involved in admixture processes with the Massim.
Moreover, archeology has revealed the presence of prehistoric pottery
in the Trobriand Islands that originated from the Collingwood
Bay61,62 (modern pottery in the Trobriands comes mostly from the
Amphlett Islands). Nearly all NO haplogroups found in the Massim
are also found in the Collingwood Bay, hence our results do not
exclude the possibility that the Massim have ancestral ties in the
Collingwood Bay, in line with the archeological evidence. However, a
pairwise haplotype-sharing analysis (Table 4) did not reveal increased
haplotype sharing between the Collingwood groups and the nearest
sampled group of Fergusson, nor the Trobriand Islanders, suggesting
Tab l e 3 NO versus AS ancestry proportions, based on NRY and mtDNA haplogroup origins and composition, in the Massim area and in
regional reference populations
NRY haplogroups MtDNA haplogroups
Population n NO ancestry (%) AS ancestry (%) Unknown ancestry (%) n NO ancestry (%) AS ancestry (%) Unknown ancestry (%)
Collingwood Bay
Wanigela 21 100.0 — — 23 73.9 26.1 —
Airara 32 93.8 6.3 — 25 60.0 40.0 —
Western Massim
Fergusson 35 77.1 22.9 — 45 44.4 55.6 —
Normanby 27 66.7 33.3 — 22 36.4 63.6 —
Mainland eastern tip 24 79.2 20.8 — 31 45.2 54.8 —
Northern Massim
Trobriand Islands 60 63.3 36.7 — 47 31.9 68.1 —
Gawa 10 40.0 60.0 — 16 37.5 62.5 —
Woodlark 13 46.2 53.8 — 19 10.5 89.5 —
Laughlan Islands 5 80.0 20.0 — 6 16.7 83.3 —
Southeastern Massim
Misima 14 92.9 7.1 — 18 83.3 16.7 —
Western Calvados 19 73.7 26.3 — 14 64.3 35.7 —
Eastern Calvados 11 90.9 9.1 — 17 88.2 11.8 —
Sudest 38 94.7 5.3 — 39 61.5 38.5 —
Rossel 80 70.0 30.0 — 110 40.9 59.1 —
Total 389 76.1 23.9 — 432 47.7 52.3 —
East Asiaa113 — 92.0 8.0 121 — 79.3 20.7
Southeast Asiaa205 9.8 82.4 7.8 199 — 80.4 19.6
Nusa Tenggaraa,b 373 85.5 13. 7 0.8 31 9.7 83.9 6.5
WNG Lowlanda,c 90 100.0 — — 121 84.3 3.3 12.4
WNG Highlandsa,c 95 98.9 1.1 — 107 92.5 — 7.5
PNG Highlandsa73 98.6 1.4 — 72 91.7 1.4 6.9
PNG Coasta65 81.5 18.5 — 80 32.5 67.5 —
Admiralty Islandsd148 81.8 18. 2 — 145 37.9 60.7 1.4
Solomon Islandse712 72.5 27.5 — 703 20.9 77. 7 1.4
Polynesiaa315 63.2 34.6 2.2 306 3.6 96.4 —
Abbreviations: AS, Asian; NO, Near Oceanian.
aKayser et al.7
bMona et al.42
cTommaseo-Ponzetta et al.10
dKayser et al.16
eDelfin et al.18
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Figure 3 MDS plots of the Massim groups based on (a)FST values derived from NRY haplogroups, (b)RST values derived from Y-STR haplotypes, (c)FST
values derived from mtDNA haplogroups and (d)FST values derived from mtDNA HVS-I haplotypes. The Laughlan Islands sample was not included in this
analysis because of its small sample size (no10).
Table 4 Pairwise number of shared haplotypes between sampled groups of the Massim area for Y-STRs (below the diagonal) and mtDNA
HVS-I (above the diagonal)
WAN AIR FER NOR MET TRO GAW WOO LAU MIS WCA ECA SUD ROS
# Hts 11 9 22 9 23 16 7 8 5 8 9 8 14 17
WAN 12 —211 311 1121 11
AIR 11 —2 2 6 3 1 2 1 2 1 2 2 2
FER 25 —4 4 6 3 3 32 1 2 4 4
NOR 25 7—3 2 1 1 1 3 2 2 3 1
MET 19 1—42 3 243 2 2 3
TRO 37 1131—33221342
GAW 81121—331 132
WOO 934 1 1—31 122
LAU 511—1 22
MIS 14 213 —4221
WCA 19 46 2 3 12—31
ECA 10 11 11 2—4 1
SUD 28 222 1 112 5—4
ROS 25 11 4 1 2124—
For population sample abbreviations, see Table 1.
The total number of observed haplotypes in each group is shown left of the matrix for Y-STR haplotypes and above the matrix for mtDNA HVS-I haplotypes, both in italic.
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that genetic exchange between these groups was rather limited. The
other genetic outlier particularly for Y-STR and mtDNA haplotypes
(less so for NRY/mtDNA haplogroups) is Rossel (Figure 3) (for
further details on Rossel see below).
Apart from the outliers, the positioning of the sampled groups is in
good agreement with geography. When we repeated the MDS analysis
without the Airara, Wanigela and Rossel groups (Supplementary
Figure S2), a strong north-south correlation with geography along the
first dimension was seen in all four plots. Notably, Seligmann21
and Malinowksi33 had provisionally subdivided the Massim—on
ethnographic grounds—into a northern and a southern portion.
We considered and tested several alternative subdivisions by means of
AMOVA, while leaving out Wanigela and Airara for the reason
explained above (Supplementary Table S7). The grouping that
explained the largest proportion of among-group variation for both
NRY and mtDNA data was a division into three groups: (1) the
western plus northern Massim, (2) the southeastern Massim
excluding Rossel and (3) Rossel. This grouping explained 15.98%
(Po0.001) of the among-group variation for mtDNA haplotypes,
14.78% (Po0.001) for mtDNA haplogroups, 10.18% (Po0.001) for
Y-STR haplotypes and 7.91% (Po0.001) for NRY haplogroups.
When performing an AMOVA with the whole Massim as one group
(again excluding Wanigela and Airara), the among-populations
percentage was 6.47% (Po0.001) for NRY haplogroups and 7.37%
(Po0.001) for Y-STR haplotypes, whereas for mtDNA haplogroups
and haplotypes this was 17.99% (Po0.001) and 18.33% (Po0.001),
respectively. Although the Massim Y-STR value (7.37%) is lower
than that obtained for the Admiralties (10.31%) and Solomons
(ex-Polynesian outliers) (11.09%), the Massim mtDNA haplotype
value (18.33%) is high compared with that of the Admiralties (12.3%)
and Solomons (ex-Polynesian outliers) (13.1%) (Supplementary
Table S8). This comparative result suggests that the Massim are more
structured mtDNA-wise than NRY-wise, and more so than other
regions of NO studied so far.
We furthermore investigated the putative effect of the Kula trading
system on genetic population substructure of the Massim. As the Kula
trade occurs between islands in a circular manner in both clockwise
and counter-clockwise direction depending on the objects traded, we
modeled the Kula system as a ring of participating trading partners
that can exchange goods with adjacent partners (Figure 1). Notably,
however, not all Massim islands participate in the Kula. From the
populations included in this study, the Calvados chain islands, Sudest
and Rossel as well as the PNG mainland populations of Airara and
Wanigela are not known to be involved in the Kula33 and were
therefore excluded from the model. Furthermore, the Laughlan
Islanders, who may be only marginally involved in the Kula,37 were
excluded because of small sample size. Genetic distances appropriate
for the marker type (Supplementary Table S6) were compared via
Mantel testing with circular trading distances. For NRY (both at the
haplogroup level and at the haplotype level) no statistically significant
correlation was observed, whereas for mtDNA a significant correlation
was observed both for haplotype data (0.42; P¼0.029) and for
haplogroup data (0.47; P¼0.019). This result can be explained by
predominantly male-mediated gene flow between islands involved in
the Kula, having a homogenizing effect on the Y-chromosome
diversity but not on the mtDNA pool. As only men traditionally
participate in the Kula voyages, this finding may indicate a genetic
signature of the Kula Ring. However, the mtDNA-based correlation
decreased and became nonsignificant when excluding Misima, which
is reported to be less intensively involved in the Kula.35,38
Genetic characterization of Rossel Islanders
Rossel Islanders, who live on the easternmost and most remote island
of the entire Massim, occupy a unique position within the Massim
because they are its only Papuan-speaking people. Their outlier
position as noted above, despite their geographic proximity to
Austronesian-speaking neighboring islanders from the southeastern
Massim, is therefore intriguing. It is also remarkable that Rossel
Islanders are characterized by a larger proportion of haplogroups of
AS origin than all other groups from the southeastern Massim
(Table 3), although all these other groups speak Austronesian
languages. Haplotype network analyses for the major NRY
(O-M110 and S-M254*) and mtDNA haplogroups (P1 and E*)
found in Rossel (Supplementary Figure S3) revealed some degree of
haplotype sharing between Rossel Islanders and other groups of the
southeastern Massim, in particular for the NO haplogroups S-M254*
and P1, suggesting a shared southeastern Massim ancestry for at least
the NO component. When and from where the strong AS ancestry
component was contributed to Rossel’s gene pool cannot be answered
precisely, but it is noteworthy that while all AS NRY haplogroups
found on Rossel also occur on other southeastern Massim islands, this
is not the case for AS mtDNA haplogroups found on Rossel, which
therefore were most likely contributed from elsewhere, perhaps from
the northern Massim. Although this finding may indicate that Rossel
Islanders have sex-biased local ancestry differences within the Massim,
our genetic data do not reveal the exceptional outlier position of
Rossel that is expected from linguistic data.
The Massim relationships to other populations
A comparison of the Massim data with reference data from other
populations of Asia/Oceania (Figure 2) highlights the Admiralty
Islands of Northern Melanesia and the PNG Coast as the most
similar reference populations to the Massim in terms of overall
haplogroup composition. Interestingly, the Massim appear to be quite
different from the geographically closer Solomon Islanders. Concern-
ing NRY, the Solomon Islanders harbor more diverse NRY lineages
than the Massim; for example, several C, K, M and O lineages present
in the Solomon Islanders18 are absent from our Massim sample,
but are also found in the Bismarck Archipelago.14 Similarly
for mtDNA, the Northern Melanesian lineages M27 and M28 are
found in the Solomons18 and in the Bismarcks,15 but not in
our Massim sample. Thus, it is likely that there were direct
links between the Bismarcks and the Solomons that bypassed the
Massim region.
To further investigate the relationships of the Massim people in the
wider context of East and Southeast Asia and Near- and Remote
Figure 4 MDS plots of regional populations based on (a)FST values derived from NRY haplogroups and (b)FST values derived from mtDNA haplogroups.
Only populations with a sample size of 10 or larger (for both NRY and mtDNA) were included. Population abbreviations are as in Supplementary Table S1.
The Admiralty16 and Solomon Islands18 populations are indicated by Adm and Sol, respectively, followed by another abbreviation indicating the
sub-population, as follows for the Admiralty Islands: AH, Andra-Hus; EK, Ere Kele; Ku, Kurti; Le, Lele; Mo, Mokerang; Na, Nali; Ni, Nyindrou; SW,
Seimat-Wuvulu; Ti, Titan; and for the Solomon Islands: Be, Bellona; Ch, Choiseul; Ge, Gela; Gu, Guadalcanal; Is, Isabel; Ko, Kolombangara; La, Lavukaleve;
Mk, Makira; Ml, Malaita, OJ, Ontong Java; Ra, Ranongga; Re, Rennell; Sa, Savo; SC, Santa Cruz; Sh, Shortlands; Si, Simbo; Ti, Tikopia; VL, Vella Lavella.
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Oceania, MDS plots were constructed based on NRY and mtDNA
haplogroup frequencies using all regional population data available
(Figure 4). In both plots, the positioning of the populations is in
agreement with geography. In the NRY plot, the Massim groups
appear close to the Austronesian-speaking Admiralty Island groups, in
line with the hypothesis that Austronesian ancestors from East/
Southeast Asia came to NO via the Bismarck Archipelago and from
there occupied other parts of NO such as the Massim, as well as
Remote Oceania.16 Wanigela, however, is distinct (consistent with
Figure 3), being closest to the Western New Guinea highlands
population to which it is very similar in NRY haplogroup composi-
tion. For mtDNA, the Massim groups appear much more dispersed,
consistent with the observation that the Massim are more structured
with respect to mtDNA than to NRY.
CONCLUSIONS
We genetically characterized, for the first time, the people of the
Massim, thereby filling another gap in the complex human genetic
history of NO. We found that the nearly exclusively Austronesian-
speaking Massim harbor components of both AS (Austronesian) and
NO (Papuan) origin with proportionally more NO Y-chromosomes
and more AS mtDNAs, similar to previous observations in Austro-
nesian-speaking groups from the Admiralty Islands north of mainland
PNG,16 the Solomon Islands18 and Polynesia,7and in line with the
Slow Boat from Asia hypothesis on Austronesian dispersal.4MtDNA-
wise, the Massim appear more structured than populations from
nearby regions such as the Admiralty Islands16 and the Solomon
Islands.18 Both NRY and mtDNA data best support a broad three-way
division of the Massim into a northwestern group, a southeastern
group (excluding Rossel) and Rossel, with larger differentiation in
mtDNA than in NRY. The Rossel Islanders, the only non-Austronesian
(ie, Papuan) speaking people within the Massim, occupy an outlier
position when compared with the other Massim groups studied,
probably as a result of isolation and genetic drift. Surprisingly,
however, Rossel Islanders exhibited a lower NO and higher AS
(Austronesian) contribution for both NRY and mtDNA than their
geographic neighbors from the southeastern Massim who speak
Austronesian languages. Considering those Massim populations that
participate in the Kula traditional trading system, a correlation
between inter-island trading distances and genetic distances was
detected for mtDNA but not for the Y-chromosome, which can be
explained by male-mediated but not female-mediated gene flow
throughout the Kula region. As only men participate in Kula
trading, this may be a genetic signature of the Kula in
contemporary inhabitants of the region. Our study thus provides
insights into how a social trading system can impact on human
genetic diversity, representing another example of the interplay
between culture and genes, in addition to residence pattern
(patrilocality versus matrilocality)39 and social stratification.40
Finally, we would like to emphasize the particular suitability of
studying the uni-parentally inherited genetic systems NRY and
mtDNA for investigating those parts of human genetic history that
are influenced by males and females differently, such as sex-biased
migrations as studied here with the Kula, and for which bi-parentally
inherited genetic diversity as obtained via genome-wide SNP data is
much less useful.
CONFLICT OF INTEREST
The authors declare no conflict of interest.
ACKNOWLEDGEMENTS
We thank all DNA donors who participated in this study. In addition, we are
grateful to representatives of the Diocese of Alotau, PNG (MSC), particularly
then Bishop Desmond Moore MSC; the entire crew of the Morning Star
(particularly then Captain Pius) for infrastructural support in collecting
samples; and all the people from the various islands who made our stay
pleasant. Furthermore, we thank Oscar Lao for statistical advice, and Michael
Dunn, Ger Reesink, Fiona Jordan and Gunter Senft for useful discussions
regarding cultural and linguistic aspects. This work was supported by the Max
Planck Society and by the Erasmus MC University Medical Center Rotterdam.
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Supplementary Information accompanies this paper on European Journal of Human Genetics website (http://www.nature.com/ejhg)
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