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Biological relationship between central and South American Chibchan speaking populations Evidence from mtDNA.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 133:753–770 (2007)
Biological Relationship Between Central and South
American Chibchan Speaking Populations:
Evidence From mtDNA
Phillip E. Melton,1* I. Briceño,2 A. Gómez,2 E.J. Devor,1,3 J.E. Bernal,2 and M.H. Crawford1
1
Department of Anthropology, University of Kansas, Lawrence, KS
Institute of Human Genetics, Pontificia Universidad Javeriana, Bogotá, Colombia
3
Molecular Genetics and Bioinformatics, Integrated DNA Technologies (IDT), Coralville, IA
2
KEY WORDS
Colombia; Ijka; Kogi; Arsario; Wayuú; Chibcha
ABSTRACT
We examined mitochondrial DNA (mtDNA)
haplogroup and haplotype diversity in 188 individuals
from three Chibchan (Kogi, Arsario, and Ijka) populations
and one Arawak (Wayuú) group from northeast Colombia
to determine the biological relationship between lower Central American and northern South American Chibchan
speakers. mtDNA haplogroups were obtained for all individuals and mtDNA HVS-I sequence data were obtained
for 110 samples. Resulting sequence data were compared
to 16 other Caribbean, South, and Central American populations using diversity measures, neutrality test statistics,
sudden and spatial mismatch models, intermatch distributions, phylogenetic networks, and a multidimensional scaling plot. Our results demonstrate the existence of a shared
maternal genetic structure between Central American
Chibchan, Mayan populations and northern South American Chibchan-speakers. Additionally, these results suggest
an expansion of Chibchan-speakers into South America
associated with a shift in subsistence strategies because of
changing ecological conditions that occurred in the region
between 10,000–14,000 years before present. Am J Phys
Anthropol 133:753–770, 2007. V 2007 Wiley-Liss, Inc.
Over the last two decades, mitochondrial DNA
(mtDNA) has been used extensively to characterize
Native American population structure and history (Wallace et al., 1985; Schurr et al., 1990; Horai et al., 1993;
Torroni et al., 1993; Schurr and Sherry, 2004). These
investigations have demonstrated that the majority of
modern Amerindian populations are characterized by
four major haplogroups (A, B, C, and D) (Schurr et al.,
1990; Torroni et al., 1993; Schurr and Sherry, 2004). A
fifth haplogroup, X, is restricted to North America
(Smith et al., 1999) and absent in South America (Dornelles et al., 2005). All mtDNA haplogroups are associated with several specific point mutations located within
the control region (CR) of the mitochondrial genome.
Frequencies of mtDNA haplogroups differ among populations and are often correlated with cultural affiliation,
linguistic family, or geographic location (O’Rourke et al.,
2000; Bolnick and Smith, 2003). Populations that typically share founding haplotypes tend to be geographically restricted, indicating more recent mutations. This
geographic restriction suggests that closely related populations share several derived haplotypes that are either
identical or differ by few mutations (Torroni et al., 1993;
Bolnick and Smith, 2003).
Initially, evidence from the four mtDNA haplogroups
was used to suggest distinct founding Native American
populations (Horai et al., 1993; Torroni et al., 1993) but
others advocated a single founding group that underwent
a genetic bottleneck (Merriwether et al., 1995; Bonatto
and Salzano, 1997; Stone and Stoneking, 1998) or two
migrations (Rubicz et al., 2003; Schurr, 2004). Evidence
from archaeology (Dixon, 1999; Dillehay, 2000; Lavallée,
2000) and molecular genetics (Bonatto and Salzano, 1997;
Tarazona-Santos et al., 2001) indicate the peopling of
South America occurred during the Pleistocene but the
number of migrations into the continent is unresolved.
Some researchers argue for a single founder South
American population (Moraga et al., 2000) while others
favor a two-wave migration model (Fox, 1996; Lalueza
et al., 1997; Keyeux et al., 2002). Fox (1996) and Lalueza
et al. (1997) originally proposed two migrations based on
a clinal distribution of mtDNA haplogroups in South
America, where A occurs at high frequencies (>50%) in
northern populations and is absent in the southern cone
and D demonstrates the opposite distribution. Moraga
et al. (2000) used evidence from sequence data in the
mtDNA CR region to dispute this hypothesis and demonstrated that modern Fuegian populations from Chile and
Argentina did not exhibit divergent sequences and suggested that southern South American populations were
descended from a single Paleoindian population. Recently,
Keyeux et al. (2002) noticed a similar A/D haplogroup
distribution in 25 indigenous populations from Colombia
separated by the Andean Cordillera. These latter researchers proposed two migrations into the continent,
C 2007
V
WILEY-LISS, INC.
C
Grant sponsor: National Science Foundation.
*Correspondence to: Phillip E. Melton, Department of Anthropology, University of Kansas, Fraser Hall Room 622, 1415 Jayhawk
Blvd., Lawrence, KS 66045, USA. E-mail: pmelton@ku.edu
Received 14 June 2006; accepted 22 December 2006
DOI 10.1002/ajpa.20581
Published online 5 March 2007 in Wiley InterScience
(www.interscience.wiley.com).
754
P.E. MELTON ET AL.
Fig. 1. Geographic distribution of the four populations used
in this study as well as other extant and extinct lower Central
and northern South American populations. Tairona and Muisca
refer to extinct Chibchan-speaking populations.
with one occurring along the Amazonian lowlands relating to the majority of eastern South American populations and then occurring along the Pacific and Caribbean
coast associated with a diaspora of Chibchan-speakers.
Populations of the Chibchan language family are distributed from eastern Honduras to the eastern shores of
Lake Maracaibo (Fig. 1) (Hoopes and Fonseca, 2003).
This language phylum contains 14 extant and six extinct
languages, divided into four regional subfamilies: (1)
Pech (Paya), spoken in eastern Honduras; (2) Votic,
spoken in Nicaragua and northern South America; (3)
Isthmic, spoken in Costa Rica and Panamá; and (4) Magdelenic, spoken in northern South America (ConstenlaUmaña, 1991). Other linguists also include other South
American populations within a larger Chibchan-Paezan
family, including the Yanomamõ, Cayapa, and Atacemeño (Greenberg, 1987; Ruhlen, 1998). Based on glottochronological evidence, Chibchan is thought to have
diverged from related languages approximately 7,000
years before present (YBP) either in Costa Rica or
Panamá as these regions have linguistic diversity
(Constenla-Umaña, 1991). The differentiation of the regional subfamilies is thought to have begun around
5,000 YBP because of a shift to agriculture and adaptation to a sedentary lifestyle (Constenla-Umaña, 1991;
Cooke and Ranere, 1992). Archaeological research conducted in lower Central and northern South America
has focused on the formation of Chibchan populations
and has demonstrated a close cultural relationship based
on shared settlement patterns, iconography, and material goods (Lange and Stone, 1984; Quilter and Hoopes,
2003). This evidence has led some researchers to suggest
the presence of a large homogeneous culture dominated
by Chibchan-speakers (Bray, 2003; Hoopes and Fonseca,
2003; Hoopes, 2005). Previous genetic research on
Chibchan populations has focused on lower Central
America because of their geographic location, bridging
the two American continents. Originally, it was thought
that these populations would exhibit high genetic diver-
sity because of their intermediate position between complex cultures in the Andes and Mesoamerica. However,
studies using both classical markers (Barrantes et al.,
1990; Bieber et al., 1996) and molecular genetics (Santos
et al., 1994; Torroni et al., 1994b; Batista et al., 1995;
Kolman et al., 1995; Kolman and Bermingham, 1997;
Ruiz-Narvaez et al., 2005) demonstrate that these populations are characterized by low amounts of genetic
diversity and a high number of private polymorphisms
not shared with neighboring populations. Several studies
have investigated mtDNA diversity in Central American
Chibchan-speakers (Santos et al., 1994; Torroni et al.,
1994b; Batista et al., 1995; Kolman et al., 1995; Kolman
and Bermingham, 1997). These populations are characterized by high frequencies of haplogroup A (>65%),
moderate frequencies of B (20–30%), absence of C, and
the infrequent presence of D. Based on mtDNA CR
sequence data these Chibchan groups demonstrate low
haplogroup and nucleotide diversity. (Santos et al., 1994;
Batista et al., 1995; Kolman et al., 1995; Kolman and
Bermingham, 1997). While archaeological and linguistic
evidence indicate a relationship between lower Central
and northern South American Chibchan groups the biological relationship between the two regions has yet to
be investigated.
One Chibchan region in northern South America containing a wealth of comparative archaeological, linguistic, ethnographic, and ethnohistoric information is the
Sierra Nevada de Santa Marta in northeast Colombia
(Reichel-Dolmatoff, 1950; Bray, 1984, 2003; OyuelaCaycedo, 1996; Uribe, 2000; Hoopes and Fonseca, 2003;
Langebaek, 2003). This mountain range rises to 5,780 m
in a little over 35 km and occurs within the Caribbean
littoral ecological environment of South America. The
extant indigenous populations (Kogi, Arsario, and Ijka)
of the region may represent the remnants of the ancient
Tairona, one of the largest Chibchan populations present
at European contact (Wilson, 1999; Bray, 2003).
In this study, we test the hypothesis that Chibchan
speaking populations demonstrate a biological relationship and how this association relates to the peopling of
South America. To accomplish this, we analyze mtDNA
haplogroup and haplotype diversity in the three extant
Sierra Nevada de Santa Marta (Arsario, Kogi, Ijka) populations and a neighboring Arawak (Wayuú) group to
gain greater insight into the genetic history of Chibchan
populations. Our initial analysis of these indigenous
populations confirmed the pattern of mtDNA RFLP variation seen in previous research (Briceño et al., 2003;
Keyeux et al., 2002), revealing haplogroups A, and C for
the Kogi and Arsario, and A, B, and C for the Ijka and
Wayuú (Melton et al., 2004; Melton et al., 2005; Melton,
2005).These results also indicated that all haplogroup A
individuals belonged to the A2 subhaplotype (Forster
et al., 1996) However, a higher than expected transistion-transversion ratio (17-8) indicated the possibility of
\phantom mutations" in the original data (Forster, 2003;
Brandstatter et al., 2005). In addition, only a small number of Kogi individuals were characterized in our earlier
research as well as some unrepresented haplogroups for
the Ijka (Melton et al., 2004, 2005; Melton, 2005). The
present study summarizes our expanded analyses
(mtDNA heavy and light chains sequenced, higher resolution, and larger sample size) and discusses the implication of new mtDNA data for understanding the biological
and geographic relationship of Chibchan-speaking populations.
American Journal of Physical Anthropology—DOI 10.1002/ajpa
755
mtDNA GENETIC RELATIONSHIP OF CHIBCHAN SPEAKERS
TABLE 1. South American indigenous population mtDNA haplogroup frequencies and diversity estimates
mtDNA haplogroup (%)
Populationa
Chibchan-Paezanb
(1) Teribe1,c
(2) Guataso1
(3) Kuna1,4 pooled
(4) Bribri-Cabecar1
(5) Huetar3
(6) Ngöbé4
(7) Cayapa2
(8) Atcemeño6
(9)Yanomamõ5
(19) Emberá7
(21) Zenu7
KogiTS
IjkaTS
ArsarioTS
Andeanb
(28) Quechua6,8 pooled
(10) Aymara6,8
(11) Mapuche9–11 pool
(12) Huilliche6,11 pool
(13)Pehuenche6,11 pool
(18) Yahgan11
(25) Fuegian12
(22) Ingano7
(36) Jujeños13
Equatorial-Tucanoanb
(23) Ticuna1,7 pool
(14) Zoro14
(15) Gavião14
(20) Wayuú7
WayuúTS
(32) Ignaciano8
(33) Trinitarion8
(34) Movima8
(35) Yuracare8
Ge-Pano-Caribb
(16) Mataco1,15,16 pool
(27) Toba15 pool
(24) Chorote11,16 pool
(17) Xavante14
(29) Pilaga15
(30) Chimane8
(31) Moseten8
n
A
B
C
D
Other
H
20
20
79
24
27
46
120
50
129
21
37
48
40
50
80.0
85.0
77.0
54.0
70.0
67.0
29.0
12.0
0.6
73.0
19.0
65.0
90.0
68.0
20.0
15.0
23.0
46.0
4.0
33.0
40.0
72.0
9.0
22.0
41.0
0.0
2.5
0.0
0.0
0.0
0.0
0.0
0.0
0.0
9.0
10.0
26.0
0.0
30.0
35.0
7.5
32.0
0.0
0.0
0.0
0.0
26.0
0.0
22.0
6.0
31.0
0.0
5.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
5.0
5.0
0.0
0.0
0.0
0.34
0.27
0.36
0.52
0.46
0.45
0.71
0.46
0.51
0.44
0.72
0.46
0.19
0.44
51
205
208
118
205
21
45
27
65
20.0
5.0
5.0
4.0
2.0
0.0
0.0
15.0
12.0
61.0
72.0
20.0
29.0
8.0
0.0
0.0
44.0
65.0
8.0
11.0
33.0
19.0
40.0
48.0
42.0
37.0
8.0
12.0
12.0
39.0
48.0
50.0
52.0
56.0
0.0
15.0
0.0
0.0
3.0
0.0
0.0
0.0
0.0
4.0
0.0
0.31
0.45
0.70
0.65
0.59
0.52
0.52
0.67
0.54
15.0
20.0
15.0
25.0
37.0
18.0
14.0
9.0
39.0
10.0
7.0
15.0
35.0
26.0
36.0
40.0
9.0
32.0
36.0
13.0
0.0
38.0
35.0
41.0
37.0
64.0
21.0
39.0
60.0
70.0
0.0
0.0
0.0
3.0
18.0
4.0
0.0
0.0
0.0
2.0
2.0
5.0
6.0
0.0
4.0
0.69
0.60
0.48
0.69
0.69
0.70
0.70
0.57
0.72
8.0
20.0
15.0
16.0
27.0
39.0
40.0
54.0
41.0
44.0
84.0
35.0
54.0
55.0
9.0
5.0
23.0
0.0
4.0
5.0
0.0
27.0
30.0
18.0
0.0
35.0
0.0
0.0
2.0
4.0
0.0
0.0
0.0
2.0
5.0
0.63
0.71
0.72
0.28
0.71
0.57
0.57
82
30
27
40
46d
22
35
22
28
129
56
34
25
26
41
20
a
References: (1) Torroni et al. 1993; (2) Rickards et al., 1999; (3) Santos et al., 1994; (4) Kolman et al., 1995; (5 ) Merriwether et al.
2000; (6) Merriwether et al., 1995; (7) Mesa et al., 2000; (8) Bert et al., 2001; (9) Ginther et al., 1993; (10) Bailliet et al., 1994; (11)
Moraga et al., 2000; (12) Lalueza et al., 1997; (13) Dipierri et al., 1998; (14) Ward et al., 1996; (15) Demarchi et al., 2001; (16)
Bianchi et al., 1995. TS, this study.
b
Linguistic affiliation as defined by Ruhlen, 1998.
c
refers to geographic location of population in Figure 2.
d
Adjusted n to account for fewer samples.
MATERIALS AND METHODS
Population samples
Blood samples belonging to 188 individuals from three
Chibchan (Kogi n ¼ 48, Ijka, n ¼ 40, and Arsario, n ¼
50) populations and one Arawak (Wayuú, n ¼ 50) group
inhabiting northeastern Colombia were collected from
randomly selected, unrelated, healthy individuals
(Briceño et al., 1996b). The Kogi (Kagaba, Cogui) are
seasonal horticulturists who inhabit the northern slopes
of the Sierra Nevada de Santa Marta. The most accurate
current estimate of their population size is 6,138 distributed (Uribe, 2000). The Ijka (Ica, Bı́ntuka, Busı́nka,
Busintana, Arhucao) are an agricultural population of
9,394 individuals inhabiting the southern side of the
Sierra Nevada de Santa Marta (Uribe, 2000). The Arsario
(Sanká, Sanhá, Guamaca, Marocaseros, Wiwa) inhabit
the southeastern slopes of the Sierra Nevada de Santa
Marta range and number *1,500 (Uribe, 2000). All three
Sierra Nevada de Santa Marta groups speak languages
within the Magdalenic subgroup of Chibcha (ConstenlaUmaña, 1991). The Wayuú (Guajira) are a semi-nomadic
pastoralist Arawakan-speaking population inhabiting
the arid La Guajira peninsula of Colombia and Venezuela
(Saler, 1992). They represent on of the largest current
extant populations in South America and number
80,000–120,000 (Yunis et al., 1994). Geographic locations
of all study populations are shown in Figure 1.
Comparative RFLP data for 37 Central and South
American populations (Table 1) were collected from the
American Journal of Physical Anthropology—DOI 10.1002/ajpa
756
P.E. MELTON ET AL.
Fig. 2. Geographic location of comparative South American study populations. Numbers correspond to populations from Table 1.
literature. Geographic locations of these populations are
shown in Figure 2. Additional RFLP data were also
collected on 31 Caribbean, and Central and South
American populations (Table 2). Hypervariable sequence
I (HVS-I) sequences were collected for 16 Caribbean,
Central, and South American groups (Table 4) and were
chosen because of their geographic proximity to the
study populations and included greater than 20 sequences, with the exception of the Tainos (n ¼ 19) and Ciboney (n ¼ 15).
DNA extraction and mtDNA analysis
DNA was extracted using phenol/chlorform techniques
by researcher at the University upon Tyne, UK (Briceño
et al., 1996a). All 188 samples were characterized for the
four major Native American mtDNA haplogroups (A-D)
using polymerase chain reaction (PCR) and associated
restriction site enzymes (HaeIII, HincII, and AluI) and
the presence/absence of the COII-tRNAlys 9-bp deletion.
Primer pairs and amplification conditions used in this
study have been previously described by Torroni et al.
(1993). A subset of 20 individuals from each of the three
Chibchan populations was characterized for a previously
described loss of a MspI restriction site found in Central
American Chibchan-speakers (Torroni et al., 1994b) at
mtDNA nucleotide position (np) 104 using PCR primers
L1 and H240. Restriction fragments were visualized
with UV light on 3% NuSieve agarose gels (FMC Bioproducts) and recorded as present or absent. The mtDNA CR
HVS-I (np 16050–16383) was sequenced for a randomly
selected subset of 110 individuals (Kogi, n ¼ 21, Ijka,
American Journal of Physical Anthropology—DOI 10.1002/ajpa
757
mtDNA GENETIC RELATIONSHIP OF CHIBCHAN SPEAKERS
TABLE 2. mtDNA haplogroup diversity in Caribbean, Central, and Northern South American populations
a
Population
Maya1
Maya2
Ancient Maya (Xcaret)3
Ancient Maya (Copan)4
Mixe5
Pima5
Mixtec (Alta)5
Mixtec (Baja)5
Zapotec5
Central American Total
Ciboney6
Tainos7
Caribbean Total
Teribe8
Guataso8
Kuna (pool)8,9
Bribri-Cabecar8
Huetar10
Boruca8
Guyami8
Ngöbé11
Central American Chibchan Total
Wounan12
Emberá12
Central American Chocoan Total
KogiTS
Kogi13
Kogi4
IjkaTS
Ijka13
Ijka14
ArsarioTS
Arsario (Wiwa)13
Arsario14
Santa Marta Chibchan Total
Guane-Butaregua13
Chimila13
Tule-Cuna13
Zenu15
Zenu16
Zenu13
Other Colombian Chibchan Total
Waunana13
Emberá15
Emberá16
Emberá13
Paez16
Paez13
Pasto13
Guambiano13
Other Colombian Paezan and Chocoan Total
Cayapa17
Atacemeño18
Yanomamö19
Yanomamö20
Yanomamö8
Yanomamö21
Other South American Chibchan-Paezan
Total
N
A
B
C
D
Unk
H
27.00
30.00
25.00
9.00
16.00
30.00
15.00
14.00
15.00
181.00
15.00
24.00
39.00
20.00
20.00
79.00
24.00
27.00
14.00
16.00
46.00
246.00
31.00
44.00
75.00
48.00
30.00
50.00
40.00
40.00
40.00
50.00
8.00
50.00
356.00
33.00
35.00
30.00
37.00
36.00
34.00
205.00
30.00
22.00
22.00
21.00
20.00
31.00
9.00
23.00
178.00
120.00
50.00
129.00
151.00
24.00
30.00
504.00
1784.00
0.52
0.63
0.84
0.00
0.63
0.07
0.73
0.93
0.33
0.52
0.07
0.00
0.03
0.80
0.85
0.77
0.54
0.70
0.21
0.69
0.67
0.65
0.29
0.23
0.26
0.65
0.37
0.58
0.90
0.83
0.92
0.68
0.25
0.64
0.65
0.12
0.89
0.50
0.19
0.22
0.15
0.34
0.00
0.73
0.76
0.33
0.60
0.58
0.67
0.04
0.46
0.29
0.12
0.02
0.00
0.00
0.13
0.09
0.38
0.22
0.33
0.04
0.00
0.31
0.50
0.13
0.07
0.33
0.22
0.00
0.00
0.00
0.20
0.15
0.23
0.46
0.04
0.72
0.31
0.33
0.30
0.19
0.52
0.36
0.00
0.00
0.00
0.03
0.00
0.03
0.00
0.00
0.00
<0.01
0.64
0.00
0.27
0.41
0.41
0.32
0.34
0.63
0.22
0.24
0.48
0.20
0.07
0.33
0.04
0.28
0.40
0.72
0.09
0.56
0.17
0.27
0.37
0.23
0.15
0.03
0.08
0.89
0.06
0.43
0.13
0.00
0.33
0.23
0.60
0.75
0.68
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.48
0.25
0.37
0.35
0.63
0.42
0.08
0.18
0.05
0.32
0.75
0.36
0.35
0.00
0.03
0.20
0.30
0.31
0.50
0.22
0.30
0.00
0.00
0.05
0.15
0.36
0.00
0.78
0.20
0.09
0.10
0.26
0.32
0.54
0.53
0.31
0.29
0.07
0.00
0.00
0.11
0.00
0.00
0.00
0.00
0.00
0.02
0.33
0.25
0.29
0.00
0.00
0.00
0.00
0.26
0.07
0.00
0.00
0.04
0.03
0.00
0.02
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.24
0.06
0.00
0.05
0.06
0.03
0.07
0.07
0.00
0.00
0.09
0.05
0.00
0.00
0.13
0.04
0.22
0.06
0.31
0.12
0.29
0.03
0.17
0.08
0.04
0.00
0.04
0.00
0.00
0.00
0.00
0.00
0.00
0.01
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.03
0.03
0.05
0.00
0.00
0.02
0.00
0.05
0.00
0.00
0.00
0.00
0.00
0.00
0.01
0.68
0.51
0.30
0.22
0.54
0.58
0.46
0.14
0.72
0.63
0.56
0.39
0.47
0.34
0.27
0.36
0.52
0.46
0.47
0.46
0.45
0.48
0.66
0.63
0.68
0.46
0.48
0.50
0.19
0.30
0.15
0.44
0.43
0.47
0.46
0.54
0.22
0.66
0.72
0.70
0.64
0.71
0.52
0.44
0.38
0.68
0.61
0.55
0.50
0.38
0.67
0.71
0.46
0.83
0.57
0.62
0.65
0.73
0.71
0.00
0.05
0.00
0.00
0.03
0.02
0.01
a
References: (1) Schurr et al., 1990; (2) Boles et al., 1995; (3) Gonzalez-Olivier et al., 2001; (4) Merriwether et al., 1997; (5) Torroni
et al., 1994a; (6) Lalueza-Fox et al., 2003; (7) Lalueza-Fox et al., 2001; (8) Torroni et al., 1993; (9) Batista et al., 1995); (10) Santos
et al., 1994; (11) Kolman et al., 1995; (12) Kolman and Bermingham, 1997; (13) Keyeux et al., 2002; (14) Briceño et al., 2003; (15)
Mesa et al., 2000; (16) Torres et al., 2006; (17) Rickards et al., 1999; (18) Merriwether et al., 1995; (19) Meriwether et al., 2000; (20)
Williams et al., 2002; (21) Lobato-da-Silva et al., 2001. TS, this study.
n ¼ 31, Arsario, n ¼ 28, and Wayuú, n ¼ 30) using PCR
primers L15976 and H16422 and the Big Dye protocol
from Applied BiosystemsTM. For sequences containing a
homopolymeric cytosine stretch from mtDNA np 16184
to 16193, nested sequencing was conducted using internal primer L16190. Sequences were aligned and compared with the human mtDNA Cambridge Reference
Sequence (CRS) (Anderson et al., 1981; Andrews et al.,
American Journal of Physical Anthropology—DOI 10.1002/ajpa
758
P.E. MELTON ET AL.
1999) using BioEdit sequence alignment editor (Hall,
1999). Point mutations at HVS-I np 16182 and 16183
were excluded from analysis because they are dependent
on the presence of a T-C transition at np 16189 (Pfeiffer
et al., 1999).
1992). These estimates were calculated using a mutation
rate of 16.5% per HVS-I nucleotide per million years
(Ward et al., 1991) with IWAVE (Sherry et al., 1994) and
Arlequin 3.0 (Excoffier et al., 2005), respectively.
Analytical techniques
Interpopulation analysis. Phylogenetic networks utilizing the median-joining (MJ) method (Bandelt et al.,
1995; Bandelt et al., 1999) were constructed to determine the genetic relationship between haplotypes found
within the study and comparative populations. These
types of phylogenetic networks offer an advantage over
other tree building techniques because they distinguish
between irresolvable and resolvable character conflicts
that occur due to homoplasy and may be interpreted as
recombination, sequence errors, or phantom mutations
(Bandelt et al., 1995). MJ networks were visualized with
Network 4.0 (www.fluxus-engineering.com) and integrated into a schematic based on previously published
Native American (Forster et al., 1996) and East Asian
(Kivisild et al., 2002) mtDNA sequences.
A MDS plot (Kruskal, 1964) was constructed to visualize the biological relationship between the study and
comparative populations. The distance method utilized
in this analysis was a dXY matrix with a Tamura-Nei
(Tamura and Nei, 1993) model of substitution and a
g-value of 0.26 (Meyer et al., 1999). The resulting MDS
plot was generated using NTSYS (Applied Biostatistics)
and the matrix was computed using Arelquin 3.0
(Excoffier et al., 2005). Estimates of population divergence (dA), average nucleotide diversity within (dX), and
between populations (dXY) were calculated using Arlequin 3.0 (Excoffier et al., 2005). Intermatch distributions
were calculated with the computer program IWAVE
(Sherry et al., 1994) to determine potential population
divergence.
Intrapopulational analysis. Mitochondrial DNA haplogroups for all study and comparative populations were
characterized for haplogroup diversity (H) using Nei’s
(1987) equation. HVS-I sequence variation for all study
and 16 comparative populations were measured for nucleotide diversity (p) and haplotype diversity (h) using
Nei’s method (1987). Three neutrality test statistics,
Tajima’s D (Tajima, 1989), Fu’s Fs (Fu, 1997), and
Harpending’s raggedness statistic, r, (Harpending, 1994)
were utilized to distinguish population growth from constant population size. Fu’s Fs is considered less conservative than both Tajima’s D and Harpending’s r (RamosOnsins and Rozas, 2002) and is more sensitive to large
population expansions expressed as large negative numbers whereas positive numbers indicate that the population may have been impacted by genetic drift (Fu, 1997;
Schneider et al., 2000). Statistically significant values
were generated through random samples under the
assumption of selective neutrality and population equilibrium using a coalescent simulation model (Hudson,
1990). All measures were calculated using Arlequin 3.0
computer package (Excoffier et al., 2005).
Distributions of pairwise differences were used to
examine population history and structure. Mismatch distributions (Rogers and Harpending, 1992; Harpending
et al., 1993) were constructed by enumerating differences between each pair of subjects and using histograms
or scatter plots to display the frequencies of nucleotide
variant sites (Rogers et al., 1996). This measure of diversity summarizes the discernible amount of genetic variation within a population. Traditionally, unimodal distributions have been viewed as indicative of population
expansions, whereas multimodal distributions indicate
population stasis (Rogers and Harpending, 1992). However, it has recently been demonstrated that populations
with a low migration rate (<50/generation) also exhibit
multiple peaks (Ray et al., 2003; Excoffier, 2004). Excoffier (2004) developed a spatial expansion mismatch model
using an infinite island model with the following four
assumptions: (1) expansion started T generations ago
from a single haploid deme; (2) expansion was instantaneous and permitted the colonization of an unlimited
number of islands; (3) after expansion, demes are all
constant size (N1), trade migrants at rate m, and result
in each deme receiving and sending N1m migrants/generation; and (4) random mutations occur at an infinite
amount site of nonrecombining DNA sequences with
rate l. This model calculates an additional parameter M
(¼ 2 N1m) and corresponds to the expected homozygosity
and becomes significant for ‘low’ M values (<50). We calculated both sudden (Rogers and Harpending, 1992) and
spatial (Excoffier, 2004) expansion mismatch distributions using Arlequin 3.0 (Excoffier et al., 2005). Estimates of past population growth may be measured using
the equation s ¼ 2lt where l equals the mutation rate
and t is the time in generations. Time estimates are
based on the mtDNA coalescent (Hudson, 1990) using
both method of moments (MOM) (Rogers, 1995) and nonlinear least squares (NLLS) (Rogers and Harpending,
RESULTS
Haplogroup frequency data
Of the 188 samples from which DNA was extracted,
183 were assigned by RFLP analysis to one of the four
founding Native American haplogroups (Schurr et al.,
1990; Torroni et al., 1993). Five Wayuú samples could not
be assigned to any Native American specific haplogroup.
Subsequent HVS-I sequencing of one of these samples
revealed that it belonged to African subhaplogroup L2a
(Salas et al., 2002), and indicated the presence of African
admixture, which had been previously demonstrated
using microsatellite and classical genetic data (Yunis
et al., 1994; Guarino et al., 1999). Subsequent sequencing of the remaining four Wayuú samples failed and
insufficient DNA remained for further RFLP analysis. It
is possible that these samples may have been C-revertants, common in northern South American EquatorialTucano populations (Torres et al., 2006). We investigated
the presence/absence of a MspI RFLP cut site in 60 haplogroup A samples from the three Santa Marta Chibchan
populations. All samples examined exhibited this restriction site, suggesting that the loss of this mutation in
Central American Chibchan groups may have occurred
after the Magdalenic subfamily diverged from the other
major Chibchan subfamilies. Haplogroup diversity (H)
and frequencies for the four study populations, 37 comparative South American, and 31 regional populations
are given in Tables 1 and 2.
American Journal of Physical Anthropology—DOI 10.1002/ajpa
759
8
25
37
3
9
7
6
9
3
2
1
110
8
–
–
–
8
7
6
–
–
–
1
30
–
14
–
3
–
–
–
4
–
–
–
21
–
–
28
–
1
–
–
–
–
2
–
31
–
11
9
–
–
–
–
5
3
–
–
28
Wayuú
Kogi
Ijka
Arsario
1
6
3
6
2
T
C
C
C
C
–
–
–
–
–
–
–
1
6
3
2
7
C
–
–
–
–
–
T
T
T
T
T
–
1
6
3
2
5
T
–
–
–
–
–
C
C
C
C
–
–
1
6
3
1
9
G
A
A
A
A
–
–
–
A
A
–
–
1
6
3
1
1
T
–
–
–
–
–
–
C
–
–
–
–
1
6
3
0
9
A
–
–
–
–
–
–
–
–
–
–
G
1
6
2
9
8
T
–
–
–
–
–
C
C
C
C
C
–
1
6
2
9
7
T
–
–
–
C
–
–
–
–
–
–
–
1
6
2
9
6
C
–
–
–
–
–
–
–
–
–
–
T
C
L2a
Total
B
C1
A2
Haplotype
CRSa
SMA1
SMA3
SMA7
SMA11
SMB1
SMC1
SMC2
SMC3
SMC4
SMC5
SML1
Haplogroup
Only variable sites are shown.
a
Revised Cambridge Reference Sequence (Andrews et al. 1999, Anderson et al., 1981).
1
6
2
9
4
C
–
–
–
–
–
–
–
–
–
–
T
1
6
2
9
0
C
T
T
T
T
–
–
–
–
–
–
–
1
6
2
7
8
C
–
–
–
–
–
–
–
–
–
–
T
1
6
2
6
5
A
–
–
–
–
–
–
–
G
G
–
–
1
6
2
4
5
C
–
–
–
–
–
–
–
–
–
T
–
1
6
2
2
3
C
–
T
T
T
–
T
T
T
T
T
T
1
6
2
1
7
T
–
–
–
–
C
–
–
–
–
–
–
1
6
1
9
2
C
–
–
–
–
–
–
T
–
–
–
T
1
6
1
8
9
T
–
C
–
–
C
–
–
–
–
–
C
1
6
1
8
4
C
–
–
–
–
–
–
–
–
T
1
6
1
2
9
G
–
–
A
A
–
–
–
–
–
–
–
1
6
1
1
1
C
T
T
T
T
–
–
–
–
–
–
–
mtDNA HVS-I sequences of 110 participants (28
Arsario, 21 Kogi, 31 Ijka, and 30 Wayuú) are shown in
Table 3. Based on diagnostic CR point mutations,
sequences belong to haplogroups A (n ¼ 73), B (n ¼ 9), C
(n ¼ 27), and L2a (n ¼ 1). Eleven haplotypes characterized by 21 nucleotide variant sites were observed when
compared with the CRS (Anderson et al., 1981; Andrews
et al., 1999). Haplogroup C demonstrated the most variation and contained five haplotypes. Four lineages
belonged to the Native American A2 subhaplogroup and
a single haplotype represented B and L2a. Four haplotypes (SMA3, SMA7, SMB1, and SMC3) were shared
between at least two groups within the four study populations. Haplotypes SMA3 and SMC3 are shared by the
Kogi and Arsario, SMA7 between the Ijka and Arsario,
and SMB1 between the Wayuú and Ijka. Of the 10
Native American haplotypes detected, six (60%) of them
had not been previously reported. The most common
haplotype, SMA7 (n ¼ 37), occurs in North American
populations: Bella-Coola, Nuu-Cha-Nuluth, Haida, and
Cheyenne (Ward et al., 1991; Ward et al., 1993; Malhi
et al., 2002), but are found in lower frequencies in South
American (Pehuenche n ¼ 3, Moraga et al., 2000, Colombian Emberá n ¼ 1, Torres et al., 2006) and Caribbean
(Ciboney, n ¼ 1, Lazleua-Fox et al., 2003) groups. Haplotypes SMA3, SMB1, and SMC1 are also shared with
other Native North and South American populations.
Table 4 summarizes diversity measures and neutrality
test statistics for the four study groups, two Caribbean,
five Central, and six South American populations. The
Ijka demonstrated the lowest haplotype diversity (0.185)
of any of the groups, even lower than the Aché, who had
been previously reported to have the lowest diversity for
any South American population (Schmitt et al., 2004).
Estimates of high haplotype diversity (>0.90) were found
in the Tainos, Ciboney, Maya, Panamanian Emberá,
Mapuche, and Wounan. Nucleotide diversity levels
ranged from a low of 0.003 (Aché) to a high of 0.02
1
6
0
6
6
A
–
–
–
–
–
–
G
–
–
–
–
HVS-I sequencing
TABLE 3. mtDNA HVS-I sequences for four study population samples
Haplogroup A (65%, 68%) and C (35%, 32%) were the
only two haplogroups present in the Kogi and Arsario,
respectively. Haplogroup A (90%) was highest in the Ijka
(90%) although small frequencies of B (2.5%) and C
(7.5%) were also present. The Wayuú, contained relatively equal amounts of haplogroup A (34%), B (24%),
and C (32%). Haplogroup D was absent from all four
study populations. The Ijka exhibited the lowest haplogroup diversity (H) 0.19 and 0.15 (Briceño et al., 2003)
of any of the populations in Tables 1 or 2. The Wayuú
(0.69) demonstrated the highest H value of any of the
study populations while the Arsario (0.44), and Kogi
(0.46) showed intermediate values. Santa Marta Chibchan populations demonstrated the lowest average group
H value from Table 2.
The three Santa Marta Chibchan populations shared a
high frequency of haplogroup A with other Chibchan
populations from Central America. The presence of haplogroup C distinguished these groups from other Chibchan-speakers. This haplogroup is absent from lower
Central American populations (Kolman and Bermingham, 1997) but occurs in high frequencies in other South
American populations (Keyeux et al., 2002). The Santa
Marta populations also differed in the absence of
haplogroup B, which was detected in a single Ijka individual.
Total
mtDNA GENETIC RELATIONSHIP OF CHIBCHAN SPEAKERS
American Journal of Physical Anthropology—DOI 10.1002/ajpa
American Journal of Physical Anthropology—DOI 10.1002/ajpa
28
31
21
46
63
29
44
31
30
39
25
29
28
129
63
19
15
151
30
34
n
4
3
3
7
7
7
20
14
6
13
4
8
7
31
3
11
10
6
8
18
10
12
10
12
10
12
23
29
17
20
10
16
16
31
7
13
12
14
18
27
No. nucleotide
variant sites
0.725
0.185
0.523
0.763
0.592
0.709
0.942
0.912
0.825
0.916
0.677
0.759
0.862
0.906
0.204
0.918
0.943
0.639
0.836
0.930
Haplotype
diversity (h)
0.012
0.004
0.009
0.012
0.009
0.010
0.018
0.020
0.016
0.017
0.009
0.011
0.012
0.014
0.003
0.008
0.009
0.011
0.018
0.017
Nucleotide
diversity (p)
1.34
0.25
1.15
1.08
1.07
2.11
3.61
10.52
4.54
11.65
0.49
1.95
0.99
9.27
0.26
22.65
48.28
1.70
6.29
24.76
M
9.85
3.01
6.00
9.93
8.16
6.83
9.11
9.52
8.18
6.82
9.59
7.02
8.25
6.72
3.05
3.45
3.22
7.64
8.52
8.78
sb
8.01
9.06
8.84
8.10
7.37
5.26
6.26
9.47
7.33
6.50
7.65
4.90
5.42
5.96
7.72
3.26
3.01
6.68
8.32
2.28
sc
1.98
1.58*
0.58
1.68
1.52
0.41
0.46
0.27
0.97
0.78
0.44
0.20
0.08
0.47
0.39
0.74
0.38
1.20
1.15
0.578
Tajima’s D
TABLE 4. Diversity measures and neutrality test statistics (Chibchan populations in italics)
5.74
2.96
5.30
3.39
2.77
1.18
4.38
1.01
4.60
0.12
3.72
0.85
1.97
8.60**
3.08
4.21**
3.68*
6.89
2.87
4.90*
Fu’s Fs
0.36*
0.68
0.42
0.11
0.24
0.15
0.03
0.05
0.16**
0.03
0.32
0.08
0.06
0.04*
0.65
0.02
0.07
0.24
0.14*
0.06
Harpending’s r
Data from: TS, this study, (1) Kolman and Bermingham, 1997, (2) Kolman et al.,1995, (3) Batista et al., 1995, (4) Santos et al., 1994, (5) Ginther et al., 1993, (6) Ward et al.,
1996, (7) Merriwether et al., 2000, (8) Schmitt et al., 2004, (9) Lalueza-Fox et al., 2001, (10) Lalueza-Fox et al., 2003, (11) Williams et al. 2002, (12) Rickards et al. 1999, (13) Bolas
et al. 1995, (14) Torroni et al. 1993. ns, not significant.
b
Sudden expansion mismatch model (Rogers and Harpending, 1992).
c
Spatial expansion mismatch model (Excoffier, 2004).
* P < 0.05, **P < 0.01.
a
Arsario
IjkaTS
KogiTS
Ngöbe2
Kuna3
Huetar4
Emberá1
Wounan1
WayuúTS
Mapuche5
Xavante6
Zoro6
Gavião6
Yanomamõ7
Aché8
Tainos9
Ciboney10
Shamatari11
Cayapa12
Maya13,14
TS
Populationa
No.
haplotypes
760
P.E. MELTON ET AL.
mtDNA GENETIC RELATIONSHIP OF CHIBCHAN SPEAKERS
761
Fig. 3. Mismatch distributions of the four study populations (Arsario, Ijka, Kogi, and Wayuú). Number of nucleotide differences
are indicated along the x-axis, and the frequency of the pairs is indicated along the y-axis.
(Wounan). The Ijka were the only population with statistically significant Tajima’s D value, indicating the effects
of either expansion or selection. Four populations
(Yanaomamõ, Tainos, Ciboney, Maya) exhibited significantly negative Fu’s Fs values, indicative of population
growth. The Yanomamõ were the only population to display a significant Harpending’s r value less than 0.05,
suggesting expansion.
Mismatch distributions for all four study populations
are displayed in Figure 3 while the M and s-values for
sudden and spatial expansion models are shown in
Table 4. All distributions are either multimodal or
bimodal with peaks between 7 and 10 and a secondary
peak between 0 and 1. Multimodal peaks are common in
Native American populations and the peak between 0
and 1 may be the product of sampling related individuals or genetic drift (Lewis et al., 2005).This type of distribution is generally interpreted as a signature of population stasis (Rogers and Harpending, 1992) but others
have indicated that multimodality may be indicative of
population substructure or due to a low number of
migrants between populations (Ray et al., 2003; Excoffier, 2004). All populations in this study demonstrated M
values less than 50 (Table 4), indicating that the spatial
expansion mismatch model (Excoffier, 2004) provided a
better fit to these data than that the sudden expansion
model (Rogers and Harpending, 1992). Based on s-values
for both models the spatial expansion model generated a
better non-linear least squares fit to s, except where
M and haplotype diversity were small (Ijka, Kogi, Aché),
due to increased variance of the mismatch distribution,
that led to increased s values (Ray et al., 2003).
MJ networks for haplogroups A and C are displayed in
Figures 4 and 5. Haplogroup A (Fig. 4), contained four
satellite clusters (16129, 16187, 16189, and 16360) and
dated to 24,486 6 7,811 YBP, using the q-statistic (q ¼
1.21 6 0.39) (Forster et al., 1996; Saillard et al., 2000).
The four satellite nodes are composed mostly of Chibchan-speakers but are regionally differentiated between
Santa Marta and Central American groups. The satellite
node (16189) demonstrated that most of the variation
coalesced at 7,063 6 3,346 (q ¼ 0.35 6 0.16). The other
three satellite nodes coalesced at dates ranging from
13,894 6 12,914 (16360, q ¼ 0.68 6 0.63) to q ¼ 0.68 6
0.63 (16129, q ¼ 0.09 6 0.07) but exhibited low variability and high variances, suggestive of limited statistical
validity. Haplogroup C (Fig. 5) included a large central
node (C1), included several South American populations,
and dated to 20,473 6 5,788 (q ¼ 1.01 6 0.29). This network is star-like and presented a number of reticulations
as well as population-specific nodes. The Santa Marta
Chibchan populations were found embedded on the edge
of the network in two clusters (16265:16319:16184, and
16325:16245) and did not share nodes with other
Caribbean, Central, or South American haplogroup C
populations. Temporal estimates provided for haplogroup
A and C were consistent with other published temporal
estimates for their origins in the Americas (Schurr, 2004;
Schurr and Sherry, 2004).
Estimates of population divergence are presented in
Figure 7 and a MDS plot is shown in Figure 6. The MDS
bidimensional plot had a high goodness of fit correlation
(r ¼ 0.97) between the original data matrix and the
resulting plot. Santa Marta populations demonstrated a
more recent divergence from Central American Chibchan-speakers and the Maya and aggregate closest to
each other in Figure 7. The Ijka were the furthest Chibcha group from other Central and South American
inhabitants. The Kuna were the most distant from Santa
Marta populations, but they are recent migrants from
the Pacific coast of Colombia (Batista et al., 1995). Of all
the proposed South American Chibchan-Paezan speak-
American Journal of Physical Anthropology—DOI 10.1002/ajpa
762
P.E. MELTON ET AL.
Fig. 4. MJ Network for Haplogroup A in 20 Caribbean, South, and Central American Indigenous populations. Centered on A2
node (includes diagnostic nucleotide sites 16111, 16223, 16290, 16319, 16362).
ers, the Cayapa appeared nearest to Central American
groups, while the Yanomamõ and the Shamatari were
the most distant. The Shamatari were closer to the
Mapuche and the Aché than to the Yanomamõ who were
closest to the Colombian Wayuú. Of the four study populations, the Wayuú were furthest from the Santa Marta
Chibchan populations. The presence of Santa Marta populations near Center American Chibchan-speakers indicates that these populations may share genetic history,
however recent gene flow between groups should have
contained identical HVS-I sequences.
Intermatch distributions were calculated between
Santa Marta Chibchan-speakers (Kogi, Arsario, Ijka),
three groups (Caribbean, Central American Chibchan
and Chocoan), and regional populations (Maya, Wayuú,
Yanomamõ, etc). Figure 8a exhibited the relationship
between Santa Marta, Central Chibcha, and the Maya.
All populations in this figure displayed two intermatch
American Journal of Physical Anthropology—DOI 10.1002/ajpa
mtDNA GENETIC RELATIONSHIP OF CHIBCHAN SPEAKERS
763
Fig. 5. MJ Network for Haplogroup C in 20 Caribbean, South, and Central American Indigenous populations. Centered on CI
node (includes diagnostic nucleotide sites 16223, 16298, 16325, 16327).
peaks, with one between 7 and 10 mutation differences
and another between 2 and 3. The second peak overlapped between these groups and indicated that these
populations may have undergone a second population
expansion. This differs from the intermatch distribution
shown in Figure 8b, which showed: (1) no overlapping
second peak between Santa Marta Chibchan populations
and Caribbean groups; (2) a minor peak for Central
American Chocoan populations; and (3) was centered
around four mutations. Intermatch distributions between
the Santa Marta groups and other populations (data not
shown) all demonstrated results similar to Figure 8b.
Average-sequence variation within populations (Fig. 6)
indicated that Chocoan speakers harbored the most
genetic diversity, followed by the Mapuche, while the
Ijka and the Aché exhibited the least.
All study and comparative populations were coalescent
dated using two different methodologies (Table 5). The
method of moments (MOM) model (Rogers, 1995) presented age estimates of 9,467 (Arsario), 1,270 (Kogi), and
25,681 (Wayuú) within the study groups. Two populations (Aché, Ijka) were not dated with this technique
because ^
u was larger than m, and resulted in negative
s-values. These dates differed significantly from those
given by the sudden (Rogers and Harpending, 1992) and
spatial (Excoffier, 2004) non-linear least square models
(NLLS) mismatch models, which presented deeper temporal estimates for all populations from Table 5. Both
MOM and NLSS are based on the mismatch distribution;
however, from these data, it appeared that the NLLS
method was more sensitive to multimodality and subsequently inflated the estimated coalescent date. Dates estimated from MOM are more consistent with dates presented in the MJ networks (Figs. 4 and 5) and with those
from the archaeological record (Cooke, 2005), while NLSS
times are more consistent with older coalescent events.
American Journal of Physical Anthropology—DOI 10.1002/ajpa
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P.E. MELTON ET AL.
DISCUSSION
This study provides additional mtDNA RFLP and new
HVS-I sequence data for four indigenous Colombian populations who live in close geographic proximity but represent two distinct linguistic families. These groups all
demonstrate a northern Colombia mtDNA RFLP pattern
as suggested by Keyeux et al. (2002). The three Santa
Marta Chibchan share a number of HVS-I genetic
characteristics with linguistically related families from
Central America, including, low haplotype diversity, positive Fu’s FS values, low M-values, overlapping intermatch distributions, and low between population diversity estimates. However, these populations do not share
mtDNA haplotypes indicating that linguistic separation
for Chibchan populations more than likely occurred during the Pleistocene/Holocene transition 10,000 YBP.
These data also support the hypothesis of an early geographic expansion of Chibchan-speakers from Central
America into South America that do not genetically overlap with contemporary immigrants in the same region.
This population expansion may have been caused by
shifting climatic conditions occurring in the region
7,000–10,000 YBP that resulted in altered human subsistence strategies (Cooke, 2005). These paleo-climatic
Fig. 6. Multidimensional scaling plot of DA distances for 20
populations found in Table 4.
changes resulted in several microenvironments that
favored endogenous cultural development and genetic
homogeneity in human populations. Furthermore, as cultural complexity increased in the region, trade was facilitated, but gene flow between populations remained low.
The majority of individuals in these three Sierra
Nevada de Santa Marta Chibchan populations belong to
haplogroup A and this is shared with other Chibchan
population from lower Central America. Where these
Santa Marta Chibchan speakers differ is in the presence
of haplogroup C, which is absent in Central American
groups. Kolman and Bermingham (1997) suggested that
haplogroup C was not present throughout Chibchan
genetic history. These data shown here appear to refute
that. A potential explanation for this is that all four of
the major Native American mtDNA haplogroups were
present at the beginning of Chibchan genetic divergence
and then subsequently lost through genetic drift. All of
these Chibchan populations have gone through a significant depopulation within the last 400 years because of
European contact and these different distributions may
be representative of that. However, this explanation is
unlikely as all Native American populations went
through these severe contact depopulation events and
several of these groups contain at least four of the five
founding haplogroups and higher mtDNA diversity than
seen in Chibchan populations (Schurr and Sherry 2004,
Kolman et al., 1995). An alternate explanation is that
these individuals belonging to haplogroup C were part of
an earlier migration to South America (Keyeux et al.,
2002; Fox 1996). This is demonstrated through three
Chibchan nodes on the haplogroup C MJ network
(Fig. 5). All of these Santa Marta Chibchan populations
are deeply rooted within the MJ network and appear on
the periphery, indicative of a significant time depth for a
distinct genetic structure to appear.
The MDS plot (Fig. 6) exhibits a relationship between
Santa Marta Chibchan populations and other Central
American groups. Contrary to previous published studies
on Chibchans (Barrantes et al., 1990; Torroni et al.,
1994b; Batista et al., 1995; Kolman et al., 1995; Bieber
et al., 1996; Kolman and Bermingham, 1997; RuizNarvaez et al., 2005), we find a close affinity between
Fig. 7. HVS-I nucleotide diversity within and between populations. Average-nucleotide differences are shown within (dX along
diagonal) and between populations (dA below diagonal, distances between Chibchan populations in bold italics) using the assumption of Tamura and Nei (1993) model of substitution with a g value of 0.26.
American Journal of Physical Anthropology—DOI 10.1002/ajpa
mtDNA GENETIC RELATIONSHIP OF CHIBCHAN SPEAKERS
765
Fig. 8. Intermatch distributions of CR sequences among several populations. Panel A plots the intermatch distributions between
Sierra Nevada de Santa Marta Chibchan and 2 goups of Central American regional populations (Central American Chibchan
(Kuna, Ngöbe, Huetar) and the Quiché Maya). Panel B plots Santa Marta Chibchan groups vs. Central American Chocoan (Emberá,
Wounan), and Caribbean populations. The numbers of nucleotide differences, between all pairs of sequences among populations, are
indicated along the x-axis, and the frequency of pairs is indicated along the y-axis.
these groups and the Maya, an observation supported by
recent unpublished evidence from archaeology and
linguistics (J. Hoopes personal communication). However,
this association is based upon a single Mayan group
from Guatemala (Boles et al., 1995), while the Maya are
a large, heterogeneous group. Further mtDNA sequence
data from other groups is needed for the testing of this
hypothesis. This Mayan-Chibchan relationship is also
exhibited in the intermatch distributions between these
three groups (Fig. 8a). These populations all exhibit a
second overlapping peak that it not shared when com-
pared to other South American populations, which is suggestive of an early population expansion in the region.
Computer simulation utilizing mtDNA haplogroup
data from North America supports the hypothesis that
the continent was first colonized along coastal and riverine routes (Fix, 2005). While exact migration routes for
South American are unknown it can be assumed the first
groups of Paleoindians moved south and over time gradually evolved into several heterogeneous eastern South
American populations (Dillehay, 2000; Lavallée, 2000;
Pearson, 2002; Cooke, 2005). Chibchan populations would
American Journal of Physical Anthropology—DOI 10.1002/ajpa
766
P.E. MELTON ET AL.
TABLE 5. Coalescent time estimates for the four study populations and its mtDNA haplotypes
Population
n
s-method of momentsa
Ageb
s-least squaresc
Ageb
s-least squaresd
Ageb
Arsario
Ijka
Kogı́
Ngöbe
Kuna
Huetar
Emberá
Wounan
Wayuúe
Mapuche
Xavante
Zoro
Gavião
Yanamamõ
Aché
Tainos
Ciboney
Shamatari
Cayapa
Maya
28
31
21
46
63
27
44
31
29
39
24
29
28
129
63
19
15
151
30
34
1.04
–
0.13
0.89
1.69
1.41
3.45
3.82
2.83
4.40
0.34
1.39
1.70
3.30
–
2.39
2.19
1.21
3.97
3.32
9,467
–
1,207
8,044
15,344
12,752
31,268
34,679
25,681
39,953
3,051
12,655
15,440
29,906
–
21,673
19,874
10,938
36,000
30,158
9.83
3.00
6.00
9.92
8.14
6.83
9.11
9.95
8.17
7.93
9.52
7.02
8.24
6.22
3.00
3.45
3.01
7.65
8.52
8.78
89,185
27,218
54,436
92,256
75,702
63,519
84,723
92,535
74,124
73,749
88,536
65,286
76,632
57,846
27,218
31,301
27,390
69,406
77,390
79,658
8.01
9.06
8.84
8.10
7.37
5.26
6.26
9.47
7.33
6.50
7.65
4.90
5.42
5.96
7.72
3.26
3.01
6.68
8.32
2.28
72,672
82,199
80,203
73,489
66,686
47,722
56,975
85,919
66,503
58,972
69,406
44,456
49,174
54,073
70,041
29,577
27,309
60,606
75,485
20,685
Chibchan populations are in italics.
pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
a
s-parameter was estimated by method of moments in which ^s ¼ m ^u, where ^u ¼ ðv mÞ, where v is the variance and m is the
mean of the mismatch distribution (Rogers, 1995).
b
Coalescent times were estimated using the equation s ¼ s/2l where l is the mutation rate for mtDNA HVS-I. Ward et al. (1991)
16.5% per HVS-I nucleotide per million years mutation rate was used.
c
s-parameter was estimated by fitting the sudden expansion estimated mismatch model to the observed mismatch distribution
through a generalized non-linear least squares approach (Rogers and Harpending, 1992).
d
s-parameter was estimated by fitting the spatial expansion estimated mismatch model to the observed mismatch distribution
through a generalized non-linear least squares approach (Excoffier, 2004).
e
One Wayuú haplotype found to be of African ancestry was excluded.
have moved along the Pacific and Caribbean coasts,
while they maintained closer contact with Central American groups (Fox, 1996; Keyeux et al., 2002). These populations also share certain genetic characteristics with
populations from the northwest coast of North America,
including a high frequency of haplogroup A and a small
number of haplotypes, such as 16189 (Ward et al., 1991;
Mahli et al., 2002). However, this relationship requires
further evidence in order to support or refute it. If this
early population expansion represented a Chibchan diaspora, it is probable that the Andean cordillera slowed
movement of people further south. As population size
increased, groups were backed up into the Panamanian
isthmus, which caused the region to become more
densely populated and blocked more migrants from the
north (O’Rourke et al., 1992). Ethnohistoric data support
this argument. The two largest Chibchan-speaking populations present at contact were from Colombia and
included the Tairona, whose maximum population size
at contact has been estimated at 468,000 (Langebaek,
2003) and the Muisca whose estimated size at Spanish
contact was 500,000 (Hoopes and Fonseca, 2003). Linguistic evidence also supports this argument. Colombia
contains the second largest number of indigenous populations in South America representing 80 different
linguistic families (Yunis et al., 1994). The geographic
distribution of these languages is more numerous and
fragmented on the southeastern side of the Andes,
whereas on the northwestern side there are fewer languages and most populations have cultural and biological affinities to either Central American (Chibchan and
Chocoan) or Caribbean (Arawak and Carib) populations.
MOM (Rogers, 1995) coalescent dates (Table 4) indicated that Chibchan populations shared similar genetic
histories, with origins within the last 15,000–8,000 YBP,
which are consistent with other temporal estimates
based on classical markers (Barrantes et al., 1990),
mtDNA (Batista et al., 1995; Kolman et al., 1995; Kolman and Bermingham, 1997), and Y-chromosome (RuizNarvaez et al., 2005) data. Coalescent dates using the
NLLS method (Rogers and Harpending, 1992) give
deeper time depths and may be associated with earlier
coalescent events but may also be an artifact of the conservative phylogenetic mutation rate (Ward et al., 1991)
used in this study. The actual mtDNA mutation rate is
controversial, and estimates differ considerably between
pedigree and phylogenetic studies (Sigurgardottir et al.,
2000; Ho et al., 2005; Ho and Larson, 2006). Preliminary
analysis of these data (not shown) using an intermediate
rate of 0.66 3 105/site and assuming 27 years/generation (Sigurgardottir et al., 2000) provide estimates more
consistent with regional archaeological evidence
(Pearson, 2002; Cooke, 2005). However, archaeological
and paleoecological studies indicate that humans have
occupied the region within this time period domesticated
crops between 9,000–7,000 YBP (Cooke, 2005).
Paleoenvironmental reconstructions in the Central
and northern South America have demonstrated that
the region was cooler and drier during the Pleistocene
than at present (Cooke, 2005). This environment was
characterized by open grassy savannas and xeric habitats, inhabited by megafauna and beneficial to human
hunter-gatherers (Lynch, 1983). Climatic oscillations
during the Younger Dryas (10,000–8,500) created warmer
and moister environments, which led to a shift toward
mesic forests, while human disturbance intensified
(Cooke, 2005). Archaeological evidence from three central Panamanian sites (Carabalı́, Vampiros, and Agua-
American Journal of Physical Anthropology—DOI 10.1002/ajpa
mtDNA GENETIC RELATIONSHIP OF CHIBCHAN SPEAKERS
dulce) demonstrated the presence of four domesticated
plants: bottle gourd (Lagenaria siceraria); arrowroot
(Maranta arundinacea) lerén (Calathe allouia), and
squash dated to between 9,000–7,000 YBP. Arrowroot
has also been found at site in highland Colombia that
date between 10,000–9,000 YBP (Bray, 2000). These
Pleistocene/Holocene climate changes also led to a number of microenvironments and as people began to alter
their environment led to reduced diversity and movement among populations in the region.
The resulting subsistence shift to horticulture is
clearly demonstrated in the genetic structure of Chibchan populations, based on mtDNA. The majority of
Chibchan populations are characterized by low haplotype
diversity values relative to most other South American
groups. In addition, they all have extremely low M
values, suggesting that there is low maternal gene flow
between groups in the region. The lowered maternal
migration reduces the level of variation within the population since the only remaining source of new genetic
material is mutation. Ethnographic information supports
this assumption as most Chibchan-speakers practice
uxorilocal marriage customs (husband moves to wife’s
home) (Reichel-Dolmatoff, 1950; Kolman et al., 1995).
This matrilocality leads to the characteristic nodes found
in the phylogenetic networks (Figs. 4 and 5), in which
Chibchan groups are primarily composed of one or two
major haplotypes along with a few singletons. Other evidence for this comes from the neutrality test statistics
(Table 4). Populations that have expanded have large
significant negative values. In the case of Chibchanspeaking groups and the majority of eastern South
American groups all values are either positive or nonsignificant negative values, indicating long term population continuity. This pattern differs from Andean (Fuselli
et al., 2003; Lewis et al., 2005), Siberian, and North
American (Zlojutro et al., 2006) populations that demonstrated recent demographic expansion. As cultural complexity increased in the region beginning around 6,000
YBP (Cooke, 2005), trade was facilitated, but maternal
gene flow remained low. While early horticultural sites
are not known from the Santa Marta region, the ecology
of the region contains five major ecological zones (tropical, subtropical, temperate, páramo, and snowline) found
in South America, four of which were intensively used
by populations in the region at Spanish contact (Wilson,
1999)
The mtDNA evidence presented here supports an
in situ development for the Santa Marta populations
(Bray, 1984; Langebaek, 2003) and suggests that people
were in the area prior to the development of social complexity (Hoopes, 2005; Hoopes and Fonseca, 2003). The
presence of long term biological continuity in the region
indicates that these populations were not mobile and
this may have facilitated the adoption of the Chibchan
language. Glottochronological evidence for the origin of
Chibcha, indicate that the language arose because of
increased sedentism as a result of the introduction of
agriculture into the region between 6,000–4,000 YBP
(Constenla-Umaña, 1991). New evidence from archaeology and other disciplines suggests that this is the time
frame for regional cultural complexity and increased
diversification (Cooke, 2005) and that social stratification
began between 2,500–1,300 YBP (Hoopes, 2005). This
latter date correlates with coalescent chronologies for
the Kogi and suggests that their origins may have
occurred during this time frame. However the Kogi show
767
close genetic affinity to the Arsario, who presented a
much earlier coalescent date, consistent with other Chibchan-speaking groups from lower Central America.
CONCLUSION
Over the last decade increased scientific inquiry has
focused on Chibcha-speaking populations from lower
Central and northern South America due to their geographic location bridging the two American continents.
This research has rejected the traditional notion of the
region as a heavily trodden pathway for migrating populations and instead suggested long term occupancy and
biological continuity. While archaeological and linguistic
research has found a cultural association between
Central and South American Chibchan speaking populations, the biological relationship remains largely unresolved. This study demonstrated that northern South
and lower Central American Chibchan speakers share a
unique genetic structure but if they share common
ancestry it occurred in the distant past. We also find an
affinity between Chibchan groups and a Mayan population. In addition, we propose an early expansion of
Chibchan-speakers from Central America into northern
South America. We propose that this expansion was
precipitated by climatic changes during the PleistoceneHolocene transition and was accompanied by a subsistence shift from hunter-gathering to horticulture.
However, in order to strengthen this hypothesis further
molecular evidence is required from the boundaries of
the Chibchan linguistic frontier, the Caribbean, Mesoamerica, and from skeletal populations.
ACKNOWLEDGMENTS
We express our appreciation to the Kogi, Arsario, Ijka,
and Wayuú people, who voluntarily agreed to participate
in the study of their molecular identity. We thank
R. John Mitchell, R. van Oorschot, and J Hoopes for
helpful discussions, CM Bravi, AJ Redd, M Zlojutro for
their comments on earlier versions of this manuscript,
TG Schurr for providing PCR primer information on the
nt 104 MspI cut site and C. Langebaek and A. OyuelaCayceo for sharing their archaeological research. We also
thank the late S.S. Papiha for facilitating this investigation of Chibchan genetic history. Carroll D. Clark award
was given.
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