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Genetic portrait of the Amazonian communities of Peru and Bolivia: The legacy of the Takanan‐speaking people

Genetic portrait of the Amazonian communities of Peru and Bolivia: The legacy of the... INTRODUCTIONDuring the colonial period in South America, Catholic missionary settlements known as Reductions promoted the forced settlement of indigenous groups to improve evangelization and administration under the “Reducciones” system. The system brought together distinct Amazon ethnic groups scattered along different regions, sometimes speaking languages that were unintelligible to each other. Reductions also facilitated the spread of transmissible diseases and slavery‐like forced work and caused a major demographic decline or collapse of Native American populations (Aikhenvald, 2012; Ludescher, 2001; Métraux, 1942). Also, genetic heterogeneity was evident in the Amazon when compared with Andean populations (Tarazona‐Santos et al., 2001). Nowadays, in the Peruvian rainforest ecoregion, about 51 languages are spoken, including Kichwa (Quechua from Andean populations), which was introduced by the Jesuit and Franciscan missionaries and used as a lingua franca. The Panoan (Shipibo‐Conibo‐Cashibo), Cocama, and Piro (or Yine, an Arawakan group) are distributed mainly along the Ucayali region (part of selva central), while Jivaroan, Shawi, and Kechwa‐Lamista are in the San Martín and Loreto Departments. Furthermore, several Arawakan‐speaking communities (such as Yanesha, Ashaninka, and Machiguenga) live in the ceja de selva, ranging from Pasco to Cusco Departments. We previously described the reductions established by missionaries in several populations of San Martín and Loreto Departments (Sandoval et al., 2016) and this scenario was similar for all Amazonian tribes. DNA studies have shown genetic relatedness between the Jivaroan, Panoan, Arawakan, Cocama, and others (Barbieri et al., 2014; Di Corcia et al., 2017; Sandoval et al., 2016).In Bolivia, there are about 33 lowland ethnic groups distributed mainly in Beni, Pando, and Santa Cruz Departments. Most names of these groups are associated with Catholic missions, like Santiago de Chiquitos or Ascención de Guarayos. At the time of Spaniard military incursions (1538–1671), the Llanos de Mojos (in Beni Department) was inhabited mostly by agriculturalists like Arawak‐speaking communities (nowadays also called “mojeños,” and including the Trinitario, Ignaciano, Javeriano, Loretano, Joaquiniano, or groups with local names such as Baure) (Block, 1994; Eriksen, 2011). In 1587, the first wave of missionaries arrived in the Mojos and Santa Cruz regions from Peru and Paraguay (Román‐López & Castro‐Mojica, 2016). Between 1682 and 1744, the Jesuits founded about 25 villages, although after their expulsion in 1767, some villages were relocated, and some newly created (Block, 1994). In 1754, at least 16 ethnic groups were registered at San Ignacio de Mojos village (Bert et al., 2004). By contrast, in the Llanos de Mojos and near the Andean foothills, some ethnolinguistic groups remained isolated, such as Canichana, Movima, Cayubaba, Itonama, Yuracare, and Tsimane (Adelaar & Muysken, 2004; Erikssen, 2011).Despite the widespread admixture, it seems that the Tupian‐speakers like Guarayo (descendants of Guaraní), Siriono (or Chori), Guaraní (scattered in Beni and Santa Cruz Departments), and Chiriguano (a pejorative name given by the Incas, also called ‘Guaraní’ in colonial times) resisted Spanish incursions (Block, 1994; Métraux, 1942; Nordenskiold, 1917; Sala et al., 2019). The nomadic Siriono families avoided contact with foreigners and remained isolated, although some individuals were brought to missions such as the Chiquitos and Yuracare villages (Lehm et al., 2004). By 1984, the Siriono population was estimated as 265 inhabitants (Lehm et al., 2004). Several tribes were subservient to others; for example, the subjugated Tapiete group adopted a Tupian language from the Chiriguano tribes (Brown et al., 1974).The Boreal Chaco was also probably a refuge for some hunter‐gatherer’ groups such as the Wichi (Matacoan‐Guaycuru language, known as Weenhayek in Bolivia) and Ayoreo (Zamucoan language), an isolated group in Bolivia (scattered clans in nearby localities), which is closely related to the “Moro” or Ayore tribe from Paraguay (Brown et al., 1974; Pérez‐Diez & Salzano, 1978). With the exception of Ayoreo, it has been shown that most populations of Gran Chaco are genetically homogenous (Demarchi & García‐Ministro, 2008). Moreover, after 1870, during the rubber‐boom period, there was displacement (and enslavement) of several ethnic groups within the Peruvian–Brazilian–Bolivian tropical lowlands (Román‐López & Castro‐Mojica, 2016). Despite this complex demographic scenario, several native Amazonian groups have still preserved part of their original culture and traditions.Recent ancient and modern DNA studies identified genealogies and connections between South American populations (Barbieri et al., 2019; Borda et al., 2020; Di Corcia et al., 2017; Gnecchi‐Ruscone et al., 2019; Nakatsuka et al., 2020; Sandoval et al., 2016). However, many questions remain, particularly on the genetic relationships between Takanan and Panoan‐speaking communities who have primarily settled between the Amazonian borders of Peru, Bolivia, and Brazil (Dixon & Aikhenvald, 1999; Métraux, 1942). The Takanan‐speaking villages (also called “Esse ejas” in Perú) are scattered on the shores of the Madre de Dios, Tambopata, Heath, and Malinowski rivers (Department of Madre de Dios, Peru); Madre de Dios, Beni, Madidi, near Portachuelo Alto, and Bajo, Riberalta and Nueva Villanueva (Departments of Beni, Pando and La Paz, Bolivia). Also, there are some isolated groups near the Abuná River (a tributary of the Madeira River in Acre‐Rondonia, Brazil), which are related to the Araona language (Takanan linguistic family). On the other hand, the Panoan‐speaking communities are distributed in the Departments of Ucayali, Madre de Dios, Huánuco and Loreto (Perú), Departments of Pando and Beni (Bolivia) and in the States of Acre, Rondonia and Amazonia of Brazil (Dixon & Aikhenvald, 1999; Eriksen, 2011; Métraux, 1942). Takanan‐ and Panoan‐speaking communities appear to have a deep demographic relationship. In this regard, Panoan and Takanan linguistic families share phonological, morphological, and lexical characteristics (Adelaar & Muysken, 2004; Aikhenvald, 2012; Valenzuela & Guillaime, 2017), but controversies persist on whether corresponding populations are genetically related as there is a lack of comparative DNA patterns to corroborate or refute this hypothesis (Dixon & Aikhenvald, 1999).Within this context, to investigate genetic relationships between Takanan and Panoan‐speaking communities, we compared data from uniparental DNA markers (Y‐chromosome—paternal line, mtDNA—maternal line) and data from communities in Llanos de Mojos and other Amazonian populations, which were used as references. Following this framework, Wichi and Ayoreo communities from Bolivia were also included to understand their interrelationships or gene flow with lowland populations.MATERIAL AND METHODSEthics statement and samplingStudy data were part of a previous project (Genographic Project—South America) that was approved by the Brazilian National Ethics Committee (CONEP resolution 763/2009) and by respective local ethics committees of the Major University of San Andrés (Bolivia), and the University of San Martín de Porres—Perú (IR B00003251‐FWA0015320). Before sampling, project objectives were explained to leaders and individual participants, according to the 1964 Helsinki Declaration and its later amendments. After an informed consent sheet was signed, saliva samples were collected from volunteers using buccal swabs. In the laboratory, DNA extraction and technical genotyping studies were performed.For Y‐chromosome analysis, we included data from Di Corcia et al. (2017), Sandoval et al. (2013, 2016), Jota et al. (2016), Guevara et al. (2016), Barbieri et al. (2014), and Roewer et al. (2013). For mtDNA analysis, we also included data from Sandoval et al. (2013, 2016). The ethnolinguistic attributes for some populations were labeled according to self‐identification of the participants.Thus, Peruvian populations comprised the following: Takanan_PE (n = 33); Jivaroan (n = 145; Achuar (n = 14), Huambisa (n = 15), Jivaro (n = 20), Awajun (n = 27), Andoas (n = 33), and Kichwas (n = 36)); Arawakan_PE (n = 172; Asháninka (n = 23), Machiguenga (n = 11), Yanesha (n = 125), and Yine (n = 13)); Cocama (n = 9); Shawi (n = 9); Bora (n = 5); Panoan (n = 85; Amahuaca‐Yaminahua (n = 10), Shipibo‐Conibo (n = 49), and Cashibo (n = 26)).Bolivian populations included: Takanan_BO (Bolivia, n = 40); Reyesano (n = 17); Tsimane (n = 34); Moseten (n = 18); Movima (n = 17); Cayubaba (n = 8); Canichana (n = 10); Arawakan_BO (n = 94; Trinitario (n = 52), Mojeño (n = 10), Ignaciano (n = 15), Joaquiniano (n = 5), Javeriano_mojeño (n = 6), Baure (n = 6)); Itonama (n = 10); Chiquitano (n = 54); Tupian (n = 98; Guarayo (n = 37), Guaraní (n = 36), Siriono (n = 21), Tapiete (n = 4)); Yuracare (n = 24); Ayoreo (n = 6), and Wichi (n = 22).For mitochondrial DNA (mtDNA) analysis, Bolivian populations included: Takanan_BO (n = 47); Reyesano (n = 28); Arawakan_BO (n = 77; Ignaciano mojeño (n = 16), Trinitario mojeño (n = 17), Joaquiniano (n = 16), Javeriano‐Loretano mojeño (n = 13), Baure (n = 15)); Tsimane (n = 14), Moseten (n = 10), Movima (n = 23), Cayubaba (n = 18), Canichana (n = 18), Itonama (n = 22), Chiquitano (n = 56), Tupian (n = 112; Guarayo (n = 45), Guaraní (n = 43), Siriono (n = 24)); Yuracare (n = 16), Ayoreo (n = 7), and Wichi (n = 29).Peruvian populations included: Takanan_PE (n = 34); Jivaroan (n = 159; Achuar (n = 14), Huambisa (n = 12), Awajun (n = 24), Andoas (n = 71, included 1 new), Kichwas (n = 38, included 1 new)); Shawi (n = 11, included 3 new), Bora (n = 4), Cocama (n = 11), Arawakan_PE (n = 63; included 33 new), Panoan (n = 17, included 12 new).In addition, for Y‐STR comparisons, Parecis‐speakers (n = 10) from Brazil were included.A map showing the approximate linguistic distribution of Takanan communities of Peru and Bolivia and other references are shown (Figure 1).1FIGUREAn approximate geographical distribution of Takanan‐speaking communities among other linguistic families (references) in Peru and Bolivia.Statistical analysisFor patrilineal analysis, firstly, five single nucleotide polymorphisms (SNPs)—C‐M130, Q‐M242, Q‐M346, Q‐L54, and Q‐M3 ‐ were genotyped using a TaqMan Real Time Polymerase Chain Reaction (PCR) 7900HT system (ABI). Next, after screening the samples via other testing platforms, the derived variants were assigned (Table S1a), and 17 short tandem repeats (STRs; Yfiler; ABI) were genotyped following a standard protocol (Jota et al., 2016; Sandoval et al., 2020) and a capillary electrophoresis platform (ABI3130XL Genetic Analyzer equipment; ABI). GeneMapper ID v3.2 (Applied Biosystems, Foster City, CA, USA) was used for the determination of Y‐STR alleles.For matrilineal analysis, PCR and sequencing procedures were performed as previously reported (Sandoval et al., 2020) using the ABI3130XL Genetic Analyzer (ABI) and SeqScape v2.6 (Applied Biosystems) program. The program MitoTool (Fan & Yao, 2011) assigned the mitochondrial haplogroups. Due to uncertainty in alignments, mitochondrial sequences at positions at 303−315, 515−522, 16,182−16,193, and 16,519 were excluded from the analyses (Sandoval et al., 2020).To infer individual relationships, Network 5.0.1.0 (http://www.fluxus‐engineering.com) was used (Bandelt et al., 1999; Polzin & Daneshmand, 2003). To evaluate interpopulation relationships and genetic diversity, we used Analysis of Molecular Variance (AMOVA) in Arlequin 3.5.1.2. (Excoffier & Lischer, 2010). For spatial visualization of genetic distances, the Principal Coordinates Analysis (PCoA), implemented in GenAlEx v6.5 (http://biology.anu.au/GenAlEx) was executed as described (Sandoval et al., 2020).RESULTSY‐chromosomeA list of 17 Y‐STR haplotypes from Native American sublineages in study populations is shown in Table S1a (including data from Jota et al., 2016). Also, geographical location and linguistic affiliation details are shown in Table S1b.Phylogenetic analyses mainly showed two subgroups of Takanan‐speaking families, both from Peru (Takanan_PE) and Bolivia (Takanan_BO) and labeled as T1 and T2, respectively (Figures 2 and S1). From Figure 2, subgroup T2, which was part of the Takanan family of Peru and Bolivia (n = 16), included one Shawi from Northwest Amazonia Peru, one Chiquitano, which was connected to one Yine (Ucayali, Arawakan), and one Kichwa from the Loreto region (Jivaroan). This T2 subgroup was linked to Panoan‐speaking individuals, along with some Arawaks and several Jivaros (e.g., only two mutation steps between four Shipibo‐Conibos and eight Takanas from Peru, when compared between Peruvian populations only (Figure S2)) and suggesting a shared genetic affinity. We identified an individual who spoke the Canichana language who was related to the Panoan group. Furthermore, some Panoan‐speaking individuals outside the main branch (Shipibo‐Conibo, Amahuaca, Yaminahua, and Cashibo) were related to Arawakan individuals (only one mutation step (Figure S2)). Also, two Cocamas and one Shipibo‐Conibo shared a common haplotype according to historical demography interactions.2FIGUREMedian joining network for 15 Y‐STR haplotypes in Peruvian and Bolivian populations depicted by different colors. Haplotypes are symbolized by circles with sizes proportional to the number of individuals, and branch lengths are proportional to STR mutation steps (indicated by numbers). Dotted lines indicate a cluster of related haplotypes.The larger subgroup of the two agglomerates of Takanas (T1, n = 47, which included one Reyesano) was related (only two mutation steps) to six individuals; four Arawakan‐speaking individuals from Bolivia (Arawakan_BO) and two Jivaroan‐speaking individuals from Peru (Figures 2 and S1). This group was related to one Cocama, two Arawaks from Bolivia, and 10 Arawak‐speaking individuals from Brazil (Arawakan_BR, Parecis) (Figure 2).In another branch of the phylogenetic tree, four Takanan‐speaking individuals from Bolivia and one Tsimane shared a common haplotype (Figure S1). It should be noted that an individual from Takanan_BO was linked (by only two mutation steps) to a group of Arawaks from Peru (Arawakan_PE, especially Yanesha, n = 18). Likewise, among the Reyesano population, practically half were related to the Takanan (mainly to T2) and the other half was dispersed in the phylogenetic tree. This second group was connected to individuals from other populations, as two Reyesanos shared different haplotypes with two individuals speaking the Arawakan language of Bolivia and one with Canichana (Figure S1).In other observations, despite a genetic affinity between most individuals with the Tupian language (including Guaraní, Guarayo “y,” Siriono “s,” and Tapiete “t”), other individuals were scattered across branches like the Chiquitano, such as Arawak language speakers (Figure S1). Also, genetic affinity was observed between the majority of Tsimane (n = 9) and Moseten‐speaking (n = 22) individuals and one Yuracare‐speaking individual. They were closely related to three Movima, one Canichana, and one Reyesano‐speaking individuals. Likewise, most Guarayos (n = 28; Figure S1) shared haplotypes with four Arawak‐speakers (Arawakan_BO), including one Canichana, two Itonama, and one Movima. They also showed affinities with five Guarayos, three Guaraní‐speakers, and one Chiquitano. Moreover, four Guaraní individuals were linked to a cluster of Panoan individuals (only one, two, or three mutation steps) (Figure 2).In terms of genetic variability at the population level (comparing 21 populations), AMOVA analysis in a PCoA plot (Figure 3) showed that Takanan populations, from both Peru and Bolivia, were close to each other and also to Jivaroan‐speaking populations of Peru and Arawakan‐speaking populations of Bolivia (Arawakan_BO). Furthermore, with the exception of Jivaroan and Arawakan_PE, the genetic distance gradient between Peruvian populations corresponded with their respective geographical areas. For the Panoan population, the genetic diversity profile was closer to Bolivian than Peruvian populations. However, when observing spatial configurations between Peruvian populations, the Panoan were a little closer to Jivaroan than Takanan populations, which were analogous to analyses at the individual level (cluster T2). Also, populations distant from the central conglomerate had a very low haplotype diversity, such as Tsimane (h = 0.4189) and Yuracare (h = 0.6159) (Table S2).3FIGUREPrincipal coordinates analysis (PCoA) for Y‐STR data in Peruvian and Bolivian populations. Reynolds’ Rst coancestry distances were used. Peruvian populations are represented by squares and Bolivian populations by spheres. Cani, Canichana; Iton, Itonama; Rey, Reyesano.MtDNAGenetic analyses were performed using only Native American A2, B2, C1/C*, and D1/D4h3a mtDNA lineages. A list of mtDNA control region haplotypes with variants scored with respect to rCRS is shown (Table S3a) and haplogroup frequency data are also shown (Table S3b).From the maternal line, phylogenetic relationships showed that several individuals from different linguistic families shared haplotypes, indicating common ancestries. For example, for the A2 lineage (Figure 4), 14 Takanan‐speaking individuals from Peru shared a haplotype with two Takanan from Bolivia and two Arawakan from Peru, which in turn were related to some Panoan, one Cocama, and several Yuracare, Jivaroan, and Chiquitano speakers, including one Cayubaba and one Takanan speaker from Bolivia (n = 14, core central group sharing the same haplotype).4FIGUREMedian joining network for mtDNA haplotypes of the A2 lineage in Peruvian and Bolivian populations (n = 205), which are depicted by different colors. Mitochondrial haplotypes are symbolized by circles with sizes proportional to the number of individuals, and branch lengths are proportional to mutation steps (e.g., two nucleotide changes are indicated in the figure).For the B2 lineage (Figure 5), some Takanan from Bolivia shared different haplotypes with Arawakan and Reyesano. In the core central group, several individuals (n = 15, Jivaroan, Reyesano, Arawakan_BO, Itonama, Tupian, Cayubaba, and Movima) who shared a haplotype.5FIGUREMedian joining network for mtDNA haplotypes of the B2 lineage in Peruvian and Bolivian populations (n = 257), which are depicted by different colors. Mitochondrial haplotypes are symbolized by circles with sizes proportional to the number of individuals, and branch lengths are proportional to mutation steps (e.g., two nucleotide changes are indicated in the figure).In C1/C* lineages (Figure 6), the Takanan of Peru and Bolivia shared some haplotypes, which through a Jivaro (only one mutation step) are related to the core central group (n = 25, Jivaroan, Shawi, Arawakan_PE, Takanan_BO, Reyesano, Moseten, Canichana, Arawakan_BO, and Yuracare) that share a haplotype. Also, other distinct haplotypes were shared between individuals with different languages. In particular, one Panoan and one Arawakan_PE shared a haplotype.6FIGUREMedian joining network for mtDNA haplotypes of C1/C* lineages in Peruvian and Bolivian populations (n = 255), which are depicted by different colors. Mitochondrial haplotypes are symbolized by circles with sizes proportional to the number of individuals, and branch lengths are proportional to mutation steps (e.g., two nucleotide changes are indicated in the figure).Finally, for D1/D4 lineages (Figure 7), the Takanan and Panoan did not share haplotypes with other individuals, unlike the core central group where a haplotype was shared by other linguistic groups (n = 11, Arawakan, Cayubaba, and Tupian).7FIGUREMedian joining network for mtDNA haplotypes of D1/D4h3a lineages in Peruvian and Bolivian populations (n = 65), which are depicted by different colors. Mitochondrial haplotypes are symbolized by circles with sizes proportional to the number of individuals, and branch lengths are proportional to mutation steps (e.g., two nucleotide changes are indicated in the figure).However, at the population level (comparing 21 populations), AMOVA results in a PCoA plot (Figure 8) showed that the Takanan of Peru (Takanan_PE) were differentiated from other populations (e.g., Wichi and Ayoreo). In contrast, the Panoan population was closer to Shawi. Furthermore, the Arawakan population of Peru was more closely linked to Jivaroan and Cocama than other populations. Finally, the isolated Ayoreo population revealed a very low haplotype diversity (h = 0.2857), followed by Tsimane (h = 0.5824) and Moseten (h = 0.6444) (Table S4).8FIGUREPrincipal coordinates analysis (PCoA) for mtDNA data in Peruvian and Bolivian populations. Reynolds’ ϕst coancestry distances were used. Peruvian populations are represented by squares and Bolivian populations by spheres. Cani, Canichana; Iton, Itonama; Rey, Reyesano; Cay, Cayubaba.DISCUSSIONBased on linguistic features, the Panoan and Takanan‐speaking peoples should be closely related, but until now this hypothesis was controversial due to a lack of comparative DNA studies confirming or refuting the notion (Dixon & Aikhenvald, 1999). Moreover, a more general hypothesis of the expansion of the Arawak language in South America approximately 2.4 thousand years ago (kya) remains unclear (Eriksen, 2011). Thus, in this study, we investigated these issues and included several tropical lowland populations from Peru and Bolivia and an Arawakan community from Brazil as references as well as the Wichi and Ayoreo communities from Bolivia in the general framework.Our results indicated the Y chromosomes from a Takanan‐speaking subgroup (T2 in Figure 2) were linked to Panoan‐speaking communities. However, the Panoan and most individuals of the Takanan T1 subgroup were more closely related to Jivaroan and Arawakan‐speaking individuals. Moreover, the observation that one Cocama individual close to T1, and two Cocama and one Shipibo‐Conibo speaking individuals shared the same haplotype (Figure S2) indicated a close genetic affinity. This may have been due to remaining gene flow traces during ancient pre‐Columbian times, or more recently the Cocama‐Shipibo confederation against the priest missions, particularly in coalition with the Arawaks and Quechuas in the rebellion led by Juan Santos Atahualpa in 1742 in the central Amazonia of Peru (Adelaar & Muysken, 2004; Aikhenvald, 2012; Ludescher, 2001). These demographic interactions could partially explain the “lexical loans” in Panoan and Ashaninka, including Quechua, an imposed lingua franca in Amazonia (Fleck, 2013; Métraux, 1942). This also putatively explains the genetic affinities between three Panoan‐speaking individuals and several Arawakan‐speaking individuals from Peru.Our previous studies on Amazonian populations in Peru also showed that one Shipibo‐speaking individual not only shared a haplotype with the Cocamas, but also with two individuals from the Loreto region and one Kechwa‐Lamista (an admixed Amazonian group) individual from the San Martín region (Sandoval et al., 2016). Remarkably, this observation showed that Takanan (from Peru‐Bolivia) and Panoan (from Peru) speakers were closely related to Arawakan and Jivaroan speakers, including Cocama (Tupian).Similarly, our results were consistent with other studies at the genomic scale (via SNP chip analysis); where Panoan‐speaking communities (Shipibo‐Conibo, Cashibo, Matsés, Nahua) shared similar genomic profiles with Arawakan‐speaking populations (Ashaninka, Yanesha), including Jivaroan groups (Huambisa, Awajun, Candoshi), Kechwa‐Lamista, Piapoco (Arawakan from Colombia), Guarani, and others (Barbieri et al., 2019; Borda et al., 2020; Gnecchi‐Ruscone et al., 2019; Nieves‐Colón et al., 2020). The wide spatial distribution of this gene pool coincides with a hypothesis on the expansion of the Arawak language in South America, likely via the Madeira and Amazon rivers, which occurred approximately 2.4 kya left archaeological vestiges in areas of Llanos de Mojos (Bolivia) and 2.2 kya in the Ucayali river, Peru (Eriksen, 2011). This population expansion could be correlated with the dispersion of some domesticated plants in the last 6–4 kya (Clement et al., 2015). During this time, the following generations likely differentiated from their main linguistic branch in a similar way to the expansion history of the Macro‐Je or Tupi‐Guaraní (Tupian) linguistic groups in the central and southeastern parts of the Amazonia of Brazil (Aikhenvald, 2012; Eriksen, 2011; Ramallo et al., 2013).Our interpretations are supported by the genetic affinity between ten Pareci from Brazil (Arawakan‐speaking tribe) and several Arawakan‐speaking individuals from Bolivia, who are related to the largest group of Takanas (T1). This observation agreed with linguistics and indicated that Saraveka (extinct Arawakan language from Bolivia) was closely related to the Pareci language (Adelaar & Muysken, 2004; Métraux, 1942).In terms of the maternal line, our data suggested that in the Bolivian and Peruvian Amazonia region, high gene flow occurred. For example, some motifs in the mitochondrial control region corresponding to B2 lineage (73‐263‐499‐16189‐16217‐16519) are widely shared between many Amazonian groups in South America, regardless of their linguistic affiliation, including Andean groups (Mazières et al., 2008; Ramallo et al., 2013; Sandoval et al., 2018). In addition, although some Takanas are differentiated from other individuals, one shared a haplotype with some Arawaks (from Peru and Bolivia). For the A2 lineage, a shared haplotype existed between one Arawakan (Arawakan_PE) and some Takanan, and was related to three Panoan individuals, one Cocama and one Jivaro, suggesting a shared genetic affinity. This observation was consistent with a previous study showing two different shared haplotypes between Arawakan and Panoan groups (Di Corcia et al., 2017). Likewise, the core central group, which is shared between a Takanan (Takanan_BO), Yuracare, Chiquitano, Jivaroan, and Cayubaba, reflects a common origin. These individuals and the Takanan are linked through one Panoan‐speaking individual who is closely related to them. Another similar case was identified by the C1 lineage, where several individuals from eight linguistic groups (core central group composed of Takanan, Arawakan, Shawi, Jivaroan, Yuracare, Canichana, Moseten, and Reyesano) shared the same haplotype, indicating they were derived from common ancestors. Also, a similar picture of shared haplotypes by different linguistic groups in some Beni region populations was previously reported (Bert et al., 2004).Among other studied populations, our results showed that the maternal haplotype diversity of Ayoreo‐speaking community has been dramatically impacted by genetic drift (h = 0.29), a picture that coincides with previous genetic studies of Gran Chaco populations (Demarchi & García‐Ministro, 2008). In the paternal line, like Tsimane (h = 0.42), the Siriono showed the lowest haplotype diversity (h = 0.41; n = 21, only three different haplotypes, data not shown in the Table S2), followed by the Guarayo (h = 0.43, data not shown in the Table S2). These groups were separated from other populations (data not shown in the PCoA plot), which was consistent with the picture described at the individual level and with historical records (Lehm et al., 2004; Métraux, 1942). The isolated populations likely were impacted by lower gene flow or bottlenecks. Meanwhile, at the individual level, one Guaraní‐speaker shared a haplotype with one Wichi. Regarding this, an Argentinian Wichi community also shared haplotypes with other Matacoan‐speaking groups such as Toba and Pilagá in the Gran Chaco region (Sala et al., 2019). Thus, both patrilineal and matrilineal analyses indicated close interrelationships and acculturation occurring in the lowlands of Bolivia, southern Brazil, western Paraguay and northern Argentina in congruence with ethnographical, linguistic, and genetic studies (Bert et al., 2004; Block, 1994; Brown et al., 1974; Demarchi & García‐Ministro, 2008; Eriksen, 2011; Métraux, 1942; Ramallo et al., 2013).Although some populations were isolated due to historical or socio‐political reasons, for example, the distant position of the Tsimane and Yuracare Bolivian communities in two‐dimensional PCoA spaces (paternal and maternal lines), we also showed that in the Peruvian and Bolivian Amazonia, there was intense inter‐population migration in line with historical records.Finally, we suggest that the Takanan, like Panoan, Cocama, and Jivaroan speakers, were derived from ancient Arawak groups that were spread through the western Amazonia of South America, providing a plausible explanation that overlaps with archaeological and linguistic arguments.AUTHOR CONTRIBUTIONConceived and designed experiments: José R. Sandoval, Ricardo Fujita, and Fabricio R. Santos. Collected samples: José R. Sandoval, Ricardo Fujita, Fabricio R. Santos, Susana Revollo, and Cinthia Cuellar. Performed laboratory experiments: José R. Sandoval, Daniela R. Lacerda, Marilza S. Jota, and Cinthia Cuellar. Analyzed data and wrote the manuscript: José R. Sandoval. All authors reviewed and approved the final version of the manuscript.ACKNOWLEDGMENTSWe thank all volunteers who donated biological samples to the previous South American Genographic Projects. We also thank Oscar Acosta, Pedro Paulo R. Vieira, David Soria H., Daniela Arteaga, Alejandro Estrada, and Donaldo Pinedo for their support in fieldwork. This study received funds from the National Geographic Society (The Genographic Project‐South America) and grants from USMP (E10012019010) of Peru, FAPEMIG and CNPq of Brazil.CONFLICT OF INTEREST STATEMENTThe authors declare no conflict of interest.DATA AVAILABILITY STATEMENTThe Y‐STRs and mtDNA data are available in the Supplementary Material files: Figures S1 and S2 and Tables S1–S4.REFERENCESAdelaar, W. F. H., & Muysken, P. C. (2004). The languages of the Andes. Cambridge CB2 2RU UK: Cambridge University Press.Aikhenvald, A. Y. (2012). The languages of the Amazon. United Kingdom: Published to Oxford Scholarship Online. https://doi.org/10.1093/acprof:oso/9780199593569.003.0001Bandelt, H. J., Forster, P., & Röhl, A. (1999). Median‐Joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1), 37–48.Barbieri, C., Barquera, R., Arias, L., Sandoval, J. R., Acosta, O., Zurita, C., Aguilar‐Campos, A., Tito‐Álvarez, A. M., Serrano‐Osuna, R., Gray, R. D., Mafessoni, F., Heggarty, P., Shimizu, K. K., Fujita, R., Stoneking, M., Pugach, I., & Fehren‐Schmitz, L. (2019). The current genomic landscape of western South America: Andes, Amazonia and Pacific Coast. Molecular Biology and Evolution, 36(12), 2698–2713.Barbieri, C., Heggarty, P., Yang Yao, D., Ferri, G., De Fanti, S., Sarno, S., Ciani, G., Boattini, A., Luiselli, D., & Pettener, D. (2014). Between Andes and Amazon: The genetic profile of the Arawak‐speaking Yanesha. American Journal of Physical Anthropology, 155, 600–609.Bert, F., Corella, A., Gené, M., Pérez‐Pérez, A., & Turbón, D. (2004). Mitochondrial DNA diversity in the Llanos de Moxos: Moxo, Movima and Yuracare Amerindian populations from Bolivia lowlands. Annals of Human Biology, 31(1), 9–28.Block, D. (1994). Mission culture on the upper Amazon: Native tradition, Jesuit enterprise, and secular policy in Moxos. pp. 1660–1880 USA: University of Nebraska Press.Borda, V., Alvim, I., Mendes, M., Silva‐Carvalho, C., Soares‐Souza, G. B., Leal, T. P., Furlan, V., Scliar, M. O., Zamudio, R., Zolini, C., Araújo, G. S., Luizon, M. R., Padilla, C., Cáceres, O., Levano, K., Sánchez, C., Trujillo, O., Flores‐Villanueva, P. O., Dean, M., … Guio, H. (2020). The genetic structure and adaptation of Andean highlanders and Amazonians are influenced by the interplay between geography and culture. Proceedings National Academy of Science USA, 117(51), 32557–32565.Brown, S. M., Gajdusek, D. C., Leyshon, W. C., Steinberg, A. G., Brown, K. S., & Curtain, C. C. (1974). Genetic studies in Paraguay: Blood group, red cell, and serum genetic patterns of the Guayaki and Ayore indians, Mennonite settlers, and seven other indian tribes of the Paraguayan Chaco. American Journal of Physical Anthropology, 41, 317–344.Clement, C. R., Denevan, W. M., Heckenberger, M. J., Junqueira, A. B., Neves, E. G., Teixeira, W. G., & Woods, W. I. (2015). The domestication of Amazonia before European conquest. Proceedings of the Royal Society B, 282, 20150813.Demarchi, D. A., & García‐Ministro, A. (2008). Genetic structure of native populations from the Gran Chaco region, South America. International Journal of Human Genetics, 8(1‐2), 131–141.Di Corcia, T., Sanchez Mellado, C., Davila Francia, T. J., Ferri, G., Sarno, S., Luiselli, D., & Rickards, O. (2017). East of the Andes: The genetic profile of the Peruvian Amazon populations. American Journal of Physical Anthropology, 163(2), 328–338.Dixon, R. M. W., & Aikhenvald, A. Y. (1999). The Amazonian Languages. Cambridge CB2 2RU, UK: Cambridge University Press.Eriksen, L. (2011). Nature and culture in prehistoric Amazonia: Using G.I.S. to reconstruct ancient ethnogenetic processes from archaeology, linguistics, geography, and ethnohistory. Lund, Sweden: Human Ecology Division, Lund University.Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567.Fan, L., & Yao, Y. G. (2011). MitoTool: A web server for the analysis and retrieval of human mitochondrial DNA sequence variations. Mitochondrion, 11, 351–356.Fleck, D. W. (2013). Panoan languages and linguistics. Anthropological Papers of the American Museum of Natural History, 99, 1–112.Gnecchi‐Ruscone, G. A., Sarno, S., De Fanti, S., Gianvincenzo, L., Giuliani, C., Boattini, A., Bortolini, E., Di Corcia, T., Sanchez Mellado, C., Dávila Francia, T. J., Gentilini, D., Di Blasio, A. M., Di Cosimo, P., Cilli, E., Gonzalez‐Martin, A., Franceschi, C., Franceschi, Z. A., Rickards, O., Sazzini, M., … Pettener, D. (2019). Dissecting the pre‐Columbian genomic ancestry of Native Americans along the Andes‐Amazonia divide. Molecular Biology and Evolution, 36(6), 1254–1269.Guevara, E. K., Palo, J. U., Guillén, S., & Sajantila, A. (2016). MtDNA and Y‐chromosomal diversity in the Chachapoya, a population from the northeast Peruvian Andes‐Amazon divide. American Journal of Human Biology, 28(6), 857–867.Jota, M. S., Lacerda, D. R., Sandoval, J. R., Vieira, P. P. R., Ohasi, D., Santos‐Júnior, J. E., Acosta, O., Cuellar, C., Revollo, S., Paz‐y‐Miño, C., Fujita, R., Vallejo, G. A., Schurr, T. G., Tarazona‐Santos, E. M., Pena, S. D. J., Ayub, Q., Tyler‐Smith, C., Santos, F. R., & The Genographic Consortium. (2016). New native South American Y chromosome lineages. Journal of Human Genetics, 61(7), 593–603.Lehm, Z., Townsend, W., Salas, H., & Lara, K. (2004). Bolivia: Estrategias, problemas y desafíos en la gestión del territorio indígena Siriono. Copenhague, Dinamarca: IWGIA.Ludescher, M. (2001). Instituciones y prácticas coloniales en la Amazonia peruana: Pasado y presente. Indiana, 17/18, 313–359.Mazières, S., Guitard, E., Crubézy, E., Dugoujon, J. M., Bortolini, M. C., Bonatto, S. L., Hutz, M. H., Bois, E., Tiouka, F., Larrouy, G., & Salzano, F. M. (2008). Uniparental (mtDNA, Y‐chromosome) polymorphisms in French Guiana and two related populations—Implications for the region's colonization. Annals of Human Genetics, 72, 145–156.Métraux, A. (1942). The native tribes of eastern Bolivia and western Mato Grosso, Vol. 134, Washington, USA: Smithsonian Institution Bureau of American Ethnology.Nakatsuka, N., Lazaridis, I., Barbieri, C., Skoglund, P., Rohland, N., Mallick, S., Harkins‐Kinkaid, K., Ferry, M., Harney, É., Michel, M., Stewardson, K., Forst, J., Durruty, M. A., Beresford‐Jones, D., Burger, R., Capriles, J., Fujita, R., Isla, J., Lau, G., … Fehren‐Schmitz, L. (2020). A paleogenomic reconstruction of the deep population history of the Andes. Cell, 181(5), 1131–1145.E21.Nieves‐Colón, M. A., Pestle, W. J., Reynolds, A. W., Llamas, B., de la Fuente, C., Fowler, K., Skerry, K. M., Crespo‐Torres, E., Bustamante, C. D., & Stone, A. C. (2020). Ancient DNA reconstructs the genetic legacies of precontact Puerto Rico communities. Molecular Biology and Evolution, 37(3), 611–626.Nordenskiold, B. E. (1917). The Guarani invasion of the Inca empire in the sixteenth century: An historical Indian migration. Geographical Review, 4, 103–121.Pérez‐Diez, A. A., & Salzano, F. M. (1978). Evolutionary implications of the ethnography and demography of Ayoreo indians. Journal of Human Evolution, 7, 253–268.Polzin, T., & Daneshmand, S. V. (2003). On Steiner trees and minimum spanning trees in hypergraphs. Operations Research Letters, 31, 12–20.Ramallo, V., Bisso‐Machado, R., Bravi, C., Coble, M. D., Salzano, F. M., Hünemeier, T., & Bortolini, M. C. (2013). Demographic expansions in South America: Enlightening a complex scenario with genetic and linguistic data. American Journal of Physical Anthropology, 150(3), 453–463.Roewer, L., Nothnagel, M., Gusmão, L., Gomes, V., González, M., Corach, D., Sala, A., Alechine, E., Palha, T., Santos, N., Ribeiro‐dos‐Santos, A., Geppert, M., Willuweit, S., Nagy, M., Zweynert, S., Baeta, M., Núñez, C., Martínez‐Jarreta, B., González‐Andrade, F., … Krawczak, M. (2013). Continent‐wide decoupling of Y‐chromosomal genetic variation from language and geography in native South Americans. Plos Genetics, 9(4), e1003460.Román‐López, D. A. E., & Castro‐Mojica, M. B. (2016). Amazonía boliviana. Visibilizando la diversidad de los pueblos de Tierras bajas. La Paz, Bolivia: ISEAT.Sala, A., Caputo, M., & Corach, D. (2019). Genetic structure of Mataco‐Guaycurú speakers from Argentina and the extent of their genetic admixture with neighbouring urban populations. Scientific Reports, 9, 17559.Sandoval, J. R., Lacerda, D. R., Acosta, O., Jota, M. S., Robles‐Ruiz, P., Salazar‐Granara, A., Vieira, P. P. R., Paz‐y‐Miño, C., Fujita, R., & Santos, F. R., & The Genographic Project Consortium. (2016). The genetic history of Peruvian Quechua‐Lamistas and Chankas: Uniparental DNA patterns among autochthonous Amazonian and Andean populations. Annals of Human Genetics, 80, 88–101.Sandoval, J. R., Lacerda, D. R., Jota, M. S., Elward, R., Acosta, O., Pinedo, D., Danos, P., Cuellar, C., Revollo, S., Santos, F. R., & Fujita, R. (2018). Genetic ancestry of families of putative Inka descent. Molecular Genetics and Genomics, 293(4), 873–881.Sandoval, J. R., Lacerda, D. R., Jota, M. S., Robles‐Ruiz, P., Danos, P., Paz‐y‐Miño, C., Wells, S., Santos, F. R., & Fujita, R. (2020). Tracing the genetic history of the ´Cañaris´ from Ecuador and Peru using uniparental DNA markers. BMC Genomics, 21(7), 413.Sandoval, J. R., Lacerda, D. R., Jota, M. S. A., Salazar‐Granara, A., Vieira, P. P. R., Acosta, O., Cuellar, C., Revollo, S., Fujita, R., & Santos, F. R., & The Genographic Project Consortium. (2013). The genetic history of indigenous populations of the Peruvian and Bolivian Altiplano: The legacy of the Uros. PLoS ONE, 8, e73006.Tarazona‐Santos, E., Carvalho‐Silva, D. R., Pettener, D., Luiselli, D., De Stefano, G. F., Labarga, C. M., Rickards, O., Tyler‐Smith, C., Pena, S. D. J., & Santos, F. R. (2001). Genetic differentiation in south Amerindians is related to environmental and cultural diversity: Evidence from the Y chromosome. American Journal of Human Genetics, 68, 1485–1496.Valenzuela, P., & Guillaume, A. (2017). Estudios sincrónicos y diacrónicos sobre lenguas Pano y Takana: Una introducción. Amerindia, 39(1), 1–49. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Annals of Human Genetics Wiley

Genetic portrait of the Amazonian communities of Peru and Bolivia: The legacy of the Takanan‐speaking people

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© 2023 John Wiley & Sons Ltd/University College London.
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Abstract

INTRODUCTIONDuring the colonial period in South America, Catholic missionary settlements known as Reductions promoted the forced settlement of indigenous groups to improve evangelization and administration under the “Reducciones” system. The system brought together distinct Amazon ethnic groups scattered along different regions, sometimes speaking languages that were unintelligible to each other. Reductions also facilitated the spread of transmissible diseases and slavery‐like forced work and caused a major demographic decline or collapse of Native American populations (Aikhenvald, 2012; Ludescher, 2001; Métraux, 1942). Also, genetic heterogeneity was evident in the Amazon when compared with Andean populations (Tarazona‐Santos et al., 2001). Nowadays, in the Peruvian rainforest ecoregion, about 51 languages are spoken, including Kichwa (Quechua from Andean populations), which was introduced by the Jesuit and Franciscan missionaries and used as a lingua franca. The Panoan (Shipibo‐Conibo‐Cashibo), Cocama, and Piro (or Yine, an Arawakan group) are distributed mainly along the Ucayali region (part of selva central), while Jivaroan, Shawi, and Kechwa‐Lamista are in the San Martín and Loreto Departments. Furthermore, several Arawakan‐speaking communities (such as Yanesha, Ashaninka, and Machiguenga) live in the ceja de selva, ranging from Pasco to Cusco Departments. We previously described the reductions established by missionaries in several populations of San Martín and Loreto Departments (Sandoval et al., 2016) and this scenario was similar for all Amazonian tribes. DNA studies have shown genetic relatedness between the Jivaroan, Panoan, Arawakan, Cocama, and others (Barbieri et al., 2014; Di Corcia et al., 2017; Sandoval et al., 2016).In Bolivia, there are about 33 lowland ethnic groups distributed mainly in Beni, Pando, and Santa Cruz Departments. Most names of these groups are associated with Catholic missions, like Santiago de Chiquitos or Ascención de Guarayos. At the time of Spaniard military incursions (1538–1671), the Llanos de Mojos (in Beni Department) was inhabited mostly by agriculturalists like Arawak‐speaking communities (nowadays also called “mojeños,” and including the Trinitario, Ignaciano, Javeriano, Loretano, Joaquiniano, or groups with local names such as Baure) (Block, 1994; Eriksen, 2011). In 1587, the first wave of missionaries arrived in the Mojos and Santa Cruz regions from Peru and Paraguay (Román‐López & Castro‐Mojica, 2016). Between 1682 and 1744, the Jesuits founded about 25 villages, although after their expulsion in 1767, some villages were relocated, and some newly created (Block, 1994). In 1754, at least 16 ethnic groups were registered at San Ignacio de Mojos village (Bert et al., 2004). By contrast, in the Llanos de Mojos and near the Andean foothills, some ethnolinguistic groups remained isolated, such as Canichana, Movima, Cayubaba, Itonama, Yuracare, and Tsimane (Adelaar & Muysken, 2004; Erikssen, 2011).Despite the widespread admixture, it seems that the Tupian‐speakers like Guarayo (descendants of Guaraní), Siriono (or Chori), Guaraní (scattered in Beni and Santa Cruz Departments), and Chiriguano (a pejorative name given by the Incas, also called ‘Guaraní’ in colonial times) resisted Spanish incursions (Block, 1994; Métraux, 1942; Nordenskiold, 1917; Sala et al., 2019). The nomadic Siriono families avoided contact with foreigners and remained isolated, although some individuals were brought to missions such as the Chiquitos and Yuracare villages (Lehm et al., 2004). By 1984, the Siriono population was estimated as 265 inhabitants (Lehm et al., 2004). Several tribes were subservient to others; for example, the subjugated Tapiete group adopted a Tupian language from the Chiriguano tribes (Brown et al., 1974).The Boreal Chaco was also probably a refuge for some hunter‐gatherer’ groups such as the Wichi (Matacoan‐Guaycuru language, known as Weenhayek in Bolivia) and Ayoreo (Zamucoan language), an isolated group in Bolivia (scattered clans in nearby localities), which is closely related to the “Moro” or Ayore tribe from Paraguay (Brown et al., 1974; Pérez‐Diez & Salzano, 1978). With the exception of Ayoreo, it has been shown that most populations of Gran Chaco are genetically homogenous (Demarchi & García‐Ministro, 2008). Moreover, after 1870, during the rubber‐boom period, there was displacement (and enslavement) of several ethnic groups within the Peruvian–Brazilian–Bolivian tropical lowlands (Román‐López & Castro‐Mojica, 2016). Despite this complex demographic scenario, several native Amazonian groups have still preserved part of their original culture and traditions.Recent ancient and modern DNA studies identified genealogies and connections between South American populations (Barbieri et al., 2019; Borda et al., 2020; Di Corcia et al., 2017; Gnecchi‐Ruscone et al., 2019; Nakatsuka et al., 2020; Sandoval et al., 2016). However, many questions remain, particularly on the genetic relationships between Takanan and Panoan‐speaking communities who have primarily settled between the Amazonian borders of Peru, Bolivia, and Brazil (Dixon & Aikhenvald, 1999; Métraux, 1942). The Takanan‐speaking villages (also called “Esse ejas” in Perú) are scattered on the shores of the Madre de Dios, Tambopata, Heath, and Malinowski rivers (Department of Madre de Dios, Peru); Madre de Dios, Beni, Madidi, near Portachuelo Alto, and Bajo, Riberalta and Nueva Villanueva (Departments of Beni, Pando and La Paz, Bolivia). Also, there are some isolated groups near the Abuná River (a tributary of the Madeira River in Acre‐Rondonia, Brazil), which are related to the Araona language (Takanan linguistic family). On the other hand, the Panoan‐speaking communities are distributed in the Departments of Ucayali, Madre de Dios, Huánuco and Loreto (Perú), Departments of Pando and Beni (Bolivia) and in the States of Acre, Rondonia and Amazonia of Brazil (Dixon & Aikhenvald, 1999; Eriksen, 2011; Métraux, 1942). Takanan‐ and Panoan‐speaking communities appear to have a deep demographic relationship. In this regard, Panoan and Takanan linguistic families share phonological, morphological, and lexical characteristics (Adelaar & Muysken, 2004; Aikhenvald, 2012; Valenzuela & Guillaime, 2017), but controversies persist on whether corresponding populations are genetically related as there is a lack of comparative DNA patterns to corroborate or refute this hypothesis (Dixon & Aikhenvald, 1999).Within this context, to investigate genetic relationships between Takanan and Panoan‐speaking communities, we compared data from uniparental DNA markers (Y‐chromosome—paternal line, mtDNA—maternal line) and data from communities in Llanos de Mojos and other Amazonian populations, which were used as references. Following this framework, Wichi and Ayoreo communities from Bolivia were also included to understand their interrelationships or gene flow with lowland populations.MATERIAL AND METHODSEthics statement and samplingStudy data were part of a previous project (Genographic Project—South America) that was approved by the Brazilian National Ethics Committee (CONEP resolution 763/2009) and by respective local ethics committees of the Major University of San Andrés (Bolivia), and the University of San Martín de Porres—Perú (IR B00003251‐FWA0015320). Before sampling, project objectives were explained to leaders and individual participants, according to the 1964 Helsinki Declaration and its later amendments. After an informed consent sheet was signed, saliva samples were collected from volunteers using buccal swabs. In the laboratory, DNA extraction and technical genotyping studies were performed.For Y‐chromosome analysis, we included data from Di Corcia et al. (2017), Sandoval et al. (2013, 2016), Jota et al. (2016), Guevara et al. (2016), Barbieri et al. (2014), and Roewer et al. (2013). For mtDNA analysis, we also included data from Sandoval et al. (2013, 2016). The ethnolinguistic attributes for some populations were labeled according to self‐identification of the participants.Thus, Peruvian populations comprised the following: Takanan_PE (n = 33); Jivaroan (n = 145; Achuar (n = 14), Huambisa (n = 15), Jivaro (n = 20), Awajun (n = 27), Andoas (n = 33), and Kichwas (n = 36)); Arawakan_PE (n = 172; Asháninka (n = 23), Machiguenga (n = 11), Yanesha (n = 125), and Yine (n = 13)); Cocama (n = 9); Shawi (n = 9); Bora (n = 5); Panoan (n = 85; Amahuaca‐Yaminahua (n = 10), Shipibo‐Conibo (n = 49), and Cashibo (n = 26)).Bolivian populations included: Takanan_BO (Bolivia, n = 40); Reyesano (n = 17); Tsimane (n = 34); Moseten (n = 18); Movima (n = 17); Cayubaba (n = 8); Canichana (n = 10); Arawakan_BO (n = 94; Trinitario (n = 52), Mojeño (n = 10), Ignaciano (n = 15), Joaquiniano (n = 5), Javeriano_mojeño (n = 6), Baure (n = 6)); Itonama (n = 10); Chiquitano (n = 54); Tupian (n = 98; Guarayo (n = 37), Guaraní (n = 36), Siriono (n = 21), Tapiete (n = 4)); Yuracare (n = 24); Ayoreo (n = 6), and Wichi (n = 22).For mitochondrial DNA (mtDNA) analysis, Bolivian populations included: Takanan_BO (n = 47); Reyesano (n = 28); Arawakan_BO (n = 77; Ignaciano mojeño (n = 16), Trinitario mojeño (n = 17), Joaquiniano (n = 16), Javeriano‐Loretano mojeño (n = 13), Baure (n = 15)); Tsimane (n = 14), Moseten (n = 10), Movima (n = 23), Cayubaba (n = 18), Canichana (n = 18), Itonama (n = 22), Chiquitano (n = 56), Tupian (n = 112; Guarayo (n = 45), Guaraní (n = 43), Siriono (n = 24)); Yuracare (n = 16), Ayoreo (n = 7), and Wichi (n = 29).Peruvian populations included: Takanan_PE (n = 34); Jivaroan (n = 159; Achuar (n = 14), Huambisa (n = 12), Awajun (n = 24), Andoas (n = 71, included 1 new), Kichwas (n = 38, included 1 new)); Shawi (n = 11, included 3 new), Bora (n = 4), Cocama (n = 11), Arawakan_PE (n = 63; included 33 new), Panoan (n = 17, included 12 new).In addition, for Y‐STR comparisons, Parecis‐speakers (n = 10) from Brazil were included.A map showing the approximate linguistic distribution of Takanan communities of Peru and Bolivia and other references are shown (Figure 1).1FIGUREAn approximate geographical distribution of Takanan‐speaking communities among other linguistic families (references) in Peru and Bolivia.Statistical analysisFor patrilineal analysis, firstly, five single nucleotide polymorphisms (SNPs)—C‐M130, Q‐M242, Q‐M346, Q‐L54, and Q‐M3 ‐ were genotyped using a TaqMan Real Time Polymerase Chain Reaction (PCR) 7900HT system (ABI). Next, after screening the samples via other testing platforms, the derived variants were assigned (Table S1a), and 17 short tandem repeats (STRs; Yfiler; ABI) were genotyped following a standard protocol (Jota et al., 2016; Sandoval et al., 2020) and a capillary electrophoresis platform (ABI3130XL Genetic Analyzer equipment; ABI). GeneMapper ID v3.2 (Applied Biosystems, Foster City, CA, USA) was used for the determination of Y‐STR alleles.For matrilineal analysis, PCR and sequencing procedures were performed as previously reported (Sandoval et al., 2020) using the ABI3130XL Genetic Analyzer (ABI) and SeqScape v2.6 (Applied Biosystems) program. The program MitoTool (Fan & Yao, 2011) assigned the mitochondrial haplogroups. Due to uncertainty in alignments, mitochondrial sequences at positions at 303−315, 515−522, 16,182−16,193, and 16,519 were excluded from the analyses (Sandoval et al., 2020).To infer individual relationships, Network 5.0.1.0 (http://www.fluxus‐engineering.com) was used (Bandelt et al., 1999; Polzin & Daneshmand, 2003). To evaluate interpopulation relationships and genetic diversity, we used Analysis of Molecular Variance (AMOVA) in Arlequin 3.5.1.2. (Excoffier & Lischer, 2010). For spatial visualization of genetic distances, the Principal Coordinates Analysis (PCoA), implemented in GenAlEx v6.5 (http://biology.anu.au/GenAlEx) was executed as described (Sandoval et al., 2020).RESULTSY‐chromosomeA list of 17 Y‐STR haplotypes from Native American sublineages in study populations is shown in Table S1a (including data from Jota et al., 2016). Also, geographical location and linguistic affiliation details are shown in Table S1b.Phylogenetic analyses mainly showed two subgroups of Takanan‐speaking families, both from Peru (Takanan_PE) and Bolivia (Takanan_BO) and labeled as T1 and T2, respectively (Figures 2 and S1). From Figure 2, subgroup T2, which was part of the Takanan family of Peru and Bolivia (n = 16), included one Shawi from Northwest Amazonia Peru, one Chiquitano, which was connected to one Yine (Ucayali, Arawakan), and one Kichwa from the Loreto region (Jivaroan). This T2 subgroup was linked to Panoan‐speaking individuals, along with some Arawaks and several Jivaros (e.g., only two mutation steps between four Shipibo‐Conibos and eight Takanas from Peru, when compared between Peruvian populations only (Figure S2)) and suggesting a shared genetic affinity. We identified an individual who spoke the Canichana language who was related to the Panoan group. Furthermore, some Panoan‐speaking individuals outside the main branch (Shipibo‐Conibo, Amahuaca, Yaminahua, and Cashibo) were related to Arawakan individuals (only one mutation step (Figure S2)). Also, two Cocamas and one Shipibo‐Conibo shared a common haplotype according to historical demography interactions.2FIGUREMedian joining network for 15 Y‐STR haplotypes in Peruvian and Bolivian populations depicted by different colors. Haplotypes are symbolized by circles with sizes proportional to the number of individuals, and branch lengths are proportional to STR mutation steps (indicated by numbers). Dotted lines indicate a cluster of related haplotypes.The larger subgroup of the two agglomerates of Takanas (T1, n = 47, which included one Reyesano) was related (only two mutation steps) to six individuals; four Arawakan‐speaking individuals from Bolivia (Arawakan_BO) and two Jivaroan‐speaking individuals from Peru (Figures 2 and S1). This group was related to one Cocama, two Arawaks from Bolivia, and 10 Arawak‐speaking individuals from Brazil (Arawakan_BR, Parecis) (Figure 2).In another branch of the phylogenetic tree, four Takanan‐speaking individuals from Bolivia and one Tsimane shared a common haplotype (Figure S1). It should be noted that an individual from Takanan_BO was linked (by only two mutation steps) to a group of Arawaks from Peru (Arawakan_PE, especially Yanesha, n = 18). Likewise, among the Reyesano population, practically half were related to the Takanan (mainly to T2) and the other half was dispersed in the phylogenetic tree. This second group was connected to individuals from other populations, as two Reyesanos shared different haplotypes with two individuals speaking the Arawakan language of Bolivia and one with Canichana (Figure S1).In other observations, despite a genetic affinity between most individuals with the Tupian language (including Guaraní, Guarayo “y,” Siriono “s,” and Tapiete “t”), other individuals were scattered across branches like the Chiquitano, such as Arawak language speakers (Figure S1). Also, genetic affinity was observed between the majority of Tsimane (n = 9) and Moseten‐speaking (n = 22) individuals and one Yuracare‐speaking individual. They were closely related to three Movima, one Canichana, and one Reyesano‐speaking individuals. Likewise, most Guarayos (n = 28; Figure S1) shared haplotypes with four Arawak‐speakers (Arawakan_BO), including one Canichana, two Itonama, and one Movima. They also showed affinities with five Guarayos, three Guaraní‐speakers, and one Chiquitano. Moreover, four Guaraní individuals were linked to a cluster of Panoan individuals (only one, two, or three mutation steps) (Figure 2).In terms of genetic variability at the population level (comparing 21 populations), AMOVA analysis in a PCoA plot (Figure 3) showed that Takanan populations, from both Peru and Bolivia, were close to each other and also to Jivaroan‐speaking populations of Peru and Arawakan‐speaking populations of Bolivia (Arawakan_BO). Furthermore, with the exception of Jivaroan and Arawakan_PE, the genetic distance gradient between Peruvian populations corresponded with their respective geographical areas. For the Panoan population, the genetic diversity profile was closer to Bolivian than Peruvian populations. However, when observing spatial configurations between Peruvian populations, the Panoan were a little closer to Jivaroan than Takanan populations, which were analogous to analyses at the individual level (cluster T2). Also, populations distant from the central conglomerate had a very low haplotype diversity, such as Tsimane (h = 0.4189) and Yuracare (h = 0.6159) (Table S2).3FIGUREPrincipal coordinates analysis (PCoA) for Y‐STR data in Peruvian and Bolivian populations. Reynolds’ Rst coancestry distances were used. Peruvian populations are represented by squares and Bolivian populations by spheres. Cani, Canichana; Iton, Itonama; Rey, Reyesano.MtDNAGenetic analyses were performed using only Native American A2, B2, C1/C*, and D1/D4h3a mtDNA lineages. A list of mtDNA control region haplotypes with variants scored with respect to rCRS is shown (Table S3a) and haplogroup frequency data are also shown (Table S3b).From the maternal line, phylogenetic relationships showed that several individuals from different linguistic families shared haplotypes, indicating common ancestries. For example, for the A2 lineage (Figure 4), 14 Takanan‐speaking individuals from Peru shared a haplotype with two Takanan from Bolivia and two Arawakan from Peru, which in turn were related to some Panoan, one Cocama, and several Yuracare, Jivaroan, and Chiquitano speakers, including one Cayubaba and one Takanan speaker from Bolivia (n = 14, core central group sharing the same haplotype).4FIGUREMedian joining network for mtDNA haplotypes of the A2 lineage in Peruvian and Bolivian populations (n = 205), which are depicted by different colors. Mitochondrial haplotypes are symbolized by circles with sizes proportional to the number of individuals, and branch lengths are proportional to mutation steps (e.g., two nucleotide changes are indicated in the figure).For the B2 lineage (Figure 5), some Takanan from Bolivia shared different haplotypes with Arawakan and Reyesano. In the core central group, several individuals (n = 15, Jivaroan, Reyesano, Arawakan_BO, Itonama, Tupian, Cayubaba, and Movima) who shared a haplotype.5FIGUREMedian joining network for mtDNA haplotypes of the B2 lineage in Peruvian and Bolivian populations (n = 257), which are depicted by different colors. Mitochondrial haplotypes are symbolized by circles with sizes proportional to the number of individuals, and branch lengths are proportional to mutation steps (e.g., two nucleotide changes are indicated in the figure).In C1/C* lineages (Figure 6), the Takanan of Peru and Bolivia shared some haplotypes, which through a Jivaro (only one mutation step) are related to the core central group (n = 25, Jivaroan, Shawi, Arawakan_PE, Takanan_BO, Reyesano, Moseten, Canichana, Arawakan_BO, and Yuracare) that share a haplotype. Also, other distinct haplotypes were shared between individuals with different languages. In particular, one Panoan and one Arawakan_PE shared a haplotype.6FIGUREMedian joining network for mtDNA haplotypes of C1/C* lineages in Peruvian and Bolivian populations (n = 255), which are depicted by different colors. Mitochondrial haplotypes are symbolized by circles with sizes proportional to the number of individuals, and branch lengths are proportional to mutation steps (e.g., two nucleotide changes are indicated in the figure).Finally, for D1/D4 lineages (Figure 7), the Takanan and Panoan did not share haplotypes with other individuals, unlike the core central group where a haplotype was shared by other linguistic groups (n = 11, Arawakan, Cayubaba, and Tupian).7FIGUREMedian joining network for mtDNA haplotypes of D1/D4h3a lineages in Peruvian and Bolivian populations (n = 65), which are depicted by different colors. Mitochondrial haplotypes are symbolized by circles with sizes proportional to the number of individuals, and branch lengths are proportional to mutation steps (e.g., two nucleotide changes are indicated in the figure).However, at the population level (comparing 21 populations), AMOVA results in a PCoA plot (Figure 8) showed that the Takanan of Peru (Takanan_PE) were differentiated from other populations (e.g., Wichi and Ayoreo). In contrast, the Panoan population was closer to Shawi. Furthermore, the Arawakan population of Peru was more closely linked to Jivaroan and Cocama than other populations. Finally, the isolated Ayoreo population revealed a very low haplotype diversity (h = 0.2857), followed by Tsimane (h = 0.5824) and Moseten (h = 0.6444) (Table S4).8FIGUREPrincipal coordinates analysis (PCoA) for mtDNA data in Peruvian and Bolivian populations. Reynolds’ ϕst coancestry distances were used. Peruvian populations are represented by squares and Bolivian populations by spheres. Cani, Canichana; Iton, Itonama; Rey, Reyesano; Cay, Cayubaba.DISCUSSIONBased on linguistic features, the Panoan and Takanan‐speaking peoples should be closely related, but until now this hypothesis was controversial due to a lack of comparative DNA studies confirming or refuting the notion (Dixon & Aikhenvald, 1999). Moreover, a more general hypothesis of the expansion of the Arawak language in South America approximately 2.4 thousand years ago (kya) remains unclear (Eriksen, 2011). Thus, in this study, we investigated these issues and included several tropical lowland populations from Peru and Bolivia and an Arawakan community from Brazil as references as well as the Wichi and Ayoreo communities from Bolivia in the general framework.Our results indicated the Y chromosomes from a Takanan‐speaking subgroup (T2 in Figure 2) were linked to Panoan‐speaking communities. However, the Panoan and most individuals of the Takanan T1 subgroup were more closely related to Jivaroan and Arawakan‐speaking individuals. Moreover, the observation that one Cocama individual close to T1, and two Cocama and one Shipibo‐Conibo speaking individuals shared the same haplotype (Figure S2) indicated a close genetic affinity. This may have been due to remaining gene flow traces during ancient pre‐Columbian times, or more recently the Cocama‐Shipibo confederation against the priest missions, particularly in coalition with the Arawaks and Quechuas in the rebellion led by Juan Santos Atahualpa in 1742 in the central Amazonia of Peru (Adelaar & Muysken, 2004; Aikhenvald, 2012; Ludescher, 2001). These demographic interactions could partially explain the “lexical loans” in Panoan and Ashaninka, including Quechua, an imposed lingua franca in Amazonia (Fleck, 2013; Métraux, 1942). This also putatively explains the genetic affinities between three Panoan‐speaking individuals and several Arawakan‐speaking individuals from Peru.Our previous studies on Amazonian populations in Peru also showed that one Shipibo‐speaking individual not only shared a haplotype with the Cocamas, but also with two individuals from the Loreto region and one Kechwa‐Lamista (an admixed Amazonian group) individual from the San Martín region (Sandoval et al., 2016). Remarkably, this observation showed that Takanan (from Peru‐Bolivia) and Panoan (from Peru) speakers were closely related to Arawakan and Jivaroan speakers, including Cocama (Tupian).Similarly, our results were consistent with other studies at the genomic scale (via SNP chip analysis); where Panoan‐speaking communities (Shipibo‐Conibo, Cashibo, Matsés, Nahua) shared similar genomic profiles with Arawakan‐speaking populations (Ashaninka, Yanesha), including Jivaroan groups (Huambisa, Awajun, Candoshi), Kechwa‐Lamista, Piapoco (Arawakan from Colombia), Guarani, and others (Barbieri et al., 2019; Borda et al., 2020; Gnecchi‐Ruscone et al., 2019; Nieves‐Colón et al., 2020). The wide spatial distribution of this gene pool coincides with a hypothesis on the expansion of the Arawak language in South America, likely via the Madeira and Amazon rivers, which occurred approximately 2.4 kya left archaeological vestiges in areas of Llanos de Mojos (Bolivia) and 2.2 kya in the Ucayali river, Peru (Eriksen, 2011). This population expansion could be correlated with the dispersion of some domesticated plants in the last 6–4 kya (Clement et al., 2015). During this time, the following generations likely differentiated from their main linguistic branch in a similar way to the expansion history of the Macro‐Je or Tupi‐Guaraní (Tupian) linguistic groups in the central and southeastern parts of the Amazonia of Brazil (Aikhenvald, 2012; Eriksen, 2011; Ramallo et al., 2013).Our interpretations are supported by the genetic affinity between ten Pareci from Brazil (Arawakan‐speaking tribe) and several Arawakan‐speaking individuals from Bolivia, who are related to the largest group of Takanas (T1). This observation agreed with linguistics and indicated that Saraveka (extinct Arawakan language from Bolivia) was closely related to the Pareci language (Adelaar & Muysken, 2004; Métraux, 1942).In terms of the maternal line, our data suggested that in the Bolivian and Peruvian Amazonia region, high gene flow occurred. For example, some motifs in the mitochondrial control region corresponding to B2 lineage (73‐263‐499‐16189‐16217‐16519) are widely shared between many Amazonian groups in South America, regardless of their linguistic affiliation, including Andean groups (Mazières et al., 2008; Ramallo et al., 2013; Sandoval et al., 2018). In addition, although some Takanas are differentiated from other individuals, one shared a haplotype with some Arawaks (from Peru and Bolivia). For the A2 lineage, a shared haplotype existed between one Arawakan (Arawakan_PE) and some Takanan, and was related to three Panoan individuals, one Cocama and one Jivaro, suggesting a shared genetic affinity. This observation was consistent with a previous study showing two different shared haplotypes between Arawakan and Panoan groups (Di Corcia et al., 2017). Likewise, the core central group, which is shared between a Takanan (Takanan_BO), Yuracare, Chiquitano, Jivaroan, and Cayubaba, reflects a common origin. These individuals and the Takanan are linked through one Panoan‐speaking individual who is closely related to them. Another similar case was identified by the C1 lineage, where several individuals from eight linguistic groups (core central group composed of Takanan, Arawakan, Shawi, Jivaroan, Yuracare, Canichana, Moseten, and Reyesano) shared the same haplotype, indicating they were derived from common ancestors. Also, a similar picture of shared haplotypes by different linguistic groups in some Beni region populations was previously reported (Bert et al., 2004).Among other studied populations, our results showed that the maternal haplotype diversity of Ayoreo‐speaking community has been dramatically impacted by genetic drift (h = 0.29), a picture that coincides with previous genetic studies of Gran Chaco populations (Demarchi & García‐Ministro, 2008). In the paternal line, like Tsimane (h = 0.42), the Siriono showed the lowest haplotype diversity (h = 0.41; n = 21, only three different haplotypes, data not shown in the Table S2), followed by the Guarayo (h = 0.43, data not shown in the Table S2). These groups were separated from other populations (data not shown in the PCoA plot), which was consistent with the picture described at the individual level and with historical records (Lehm et al., 2004; Métraux, 1942). The isolated populations likely were impacted by lower gene flow or bottlenecks. Meanwhile, at the individual level, one Guaraní‐speaker shared a haplotype with one Wichi. Regarding this, an Argentinian Wichi community also shared haplotypes with other Matacoan‐speaking groups such as Toba and Pilagá in the Gran Chaco region (Sala et al., 2019). Thus, both patrilineal and matrilineal analyses indicated close interrelationships and acculturation occurring in the lowlands of Bolivia, southern Brazil, western Paraguay and northern Argentina in congruence with ethnographical, linguistic, and genetic studies (Bert et al., 2004; Block, 1994; Brown et al., 1974; Demarchi & García‐Ministro, 2008; Eriksen, 2011; Métraux, 1942; Ramallo et al., 2013).Although some populations were isolated due to historical or socio‐political reasons, for example, the distant position of the Tsimane and Yuracare Bolivian communities in two‐dimensional PCoA spaces (paternal and maternal lines), we also showed that in the Peruvian and Bolivian Amazonia, there was intense inter‐population migration in line with historical records.Finally, we suggest that the Takanan, like Panoan, Cocama, and Jivaroan speakers, were derived from ancient Arawak groups that were spread through the western Amazonia of South America, providing a plausible explanation that overlaps with archaeological and linguistic arguments.AUTHOR CONTRIBUTIONConceived and designed experiments: José R. Sandoval, Ricardo Fujita, and Fabricio R. Santos. Collected samples: José R. Sandoval, Ricardo Fujita, Fabricio R. Santos, Susana Revollo, and Cinthia Cuellar. Performed laboratory experiments: José R. Sandoval, Daniela R. Lacerda, Marilza S. Jota, and Cinthia Cuellar. Analyzed data and wrote the manuscript: José R. Sandoval. All authors reviewed and approved the final version of the manuscript.ACKNOWLEDGMENTSWe thank all volunteers who donated biological samples to the previous South American Genographic Projects. We also thank Oscar Acosta, Pedro Paulo R. Vieira, David Soria H., Daniela Arteaga, Alejandro Estrada, and Donaldo Pinedo for their support in fieldwork. This study received funds from the National Geographic Society (The Genographic Project‐South America) and grants from USMP (E10012019010) of Peru, FAPEMIG and CNPq of Brazil.CONFLICT OF INTEREST STATEMENTThe authors declare no conflict of interest.DATA AVAILABILITY STATEMENTThe Y‐STRs and mtDNA data are available in the Supplementary Material files: Figures S1 and S2 and Tables S1–S4.REFERENCESAdelaar, W. F. H., & Muysken, P. C. (2004). The languages of the Andes. Cambridge CB2 2RU UK: Cambridge University Press.Aikhenvald, A. Y. (2012). The languages of the Amazon. United Kingdom: Published to Oxford Scholarship Online. https://doi.org/10.1093/acprof:oso/9780199593569.003.0001Bandelt, H. J., Forster, P., & Röhl, A. (1999). Median‐Joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1), 37–48.Barbieri, C., Barquera, R., Arias, L., Sandoval, J. R., Acosta, O., Zurita, C., Aguilar‐Campos, A., Tito‐Álvarez, A. M., Serrano‐Osuna, R., Gray, R. D., Mafessoni, F., Heggarty, P., Shimizu, K. K., Fujita, R., Stoneking, M., Pugach, I., & Fehren‐Schmitz, L. (2019). The current genomic landscape of western South America: Andes, Amazonia and Pacific Coast. Molecular Biology and Evolution, 36(12), 2698–2713.Barbieri, C., Heggarty, P., Yang Yao, D., Ferri, G., De Fanti, S., Sarno, S., Ciani, G., Boattini, A., Luiselli, D., & Pettener, D. (2014). Between Andes and Amazon: The genetic profile of the Arawak‐speaking Yanesha. American Journal of Physical Anthropology, 155, 600–609.Bert, F., Corella, A., Gené, M., Pérez‐Pérez, A., & Turbón, D. (2004). Mitochondrial DNA diversity in the Llanos de Moxos: Moxo, Movima and Yuracare Amerindian populations from Bolivia lowlands. Annals of Human Biology, 31(1), 9–28.Block, D. (1994). Mission culture on the upper Amazon: Native tradition, Jesuit enterprise, and secular policy in Moxos. pp. 1660–1880 USA: University of Nebraska Press.Borda, V., Alvim, I., Mendes, M., Silva‐Carvalho, C., Soares‐Souza, G. B., Leal, T. P., Furlan, V., Scliar, M. O., Zamudio, R., Zolini, C., Araújo, G. S., Luizon, M. R., Padilla, C., Cáceres, O., Levano, K., Sánchez, C., Trujillo, O., Flores‐Villanueva, P. O., Dean, M., … Guio, H. (2020). The genetic structure and adaptation of Andean highlanders and Amazonians are influenced by the interplay between geography and culture. Proceedings National Academy of Science USA, 117(51), 32557–32565.Brown, S. M., Gajdusek, D. C., Leyshon, W. C., Steinberg, A. G., Brown, K. S., & Curtain, C. C. (1974). Genetic studies in Paraguay: Blood group, red cell, and serum genetic patterns of the Guayaki and Ayore indians, Mennonite settlers, and seven other indian tribes of the Paraguayan Chaco. American Journal of Physical Anthropology, 41, 317–344.Clement, C. R., Denevan, W. M., Heckenberger, M. J., Junqueira, A. B., Neves, E. G., Teixeira, W. G., & Woods, W. I. (2015). The domestication of Amazonia before European conquest. Proceedings of the Royal Society B, 282, 20150813.Demarchi, D. A., & García‐Ministro, A. (2008). Genetic structure of native populations from the Gran Chaco region, South America. International Journal of Human Genetics, 8(1‐2), 131–141.Di Corcia, T., Sanchez Mellado, C., Davila Francia, T. J., Ferri, G., Sarno, S., Luiselli, D., & Rickards, O. (2017). East of the Andes: The genetic profile of the Peruvian Amazon populations. American Journal of Physical Anthropology, 163(2), 328–338.Dixon, R. M. W., & Aikhenvald, A. Y. (1999). The Amazonian Languages. Cambridge CB2 2RU, UK: Cambridge University Press.Eriksen, L. (2011). Nature and culture in prehistoric Amazonia: Using G.I.S. to reconstruct ancient ethnogenetic processes from archaeology, linguistics, geography, and ethnohistory. Lund, Sweden: Human Ecology Division, Lund University.Excoffier, L., & Lischer, H. E. L. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564–567.Fan, L., & Yao, Y. G. (2011). MitoTool: A web server for the analysis and retrieval of human mitochondrial DNA sequence variations. Mitochondrion, 11, 351–356.Fleck, D. W. (2013). Panoan languages and linguistics. Anthropological Papers of the American Museum of Natural History, 99, 1–112.Gnecchi‐Ruscone, G. A., Sarno, S., De Fanti, S., Gianvincenzo, L., Giuliani, C., Boattini, A., Bortolini, E., Di Corcia, T., Sanchez Mellado, C., Dávila Francia, T. J., Gentilini, D., Di Blasio, A. M., Di Cosimo, P., Cilli, E., Gonzalez‐Martin, A., Franceschi, C., Franceschi, Z. A., Rickards, O., Sazzini, M., … Pettener, D. (2019). Dissecting the pre‐Columbian genomic ancestry of Native Americans along the Andes‐Amazonia divide. Molecular Biology and Evolution, 36(6), 1254–1269.Guevara, E. K., Palo, J. U., Guillén, S., & Sajantila, A. (2016). MtDNA and Y‐chromosomal diversity in the Chachapoya, a population from the northeast Peruvian Andes‐Amazon divide. American Journal of Human Biology, 28(6), 857–867.Jota, M. S., Lacerda, D. R., Sandoval, J. R., Vieira, P. P. R., Ohasi, D., Santos‐Júnior, J. E., Acosta, O., Cuellar, C., Revollo, S., Paz‐y‐Miño, C., Fujita, R., Vallejo, G. A., Schurr, T. G., Tarazona‐Santos, E. M., Pena, S. D. J., Ayub, Q., Tyler‐Smith, C., Santos, F. R., & The Genographic Consortium. (2016). New native South American Y chromosome lineages. Journal of Human Genetics, 61(7), 593–603.Lehm, Z., Townsend, W., Salas, H., & Lara, K. (2004). Bolivia: Estrategias, problemas y desafíos en la gestión del territorio indígena Siriono. Copenhague, Dinamarca: IWGIA.Ludescher, M. (2001). Instituciones y prácticas coloniales en la Amazonia peruana: Pasado y presente. Indiana, 17/18, 313–359.Mazières, S., Guitard, E., Crubézy, E., Dugoujon, J. M., Bortolini, M. C., Bonatto, S. L., Hutz, M. H., Bois, E., Tiouka, F., Larrouy, G., & Salzano, F. M. (2008). Uniparental (mtDNA, Y‐chromosome) polymorphisms in French Guiana and two related populations—Implications for the region's colonization. Annals of Human Genetics, 72, 145–156.Métraux, A. (1942). The native tribes of eastern Bolivia and western Mato Grosso, Vol. 134, Washington, USA: Smithsonian Institution Bureau of American Ethnology.Nakatsuka, N., Lazaridis, I., Barbieri, C., Skoglund, P., Rohland, N., Mallick, S., Harkins‐Kinkaid, K., Ferry, M., Harney, É., Michel, M., Stewardson, K., Forst, J., Durruty, M. A., Beresford‐Jones, D., Burger, R., Capriles, J., Fujita, R., Isla, J., Lau, G., … Fehren‐Schmitz, L. (2020). A paleogenomic reconstruction of the deep population history of the Andes. Cell, 181(5), 1131–1145.E21.Nieves‐Colón, M. A., Pestle, W. J., Reynolds, A. W., Llamas, B., de la Fuente, C., Fowler, K., Skerry, K. M., Crespo‐Torres, E., Bustamante, C. D., & Stone, A. C. (2020). Ancient DNA reconstructs the genetic legacies of precontact Puerto Rico communities. Molecular Biology and Evolution, 37(3), 611–626.Nordenskiold, B. E. (1917). The Guarani invasion of the Inca empire in the sixteenth century: An historical Indian migration. Geographical Review, 4, 103–121.Pérez‐Diez, A. A., & Salzano, F. M. (1978). Evolutionary implications of the ethnography and demography of Ayoreo indians. Journal of Human Evolution, 7, 253–268.Polzin, T., & Daneshmand, S. V. (2003). On Steiner trees and minimum spanning trees in hypergraphs. Operations Research Letters, 31, 12–20.Ramallo, V., Bisso‐Machado, R., Bravi, C., Coble, M. D., Salzano, F. M., Hünemeier, T., & Bortolini, M. C. (2013). Demographic expansions in South America: Enlightening a complex scenario with genetic and linguistic data. American Journal of Physical Anthropology, 150(3), 453–463.Roewer, L., Nothnagel, M., Gusmão, L., Gomes, V., González, M., Corach, D., Sala, A., Alechine, E., Palha, T., Santos, N., Ribeiro‐dos‐Santos, A., Geppert, M., Willuweit, S., Nagy, M., Zweynert, S., Baeta, M., Núñez, C., Martínez‐Jarreta, B., González‐Andrade, F., … Krawczak, M. (2013). Continent‐wide decoupling of Y‐chromosomal genetic variation from language and geography in native South Americans. Plos Genetics, 9(4), e1003460.Román‐López, D. A. E., & Castro‐Mojica, M. B. (2016). Amazonía boliviana. Visibilizando la diversidad de los pueblos de Tierras bajas. La Paz, Bolivia: ISEAT.Sala, A., Caputo, M., & Corach, D. (2019). Genetic structure of Mataco‐Guaycurú speakers from Argentina and the extent of their genetic admixture with neighbouring urban populations. Scientific Reports, 9, 17559.Sandoval, J. R., Lacerda, D. R., Acosta, O., Jota, M. S., Robles‐Ruiz, P., Salazar‐Granara, A., Vieira, P. P. R., Paz‐y‐Miño, C., Fujita, R., & Santos, F. R., & The Genographic Project Consortium. (2016). The genetic history of Peruvian Quechua‐Lamistas and Chankas: Uniparental DNA patterns among autochthonous Amazonian and Andean populations. Annals of Human Genetics, 80, 88–101.Sandoval, J. R., Lacerda, D. R., Jota, M. S., Elward, R., Acosta, O., Pinedo, D., Danos, P., Cuellar, C., Revollo, S., Santos, F. R., & Fujita, R. (2018). Genetic ancestry of families of putative Inka descent. Molecular Genetics and Genomics, 293(4), 873–881.Sandoval, J. R., Lacerda, D. R., Jota, M. S., Robles‐Ruiz, P., Danos, P., Paz‐y‐Miño, C., Wells, S., Santos, F. R., & Fujita, R. (2020). Tracing the genetic history of the ´Cañaris´ from Ecuador and Peru using uniparental DNA markers. BMC Genomics, 21(7), 413.Sandoval, J. R., Lacerda, D. R., Jota, M. S. A., Salazar‐Granara, A., Vieira, P. P. R., Acosta, O., Cuellar, C., Revollo, S., Fujita, R., & Santos, F. R., & The Genographic Project Consortium. (2013). The genetic history of indigenous populations of the Peruvian and Bolivian Altiplano: The legacy of the Uros. PLoS ONE, 8, e73006.Tarazona‐Santos, E., Carvalho‐Silva, D. R., Pettener, D., Luiselli, D., De Stefano, G. F., Labarga, C. M., Rickards, O., Tyler‐Smith, C., Pena, S. D. J., & Santos, F. R. (2001). Genetic differentiation in south Amerindians is related to environmental and cultural diversity: Evidence from the Y chromosome. American Journal of Human Genetics, 68, 1485–1496.Valenzuela, P., & Guillaume, A. (2017). Estudios sincrónicos y diacrónicos sobre lenguas Pano y Takana: Una introducción. Amerindia, 39(1), 1–49.

Journal

Annals of Human Genetics – Wiley

Published: Sep 1, 2023

Keywords: Amazonia; mtDNA; Panoan language; Takanan language; Y‐STRs

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