Content area
In northeast Argentina, different Amerindian communities share territory and history with settlers, mainly Europeans. Due to miscegenation, the current Argentinean population has a particular structure that can be described through X chromosome variation. The objectives of this study were to describe the variation of 10 X-chromosome short tandem repeats (X-STRs) in urban populations of the Argentinean regions known as Gran Chaco and Mesopotamia, report the forensic parameters of these STRs, and estimate the European and indigenous genetic components in these regions. Population and forensic parameters were estimated for 419 individuals from the analyzed populations, including two indigenous groups, Wichí and Mocoví, previously reported. Population structure was estimated through FST and RST distances and analysis of molecular variance. The indigenous American and European components were assessed with STRUCTURE. X-STRs showed a high level of genetic variability in urban and indigenous populations. Indigenous people of the Gran Chaco region showed significant differentiation from the urban samples (FST = 5.5%) and among themselves (FST = 5.3%). Genetic differentiation among urban groups was almost negligible, except that the population from Misión Nueva Pompeya differed from the rest of the city populations. Forensic parameters indicate that these X-STRs are useful as a complement to paternity tests. The set of 10 STRs could be a good tool for examining population differences.
Full text
Argentinean Population History and Present Composition
The current population of Argentina is the result of several generations of intermixing among various groups at different times, including indigenous communities, Spanish conquerors (early 1500s), Africans (arriving as slaves since the late 1500s), and a large European immigrant population (arriving between 1870 and 1950) (Avena et al. 2006). The European component in Argentina was introduced by two major events: Spanish colonization, which was violent, and the successive migratory waves of Europeans who fled because of wars and famine (Martínez Sarasola 2005; Gallero and Krautstofl 2009). Miscegenation was strong: a considerable proportion of the Argentine population is reported to have at least one indigenous American ancestor (Corach et al. 2010).
This work focuses on two regions of Argentina: Gran Chaco, which includes the provinces of Chaco, Formosa, Santa Fe (partly), Salta, and Santiago del Estero; and Mesopotamia, which includes the provinces of Misiones, Corrientes, and Entre Ríos. In particular, Mesopotamia and Gran Chaco have well-distinguished phytogeographic characteristics and different indigenous populations (Martínez Sarasola 2005; Heguy 2012).
The Gran Chaco region consists of an extensive wooded plain inhabited by indigenous people of the Mataco-Mataguayo, Guaycurú, Lule-Vilela, Arawak, and Tupi-Guaraní linguistic groups (Martínez Sarasola 2005), which according to Crossetti et al. (2008) arrived to the region about 5,000 years ago. The region within Gran Chaco that was referred to as the "Impenetrable Chaqueño" by early European settlers is inhabited mainly by the Wichí people, who encountered Franciscan missionaries in 1900, upon the founding of the Nueva Pompeya Mission (Franceschi and Dasso 2010).
The first Europeans arrived to the province of Chaco in 1528 and tried to occupy the land inhabited by indigenous communities. In 1872 a group of people from the neighboring province of Corrientes and Italian immigrants settled in this region (Tissera 2008; de Pompert de Valenzuela 2008). In 1875 the city of Resistencia was founded, and in 1884 it was consecrated as capital of the province of Chaco, as it is at present (Tissera 2008; de Pompert de Valenzuela 2008). Between 1895 and 1914 people from Paraguay and from the province of Corrientes arrived to the city (Franceschi and Dasso 2010; Solá 2009). At the beginning of the 20th century, the population of the Chaco was small, heterogeneous, and unequally distributed in the province (Maeder 1997).
In the case of the Mesopotamian region, according to Heguy (2012) the Guaraní people arrived from the Amazonian region at least 1,000 years ago, following the natural course of the Paraná and Paraguay Rivers (Sala et al. 2010; Tarragó 2000). In 1604 the Jesuits arrived in the current province of Misiones during the Spanish invasion of the area and established numerous missions, but in 1767 the Jesuits were expelled from America, and indigenous emigrated to Corrientes and Santa Fe Provinces for work, while others rejoined their native communities (Heguy 2012). After the initial Spanish settlers, Misiones received a later wave of immigration in the northern part of the province, mainly of German migrants. That colonization gave rise to settler cities, such as Eldorado, Puerto Rico, and Montecarlo (Junta de Estudios Históricos del Municipio de Eldorado 2015).
The capital city of Corrientes, also named Corrientes, was founded by Spaniards and their descendants born in America. The initial settlers of the city of Corrientes gradually joined the local Amerindian population (Vara 1985). In contrast with the situation in Misiones, there were only a few religious missions in the province (Heguy 2012; Pérez Colmán 1936).
X Chromosome
The patterns of allele distribution of different markers in the X chromosome can be very informative in comparative studies because of the special features of the X chromosome that make it a potential source to uncover ethnic differences (Bourgeois et al. 2009; Szibor 2007). From the perspective of population genetics, variation of the human X chromosome is a valuable complement to the genetic variation of autosomes. Given its mode of inheritance, the X chromosome presents a lower rate of mutation, showing different genetic diversity than autosomes and offering particular opportunities to selection action. It is also more exposed to the effects of genetic drift and is therefore likely to show more pronounced population structures (Hamosh et al. 2000; Schaffner 2004; Szibor 2007).
Short tandem repeats (STRs) are very polymorphic markers widely used in forensic and population genetics. Their high mutation rates and multiallelic spectra make STRs particularly useful for population studies. In forensic genetics, X-chromosome STRs (X-STRs) can complement the analysis of Y-chromosome and autosomal STRs, especially in paternity cases where the offspring is female or in some complex kinship testing cases (Santamaría et al. 2018).
Information on uniparental variability for populations in the north of Argentina showed a high component of Amerindian mitochondrial DNA and a very low proportion of indigenous Y chromosome (Bobillo et al. 2010; Rodríguez Golpe et al. 2017a, 2017b; Salas et al. 2008). These results supported the historical events that the first encounters between indigenous women and Spanish men gave rise to an important mestizo society. Given the pattern of inheritance of X-chromosome variation, females can influence X-chromosome variation of current populations twice as much as males, so we can interpret that an important indigenous component may be present more in X-chromosome variation than in autosomal chromosomes. Each region of Argentina has a particular history and a different contribution of European and indigenous genetic components. Even the Amerindian groups that inhabited the territory were different: the Wichí and Mocoví people, among others, predominated in Gran Chaco, while the Guaraní people predominated in Mesopotamia. Moreover, in a previous study, genetic differences have been found among some of these indigenous communities (Catanesi et al. 2007).
The aim of this study was to describe the variation of 10 polymorphisms of the X-STR in six urban populations of Gran Chaco and Mesopotamia, report the forensic parameters of these X-STRs to increase the forensic databases, and estimate the European and indigenous genetic components in these regions. In addition, we compared our data with information from other indigenous and urban Argentine populations to evaluate the usefulness of X-STRs to differentiate among indigenous communities, and to understand the genetic background of the different urban populations in the light of their different admixed origins.
Methods
Populations
We analyzed a total of 419 samples from healthy, unrelated persons of both sexes from five different locations at three provinces in northeastern Argentina (see Figure 1): the capital city of Chaco (Resistencia; n = 141: 78 females, 63 males), a small city of Chaco (Misión Nueva Pompeya; n = 54: 23 females, 31 males), the capital city of Corrientes (Corrientes; n = 92: 32 females, 60 males), the capital city of Misiones (Posadas; n = 52: 28 females, 24 males),
Figure 1. Geographical location of the populations analyzed and other populations used for comparison: Chaco, Corrientes, and Misiones (this work); Entre Ríos, Córdoba, Buenos Aires, and Río Negro (); and Mocoví and Wichí indigenous from the Gran Chaco region ().
and another important city of Misiones (Eldorado; n = 54). Concerning Eldorado, samples were separated into two groups according to the grandparents' reported origin, labeled Eldorado A(n = 27: 13 females, 14 males) when donors knew that their four grandparents were German and/or Swiss, and Eldorado B for donors who did not know the origin of all four grandparents (n = 27: 11 females, 16 males) (Di Santo Meztler et al. 2018).
Adult donors were recruited in health facilities and private health centers and asked to participate in this project while waiting for a medical appointment. The health institutions were as follows: samples from Posadas were from different public hospitals of the city; Resistencia, from Hospital Central de Odontología and two private centers, Sanatorio Frangioli and Sanatorio Güemes; and Misión Nueva Pompeya, from Hospital Regional Misión Nueva Pompeya. Samples from Eldorado were collected in a private laboratory of clinical analysis, and those from Corrientes were collected during a campaign by physician Darío Martín González. The project was approved by the Ethics Committee at the Instituto Multidisciplinario de Biología Celular. DNA was isolated from buccal cells and peripheral blood samples as described in Gemmell and Akiyama (1996). Seven populations were used for comparison, from Entre Ríos, Córdoba, Buenos Aires, and Río Negro (Argentina) and Galicia (Spain) from Gusmão et al. (2009); and Mocoví and Wichí populations from Glesmann et al. (2013). The lack of references for African populations in public databases for the STR markers included in this work prevented us from making comparisons or calculating a possible African contribution.
Genetic Determinations
Samples were genotyped for 10 noncoding X-STR markers (DXS8378, DXS9902, DXS7132, DXS9898, DXS6809, DXS7133, DXS6789, GATA172D05, GATA31E08, and DXS7423) in a single multiplex reaction, according to Gusmão et al. (2008, 2009). Polymerase chain reaction fragments were separated and detected through capillary electrophoresis in an ABI PRISM 3130 genetic analyzer (Applied Biosystems, Inc.).
Statistical Analysis
Allele frequencies were calculated employing the software RStudio (version 0.99.893; R Core Team 2008). Heterozygosity and Hardy-Weinberg equilibrium were calculated only for female subsamples. Genetic distances were approached through analysis of molecular variance (AMOVA); FST and RST distances using both female and male data were analyzed using Arlequin, version 3.5 (Excoffier and Lischer 2010). The program Past was used to make multidimensional scaling (MDS) graphics (Hammer et al. 2001). To infer the population structure, STRUCTURE (version 2.1; Hubisz et al. 2009) was used, assuming a model of k population groups, with k ranging from 1 to 5; all runs were performed using a burn-in period of 105 iterations followed by 105 iterations, and a repetition number of 10. To choose the best k in each case, Structure Harvester software was used (Earl and von Holdt 2012). Bonferroni correction was applied in all analyses except for AMOVA. The tables for R, STRUCTURE, and Arlequin were adapted using GA-TA (http://gata.fcaglp.unlp.edu.ar/).
Another feature to consider is the forensic efficiency of using DNA markers in casework involving relationship testing. Such estimates describe the theoretical value of using the specific markers for different forensic genetic situations and differ from case-specific values. The estimation of such parameters is most often based on the number of distinctive alleles found in the population and their corresponding frequencies. The power of discrimination (PD) is defined as the probability of discriminating between two unrelated individuals. Polymorphism informative content (PIC) can be interpreted as the probability that the maternal and paternal alleles of a child are deducible, or the probability of being able to deduce which allele a parent has transmitted to the child (Botstein et al. 1980; Guo and Elston 1999). The power of exclusion (PE) is defined as the fraction of individuals having a DNA profile that is different from that of a randomly selected individual in a typical paternity case. The value for each individual case will vary (Brenner and Morris 1990). These parameters were performed using the online tool provided by ChrXSTR.org 2.0 (http://www.chrx-str.org/) (Szibor et al. 2006).
Results
Allele Frequencies, Hardy-Weinberg Equilibrium, and Heterozygosity
The frequencies and the observed and expected heterozygosity of the 10 STR alleles for the six populations are shown in Table 1. The alleles DXS9902*15, DXS7132*10, GATA1705*14, and DXS6809*37 were present only in the Resistencia population; DXS9898*17 was observed only in Misión Nueva Pompeya, DXS6789*13 was found only in Corrientes, and DXS7423*12 was observed only in Eldorado. There were no significant differences in allele frequencies between females and males. The highest values for the number of alleles (nx) were found in the capital cities and in Misión Nueva Pompeya, and the lowest was observed in Eldorado A (see Supplementary Table S1).
Frequency distributions fitted the Hardy-Weinberg equilibrium with the exceptions of GATA31E08 for Corrientes (p = 0.03), DXS7133 for Eldorado A (p = 0.02), GATA172D05 for Eldorado B(p = 0.03) and Resistencia (p = 0.04), and DXS7132
Figure 2. MDS graphic using RST. Cor = Corrientes, Pos = Posadas, EldA = Eldorado A, EldB = Eldorado B, Res = Resistencia, MNP = Misión Nueva Pompeya, Moc = Mocoví, Wich = Wichí, BA = Buenos Aires, Cba = Córdoba, ER = Entre Ríos, RN = Río Negro, Gal = Galicia.
for Misión Nueva Pompeya (p = 0.04). These values were not significant after Bonferroni correction (p = 0.005).
STRs showed high heterozygosity in all cases. The highest average heterozygosity was found in Eldorado B (0.75), followed in decreasing order by Posadas, Mision Nueva Pompeya, Resistencia, Corrientes, and Eldorado A (Table 1). The forensic parameters PIC, PE, and PD are reported in Supplementary Table S2 for the samples in this study and for Wichí and Mocoví. For Corrientes and
Mocoví the highest values for these parameters were found for DXS7132; for Posadas, Eldorado A, and Eldorado B the highest values were found for GATA172D05; and for Resistencia, Misión Nueva Pompeya, and Wichí the highest values were found for DXS6809.
Population Structure and Comparisons among Urban and Indigenous Populations
RST and FST distances are shown in Supplementary Table S3. For both distances, the highest values are observed between indigenous and urban groups, and the lowest, non-statistically different from zero, were among urban samples, with the exception of Misión Nueva Pompeya, which differed from most of the urban populations. Distance values between the two indigenous populations, Mocoví and Wichí, are high and similar to the values shown between them and the urban samples. An MDS plot using RST distances is shown in Figure 2. The first dimension of the graph separates indigenous people of Gran Chaco from the rest of the populations, suggesting an Amerindian component to the left of the plot and a European component to the right. The second dimension separates the two indigenous populations, with the Wichí people located on the top and the Mocoví at the bottom. Misión Nueva Pompeya is a particular case because it is clustered in an intermediate position between indigenous and urban populations.
AMOVA calculations allowed an estimation of the amount of population variability behind the clusters observed in the MDS plot. High values of AMOVA (FST = 5.2%; p < 0.001) were observed among the two indigenous groups and the urban samples from Gran Chaco (Resistencia and Misión Nueva Pompeya regions). A similar value was observed in the comparison between Wichí and Mocoví (global FST = 5.5%; p < 0.001). When only urban populations were considered, the global FST was extremely low, either when Gran Chaco and Mesopotamia were compared (0.5%; p < 0.001) or when all Argentinean samples were included (0.3%; p < 0.01). Variability among populations from the cities was almost negligible (0.5% for Gran Chaco and Mesopotamia regions combined, 0.3% for all Argentinean urban cities).
We used STRUCTURE software to infer the Amerindian and European proportion in urban populations of Argentina, employing the data of
Figure 3. Bar plot of k = 2 for Corrientes (1), Posadas (2), Eldorado A (3), Eldorado B (4), Resistencia (5), Misión Nueva Pompeya (6), Mocoví (7), Wichí (8), Buenos Aires (9), Córdoba (10), Entre Ríos (11), Río Negro (12), Galicia (13).
two indigenous communities of Wichí and Mocoví and the European population of Galicia (Spain) as references. Table 2 indicates the proportion of membership of each predefined population in each of the two clusters. We associated an indigenous component to cluster 1 and a European component to cluster 2. As expected, all urban samples had a large proportion of cluster 2. In contrast, all indigenous populations had a large proportion of cluster 1. Misión Nueva Pompeya showed more Amerindian component (39%) than the remaining urban populations of northeastern Argentina (16.4–33.6%). The information of Table 2 is graphically represented in Figure 3. A comparison of the individual bars shows that the internal heterogeneity within each population is high.
Regarding forensic parameters, the set of 10 STRs was informative in both urban and indigenous populations. In an analysis of each marker separately, the forensic parameters are notably more informative in the urban samples, but when considered together their power of discrimination is high not only in urban populations (as expected) but also in indigenous communities of Wichí and Mocoví.
Discussion
In this work, we describe the variation of 10 X-STRs in six urban populations from the Argentinean regions of Gran Chaco (Resistencia and Misión Nueva Pompeya) and Mesopotamia (Corrientes, Posadas, and Eldorado A and B populations). Population parameters are consistent with the expected outcome for urban populations with high gene flow. The capital cities of the northeastern provinces considered in this work were initially settled by people from several origins, and afterward they have received immigration from other regions of Argentina and from bordering countries, resulting in an identity particular to each city.
Our results are in accordance with previous reports on X-chromosome variation in other populations (Gomes et al. 2009; Gusmão et al. 2009; Zambrano et al. 2015). Although no evidence of population stratification along Argentina was recently reported for a different set of X-STR markers, no indigenous populations were included in that study (García et al. 2019).
We observed a high level of genetic diversity in all populations, including indigenous communities, as expected for multiallelic markers selected for forensic purposes. Demarchi and García Ministro (2008) had observed a high level of genetic diversity in indigenous people from Chaco, analyzing both mitochondrial and Y-chromosome markers, a fact that is noticeable in communities with relatively low population sizes.
Although our sample size might not exactly represent some of the populations here considered, these data differentiate urban populations from indigenous groups (see Figures 2 and 3). Interestingly, genetic distances and admixture values joined Eldorado B, Río Negro, and Misión Nueva Pompeya in a group with an Amerindian component of >30%, while Eldorado A exhibited a much lower Amerindian component. It is also important to remark that we have already reported a substructure in X-chromosome variability of the population of Eldorado city, likely originated by European migratory flow at the beginning of the 20th century (Di Santo Meztler et al. 2018). These results illustrate how colonization took place in Eldorado city, given that immigrants were distributed by the owner of the lands (Mr. Adolfo Schwelm) in separate land plots according to their different nationalities (Junta de Estudios Históricos del Municipio de Eldorado 2015).
Our results are consistent with the fact that current Argentinean populations originated in an admixture of inhabitants descending from indigenous and Spanish settlers, with later contributions from other European countries, mostly Italians. A particular case is the population of Misión Nueva Pompeya, which does not cluster with those from other Argentinean cities in the MDS plot and shows the highest indigenous admixture value (0.390) among those sampled. According to their geographic position in Chaco Province, where the Wichí indigenous people are distributed, one would expect the contribution of Wichí population. However, in the MDS plot, Misión Nueva Pompeya does not show any particular relationship with the Wichí but nonetheless had an intermediate position. Cultural differences can be the main factor of separation between urban people living in Misión Nueva Pompeya and indigenous communities living in the proximities of the city. Wichí people tend to marry persons living within their communities, with whom they share language and uses. Another possible factor for the lack of any particular closeness between Misión Nueva Pompeya and Wichí could be the fact that this city started as a mission, which was founded and abandoned several times. In each episode, the indigenous people who inhabited the mission returned to the forest (Colazo 2003), and at each refoundation, a new group of indigenous people contributed to the city, making it difficult for them to integrate to urban habits. This process, together with the presence of admixed people who came to the city for administrative work, contributed to the particular genetic background of Misión Nueva Pompeya. Concerning the Mocoví community, their position in the plot shows that they are currently less isolated and maintain a certain amount of contact with urban people, gradually joining the urban population looking for education and job, as previously reported (Franceschi and Dasso 2010).
The STRs here analyzed, which were initially selected for forensic purposes (Gusmão et al. 2009) and have been widely used for resolution of paternity cases, showed an overall high intra-population genetic diversity. Moreover, they also showed interpopulation diversity, as they proved to be useful for discriminating not only urban from indigenous populations but also between indigenous populations. In this way, our results revealed a relationship between historical events and the genetic information contained in the X chromosome. Another set of markers is gaining place among human identification laboratories within Argentina, the STR Investigator Argus X-12, which includes 12 STRs conforming to four linkage groups, and some information on the variation of these markers in Argentina is currently available (García et al. 2019). However, the STRs included in the present work have been widely applied in both population and forensic studies in Argentina, with good results. Therefore, further analyses in both sets of markers would be desirable to characterize in depth these and other populations from Argentina and from South America as a whole.
Conclusions
In summary, this set of 10 X-STRs is informative for forensic purposes in both urban and indigenous populations, being useful as a complement to paternity tests of female kinship. These X-chromosome markers showed a significant differentiation among indigenous and urban populations, allowing an estimation of the amount of the Amerindian component present in the urban communities. Further studies using these X-STRs would be very useful for the characterization of other Argentinean populations and for understanding particular historical events that have taken place in each region.
acknowledgments
We thank Raúl Brindi, Pablo Martina, Daniela Arntzen, Martín González, Isaías Armoa, and Carina Argüelles for collecting samples from donors. We thank Marisa Roman (St. Joseph's University, Philadelphia, PA) and Alejandro Roman (University of Pennsylvania, Philadelphia, PA) for revising the manuscript. M.E.E. acknowledges support from 2017 SGR 1630 Grup de Recerca en Antropologia Biològica. This work was supported by grants from Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina (PIP 2015-2017 11220150100930, and PUE 2017-2022 22920170100105CO), and from Universidad Nacional de La Plata, Argentina (PID 2019-2020 N895).
Footnotes
1. Laboratorio de Diversidad Genética, Instituto Multidisciplinario de Biología Celular, Comisión de Investigaciones Científicas de la Provincia de Buenos Aires – Universidad Nacional de La Plata – Consejo Nacional de Investigaciones Científicas y Técnicas, La Plata, Argentina.
2. Section of Zoology and Biological Anthropology, Department of Evolutionary Biology, Ecology, and Environmental Sciences, and Biodiversity Research Institute, University of Barcelona, Barcelona, Spain.
3. Instituto Argentino de Radioastronomía, Centro Científico Tecnológico – La Plata, Consejo Nacional de Investigaciones Científicas y Técnicas, Comisión de Investigaciones Científicas de la Provincia de Buenos Aires, Villa Elisa, Argentina.
4. Departamento de Antropología, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata, Argentina.
5. Cátedra de Genética, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata, Argentina.
Avena, S. A., A. S. Goicoechea, J. M. Dugoujon et al. 2006. Mezcla génica en la Region Metropolitana de Buenos Aires. Medicina (B. Aires) 66:113–118.
Bobillo, M. C., B. Zimmermann, A. Sala et al. 2010. Amerindian mitochondrial DNA haplogroups predominate in the population of Argentina: Towards a first nationwide forensic mitochondrial DNA sequence database. Int. J. Legal Med. 124:263–268.
Botstein, D., R. L. White, M. Skolnick et al. 1980. Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am. J. Hum. Genet. 32:314–331.
Bourgeois, S., V. Yotova, S. Wang et al. 2009. X-chromosome lineages and the settlement of the Americas. Am. J. Phys. Anthropol. 140:417–428.
Brenner, C. H., and J. W. Morris. 1990. Paternity index calculations in single locus hypervariable DNA probes: Validation and other studies. In Proceedings for the International Symposium on Human Identification 1989. Madison, WI: Promega Corporation, 21–52.
Catanesi, C. I., P. F. Martina, G. Giovambattista et al. 2007. Geographic structure in Gran Chaco Amerindians based five X-chromosome STRs. Hum. Biol. 79:463–474.
Colazo, S. 2003. Relatos orales, historia y temporalidad. In Comunicaciones Científicas y Tecnológicas. Corrientes, Argentina: Universidad Nacional del Nordeste.
Corach, D., O. Lao, C. Bobillo et al. 2010. Inferring continental ancestry of Argentineans from autosomal, Y-chromosomal and mitochondrial DNA. Ann. Hum. Genet. 74:65–76.
Crossetti, S. G., D. A. Demarchi, P. E. Raimann et al. 2008. Autosomal STR genetic variability in the Gran Chaco native population: Homogeneity or heterogeneity? Am. J. Hum. Biol. 20:704–711.
Demarchi, D. A., and A. García Ministro. 2008. Genetic structure of native populations from the Gran Chaco region, South America. Int. J. Hum. Genet. 8:131–141.
de Pompert de Valenzuela, M. C. 2008. El poblamiento del Chaco: Génesis y primitivo desarrollo. Corrientes, Argentina: Moglia SRL.
Di Santo Meztler, G. P., S. del Palacio, M. E. Esteban et al. 2018. Genetic differentiation of north-east Argentina populations based on 30 binary X chromosome markers. Front. Genet. 9:208.
Earl, D. A., and B. M. von Holdt. 2012. Structure Harvester: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4:359–361.
Excoffier, L., and H. E. Lischer. 2010. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10:564–567.
Franceschi, Z. A., and M. C. Dasso. 2010. Etno-grafías: La escritura como testimonio entre los Wichí. Buenos Aires, Argentina: Corregidor.
Gallero, M. C., and E. M.. 2009. Proceso de poblamiento y migraciones en la Provincia de Misiones, Argentina (1881–1970). Avá 16:245–264.
García, M. G., C. I. Catanesi, G. A. Penacino et al. 2019. X-chromosome data for 12 STRs: Towards an Argentinian database of forensic haplotype frequencies. Forensic Sci. Int. Genet. 41:e8–e13.
Gemmell, N. J., and S. Akiyama. 1996. An efficient method for the extraction of DNA from vertebrate tissues. Trends Genet. 12:338–339.
Glesmann, L. A., P. F. Martina, and C. I. Catanesi. 2013. Genetic variation of X-STRs in the Wichí population from Chaco Province, Argentina. Hum. Biol. 85:687–698.
Gomes, I., V. Pereira, V. Gomes et al. 2009. The Karimojong from Uganda: Genetic characterization using an X-STR decaplex system. Forensic Sci. Int. Genet. 3:e127–e128.
Guo, X., and R. C. Elston. 1999. Linkage information content of polymorphic genetic markers. Hum. Hered. 49:112–118.
Gusmão, L., C. Alves, P. Sánchez-Diz et al. 2008. Results of the GEP-ISFG collaborative study on an X-STR decaplex. Forensic Sci. Int. Genet. Suppl. Ser. 1:677–679.
Gusmão, L., P. Sánchez-Diz, C. Alves et al. 2009. A GEP ISFG collaborative study on the optimization of an X-STR decaplex: Data on 15 Iberian and Latin American populations. Int. J. Legal Med. 123:227–234.
Hammer, Ø., D. A. T. Harper, and P. D. Ryan. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4:1–9. https://palaeo-electronica.org/2001_1/past/past.pdf.
Hamosh, A., A. F. Scott, J. Amberger et al. 2000. Online Mendelian Inheritance in Man (OMIM). Hum. Mutat. 15:57–61.
Heguy, S. 2012. Misiones: Jesuitas y Guaraníes: Una experiencia única. Buenos Aires, Argentina: Golden Company.
Hubisz, M. J., D. Falush, M. Stephens et al. 2009. Inferring weak population structure with the assistance of sample group information. Mol. Ecol. Resour. 9:1,322–1,332.
Junta de Estudios Históricos del Municipio de Eldorado, ed. 2015. Historias de Eldorado. Vol. 2. Eldorado, Misiones: Junta de Estudios Históricos del Municipio de Eldorado.
Maeder, E. J. A. 1997. Historia del Chaco. Collection "Historia de Nuestras Provincias," no. 18. Buenos Aires: Plus Ultra.
Martínez Sarasola, C. 2005. Nuestros paisanos los Indios. Vida, historia y destino de las comunidades indígenas en la Argentina. Buenos Aires, Argentina: Emecé.
Pérez Colmán, C. B. 1936. Historia de Entre Ríos: Época Colonial, 1520–1810. Paraná, Argentina: Imprenta de la Provincia.
R Core Team. 2008. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org.
Rodríguez Golpe, D. C., M. E. Schwab, E. Aquilano et al. 2017a. Linajes maternos en las ciudades de Formosa y Corrientes, Argentina. In Libro de Resúmenes de las Decimoterceras Jornadas Nacionales de Antropología Biológica: Horizontes en antropología biológica, R. A. Guichón, P. García Laborde, L. O. Valenzuela, J. M. B. Motti, and M. Martucci, eds. La Plata, Buenos Aires, Argentina: Asociación de Antropología Biológica, 114.
Rodríguez Golpe, D. C., M. E. Schwab, P. Paz Sepúlveda et al. 2017b. Aportes de los linajes paternos nativos y alóctonos a las poblaciones contemporáneas de Formosa y Corrientes, Argentina. In Libro de Resúmenes de las Decimoterceras Jornadas Nacionales de Antropología Biológica: Horizontes en antropología biológica, R. A. Guichón, P. García Laborde, L. O. Valenzuela, J. M. B. Motti, and M. Martucci, eds. La Plata, Buenos Aires, Argentina: Asociación de Antropología Biológica, 163.
Sala, A., C. F. Argüelles, M. E. Marino et al. 2010 Genetic analysis of six communities of Mbyá-Guaraní inhabiting northeastern Argentina by means of nuclear and mitochondrial polymorphic markers. Hum. Biol. 82:433–456.
Salas, A., J. C. Jaime, V. Álvarez-Iglesias et al. 2008. Gender bias in the multiethnic genetic composition of central Argentina. J. Hum. Genet. 53:662–674.
Santamaría, J., M. M. Álvarez-Álvarez, M. E. Esteban et al. 2018. Dinucleotide (CA)n tandem repeats on the human X-chromosome and the history of the Mediterranean populations. Ann. Hum. Biol. 45:72–76.
Schaffner, S. F. 2004. The X chromosome in population genetics. Nat. Rev. Genet. 5:43–51.
Solá, M. D. 2009. Región Chaqueña: Wichís. In Aborígenes Argentinos. Buenos Aires, Argentina: Editorial Gradifco, 27–60.
Szibor, R. 2007. X-chromosomal markers: Past, present and future. Forensic Sci. Int. Genet. 1:93–99.
Szibor, R., S. Hering, and J. Edelmann. 2006. A new web site compiling forensic chromosome X research is now online. Int. J. Legal Med. 120:252–254.
Tarragó, M. N., ed. 2000. Nueva historia Argentina: Los pueblos originarios y la Conquista. Buenos Aires, Argentina: Editorial Sudamericana.
Tissera, R. M. 2008. Chaco: Historia general. Resistencia, Chaco, Argentina: Librería de la Paz.
Vara, A. 1985. Todo es historia: Corrientes en el Mundo Guaranítico. Buenos Aires, Argentina: Talleres Gráficos de Alemann SRL.
Zambrano, A. K., G. Morejón, J. Galarza et al. 2015. Genetic data of an X-STR decaplex in Ecuadorian population (P). Forensic Sci. Int. Genet. Suppl. Ser. 5:e91–e92.
Copyright Wayne State University Press Winter 2019