AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 133:1067–1079 (2007)

Morphological Differentiation of Aboriginal Human Populations From Tierra del Fuego (Patagonia): Implications for South American Peopling S. Ivan Perez,* Valeria Bernal, and Paula N. Gonzalez CONICET, Divisio´n Antropologı´a, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata 1900, Buenos Aires, Argentina KEY WORDS mtDNA

South American aborigines; evolutionary relationships; geometric morphometrics;

ABSTRACT This study aims to integrate the craniofacial morphological variation of southern South American populations with the results of mtDNA haplogroup variation, to discuss the South America peopling. Because the causes of morphological differentiation of Fueguian populations are still a controversial subject, the comparison with neutral variation could contribute to elucidate them. Samples of human remains from South America regions were used to analyze the evolutionary relationships. Several craniofacial traits observed in frontal and lateral view were analyzed by means of geometric morphometrics techniques, and the evolutionary relationships based on morphological and molecular data were established in base to ordination analyses. The results from the facial skeleton agree with those obtained from mtDNA haplogroup frequencies, with La Pampa/Chaco samples detached from the Patagonian

samples. Hence, the same mechanism that accounts for the pattern of frequency of haplogroups could explain the variation found in facial skeleton among the samples. It is suggested that such geographic pattern of craniofacial and molecular diversity may reflect the effect of genetic drift that occurred in the small founding populations isolated by distance or geographic barriers. Conversely, the results obtained using the traits from the lateral view slightly differ from the molecular results, showing differences between southernmost Patagonian and the other samples. Therefore, mechanisms other than genetic drift (e.g., natural selection) could have acted to shape the pattern observed in some craniofacial structures present in the lateral view, characterized by the fact that the southernmost Patagonian samples display the most robust and dolichocephalic crania. Am J Phys Anthropol 133:1067–1079, 2007. V 2007 Wiley-Liss, Inc.

The biological origin and evolution of the aboriginal populations from southernmost Patagonia and Tierra del Fuego have been intensely studied since the end of the 19th century (e.g. Hyades and Deniker, 1891; Imbelloni, 1923, 1937; Bo´rmida, 1953, 1954; Cocilovo and Guicho´n, 1985, 1986; Gusinde, 1989; Lahr, 1995; Herna´ndez et al., 1997; Lalueza et al., 1997a; Garcia-Bour, 1998; GarciaBour et al., 1998, 2004; Moraga et al., 2000; Gonza´lezJose´ et al., 2004). These early investigations already pointed out the craniofacial singularity of these populations in relation to other American populations (see Imbelloni, 1937; Munizaga, 1976; Marcellino and Colantonio, 1985), characterized particularly by high levels of craniofacial robusticity and dolichocephaly (e.g. Imbelloni, 1937; Lahr, 1995). Different hypotheses were proposed to account for such singularity, but most of them can be grouped in two propositions: (a) a different ancestral origin for Fueguian and most other American populations; (b) a local process of diversification. In the late 19th and early 20th centuries, several authors argued that the human groups occurring in Tierra del Fuego, particularly the Yamanas, were members of an antique race that peopled America early, before the arrival of Asian-descent populations, which gave origin to the Amerindians. This hypothesis was maintained, together with the multiple waves model of American peopling, based on the fact that the craniofacial morphology (i.e., robusticity and dolichocephaly) of these populations was similar to the morphology considered archaic in recent populations from Tasmania,

Australia and Melanesia (Imbelloni, 1937, 1938). Recently, multivariate craniometric analysis suggested the existence of two ‘‘human stocks’’ that peopled South America, one corresponding to the first human migration to the continent, the Palaeoamericans, originated in a pre-Asian-descent population inhabiting Asia in pre-glacial times (morphologically similar to modern Australians aborigines), and the other corresponding to a second migration, with Asian-descent (in the past named Mongoloid) characteristics, from which most of the modern Amerindians derived (Neves and Pucciarelli, 1989, 1990; Lahr, 1995; Neves et al., 1999; Gonza´lez-Jose´ et al., 2003; Pucciarelli et al., 2003; Sardi et al., 2004, 2005). In this context, several investigators have maintained that the Tierra del Fuego populations as well as other groups such as the ethnographical Pericu´ group of Baja California would be a relict of the former Palaeoamericans

C 2007 V

WILEY-LISS, INC.

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Grant sponsor: CONICET, Universidad Nacional de La Plata. *Correspondence to: S. Ivan Perez, Divisio´n Antropologı´a, Facultad de Ciencias Naturales y Museo, Museo de La Plata, Paseo del Bosque s/n. La Plata 1900, Argentina. E-mail: [email protected] Received 15 September 2006; accepted 6 March 2007 DOI 10.1002/ajpa.20633 Published online 25 May 2007 in Wiley InterScience (www.interscience.wiley.com).

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(Lahr, 1995; Herna´ndez et al., 1997; Lalueza et al., 1997a; Gonza´lez-Jose´ et al., 2003). On the other hand, several multivariate craniometric studies performed in the 1980s and 1990s (Cocilovo, 1981; Cocilovo and Di Rienzo, 1984, 1985; Cocilovo and Guicho´n, 1985, 1986; Rothhammer and Silva, 1990; Rothhammer et al., 1997) found that the Tierra del Fuego populations form a differentiated group with respect to other South Americans populations (e.g., from Patagonia, Pampa, Sierras Centrales, and Norwest Argentina), and such differentiation is associated to latitudinal location of populations (see Guicho´n, 2002). Some investigators proposed that the existence of this geographic pattern suggests that the differentiation of Tierra del Fuego populations could have emerged by local processes as gene flow, genetic drift, or natural selection (Cocilovo and Di Rienzo, 1984, 1985; Cocilovo and Guicho´n, 1985, 1986; Rothhammer and Silva, 1990), and all populations of the southern South America would be derived from one Asian-descent population or a group of related Asiatic populations (Moraga et al., 2000). This idea agrees with the hypothesis maintained early by Hrdlicka (1912) and then by Turner II (1984) and Greenberg et al. (1986), who, on the basis of craniometric, dental, and linguistic data, established that all South American populations descended from a unique Asiandescent population. The study of evolutionary relationships in human populations from Tierra del Fuego was mainly limited to craniofacial data until the end of the 20th century, but in recent years several analyses have used mtDNA for the study of the differentiation of Tierra del Fuego populations (Merriwether et al., 1995; Lalueza, 1996; Lalueza et al., 1997b; Garcia-Bour et al., 1998, 2004; Moraga et al., 2000). The results obtained also support the singularity of Fueguian populations, and the cause for it was attributed either to a different ancestral origin (e.g. Lalueza et al., 1997b; Garcia-Bour et al., 1998) or an in situ differentiation (e.g. Merriwether et al., 1995). However, the most recent phylogenetic analyses of mtDNA and Y chromosome support the existence of a unique origin for South American populations, including the Tierra del Fuego groups (Moraga et al., 2000; Garcia-Bour et al., 2004). In summary, the results obtained using morphological and molecular data find that Fueguian populations are distinct from the rest of Amerindians, but some controversies arise in relation to the magnitude and causes of such distinctiveness. This might be partially due to the genealogical information carried by each type of data. DNA data are free from environmental influence during ontogeny, and in the case of the mtDNA and some portions of Y chromosome, they do not seem to be undergoing recombination, are transmitted intact from parents to offspring and have relatively high rates of mutation (Brown et al., 1979; Giles et al., 1980; Case and Wallace, 1981; Jobling and Tyler-Smith, 2003). Conversely, the craniofacial differences among human populations result from genetic and environmental variation (i.e. phenotypic plasticity). The genetic apportionment of craniofacial differences reflects generally recurrent processes such as gene flow and genetic drift and nonrecurrent events such as expansion, contraction, and population replacement (Relethford and Lees, 1982; Templeton et al., 1995; Templeton, 1998). However, in some populations the heritable craniofacial morphology can be the result of natural selection (Roseman, 2004; Bernal et al.,

2006), even though these influences can be considered negligible in a global scale (Relethford, 2004). For instance, some studies suggest that natural selection appears to have shaped the among-region differences in the modern human cranium (e.g. nasal shape), principally in cold climate regions such as Siberia and Tierra del Fuego (Herna´ndez et al., 1997; Lalueza et al., 1997a; Gonza´lez-Jose´, 2003; Roseman, 2004; Bernal et al., 2006). Therefore, natural selection as well as phenotypic plasticity can generate homoplasies in craniofacial variation without a genealogical meaning (Lieberman, 1999; Collard and Wood, 2000). Even though the integration of molecular and morphological evidence could allow a much better understanding of the process that gave rise to the distinctiveness of southernmost Patagonian populations, such a joint analysis has not been performed to date. The aim of this work is to integrate the craniofacial morphological variation of southern South American populations with the results of mtDNA haplogroup variation in order to contribute to the discussion about South America peopling. Specifically, this research tests that hypothesis that the craniofacial singularity of southernmost Patagonian populations is related to evolutionary local process (i.e., genetic drift and natural selection). Furthermore, the results obtained are discussed considering the phylogenetic studies of mtDNA and Y chromosome. Because the causes of craniofacial morphological differentiation of Tierra del Fuego populations are still a controversial subject, the comparison with neutral variation depicted by molecular data could contribute in the discussion of this problem. Several samples of osseous remains from Chaco, Pampa and Patagonia regions of South America (Fig. 1) with mtDNA information (Moraga et al., 2000; Demarchi et al., 2001; Goicoechea et al., 2001) are used in this work for the analysis of evolutionary relationships. The craniofacial morphometric variation is analyzed with geometric morphometrics techniques (Adams et al., 2004) employing an arrangement of landmarks and semilandmarks (Bookstein, 1997), which are a powerful tool for the analysis of morphological variation (Gunz et al., 2004; Sheets et al., 2004; Perez et al., 2006).

MATERIALS AND METHODS Samples In this work we analyze seven samples of undeformed male and female adult (ca. 18–45 years) crania from Patagonia, Pampa, and Chaco (Fig. 1; Tables 1 and 2). These samples come from local population or demes with available mtDNA information (Table 2; Moraga et al., 2000; Demarchi et al., 2001; Goicoechea et al., 2001). Estimations of sex and age were made on the basis of cranial and pelvic features (Buikstra and Ubelaker, 1994). The specimens are housed at Museo de La Plata (La Plata, Argentina), Museo Etnogra´fico, J. B. Ambrosetti, (Buenos Aires, Argentina) and Instituto de la Patagonia Austral (Punta Arenas, Chile). Numerous authors have stated the difficulty of defining human demes for evolutionary relationships analysis; the most frequently used criteria are ethnographic units (e.g. tribes) and geographically defined clusters of people (e.g. regions, villages) (Cavalli-Sforza et al., 1994). Moraga et al. (2000), Demarchi et al. (2001), and Goicoechea et al. (2001) grouped individuals according to their ethnic affinities because the living groups they

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MORPHOLOGICAL DIFFERENTIATION OF HUMAN POPULATIONS FROM TIERRA DEL FUEGO analyzed were not located in their traditional area. The skeletal samples analyzed here were grouped based on ethnographic criteria, and in those cases for which ethnic affinity was unknown, the individuals were clustered geographically. The remains of Mapuches from Salinas Grandes (Province of La Pampa, Argentina), Tobas from Chaco, Yamanas and Selknam from Tierra del Fuego and Aonikenk from South Continental Patagonia correspond to populations from historical times (ca. S XVII to XIX) related to the corresponding ethnographic groups. On the other hand, later late Holocene (ca. 1,500 years BP to historical times) samples from Formosa and

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Chubut (Fo and ChV) correspond geographically to the distribution of Matacos and Tehuelches, respectively, at the time of European contact.

Analysis of mtDNA haplogroups Frequencies of mtDNA haplogroups obtained from published data (Table 2) were employed for the calculation of Euclidian distance between the analyzed samples that was then used to estimate haplogroup-based evolutionary relationships among these groups. Euclidean distance was used because the morphometric analysis uses the same geometric space; however most distance measurements give similar results (Cavalli-Sforza et al., 1994). The description of the methods used to extract, amplify and determine mtDNA haplogroups is detailed in Moraga et al. (2000), Demarchi et al. (2001), and Goicoechea et al. (2001). The matrices based on Euclidean distance for haplogroups frequency were used to perform Principal Coordinate analyses (PCO, which performed over Euclidean distances generates the same results as a Principal Component analysis on the original variables). The first principal coordinates scores display a low dimensional representation of the distance matrix (Gower, 1966). Principal Coordinates analysis involves transforming a distance matrix into a matrix of associations from which latent roots and vectors are extracted using singular value decomposition. As each successive component accounts for the majority of the total residual variance, only a few axes (commonly two or three) are needed to represent the distance matrix.

Geometric morphometrics analysis of cranial traits

Fig. 1. Map showing geographic location of the crania samples analyzed. Drawing by Marina Perez.

Images of the skulls in frontal and lateral view were obtained with an Olympus SP 350 digital camera. These views were selected according to previous works that discussed the peopling of the southernmost South America using facial data (e.g. Cocilovo and Di Rienzo, 1984, 1985; Cocilovo and Guicho´n, 1985, 1986; Rothhammer and Silva, 1990) or traits observed principally in lateral norm (i.e., robusticity and dolichocephaly; Imbelloni, 1937; Lahr, 1995). For frontal view images the skulls were positioned in the Frankfurt plane and the camera lens was located in the coronal plane; the images were taken at 250 mm from the prosthion point. For lateral view images the photographs were taken at 300 mm from the euryon point, placing the skull in the Frankfurt plane and the camera lens in the midsagittal plane. Eight landmarks and thirty-four semilandmarks were obtained from the frontal view (Fig. 2a); seventeen landmarks and twenty semilandmarks were obtained from the lateral view (Fig. 2b). The application MakeFan6

TABLE I. Samples analyzed Samples

Abrr.

M

F*

T*

Region

Toba Formosa Mapuche Chubut Valley Aonikenk Selknam Yamana

To Fo Ma ChV Ao Selk Yam

8 7 15 10 9 9 8

– 5 16 10 – 8 8

8 12 31 20 9 17 16

Chaco Chaco Pampa North Patagonia South Patagonia Tierra del Fuego (South Patagonia) Tierra del Fuego (South Patagonia)

*

*

n for morphometric analyses.

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S.I. PEREZ ET AL. TABLE II. mtDNA haplogroups frequencies

Samples

n

A

B

C

D

References

Toba Formosa Mapuche Chubut Valley Aonikenk Selknam Yamana

30 44 58 31 15 13 32

13.3 9.1 6.1* 0 0 0 0

46.7 54.5 36* 20.7 0 0 0

6.7 20.5 23.9* 24.1 26.7 50* 63

26.7 15.9 34* 55.2 73.3 50* 37

Demarchi et al., 2001 Demarchi et al., 2001 Demarchi et al., 2001 Goicoechea et al., 2001 Demarchi et al., 2001 Demarchi et al., 2001 Demarchi et al., 2001; Moraga et al., 2000

*

These frequencies were modified because in this study the haplogroups included in the category ‘‘Others’’ were not considered.

Fig. 2. Allocated landmarks (n) and semilandmarks (l) on craniofacial structures registered. Drawing by Marina Perez.

(Sheets, 2003), which places alignment ‘‘fans’’ at equal angular displacements along a curve, was used to ensure consistent placement of the craniofacial semilandmark coordinates. Both landmarks and semilandmarks were afterwards digitized using tpsDIG 1.40 software (Rohlf, 2006). The effects of location, scaling and orientation in landmark configurations were removed using Generalized Procrustes analysis (Gower, 1975; Rohlf, 1990; Rohlf and Slice, 1990). Centroid size was used as size measurement (Bookstein, 1991). Semilandmarks of the crania were aligned by means of perpendicular projection or minimum Procrustes distance criteria (Andresen et al., 2000; Bookstein et al., 2002; Sheets et al., 2004; Perez et al., 2006). This operation extends the generalized least square (GLS) Procrustes superimposition (Gower, 1975; Rohlf, 1990; Rohlf and Slice, 1990): sliding the semilandmarks along the outline curve until they match as well as possible the positions of corresponding points along the outline of a reference specimen (Adams et al., 2004). This is done because the variation along tangent directions is not informative, and only the coordinate normal to the outline bears information about differences between specimens or groups (Bookstein, 1997; Bookstein et al., 2002). In this study, tpsRelw 1.44 (Rohlf, 2006) was used to align the semilandmarks along their respective curves, sliding them along so as to minimize the Procrustes distance between the subject and the ref-

erence (Sampson et al., 1996; Sheets et al., 2004; Perez et al., 2006). Consensus specimens (Bookstein, 1991) were calculated for each sample. Since morphometric means based on at least five individuals are accurate for intraspecific comparisons (Perez, 2006; Polly, 2003, 2005), only samples with more than five individuals were included. Shape differences between these specimens were studied by thin-plate splines (Bookstein, 1989) and Relative Warps analysis (Bookstein, 1991; Rohlf, 1993). The Relative warps are principal components obtained from the covariance matrix of partial warps and they describe localized change among landmarks and semilandmarks, as well as uniform vectors that describe global change (Bookstein, 1991; Rohlf, 1993, 1996). The first relative warps, as principal coordinates, can be interpreted as the dimensions that best reproduce the Euclidean distances (see Slice, 2001) between all the cases of the data set using linear combinations of the original variables (see Reyment and Jo¨reskog, 1993). The Euclidean distance, as in the haplogroup-based approach, was used to estimate the morphometric-based evolutionary relationships among groups. The alpha parameter, which determines the relative weighting of the principal warps (eigenvectors of the bending energy matrix, see Bookstein, 1991; Rohlf, 1993, 1996) at different scales, was set at 0 (zero), as suggested by Rohlf (1993). An important

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MORPHOLOGICAL DIFFERENTIATION OF HUMAN POPULATIONS FROM TIERRA DEL FUEGO aspect of this analysis is that one can express the results of statistical analysis as an intuitive deformation grid diagram of each case over the mean form or reference. The analyses were performed using the Relative warps 1.44 software (Rohlf, 2006). The patterns of ordination produced by Relative Warps and Principal Coordinate analyses, as well as the geographic location of the samples, were compared using the Procrustes method (Gower, 1971; Peres-Neto and Jackson, 2001). This method scales and rotates the ordinations, using a minimum squared differences criterion, to find an optimal superimposition that maximizes their fit. The sum of the squared residuals between configurations in their optimal superimposition can then be used as a measurement of association (m12; Gower, 1971). A permutation procedure (PROTEST; 10,000 permutations) has been used afterwards to assess the statistical signifi-

Fig. 3. Principal coordinates analysis based on the molecular data in Table 2.

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cance of the Procrustean fit (Jackson, 1995). Procrustes analysis was performed using vegan 1.4.4 package for R 1.9.1 (Ihaka and Gentleman, 1996).

RESULTS The principal coordinate scores based on molecular data (Table 2) show that the samples from Patagonia and Tierra del Fuego are separated from the Chaco and Mapuche samples (Fig. 3). The Chaco and Mapuche samples are close to each other along positive values of first principal coordinate, and the Yamana, Chubut Valley, Aonikenk and Selknam samples are in the opposite extreme along this principal coordinate. When frontal view landmarks and semilandmarks of male and female individuals are analyzed the relative warps show similar results to the observed in haplogroups analyses (Fig. 4a,b). The Relative Warps analysis (Fig. 4a,b) shows that axes 1 and 2 separate the Patagonian (including Tierra del Fuego) from the Pampa and Chaco samples. The Procrustes analysis shows high values of association between morphometric and haplogroup data (male: m12 ¼ 0.71, P ¼ 0.05; and female m12 ¼ 0.73; P ¼ 0.21). Figure 5 displays the variation between Pampa/Chaco and Patagonian samples based on Relative Warps analyses performed with semilandmarks of male and female samples. The analysis of frontal landmarks and semilandmarks of male individuals shows shape differences between samples that are located in the orbital and zygomatic regions (Fig. 5a,b). For female individuals the main shape differences between Pampa/Chaco and Patagonian samples are located in the orbital region (Fig. 5c,d). On the other hand, when the lateral view landmarks and semilandmarks of male individuals are analyzed the relative warps differ slightly from the results of haplogroups analyses (Fig. 6a,b). The male southern Patagonian and Tierra del Fuego samples (Aonikenk, Selknam and Yamana) differ from the others samples (Toba, Formosa, Mapuche and Chubut Valley), and the female sample does

Fig. 4. Relative warps analysis based on landmark and semilandmark data of frontal view for male and female individuals (a and b, respectively).

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Fig. 5. Deformation grids representing the variation in frontal view between the Pampa/Chaco and Tierra del Fuego samples in relative warps analysis for male (a and b, respectively) and female individuals (c and d, respectively).

not show a clear geographic pattern of variation. The Procrustes analysis shows lower association values between morphometric and haplogroup data than frontal view data (male: m12 ¼ 0.49, P ¼ 0.59; and female m12 ¼ 0.64, P ¼ 0.52). Figure 7 shows the shape variation between southern Patagonian and Pampa/Chaco samples based on Relative Warps analyses performed with semilandmarks of male and female samples. The analysis of lateral view of male individuals shows that the shape differences between

samples are located in the relative length and height of the cranial vault, and the robusticity of zygomatic, glabellar and mastoid regions (Fig. 7a,b). The samples from Tierra del Fuego and southern Patagonia show the greatest robusticity and the longest but lowest crania (Fig. 7b). The analysis of females indicates little variation in these traits among samples (Fig. 7c,d). Finally, the Procrustes analysis shows high association values between haplogroup data and the geographic

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MORPHOLOGICAL DIFFERENTIATION OF HUMAN POPULATIONS FROM TIERRA DEL FUEGO

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Fig. 6. Relative warps analysis based on landmark and semilandmark data of lateral view for male and female individuals (a and b, respectively).

Fig. 7. Deformation grids representing the variation in lateral view between the Pampa/Chaco and Tierra del Fuego samples in Relative warps analysis for male (a and b, respectively) and female individuals (c and d, respectively).

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localization of the samples (m12 ¼ 0.78, P ¼ 0.02). The association between morphometric data and geographic settlement was high and significant for males (frontal view: m12 ¼ 0.65, P ¼ 0.04; and lateral view m12 ¼ 0.67, P ¼ 0.02), but low and non significant for females (frontal view: m12 ¼ 0.59, P ¼ 0.32; and lateral view m12 ¼ 0.49, P ¼ 0.62). The geographic pattern observed for haplogroup and facial data (Figs. 3 and 4) is explained by the clear separation between Patagonian and Chaco/ Pampa samples. However, the high association of ordinations based on morphometric data from lateral view with geographic localization for male individuals is explained by the clear separation between southernmost continental Patagonian/Tierra del Fuego (Aonikenk, Selknam and Yamana) and north Patagonian, Pampa and Chaco samples (Chubut Valley, Mapuche, Toba and Formosa) (Fig. 6a). The high craniofacial robusticity and dolichocephaly are present only in the southernmost Patagonian and Tierra del Fuego samples (Figs. 6a and 7b).

DISCUSSION The results of the analysis of haplogroups frequency presented here show that the local populations are differentiated by their spatial distance, displaying a latitudinal gradient (Fig. 3; Table 2). These are the results generally observed for the variation of haplogroups in South America, with a pattern of decreasing A and B haplogroups from north to south, whereas the haplogroups C and D tend to increase in the same direction (Moraga et al., 2000; Schurr, 2004; Schurr and Sherry, 2004; Garcia et al., 2006). It is important to take into account some limitations of mtDNA haplogroup data, such as the influence of stochastic factors as sampling error, because they are single genetic systems (CavalliSforza et al., 1994; Goicoechea et al., 2001), and the fact that these data represent only one marker inherited solely from a parent (Bravi, 2005; Jobling and TylerSmith, 2003). However, the phylogenetic analyzes of mtDNA (Moraga et al., 2000; Bravi, 2005) and the study of Y-STRs sequences (Garcia-Bour et al., 2004) support the present results. The phylogenetic analysis of the Dloop mtDNA sequences of Tierra del Fuego and other South American populations demonstrate that C and D mtDNA haplogroups present in the southernmost populations are grouped with the corresponding haplogroup sequences from other South American populations (Moraga et al., 2000). Similarly, the analysis of mtDNA HVRI region for a skeletal sample from Tierra del Fuego shows that all the sequences can be easily ascribed to the Amerindian haplogroups C and D (Garcia-Bour et al., 2004). The study of Y-STRs sequences shows similar results (Garcia-Bour et al., 2004). These analyses support a common origin for all South American populations and suggest that the differentiation in haplogroup frequency was a local phenomenon, due to the loss of haplogroups A and B in Tierra del Fuego and southern continental Patagonian populations (Moraga et al., 2000; Garcia-Bour et al., 2004; Schurr, 2004; Schurr and Sherry, 2004). This trend is explained by Moraga et al. (2000) as the result of founder effect, which occurred during the initial peopling of the Southern Cone of the continent by small Pleistocene hunter–gatherer groups. Because the loss of genetic variation due to instability or bottlenecks (genetic drift) is a common phenomenon in small populations (Excoffier and Schneider, 1999; Fuselli

et al., 2003), such hypothesis seems likely. In summary, the analyses of Y chromosome and mtDNA (Fig. 3; Moraga et al., 2000; Garcia-Bour et al., 2004; Schurr and Sherry, 2004) suggest that the process of differentiation of Tierra del Fuego and southern Patagonia populations could be local, and do not support the hypothesis that the Fueguians are descended from a pre-Asian-descent group different than that for the others Amerindians as was suggested on the basis of morphological evidence (Imbelloni, 1937; Lahr, 1995; Herna´ndez et al., 1997; Lalueza et al., 1997a; Gonza´lez-Jose´ et al., 2001). The craniofacial morphology analyzed in this study yields slightly different results according to the structures compared. The results from the facial skeleton of male and female samples agree with those obtained from mtDNA haplogroup frequencies, resulting in all Patagonian samples (Chubut Valley, Aonikenk, Selknam and Yamana) being detached from Pampa and Chaco samples (Figs. 3 and 4). Hence, the same mechanism that accounts for the pattern of frequency of haplogroups could explain the variation found in facial skeleton among the samples from the area under study. Conversely, when the lateral view is analyzed only the southernmost Patagonian and Tierra del Fuego male samples (Selknam, Aonikenk, and Yamana) are clustered together (Fig. 6a). The deformation grids show that southernmost Patagonian and Tierra del Fuego samples have the most robust and dolichocephalic crania (Fig. 7b). These results allow hypothesizing that mechanisms other than genetic drift (i.e. natural selection) acted to shape the pattern observed in the craniofacial structures present in the lateral view. Finally, the differentiation among samples on the basis of robusticity and dolichocephaly is not clearly present in female individuals (Fig. 7c,d). This can be due either to the low morphological differentiation among female individuals or to the fact that we were not able to analyze a set of samples equivalent to the male ones, since some samples were not represented by female individuals. Further analyses are needed to elucidate the causes of these different results between females and males in the pattern of morphological variation. Our results about facial morphology agree with previous studies (Cocilovo, 1981; Cocilovo and Di Rienzo, 1984, 1985; Cocilovo and Guicho´n, 1985, 1986; Rothhammer and Silva, 1990; Rothhammer et al., 1997 Guicho´n, 2002) that find strong association between morphological and geographical distance. The hypothesis of a local origin for the morphological variation of Tierra del Fuego was advanced on the basis of such results. In particular, the detected pattern of latitudinal variation was interpreted as the result of founder effect or isolation by distance (Rothhammer and Silva, 1990; see discussion in Moraga et al., 2000). The previous statements contrasts with the hypothesis that explains the craniofacial singularity of Fueguian populations as the result of a separate origin and isolation from the remaining Amerindian populations (Lahr, 1995; Hernandez et al., 1997; Lalueza et al., 1997; Gonza´lez-Jose´ et al., 2001). Under this hypothesis the southernmost populations could have retained the ancestral characters, which were present in the first inhabitants of America. This idea has been very widespread since the end of the 19th century, although in somewhat different versions. The first researchers included the Yamanas from Tierra del Fuego and other ethnographic groups, such as the Botocudos from Brazil and the

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MORPHOLOGICAL DIFFERENTIATION OF HUMAN POPULATIONS FROM TIERRA DEL FUEGO Pericu´ from Baja California, within the Lagoa Santa race (derived from the Lagoa Santa site in Minas Gerais, Brazil), which represents the first inhabitants of America (ten Kate, 1884, 1885, 1892; Hansen, 1888; Hyades and Deniker, 1891; Sergi, 1911; von Eickstedt, 1934). Quatrofages (1879) defined this race, also named La´guida (Imbelloni, 1937, 1938) or Paleo-american (Deniker, 1900) for other researches. The ‘‘antiquity’’ of these groups was proposed based on their craniofacial traits, which were considered as ‘‘primitive’’ due to their resemblance to Australian-Melanesian populations (Sergi, 1887, 1911; Hooton, 1933; Gusinde, 1989; among others; see Marcellino and Colantonio, 1985). Imbelloni (1937) divided the Lagoa Santa race into Fue´guidos, represented by the Yamanas from Tierra del Fuego, and La´guidos, represented by the prehistoric inhabitants of Lagoa Santa region. The former were considered as the first inhabitants of America by reason of their marginal geographical position (Imbelloni, 1937). More recently, some authors have established that relicts of the Palaeoamerican stock could be observed in geographically isolated areas of the New World. In these studies, Tierra del Fuego, Bogota´ savannah and Baja California (Lahr, 1995; Hernandez et al., 1997; Lalueza et al., 1997a; Gonza´lez-Jose´ et al., 2003, 2004; Neves et al., 2006; Pucciarelli et al., 2006) are considered as areas with ‘‘relict populations’’ in a similar way to the previous works (e.g. ten Kate, 1884, 1885; Imbelloni, 1937, 1938). It is remarkable that the works that found little variation between Tierra del Fuego and other South American populations, which could be explained by local processes, were performed using facial craniometrical measurements (a procedure developed to avoid the influence of cranial deformation; Cocilovo and Di Rienzo, 1984, 1985; Cocilovo and Guicho´n, 1985, 1986; Rothhammer and Silva, 1990; Guicho´n, 2002). In contrast, the works that asserted the existence of two human stocks in South America (or several in the case of early works) found differences principally in cranial length, height and breadth, as well as robusticity (Imbelloni, 1937; Neves and Pucciarelli, 1989; Lahr, 1995; Gonza´lez-Jose´ et al., 2003, 2004). Such discrepancies could be related to the main causes of morphological variation in the different osseous structures (Atchley and Hall, 1991; Hanken and Hall, 1993). As noted above, slightly different results between structures corresponding to frontal and lateral views, which could be linked to different evolutionary mechanisms, were also found in the present study. Regarding this, a number of surveys have demonstrated that the human skull is subdivided into partially autonomous modules that may correspond to functional and development subunits (Cheverud, 1996; Leamy et al., 1999; Gonza´lez-Jose´ et al., 2004b). Given the genetic architecture of a modular structure, this implies that pleiotropic effects are concentrated within modules but are relatively weak among modules (Cheverud, 1996; Wagner, 1996; Leamy et al., 1999; Klingenberg et al., 2004). As it has been shown in previous works, the facial skeleton bears key information about evolutionary relationships, i.e. the apportionment of genetic variation among interbreeding demes (Smith, 2006; Perez et al., 2007). The traits analyzed in lateral view are less consistent with the evolutionary relationships established by means of molecular data probably because the analyzed traits, such as robusticity, might be related to environmental factors (Churchill, 1998; Bulbeck, 2001; Bernal et al.,

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2006). The greater dolichocephaly in these populations may be partially due to the robusticity of the glabella and nuchal crest, since these traits show high association with the relative length of the crania in the samples from the studied area, particularly in male individuals. The results of Singular warps analysis show a correlation of 0.94 between the first axis representing the robusticity and the first axis representing the vault contour (Perez et al., 2006, unpublished results). The study of the inner and outer mid-sagittal vault to evaluate the contribution of bone thickness to cranial shape would be useful to achieve a better understanding of the relationship between robusticity and dolichocephaly. In this way, the results obtained by Bookstein et al. (1999), based on the comparison of interior and exterior frontal bone profiles of archaic and modern Homo, indicate that both aspects vary independently, with the inner frontal table being very conservative whereas the outer table is highly variable and reflects brow-ridge structure. The craniofacial robusticity present in the populations from the area has been recently discussed in terms of the influence of mechanical loading, phylogenetic and climatic factors (Lahr and Wright, 1996; Lalueza et al., 1997a; Bernal et al., 2005, 2006). Gonzalez et al. (unpublished results) demonstrate that the differences in these traits between Tierra del Fuego-southern Patagonian and other South American populations are present early in the ontogeny (around 5 years old), providing evidence against phenotypic plasticity due to high mechanical loading as the main cause of robusticity. Additional evidence in support of this affirmation is presented by Bernal et al. (2005, 2006) through the quantification of dental macrowear as a measurement of mechanical loading sustained by individuals and the comparison of samples belonging to populations with diets based on hard and soft foods. The results indicate no association between hardness of consumed food and degree of robusticity since some skulls of hunter–gatherers showed the same development of robust features as farmers’ skulls (Bernal et al., 2006). Likewise, the dental wear observed in southern Patagonia samples is comparatively low in relation to other South American samples (Bernal et al., 2005). Therefore, the difference in biomechanical loadings sustained by the individuals does not seem to be the main cause of variation in robusticity among these populations. On the other hand, the comparison of craniofacial morphology of early-middle Holocene samples from South America with late Holocene samples from Tierra del Fuego does not support the hypothesis that robusticity results from the retention of ancestral characters (Bernal et al., 2006). Whereas the later late Holocene samples from South Patagonia exhibit high levels of craniofacial robusticity, the earlier samples from this region as well as those from other regions of South America show lesser development of robust features (Bernal et al., 2006). In contrast, Bernal et al. (2006) found a significant association between latitude and craniofacial robusticity, with the most robust craniofacial morphologies occurring at the highest latitudes (similar to the pattern found in this work). The hypothesis proposed is that the action of climatic factors may account for the features observed, since several authors have proposed that skeletal robusticity in cold-adapted populations can result from endocrine action (see discussion in Churchill, 1998). This is partially supported because the influence of climate on several physiological characteristics (e.g. increased basal metabolic rates partially

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related to upregulation of thyroid hormones) is well documented (Leonard et al., 2002; Snodgrass et al., 2005) and because the systemic physiological control over robusticity throughout the skeleton has been demonstrated by experimental studies. Such studies have documented the stimulating effect of hormones on craniofacial robusticity, cranial vault thickening, brow-ridge growth (Lieberman, 1996), development of major areas of muscle attachment (e.g. malar bone; Vogl et al., 1993), as well as muscle development (Riesenfeld, 1975; Vogl et al., 1993). These changes could explain the high robusticity and dolychocephaly in the southern Patagonian and Tierra del Fuego samples, particularly because the dolychocephaly in these populations is related with a major development of glabellar and occipital muscle attachment areas in male individuals (Figs. 6a and 7b).

ACKNOWLEDGMENTS We are sincerely grateful to Sergio Furtado dos Reis for his discussions about origin and causes of morphological variation, which inspired the research presented in this manuscript. We thank Hector M. Pucciarelli (Divisio´n Antropologı´a, Facultad de Ciencias Naturales y Museo, La Plata, Argentina), Ine´s Baffi and Leandro Luna (Museo Etnogra´fico ‘‘J. B. Ambrosetti’’, Buenos Aires, Argentina), Mateo Martinic (Instituto de la Patagonia Austral de la Universidad de Magallanes) for granting access to the human skeletal collections under their care. We also thank to Cecilia Morgan and Amelia Barreiro for help with the English version of the manuscript and Marina Perez for the drawings (Figs. 1 and 2).

LITERATURE CITED CONCLUSION The craniofacial singularity of the Tierra del Fuego and southern Patagonia populations was established based on their high robusticity and dolichocephaly with respect to the rest of Amerindians. This pattern do not seem to be the result of multiple migratory events, in which the southernmost populations are seen as descendants of the first American settlers whereas the Amerindians would descend from a later Asian-descent migration, because mtDNA data indicate that the same haplogroups are shared by all South American populations, including those from the extreme South of the continent (Moraga et al., 2000; Garcia-Bour et al., 2004). In addition, the hypothesis of a Paleoamerican origin for these populations is based on comparisons with samples of human remains from South America dated to the early-middle Holocene (e.g. Lagoa Santa ca. 9000–6000 year 14C BP, Dillehay, 2000; Neves and Hubbe, 2005; Tequendama, ca. 7300–5800 year 14C BP, Correal Urrego and van der Hammen, 1977; Arroyo Seco 2 ca. 7800– 6300 year 14C BP, Politis and Madrid, 2001; and Ban˜o Nuevo ca. 9000–8500 year 14C BP, Mena and Reyes, 2001), which represent populations corresponding to moments posterior to the diversification of the first settlers. On the other hand, our results show a clear geographical ordination of the samples based on mtDNA haplogroup frequency and facial morphology, grouping all Patagonia samples. This geographic pattern of facial and molecular diversity may reflect the effect of genetic drift that occurred in the small founding populations isolated by distance or geographic barriers (O’Rourke et al., 1999; Powell and Neves, 1999; Moraga et al., 2002; Fuselli et al., 2003; Schurr, 2004). However, our results suggest that different evolutionary mechanisms, such as natural selection, could have affected other traits, e.g. robusticity, since the pattern of variation obtained with these data differ from those obtained from molecular data, showing a clear differentiation of the southern Patagonian and Tierra del Fuego samples. This hypothesis requires further analysis focused on the estimation of the rate of morphological change in populations under diverse environmental conditions and different evolutionary processes. In particular, it is important to determine whether genetic drift or natural selection could account for the singular morphology of later late Holocene populations from Tierra del Fuego and southern Patagonia.

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