Morphological differentiation of aboriginal human populations from Tierra del Fuego (Patagonia):...

Morphological Differentiation of Aboriginal HumanPopulations From Tierra del Fuego (Patagonia):Implications for South American Peopling

S. Ivan Perez,* Valeria Bernal, and Paula N. Gonzalez

CONICET, Division Antropologıa, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata,La Plata 1900, Buenos Aires, Argentina

KEY WORDS South American aborigines; evolutionary relationships; geometric morphometrics;mtDNA

ABSTRACT This study aims to integrate the cranio-facial morphological variation of southern South Ameri-can populations with the results of mtDNA haplogroupvariation, to discuss the South America peopling.Because the causes of morphological differentiation ofFueguian populations are still a controversial subject,the comparison with neutral variation could contributeto elucidate them. Samples of human remains fromSouth America regions were used to analyze the evolu-tionary relationships. Several craniofacial traits observedin frontal and lateral view were analyzed by means ofgeometric morphometrics techniques, and the evolution-ary relationships based on morphological and moleculardata were established in base to ordination analyses.The results from the facial skeleton agree with thoseobtained from mtDNA haplogroup frequencies, with LaPampa/Chaco samples detached from the Patagonian

samples. Hence, the same mechanism that accounts forthe pattern of frequency of haplogroups could explainthe variation found in facial skeleton among the sam-ples. It is suggested that such geographic pattern of cra-niofacial and molecular diversity may reflect the effect ofgenetic drift that occurred in the small founding popula-tions isolated by distance or geographic barriers. Con-versely, the results obtained using the traits from thelateral view slightly differ from the molecular results,showing differences between southernmost Patagonianand the other samples. Therefore, mechanisms otherthan genetic drift (e.g., natural selection) could haveacted to shape the pattern observed in some craniofacialstructures present in the lateral view, characterized bythe fact that the southernmost Patagonian samples dis-play the most robust and dolichocephalic crania. Am JPhys Anthropol 133:1067–1079, 2007. VVC 2007 Wiley-Liss, Inc.

The biological origin and evolution of the aboriginalpopulations from southernmost Patagonia and Tierra delFuego have been intensely studied since the end of the19th century (e.g. Hyades and Deniker, 1891; Imbelloni,1923, 1937; Bormida, 1953, 1954; Cocilovo and Guichon,1985, 1986; Gusinde, 1989; Lahr, 1995; Hernandez et al.,1997; Lalueza et al., 1997a; Garcia-Bour, 1998; Garcia-Bour et al., 1998, 2004; Moraga et al., 2000; Gonzalez-Jose et al., 2004). These early investigations alreadypointed out the craniofacial singularity of these popula-tions in relation to other American populations (seeImbelloni, 1937; Munizaga, 1976; Marcellino and Colan-tonio, 1985), characterized particularly by high levels ofcraniofacial robusticity and dolichocephaly (e.g. Imbel-loni, 1937; Lahr, 1995). Different hypotheses were pro-posed to account for such singularity, but most of themcan be grouped in two propositions: (a) a different ances-tral origin for Fueguian and most other American popu-lations; (b) a local process of diversification.In the late 19th and early 20th centuries, several

authors argued that the human groups occurring inTierra del Fuego, particularly the Yamanas, were mem-bers of an antique race that peopled America early,before the arrival of Asian-descent populations, whichgave origin to the Amerindians. This hypothesis wasmaintained, together with the multiple waves model ofAmerican peopling, based on the fact that the craniofa-cial morphology (i.e., robusticity and dolichocephaly)of these populations was similar to the morphology con-sidered archaic in recent populations from Tasmania,

Australia and Melanesia (Imbelloni, 1937, 1938). Re-cently, multivariate craniometric analysis suggested theexistence of two ‘‘human stocks’’ that peopled SouthAmerica, one corresponding to the first human migrationto the continent, the Palaeoamericans, originated in apre-Asian-descent population inhabiting Asia in pre-gla-cial times (morphologically similar to modern Austral-ians aborigines), and the other corresponding to a secondmigration, with Asian-descent (in the past named Mon-goloid) characteristics, from which most of the modernAmerindians derived (Neves and Pucciarelli, 1989, 1990;Lahr, 1995; Neves et al., 1999; Gonzalez-Jose et al.,2003; Pucciarelli et al., 2003; Sardi et al., 2004, 2005). Inthis context, several investigators have maintained thatthe Tierra del Fuego populations as well as other groupssuch as the ethnographical Pericu group of Baja Califor-nia would be a relict of the former Palaeoamericans

Grant sponsor: CONICET, Universidad Nacional de La Plata.

*Correspondence to: S. Ivan Perez, Division Antropologıa, Facul-tad de Ciencias Naturales y Museo, Museo de La Plata, Paseo delBosque s/n. La Plata 1900, Argentina.E-mail: [email protected]

Received 15 September 2006; accepted 6 March 2007

DOI 10.1002/ajpa.20633Published online 25 May 2007 in Wiley InterScience

(www.interscience.wiley.com).

VVC 2007 WILEY-LISS, INC.

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

(Lahr, 1995; Hernandez et al., 1997; Lalueza et al.,1997a; Gonzalez-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 andGuichon, 1985, 1986; Rothhammer and Silva, 1990;Rothhammer et al., 1997) found that the Tierra delFuego populations form a differentiated group withrespect to other South Americans populations (e.g., fromPatagonia, Pampa, Sierras Centrales, and NorwestArgentina), and such differentiation is associated to lati-tudinal location of populations (see Guichon, 2002).Some investigators proposed that the existence of thisgeographic pattern suggests that the differentiation ofTierra del Fuego populations could have emerged bylocal processes as gene flow, genetic drift, or naturalselection (Cocilovo and Di Rienzo, 1984, 1985; Cocilovoand Guichon, 1985, 1986; Rothhammer and Silva, 1990),and all populations of the southern South America wouldbe derived from one Asian-descent population or a groupof related Asiatic populations (Moraga et al., 2000). Thisidea agrees with the hypothesis maintained early byHrdlicka (1912) and then by Turner II (1984) and Green-berg et al. (1986), who, on the basis of craniometric,dental, and linguistic data, established that all SouthAmerican populations descended from a unique Asian-descent population.The study of evolutionary relationships in human pop-

ulations from Tierra del Fuego was mainly limited tocraniofacial data until the end of the 20th century, butin recent years several analyses have used mtDNA forthe study of the differentiation of Tierra del Fuego popu-lations (Merriwether et al., 1995; Lalueza, 1996; Laluezaet al., 1997b; Garcia-Bour et al., 1998, 2004; Moragaet al., 2000). The results obtained also support the singu-larity of Fueguian populations, and the cause for it wasattributed either to a different ancestral origin (e.g.Lalueza et al., 1997b; Garcia-Bour et al., 1998) or anin situ differentiation (e.g. Merriwether et al., 1995).However, the most recent phylogenetic analyses ofmtDNA and Y chromosome support the existence of aunique origin for South American populations, includingthe 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 aredistinct from the rest of Amerindians, but some contro-versies arise in relation to the magnitude and causes ofsuch distinctiveness. This might be partially due to thegenealogical information carried by each type of data.DNA data are free from environmental influence duringontogeny, and in the case of the mtDNA and some por-tions of Y chromosome, they do not seem to be under-going recombination, are transmitted intact from parentsto 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, thecraniofacial differences among human populations resultfrom genetic and environmental variation (i.e. pheno-typic plasticity). The genetic apportionment of craniofa-cial differences reflects generally recurrent processessuch as gene flow and genetic drift and nonrecurrentevents such as expansion, contraction, and populationreplacement (Relethford and Lees, 1982; Templetonet al., 1995; Templeton, 1998). However, in some popula-tions the heritable craniofacial morphology can be theresult of natural selection (Roseman, 2004; Bernal et al.,

2006), even though these influences can be considerednegligible in a global scale (Relethford, 2004). Forinstance, some studies suggest that natural selectionappears to have shaped the among-region differences inthe modern human cranium (e.g. nasal shape), princi-pally in cold climate regions such as Siberia and Tierradel Fuego (Hernandez et al., 1997; Lalueza et al., 1997a;Gonzalez-Jose, 2003; Roseman, 2004; Bernal et al.,2006). Therefore, natural selection as well as phenotypicplasticity can generate homoplasies in craniofacial varia-tion without a genealogical meaning (Lieberman, 1999;Collard and Wood, 2000).Even though the integration of molecular and morpho-

logical evidence could allow a much better understand-ing of the process that gave rise to the distinctiveness ofsouthernmost Patagonian populations, such a joint anal-ysis has not been performed to date. The aim of thiswork is to integrate the craniofacial morphological varia-tion of southern South American populations with theresults of mtDNA haplogroup variation in order to con-tribute to the discussion about South America peopling.Specifically, this research tests that hypothesis that thecraniofacial singularity of southernmost Patagonian pop-ulations is related to evolutionary local process (i.e.,genetic drift and natural selection). Furthermore, theresults obtained are discussed considering the phyloge-netic studies of mtDNA and Y chromosome. Because thecauses of craniofacial morphological differentiation ofTierra del Fuego populations are still a controversialsubject, the comparison with neutral variation depictedby molecular data could contribute in the discussion ofthis problem. Several samples of osseous remains fromChaco, 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 usedin this work for the analysis of evolutionary relation-ships. The craniofacial morphometric variation is ana-lyzed with geometric morphometrics techniques (Adamset al., 2004) employing an arrangement of landmarksand semilandmarks (Bookstein, 1997), which are apowerful 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 undeformedmale and female adult (ca. 18–45 years) crania fromPatagonia, Pampa, and Chaco (Fig. 1; Tables 1 and 2).These samples come from local population or demes withavailable 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 ofcranial and pelvic features (Buikstra and Ubelaker,1994). The specimens are housed at Museo de La Plata(La Plata, Argentina), Museo Etnografico, J. B. Ambro-setti, (Buenos Aires, Argentina) and Instituto de la Pata-gonia Austral (Punta Arenas, Chile).Numerous authors have stated the difficulty of defin-

ing human demes for evolutionary relationships analy-sis; the most frequently used criteria are ethnographicunits (e.g. tribes) and geographically defined clusters ofpeople (e.g. regions, villages) (Cavalli-Sforza et al.,1994). Moraga et al. (2000), Demarchi et al. (2001), andGoicoechea et al. (2001) grouped individuals according totheir ethnic affinities because the living groups they

1068 S.I. PEREZ ET AL.

American Journal of Physical Anthropology—DOI 10.1002/ajpa

analyzed were not located in their traditional area. Theskeletal samples analyzed here were grouped based onethnographic criteria, and in those cases for which eth-nic affinity was unknown, the individuals were clusteredgeographically. The remains of Mapuches from SalinasGrandes (Province of La Pampa, Argentina), Tobas fromChaco, Yamanas and Selknam from Tierra del Fuegoand Aonikenk from South Continental Patagonia corre-spond to populations from historical times (ca. S XVII toXIX) related to the corresponding ethnographic groups.On the other hand, later late Holocene (ca. 1,500 yearsBP to historical times) samples from Formosa and

Chubut (Fo and ChV) correspond geographically to thedistribution of Matacos and Tehuelches, respectively, atthe time of European contact.

Analysis of mtDNA haplogroups

Frequencies of mtDNA haplogroups obtained frompublished data (Table 2) were employed for the calcula-tion of Euclidian distance between the analyzed samplesthat was then used to estimate haplogroup-based evolu-tionary relationships among these groups. Euclidean dis-tance was used because the morphometric analysis usesthe same geometric space; however most distance meas-urements give similar results (Cavalli-Sforza et al.,1994). The description of the methods used to extract,amplify and determine mtDNA haplogroups is detailedin Moraga et al. (2000), Demarchi et al. (2001), and Goi-coechea et al. (2001).The matrices based on Euclidean distance for hap-

logroups frequency were used to perform Principal Coor-dinate analyses (PCO, which performed over Euclideandistances generates the same results as a PrincipalComponent analysis on the original variables). The firstprincipal coordinates scores display a low dimensionalrepresentation of the distance matrix (Gower, 1966).Principal Coordinates analysis involves transforming adistance matrix into a matrix of associations from whichlatent roots and vectors are extracted using singularvalue decomposition. As each successive componentaccounts for the majority of the total residual variance,only a few axes (commonly two or three) are needed torepresent the distance matrix.

Geometric morphometrics analysis ofcranial traits

Images of the skulls in frontal and lateral view wereobtained with an Olympus SP 350 digital camera. Theseviews were selected according to previous works that dis-cussed the peopling of the southernmost South Americausing facial data (e.g. Cocilovo and Di Rienzo, 1984,1985; Cocilovo and Guichon, 1985, 1986; Rothhammerand Silva, 1990) or traits observed principally in lateralnorm (i.e., robusticity and dolichocephaly; Imbelloni,1937; Lahr, 1995). For frontal view images the skullswere positioned in the Frankfurt plane and the cameralens was located in the coronal plane; the images weretaken at 250 mm from the prosthion point. For lateralview images the photographs were taken at 300 mmfrom the euryon point, placing the skull in the Frankfurtplane and the camera lens in the midsagittal plane.Eight landmarks and thirty-four semilandmarks wereobtained from the frontal view (Fig. 2a); seventeen land-marks and twenty semilandmarks were obtained fromthe lateral view (Fig. 2b). The application MakeFan6

TABLE I. Samples analyzed

Samples Abrr. M* F* T* Region

Toba To 8 – 8 ChacoFormosa Fo 7 5 12 ChacoMapuche Ma 15 16 31 PampaChubut Valley ChV 10 10 20 North PatagoniaAonikenk Ao 9 – 9 South PatagoniaSelknam Selk 9 8 17 Tierra del Fuego (South Patagonia)Yamana Yam 8 8 16 Tierra del Fuego (South Patagonia)

* n for morphometric analyses.

Fig. 1. Map showing geographic location of the crania sam-ples analyzed. Drawing by Marina Perez.

1069MORPHOLOGICAL DIFFERENTIATION OF HUMAN POPULATIONS FROM TIERRA DEL FUEGO


(Sheets, 2003), which places alignment ‘‘fans’’ at equalangular displacements along a curve, was used to ensureconsistent placement of the craniofacial semilandmark coor-dinates. Both landmarks and semilandmarks were after-wards digitized using tpsDIG 1.40 software (Rohlf, 2006).The effects of location, scaling and orientation in land-

mark configurations were removed using GeneralizedProcrustes analysis (Gower, 1975; Rohlf, 1990; Rohlf andSlice, 1990). Centroid size was used as size measurement(Bookstein, 1991). Semilandmarks of the crania werealigned by means of perpendicular projection or mini-mum Procrustes distance criteria (Andresen et al., 2000;Bookstein et al., 2002; Sheets et al., 2004; Perez et al.,2006). This operation extends the generalized leastsquare (GLS) Procrustes superimposition (Gower, 1975;Rohlf, 1990; Rohlf and Slice, 1990): sliding the semiland-marks along the outline curve until they match as wellas possible the positions of corresponding points alongthe outline of a reference specimen (Adams et al., 2004).This is done because the variation along tangent direc-tions is not informative, and only the coordinate normalto the outline bears information about differencesbetween specimens or groups (Bookstein, 1997; Book-stein et al., 2002). In this study, tpsRelw 1.44 (Rohlf,2006) was used to align the semilandmarks along theirrespective curves, sliding them along so as to minimizethe Procrustes distance between the subject and the ref-

erence (Sampson et al., 1996; Sheets et al., 2004; Perezet al., 2006).Consensus specimens (Bookstein, 1991) were calcu-

lated for each sample. Since morphometric means basedon at least five individuals are accurate for intraspecificcomparisons (Perez, 2006; Polly, 2003, 2005), only sam-ples with more than five individuals were included.Shape differences between these specimens were studiedby thin-plate splines (Bookstein, 1989) and RelativeWarps analysis (Bookstein, 1991; Rohlf, 1993). The Rela-tive warps are principal components obtained from thecovariance matrix of partial warps and they describelocalized change among landmarks and semilandmarks,as well as uniform vectors that describe global change(Bookstein, 1991; Rohlf, 1993, 1996). The first relativewarps, as principal coordinates, can be interpreted asthe dimensions that best reproduce the Euclidean dis-tances (see Slice, 2001) between all the cases of the dataset using linear combinations of the original variables(see Reyment and Joreskog, 1993). The Euclidean dis-tance, as in the haplogroup-based approach, was used toestimate the morphometric-based evolutionary relation-ships among groups. The alpha parameter, which deter-mines the relative weighting of the principal warps(eigenvectors of the bending energy matrix, see Book-stein, 1991; Rohlf, 1993, 1996) at different scales, wasset at 0 (zero), as suggested by Rohlf (1993). An important

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

TABLE II. mtDNA haplogroups frequencies

Samples n A B C D References

Toba 30 13.3 46.7 6.7 26.7 Demarchi et al., 2001Formosa 44 9.1 54.5 20.5 15.9 Demarchi et al., 2001Mapuche 58 6.1* 36* 23.9* 34* Demarchi et al., 2001Chubut Valley 31 0 20.7 24.1 55.2 Goicoechea et al., 2001Aonikenk 15 0 0 26.7 73.3 Demarchi et al., 2001Selknam 13 0 0 50* 50* Demarchi et al., 2001Yamana 32 0 0 63 37 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.



aspect of this analysis is that one can express the resultsof statistical analysis as an intuitive deformation griddiagram of each case over the mean form or reference.The analyses were performed using the Relative warps1.44 software (Rohlf, 2006).The patterns of ordination produced by Relative Warps

and Principal Coordinate analyses, as well as the geo-graphic location of the samples, were compared usingthe Procrustes method (Gower, 1971; Peres-Neto andJackson, 2001). This method scales and rotates the ordi-nations, using a minimum squared differences criterion,to find an optimal superimposition that maximizes theirfit. The sum of the squared residuals between configura-tions in their optimal superimposition can then be usedas a measurement of association (m12; Gower, 1971). Apermutation procedure (PROTEST; 10,000 permutations)has been used afterwards to assess the statistical signifi-

cance of the Procrustean fit (Jackson, 1995). Procrustesanalysis was performed using vegan 1.4.4 package for R1.9.1 (Ihaka and Gentleman, 1996).

RESULTS

The principal coordinate scores based on moleculardata (Table 2) show that the samples from Patagoniaand Tierra del Fuego are separated from the Chaco andMapuche samples (Fig. 3). The Chaco and Mapuche sam-ples are close to each other along positive values of firstprincipal coordinate, and the Yamana, Chubut Valley,Aonikenk and Selknam samples are in the oppositeextreme along this principal coordinate.When frontal view landmarks and semilandmarks of

male and female individuals are analyzed the relativewarps show similar results to the observed in hap-logroups analyses (Fig. 4a,b). The Relative Warps an-alysis (Fig. 4a,b) shows that axes 1 and 2 separate thePatagonian (including Tierra del Fuego) from the Pampaand Chaco samples. The Procrustes analysis shows highvalues of association between morphometric and hap-logroup data (male: m12 ¼ 0.71, P ¼ 0.05; and femalem12 ¼ 0.73; P ¼ 0.21). Figure 5 displays the variationbetween Pampa/Chaco and Patagonian samples based onRelative Warps analyses performed with semilandmarksof male and female samples. The analysis of frontallandmarks and semilandmarks of male individualsshows shape differences between samples that arelocated in the orbital and zygomatic regions (Fig. 5a,b).For female individuals the main shape differencesbetween Pampa/Chaco and Patagonian samples arelocated in the orbital region (Fig. 5c,d).On the other hand, when the lateral view landmarks and

semilandmarks of male individuals are analyzed the rela-tive warps differ slightly from the results of haplogroupsanalyses (Fig. 6a,b). The male southern Patagonian andTierra del Fuego samples (Aonikenk, Selknam andYamana) differ from the others samples (Toba, Formosa,Mapuche and Chubut Valley), and the female sample does

Fig. 3. Principal coordinates analysis based on the molecu-lar data in Table 2.

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



not show a clear geographic pattern of variation. The Pro-crustes analysis shows lower association values betweenmorphometric and haplogroup data than frontal view data(male: m12 ¼ 0.49, P ¼ 0.59; and female m12 ¼ 0.64, P ¼0.52). Figure 7 shows the shape variation between south-ern Patagonian and Pampa/Chaco samples based on Rela-tive Warps analyses performed with semilandmarks ofmale and female samples. The analysis of lateral view ofmale individuals shows that the shape differences between

samples are located in the relative length and height of thecranial vault, and the robusticity of zygomatic, glabellarand mastoid regions (Fig. 7a,b). The samples from Tierradel Fuego and southern Patagonia show the greatestrobusticity and the longest but lowest crania (Fig. 7b). Theanalysis of females indicates little variation in these traitsamong samples (Fig. 7c,d).Finally, the Procrustes analysis shows high association

values between haplogroup data and the geographic

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



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

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



localization of the samples (m12 ¼ 0.78, P ¼ 0.02). Theassociation between morphometric data and geographicsettlement was high and significant for males (frontalview: 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 (fron-tal view: m12 ¼ 0.59, P ¼ 0.32; and lateral view m12 ¼0.49, P ¼ 0.62). The geographic pattern observed forhaplogroup and facial data (Figs. 3 and 4) is explainedby the clear separation between Patagonian and Chaco/Pampa samples. However, the high association of ordina-tions based on morphometric data from lateral view withgeographic localization for male individuals is explainedby the clear separation between southernmost continen-tal Patagonian/Tierra del Fuego (Aonikenk, Selknamand Yamana) and north Patagonian, Pampa and Chacosamples (Chubut Valley, Mapuche, Toba and Formosa)(Fig. 6a). The high craniofacial robusticity and dolichoce-phaly are present only in the southernmost Patagonianand Tierra del Fuego samples (Figs. 6a and 7b).

DISCUSSION

The results of the analysis of haplogroups frequencypresented here show that the local populations are dif-ferentiated by their spatial distance, displaying a latitu-dinal gradient (Fig. 3; Table 2). These are the resultsgenerally observed for the variation of haplogroups inSouth America, with a pattern of decreasing A and Bhaplogroups from north to south, whereas the hap-logroups 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 intoaccount some limitations of mtDNA haplogroup data,such as the influence of stochastic factors as samplingerror, because they are single genetic systems (Cavalli-Sforza et al., 1994; Goicoechea et al., 2001), and the factthat these data represent only one marker inheritedsolely from a parent (Bravi, 2005; Jobling and Tyler-Smith, 2003). However, the phylogenetic analyzes ofmtDNA (Moraga et al., 2000; Bravi, 2005) and the studyof Y-STRs sequences (Garcia-Bour et al., 2004) supportthe present results. The phylogenetic analysis of the D-loop mtDNA sequences of Tierra del Fuego and otherSouth American populations demonstrate that C and DmtDNA haplogroups present in the southernmost popu-lations are grouped with the corresponding haplogroupsequences from other South American populations(Moraga et al., 2000). Similarly, the analysis of mtDNAHVRI region for a skeletal sample from Tierra del Fuegoshows that all the sequences can be easily ascribed tothe Amerindian haplogroups C and D (Garcia-Bouret al., 2004). The study of Y-STRs sequences shows simi-lar results (Garcia-Bour et al., 2004). These analysessupport a common origin for all South American popula-tions and suggest that the differentiation in haplogroupfrequency was a local phenomenon, due to the loss ofhaplogroups A and B in Tierra del Fuego and southerncontinental Patagonian populations (Moraga et al., 2000;Garcia-Bour et al., 2004; Schurr, 2004; Schurr andSherry, 2004). This trend is explained by Moraga et al.(2000) as the result of founder effect, which occurredduring the initial peopling of the Southern Cone of thecontinent by small Pleistocene hunter–gatherer groups.Because the loss of genetic variation due to instability orbottlenecks (genetic drift) is a common phenomenon insmall populations (Excoffier and Schneider, 1999; Fuselli

et al., 2003), such hypothesis seems likely. In summary,the analyses of Y chromosome and mtDNA (Fig. 3; Mor-aga et al., 2000; Garcia-Bour et al., 2004; Schurr andSherry, 2004) suggest that the process of differentiationof Tierra del Fuego and southern Patagonia populationscould be local, and do not support the hypothesis thatthe Fueguians are descended from a pre-Asian-descentgroup different than that for the others Amerindians aswas suggested on the basis of morphological evidence(Imbelloni, 1937; Lahr, 1995; Hernandez et al., 1997;Lalueza et al., 1997a; Gonzalez-Jose et al., 2001).The craniofacial morphology analyzed in this study

yields slightly different results according to the struc-tures compared. The results from the facial skeleton ofmale and female samples agree with those obtained frommtDNA haplogroup frequencies, resulting in all Patago-nian samples (Chubut Valley, Aonikenk, Selknam andYamana) being detached from Pampa and Chaco samples(Figs. 3 and 4). Hence, the same mechanism thataccounts for the pattern of frequency of haplogroupscould explain the variation found in facial skeletonamong the samples from the area under study. Con-versely, when the lateral view is analyzed only thesouthernmost Patagonian and Tierra del Fuego malesamples (Selknam, Aonikenk, and Yamana) are clusteredtogether (Fig. 6a). The deformation grids show thatsouthernmost Patagonian and Tierra del Fuego sampleshave the most robust and dolichocephalic crania (Fig.7b). These results allow hypothesizing that mechanismsother than genetic drift (i.e. natural selection) acted toshape the pattern observed in the craniofacial structurespresent in the lateral view. Finally, the differentiationamong samples on the basis of robusticity and dolichoce-phaly is not clearly present in female individuals (Fig.7c,d). This can be due either to the low morphologicaldifferentiation among female individuals or to the factthat we were not able to analyze a set of samples equiva-lent to the male ones, since some samples were not rep-resented by female individuals. Further analyses areneeded to elucidate the causes of these different resultsbetween females and males in the pattern of morphologi-cal variation.Our results about facial morphology agree with previ-

ous studies (Cocilovo, 1981; Cocilovo and Di Rienzo,1984, 1985; Cocilovo and Guichon, 1985, 1986; Rothham-mer and Silva, 1990; Rothhammer et al., 1997 Guichon,2002) that find strong association between morphologicaland geographical distance. The hypothesis of a local ori-gin for the morphological variation of Tierra del Fuegowas advanced on the basis of such results. In particular,the detected pattern of latitudinal variation was inter-preted as the result of founder effect or isolation by dis-tance (Rothhammer and Silva, 1990; see discussion inMoraga et al., 2000).The previous statements contrasts with the hypothesis

that explains the craniofacial singularity of Fueguianpopulations as the result of a separate origin and isola-tion from the remaining Amerindian populations (Lahr,1995; Hernandez et al., 1997; Lalueza et al., 1997;Gonzalez-Jose et al., 2001). Under this hypothesis thesouthernmost populations could have retained the ances-tral characters, which were present in the first inhabi-tants of America. This idea has been very widespreadsince the end of the 19th century, although in somewhatdifferent versions. The first researchers included theYamanas from Tierra del Fuego and other ethnographicgroups, such as the Botocudos from Brazil and the



Pericu from Baja California, within the Lagoa Santarace (derived from the Lagoa Santa site in Minas Gerais,Brazil), which represents the first inhabitants of Amer-ica (ten Kate, 1884, 1885, 1892; Hansen, 1888; Hyadesand Deniker, 1891; Sergi, 1911; von Eickstedt, 1934).Quatrofages (1879) defined this race, also namedLaguida (Imbelloni, 1937, 1938) or Paleo-american(Deniker, 1900) for other researches. The ‘‘antiquity’’ ofthese groups was proposed based on their craniofacialtraits, which were considered as ‘‘primitive’’ due to theirresemblance to Australian-Melanesian populations(Sergi, 1887, 1911; Hooton, 1933; Gusinde, 1989; amongothers; see Marcellino and Colantonio, 1985). Imbelloni(1937) divided the Lagoa Santa race into Fueguidos, rep-resented by the Yamanas from Tierra del Fuego, andLaguidos, represented by the prehistoric inhabitants ofLagoa Santa region. The former were considered as thefirst inhabitants of America by reason of their marginalgeographical position (Imbelloni, 1937). More recently,some authors have established that relicts of the Palae-oamerican stock could be observed in geographically iso-lated areas of the New World. In these studies, Tierradel Fuego, Bogota savannah and Baja California (Lahr,1995; Hernandez et al., 1997; Lalueza et al., 1997a; Gon-zalez-Jose et al., 2003, 2004; Neves et al., 2006; Pucciar-elli et al., 2006) are considered as areas with ‘‘relict pop-ulations’’ in a similar way to the previous works (e.g. tenKate, 1884, 1885; Imbelloni, 1937, 1938).It is remarkable that the works that found little varia-

tion between Tierra del Fuego and other South Americanpopulations, which could be explained by local processes,were performed using facial craniometrical measure-ments (a procedure developed to avoid the influence ofcranial deformation; Cocilovo and Di Rienzo, 1984, 1985;Cocilovo and Guichon, 1985, 1986; Rothhammer andSilva, 1990; Guichon, 2002). In contrast, the works thatasserted the existence of two human stocks in SouthAmerica (or several in the case of early works) found dif-ferences principally in cranial length, height andbreadth, as well as robusticity (Imbelloni, 1937; Nevesand Pucciarelli, 1989; Lahr, 1995; Gonzalez-Jose et al.,2003, 2004). Such discrepancies could be related to themain causes of morphological variation in the differentosseous structures (Atchley and Hall, 1991; Hanken andHall, 1993).As noted above, slightly different results between

structures corresponding to frontal and lateral views,which could be linked to different evolutionary mecha-nisms, were also found in the present study. Regardingthis, a number of surveys have demonstrated that thehuman skull is subdivided into partially autonomousmodules that may correspond to functional and develop-ment subunits (Cheverud, 1996; Leamy et al., 1999; Gon-zalez-Jose et al., 2004b). Given the genetic architectureof a modular structure, this implies that pleiotropiceffects are concentrated within modules but are rela-tively weak among modules (Cheverud, 1996; Wagner,1996; Leamy et al., 1999; Klingenberg et al., 2004). As ithas been shown in previous works, the facial skeletonbears key information about evolutionary relationships,i.e. the apportionment of genetic variation among inter-breeding demes (Smith, 2006; Perez et al., 2007). Thetraits analyzed in lateral view are less consistent withthe evolutionary relationships established by means ofmolecular data probably because the analyzed traits,such as robusticity, might be related to environmentalfactors (Churchill, 1998; Bulbeck, 2001; Bernal et al.,

2006). The greater dolichocephaly in these populationsmay be partially due to the robusticity of the glabellaand nuchal crest, since these traits show high associa-tion with the relative length of the crania in the samplesfrom the studied area, particularly in male individuals.The results of Singular warps analysis show a correla-tion of 0.94 between the first axis representing therobusticity and the first axis representing the vault con-tour (Perez et al., 2006, unpublished results). The studyof the inner and outer mid-sagittal vault to evaluate thecontribution of bone thickness to cranial shape would beuseful to achieve a better understanding of the relation-ship between robusticity and dolichocephaly. In this way,the results obtained by Bookstein et al. (1999), based onthe comparison of interior and exterior frontal bone pro-files of archaic and modern Homo, indicate that bothaspects vary independently, with the inner frontal tablebeing very conservative whereas the outer table is highlyvariable and reflects brow-ridge structure.The craniofacial robusticity present in the populations

from the area has been recently discussed in terms ofthe influence of mechanical loading, phylogenetic and cli-matic factors (Lahr and Wright, 1996; Lalueza et al.,1997a; Bernal et al., 2005, 2006). Gonzalez et al. (unpub-lished results) demonstrate that the differences in thesetraits between Tierra del Fuego-southern Patagonianand other South American populations are present earlyin the ontogeny (around 5 years old), providing evidenceagainst phenotypic plasticity due to high mechanicalloading as the main cause of robusticity. Additional evi-dence in support of this affirmation is presented byBernal et al. (2005, 2006) through the quantification ofdental macrowear as a measurement of mechanical load-ing sustained by individuals and the comparison of sam-ples belonging to populations with diets based on hardand soft foods. The results indicate no associationbetween hardness of consumed food and degree of robus-ticity since some skulls of hunter–gatherers showed thesame development of robust features as farmers’ skulls(Bernal et al., 2006). Likewise, the dental wear observedin southern Patagonia samples is comparatively low inrelation to other South American samples (Bernal et al.,2005). Therefore, the difference in biomechanical load-ings sustained by the individuals does not seem to bethe main cause of variation in robusticity among thesepopulations. On the other hand, the comparison of cra-niofacial morphology of early-middle Holocene samplesfrom South America with late Holocene samples fromTierra del Fuego does not support the hypothesis thatrobusticity results from the retention of ancestral char-acters (Bernal et al., 2006). Whereas the later late Holo-cene samples from South Patagonia exhibit high levelsof craniofacial robusticity, the earlier samples from thisregion as well as those from other regions of SouthAmerica show lesser development of robust features(Bernal et al., 2006). In contrast, Bernal et al. (2006)found a significant association between latitude and cra-niofacial robusticity, with the most robust craniofacialmorphologies occurring at the highest latitudes (similarto the pattern found in this work). The hypothesis pro-posed is that the action of climatic factors may accountfor the features observed, since several authors haveproposed that skeletal robusticity in cold-adapted popu-lations can result from endocrine action (see discussionin Churchill, 1998). This is partially supported becausethe influence of climate on several physiological charac-teristics (e.g. increased basal metabolic rates partially



related to upregulation of thyroid hormones) is welldocumented (Leonard et al., 2002; Snodgrass et al.,2005) and because the systemic physiological controlover robusticity throughout the skeleton has been dem-onstrated by experimental studies. Such studies havedocumented the stimulating effect of hormones on cra-niofacial robusticity, cranial vault thickening, brow-ridgegrowth (Lieberman, 1996), development of major areasof muscle attachment (e.g. malar bone; Vogl et al., 1993),as well as muscle development (Riesenfeld, 1975; Voglet al., 1993). These changes could explain the highrobusticity and dolychocephaly in the southern Patago-nian and Tierra del Fuego samples, particularly becausethe dolychocephaly in these populations is related with amajor development of glabellar and occipital muscleattachment areas in male individuals (Figs. 6a and 7b).

CONCLUSION

The craniofacial singularity of the Tierra del Fuegoand southern Patagonia populations was establishedbased on their high robusticity and dolichocephaly withrespect to the rest of Amerindians. This pattern do notseem to be the result of multiple migratory events, inwhich the southernmost populations are seen as de-scendants of the first American settlers whereas theAmerindians would descend from a later Asian-descentmigration, because mtDNA data indicate that the samehaplogroups are shared by all South American popula-tions, including those from the extreme South of the con-tinent (Moraga et al., 2000; Garcia-Bour et al., 2004). Inaddition, the hypothesis of a Paleoamerican origin forthese populations is based on comparisons with samplesof human remains from South America dated to theearly-middle Holocene (e.g. Lagoa Santa ca. 9000–6000year 14C BP, Dillehay, 2000; Neves and Hubbe, 2005;Tequendama, ca. 7300–5800 year 14C BP, Correal Urregoand van der Hammen, 1977; Arroyo Seco 2 ca. 7800–6300 year 14C BP, Politis and Madrid, 2001; and BanoNuevo ca. 9000–8500 year 14C BP, Mena and Reyes,2001), which represent populations corresponding tomoments posterior to the diversification of the first set-tlers. On the other hand, our results show a clear geo-graphical ordination of the samples based on mtDNAhaplogroup frequency and facial morphology, groupingall Patagonia samples. This geographic pattern of facialand molecular diversity may reflect the effect of geneticdrift that occurred in the small founding populations iso-lated 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 resultssuggest that different evolutionary mechanisms, such asnatural selection, could have affected other traits, e.g.robusticity, since the pattern of variation obtained withthese data differ from those obtained from moleculardata, showing a clear differentiation of the southern Pat-agonian and Tierra del Fuego samples. This hypothesisrequires further analysis focused on the estimation ofthe rate of morphological change in populations underdiverse environmental conditions and different evolu-tionary processes. In particular, it is important to deter-mine whether genetic drift or natural selection couldaccount for the singular morphology of later late Holo-cene populations from Tierra del Fuego and southernPatagonia.

ACKNOWLEDGMENTS

We are sincerely grateful to Sergio Furtado dos Reisfor his discussions about origin and causes of morphologi-cal variation, which inspired the research presented inthis manuscript. We thank Hector M. Pucciarelli (Divi-sion Antropologıa, Facultad de Ciencias Naturales yMuseo, La Plata, Argentina), Ines Baffi and LeandroLuna (Museo Etnografico ‘‘J. B. Ambrosetti’’, BuenosAires, Argentina), Mateo Martinic (Instituto de la Pata-gonia Austral de la Universidad de Magallanes) forgranting access to the human skeletal collections undertheir care. We also thank to Cecilia Morgan and AmeliaBarreiro for help with the English version of the manu-script and Marina Perez for the drawings (Figs. 1 and 2).

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