Review

doi: 10.1111/j.1469-1809.2009.00537.x

The Late Pleistocene Colonization of South America: An Interdisciplinary Perspective

Francisco Rothhammer1,2 and Tom D. Dillehay3,4 1 Instituto de Alta Investigaci on, Universidad de Tarapac a, Arica Chile 2 Programa de Genetica Humana, Instituto de Ciencias Biom edicas, Facultad de Medicina, Universidad de Chile, Santiago, Chile 3 Department of Anthropology, Vanderbilt University, Nashville, TN, USA 4 Instituto de Ciencias Sociales, Universidad Austral de Chile, Chile

Summary
In this article, we briey review scenarios for the rst peopling of the New World, including the Clovis First/Single Origin, Tripartite, and Dual Migration models. We then discuss bioanthropological, molecular genetic, archaeological and biogeographic evidence for the peopling of the continent. To conclude, we draw on different lines of evidence to make inferences concerning the timing, direction, and type of early human dispersion in South America.
Keywords: Colonization of South America, multidisciplinary approach, provisional peopling model

Introduction
This essay considers the rst human colonization of South America from an interdisciplinary perspective, including bioanthropological, genetic, archaeological and biogeographical evidence. Our objectives are twofold. First, we briey review models that have been proposed for the peopling of the New World, with special reference to the southern hemisphere, including the Clovis First/Single Origin (Hrdli cka, 1937; Haynes, 2002), Tripartite (Greenberg et al., 1986), and Dual Migration (Neves & Hubbe, 2005) models. Second, we review some key results from bioanthropology, genetics, and archaeology and their implications particularly regarding the peopling of South America. Models based primarily on data from a single discipline and/or methodological approach are perhaps less likely to advance our understanding of initial human migrations. Our intention here is to build on previous integrated analyses (e.g., Neves et al., 2003; Dillehay, 2008; Fagundes et al., 2008; Goebel et al., 2008; Gonz alez-Jos e et al., 2008) and to provide a broad critique and a simplifying perspective.

The Clovis First/Single Origin Model

For decades the prevailing view among scholars interested in the peopling of the Americas has been that Paleoindians arrived in the New World via Beringia from northeast Asia during Clovis times around 11,500 years ago, and that they were the direct ancestors of present-day Amerinds (Dillehay, 1999; Dixon, 2001; Adovasio & Page, 2002; Haynes, 2002; Meltzer, 2004; Goebel et al., 2008). This perspective of the rst peopling of the Americas is termed the Clovis First/Single Origin hypothesis, which was rst proposed by Ales Hrdli cka (1937), a major participant in the typology and race debates in biological anthropology during the early part of the 20th century (Blakey, 1987). After the discovery of Folsom Man in the 1920s, Hrdlicka vigorously refuted all claims for any human presence more than 4000 years old in the New World. However, the discovery of the Clovis site in 1932 turned him into one of the leading advocates in revising the perception of the rst humans entering the New World and he conceded that they may have arrived in late Pleistocene times. When Clovis projectile points later appeared at numerous sites in North America, often associated with the bone remains of extinct mammals such as mammoth (dated by radiocarbon means to ca. 11,000 years ago) the idea of Clovis Paleoindians having been the rst Americans was born. The Clovis First/Single Origin model was later modied to t the newly devised chronological and cultural schemes for the initial peopling of the Americas (e.g., Haynes, 2002). More recently, archaeological evidence from various sites scattered throughout the
C 2009 The Authors 2009 Blackwell Publishing Ltd/University College London

Corresponding author: Prof. Francisco Rothhammer, Instituto de Alta Investigacion, Universidad de Tarapaca, Arica 1001236, Chile. Tel: 56-058-230334; Fax: 56-058-255371; E-mail: frothham@ med.uchile.cl
Annals of Human Genetics (2009) 73,540549

540

Journal compilation

Late Pleistocene Colonization of South America

Americas and dating from before Clovis times (e.g., Dillehay, 1997; McAvoy & McAvoy, 1997; Adovasio et al., 1999; cf. Goebel et al., 2008), has overturned the ClovisFirst paradigm, establishing that the rst humans arrived in North and South America in pre-Clovis times (c.f., Bryan, 1986; Dillehay, 1997, 2000; Adovasio & Page, 2002; Stanford & Bradley, 2002; Meltzer, 2004, 2006; Goebel et al., 2008). Shortly after the discovery of the Clovis site, the question arose as to how early hunters had reached the mid-latitudes of North America during the Wisconsin Glaciation (between 25,000 and 10,000 years B.P.), at a time when the northern half of the continent was thought to be buried beneath two extensive ice sheets called Laurentide and Cordilleran. In 1933, W.A. Johnston proposed the existence of an ancient passage between the two glaciers, later termed the icefree corridor by Antevs, which stretched from the Yucon to northern Montana (Jackson et al., 1997). New geological and archaeological information has doubted the existence of this corridor (Jackson et al., 1997; Mandryk et al., 2001; Clague et al., 2004), however, leading researchers to consider other routes of entry from Beringia. Several investigators (Fladmark, 1979, 1983; Dixon, 1993; Gruhn, 1994; Erlandson, 2002) have suggested that the earliest human migration to the Americas may have occurred along the north-west coast through the use of watercraft to navigate the oceanic edges of the continent. Coastal stretches may have been deglaciated by about 16,000 B.P. (Mann & Peteet, 1994; Mandryk et al., 2001). The coastal entry hypothesis has recently gained increased support particularly as a consequence of (1) geological research in Alaska and the Yukon (e.g., Jackson et al., 1997; Mandryk et al., 2001), which has established new chronologies for major climatic events in the region and further questioned the existence of the corridor model, (2) the more general acceptance of a pre-Clovis culture, and (3) the discovery of several early coastal sites along the north-west coast of North America and the Pacic coast of South America (Keefer et al., 1998; Sandweiss et al., 1998; Dixon, 2006: Dillehay et al., 2008).

tic, bioanthropological and genetic grounds (Morell, 1990; Neves & Pucciarelli, 1991; Szathm ary, 1993a,b; Lahr, 1995; Merriwether et al., 1995) and never had a widespread and lasting impact on the way researchers considered the peopling of South America.

The Dual Migration Hypothesis

During the 1990s, North American patterns of cranial variability were examined and found to exhibit heterogeneous morphological trends, supporting the view that different populations entered the New World at various time intervals. Furthermore, although the closest morphological afnities were with Asian populations, the data could not be used to specify the time of entry or the number of founding populations (Steele & Powell, 1992; Jantz & Owsley, 2001). Recently, a group of South American researchers (Neves & Pucciarelli, 1990, 1991; Neves et al., 2003; Neves & Hubbe, 2005) have suggested, on the basis of a comparison of skulls from Lagoa Santa, Brazil, with late prehistoric and modern Amerindian crania, that craniometric variation in the New World reveals two different, discrete patterns, termed Paleoamerican and Amerindian. Whereas Paleoamericans tend to morphologically resemble present-day Australians, Melanesians, and Sub-Saharan Africans, late prehistoric and modern Amerinds show a greater resemblance to northern Asians. The proponents of this hypothesis claimed that two successive migrations, stemming from different geographical and chronological sources, were responsible for the observed patterns of variation. According to this model, similarities among Australians, Late Pleistocene Asians (e.g., the Zhoukoudien Upper Cave, Minatogawa and Liujiang skulls) and Paleoamericans can be explained by descent from South-eastern Asia (Neves et al., 2003). Paleoamericans are believed to have arrived following a terrestrial route by 15,000 B.P., whereas Amerindians came about 4000 years later along a similar route (Hubbe et al., 2003; Pucciarelli, 2004). Since the Lagoa Santa skulls have gained a protagonist position in South American physical anthropology, it is useful to review their history in more detail. The crania were initially collected by the Danish explorer Peter Lund in the caves of Lagoa Santa, Brazil, between 1835 and 1844. Lund, based on the Paleolithic chronology of Europe, assigned a great antiquity to the skulls; this was later challenged by McCown (1963) and others. Subsequently, inspired by the putative antiquity of the long and narrow headed Lagoa Santa crania, the French anthropologist Paul Rivet published the morphometrical analysis of 17 skulls of the same type selected from a series of 78 undeformed specimens of indeterminate age collected from several rock shelters in Paltacalo, southern Ecuador (McCown, 1963). Shortly thereafter, Rivet published a revision of the racial position of a series of modern
Annals of Human Genetics (2009) 73,540549

The Tripartite Model

In the 1980s, Greenberg et al. (1986) and Turner (1987) employed linguistic, dental, and genetic data to suggest that the Americas were peopled by three different migrations: (1) the early Amerindians who rst reached the interior of Alaska and the Yukon and then spread to some territories of Canada and eventually to the rest of the New World; (2) subsequently, the north-west Pacic coast was colonized by Na-Dene speakers; and (3) lastly, the Arctic was occupied by Eskimos. Although this hypothesis received considerable attention in attempting to explain the peopling of the Americas from an interdisciplinary perspective, it was later strongly challenged on linguis-

C 2009 The Authors Journal compilation C 2009 Blackwell Publishing Ltd/University College London

541

F. Rothhammer and T. D. Dillehay

Peric u skulls from the Baja California Peninsula (Rivet, 1909). The Baja skulls were suggested to belong, together with the Paltacalo skulls, to different branches of a Lagoa Santa race, and to resemble Australian and Melanesian crania. (We note, parenthetically, that the same modern Peric u skulls were recently used as evidence for the existence of a Paleoamerican pocket in the lower part of Baja California, which apparently survived in the area due to hypothetical climatic changes and geographic isolation during the middle Holocene (Gonz alezJos e et al., 2003).) The Paltacalo skulls eventually acquired a fuzzy aura of antiquity among scholars and became, along with the Lagoa Santa crania, the homotypes of the long and narrow-headed ancient Lagoa Santa or Paleoamerican race (c.f., McCown, 1963). McCown described in detail further developments of what he called a curious intellectual edice, and concluded that the initial demonstration of Rivets race of Lagoa Santa is based upon material that a properly trained modern anthropologist cannot but regard as utterly inadequate (McCown, 1963). In order to cope with the problems derived from the disputed antiquity of the Lagoa Santa skulls, for which only two radiocarbon dates have been reported (9720 128 and 9028 120 B.P. non-calibrated; Neves & Hubbe, 2005), Neves generated a more reliable chronological framework of the skulls in the 1990s. Two skulls of the studied samples now date back to ca. 11,000 B.P., namely the Conns skull from Lapa Mortu aria (cave) (Walter et al., 1937) and Luzia from Lapa Vermelha IV (Prous & Fogac a, 1999). Both skulls were reported to have been dated on charcoal, associated either stratigraphically or directly with the burials (Neves & Hubbe, 2005). Since the rst studies were based on a very small sample of crania, additional efforts to increase sample size were subsequently made, assembling a collection of 81 specimens from Central Brazil. The vast majority of the skulls (n = 74) were found to date between 8000 and 8500 years B.P. (Neves & Hubbe, 2005). An exploratory statistical comparison with Howells database (Howells, 1996) established that the Lagoa Santa skulls resemble present-day Australian/ Melanesian and Africans conrming the results reported at the beginning of the last century by Rivet for his Lagoa Santa race. Rivet (1943) interpreted this similarity as proof of an ancient migration to America across the Pacic Ocean, whereas the proponents of the dual migrational hypothesis have postulated a terrestrial route from Africa to America via Asia (Neves & Hubbe, 2005). In order to be phylogenetically informative, cranial variation should be selectively neutral and not strongly affected by stochastic microevolutionary forces (drift). A number of recent studies indicate that in modern human populations skull size and shape are not predominantly the result of selection, but mainly result from the interaction between gene ow and drift and, to a lesser extent, mutation (Relethford, 2002; Ackermann & Cheverud, 2004; Gonz alez-Jos e et al., 2008).
542
Annals of Human Genetics (2009) 73,540549

Operating under the assumptions of a migration/founder model, Powell & Neves (1999) examined a series of Paleoindian and Archaic crania from North and South America and compared these data to a large world-wide sample of late Holocene remains to assess within- and among-group variation and to determine how the observed pattern could be interpreted in terms of population history and structure. Powell & Neves (1999) suggested that their cranial data were consistent with the rst Americans having been derived from an undifferentiated Asian population that was not ancestral to modern American Indians. No doubt, this result can be accommodated to support multiple migration scenarios. Nevertheless, according to the same authors, the assumptions underlying the model were not very realistic and when the data were analyzed controlling for the effects of drift, the rst Americans were no longer differentiated from modern Amerindians.

Classical Genetic Data

Turning to information provided by synthetic genegeography graphs based on blood group and protein data, we note that maps of South America based on a small number of polymorphic loci are, as expected, not very informative (ORourke & Suarez, 1985). Increasing the number of loci results in maps where the rst principal component (roughly 50% of gene frequency variation) reveals clines extending from north-western to south-eastern South America that can be interpreted as indicative of very early population displacements from the Isthmus of Panama to the Brazilian coast and down to the southern cone of the continent (Rothhammer & Silva, 1992; Rothhammer et al., 1997). Maps based on the second and third principal component exhibit clines which are more difcult to interpret, but which may indicate population movements during the Late Archaic/Early Formative along available waterways in search of new alluvial land in the Amazon ood plain, as claimed by Lathrap (1970). CavalliSforza et al. (1994), suggested an early southward migration along the western side of the Andes, consistent with the interpretation that modern speakers of Andean languages may represent descendants of the rst occupiers of the region. Lastly, an analysis of 31 protein systems obtained in 29 Amazonian populations agreed with a previously observed differentiation between northern and southern Brazil, suggesting that the Amazon river could have constituted a barrier to north-south gene ow or that genetically differentiated groups may have entered the region from the west (Callegari-Jacques et al., 1994)

Molecular Genetic Evidence

Mitochondrial and Y-chromosome variation in North and South America indicate unambiguously that all Native
C C 2009 The Authors 2009 Blackwell Publishing Ltd/University College London

Journal compilation

Late Pleistocene Colonization of South America

Americans came from Asia and not from Melanesia, Australia, Africa, or Europe (Karafet et al., 2006; Merriwether, 2006; Wang et al., 2007). Five mtDNA (A; B; C; D and X) and two Y-chromosome (C and Q) founding haplogroups, which are all present among native populations of Siberia account for the molecular variability observed among extant Native American populations (Derenko et al., 2001; Zegura et al., 2004; Starikovskaya et al., 2005). The complete sequencing of 84 mtDNAs have lled gaps in the internal sequence variation of A,C and D, contributing to improve the resolution of the mtDNA phylogeny in Siberia-Beringia (Volodko et al., 2008) Haplogroup X includes many lineages, some of which are present in Europe and Asia. Nevertheless, the lineage found in American Indians is different from those observed in Eurasia (Merriwether, 2006). Ancient mtDNA analysis has until now yielded the same founding haplogroups described in extant populations, thus conrming the genetic continuity between extinct and extant Native American populations (Stone & Stoneking, 1998; Kemp et al., 2007). Consequently, many migration models based on the presence or absence of certain haplogroups have lost much explanatory usefulness (c.f., Goebel et al., 2008). In an extensive study on patterns of genetic variation in Native Americans from both North and South America, Wang et al. (2007) reported the results of the analysis of 678 microsatellite markers genotyped in 422 individuals representing 24 Native American populations. The analysis of the data revealed a progressive reduction of variability starting from Africa through Asia and down from the Bering Strait to North and South America, consistent with a serial founding Africanorigin model of human evolution (Prugnolle et al., 2005; Ramachandran et al., 2005). Noteworthy was the observation in South America of a west-to-east difference in genetic diversity, showing that eastern (Brazilian) populations had the lowest levels of heterozygosity. This pattern was also observed with mitochondrial DNA (Fuselli et al., 2003; Lewis et al., 2004) and Y-chromosome markers (Tarazona-Santos et al., 2001). The fact that Brazil exhibits the lowest levels of variation suggests an initial colonization of western South America and a subsequent peopling of the eastern part by western subgroups, conrming the interpretation of the results of a previous genetic analysis of Amazonian tribes (Callegari-Jacques et al., 1994). Colonization routes also were examined by Wang et al. (2007), by evaluating the relationship between heterozygosity and effective geographic distances. When coastlines were treated as preferred routes, there was an increase in negative correlation between heterozygosity and distance from the Bering Strait. A relative genetic similarity between Andean and Mesoamerican populations was also observed by Wang et al. (2007) and was interpreted as consistent with an early coastal colonization. An alternative interpretation is that the two most developed pre-Columbian cultures in

the Americas ourished precisely in Mexico and Peru, and that the observed genetic afnities could be the result of late pre-Hispanic (or even early Hispanic) contact between them. We note in passing, that anecdotal information reported by the Spanish chroniclers suggests that in Peru, under the rule of Tupac Inca Yupanqui, long transpacic voyages along the Pacic coast and out to sea were organized using large balsas (rafts) (Rivet, 1943; Cabello-Valboa, 1951; Pietschmann, 1906).

Archaeological Data and Biogeography of South America

The late Pleistocene archaeological record of South America differs from that of North America in many ways (Bryan, 1973, 1986; Dillehay, 1999; Miotti et al., 2003; Borrero, 2006). Among these, there is an absence in South America of a continent-wide stone tool style like Clovis and of evidence for the long-distance movement of raw lithic material. The presence of sharply contrasting environments in the southern hemisphere favoured the establishment of distinct regional cultural traditions at the outset of human dispersion. Furthermore, the extensive ice sheets covering high latitudes limited the movement of colonizers in North America in contrast with South America where the glacial effect was conned to patchy high altitude and latitude areas (Clapperton, 1993). The archaeological evidence of human entry into South America before 15,000 B.P. is weak and only presumed at this time. However, given the evidence conrming the presence of humans probably centuries before 12,500 B.P., the likely entry date should lie between 15,000 and 13,500 B.P. Between at least 11,000 and 10,000 B.P. South America witnessed several major changes, including the increased use of coastal resources, demographic concentration in major river basins, and modication of landscapes and plant and animal distributions. Some 1000 years later an increase of site density, technological diversication, plant domestication, and appearance of ritual practices indicate that the initial impulses toward cultural complexity had developed in South America, probably within only a few millennia after the initial arrival of colonizers (Dillehay, 2000; Lavallee, 2000). No doubt, sharp contrasting environments characterized the continent during the late Pleistocene and Pleistocene to Holocene transition and contributed to cultural developments that show a steady shift away from sub-continental uniformity and toward the establishment of distinct regional, cultural, and especially technological traditions (Bryan, 1973, 1986; Prieto, 1996; Dillehay, 1999; Borrero, 2006). The impact of climatic and environmental changes on these developments is not well understood. There is evidence of a signicant temperature rise between 15,000 and 14,000 B.P. and a subsequent warmAnnals of Human Genetics (2009) 73,540549

C 2009 The Authors Journal compilation C 2009 Blackwell Publishing Ltd/University College London

543

F. Rothhammer and T. D. Dillehay

ing trend lasting until 10,500 B.P. (Rull, 1996; Prieto, 1996; Latrubesse & Rambonell, 1994; Weng et al., 2004; Bush & John, 2006). South America is biogeographically divisible into four major areas: the Andes, the tropical and temperate plains of Colombia, Venezuela, and Brazil, the highlands of east Brazil and the Guyanas, and the southern Pampa and Patagonian grasslands. These divisions are important for considering hypothetical migration routes into the southern hemisphere (c.f., Bennett & Bird, 1964). The Andean mountain chain, the vast Amazonian basin, and the southern grasslands were doubtless a combined barrier for isolating some human populations geographically and genetically, regularly disrupting gene ow between geographically contiguous populations, and producing some of the regional skeletal and genetic differences discussed earlier. Although foraging mobility undoubtedly continued throughout the terminal Pleistocene to early Holocene periods, reduced mobility in some regions probably derived from the increasing use of local resources constitutes one potential explanation for the bioanthropological heterogeneity observed across the continent. Both genetic and morphological signals of marked diversity between the Andes and the eastern lowlands of the continent, generally agree with differences observed in the technological and subsistence patterns in these two regions. Continental ice sheets started to melt and the sea levels began to rise between 14,000 and 13,000 B.P. The Pacic and Atlantic shelves and many areas in Tierra del Fuego were ooded, as were any archaeological sites, making the study of early migration routes along the coasts very difcult. These and other late Pleistocene environmental changes introduced signicant resource-related changes that likely favoured social learning and bonding and technological change, as evidenced by a wide array of local and regional stone tool technologies and subsistence patterns in place by at least 10,500 years ago (Kipnis, 1998; Dillehay, 2000; Salemme & Miotti, 2002; Flegenheimer et al., 2006; Le on-Canales, 2007). The broad network of environmental responses by people across the continent clearly included more than the development of social bonding and strategies for sharing resources. There is so much diversity across the continent at this time and later that it is difcult to say to what degree the eastern lowlands were culturally different from the Andean region or the southern grasslands were from the Amazon basin or northern tropical forests. Regional technological diversity suggests that there were specic responses by different groups to the great variations in local habitats and raw material availability that existed across the continent, especially in the Andean region. Technology offered a exible, rapid means of responding to climate and other changes at a range of scales from daily needs of individuals to long-term trends experienced over generations.
544

Several sub-continental studies have emphasized the instability of climates during terminal glacial, deglaciation, and the transition to the early Holocene from ca. 13,000 to 10,000 years ago (Bennett et al., 2000; Bush & John, 2006; Lovell & Kelly, 2008). For humans, these cyclical periods of climatic stability and instability would have placed additional selective pressures on integrated biological and behavioural responses to increased resource variability. At the continental scale, populations distributed across Amazonia or along the Pacic coastal shelf during warm deglaciation, possibly would have become geographically isolated during times of augmented aridity. Increased precipitation and vegetation growth in some areas after 11,000 B.P. may have pushed some populations outward towards the better vegetated and watered areas, such as the Amazonian rainforest and the mid-latitudes and western altitudes of the continent. Such repeated cycles and disruptions of landscapes were doubtless a force for isolating populations geographically, biologically, and consequently genetically, regularly disrupting gene ow even between contiguous populations and more so between those on the east and west sides of the continent. At sub-continental scales, expansions and contractions of environments during the terminal Pleistocene and early Holocene period (ca. 12,000 10,000 B.P.) would have drawn in or pushed out human populations from north to south, or vice versa, as well as eastwards into the Amazon basin during times of expansion or retreat from aridity, for example. The disruption of contact between regional populations combined with occasional severe downturns, causing local animal and possibly human extinctions, also would have contributed to the development of regional differences in skeletal morphology, gene pools, and social and technological behaviours. Although social processes must also be taken into consideration to explain these differences in the morphological, genetic, and archaeological records, for which there is currently no hard evidence, the periodicity and extremes of late Pleistocene climatic cycles must have underlain a process of accretionary or mosaic emergence of human and cultural variation within South America. Considering the various sources of evidence discussed above one can outline a possible scheme of human dispersion in South America. Hunters and gatherers who migrated to South America via the Isthmus of Panama could have entered the Andean highlands by way of the Cauca and Magdalena river valleys which ow from south to north in Colombia. Once adjusted to the highland environment there would have been few barriers for moving further south, although some high altitude areas were covered by glaciers. Some groups may also have migrated eastward following the Caribbean rim of Venezuela, the Guyanas, and north-east Brazil and others into the interior of Venezuela and afterwards south-east or southwest along several large river systems into the Amazon basin. People may also have migrated along the Pacic coast down to

Annals of Human Genetics (2009) 73,540549 Journal compilation

C

C 2009 The Authors 2009 Blackwell Publishing Ltd/University College London

Late Pleistocene Colonization of South America

Chile, following favourable shing localities and using watercraft (Rothhammer & Silva, 1992; Cavalli-Sforza et al., 1994; Keefer et al., 1998; Sandweiss et al., 1998; Stothert, 1998; Wiesner, 1999; Wang et al., 2007). From the Amazon basin and/or the Andes of north-west Argentina, people could have entered the open parkland country of eastern Brazil and also could have spread throughout the Pampas and Patagonia. As mentioned above, genetic data from Native Brazilian populations suggests that the Amazon River constituted a barrier to north-south gene ow. There is also the possibility that genetically divergent groups may have entered the region from Colombia, Venezuela, and the Guyanas in the north and from Argentina in the south (Fig. 1).

There is evidence in parts of north-western and central South America that several plant species were deliberately manipulated and possibly domesticated in terminal Pleistocene times (Piperno & Pearsall, 1998; Piperno & Stothert, 2003). What is not understood is whether there are any connections between broad-spectrum diets in environments where potentially domesticable plants occurred, specic resource zones, and social changes that might have favoured the rst impulses toward food production. Similar connections need to be ascertained for the kinds of human and camelid interactions that took place during this period in the puna and altiplano zones of the central and south-central Andes. Diets, resource zones, and local human population histories constitute only

Figure 1 Hypothesized migration routes into and throughout South America, as well as some of the major regional archaeological sites dating to the late Pleistocene period.
C 2009 The Authors Journal compilation C 2009 Blackwell Publishing Ltd/University College London

Annals of Human Genetics (2009) 73,540549

545

F. Rothhammer and T. D. Dillehay

some of the variables required to understand the development of early cultural diversity, food production within a relatively short period of time after humans arrived, in comparison to the Old World, and how ecological constraints and opportunities played out in setting the stage for subsequent sedentary and later more complex societies in South America.

Acknowledgements
We thank the Editor and anonymous reviewers for helpful advice. We also acknowledge gratefully the collaboration of Will Wilcox in the elaboration of the image showing location of archaeological sites and possible migration routes. Financial support was provided by Fondecyt 1095006 and Convenio de Desempe no UTA/Mecesup-2 grants.

Conclusion
South America was probably colonized between at least 15,000 and 13,500 B.P. most likely by one migration wave. Archaeologists have noted that the peopling of the southern hemisphere differed in many ways from that of North America. Most signicant has been the observation that no single culture dominated the South American continent the way Clovis did. Several factors likely account for this early diversity including geographic barriers to human movement (Andean Highlands and Amazon River), climatic changes, shifts in resource areas, new settlement patterns, new lifestyles, innovative technologies (e.g. domestication of plants), and new social organizations, among others. In addition, the relative isolation derived from an absence of later migrants, as seems to have occurred for North America, may have contributed to early biological diversication and cultural complexity of South America. The west and east sides of South America have different archaeological records, different chronologies and different human histories. No doubt, these factors are reected in distinctive patterns of genetic, morphological and cultural variation. Although South America still does not have sufcient interdisciplinary data from archaeology, genetics, bioanthropology and biogeography to precisely model the timing and processes involved in the rst peopling of the continent, a tentative scheme of dispersal of rst colonizers can be outlined (Fig. 1). The conclusion which may be drawn from this review of various interdisciplinary approaches to understand the initial peopling of South America is a positive one, with continued new insights being made in analytical techniques, yielding more reliable results over a greater temporal and spacial framework. Whereas any one approach may produce new and different data and insights, as well as misleading results, and various degrees of variation are likely among the ndings they provide, new data and techniques should continue to reveal patterns not only specic to South America, but others that relate to hemisphere-wide processes of migration and colonization. In fact, theoretical generalizations of studies of the rst Americans have been scanty and their contribution to global issues discrete. In this context, we wish to emphasize the uniqueness of the colonization of South America as a model to contribute to the understanding of the more general process of adaptive radiation of populations anywhere.
546
Annals of Human Genetics (2009) 73,540549 Journal compilation
C

References
Ackermann, R. R. & Cheverud, J. M. (2004) Detecting genetic drift versus selection in human evolution. Proc Natl Acad Sci USA 101, 1794617951. Adovasio, J. M., Pedler, D., Doanhue, J. & Stuckenrath, R. (1999) No Vestige of a Beginning nor Prospect for an End: Two Decades of Debate on Meadowcroft Shelter. In: Ice Age Peoples of North America (eds. R. Bonnichsen and K. Turmire), pp. 416431. Oregon State University Press. Adovasio, J. & Page, J. (2002) The First Americans: In Pursuit of Archaeologys Greatest Mystery. New York: Random House. Bennett, W. C. & Bird, J. (1964) Andean Culture History. Garden City, New York: The Natural History Press. Bennett, K. D., Haberle, S. G. & Lumley, S. H (2000). The Last Glacial-Holocene Transition in Southern Chile. Science 290, 325 328. Blakey, M. L. (1987) Intrinsic social and political biology in the history of American Physical Anthropology. Critique of Anthropology 7, 735. Borrero, L. (2006) Paleoindians without Mammoths and Archaeologists without Projectile Points? The Archaeology of the First Inhabitants of the Americas. In: Paleoindian Archaeology: A Hemispheric Perspective (eds. J. E. Morrow & C. Gnecco), pp. 920. University Press of Florida. Bryan, A. (1973) Paleoenvironments and cultural diversity in Late Pleistocene South America. Q Res. 3, 237256. Bryan, A. (1986) Paleoamerican prehistory as seen from South America. In: New Evidence for the Pleistocene Peopling of the New World (ed. A. Bryan), pp. 114. Orono, ME: Center for the Study of Early Man. Bush, M. B. & John R. F. (2006) Tropical Rainforest Responses to Climatic Change (eds. M. B. Bush & R. F. John). Berlin: Springer. Cabello-Valboa, M. (1951) Miscel anea ant artica. Una historia del antiguo Per u, pp. 322324. Lima. Callegari-Jacques, S. M., Salzano, F. M., Weimer, T. A., Hutz, M. H., Black, F. L., Santos, S. E., Guerreiro, J. F., Mestriner, M. A. & Pandey, J. P. (1994) Further blood genetic studies on Amazonian diversity-data from four Indian groups. Ann Hum Biol 21, 465481. Cavalli-Sforza, L. L., Menozzi, P. & Piazza, A. (1994) The history and geography of human genes. Priceton: Princeton University Press. Clague, J. J., Mathewes, R. W. & Ager, T. A. (2004) In: Entering America: Northeast Asia and Beringia before the Last Glacial Maximum (ed. D. B. Madsen), pp. 6394. Salt Lake City: University of Utah Press. Clapperton, C. M. (1993) Quaternary Geology and Geomorphology of South America. Amsterdam: Elvesier. Derenko, M. V., Grzybowski, T., Malyarchuk, B. A., Czarny, J., Mi scicka-Sliwka, D. & Zakharov, I. A. (2001) The Presence of Mitochondrial Haplogroup X in Altaians from South Liberia. Am J Hum Genet 69, 237241.
C 2009 The Authors 2009 Blackwell Publishing Ltd/University College London

Late Pleistocene Colonization of South America

Dillehay, T. D. (1997) Monte Verde. A Late Pleistocene Settlement in Chile. Vol. 2. The Archaeological Context and Interpretation, p. 1071. Washington, DC, London: Smithsonian Institution Press. Dillehay, T. D. (1999) The late Pleistocene Cultures of South America. Evol Anthropol 7, 206216. Dillehay, T. D. (2000) The Settlement of the Americas. New York: Basic Books. Dillehay, T. D. (2008) Probing Deeper into rst American studies. Proc Natl Acad Sci USA 106, 971978. Dillehay, T. D., Ramirez, C., Pino, M., Collins, M., Rossen, J. & Pino-Navarro, D. (2008) Monte Verde: Seaweeds, food, and medicine and the peopling of the Americas. Science 325, 1287 89. Dixon, E. J. (1993) Quest for the Origins of the First Americans. Albuquerque: University of New Mexico Press. Dixon, E. J. (2001) Human colonization of the Americas: Timing, technology and process. Quatenary Sci Rev 20, 277299. Dixon, E. J. (2006) Peopling of the Americas. How and when did people rst come to North America? Athena Review 3, 2. Erlandson, J. (2002). Anatomically modern humans, maritime voyaging, and the Pleistocene colonization of the Americas. In: The First Americans, the Pleistocene Colonization of the New World (ed. N. G. Jablonski), No. 27, pp. 5992. Memoirs of the California Academy of Sciences. Fagundes, N. J., Kanitz, R., Eckert, R., Valls, A. C., Bogo, M. R., Salzano, F. M., Smith, D. G., Silva, W. A., Jr., Zago, M. A., Ribeiro-dos-Santos, A. K., Santos, S. E., Petzl-Erler, M. L. & Bonatto, S. L. (2008) Mitochondrial population genomics supports a single pre-Clovis origin with a coastal route for the peopling of the Americas. Am J Hum Genet 82, 58392. Fladmark, K. R. (1979) Routes: Alternative Migration Corridors for Early Man in North America. American Antiquity 44, 5569. Fladmark, K. R. (1983) Times and Places: Environmental Correlates of Mid-to-Late Wisconsin Human Population Expansion in North America. In: Early Man in the New World (ed. R. Shutler), pp. 1342. Beverly Hills: Sage Publication. Flegenheimer, N., Bayon, C. & Pupio A. (2006) Llegar a un Nuevo Mundo: La Arqueolog a de los Primeros Pobladores del Actual Territorio Argentino. Museo y Archivo Hist orico Municipal, Bahia Blanca. Fuselli, S., Tarrazona-Santos, E., Dupenloup I., Soto, A. & Luiselli, D. (2003) Mitocondrial DNA diversity in South America and the genetic history of Andean highlanders. Mol Biol Evol 20, 1682 1691. Goebel, T., Waters, M. & ORourke, R. (2008) The late pleistocene dispersal of modern humans in the Americas. Science 319, 1497 1502. Gonz alez-Jos e, R., Gonz alez-Mart n, A., Hern andez, M., Pucciarelli, H. M., Sardi, M., Rosales, A. & Van Der Molen, S. (2003) Craniometric evidence for Palaeoamerican survival in Baja California. Nature 425, 6265. Gonz alez-Jos e, R., Bortolini, M. C., Santos, F. R. & Bonatto, S. L. (2008) The peopling of America: craniofacial shape variation on a continental scale and its interpretation from an interdisciplinary view. Am J Phys Anthropol 137, 175187. Greenberg, J. H., Turner, C. G. & Zegura, S. L. (1986) The settlement of the Americas: a comparison of the linguistic, dental and genetic evidence. Curr Anthropol 27, 477495. Gruhn, R. (1994) The Pacic Coast Route of Initial Entry: An Overview. In: Method and Theory for Investigating the Peopling of the Americas (eds. R. Bonnichsen & D. G. Steele). Corvallis, OR, USA: Center for the Study of the First Americans, Oregon State University.

Haynes, G. A. (2002) The early settlement of North America: The Clovis Era. Cambridge: Cambridge University Press. Howells, W. W. (1996) Howells craniometric data on the Internet. Am J Phys Anthropol 101, 441442. Hrdli cka, A. (1937) The origin and antiquity of the American Indian. Annu Rep Smithson Inst Washington 1923, 481494. Hubbe, M., Mazzuia, E. T. A., Atui, J. P. V. & Neves, W. A. (2003) A primeira descoberta de America. Sao Paulo: Sociedade Brasileira de Gen etica. Jackson, L. E., Jr., Phillips, F. M., Shimamura, K. & Little, E. C. (1997) Cosmogenic 36Cl dating of the Foothills erratics train, Alberta, Canada. Geology 25, 195198. Jantz, R. L. & Owsley, D. W. (2001) Variation among early North American crania. Am J Phys Anthropol 114, 146155. Karafet, T. M., Zegura, S. L. & Hammer, M. F. (2006) In: Handbook of North American Indians Vol. 3: Environment, Origins and Populations (eds. D. Ubelaker, W. C. Sturtevant & D. Stanford), pp. 831839. Washington, DC: Smithonian Institution Press. Keefer, D. K., deFrance, S. D., Moseley, M. E., Richardson, J. B., III, Satterlee, D. R. & Day-Lewis, A. (1998) Early maritime Economy and El Ni no events at Quebrada Tacaguay, Per u. Science 281, 18301832. Kemp, B. M., Malhi, R. S., McDonough, J., Bolnick, D. A., Eshleman, J. A., Rickards, O., Martinez-Labarga, C., Johnson, J. R., Lorenz, J. G., Dixon, E. J., Field, T. E., Heaton, T. H., Worl, R. & Smith, D. G. (2007) Genetic analysis of early holocene skeletal remains from Alaska and its implications for the settlement of the Americas. Am J Phys Anthropol 132, 605621. Kipnis, R. (1998) Early hunter-gatherers in Americas: Perpsectives from central Brazil. Antiquity 72, 581592. Lahr, M. M. (1995). Patterns of modern human diversication: implications for Amerindian origins. Am J Phys Anthropol 38, 163 198. Lathrap, D. W. (1970) The Upper Amazon. Southampton: Thames and Hudson. Latrubesse, E. M. & Rambonell, C. (1994) A climatic model for southwestern Amazonia in late glacial times. Quaternary Int 21, 163169. Lavallee, D. (2000) The First South Americans. Salt Lake City: University of Utah Press. Le on-Canales, E. (2007) Or genes Humanos en los Andes del Per u. Lima: Universidad San Martin de Porres. Lewis, C. M., Tito, R. Y., Lizarraga, B. & Stone, A. C. (2004) Land, language and loci : mt DNA in Native Americans and the genetic history of Peru. Am J Phys Anthropol 127, 351360. Lovell, T. V. & Kelly, M. A. (2008) Was the yonger dryas global? Science 321, 348349. Mandryk, C. A. S., Josenhans, H., Fedje, D. W. & Mathewes, R. W. (2001) Late Quaternary paleoenvironments of Northwestern North America: implications for inland versus coastal migration routes. Quaternary Sci Rev 20, 301314. Mann, D. H. & Peteet, D. M. (1994) Extent and timing of the last glacial maximum in southwestern Alaska. Quaternary Res 42, 136148. McAvoy, J. M. & McAvoy, L. D. (1997) Archaeological Investigations of Site 44SX202, Cactus Hill, Sussex County, Virginia. Virginia Department of Historic Resources, Research Report 8, Richmond, VA. McCown, T. D. (1963) Handbook of South American Indians, Vol. 6, pp. 19. New York: Cooper Square Publishers. Meltzer, D. J. (2004) Peopling of North America. In: The Quaternary period in the United States (eds. A. Gillespie, S. C. Porter & B. Atwater), pp. 53963. New York: Elsevier Science.
Annals of Human Genetics (2009) 73,540549

C 2009 The Authors Journal compilation C 2009 Blackwell Publishing Ltd/University College London

547

F. Rothhammer and T. D. Dillehay

Meltzer, D. J. (2006) Paleoamerican origins: Beyond clovis. J Field Archaeology 31, 441443. Merriwether, D., Rothhammer, F. & Ferrell, R. (1995). Distribution of the four founding lineage haplotypes in native americans suggests a single wave of migration for the new world. Amer J Phys Anthropol 98, 411430. Merriwether, D. (2006) In: Handbook of North American Indians Vol. 3: Environment, Origins and Populations (eds. D. Ubelaker, W. C. Sturtevant & D. Stanford), pp. 817830. Washington, DC: Smithonian Institution Press. Miotti, L. L., Salemme, M. & Flegenheimer, N. (2003). Where the South Winds Blow: Ancient Evidence of Paleo-South Americans. College Station, USA: Texas A&M University Press. Morell, V. (1990) Confusion in earliest America. Science 248, 439 441. Neves, W. A. & Hubbe, M. (2005) Cranial morphology of early Americans from Lagoa Santa, Brazil: implications for the settlement of the New World. Proc Natl Acad Sci 102(51), 1830918314. Neves, W. A., Prous, A., Gonzalez-Jose, R., Kipnis, R. & Powell, J. (2003) Early Holocene human skeletal remains from Santana do Riacho, Brazil: implications for the settlement of the New World. J Hum Evol 45, 1942. Neves, W. A. & Pucciarelli, H. M. (1990) The origin of the rst Americans: an analysis based on the cranial morphology of early South American human remains. Am J Phys Anthropol 81, 274. Neves, W. A. & Pucciarelli, H. M. (1991) Morphological afnities of the rst Americans: an exploratory analysis based on early South American human remains. J Hum Evol 21, 261273. ORourke, D. H. & Suarez, B. K. (1985) Pattern and correlates of genetic variation in South Amerindians. Ann Hum Biol 13, 1332. Piperno, D. R. & Pearsall, D. M. (1998) The Origins of Agriculture in the Lowland Neotropics. New York: Academic Press. Piperno, D. & Stothert, K. (2003) Phytolith evidence for early holocene cucurbita domestication in southwest Ecuador. Science 299, 10541057. Pietschmann, R. (1906) Geschichte des Inkareiches von Pedro Sarmiento de Gamboa Abhandlungen der koeniglichen Gesellschaft der Wissenschaften zu Goettingen. In: Philologischhistorische Klasse. Berlin. Powell, J. F. & Neves, W. A. (1999) Craniofacial morphology of the rst Americans: pattern and process in the peopling of the New World. Am Phys Anthropol 42, 153188. Prieto, A. R. (1996) Late quaternary vegetational and climatic changes in the Pampa grassland of Argentina. Quaternary Res 45, 7388. Prous, A. & Fogac a, E. (1999) Archaeology of the PleistoceneHolocene boundary in Brazil. Quat Int 53/54, 2141. Prugnolle, F., Manica, A. & Balloux, F. (2005) Geography predicts neutral genetic diversity of human populations. Curr Biol 15, R159-R160. Pucciarelli, H. M. (2004) Migraciones y variaci on craniofacial humana en Am erica. Complutum 15, 225247. Ramachandran, S., Dreshpande, O., Roesman, C. C., Rosenberg, N. A., Feldman, M. W. & Cavalli-Sforza, L. L. (2005) Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. Proc Natl Acad Sci USA 102, 1594215947. Relethford, J. H. (2002) Apportionment of global human genetic diversity based on craniometrics and skin color. Am J Phys Anthropol 118, 393398. Rivet, P. (1909) Los Or genes del Hombre Americano. Mexico-Chile: Fondo de Cultura Econ omica.

Rivet, P. (1943) Recherches anthropologiques sur la BasseCalifornie. J Soc Amer Paris 6, 3109. Rothhammer, F. & Silva, C. (1992) Gene geography of Souh America:Testihg models of population displacement based on archeological evidence. Am J Phys Anthropol 89, 441446. Rothhammer, F., Silva, C., Callegari-Jacques, S. M., Llop, E. & Salzano, F. M. (1997) Gradients of HLA diversity in South American Indians. Ann Hum Biol 24, 197208. Rull, V. (1996) Late pleistocene and holocene climates of Venezuela. Quat Int 31, 8594. Salemme, M & Miotti, L. (2002) South America: long and winding roads for the rst Americans at the Pleistocene/Holocene transition. Editors Salemme, M, & Miotti, L. Quat Int 109110, 1179. Sandweiss, D. H., McInnis, H., Burger, R., Cano, A., Ojeda, B., Paredes, R., Sandweiss, M. del C. & Lascock, M. (1998) Quebrada Jaguay: Early South American maritime adaptations. Science 281, 18301832. Stanford, D. & Bradley, B. (2002). Ocean trails and prairie paths? Thoughts about Clovis Origins. In Jablonski, N., editor. The First Americans: The Pleistocene colonization of the New World. Memoirs of the California Academy of Sciences 27. 255271. Starikovskaya, E. B., Sukernik, R. I., Derbeneva, O. A., Volodko, N. V., Ruiz-Pesini, E, Torroni, A., Brown, M. D., Lott, M. T., Hosseini, S. H., Huoponen, K. & Wallace, D. C. (2005) Mitochondrial DNA diversity in indigenous populations of the southern extent of Siberia, and the origins of Native American haplogroups. Ann Hum Genet 69, 6789. Steele, D. G. & Powell, J. F. (1992) Peopling of the Americas: paleobiological evidence. Hum Biol 64, 303336. Stone, A. C. & Stoneking, M. (1998) mtDNA analysis of a prehistoric Oneota population: implications for the peopling of the New World. Am J Hum Genet 62, 11531170. Stothert, K. (1998) An early holocene maritime adaptation in southwest Ecuador: New perspectives on the Las Vegas evidence. Paper presented at 63rd Ann. Meeting of the SAA, Seattle. Szathm ary, E. J. E. (1993a) MtDNA and the peopling of the Americas. Am J Hum Genet 53, 793799. Szathm ary, E. J. E. (1993b) Genetics of aboriginal North Americans. Evol Anthropol 1, 202220. Tarazona-Santos, E., Carvalho-Silva, D. R., Pettener, D., Luiselli, D., De Stefano, G. F., Labarga, C. M., Rickards, O., Tyler Smith, C., Pena, S. D. & Santos, F. R. (2001) Genetic differentiation in South America is related to environmental and cultural diversity:evidence from the Y chromosome. Am J Hum Genet 68, 14851496. Turner, C. G. (1987) Late Pleistocene and Holocene population history of East Asia based on dental variation. Am J Phys Anthropol 73, 305321. Volodko, N. V., Starikovskaya, E. B., Mazunin, I. O., Eltsov, N. P., Naidenko, P. V., Wallace, D. C. & Sukernik, R. I. (2008) Mitochondrial genome diversity in arctic Siberians, with particular reference to the evolutionary history of Beringia and Pleistocenic peopling of the Americas. Am J Hum Genet 82, 10841100. Walter, H. V., Cathoud, A. & Mattos, A. (1937) The Conns man. A contribution to the study of early man in South America. In: Early Man: As depicted by leading authorities at the International Symposioum of the Academy of Natural Sciences, Philadelphia, March 1937 (ed. G. G. MacCurdy) London: Lippincott. Wang, S., Lewis, C. M., Jakobsson, M., Ramachandran, S., Ray, N., Bedoya, G., Rojas, W., Parra M. V., Molina, J. A., Gallo, C., Mazzotti, G., Poletti, G., Hill, K., Hurtado, A. M., Labuda, D.,

548

Annals of Human Genetics (2009) 73,540549 Journal compilation

C

C 2009 The Authors 2009 Blackwell Publishing Ltd/University College London

Late Pleistocene Colonization of South America

Klitz W., Barrantes, R., Bortolini, M. C., Salzano, F. M., PetzlErler, M. L., Tsuneto, L. T., Llop, E., Rothhammer, F., Excofer, L., Feldman, M. W., Rosenberg, N. A. & Ruiz-Linares, A. (2007) Genetic variation and population structure in native Americans. PLoS Genet 3, e185. Weng, C., Bush, M. B. & Silman, M. R. (2004) An analysis of modern pollen rain on an elevational gradient in southern Peru. J Trop Ecol 20, 113124. Wiesner, G. (1999) Early Ecuador people were maritime adapted. Mammoth Trumpet 14, 411.

Zegura, S. L., Karafet, T. M., Zhivotovsky, L. A. & Hammer, M. F. (2004) High-resolution SNPs and microsatellite haplotypes point to a single, recent entry of Native American Y chromosomes into the Americas. Mol Biol Evol 21, 164175.

Received: 8 October 2008 Accepted: 24 June 2009

C 2009 The Authors Journal compilation C 2009 Blackwell Publishing Ltd/University College London

Annals of Human Genetics (2009) 73,540549

549