doi 10.4436/jass.90019 JASs Invited Reviews Journal of Anthropological Sciences Vol. 90 (2012), pp. 81-97

Dynamics of genetic and morphological variability within Neandertals

John Hawks

Department of Anthropology, University of Wisconsin-Madison, 5240 Social Science Building 1180 Observatory Drive, Madison, WI 53706, USA e-mail: [email protected]

Summary - Paleogenomics may suggest changes to the way anthropologists have discussed the dynamics and morphological diversity among Neandertals. Genetic comparisons show that later Neandertals had relatively low autosomal genetic variation compared to recent . The known mitochondrial sample from Neandertals covers a broader geographic and temporal range, and shows greater diversity. This review addresses how genetic data compare to morphological and archaeological evidence about variation and dynamics. Traditional views emphasized the morphological differences between western and eastern Neandertal populations, and between early and later Neandertals. Genomes broadly support these groupings, without resolving the outstanding question of the affinities of specimens from southwest Asia. However, the pattern of genetic variation appears to reject a long, in situ transformation of Neandertal groups over time, suggesting instead a more rapid process of regional dispersal and partial population replacement. Archaeological indicators sample dynamics on a much finer timescale than morphological or genetic evidence, and point to dispersal and turnover among Neandertals on a regional scale. In this way, genetic evidence may provide a bridge between the timescales relevant to morphological and archaeological comparisons. New ways of looking at the morphology of Neandertals may yield a better picture of their interactions and movements.

Keywords - Ancient DNA, population dynamics, , Europe, Central Asia, mtDNA, Vindija, Mezmaiskaya.

Morphological evidence and archaeological with fewer than two dozen mtDNA sequences evidence document Neandertal populations at (Dalen et al., 2012), and only six specimens with different timescales. Morphology tells us about substantial nuclear DNA information (Green et change over tens of thousands of years, and vari- al., 2010). Despite the small sample, these data ation across regions spanning millions of square already may prompt us to revisit the sizes and kilometers. Archaeology can document change in dynamics of Neandertal populations and their behavior at a single site, among a group of sites in connections or isolation across regions. a single region, or between successive industries Following long precedent, I consider spanning a few thousand years. Yet few archaeo- Neandertals as an ancient population logical assemblages are associated with skeletal extending across Europe and parts of West and remains. In some ways, the weakness of each of Central Asia between approximately 200,000 these kinds of evidence is a strength of the other. and 30,000 years ago. The definition oversimpli- Genetic evidence provides a bridge between fies. It excludes skeletal samples before 200,000 the two timescales of morphological and archae- years ago that display clear anatomical similari- ological evidence. At this writing, the genetic ties with later Neandertals. Some ancient popula- data from Neandertal skeletal remains are sparse, tions before 200,000 years ago surely gave rise to

the JASs is published by the Istituto Italiano di Antropologia www.isita-org.com 82 Genetic and Morphological Variability in Neandertals

the later Neandertals, and some workers attrib- have some confidence in diagnosing the individ- ute of this antiquity to the Neandertal ual as part of a population. But such population (Stringer, 2012), but their variabil- a diagnosis in most cases depends on a combina- ity is not considered here. The definition also tion of several traits, each individually present in excludes Upper people of Europe who a small fraction of modern humans, but unlikely followed the Neandertals, and who shared some to occur together outside of (Rak et of their morphological characteristics (Frayer, al., 2002). Even when we consider discrete traits, 1993). Most important, the definition oversim- the problem of diagnosing a Neanderthal speci- plifies by neglecting the morphological diversity men is similar in form to the problem of diag- across the geographic range it encompasses. nosing the ancestry of a modern human specimen As described below, the Neandertal population in a forensic context. No single feature can estab- included substantial morphological and behavioral lish a high confidence in distinguishing whether variation. A look within the European and Asian a specimen is European or African in ancestry range of Neandertals finds great morphological today. Traits differ in frequency in these groups, diversity, which earlier researchers often related to allowing us to use traits in combination as foren- a time axis from early to late, and a geographic sic indicators. Nevertheless the frequencies of the axis from east to west. Different parts of this range traits are the measures of diversity within groups, were the areas of different archaeological indus- not the difference in frequencies between groups. tries, which a succession over time in each region When we consider metric traits, the diversity of that represents a depth of time. Genetic evidence Neanderthal populations is even clearer. By sta- now helps to clarify this distribution while adding tistical measures such as the coefficient of varia- new evidence about the movements and popula- tion (CV), Neandertal samples do not differ sig- tion sizes that contributed to it. The groups of nificantly in variation when compared to skeletal specimens that share genetic similarities are not samples of later human populations (Hawks & the same as those sharing morphological similari- Wolpoff, 2001; Hawks et al., 2000). ties. Far from a unitary group evolving in isolated There have been two reasons in recent years glacial conditions, the Neandertals appear to have why researchers have neglected diversity in favor been a highly dynamic population with the poten- of uniformity in their description of Neandertals. tial for rapid migration and long-distance disper- The first is a concern about whether special- sal. This perspective adds context to the archaeo- ists can diagnose Neandertals from fragmentary logical record of and initial specimens. In much of western Europe, the earli- cultural changes. est Upper Paleolithic archaeological is the early Aurignacian, dating to before 35,000 years ago. In some areas there are “transitional” The context of Neandertal industries such as Châtelperronian, Uluzzian morphological variation (Peresani, 2008), or Lincombian-Ranisian- Jerzmanowician (LRJ) (Flas, 2011). These indus- tries combine technical elements found in later When we describe Neandertals as a “diverse” Upper Paleolithic industries with raw material population, that word demands some con- procurement and organizational strategies of text. Anthropologists have often claimed that earlier, Middle Paleolithic traditions. Of these, Neandertals are pointedly not diverse, emphasizing only the Châtelperronian of southwest is the uniformity of Neandertal morphology instead associated with any relatively complete skeletal of its diversity. A few discrete traits are indeed specimen, at Saint-Cesaire, France, as well as relatively uniform in some Neandertal samples, other fragmentary remains from other sites. Even such as the suprainiac fossa (Frayer, 1993). When in this case archaeologists continue to disagree a skeletal specimen preserves such traits, we can about the strength of association of the skeletal J. HawksJ. Hawks 83

remains with the tools. Uluzzian and LRJ sites encountered other human populations after include only less complete specimens: for exam- 45,000 years ago, they would have been strongly ple, Kent’s Cavern (Higham et al., 2011), or differentiated in morphology with little overlap (Benazzi et al., 2011). The in the range of variation. This assumption can problem of skeletal associations extends forward be defended in terms of paleoenvironment and into the early Aurignacian industries in Europe cultural dynamics. European Neandertals lived up to 30,000 years ago (Churchill & Smith, recurrently, if not continuously, in periglacial 2000). A paramount problem in the anatomi- conditions. Changes in culture, as evidenced by cal study of Neandertals is to document the bio- archaeological industries, initially proceeded very logical makers of the earliest Upper Paleolithic slowly, and began to exhibit greater regional diver- industries (e.g., Bailey et al., 2009). Only a small sity and temporal turnover only toward the end number of skeletal remains have been identified of the Neandertals’ existence. Their unique ana- in association with terminal Middle and initial tomical configuration emerged within this con- Upper Paleolithic assemblages, nearly all frag- text. What could be more natural than to assume mentary. In this context, identifying whether that the forces of selection and drift had slowly a specimen is “Neandertal” or “modern” may driven them to greater and greater anatomical depend very strongly on a single trait. By decom- specialization within this unique environment? posing Neandertal identity into the morphology Yet, our current understanding of the of an individual trait, Neandertals are made to Neandertals shows that they did not experience look more morphologically homogeneous than if a slow, plodding march toward anatomical spe- many traits could be considered together. cialization. With more discoveries from extreme The second reason for emphasizing eastern Europe and central Asia, it seems that Neandertal morphological uniformity has been the center of Neandertal evolution may not the widespread assumption that Neandertal traits have been Europe at all. The anatomical record are a result of long evolution in isolation from of western Europe lay at one geographic end other human populations. Earlier workers had of a broad distribution, and the few specimens discussed the status of Neandertals as a possibly of Neandertals from central Asia show intrigu- isolated population, but Howell (1952) clearly ing differences from Neandertals in the west. presented the hypothesis that isolation in glacial The Teshik-Tash individual, for example, shows Europe gave rise to divergent morphological trends craniometric and mandibular affinities to the in the Late Pleistocene populations of Europe and Upper Paleolithic sample of Europe (Glantz et West Asia. More recently, Hublin (1998) sug- al., 2009). This does not eliminate the identifica- gested that long isolation of Neandertals could tion of this specimen as a Neandertal, but it does explain the evolution of their morphological pat- suggest that the morphological variability of the tern by genetic drift and local selection, both of eastern Neandertals encompassed variation not which would predict a reduction in the variability often found in Europe at the same time. of this population. The strength of this explana- We can adopt a more nuanced view of the tion was that it provided an explanation for the diversity within and among Neandertal popula- mosaic appearance of Neandertal traits over time tions. The main impediment to understanding within Middle Pleistocene Europeans (Stringer & Neandertal diversity is the limit on the skeletal Hublin, 1999). record. The Neandertals are the best-known of These two concerns are interrelated. Both rest any human population before 40,000 years ago. on an assumption that Neandertal populations However, even with hundreds of known speci- changed relatively slowly, developing specializa- mens, only a few individuals represent any single tions that were not shared with contemporary part of Neandertal anatomy. Today we can talk human populations elsewhere in the world. In about the diversity of Neandertals only at the this model of evolution, when the Neandertals broadest regional scale.

www.isita-org.com 84 Genetic and Morphological Variability in Neandertals

Early concepts of Neandertal already known in contemporary people, allowing diversity their anatomy to be brought within the compass of morphological “laws.” Humans to be com- How can we continue to advance our knowl- pared with Neandertals were pathological vari- edge of Neandertal diversity in the face of a frag- ants within populations, not members of very mentary record? An examination of the different populations. history of the Neandertal problem adds some By contrast, others attempted to place perspective on this vital question. Neandertals by considering the gradations among At the beginning, when only a handful of human racial groups. For example, Huxley (1864) Neandertal specimens were known, anthropolo- suggested that human variation was so great that gists defined Neandertal “diversity” mostly in “it is possible to select a series which shall lead by terms of obvious differences from humans and insensible gradations from the Neanderthal skull other fossil (or purported fossil) specimens. The up to the most ordinary forms”. Quatrefages and initial Neandertal discoveries were specimens Hamy (1882) put the Neandertal skull as part of that represented the later part of the Neandertals’ a primitive race of humans. existence. First to be recognized was Feldhofer, The morphology of a large sample of earlier then the specimen from Forbes Quarry, Neandertals represented at , , was and Engis, (both discovered earlier) later described only in the first decade of the twen- from Spy, Belgium and the classic French speci- tieth century (Gorjanovic-Kramberger, 1906). mens from (Peyrony & Capitan, The Saccopastore specimens from Rome also 1909) and La Chapelle-aux-Saints (Boule, fall within the early part of the Neandertal range 1911). This sample of skeletal remains represents (Bruner & Manzi, 2006), and were described the time period between approximately 70,000 by Sergi (1948a,b). The recovery of these ear- and 45,000 years ago. All were found within an lier Neandertals, from the Riss-Würm intergla- area of a million square kilometers of Western cial and earlier, showed anatomical continuity Europe, only a small fraction of the area we now between Neandertals and more ancient human recognize as the total Neandertal range. Hence, populations. With these samples, the issue of the initial descriptions of Neandertals were of a anatomical variation could be conceived in a biased population: Western European, long after time dimension. McCown & Keith (1939) Neandertal origins, and yet well before any pos- conceived the skeletal sample from Skhul and sible contact of Neandertals with initial Upper Tabun, in , to have come from a popula- Paleolithic people. Accentuating the morpho- tion that may have been a contemporary of the logical difference between this sample and recent European Neandertals of the last interglacial. In humans was very simple. their description, these samples represented a After the first descriptions of Neandertals, population evolving from a more modern to a some anatomists attempted to accommodate more specialized type. The variation across time them within human variability by extrapolating was related to an evolutionary model of increas- from the anatomical patterns of developmen- ing divergence between Neandertal and modern tal abnormalaties or rare morphological cor- human populations. relates of disease. Rudolf Virchow asserted that Yet, several discoveries from the early twen- the Neandertal skeleton was rachitic (Virchow, tieth century distracted many anthropologists 1872), while J. Barnard Davis (1867) maintained by appearing to support the argument for an that the Neandertal skull presented an extreme ancient, much more modern “presapiens” form case of synostosis, accounting for its elongated in Europe. Today we appreciate that the suppos- shape and complete suture closure. In the view edly early fossil sample included specimens of of these anatomists, the Neandertals presented questionable or much later provenance, such as a logical extreme of morphological tendencies Fontéchevade and the infamous Piltdown skull. J. HawksJ. Hawks 85

These did not entirely explain the Presapiens Zuttiyeh) to (Teshik-Tash). Howell idea, however, which emerged from the align- did not assign these Asian fossils explicitly to the ment of specimens on a morphological axis from early Neandertal group. Howell distinguished modern to Neandertal extremes. For example, the early Neandertals from classic Neandertals Vallois (1954) argued that specimens lacking by eight cranial features, largely associated with specific Neandertal characters must therefore smaller and more compact vaults and less midfa- represent a distinct group with a phyletic con- cial prognathism. He also claimed that the post- nection to modern humans. Weidenreich (1940) cranial skeleton of this early Neandertal sample did not accept a presapiens population as spe- was “more anatomically modern” than that of cifically distinct from Neandertals, but did cat- later Neandertals. egorize samples as sapiens based on the absence of Neandertal characteristic morphology Classic Neandertals irrespective of date (e.g., Swanscombe grouped This group included most of the well-known with Skhul as “H. sapiens intermediate”. These remains from the Würm glaciation in Europe. In examples illustrate a slow trend toward accept- today’s terms, this sample would include speci- ance of two propositions about the evolution mens as old as 100,000 years and as recent as of Neandertals and modern humans: “Modern” 40,000 years. Howell characterized this set by morphological traits may in many cases be primi- cranial features, acknowledging that the sample tive, while the morphological traits of Neandertals of Early Neandertal postcrania was not suffi- may in many cases be derived, or “specialized”. ciently numerous to make clear statements about differences with the classic Neandertals. He also pointed out that this set of specimens were known Neandertal variation and “varieties” exclusively from southwestern Europe, with west- ern and constituting the eastern- By midcentury, the broad outline of most boundaries of the classic Neandertal range. Neandertal variation was visible in the avail- able sample. An early population of Neandertals Southwest Asian Neandertals exhibited the distinctive traits of that popula- This group included the entire known fos- tion only to a slight degree. These became more sil record of the Levant to the Zagros, including accentuated over time, up to the end of the Skhul, Tabun, Zuttiyeh, and Qafzeh (all in the Neandertals’ existence. Howell (1957) consid- Levant) and Shanidar, . Howell noted the ered the variation within the known sample of divergent opinions of anthropologists about the Neandertals by describing three varieties. His evolutionary scenario that generated this sample. summary helped to crystallize the description of He offered the opinion that the initial popula- Neandertal change over time and variation across tion of the Levant represented by Tabun had space. In Howell’s description, the varieties were: affinities with Early Neandertal people, and that the region had undergone a trend of “sapiensiza- Early Neandertals tion” explaining the Skhul sample. This group included the Neandertals from Howell identified these varieties of Neandertals Krapina, Saccopastore, and Ehringsdorf. These to clarify his position on the Neandertal ances- are European sites (Croatia, Italy, and Germany) try of recent humans. In his view, several previ- representing times from last interglacial (now ous authors had been too categorical in their dated at approximately 120,000 years ago) or insistence that Neandertals could not have been earlier. Howell additionally mentioned several ancestors of modern peoples. He allowed that Asian specimens, including those from Tabun, the classic Neandertals may have been too spe- Zuttiyeh and Teshik-Tash. This is a motley cialized to have given rise to later populations group, stretching from the Levant (Tabun and within Europe. But the early Neandertals were

www.isita-org.com 86 Genetic and Morphological Variability in Neandertals

less anatomically specialized and may have been present the skeletal evidence from the Central Asian ancestral to modern humans in some other, non- Neandertal sites is insufficient to test whether these European, region. Moreover, the Southwest Asian represent a similar population those further south. Neandertals appeared to provide evidence of an There is reason to suspect greater complex- evolutionary trend toward modern humans. ity. Howell’s “Southwest Asian Neandertal” sample has been a focus of repeated debate. At the time he wrote, McCown & Keith’s (1939) Emerging problems with Neandertal description of the Skhul and Tabun remains had varieties grouped these as representatives of a single popu- lation, anatomically intermediate between classic Howell’s (1957) paper was fundamen- Neandertals and modern humans. Howell advo- tal to the definition of Neandertal variation. cated this combined sample as a single undiffer- His groupings have in later years been widely entiated population. Some recent authors have repeated. In the abstract, Howell’s scheme dif- followed this position (Arensburg & Belfer- ferentiated Neandertals along two axes: east (in Cohen, 1998; Kidder et al., 1992), while others particular the Levant) versus west, and early have preferred to separate the Levantine skel- versus late. Both these axes help to organize the etal sample into at least two different groups: morphological comparison of Neandertal sam- Neandertals (generally Amud and Kebara, some- ples. In addition, some workers have emphasized times Tabun B), and modern humans (generally a north-south axis of variation within Europe. Skhul, Qafzeh, sometimes Tabun C). The differences between classic Neandertals A problematic aspect of the idea of Levantine and early Neandertals, such as the Krapina and Neandertals is that the very features that distin- Saccopastore samples, have repeatedly been guish them from European Neandertals tend to observed, as reviewed by Hawks & Wolpoff align them with modern humans. For example, (2001). The distinction between early and clas- the Amud skeleton has stature and limb propor- sic Neandertals emerged from the work of tions that set it apart from European Neandertals, Gorjanovic-Kramberger (1906), Weidenreich but that fall within the range of variability of the (1928, 1943), Weinert (1936) and Sergi (1948). Skhul and Qafzeh skeletal remains. Trinkaus Many workers have pursued the hypothesis that (1995) considered the Near East, including classic Neandertals represent a specialized popu- Shanidar and the Levantine samples, to include lation evolving in partial isolation from other two forms of hominins: “late archaic” and “mod- ancient people. Under such a hypothesis, the ern” forms. He argued that the late archaic forms early Neandertals are expected to exhibit fewer of in the Near East have no close connection to the distinct Neandertals characteristics compared European Neandertals, and that similar features to later, classic Neandertals. reflect mosaicism or generalized archaic mor- The east-west axis of variation has been fre- phology in both evolving populations. quently recognized in morphological comparisons Several workers after Howell added the (Voisin, 2006). However, the east-west axis within concept of a north-south axis of Neandertal Neandertals today presents much more potential diversification within Europe. Rosas and col- complexity than in Howell’s time. If the popula- leagues (2006) noted that southern Neandertals tions of Central Asia before 40,000 years ago were tend to have increased heights of the lower face Neandertals, and if the Shanidar and Levantine and broader faces than the northern sample of sites also represent Neandertals, the eastern “pole” Neandertals within Europe. Because the line sep- of Neandertals was bifurcated to the north and arating north and south must run along the very south of the Black Sea-Caspian Sea corridor. There long east-west axis of Europe, there are many is no reason to expect that these two areas would possible ways to divide the continent into north- have aligned along the same morphological axis. At ern and southern samples. J. HawksJ. Hawks 87

Paleogenetics (e.g., Serre et al., 2004; Currat & Excoffier, 2004). Additionally, no ancient specimens of The data from paleogenetics of Neandertals modern humans have been found to share a have rapidly changed during the past few years. Neandertal-like mtDNA type (Serre et al., 2004; As a result, descriptions of the state of the evi- Caramelli et al., 2003). As discussed below, the dence from as recently as 2005 are now obso- hypothesis of no Neandertal ancestry for living lete. In that time, the synthesis of Neandertal people has been contradicted by nuclear DNA DNA evidence has proceeded from a very simple evidence (Green et al., 2010). Yet the lack of model to one involving more complicated popu- mtDNA sharing between Neandertal and later lation interactions and movements. human populations is not consistent with a neutral explanation rooted in Upper Paleolithic Mitochondrial DNA demographic growth (Manderscheid and Rogers, The complete mitochondrial genomes 1996; Ghirotto et al., 2011). One hypothesis of more than a dozen Neandertals have been that would reconcile the mtDNA and nuclear described and small fractions of the mitochon- genetic data is that the mtDNA of Neandertals drial sequences are known for many more. These was subject to negative selection in competition extend from as far to the east as Okladnikov with mtDNA clades present in modern humans in the low Altai (Krause et al., 2007), and (Hawks, 2006). Another possibility is repeated as far west as El Sidrón in (Lalueza-Fox et demographic turnover. al., 2012). The distance between those two sites The pattern of mtDNA evolution within encompasses nearly the entire east-west range Neandertals suggests that repeated turnover of the known for the Neandertals. The north-south population of European Neandertals did happen. extent of data is much more restricted, as none of When considering the entire sample of mtDNA, the sites from present-day Israel or Iraq have yet the amount of variation within the Neandertal yielded genetic evidence. Dalén and colleagues sample is approximately equal to the variation (2012) have recently reviewed the mtDNA evi- within living people across the same geographic dence from Neandertals, including a full list range, from Spain to Central Asia (Caramelli of those specimens that have yielded mtDNA et al., 2008; Krause et al., 2007). The common sequences. These include specimens from El ancestor of all Neandertal mtDNA sequences Sidrón (Lalueza-Fox et al., 2012) and Valdegoba, lived approximately 200,000 years ago, around Spain (Dalén et al., 2012), , Belgium the same time as the modern human mtDNA (Orlando et al., 2006), Feldhofer, Germany last common ancestor (Dalen et al., 2012). Taken (Krings et al., 1999), Monti Lessini, Italy by themselves, these comparisons are consistent (Caramelli et al., 2008), Vindija, Croatia (Green with the hypothesis that Neandertals had approx- et al., 2008), Mezmaiskaya (Ovchinnikov et al., imately the same population structure and demo- 2000) and Okladnikov, (Krause et al., graphic history as modern Eurasians. However, 2007) and Teshik-Tash, Uzbekistan (Krause et when we compare earlier and later Neandertals, al., 2007). All these specimens can be connected the picture is more complex. The sample of by a phylogenetic tree that does not include any Neandertal mtDNA taken from European sequences from other known samples of living specimens after 50,000 years ago is depauper- humans or ancient DNA from modern human ate in variation compared to the full sample specimens. (Lalueza-Fox et al., 2008). The lack of variation No known living people have mtDNA in later European Neandertals is not consistent sequences that belong to the clade shared by with these being a sample drawn from a small all known Neandertals, a fact that strongly geographic area of a larger distribution, with- influenced many researchers to believe that out demographic turnover (Dalen et al., 2012). Neandertals had become extinct without issue Instead, it appears that the western part of the

www.isita-org.com 88 Genetic and Morphological Variability in Neandertals

Neandertal range underwent at least one episode eastern range with greater diversity and much of large-scale migration and partial population earlier specimens in Western Europe. replacement. A tightly related clade of sequences The most celebrated result from the nuclear includes the specimens from Vindija, El Sidrón DNA evidence is the finding that non-African and Feldhofer, seven specimens in all. These are populations today derive a proportion of their all among the latest Neandertals in the west. The ancestry from Neandertals (Green et al., 2010). Central Asian or eastern European portion of the The fraction of ancestry represented by such Neandertal range retained greater mtDNA varia- introgression from Neandertals is between 1 and tion in this later time period, possibly indicating 4 percent of the genealogical ancestry of individ- that this area was a source for later Neandertals in uals with European, Asian or other non-African Western Europe. Dalen and colleagues suggested origins. Some of the similarity of non-Africans to that a mass dispersal of Neandertals from the Neandertals may be attributable to the ancient eastern into the western part of their range would Middle Pleistocene structure of African popula- be consistent with the mtDNA phylogeography. tions (Eriksson & Manica, 2012), but this effect An alternative hypothesis is that alone cannot explain the pattern of similarities, on Neandertal mtDNA affected the frequency of which therefore require substantial introgression clades in Western Europe. (Yang et al., 2012). It is possible that some simi- Fabre and colleagues (2009) also emphasized larities of living people and Neandertals resulted a biogeographic division of mtDNA into eastern from gene flow between Neandertals and African and western groups. They used a different meth- contemporaries before the Late Pleistocene dis- odology, focused upon whether the geographic persal of modern populations. At present, there range of Neandertals could be divided into repli- is no indication that Europeans have substantially cable subsamples. In addition to the division into more Neandertal ancestry than Asians or other Central Asian and European groups, the study peoples outside Africa (Green et al., 2010). The also suggested that the Italian and Croatian spec- Denisova genome represents a population with imens might belong to a “southern” group. This substantial genetic separation from Neandertals study did not consider the times represented by (Reich et al., 2010). This population is repre- different sites, and adding the dynamic reflected sented only by three individuals from Denisova by time would likely change the groupings. By Cave, in the . However, the testing a priori models, the study avoided some population was among the ancestors of native of the problems attendant upon the tree-based Aboriginal Australians and related peoples of New approaches described above. Guinea and Oceania (Reich et al., 2011). The introgression from these ancient populations into Nuclear DNA recent humans is not a focus of this paper, which Three Neandertals from Vindija have been is about the dynamics of Neandertal populations. represented by substantial sequencing of the Nuclear DNA variation among the known nuclear genome, averaging nearly 1x coverage Neandertal genomes is very limited compared to for each of them. Much smaller fractions of that found in living human populations. By using the nuclear genome have been recovered from the genome of the Denisova specimen as an out- Neandertal specimens from Feldhofer Cave, El group, Reich and colleagues (2010) showed that Sidrón, and Mezmaiskaya (Green et al., 2010). the variation across the Neandertal geographic All of these except for Mezmaiskaya are among range, from Mezmaiskaya to El Sidrón, is very the group of later Western European Neandertals low compared to the variation within humans discussed above, all of which fall into a single today, or between Neandertals and the Denisova mtDNA clade. This is therefore a highly con- genome. They interpreted this low variation strained set of Neandertals in space and time. within Neandertals as evidence for a bottleneck The full set of mtDNA extends includes an in the population history of Neandertal groups. J. HawksJ. Hawks 89

If we add the Denisova genome, which is quite Reconciling paleogenomics and genetically divergent from Neandertals, the total morphology variation of the archaic human sample is only slightly greater than the variation among the The discussion of genetic diversity among most distant human populations today. these Neandertals has not yet attempted to rec- The low nuclear DNA diversity of these late, oncile their genealogical arrangement with mostly Western European Neandertals more or morphological classification schemes. The later less matches the low mtDNA diversity found Western European Neandertals that share a in the same sample. This reduces the prob- close mtDNA genealogical connection (Vindija- ability that natural selection specific to mtDNA Feldhofer-El Sidrón) are not synonymous with can explain the mtDNA phylogeography of “classic Neandertals”. The well-known clas- Neandertals. In the absence of selection, nei- sic Neandertals include specimens such as La ther geography nor time considered alone would Chapelle-aux-Saints (France), , be sufficient to explain the grouping of the Monte Circeo 1 (Guattari) as well as Feldhofer 1. later, western subset of Neandertals into a tight This classic Neandertal sample includes specimens mtDNA genealogical arrangement. One possible earlier than 70,000 years old and some as recent explanation is a movement of Neandertals from as 45,000 years ago. The classic Neandertals flank the eastern to western part of their range some- both the earlier and later sides of the 50,000-year- time after the origin of this clade, some 60,000 ago dispersal of Neandertals proposed by Dalen years ago. This movement would have to have and colleagues (Dalen et al., 2012). replaced a large fraction of the mtDNA gene Meanwhile, the clade that connects late pool of earlier Neandertals in western Europe; European Neandertal mtDNA into a tight cluster otherwise, clades shared by earlier Neandertals includes great morphological diversity. The two such as Scladina would still be found among the Vindija mtDNA sequences included by Dalén later Neandertals. The replacement of earlier, and colleagues (Dalen et al., 2012) are both from more diverse mtDNA clades would be easier if layer G3 of the site, perhaps 40,000 years old. the effective number of Neandertals in western Both are derived from postcranial fragments Europe was very small. A small effective size does without diagnostic morphological traits. The not necessarily imply a very small census popu- other material from G3 includes cranial, mandib- lation size (Hawks, 2008), and might point to ular and dental remains that are not synonymous a way to uncover population dynamics of this with classic Neandertal morphology (Ahern, population, as discussed below. 2004). These late Neandertals from Vindija The reduced variation of nuclear and mtDNA display less pronounced morphology than clas- in the late western Neandertals reflects high sic Neandertals and lack traits that are common genetic drift in this component of the Neandertal in the earlier classic Neandertals (Smith, 1992). population. Genetic drift may reflect many dif- These specimens are connected to Feldhofer and ferent demographic phenomena, including small El Sidrón not only by mtDNA relationships but population size, recurrent movement, extinction also their very low nuclear DNA diversification. and recolonization of small subpopulations (Eller If the Vindija specimens can be lumped together et al., 2004), or selection-migration interaction. in mtDNA and nuclear DNA diversity with the We do not have nuclear genetic data from ear- remains from El Sidrón and Feldhofer, it seems lier Neandertals, and so we cannot directly test possible that traditional morphological group- the hypothesis of a population bottleneck in the ings will fail to capture real biological differences classic or later Neandertals. Nuclear genetic sam- among Neandertal populations. pling of a broader range of Neandertals, includ- Two avenues of evidence will provide more ing eastern and earlier specimens, might uncover insights about Neandertal population dynamics. substantially more variation. Obviously, uncovering more nuclear genomes

www.isita-org.com 90 Genetic and Morphological Variability in Neandertals

from Neandertals or early Upper Paleolithic glaciations, but that long-distance migrations humans would advance our knowledge greatly. and recolonizations of formerly periglacial habi- Tempering this expectation is that the later west- tat was an important cause of population change ern Neandertals, with lower genetic diversity, in Neandertals and the modern humans who are the ones most likely to provide more genetic encountered them. data. Earlier Neandertals, and the Neandertals Today, our knowledge of the geographic from central Asia, would be most useful to range of the Neandertals confirms their existence uncover new knowledge about the population across a broad range of climate regimes. From dynamics of this ancient group. A second source the Altai to Spain, the known geographic range of evidence may come from the introgression of of Neandertals covered more than 7000 kilom- Neandertal genes into later human populations. eters east to west. On the longitudinal range is As we begin to uncover the genes in living peo- little doubt, because of the mtDNA evidence ple that came from Neandertals, we face the pos- European Neandertal specimens to Okladnikov sibility that these genes may represent different Cave (Krause et al., 2007). Okladnikov is at ancient Neandertal groups to greater or lesser present the easternmost site to produce skeletal degrees. The initial work on Neandertal genetics remains attributable to Neandertals, although suggested that most of the population mixture other sites with similar archaeology are found with Neandertals may have happened in west in the Altai. The Neandertals also covered a Asia (Green et al., 2010). That would suggest substantial range in latitude. The northernmost that European Neandertals are themselves some- Neandertal site may be Byzovaya, which does what genetically distinct from the population not present skeletal remains but does include a that gave rise to most Neandertal genes in recent Late Mousterian assemblage with some techni- populations. Comparing different Neandertals cal links to central European Neandertal sites with each other will help us uncover the structure (Slimak et al., 2011). The earliest faunal evidence of the population that gave rise to Neandertal from Mamontovaya Kurya is earlier than the ancestry in living people. By doing so, we may Byzovaya evidence and also contemporary with gain an additional genetic probe into the period late Neandertals. However, these sites are at the before 60,000 years ago, as Neandertal popula- end of the Neandertals’ timespan, and possibly tions had differentiated before the large-scale represent the activity of subsequent people. The encounters with dispersing people from Africa. paleoecological reconstruction of Mousterian sites encompasses almost the entire range of European ecological contexts, except for Alpine Population dynamics and Arctic biomes (Banks et al., 2008). Although the European climatic conditions oscillated During the 1950s, as anthropologists began considerably during the Late Pleistocene, the to acknowledge the morphological diversity of Neandertals seem likely to have been capable of Neandertal populations, they became increas- adapting to changing conditions, either by track- ingly concerned with the Neandertal potential for ing ecotones as climate shifted or by changing individual dispersal and population movement. their subsistence strategies to meet new require- The attention to “early” Neandertals as a group ments. In other words, the archaeological record dating to the last interglacial brought with it the by itself is sufficient to show us that Neandertal understanding that Neandertals had persisted populations were highly dynamic in areas where through at least one entire glacial cycle. Howell habitation was possible only during intermittent (1952) proposed that glacial cycles provided climatic periods. the isolation that enabled classic Neandertals to Archaeological evidence alone gives us evolve their specialized anatomy. Weckler (1954) some indications that Neandertals rapidly colo- argued that isolation was one consequence of nized new regions when they became suitable J. HawksJ. Hawks 91

for habitation. The possible excursions of Late estimates of the total number of Neandertals Mousterian people north of the Arctic Circle to representing traditions such as the Mousterian of Byzyvaya and Mamontovaya Kurya are strong Tradition (MTA) are as low as a few indicators of such a potential, if these sites truly hundred individuals total (Richter, 2006). Across represent Neandertal activity. Bar-Yosef (1992) peninsular Europe, there may have been fewer suggested that later Neandertal sites in the than 10,000 Neandertals living at any given Levant, including Amud and Kebara, may repre- time, an indication of the census population size. sent the recolonization of this area from Europe Certainly, the genetic variation of Neandertals as cold conditions intensified during the Wurm is consistent with a very small effective popu- glaciation. Shea (2008) considered the record of lation size. Many factors reduce genetic varia- modern and Neandertal activity in the Levant to tion relative to census population size (Hawks, represent multiple cases of population turnover, 2008), including two of particular relevance to as climate shifts caused successive populations Neandertal population structure: extinction and of Paleolithic humans to abandon the area or recolonization of groups (Eller et al., 2004), become locally extinct. and broader regional-scale cultural replacement Across northwestern Europe, from Britain to in the presence of selection (Premo & Hublin, , an area of more than a million square kil- 2009). Such small groups and regional popula- ometers was abandoned by Neandertals during tions would have very little genetic “inertia” the early stages of the last glaciation and not rein- against the long-term effect of gene flow. Genetic habited until after approximately 60,000 years continuity in this scenario could never persist for ago. The intermittent occupation of these parts long against even a moderate amount of immi- of Europe was likely not a function of “habitat gration acting over many generations. tracking” by Neandertals, but instead a record of Genetics now leads us to a picture of a highly regional expansions and partial extinctions when dynamic Neandertal population. This should climatic conditions deteriorated (Hublin & not be a surprise in the context of the archaeo- Roebroeks, 2009). White & Pettitt (2011) sug- logical record, which shows abundant evidence gested a very small Neandertal population size for regional-scale population movement and in northwestern Europe during the late Middle rapid changes to cultures and adaptive strategies. Paleolithic, and considered the possibility that But it is not clear that the genetic and archaeo- the occupation of Britain was maintained as logical data actually converge on a single picture seasonal camps rather than permanent of population dynamics. settlement. This kind of occupation would put movements of several hundred kilometers into the ordinary behavioral pattern of individual Archaeological and genetic Neandertals. At an extreme, the survival of evidence: a case study Neandertals on the northwestern tier of Europe may have been precarious (White, 2006). From A close look at a single archaeological exam- the perspective of population dynamics, this ple helps to demonstrate the difficulty of recon- does not suggest a dense, stable population, but ciling archaeological and genetic observations instead one of great mobility and repeated ability into a single population model. The Quina to colonize and exploit new opportunities. Mousterian in southwestern France appears to We cannot consider Neandertal population represent a regional Neandertal adaptive pat- dynamics without discussing the probable effects tern. As climate conditions gave rise to a mix of of small population numbers on their distribu- steppe and boreal forest, Neandertals specialized tion. The estimation of population numbers on reindeer, and to a lesser extent horse, replac- from archaeological site densities is imprecise ing an earlier strategy using a broader mix of with many sources of error. Nevertheless, some large . The accompanying toolkit has been

www.isita-org.com 92 Genetic and Morphological Variability in Neandertals

recovered from many sites in the region, consist- Portel and the older sites of Genay and Payre. ently overlying earlier Denticulate and Typical Their comparisons were necessarily limited but Mousterian assemblages (Guerin et al., 2012). showed a lack of regional differentiation between As we consider this kind of technical tran- this set of Neandertals and the remainder of the sition, it is not obvious how the earlier and Neandertal sample from across Europe. Within later Neandertals of southwestern France were Spain, Rosas and colleagues (2006) described the related to each other. The transition in this area, mandibular remains from El Sidrón, including around 60,000 years ago, is a temporal bound- them in several comparisons of regional samples ary between traditions each of which lasted for of Neandertals. They found evidence for a sig- thousands of years. Certainly it is possible that nificant difference in mandibular morphology the earlier population underwent cultural adap- between “northern” and “southern” samples, tive evolution, suiting it better to the changing which they attribute to a smaller dentition and ecology, and resulting in the later cultural tradi- degree of midfacial prognathism in the southern tion. But it is also possible that ideas spread when sample. However, these “northern” and “south- people themselves spread. ern” sets each include specimens known to be Cultural change and spatial dispersal were part of the “late western Neandertals” that pre- likely interlinked. An effective faunal procure- serve low genetic variability. To the extent that ment strategy may open up habitat that earlier there is a morphological difference here, it does Neandertals had less success exploiting. The not match the genetic pattern. colder parts of Germany seem to have seen the In short, morphological comparisons across spread of reindeer hunters during MIS 4, in the relevant time span in France and Spain are an occupation that may have been thin on the insufficient to support the hypothesis of a large- ground but potentially occupied a broad area scale migration bringing in a new mtDNA type. (Uthmeier et al., 2011). As different Neandertal Yet it is difficult to imagine that a widespread groups used different adaptive strategies, some movement of Neandertals could reach northern would have expanded in geographic range, some- Spain by around 50,000 years ago without pass- times into new previously unoccupied territory ing through southwestern France or affecting the but often into territories formerly occupied by skeletal sample of Spain. Possibly the very small groups with different cultural strategies. Could sample of physical remains will simply be insuf- northern Neandertal reindeer hunters have fol- ficient to test hypotheses of population dynamics lowed their herds right down into the heartland on this scale. of France, as conditions grew colder, replacing If the Neandertals of southwestern France, their cousins to the south? for example, were fewer than 1000 individuals, Despite the evidence for cultural change, how could they have maintained identifiable as far as we know the morphological varia- traditions of stone technology for thousands of tion across this cultural transition was con- years? If their gene pool was constantly in flux tinuous. Before 60,000 years ago, southwestern due to immigration and long-distance move- France was inhabited by people we call classic ment of individuals, how could their cultures Neandertals. Skeletal associations with Quina not have rapidly changed beyond recognition? In Mousterian, for example from Les Pradelles this scenario it seems necessary to assume very (Mussini, 2011) and , present no strong reinforcement of technology by learning obvious appearance of morphological disconti- biases, probably mediated by the observed util- nuity with other classic Neandertals. Condemi ity of choices within the local ecology and colleagues (2010) considered the dental (Henrich, 2001). Learning and cognition may sample from the Rhône valley of southeastern have supported a dynamic Neandertal popula- France, including the well-known classic and tion, enabling their persistence in a tenuous pale- late Neandertal sites of Hortus, Tournal and Le oclimatic regime. J. HawksJ. Hawks 93

Conclusion variability. It is conceivable that these samples represent or an equally divergent A synthetic view of Neandertal popula- ancient population. The counterargument to tion dynamics must incorporate morphologi- such a hypothesis is that Neandertals must have cal, genetic and archaeological observations. Of mixed with modern humans somewhere, and these three, the archaeological record is the most the likely geographic location for such exchange, sensitive indicator of regional-scale changes on before modern humans spread throughout a millennial timescale. Within the broad scope Eurasia, was the Levant. Nevertheless, the Altai of the Mousterian in Europe and Central Asia, Mountains were a point of population inter- archaeologists have recognized regional variants action across potentially tens of thousands of that cover hundreds of thousands of square kil- years, within a smaller land area than West Asia. ometers of geographic area. But archaeological The Levant, Arabian peninsula, Mesopotamia, evidence is highly specific and particular to a Anatolia and the Caucasus constitute a large area given region. As we examine a detailed case study in which diverse populations of Neandertals and within a region, it may be difficult or impossible other may have coexisted. to find morphological and genetic correlates of Several important questions have not been changes in archaeological industries and tradi- addressed in this paper. Late Neandertals, in the tions. Archaeology does provide insight into the period after 40,000 years, remain to be geneti- ways the Neandertals maintained their popula- cally sampled. They may represent a further stage tion in the face of regional movements, suggest- of population turnover within the Neandertals, ing logistical strategies that may have involved or may bear the influence of modern human temporary summer occupations at some distance ancestry. The morphology of Central Asian from their core territories. Neandertals remains poorly known, as does the The genetic data force us to adopt a new pattern of connection between Central Asia and stance on the of Neandertal populations. Southwest Asia. What we now know is that the A long, slow evolution of Neandertal popula- traditional category of “classic” Neandertals is tions cannot account for the evidence of long- insufficient to describe the genetic variability distance interactions and movement on relatively and dynamics of Late Pleistocene Europeans. short time scales. The redefinition of Neandertal That finding alone should cause us to revisit the population groupings should begin immedi- connection between skeletal and archaeological ately. We may soon have genetic data from many evidence of Neandertals. more Neandertal specimens. Given the unex- pected finding of diversity from the Denisova specimen (Reich et al., 2010) it is possible that References some other Asian “Neandertal” populations will turn out to represent equally divergent human Ahern J.C.M., Karavanić I., Paunović M., populations. As we consider the “Southwestern Janković I. & Smith F.H. 2004. New discov- Asian” Neandertals in Howell’s (1957) review, eries and interpretations of hominid fossils and we can already see how that collection of speci- artifacts from , Croatia. J. Hum. mens may have included a heterogenous collec- Evol., 46:27 - 67. tion representing several distinct populations. Arensburg B. & Belfer-Cohen A. 1998. Sapiens Anthropologists today disagree about whether and Neandertals. In Akazawa T., Aoki K. & Shanidar, Amud and Kebara should be counted Bar-Yosef O. (eds): Neandertals and Modern among the Neandertals. Humans in Western Asia, pp. 311–322. Plenum We should not too readily assume that Press, New York. gene sequences from such specimens would fall Bailey S.E., Weaver T.D. & Hublin J.-J. 2009. within the known pattern of Neandertal genetic Who made the Aurignacian and other early

www.isita-org.com 94 Genetic and Morphological Variability in Neandertals

Upper Paleolithic industries? J. Hum. Evol., Currat M. & Excoffier L. 2004. Modern humans 57:11 - 26. did not admix with Neanderthals during their Banks W.E., D’Errico F., Peterson T.A., Kageyama range expansion into Europe. PLoS Biol., 2: e421. M., Sima A. & Sánchez-Goñi M.-F. 2008. Dalén L., Orlando L., Shapiro B., Durling M. by competitive exclu- B., Quam R., Gilbert T.M.P., Díez Fernández- sion. PloSOne, 3:e3972. Lomana C.J., Willerslev E., Arsuaga J.-L., Bar-Yosef O. 1995. The Role of Climate in the Götherström A., et al. 2012. Partial genetic Interpretation of Human Movements and turnover in Neandertals: continuity in the east Cultural Transformations in Western Asia. In and population replacement in the west. Mol. Vrba E.S., Denton G.H., Partridge T.C. & Biol. Evol. (in press). Burckle L.H. (eds): Paleoclimate and Evolution Davis J.B. 1867. Thesaurus Craniorum: catalogue with Emphasis on Human Origins. Paleoclimate of the skulls of the various races of man, in the col- and Evolution with Emphasis on Human Origins, lection of Joseph Barnard Davis. London. pp. 507–523. New Haven, CT. Eller E., Hawks J. & Relethford J.H. 2004. Benazzi S., Douka K., Fornai C., Bauer C.C., Local Extinction and Recolonization, Species Kullmer O., Svoboda J., Pap I., Mallegni F., Effective Population Size, and Modern Human Bayle P. & Coquerelle M. 2011. Early dis- Origins. Hum. Biol., 76:689–709. persal of modern humans in Europe and im- Eriksson A., Manica A. 2012. Effect of ancient plications for Neanderthal behaviour. Nature, population structure on the degree of polymor- 479:525-528. phism shared between modern human popula- Boule M. 1911. L’homme fossile de la Chapelle- tions and ancient hominins. Proc. Natl. Acad. aux-Saints. Annales de Paléontologie, 6. Sci. U.S.A., 109:13956-13960. Bruner E., Manzi G. 2006. Saccopastore 1: the Fabre V., Condemi S. & Degioanni A. 2009. earliest Neanderthal? A new look at an old cra- Genetic evidence of geographical groups among nium. In Hublin J.-J., Harvati K. & Harrison Neanderthals. PloS One, 4:e5151. T. (eds): Neanderthals Revisited: New Approaches Féblot-Augustins J. 1997. La circulation des and Perspectives, pp. 23 - 36. Dordrecht. matières premières au Paléolithique. Halshs, Caramelli D., Lalueza-Fox C., Vernesi C., Lari e00436342. M., Casoli A., Mallegni F., Chiarelli B., Flas D. 2011. The Middle to Upper Paleolithic transi- Dpanloup I., Bertranpetit J. & Barbujani G. tion in Northern Europe: the Lincombian-Ranisian- Evidence for a genetic discontinuity between Jerzmanowician and the issue of acculturation of the Neandertals and 24,000-year-old anatomi- last Neanderthals. World Archaeol., 43:605 - 627. cally modern Europeans. Proc. Natl. Acad. Sci. Frayer D.W. 1993. Evolution at the European U.S.A., 100:6593–6597. edge: Neanderthal and Upper Paleolithic rela- Caramelli D., Milani L., Stanyon R. & Fox C.L. tionships. Préhistoire Européenne, 2:9–69. 2011. Towards Neanderthal Paleogenomics. In Ghirotto S., Tassi F., Benazzo A. & Barbujani G. Condemi S. & Weniger G-C. (eds): Continuity 2011. No evidence of Neandertal admixture in and Discontinuity in the Peopling of Europe, p. the mitochondrial genomes of early European 219-221. Dordrecht. modern humans and contemporary Europeans. Churchill S.E. & Smith F.H. 2000. Makers of Am. J. Phys. Anthropol., 146:242-52. the Early Aurignacian of Europe. Yearb. Phys. Glantz M., Athreya S. & Ritzman T. 2009. Anthropol., 43:61–115. Is Central Asia the eastern outpost of the Condemi S., Voisin J.-L., Belmaker M. & Moncel Neandertal range? A reassessment of the Teshik- M.-H. 2010. Revisiting the Question of Tash child. Am. J. Phys. Anthropol., 138:45 - 61. Neandertal Regional Variability: a View from Gorjanovič-Kramberger D. 1906. Der diluviale the Rhône Valley Corridor. Coll. Anthropol., Mensch von Krapina in Kroatien. Földtany 3:787-796. Közlöny, 36:307–322. J. HawksJ. Hawks 95

Green R.E., Krause J., Briggs A.W., Maricic T., In Akazawa T., Aoki K. & Bar-Yosef O. (eds): Stenzel U., Kircher M., Patterson N., Li H., Zhai Neandertals and Modern Humans in Western W., Fritz M.H., et al. 2010. A draft sequence of Asia, pp. 295–310. Plenum Press, New York. the Neandertal genome. Science, 328:710–722. Hublin J.-J. & Roebroeks W. 2009. Ebb and Green R.E., Malaspinas A.S., Krause J., Briggs A.W., flow or regional extinctions? On the character Johnson P.L., Uhler C., Meyer M., Good J.M., of Neandertal occupation of northern environ- Maricic T., Stenzel U. 2008. A complete Neandertal ments. C. R. Palévol, 8:503 - 509. mitochondrial genome sequence determined by Huxley T.H. 1864. Further Remarks upon the high-throughput sequencing. Cell, 134:416–426. Human Remains from the Neanderthal. Nat. Guérin G., Discamps E., Lahaye C., Mercier N., Hist. R. Q. J., 1:429–446. Guibert P., Turq A., Dibble H.L., McPherron Kidder J.H., Jantz R.L. & Smith F.H. 1992. S.P., Sandgathe D., Goldberg P., et al. 2012. Defining modern humans: a multivariate ap- Multi-method (TL and OSL), multi-material proach. In Bräuer G. & Smith F.H. (eds): (quartz and flint) dating of the Mousterian site Continuity or Replacement? Controversies in of Roc de Marsal (Dordogne, France): correlat- Homo sapiens Evolution, pp. 157–177. Balkema, ing Neanderthal occupations with the climatic Rotterdam. variability of MIS 5-3. J. Archaeol. Sci. (in press). Krause J., Orlando L., Serre D., Viola B., Hawks J. & Wolpoff M.H. 2001. The accretion Prüfer K., Richards M.P., Hublin J.-J., model of Neandertal evolution. Evolution, Hänni C., Derevianko A.P. & Pääbo S. 2007. 55:1474–1485. Neanderthals in Central Asia and . Hawks J. 2006. Selection on mitochondrial DNA Nature, 449:902–904. and the Neanderthal problem. In Hublin J-J., Krings M., Geisert H., Schmitz R.W., Krainitzki. Harvati K. & Harrison T. (eds): Neanderthals 1999. DNA sequence of the mitochondrial Revisited: New Approaches and Perspectives, p. hypervariable region II from the Neandertal 221– 238. Dordrecht. type specimen. Proc. Natl. Acad. Sci. U.S.A., Hawks J. 2008. From Genes to Numbers: Effective 96:5581–5585. Population Sizes in . In Lalueza-Fox C., Gigli E., Sánchez-Quinto F., de Bocquet-Appel J.-P. (ed): Recent Advances in la Rasilla M., Fortea J. & Rosas A. 2012. Issues Paleodemography, pp. 9–30. Springer, Amsterdam. from Neandertal genomics: Diversity, adap- Henrich J. 2001. Cultural Transmission and the tation and hybridisation revised from the El Diffusion of Innovations: Adoption Dynamics Sidrón case study. Quat. Int., 247:10 - 14. Indicate that Biased Cultural Transmission is Manderscheid E.J. & Rogers A.R. 1996. Genetic the Predominate Force in Behavioral Change. Admixture in the Late Pleistocene. Am. J. Phys. Am. Anthropol., 103:992-1013. Anthropol., 100:1–5. Higham T., Compton T., Stringer C., Jacobi R., McCown T.D. & Keith A. 1939. The Stone Age Shapiro B., Trinkaus E., Chandler B., Öning Man of Mount Carmel: The Fossil Human F., Collins C. & Hillson S. 2011.The earliest Remains from the Levalloiso-Mousterian. evidence for anatomically modern humans in Clarendon Press, Oxford. northwestern Europe. Nature, 479:521-524. Mussini C. 2011. Les restes humains moustériens des Howell F.C. 1952. Pleistocene glacial ecology and Pradelles (Marillac-le-Franc, Charente, France) : the evolution of “Classic Neandertal” man. étude morphométrique et réflexions sur un aspect Southwest J. Anthropol., 8:377–410. comportemental des Néandertaliens. Thèse de doc- Howell F.C. 1957. The evolutionary significance torat en Anthropologie biologique, Bordeaux 1. of variation and varieties of “Neanderthal” Orlando L., Darlu P., Toussaint M., Bonjean man. Q. Rev. Biol., 32:330–347. D., Otte M. & Hänna C. 2006. Revisiting Hublin J.-J. 1998. Climatic changes, paleogeog- Neandertal Diversity with a 100,000 Year Old raphy and the evolution of the Neandertals. mtDNA Sequence. Curr. Biol., 16:R400–R402.

www.isita-org.com 96 Genetic and Morphological Variability in Neandertals

Peresani M. 2008. A New Cultural Frontier for the Shea J.J. 2008.Transitions or turnovers? Last Neanderthals: The Uluzzian in Northern Climatically-forced extinctions of Homo sapi- Italy. Curr. Anthropol., 49:725–731. ens and Neanderthals in the east Mediterranean Peyrony D. & Capitan L. 1909. Deux squelettes Levant. Quat. Sci. Rev., 27:2253 - 2270. humains au milieu de foyers de l’époque mousté- Slimak L., Giraud Y. 2007 .Circulations sur rienne. Comptes-rendus des séances de l’Académie plusieurs centaines de kilomètres durant le des Inscriptions et Belles-Lettres, 53:797-806. Paléolithique moyen. Contribution à la con- Premo L.S. & Hublin J.-J. 2009. Culture, naissance des sociétés néandertaliennes. C. R. Population Structure, and Low Genetic Palévol., 6:359 - 368. Diversity in Pleistocene Hominins. Proc. Natl. Slimak L., Svendsen J.I., Mangerud J., Plisson H., Acad. Sci. U.S.A., 106:33–37. Heggen H.P., Brugère A. & Pavlov P.Y. 2011. Quatrefages A. & Hamy E.T. 1882. Crania Late Mousterian Persistence near the Arctic Ethnica. Les crânes des races humaines. J. B. Circle. Science, 332:841–845. Baillière et fils, Paris. Smith F.H. 1982. Upper Pleistocene hominid Rak Y., Ginzburg A., Geffen E. 2002. Does Homo evolution in South-Central Europe: A review neanderthalensis play a role in modern human of the evidence and analysis of trends. Curr. ancestry? The mandibular evidence. Am. J. Anthropol., 23:667–703. Phys. Anthropol., 119:199 - 204. Stringer C. 2012. The status of Reich D., Green R.E., Kircher M., Krause J., (Schoetensack 1908). Evol. Anthropol., 21:101 - 107. Patterson N., Durand E.Y., Viola B., Briggs Stringer C.B. & Hublin J.-J. 1999. New age esti- A.W., Stenzel U., Johnson P.L.F., et al. 2010. mates for the Swanscombe hominid and their Genetic history of an archaic hominin group significance for human evolution. J. Hum. from in Siberia. Nature, Evol., 37:873–877. 468:1053–1060. Trinkaus E. 1995. Near Eastern Late Archaic Richter J. 2008. Neanderthals in their landscape. Humans. Paleorient, 21:9-24. In Demarsin B. & Otte M. (eds): Neanderthals Uthmeier T., Kels H., Schirmer W. & Böhner U. in Europe, pp. 17–32. Proceedings of the 2011. Neanderthals in the Cold: Middle Paleolithic International Conference, held in the Gallo- Sites from the Open-Cast Mine of Garzweiler, Roman Museum in Tongeren, ATVATVCA, Nordrhein-Westfalen (Germany). In Conard N.J. Gallo-Roman Museum, Luik-Tongeren. & Richter J. (eds): Neanderthal Lifeways: Subsistence Rosas A., Martínez-Maza C., Bastir M., García- and Technology, pp. 25 - 41. Kluwer, Dordrecht. Tabernero A., Lalueza-Fox C., Huguet R., Ortiz Vallois H.V. 1954. Neanderthals and presapiens. J.E., Julià R., Soler V. & de Torres T. 2006. J. R. Anthropol. Inst., 84:111–130. Paleobiology and comparative morphology of a late Virchow R. 1872. Untersuchung des Neanderthal- Neandertal sample from El Sidron, Asturias, Spain. Schädels. Z. Ethnol., 4:157–165. Proc. Natl. Acad. Sci. U.S.A., 103:19266-19271. Voisin J.L. 2006. Speciation by distance and tem- Sergi S. 1948. Il crania del secondo paleanthro- poral overlap: a new approach to understanding po de Saccopastore. Paleontolographia Italica, Neanderthal evolution. In Hublin J.-J., Harvati K. 42:25–164. & Harrison T. (eds): Neanderthals revisited: new ap- Sergi S. 1948. Craniometria e craniografia del proaches and perspectives, pp. 299-314. Dordrecht. primo paleantropo di Saccopastore. Atti Accad. Weckler J.E. 1954. The Relationships Between Naz. Lincei, 5:1–59. Neanderthal Man and Homo sapiens. Am. Serre D., Langaney A., Chech M., Teschler-Nicola Anthropol., 56:1003–1025. M., Paunovic M., Mennecier P., Hofreiter M., Weidenreich F. 1928. Entwicklungs- und Rassentypen Possnert G. & Pääbo S. 2004. No evidence of des Homo primigenius. Natur und Museum, 58. Neandertal mtDNA contribution to early mod- Weidenreich F. 1940. Some Problems Dealing ern humans. PLoS Biol., 2:0313–0317. with Ancient Man. Am. Anthropol., 42:375-383. J. HawksJ. Hawks 97

Weidenreich F. 1943. The “Neanderthal Man” Edge of the Pleistocene World. J. World Prehist., and the ancestors of Homo sapiens. Am. 24:25 - 97. Anthropol., 45:39–48. Wolpoff M.H. & Lee S.-H. 2001. The Late Weinert H. 1936. Der Urmenschenschädel von Pleistocene human species of Israel. Bull. Mém. Steinheim. Z. Morphol. Anthropol., 35:413–518. Soc. Anthropol. Paris, 13:291-310. White M.J. 2006. Things to do in Doggerland Yang M.A., Malaspinas A.-S., Durand E.Y. & when you’re dead: surviving OIS3 at the north- Slatkin M. 2012. Ancient structure in Africa un- western-most fringe of Middle Palaeolithic likely to explain Neanderthal and non-African Europe. World Archaeol., 38:547 - 575. genetic similarity. Mol. Biol. Evol., 29:2987-95. White M.J. & Pettitt P.B. 2011. The British Late Middle Palaeolithic: An Interpretative Synthesis of Neanderthal Occupation at the Northwestern Editor, Giovanni Destro Bisol

www.isita-org.com