Dynamics of genetic and morphological variability within Neandertals

Genetic evidence from Neandertals may reflect complex population dynamics that a hundred years of morphological comparisons have barely hinted. Neandertal mtDNA and nuclear genomes show that there may have been large population movements and flows across their European and central Asian range. One provocative finding suggests that early European Neandertals such as those from Krapina and Saccopastore may have had little genetic input into later Neandertal populations of Europe because of migration from central Asia Dalen:2012.

Following long precedent, I consider Neandertals as an ancient human population extending across Europe and parts of West and Central Asia between approximately 200,000 and 30,000 years ago. The definition oversimplifies. It excludes skeletal samples before 200,000 years ago that display clear anatomical similarities with later Neandertals, even if individual specimens may not possess a full suite of Neandertal-like characteristics. It also excludes people of Upper Paleolithic Europe who followed the Neandertals, and who also share some of their characteristics. As we now understand, most living people share a fraction of Neandertal genes Green:draft:2010. Most important, the definition oversimplifies by neglecting the morphological diversity across the geographic range it encompasses.

A look within the core European and Asian range of Neandertals finds great diversity and differentiation. Cranial and postcranial anatomy mark regional differences between Neandertals from Europe and southwest Asia. The southwest Asian Neandertals are outside the anatomical range of European Neandertals for many characteristics, and cannot be easily differentiated from modern humans in that area Wolpoff:Lee:2001. Early European Neandertals, chiefly from Krapina and Saccopastore, are morphologically different from most later Neandertals in Europe. Individual specimens far from the Europe or West Asia also share Neandertal similarities, suggestive of gene flow or shared ancestry over a much broader space.

Putting morphology and genetics together will allow us to build a synthetic view of Neandertal population dynamics. In some instances, the current genetic evidence suggests events that cannot be corroborated by morphological evidence. Far from a unitary group evolving in isolated glacial conditions, the Neandertals appear to have been a highly dynamic population with the potential for rapid migration and long-distance dispersal. This perspective adds context to the archaeological record of Middle Paleolithic and initial Upper Paleolithic cultural changes.

The context of Neandertal morphological variation

It has been common for anthropologists to emphasize the unity of Neandertal morphology, instead of its diversity. There have been two reasons for this emphasis in recent years. First, a paramount problem in European prehistory is to identify the biological makers of the earliest Upper Paleolithic industries Bailey:Aurignacian:2009. Only a small number of skeletal remains have been identified in association with terminal Middle and initial Upper Paleolithic assemblages, nearly all fragmentary. In this context, identifying whether a specimen is “Neandertal” or “modern” can may depend very strongly on a single trait. By decomposing Neandertal identity into the morphology of an individual trait, Neandertals are made to look more morphologically homogeneous than if many traits could be considered together.

The second reason for emphasizing Neandertal morphological unity has been the assumption that long isolation might explain the evolution of their distinctive traits. This idea can be traced to Howell Howell:1952 who introduced the hypothesis that isolation in glacial Europe gave rise to divergent morphological trends in the Late Pleistocene populations of Europe and West Asia. Other workers followed this concept with related models. Hublin Hublin:1998 suggested that long isolation of Neandertals could explain the evolution of their morphological pattern by genetic drift and local selection, both of which would predict a reduction in the variability of this population. The strength of this explanation was that it provided an explanation for the mosaic appearance of Neandertal traits over time within Middle Pleistocene Europeans Stringer:Hublin:1999. However, even strong genetic drift need not reduce the variability of a population, and in fact morphological variability in Europe did not decrease for most Neandertal traits accretion.

These two concerns are interrelated. Both rest on an assumption that Neandertal populations were relatively static, and could have changed only very slowly. This assumption can be defended in terms of paleoenvironment and cultural dynamics. European Neandertals lived recurrently, if not continuously, in periglacial conditions. Changes in culture, as evidenced by archaeological industries, initially proceeded very slowly, and began to exhibit greater regional diversity and temporal turnover only toward the end of the Neandertals’ existence. Their unique anatomical configuration emerged within this context. What could be more natural than to assume that the forces of selection and drift had slowly driven them to greater and greater anatomical specialization within this unique environment?

Yet, our current understanding of the Neandertals shows that they did not experience a slow, plodding march toward anatomical specialization. With more discoveries from extreme eastern Europe and central Asia, it seems that the center of Neandertal evolution may not have been Europe at all. The anatomical record of western Europe lay at one geographic end of a broad distribution, and the few specimens of Neandertals from central Asia show intriguing differences from Neandertals in the west Glantz:2009.

If rapid evolution of earlier Neandertals were possible, then we would not need a long history of isolation to explain Neandertal morphology. If rapid evolution of the latest Neandertals were possible, we would not assume that late Middle and early Upper Paleolithic specimens must either represent earlier Neandertal or later modern populations; they could just as easily be a variable anatomical mixture of these.

We can adopt a more nuanced view of the diversity within and among Neandertal populations. The main impediment to understanding Neandertal diversity is the limit on the skeletal record. The Neandertals are the best-known of any human population before 40,000 years ago. However, even with hundreds of known specimens, only a few individuals represent any single part of Neandertal anatomy. Today we can talk about the diversity of Neandertals only at the broadest regional scale.

A history of Neandertal diversity

An examination of the history of the Neandertal problem adds perspective on how our understanding their morphological diversity can continue to advance. At the beginning, Neandertal “diversity” was defined mostly in terms of their difference from humans and other fossil (or purported fossil) specimens. The initial Neandertal discoveries were specimens from the later part of the Neandertals’ existence. First to be recognized was Feldhofer, then Forbes Quarry and Engis (both discovered earlier), Spy and later the classic French specimens from La Ferrassie Peyrony:Capitan:1909 and La Chapelle-aux-Saints Boule:1911a. Only these last were recovered at a time when the morphology of earlier Neandertals, represented at Krapina, had been described Gorjanovic-Kramberger:1906a. Specimens later recognized as intermediate between modern and Neandertal extremes were discovered relatively late in the process.

After the first descriptions of Neandertals, some anatomists attempted to accommodate them within human variability by extrapolating from the anatomical patterns of developmental abnormalaties or rare morphological correlates of disease. Rudolf Virchow asserted that the Neandertal skeleton was rachitic Virchow:1872, while J. Barnard Davis maintained that the Neandertal skull presented an extreme case of synostosis, accounting for its elongated shape and complete suture closure. In the view of these anatomists, the Neandertals presented a logical extreme of morphological tendencies already known in contemporary people, allowing their anatomy to be brought within the compass of morphological “laws.” Humans to be compared with Neandertals were pathological variants within populations, not members of very different populations.

By contrast, others attempted to place Neandertals by considering the gradations among human racial groups. For example, Huxley Huxley:1864 suggested that human variation was so great that “it is possible to select a series which shall lead by insensible gradations from the Neanderthal skull up to the most ordinary forms”. Quatrefages and Hamy Quatrefages:Hamy:1882 put the Neandertal skull as part of a primitive race of humans. The recovery of earlier Neandertals, from the Riss-Würm interglacial and earlier, ultimately showed the anatomical continuity between Neandertals and more ancient human populations.

Yet, several discoveries from the early twentieth century distracted many anthropologists by appearing to support the argument for an ancient, much more modern “presapiens” form in Europe. Today we appreciate that the supposedly early fossil sample included specimens of questionable or much later provenance, such as Fontéchevade and the infamous Piltdown skull. These did not entirely explain the Presapiens idea, however, which emerged from the alignment of specimens on a morphological axis from modern to Neandertal extremes. For example, Vallois argued that specimens lacking specific Neandertal characters must therefore represent a distinct group with a phyletic connection to modern humans Vallois:1954. Weidenreich did not accept a presapiens population as specifically distinct from Neandertals, but did categorize samples as Homo sapiens based on the absence of Neandertal characteristic morphology irrespective of date (e.g., Swanscombe grouped with Skhul as “H. sapiens intermediate” Weidenreich:problems:1940. McCown and Keith McCown:1939 described the Neandertal similarities within the sample from Skhul and Tabun as representing a population evolving from a more modern to a more specialized type. These examples illustrate a slow trend toward acceptance two propositions about the evolution of Neandertals and modern humans: “Modern” morphological traits may in many cases be primitive, while the morphological traits of Neandertals may in many cases be derived, or “specialized”.

Neandertal variation and "varieties"

Howell Howell:1957 discussed the variation of Neandertals by describing three varieties. His summary helped to crystallize the description of Neandertal change over time and variation across space. The varieties were:

“Early Neandertals”. This group included Krapina, Saccopastore and Ehringsdorf. Howell additionally mentioned several Asian specimens, including those from Tabun, Zuttiyeh and Teshik-Tash, without explicitly assigning them to this group. Howell distinguished the early Neandertals from classic Neandertals by eight cranial features, largely associated with smaller and more compact vaults and less midfacial prognathism. He also claimed the postcranial skeleton of this early Neandertal sample to be “more anatomically modern” than that of later Neandertals.

“Classic Neandertals”. This group included most of the well-known remains from the Würm glaciation in Europe. Howell characterized this set by cranial features, acknowledging that the sample of Early Neandertal postcrania was not sufficiently numerous to make clear statements about differences with the classic Neandertals. He also pointed out that this set of specimens were known exclusively from southwestern Europe, from western Germany and Italy on the eastern tier.

“Southwest Asian Neandertals”. This group included the entire known fossil record of the region, including Skhul, Tabun, Zuttiyeh, Qafzeh and Shanidar. Howell noted the divergent opinions of anthropologists about the evolutionary scenario that generated this sample. He offered the opinion that the initial population of the Levant represented by Tabun had affinities with Early Neandertal people, and that the region had undergone a trend of “sapiensization” explaining the Skhul sample.

Howell identified these varieties of Neandertals to clarify his position on the Neandertal ancestry of recent humans. In his view, several previous authors had been too categorical in their insistence that Neandertals could not have been ancestors of modern peoples. He allowed that the classic Neandertals may have been too specialized to have given rise to later populations within Europe. But the early Neandertals were less anatomically specialized and may have been ancestral to modern humans in some other, non-European, region. Moreover, the Southwest Asian Neandertals appeared to provide evidence of an evolutionary trend toward modern humans.

These groupings have in later years been widely repeated. The differences between classic Neandertals and early Neandertals, such as the Krapina and Saccopastore samples, has repeatedly been observed, as reviewed by Hawks and Wolpoff accretion. The distinction between early and classic Neandertals emerged from the work of Gorjanovic-Kramberger Gorjanovic-Kramberger:1906a, Weidenreich Weidenreich:1928, Weidenreich:1943, Weinert Weinert:1936 and Sergi Sergi:1948a.

Howell’s “Southwest Asian Neandertal” sample deserves further comment. At the time he wrote, McCown and Keith’s description of the Skhul and Tabun remains McCown:1939 had grouped these as representing a single population, anatomically intermediate between classic Neandertals and modern humans. Howell advocated this combined sample as a single population. Some recent authors have followed this position Arensburg:1998, Kidder:1992, Kramer:1999

Thus, although they served an important role in the history of anthropology, Howell’s categories have not been universally accepted. I note them here to consider how the discussion of Neandertal variability emerged during the last 50 years. Today, as we consider paleogenetic evidence, these categories have very little ability to inform us about the relation between morphological and genetic information. Early Neandertals as discussed above have not yet produced any genetic data, except for the Teshik-Tash specimen. None of Howell’s Southwest Asian Neandertals are represented by sequence data to date, regardless of their morphological interpretation. New Neandertal specimens from central Asia and extreme eastern Europe have provided an unexpected trove of genetic information, although with the exception of Teshik-Tash they have never figured strongly in the discussion of morphological diversity within Neandertals. All of the remaining genetic data come from Howell’s classic Neandertals, the set within which previous morphological studies have least attempted to explain variability. In other words, genetic data require us to redefine historical conceptions of Neandertal groupings and variability.

Paleogenetics

The data from paleogenetics of Neandertals have rapidly changed during the past few years. As a result, descriptions of the state of the evidence from as recently as 2005 are now obsolete. In that time, the synthesis of Neandertal DNA evidence has proceeded from a very simple model to one involving more complicated population interactions and movements. No known living people have mtDNA sequences that belong to the clade shared by all known Neandertals. Initially, this fact strongly influenced many researchers to believe that Neandertals had become extinct without issue (e.g., Serre:2004, Currat:2004. Later, the sequencing of nuclear genomes of Neandertals demonstrated that a fraction of the ancestry of living non-Africans can be traced to these ancient people Green:draft:2010. This simple question provides the beginning of our understanding of genetic diversity within Neandertals. We can use samples from different Neandertal individuals, as well as the genetic material they share with some living people, to test hypotheses about the population structure and dynamics of Neandertal populations.

The complete mitochondrial genomes of more than a dozen Neandertals have been described and small fractions of the mitochondrial sequences are known for many more. These extend from as far east as Okladikov Cave in the low Altai, and as far west as El Sidrón in Spain, encompassing nearly the entire east-west range known for the Neandertals. The north-south extent of data is much more restricted, as none of the sites from present-day Israel or Iraq have yielded genetic evidence. In addition to the mtDNA, three Neandertals from Vindija are represented by substantial sequencing of the nuclear genome, averaging nearly 1x coverage for each of them. Much smaller fractions of the nuclear genome have been recovered from Neandertal specimens from Feldhofer Cave, El Sidrón, and Mezmaiskaya.

Mitochondrial genomes show that the Neandertal population was far from static across the time of its existence. As a general observation, Neandertal mtDNA diversity is less than is present among humans worldwide, with a common ancestor estimated for Neandertal mtDNA sequences only a little before 110,000 years ago Lalueza-Fox:issues:2012. Late Neandertals in peninsular Europe, including three Vindija specimens and two each from Feldhofer and El Sidrón, form a tight mtDNA clade with an ancestor as recent as 60,000 years ago Dalen:2012. For the current discussion, I will term this set as the “late western Neandertals”. By contrast, some earlier European and central Asian Neandertals belong to an mtDNA genealogical tree nearly twice as deeply rooted. These include western European specimens such as Valdegoba and Scladina, as well as Neandertals from the very far east, such as Okladnikov and Teshik-Tash. What seems to unite the earlier Neandertals is time, rather than space Dalen:2012. Mezmaiskaya and Monte Lessini (from the Caucasus and Italy, respectively) belong to mtDNA branches that cluster with the late western Neandertals. Dalén and colleagues hypothesize a movement of eastern Neandertals into the west sometime around 50,000 years ago, resulting in a partial replacement of western Neandertals.

Neither geography nor time considered alone are sufficient to explain the grouping of the later, western subset of Neandertals into a tight mtDNA genealogical arrangement. One possible explanation is a movement of Neandertals from the eastern to western part of their range sometime after the origin of this clade, some 60,000 years ago. This movement would have to have replaced a large fraction of the mtDNA gene pool of earlier Neandertals in western Europe; otherwise, clades shared by earlier Neandertals such as Scladina would still be found among the later Neandertals. The replacement of earlier, more diverse mtDNA clades would be easier if the effective number of Neandertals in western Europe was very small. A small effective size does not necessarily imply a very small census population size Hawks:effective:2008, and might point to a way to uncover population dynamics of this population, as discussed below.

Nuclear DNA variation among Neandertals is very limited compared to that found in living human populations. By using the genome of the Denisova specimen as an outgroup, Reich and colleagues Reich:Denisova:2010 showed that the variation across the Neandertal geographic range, from Mezmaiskaya to El Sidrón, is very low compared to the variation within humans today, or between Neandertals and the Denisova genome. They interpreted this low variation within Neandertals as evidence for a bottleneck in the population history of Neandertal groups. The nuclear genetic sequences available, from Vindija, Feldhofer, Mezmaiskaya and El Sidrón, are a broader group than the “late western Neandertals” discussed above with low mtDNA variation, because of the addition of Mezmaiskaya. The most striking use of the mtDNA data from Dalen and colleagues Dalen:2012 is to note just how unrepresentative the nuclear DNA sample from Vindija, El Sidrón, Mezmaiskaya and Feldhofer actually is. These six specimens represent only a single small clade of the Neandertal mtDNA genealogy. Nuclear genetic sampling of a broader range of Neandertals might uncover substantially more variation.

The reduced variation of nuclear and mtDNA in the late western Neandertals reflects high genetic drift in this component of the Neandertal population. Genetic drift may reflect many different demographic phenomena, including small population size, recurrent movement, extinction and recolonization of small subpopulations, or selection-migration interaction. We do not have nuclear genetic data from earlier Neandertals, and so we cannot directly test the hypothesis of a population bottleneck in the classic or later Neandertals.

The discussion of genetic diversity among these Neandertals has not yet attempted to reconcile their genealogical arrangement with morphological classification schemes. The set of “late western Neandertals” known to share a close mtDNA genealogical connection (Vindija-Feldhofer-El Sidrón) is not synonymous with “classic Neandertals”. The well-known classic Neandertals include specimens such as La Chapelle-aux-Saints, La Ferrassie 1, Monte Circeo 1 (Guattari) as well as Feldhofer (Neandertal) 1. This classic Neandertal sample stretches across a substantial span of time. Most important, the classic Neandertals flank both the earlier and later sides of the 50,000-year-ago event proposed by Dalen and colleagues Dalen:2012. The two Vindija mtDNA sequences included by Dalén and colleagues Dalen:2012 are both from layer G3 of the site, perhaps 40,000 years old, and both are derived from postcranial fragments without diagnostic morphological traits. Even so, the other material from G3 include cranial, mandibular and dental remains that are not synonymous with classic Neandertal morphology Ahern:2004. These late Neandertals from Vindija display less pronounced morphology or lacking traits that are common in the earlier classic Neandertals Smith:trends:1982. If these can be lumped together in mtDNA and nuclear DNA diversity with the remains from El Sidrón and Feldhofer, it seems possible that traditional morphological groupings will fail to capture real biological differences among Neandertal populations.

Two avenues of evidence will provide more insights about Neandertal population dynamics. Obviously, uncovering more nuclear genomes from Neandertals or early Upper Paleolithic humans would advance our knowledge greatly. Tempering this expectation is that the later western Neandertals, with lower genetic diversity, are the ones most likely to provide more genetic data. Earlier Neandertals, and the Neandertals from central Asia, would be most useful to uncover new knowledge about the population dynamics of this ancient group. A second source of evidence may come from the introgression of Neandertal genes into later human populations. As we begin to uncover the genes in living people that came from Neandertals, we face the possibility that these genes may represent different ancient Neandertal groups to greater or lesser degrees. The initial work on Neandertal genetics suggested that most of the population mixture with Neandertals may have happened in west Asia Green:draft:2010. That would suggest that European Neandertals are themselves somewhat genetically distinct from the population that gave rise to most Neandertal genes in recent populations. Comparing different Neandertals with each other will help us uncover the structure of the population that gave rise to Neandertal ancestry in living people. By doing so, we may gain an additional genetic probe into the period before 60,000 years ago, as Neandertal populations had differentiated before the large-scale encounters with dispersing people from Africa.

Population dynamics

From the Altai to Spain, the known geographic range of Neandertals covered more than 7000 kilometers east to west. At least intermittently, this population occupied more than 30 degrees of latitude, as far north as Byzovaya Slimak:2011 and as far south as the Levant. The excursions of Late Mousterian people north of the Arctic Circle suggest that the Neandertals rapidly colonized new regions when they became suitable for habitation. The paleoecological reconstruction of Mousterian sites encompasses almost the entire range of European ecological contexts, except for Alpine and Arctic biomes Banks:2008. Although the European climatic conditions oscillated considerably during the Late Pleistocene, the Neandertals seem likely to have been capable of adapting to changing conditions, either by tracking ecotones as climate shifted or by changing their subsistence strategies to meet new requirements. In other words, the archaeological record by itself is sufficient to show us that Neandertal populations were highly dynamic in areas where habitation was possible only during intermittent climatic periods.

Across northwestern Europe, from Britain to Poland, an area of more than a million square kilometers was abandoned by Neandertals during the early stages of the last glaciation and not reinhabited until after approximately 60,000 years ago. The intermittent occupation of these parts of Europe was likely not a function of “habitat tracking” by Neandertals, but instead a record of regional expansions and partial extinctions when climatic conditions deteriorated Hublin:Roebroeks:2009. White and Pettitt White:Pettitt:2011 suggest a very small Neandertal population size in northwestern Europe during the late Middle Paleolithic, and consider the possibility that the occupation of Britain was maintained as seasonal hunting camps rather than permanent settlement. This kind of occupation would put movements of several hundred kilometers into the ordinary behavioral pattern of individual Neandertals. At an extreme, the survival of Neandertals on the northwestern tier of Europe may have been precarious White:doggerland:2006. From the perspective of population dynamics, this does not suggest a dense, stable population, but instead one of great mobility and repeated ability to colonize and exploit new opportunities.

Earlier anthropologists also suggested that the Neandertal population had been dynamic in its potential for dispersal and movement. Most such suggestions centered around the role of the Pleistocene glaciations as an impetus for migration and recurrent isolation. For Howell Howell:1952, glacial cycles provided the isolation that enabled classic Neandertals to evolve their specialized anatomy. Weckler Weckler:1954 argued that isolation was one consequence of glaciations, but that long-distance migrations and recolonizations of formerly periglacial habitat was an important cause of population change in Neandertals and the modern humans who encountered them.

Genetics now leads us to a picture of a highly dynamic Neandertal population. This should not be a surprise in the context of the archaeological record, which shows abundant evidence for regional-scale population movement and rapid changes to cultures and adaptive strategies. But it is not clear that the genetic and archaeological data actually converge on a single picture of population dynamics.

A close look at a single archaeological example helps to demonstrate this point. The Quina Mousterian in southwestern France appears to represent a regional Neandertal adaptive pattern. As climate conditions gave rise to a mix of steppe and boreal forest, Neandertals specialized on reindeer, and to a lesser extent horse, replacing an earlier strategy using a broader mix of large fauna. The accompanying toolkit has been recovered from many sites in the region, consistently overlying earlier Denticulate and Typical Mousterian assemblages Guerin:2012.

As we consider this kind of technical transition, it is not obvious how the earlier and later Neandertals of southwestern France were related to each other. The transition in this area, around 60,000 years ago, is a temporal boundary between traditions that each lasted for thousands of years. Certainly it is possible that the earlier population underwent cultural adaptive evolution, suiting it better to the changing ecology, and resulting in the later cultural tradition. But it is also possible that ideas and people spread together, as the more effective cultural strategies of northern Neandertals enabled them to make incursions into the territory further to the south. Long-term Pleistocene climate changes may have provided the impetus for both interaction and conflict.

Cultural change and spatial dispersal were likely interlinked. An effective faunal procurement strategy may open up habitat that earlier Neandertals had less success exploiting. The colder parts of Germany seem to have seen the spread of reindeer hunters during MIS 4, in an occupation that may have been thin on the ground but potentially occupied a broad area Uthmeier:2011. As different Neandertal groups used different adaptive strategies, some would have expanded in range, sometimes into new previously unoccupied territory but often into territories formerly occupied by groups with different cultural strategies. Could northern Neandertal reindeer hunters have followed their herds right down into the heartland of France, as conditions grew colder, replacing their cousins to the south?

Despite the evidence for cultural change, as far as we know the morphological variation across this cultural transition was continuous. Before 60,000 years ago, southwestern France was inhabited by people we call classic Neandertals. Skeletal associations with Quina Mousterian, for example from Les Pradelles Mussini:2011 and Combe Grenal, present no obvious appearance of morphological discontinuity with other classic Neandertals. Condemi and colleagues Condemi:Rhone:2010 considered the dental sample from the Rhône valley of southeastern France, including the well-known classic and late Neandertal sites of Hortus, Tournal and Le Portel and the older sites of Genay and Payre. Their comparisons were necessarily limited but showed a lack of regional differentiation between this set of Neandertals and the remainder of the Neandertal sample from across Europe. Within Spain, Rosas and colleagues Rosas:ElSidron:2006 described the mandibular remains from El Sidrón, including them in several comparisons of regional samples of Neandertals. They found evidence for a significant difference in mandibular morphology between “northern” and “southern” samples, which they attribute to a smaller dentition and degree of midfacial prognathism in the southern sample.

In short, morphological comparisons across the relevant time span in France and Spain are insufficient to support the hypothesis of a large-scale migration bringing in a new mtDNA type. Yet it is difficult to imagine that a widespread movement of Neandertals could reach northern Spain by around 50,000 years ago without passing through southwestern France or affecting the skeletal sample of Spain. Possibly the very small sample of physical remains will simply be insufficient to test hypotheses of population dynamics on this scale.

We cannot consider Neandertal population dynamics without discussing the probable effects of low population size on their distribution. The estimation of population numbers from archaeological site densities is imprecise with many sources of error. Nevertheless, some estimates of the total number of Neandertals representing traditions such as the Mousterian of Acheulean Tradition (MTA) are as low as a few hundred individuals total Richter:2006. Across peninsular Europe, there may have been fewer than 10,000 Neandertals living at any given time, an indication of the census population size. Certainly, the genetic variation of Neandertals is consistent with a very small effective population size. Many factors reduce genetic variation relative to census population size Hawks:effective:2008, including two of particular relevance to Neandertal population structure: Extinction and recolonization of groups Eller:2004, and broader regional-scale cultural replacement in the presence of selection Premo:Hublin:2009. Such small groups and regional populations would have very little genetic “inertia” against the long-term effect of gene flow. Genetic continuity in this scenario could never persist for long against even a moderate amount of immigration acting over many generations.

If the Neandertals of southwestern France, for example, were fewer than 1000 individuals, how could they have maintained identifiable traditions of stone technology for thousands of years? If their gene pool was constantly in flux due to immigration and long-distance movement of individuals, how could their cultures not have rapidly changed beyond recognition? In this scenario it seems necessary to assume very strong reinforcement of technology by learning biases, probably mediated by the observed utility of stone tool choices within the local ecology Henrich:2001. Learning and cognition may fundamental supports for a dynamic Neandertal population, enabling their persistence in a tenuous paleoclimatic regime.

Conclusion

The genetic data force us to adopt a new stance on the nature of Neandertal populations. A long, slow evolution of Neandertal populations cannot account for the evidence of long-distance interactions and movement on relatively short time scales. The archaeological record may be a more sensitive indicator of regional-scale changes than the morphological record of skeletal biology. Archaeology also gives us insight into the ways the Neandertals maintained their population in the face of regional movements and logistical strategies may have involved temporary summer occupations at some distance from their core territories.

The redefinition of Neandertal population groupings should begin immediately. We may soon have genetic data from many more Neandertal specimens. Given the unexpected finding of diversity from the Denisova specimen Reich:Denisova:2010, it is possible that some other Asian “Neandertal” populations will turn out to represent equally divergent human populations. We should not too readily assume that Shanidar, or Skhul, or Amud, for example, will lie within the known pattern of Neandertal genetic variability. What we now know is that the traditional category of “classic” Neandertals is insufficient to describe the genetic variability and dynamics of Late Pleistocene Europeans. Obviously we must proceed much further with the comparison of physical remains before we will be able to test any connections between cultural and biological transitions within Neandertals.