Illinois State University ISU ReD: Research and eData
Theses and Dissertations
5-30-2014
The Effects Of Cold Adaptation On The Growth And Development Of The Neandertal Cranial Base
Sarah Caldwell Illinois State University, [email protected]
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Recommended Citation Caldwell, Sarah, "The Effects Of Cold Adaptation On The Growth And Development Of The Neandertal Cranial Base" (2014). Theses and Dissertations. 195. https://ir.library.illinoisstate.edu/etd/195
This Thesis is brought to you for free and open access by ISU ReD: Research and eData. It has been accepted for inclusion in Theses and Dissertations by an authorized administrator of ISU ReD: Research and eData. For more information, please contact [email protected]. THE EFFECTS OF COLD ADAPTATION ON THE GROWTH AND
DEVELOPMENT OF THE NEANDERTAL
CRANIAL BASE
Sarah J. Caldwell
92 Pages August 2014
Neandertals and modern humans possess very different craniofacial shapes. Some recent work has attributed these contrasting shapes specifically to differences in brain development, which are extrapolated to mean differences in cognitive function. However, this may not necessarily be the case. In this paper, it is suggested that a size increase in the cranial base and rapid cranial growth are due not to cognitive differences, but environmental factors, specifically Neandertal adaptation to cold. Adaptation to cold would not only explain the more rapid growth of the Neandertal cranium, but also elongation of the cranial base via elongation of the nasopharynx for maximizing air conditioning capabilities.
The results indicate a closer relationship between Neandertals and cold-adapted modern humans than either of these groups with the other two considered (early modern humans and warm-adapted modern humans). While all variables in the cranium are correlated to some degree, cranial base length is most strongly correlated with measures of facial projection. This indicates that, along with some other factors, elongation of the cranial base greatly affects projection of the face; this could be caused via elongation of the nasopharynx due to cold-adaptation. Cold adaptation early in Neandertal children would have prepared them for the harsh environment that they are born and raised in, allowing for a higher chance of survival in a harsher environment. Thus, environmental factors are considered a valid argument for the differing shapes and developmental trajectories of Neandertals and modern humans. THE EFFECTS OF COLD ADAPTATION ON THE GROWTH AND
DEVELOPMENT OF THE NEANDERTAL
CRANIAL BASE
SARAH J. CALDWELL
A Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of
MASTER OF SCIENCE
Department of Sociology and Anthropology
ILLINOIS STATE UNIVERSITY
2014 Copyright 2014 Sarah J. Caldwell THE EFFECTS OF COLD ADAPTATION ON THE GROWTH AND
DEVELOPMENT OF THE NEANDERTAL
CRANIAL BASE
SARAH J. CALDWELL
COMMITTEE MEMBERS:
Fred H. Smith, Chair
Maria O. Smith ACKNOWLEDGMENTS
I would be lying if I said that writing a thesis was my favorite past time, though I also would not be giving the endeavor enough credit if I said that I wasn’t extremely grateful to have had the opportunity to do so. My biggest thanks can go to none other than Dr. Fred Smith, my advisor and chair, for taking a chance on me and for his guidance, which has been truly invaluable. I don’t think I could have asked for a better graduate mentor. Dr. Maria Smith also deserves my sincerest thanks for her never ending willingness to discuss all manner of things scientific, her assistance, and constant encouragement. Dr. Steven Juliano has been an incredible help with the statistics that I legitimately could not have performed or interpreted without his guidance. And finally, my undergraduate advisor, Dr. Don Gaff, also deserves my appreciation. I was no longer his responsibility and he still proofread everything I sent to him with minimal resistance.
I also cannot conclude without thanking my friends who tolerated my obsessiveness and encouraged me without hesitation. My most heartfelt thanks go to Rob
Lewis, Kayla Yario, Dan Dawson, and Jamie Thomas. I also must thank my fellow graduate students who experienced/suffered through/reveled in this experience with me:
Deb Neidich, Katie Lacy, Ian Fricker, Cori Rich, Alison Hodges, Ian Fricker, Jeff
Painter, Sarah Boncal, Andrew Mallo and Scott Drapalik.
S. J. C.
i
CONTENTS
Page
AKNOWLEDGMENTS i
CONTENTS ii
TABLES iv
FIGURES vi
CHAPTER
I. INTRODUCTION 1
II. REVIEW OF RELATED LITERATURE 3
Introduction to Neandertals 3 Integration of the Cranium 11 Structure of the Cranial Base 12 Ontogeny of the Basicranium 13 Structure of the Splanchnocranium 15 Ontogeny of the Splanchnocranium 16 Interactions between the Cranial Base and the Face 17 Evidence of Cold Adaptation in the Cranium 17
III. MATERIALS 21
IV. METHODS 24
Cranial Measurements 24 Statistical Methods 26
V. RESULTS 30
ii
Mean Values for Cranial Measurements 30 Pearson Correlations 35 Canonical Output for Cold Group vs. Warm Group 37 Canonical Output for Cold Group vs. Neandertals 38 Canonical Output for Warm Group vs. Neandertals 40 Canonical Output for Neandertals vs. Early Modern Humans 42 Canonical Output for Cold Modern vs. Early Modern Humans 43 Canonical Output for Warm Modern vs. Early Modern Humans 44 Canonical Output for All Modern Humans vs. Archaic Humans 45 Canonical Output for All Humans vs. Neandertals 46 Contrasts 47
VI. SUMMARY 52
VII. DISCUSSION 54
Neurocranial Dimensions 54 Splanchnocranial Developments 57 Neandertal Upper Respiratory Tract 62 Neandertal Growth 64 Splanchnocranial Growth 65 Neurocranial Growth 67
VIII. CONCLUSIONS 69
REFERENCES 73
iii
TABLES
Table Page
1. Samples Chosen from W.W. Howells Collection 22
2. Adult Neandertals 22
3. Adult Anatomically/ Early Modern Humans 23
4. Means, Standard Error, and Range for Cranial Base Length 30
5. Means, Standard Error, and Range for Cranial Breadth 31
6. Means, Standard Error, and Range for Cranial Height 32
7. Means, Standard Error, and Range for Facial Projection 33
8. Means, Standard Error, and Range for Facial Height 34
9. Neandertal Cranial Correlations 35
10. Early Modern Human Cranial Correlations 36
11. Cold-Adapted Modern Human Cranial Correlations 36
12. Warm-Adapted Modern Human Cranial Correlations 36
13. MANOVA Test Criteria: Cold-Adapted MH vs. Warm-Adapted MH 37
14. Canonical Coefficients for Cold-Adapted MH vs. Warm-Adapted MH 38
15. MANOVA Test Criteria: Cold-Adapted MH vs. Neandertals 39
16. Canonical Coefficients for Cold-Adapted MH vs. Neandertals 39
17. MANOVA Test Criteria: Warm-Adapted MH vs. Neandertals 40
18. Canonical Coefficients for Warm-Adapted MH vs. Neandertals 41
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19. MANOVA Test Criteria: Neandertals vs. Early MH 42
20. Canonical Coefficients for Neandertals vs. Early MH 42
21. MANOVA Test Criteria: Cold-Adapted MH vs. Early MH 43
22. MANOVA Test Criteria: Warm-Adapted MH vs. Early MH 44
23. Canonical Coefficients for Warm-Adapted MH vs. Early MH 44
24. MANOVA Test Criteria: Modern Humans vs. Archaic Humans 45
25. Canonical Coefficients for Modern Humans vs. Archaic Humans 46
26. MANOVA Test Criteria: Humans vs. Neandertals 46
27. Canonical Coefficients for Humans vs. Neandertals 47
28. Contrasts with Dependent Variable – log Cranial Base Length 47
29. Contrasts with Dependent Variable – log Cranial Height 48
30. Contrasts with Dependent Variable – log Cranial Breadth 49
31. Contrasts with Dependent Variable – log Facial Projection 50
32. Contrasts with Dependent Variable – log Facial Height 51
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FIGURES
Figure Page
1. Cranial Base Anatomy 1
2. Neandertal and Modern Human Cranial Comparison 6
3. Cranial Base Flexure and Synchondroses Location 13
4. Cranial Measurements 25
5. LSMeans for Cranial Base Length 31
6. LSMeans for Cranial Breadth 32
7. LSMeans for Cranial Height 33
8. LSMeans for Facial Projection 34
9. LSMeans for Facial Height 35
10. Influential Variables – Cold-Adapted MH vs. Warm-Adapted MH 38
11. Influential Variables – Cold-Adapted MH vs. Neandertals 40
12. Influential Variables – Warm-Adapted MH vs. Neandertals 41
13. Influential Variables – Early MH vs. Neandertals 43
14. Influential Variables – Early MH vs. Warm-Adapted MH 45
15. Nasopharyngeal Anatomy 61
vi
CHAPTER I
INTRODUCTION
The basicranium plays a critical, multifaceted role in cranial structure and development. It is the foundation of the skull and is composed of parts of five bones: portions of the occipital, the right and left temporal bones, the sphenoid, and the entire ethmoid (see Figure 1).
Figure 1: Cranial Base Anatomy - This figure shows the structure of the cranial base, as well as other major features. The frontal appears in pink, ethmoid in purple, the sphenoid in yellow, temporals as the paired purple bones, and the occipital is grey (OpenStax, 2013). The darkened area represents the cranial base.
1
The resulting construct connects the skull with the vertebral canal and anchors the splanchnocranium to the neurocranium. It performs many functions, including providing safe passage for cranial nerves and the brain stem and maintaining conduits for the circulation system of the brain. It is affected by, and has profound effects on, various aspects of the development of the cranium.
In Neandertals, this cranial base is elongated, especially in the anterior portion
(Smith, 1991; Trinkaus, 2003); however, what exactly this means for the development of the Neandertal cranium has not be explicitly explored. A number of explanations will be considered here, including environmental factors and differences in growth rate.
Environmental variables appear to exert significant influence over the development of certain cranial structures, especially those of the splanchnocranium (Franciscus and
Trinkaus 1988; Hernandez et al., 1997; Yokley, 2009; Noback et al., 2011; Bastir and
Rosas, 2013), which is closely related to development and function of the cranial base.
The purpose of this study is to explore the validity of cold adaptation and differences in heterochrony as factors in basicranial evolution, with reference to the relationship between anatomically modern Homo sapiens sapiens and Homo sapiens neanderthalensis.
2
CHAPTER II
REVIEW OF RELATED LITERATURE
Introduction to Neandertals
Neandertals were a group of hominins that existed in Eurasia between about 225 to 32 thousand years ago (Smith, 2013). The first Neandertal specimen to be recognized as a potential primitive human form was found in a quarry in the Neander Valley of
Germany in 1856 (Schmitz et al., 2002) and consisted of 15 pieces of postcranial skeleton and a cranial vault (Cartmill and Smith, 2009). While these bones had at one point been interpreted to belong to an extinct species of cave bear, they were later identified as human by a local teacher, J. Fuhlrott. He, along with a professor of anatomy at the University of Bonn, H. Schaaffhausen, presented the first comprehensive analysis of the skeletal material (Schmitz et al., 2002).
Early interpretations classified the bones as unequivocally human because of the large cranial capacity (Cartmill and Smith, 2009). However, the find was regarded as a primitive or barbaric form of Homo sapiens because of its brow ridges and cranial vault form (Schaaffhausen, 1858; Huxley, 1863; Schaaffhausen, 1888). Another interpretation considered it to be a pathological modern human (Virchow, 1872), but as more specimens were found, this claim was hard to maintain. The most common interpretation
3 of Neandertals arose in 1864 and considered Neandertals to be not a race of primitive modern humans, but rather a completely different species, Homo neanderthalensis (King,
1864). This idea that Neandertals represented a separate species persisted and was later supported by Schwalbe (1906) and Gorijanović-Kramberger (1906), among others.
Although it is almost ubiquitously accepted now in the 21st century that Neandertals are the closest relatives of modern humans, the question of their exact relationship still stands. Were they an evolutionary dead end, a direct linear ancestor, or is their relationship to modern humans more complicated?
There is long-standing evidence of human occupation in Europe. The oldest human remains found in Europe seem to be from the site of Sima del Elefante in Spain and are dated to the Early Pleistocene at 1.1-1.2 mya (Carbonell et al., 2008). It is unclear whether these fossils represent one million years of continuous inhabitance in Europe, or fleeting migrations of groups that either failed to permanently colonize or returned from where they came. Pre-Neandertal hominins classified as unequivocally human early in
Europe are traditionally placed within one of two taxons, Homo heidelbergensis or Homo sapiens heidelbergensis, which are colloquially referred to as Heidelbergs. The earliest solid evidence of Heidelbergs comes from the Middle Pleistocene at the site of Gran
Dolina in Atapuerca, Spain, which is dated to around 700 kya (Pares and Parez-Gonzalez,
1995; Falgueres et al., 1999). The oldest Heidelberg specimen from North Central Europe is a mandible, the Mauer mandible, which dates back to 600 kya (Wagner et al., 2010).
Other Heidelberg-type fossils have been found, mostly in Spain at the site of Sima de los
Huesos (Bischoff et al., 2007), which are dated to around 500 ky old.
4
Climate during the Early and Middle Pleistocene was highly variable and fluctuated wildly. There is evidence for up to five major cold periods during the Middle
Pleistocene that began about 640 kya, with each lasting around 100 ky (Heslop et al.,
2002; Li et al., 2008). These were marked by rapid changes from glacial to interglacial periods, with shorter, more rapid climatic oscillations within these intervals (Dennell et al., 2011). The most well-know are the Heinrich Events and the extent of these rapid changes are known from ice cores throughout the world (Heinrich, 1988; Bar-Matthews et al., 2003; Shackelton et al., 2004). Middle Pleistocene interglacials were generally very short, and the climate during this time period is considered to have been much colder in
Europe than in modern day (Dennell et al., 2011). Heidelbergs and later, Neandertals, were likely not living at the heart of the glaciers but were probably exploiting glacial refugia in the Balkans and the Iberian peninsula during this colder time (Carrion et al.,
2003; Finlayson and Carrion, 2007).
Neandertals were widely spread, from the coasts of Western Europe (Zilhão,
1998; Bicho, 2005) to the mountains of Central Europe (Trinkaus, 1987; Krause et al.,
2007). In Europe, they stretch south to Gibraltar (Dean et al., 1986; Blain et al., 2013), and north to north-central Germany and the Netherlands (Smith, 1984; Ahern et al.,
2013), but the southern-most findings of skeletal remains are at the site of Kebara in
Israel (Valladas et al., 1987; D’Anastasio et al., 2013). However, the extent of
Mousterian sites without associated Neandertal skeletal remains (d’Errico, et al. 2009;
Slimak et al., 2011) and knowledge of climatic fluctuations (Roebroeks et al., 1992) might suggest that their ranges could have been larger than what is revealed by the fossil material.
5
Temporally, “Classical” Neandertals undoubtedly existed during the last interglacial (Mellars, 1996; Janković, 2004); the specimens from the oldest part of the this period are dated to around 130-150 kya (Rink et al., 1995; Condemni, 2001).
However, there are some sites and samples that may indicate that Neandertal existence extended even further back in time, perhaps back to 200 kya (Blackwell and Schwarcz,
1986; Grün and Stringer, 1991; Guipert et al., 2007). The most recent Neandertals, based on the presence of human fossil remains, are from Central Europe (Smith et al., 1999;
Higham et al., 2006) around 32-33 kya.
Neandertals are traditionally thought to have possessed a number of features that made them distinct form modern humans. Some of these that appear in classic
Neandertals are traits such as long, low, and wide cranial vaults (Howell, 1952; Cartmill and Smith, 2009), less-flexed and elongated cranial bases (Smith, 1991; Lieberman et al.,
2000), and an occipital bun (Brose and Wolpoff, 1971; Gunz and Harvati, 2007). Despite having an overall different cranial form, Neandertals do possess some features that are similar to modern humans, such as a large cranial capacity (Tobias, 1971; Ruff et al.,
1997; Holloway, 2000).
Figure 2: Neandertal and Modern Human Cranial Comparison - This figure is a comparison between modern humans (B) and Neandertals (A) in general cranial shape; note the longer, lower cranium of the Neandertal, with an overall larger and more projecting face.
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Neandertal facial skeletons are considered to be very large in all dimensions
(Cartmill and Smith, 2009); Neandertal faces possess a large piriform aperture (Coon,
1962; Franciscus and Trinkaus, 1988), inflated paranasal sinuses (Smith and Raynard,
1980; Laitman et al., 1996), an overall larger and more prognathic face, especially in the mid-face, (Rak, 1986; Trinkaus, 1986) and more substantial supraorbital tori (Smith and
Ranyard, 1980; Russell, 1985). Their general body form is overall more robust and stout with shortened distal limb segments and stronger musculature (Howell, 1952; Cartmill and Smith, 2009).
Neandertals possessed a sophisticated toolkit that was made up of numerous types of stone tools with a much wider range of uses than toolkits before them (Hayden, 1993;
Kuhn, 1995; Roebroeks and Gamble, 1999; Dibble and McPherron, 2006). The technology associated most commonly with Neandertals is the Mousterian (Hoffecker et al., 2000; Finlayson et al., 2006). A few wooden implements have been found, including spears (Movius, 1950; Carbonell and Castro-Curel, 1992). While sophisticated bone tools were previously thought to be generally lacking during much of the Mousterian (Mellars,
1996; Münzel and Conard, 2004), more recent work has identified that the oldest bone tools found in Europe seem to be associated with Neandertals (Soressi et al., 2013). In addition, bone points have been identified from Central Europe (Monet-White, 1996) and other bone artifacts have been found in context with initial Upper Paleolithic-associated
Neandertals (Hublin et al., 1996; Karavanić and Smith, 1998; Svoboda, 2006).
Evidence of fire is found at Neandertal sites; sometimes repeatedly in the same place, indicating multiple uses of one location (Bar-Yosef et al., 1992; Rigaud et al.,
1995; Barton 2000; Schliegl et al., 2003). Within Neandertal toolkits, there is no evidence
7 of bone needles, suggesting that Neandertals were not making tailored clothing until at least the Châtelperronian (Gilligan, 2007). House-like structures are limited to one relatively sophisticated ruin associated with the Châtelperronian in France (Klein, 2003).
Neandertal toolkits, the pattern of seasonal zooarchaeological remains (Marean, 1998;
Grayson and Delpech, 2006), and some interpretations of injury patterns (Berger and
Trinkaus, 1995; Trinkaus, 2012) suggest that Neandertals were successful hunters that supplemented their diets with plant resources (Hardy, 2004; Lev et al., 2005; Henry et al.,
2011).
Neandertal language and cognitive ability is still a matter of disagreement still amongst paleoanthropologists. With identical cranial capacities (Cartmill and Smith,
2009), it seems clear that if there is a difference, it lays more in the wiring of the brain than with external structure and shape. A number of studies have examined Neandertal endocasts and based on the exterior morphology found no distinct differences in structure from that of anatomically modern humans (Holloway, 1981, 1985; Holloway et al.,
2004). Broca’s and Wernicke’s areas, which are important in speech, were also found to have no significant differences between humans and Neandertals (Holloway and de La
Coste-Lareymondie, 1982; Holloway, 1983, 1985). However, the internal structure is unable to be examined and histological examinations are impossible, leaving a plethora of questions unanswered.
It is well known that during the Upper Paleolithic in Europe modern humans were producing elaborate art (Klein, 1999, 2003; Conard, 2003). Although symbolic thought amongst Neandertals was once a point of contention amongst scholars, personal adornments and evidence of art is now relatively widely found at Neandertal sites (Zilhão
8 et al., 2009; Caron et al., 2011; Zilhão, 2011; Finlayson et al., 2012; Zilhão, 2012;
Burdukiewicz, 2014). The most easily identifiable art in context with Neandertals is from
Châtelperronian sites (Hublin et al., 1996). Although it has been argued that the
Châtelperronian was culturally appropriated from the modern human Aurignacian
(White, 2003), some argue that this cultural complex has never been temporally associated with modern humans (Zilhão et al., 2006). This suggests Neandertal- associated art was an independently developed phenomenon.
Religion or spirituality amongst Neandertals has not been established conclusively, although there is some evidence of post-mortem processing of bones
(Defleur et al., 1999; Rosas et al., 2006). However, the reason behind this is unclear.
Evidence of burial pits (Vlček, 1973; Vandermeersch, 1976; Harrold, 1980; Bar-Yosef et al., 1992; Defleur, 1993) and flexed burials indicate that some Neandertals may have been intentionally buried (Straus, 1989; Schmitz et al., 2002; Smith et al., 2006).
However, it’s not entirely clear if these burials are due to symbolic religious thought
(Defleur, 1993) or simply the necessity to dispose of a corpse (Klein, 1999).
Although Neandertals possess distinctive morphological features that define them as “different,” there are a number of Neandertal and modern human qualities that blur the line between the two supposedly separate species. Some fossil material, such as that of the child from Lagar Velho in Portugal, exhibit a mixture of traits that suggest some integration with Neandertals at some point in time, such as fundamentally human cranial form and Neandertal-like body proportions (Duarte et al., 1999; Trinkaus and Zilhão,
2002). Conversely, some human-like features are found in the possible Neandertal infant from Mezmaiskaya (Hawks and Wolpoff, 2001).
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Central Europe especially seems to be an especially popular zone of hybridization for Neandertals and modern humans. Specimens from the Czech Republic appear to be fundamentally modern in their overall form, but possess some cranial features such as hemibuns, retromolar spaces, and incipient suprainiac fossae (Wolpoff 1999; Smith,
1982, 1984; Frayer et al., 2006; Cartmill and Smith, 2009; Ahern et al., 2013) that are coined as Neandertal features. The ever popular fossils from Vindija in Croatia exhibit features that are Neandertal, but are also reminiscent of modern humans; these features lay in the cranium, (Wolpoff et al., 1981; Smith et al., 1989; Ahern et al., 2002; Ahern et al., 2004), the splanchnocranium (Smith, 1992; Cartmill and Smith, 2009), and the mandible (Wolpoff et al., 1981).
The recent publication of the Neandertal genome has revealed a plethora of information ripe for interpretation (Green et al., 2010). Sharing more genetic similarity with non-African populations than African populations could be an indication that
Neandertals interbred with recent modern humans when they exited Africa and entered
Central Europe (Green et al., 2010; Sankararaman et al., 2012). Recent estimates of the contribution of Neandertals to the modern human genome put the estimate at a conservative 1-3% (Prüfer et al., 2014; Green et al., 2010; Sankararaman et al., 2014) using highly discriminatory analyses. This indicates that modern humans may have acquired some their modern features from Neandertals, such as characteristics of the ever important immune system (Abi-Rached et al., 2011).
These features, while interesting by themselves, raise some questions when considering the relationship between modern humans and Neandertals. The puzzle most pertinent to this investigation is considering how far removed these different features
10 make Neandertals from anatomically modern humans. It is no question that they are different, but how different? Are they a different species, or a subspecies? Some authors have attributed differences, specifically those in the cranium, as an indication that
Neandertals and modern humans could not possibly have been the same species
(Tattersall, 1986, 1992; Tattersall and Schwartz, 1999). However, genetic, morphological, and even some archaeological evidence suggests some of these features that may be seen as imperative to creating a species line between Neandertals and humans may simply be a result of changes in climate and the corresponding morphological adaptation of human populations, and the key may lay in the cranial base.
Integration of the Cranium
Integration of cranial components is essential to consider when an examination of any portion of the cranium is undertaken (Lieberman, 2011). The cranium exhibits two types of integration: functional and developmental integration. Functional integration occurs when the various components work together to function effectively as a whole.
Developmental integration explains which genetic, epigenetic, and environmental factors affect overall integration during growth and development. It is changes in these primary types of integration that create the differences seen between modern human crania and those of apes. Four main changes that occur are brain growth (including endocranial fossae growth), flexing of the cranial base, foramen magnum central migration with a more horizontal nuchal plane, and a smaller, less prognathic face (Lieberman, 2011).
Some authors have loosely attributed these different growth trajectories to differences in cognitive development; however, what this truly means in terms of differences between
Neandertals and modern humans is still unknown.
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Structure of the Cranial Base
The basicranium possesses many features that are essential to the overall growth, development, and integration of the cranium. It is comprised of portions of five bones, as was mentioned before (Figure 1) and is divided into three regions: the anterior, middle, and posterior. The anterior region begins at the posterior margins of the frontal sinus with the sides of the frontal bone and the lesser wings of the sphenoid forming the lateral margins. The middle region of the basicranium is formed anteriorly by the greater wings of the sphenoid and posteriorly by the clivus. The lateral portion of the middle basicranium is formed by the greater wings of the sphenoid as they curve to meet the squama of the temporal bones. Finally, the posterior portion of the cranial base is made up anteriorly by the basiocciput and the basisphenoidal region, while the lateral and posterior portions are formed by the posterior margin of the petrous bone curving around and joining with the occipital squama (Joshi and Meyers, 2013).
There are three depressions (fossae) in the floor of the basicranium: the posterior fossae, which support the hind brain, the middle fossae, which support the temporal lobes, and the anterior fossae, which support the frontal lobes and olfactory bulbs. In
Homo sapiens, the basicranium flexes at three synchondroses (see Figure 3): the spheno- occipital, mid-sphenoidal, and spheno-ethmoidal (Lieberman and McCarthy, 1999;
Lieberman, 2011).
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Figure 3: Cranial Base Flexure and Synchondroses Location - This illustration highlights the three basicranial synchondroses; the sphenoi-ethmoidal synchondrosis is the most anterior, the spheno-occipital is the most posterior, and the mid-sphenoidal is midway between the two
This flexure is thought to serve the purpose of increasing room to accommodate a more rapidly growing brain that reaches larger sizes, as in the case with modern humans
(Gould, 1977). These synchondroses are also the point of flexure in Neandertals, although they flex to a lesser degree (Green, 1990; Lieberman et al., 2000) despite an identically-sized brain.
Ontogeny of the Basicranium
During development, the cranial base first forms from mesenchyme as a cartilaginous platform called the chondrocranium. The chondrocranium is initially unevenly shaped and forms from 18 cartilaginous precursors that occur bilaterally (Kjaer,
1990; Lieberman et al., 2000). These eventually aggregate into the approximate shape of the cranial base, leaving spaces for the already developing blood vessels that feed the
13 brain, and the nerves that stem from the basal portion of the brain; these spaces eventually become the cranial foramina (Lieberman, 2011).
After approximately eight weeks in utero, a minimum of 41 ossification centers develop within the cartilaginous chondrocranium. This causes hypertrophy and death of the cartilage, which is eventually replaced fully by bone. Ossification proceeds anteriorly
(Hamilton et al., 1964) and when this process is completed, the only portions of the basicranium that remain unossified are the three synchondroses. These synchondroses are the primary locations of growth after the chondrocranium is completely replaced by bone, and are also where flexion of the cranial base occurs (Lieberman et al., 2000; Lieberman,
2011).
Cranial base flexure occurs prominently within the first year of life when brain growth rates are high, and the anterior portion of the base elongates. The flexure of the cranial base is found to be associated with brain size (Lieberman and McCarthy, 1999;
Lieberman et al., 2008). Experimental work on rats and chimpanzees show an increase in brain size is associated with a more flexed cranial base. Bastir et al. (2010) found that as the brain grows postnatally in modern humans, it is continuously associated with increased flexing of the basicranium. Inhibition of growth at the spheno-occipital synchondroses has led to more flexed basicrania, likely due to prevention of normal growth in the usual direction (Reidenberg and Laitman, 1991). In fact, studies on head binding in certain cultures show that practices that prevent brain growth in the normal fashion lead to a more-flexed basicranium (Cheverud et al., 1992; Kohn et al., 1993).
This is different from the development of apes because their posterior basicranium
14 elongates and the cranial base does not flex to the same degree as in modern humans
(Green, 1990; Smith, 1991; Cartmill and Smith, 2009).
Structure of the Splanchnocranium
A discussion of the basicranium cannot be undertaken without considering other portions of the cranium due to the high degree of integration that the splancnocranium and neurocranium exhibit so the structure, ontogeny, and function of the splanchnocranium will be discussed below. The splanchnocranium, while important by itself, is also found to be highly related to changes in the cranial base (Bastir et al., 2006;
Rosas et al., 2006; Bastir, 2008; Lieberman et al., 2008). Because the cranial base forms part of the structural foundation that the splanchnocranium hangs from, forces that act upon one of these features are understandably going to cause changes in the other feature.
The splanchnocranium is arguably the most complicated structure of the entire cranium; the various margins of its sections make up walls of other structures, such as the roof of the oral cavity being the floor of the nasal cavity. This means the face is not only the most complicated part of the cranium, but also the most well-integrated (Enlow,
1982). While the compartments of the face are able to be picked apart to some extent, they are not independent of one another and are greatly affected by growth in other sections of the cranium. The splanchnocranium is also under great influence by the organs that it grows around, such as the eyes, pharynx, and masticatory muscles; changes in these soft tissue structures such as more robust masticatory muscles can cause associated changes in the face (Enlow, 1982).
While this interdependence makes it quite difficult to divide up the face in any meaningful and discrete way, Lieberman (2011) divides it up into three sections: the
15 upper face, which houses the eyes and is made up of the area below the frontal lobes of the brain, the middle face which mostly surrounds the nasal cavity, and the lower face which is made up of the area that surrounds the oral cavity. While this is a good way to separate facial sections, it is still important to emphasize and reiterate that these three areas are not discrete and depend on the growth of one another.
Ontogeny of the Splanchnocranium
The features of the face, such as the nose and mouth, first appear as depressions in the first few weeks of development. As the entire head grows the covering for the mouth, the stomodeum, cannot increase at the same rate and ruptures, opening the pharynx and respiratory system to the outside (Enlow, 1982). The pharyngeal arches develop into various portions of the head and neck, such as the hyoid and the laryngeal cartilages, and the mandibular/maxillary complex. The nasal openings develop from two swellings below the forehead as the eyes are pushed into a forward-facing position by the enlarging brain. Bone has formed in the mandibular and maxillary arches. A nasal septum forms as the palate closes; this separates the oral and nasal cavities from one another. Finally, at about seven to nine weeks, the face is actually recognizable (Enlow, 1982).
As the growth of the splanchnocranial components proceeds, there is also some structural displacement of the face. The nasomaxillary complex enlarges and is moved forward and inferiorly as the mid-portion of the cranial base grows. This is achieved via bone resorption on the nasal cavity side of the maxilla and bone deposition on the palatal side. Although this process sounds straight forward enough, there is a high degree of variability in this process of nasomaxillary shift, which creates the variance seen in modern human groups with regards to facial dimensions (Enlow, 1982).
16
Interactions between the Cranial Base and the Face
Because of the tight relationship between cranial base length, flexure, and facial structure, it is important to undertake a discussion on the effects of these structures on one another. Elongated faces have been found on many occasions to be associated with a less flexed basicrania (Biegert, 1957; Rosas et al., 2006; Lieberman et al., 2008; Bastir et al., 2010). In hominins that possess “large” faces, the cranial base is less flexed regardless of encephalization. This is the case in Neandertals; they possess identically sized brains as modern humans, but a more prognathic face and a less flexed cranial base.
Trinkaus (2003) lends some insight in the case of Neandertals. He explores the idea that the Neandertal face is not actually long; relative to Neandertals, modern human faces are actually reduced when compared earlier archaic specimens. The author finds that Neandertals possess a much longer value for nasion to basion measurement. This measurement, while technically quantifying cranial base length, is also composed of portions of projection of the nasal root and the mid-sagittal supraorbital torus. However, regardless of whether Neandertal faces are long, or modern human faces are short, the point is still the same; Neandertals have a longer and less flexed cranial base, and a more prognathic face than modern Homo sapiens.
Evidence of Cold Adaptation in the Cranium
Since it became obvious to investigators that populations living in different climatic zones possessed differing features that allow them to adapt to those zones, anthropologists have pursued an explanation of exactly how these people differ and what that means for Homo sapiens’ capacity to adapt to differing environments. Several studies have addressed differences in cranial structures between groups in cold
17 environments and warm environments. Selection for cold adaptation in the cranium seems to focus on creating a more brachycephalic cranial shape (Roberts, 1978; Beals et al., 1984; Baharati et al., 2001; Nowaczewska et al., 2011), smaller paranasal sinus size
(Koertvelyessy, 1972; Rae et al., 2003; Rae et al., 2006), a higher, narrower nasal aperture and longer nasopharyngeal structures (Franciscus and Trinkaus, 1988;
Hernandez et al., 1997; Roseman and Weaver, 2004; Harvati and Weaver, 2006; Rae et al., 2006; Yokley, 2009; Bastir and Rosas, 2013), and alterations in overall facial shape
(Bernal et al., 2006; Rae et al., 2006; Hubbe et al., 2009; Sardi and Rozzi, 2012).
In addition to differences in cranial form, a number of studies have addressed changes in infant weight and growth rates in cold climates. Children are arguably the most vulnerable to extreme temperatures; their bodies are unable to expend the energy needed to maintain warmth for long enough periods of time to sufficiently prevent hypothermia in the absence of a care provider. Because of this, it is not unusual to find that children possess a specific physiological adaptation to assist them in times of trouble in the cold: high levels of brown adipose tissue (Dawkins and Scopes, 1965; Aherne and
Hull, 1966; Heaton, 1972; Lean et al., 1986; Hu et al., 2012). Brown adipose tissue
(BAT) aids in facilitation of non-shivering thermogenesis (Ouellet et al., 2012), which allows infants and children to maintain body temperature without undergoing the metabolically draining act of shivering.
Infant and child growth has also been extensively addressed, and there are a number of patterns worth mentioning. Infants born in the autumn and winter exhibit higher birth weights and have less of a chance of being low birth weight or premature
(Murray et al., 2000; Floures et al., 2009; Strand et al., 2012). This is due to most
18 maternal and infant growth taking place during the third trimester (Wen et al., 1990;
Siega-Riz et al., 1995) and when this is cut short, that growth is unable to be completed before the infant is born. In addition, postnatal growth has been found to be of a higher rate in infants that existed in cooler conditions during the first two weeks of life (Glass et al., 1968).
Maternal body mass is also important when considering infant size. Groups that have adapted to cold environments tend to have higher body mass indices (BMI); this is usually due to higher weight and body proportioning, as well as energetics (Katzmarzyk and Leonard, 1998; Wells, 2012). Although cold-adaptation specifically has not been addressed with regards to infant birth weight, maternal weight and body mass index has
(Cnattingius et al., 1998). Maternal BMI is found to be positively associated with infant birth weight, although the distinction between high fat and high muscle was not made.
These results suggest that the general trend in individuals that have lived in a cold environment is selection for larger mothers and bigger infants that develop into adults with smaller maxillary sinuses, more elongated nasal passages, and higher nasal apertures. Craniofacial growth in cold environments has experimentally been found to be more rapid and continues for a longer period of time, which is what has been found in modern human growth studies on infants and children. Sardi and Rozzi, (2012) found that faces belonging to living modern Europeans grew until the eruption of the third molar and faces of modern South Africans ceased growth around the eruption of the second molar; they attributed this to a longer period of growth due to adaptation to cold in modern Europeans.
19
Taking all of these lines of evidence into consideration, an attempt to connect cold adaptation and neurocranial dimensions will be undertaken in the current study. The cranium is highly integrated so detecting which portion influences another can be challenging (Lieberman et al., 2000). Because of the degree of integration, however, there is possibility for multiple structures to affect one another in different ways.
Elongation in the cranial base of rats has shown differences in positioning of the face
(Rae et al., 2006), and growth in the cranial base affects the movement of the face
(Enlow, 1975). However, because the cranial base continues remodeling throughout adolescence (Enlow, 1975), there could be potential for changes in the cranial base due to modifications in the face, as some authors have suggested (Bastir et al., 2007; Bastir et al., 2010). Climatic variables have the potential to make these changes because the extremely plastic upper respiratory tract is structurally supported by the anterior cranial base. Although it is obvious that all parts are connected and influence one another, the primary goal of this investigation will be to assess the effects of cold adaptation on the splanchnocranium, and connect these changes to modifications in cranial base length of
Neandertals.
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CHAPTER III
MATERIALS
Modern human data were derived from the free access W.W. Howells craniometric data set, which was collected between 1965 and 1980 (Howells, 1989). This data set consists of 82 measurements taken from 2524 crania representing 28 different populations collected from throughout the world. Because the purpose of this investigation is to examine cold adapted groups, four groups were chosen from this data set that represent modern humans in cold environments. As a comparison, four groups from warm/hot areas of the Earth were also chosen (Table 1).
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Table 1: Samples Chosen from W.W. Howells Collection Climate Population Region Total Norse Oslo, Norway 110 Buriat Lake Baikal, Siberia 109 Cold Inuit Greenland 108 Ainu Northern Japan 83 Total 410 Egyptians Northern Africa 111 Dogon Mali, Western African 99 Warm Zulu Southern Africa 101 Andamen Andamen Island, India 37 Total 348 Total in Entire Sample 758
Table 1: This table outlines the groups that were selected and the totals for each; three Asian groups and one European group made up the cold-adapted sample while three African groups and one South Asian group comprised the warm-adapted sample.
A small sample of Neandertals (Table 2) was taken from pre-collected data.
Because of fragmentation of the fossil samples and availability of measurements, only five Neandertals were able to be recorded and included in the model. The average taken from Weaver et al. (2007) was the only data published in their paper; it was an average of all of the Neandertal specimens used in their examination. Because their analysis included more specimens it was dubbed a more appropriate average to use.
Table 2: Adult Neandertals La Chapelle-aux-Saints Smith (pers. comm.) La Ferrasie Smith (pers. comm.) Amud I Suzuki and Takai (1970) Monte Circeo Suzuki and Takai (1970) Petralona Suzuki and Takai (1970) Average Weaver et al. 2007
Table 2: There were five Neandertal specimens used in this investigation, and one average borrowed from a previously published work.
22
A sample of early modern humans was also used from a collection of previously collected and published measurements (Table 3). The sample of early modern humans was also fragmented so only 15 were able to be utilized in this investigation. These samples span a very wide temporal period, from Skhūl V, which is dated between
120,000 and 80,000 years old (Mercier et al., 1993) and the Ofnet Cave material, dated to approximately 6500 B.C. (Frayer, 1997). While these do span a very wide time period, they are all considered to be Pleistocene or early post-Pleistocne Homo sapiens sapiens, and therefore are included in the analysis.
Table 3: Adult Anatomically/ Early Modern Humans Mladeč 1 Smith (pers. comm) Dolní Věstonice 3 Smith (pers. comm) Skhūl V Smith (pers. comm) Abri Pataud Smith (pers. comm) Cro-Magnon 1 Smith (pers. comm) Oberkassel D999 Smith (pers. comm) Oberkassel D998 Smith (pers. comm) Kaufertsberg Sv002/01 Smith (pers. comm) OFNET 2497 Smith (pers. comm) OFNET 2504 Smith (pers. comm) OFNET 2486 Smith (pers. comm) OFNET 2496 Smith (pers. comm) OFNET II SV001 Smith (pers. comm) OFNET 2481 Smith (pers. comm)
Table 3: These are the early modern humans used for the investigation; the Ofnet material and the Kaufertsberg specimen are all Mesolithic, while the rest are Paleolithic.
23
CHAPTER IV
METHODS
Cranial Measurements
Five measurements were used quantify various portions of the cranium. Basion to nasion is the measure of the length of the cranial base (CBL), quantifying the segment that is the foundation for the facial skeleton and forms parts of the nasopharynx. Basion to prosthion measures upper facial length (UFL), while nasion to prosthion measures upper facial height (UFH). Basion to bregma measures cranial height (CH), and cranial breadth (CB) is from euryon to euryon. Euryon is located at different levels for individual skulls but is measured high on the parietals. These measurements are illustrated in Figure
4.
These measurements were chosen because they quantify various neurocranial and splanchnocranial dimensions that have been found to be very closely related to one another by previous investigators. Because it has been suggested and shown experimentally that the basicranium has extreme effects on the development of the neurocranium (Lieberman et al., 2000), these anatomical points and measurements were chosen to discover exactly how related, and in what way, these chosen samples and specimens are to one another in the context of this investigation. This is also the reason
24 these particular facial variables were chosen; the face has been found to have a certain degree of independence from other measurements of the cranium (Enlow, 1982), so these were chosen to assess to what degree the face was independent in this model, detect splanchnocranial relationships with the cranial base, and examine how these facial structures relate to neurocranial and basicranial dimensions.
Figure 4: Cranial Measurements - This figure reveals the measurements and locations of anatomical points used in the investigation.
The five measurements listed above quantify various dimensions of the cranium, and use four different anatomical points. These points are basion, which is taken from the most anterior portion of the foramen magnum, nasion, which is taken at the intersection of the two nasal bones with the frontal bone, bregma, which lays at the intersection of the two parietals and the frontal bone, and prosthion, which is a point between the upper incisors on the alveolus. Cranial breadth is taken at euryon; this is the widest part of the parietals and varies from person to person.
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Statistical Methods
For this investigation, several statistical methods will be used to analyze the data.
First, a Pearson correlation will be undertaken to detect correlations between measurements within groups, then a multivariate analysis of variance (MANOVA) will be performed to detect the degree of difference between groups and parse out the contributing variables, and finally, contrasts will be used to compare groups against one another for each measurement used.
First, a Pearson correlation will be calculated to determine the correlation between each of the measurements in each of the groups. The purpose of a Pearson correlation is to determine the linear relationship between two variables, and the strength of this relationship (Bolboaca and Jäntschi, 2006). The Pearson coefficient manifests as a value between -1 and +1, where the negative numbers indicate a negative correlation, and a positive number indicates a positive correlation. Variables are considered slightly correlated if they are below +/- 0.30, moderately correlated f they are between +/- 0.30 and 0.50, and strongly correlated if they are above +/- 0.50. Correlations were performed on the raw data.
Secondly, a MANOVA (multivariate analysis of variance) will be performed. The purpose of a multivariate analysis of variance is to explore the differences in a number of dependent variables across different groups (Hatcher and Stepanski, 1994). The
MANOVA is an extension of the regular ANOVA (analysis of variance), but considers more than one dependent variable that may have multiple correlated responses (Weinfurt,
1995); differences between independent variables are not dependent on just one variable, but perhaps the interaction of several different dependent variables.
26
Before the MANOVA was performed the data were log-transformed. Some biological data, such as craniometric data, do not always behave under the assumptions of the required statistical test (McDonald, 2009). The log-transformation was chosen because it is commonly used in morphometric studies (Plavcan, 2012; Raghaven, et al.,
2013), and is the easiest and most convenient transformation to perform (Plavcan and
Cope, 2002). In this case, the data were transformed so that they met the assumptions of normality and homoscedasticity (Hill and Lewicki, 2007).
MANOVA output supplies canonical coefficients. Canonical coefficients reveal which variables contribute the most to the differences between groups (Hatcher and
Stepanski, 1994). Wilks’ Lambda is used as an overall test to tell if the compared groups’ cranial measurements compared all at once are statistically significantly different from one another. The MANOVA will be performed via the GLM (generalized linear model) procedure using the PROC GLM command in the statistical software package, SAS
(Hatcher and Stepanski, 1994).
Lastly, there will be eight contrasts performed. These contrasts were chosen to parse out differences and similarities in these five cranial measurements between groups. Although early modern humans and the two modern human groups are considered part of the same species, it is still important for the context of evolution in the Pleistocene to examine the contrasts and see if any differences lay between these similar, but not necessarily identical, groups. The contrasts that were performed are outlined below:
1. Modern human cold group vs. modern human warm group
2. Modern human cold group vs. Neandertal
27
3. Modern human warm group vs. Neandertal
4. Neandertal vs. early modern humans
5. Modern human cold group vs. early modern humans
6. Modern human warm groups vs. early modern humans
7. All modern humans (cold and warm) vs. archaic humans (early modern
humans and Neandertals)
8. Neandertals vs. all humans (cold group, warm group, and early modern
humans)
With each contrast, the change of Type I error increases. Type I error is the chance that a null hypothesis may be incorrectly rejected when should actually be accepted (Lieberman and Cunningham, 2009). As the number of hypotheses in a test increases, the likelihood of one of those outcomes being a unique event also increases. To correct for this increased chance, a Bonferroni correction is used (Bland and Altman,
1995; McDonald, 2009). The equation for a Bonferroni correction is as follows
(McDonald, 2009):
αc = αe / s
In a Bonferroni correction, αc is the comparisonwise error that we are solving for,
αe is the overall experimentwise error (0.5 in all tests unless stated otherwise) and s is the number of contrasts performed, which is eight in this case. The corrected alpha at which all contrasts will be assessed is:
αc = 0.00625
All graphical representations use least square means. “Least squared mean” is jargon used by SAS for what are sometimes referred to as estimated marginal means
28
(Searle et al., 1980). They will be identical to the arithmetic means when the design is balanced. However, in the case of the current design, not all individuals in groups have present values for each measurement, so the least squared means are calculated to be adjusted to other variables in the model, and are more representative than the arithmetic mean.
29
CHAPTER V
RESULTS
Mean Values for Cranial Measurements
The first set of results highlight the means for Neandertals, early modern humans, cold-adapted modern humans, and warm-adapted modern humans. Tables 4-8 outline summary statistics for the four groups and their various measurements, and Figures 5-9 relay this information graphically.
Table 4: Means, Standard Error, and Range for Cranial Base Length Group LSMean Standard Error Range (mm) Cold-Adapted Modern 101.19 1.002554 88 – 119 Early Modern 99.323245 1.013937 82 – 106 Neandertals 112.2944 1.0234311 103 – 124 Warm-Adapted Modern 97.51169 1.00278 85 – 114
Table 4: This table outlines the LS means, standard errors, and ranges for all of the groups in their values for cranial base length.
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Figure 5: LSMeans for Cranial Base Length 115
110
105
100
95 CranialBase Length
90
85 CM EM N WM Group
Figure 5: This figure graphically represents the means of the four included groups for cranial base length; as with three of the other measurements, Neandertals have the highest mean, followed by cold-adapted modern humans.
Table 5: Means, Standard Error, and Range for Cranial Breadth Group LSMean Standard Error Range (mm) Cold-Adapted Modern 140.6 1.0026 120 – 167 Early Modern 138.7 1.0144 126 – 151 Neandertals 153.9 1.0242 148.7 – 159 Warm-Adapted Modern 134.8 1.0028 118 – 152
Table 5: This table outlines the LS means, standard errors, and ranges for all of the groups in their values for cranial breadth.
31
Figure 6: LSMeans for Cranial Breadth 160
155
150
145
CranialBreadth 140
135
130 CM EM N WM Group
Figure 6: This figure graphically represents the means of the four included groups for cranial breadth; this represents the only measurement where warm-adapted modern humans are second to Neandertals, instead of cold-adapted modern humans.
Table 6: Means, Standard Error, and Range for Cranial Height Group LSMean Standard Error Range (mm) Cold-Adapted Modern 132.2507 1.0022936 115 – 150 Early Modern 131.62806 1.012506 115 – 143 Neandertals 129.381 1.0210138 123 – 143 Warm-Adapted Modern 130.11069 1.0024958 117 – 152
Table 6: This table outlines the LS means, standard errors, and ranges for all of the groups in their values for cranial height.
32
Figure 7: LSMeans for Cranial Height 134
133
132
131
130 CranialHeight 129
128
127 CM EM N WM Group
Figure 7: This figure graphically represents the means of the four included groups for cranial height; this figure shows that Neandertals have the lowest values for cranial height while cold-adapted modern humans possess the highest values.
Table 7: Means, Standard Error, and Range for Facial Projection Group LSMean Standard Error Range (mm) Cold-Adapted Modern 98.398448 1.0029989 82 – 114 Early Modern 97.053327 1.01637 80 – 117 Neandertals 117.62352 1.0275546 108 – 127 Warm-Adapted Modern 96.623012 1.0032634 82 – 116
Table 7: This table outlines the LS means, standard errors, and ranges for all of the groups in their values for facial projection.
33
Figure 8: LSMeans for Facial Projection 125
120
115
110
105
FacialProjection 100
95
90 CM EM N WM Group
Figure 8: This figure represents the means of the four included groups for facial projection; this figure shows that Neandertals have the highest values for facial projection and are followed by cold-adapted modern humans.
Table 8: Means, Standard Error, and Range for Facial Height Group LSMean Standard Error Range (mm) Cold-Adapted Modern 68.394572 1.0037504 57 - 82 Early Modern 66.10953 1.0205148 57 – 95 Neandertals 86.641118 1.0345644 84 – 89 Warm-Adapted Modern 64.156024 1.0040814 52 – 77
Table 8: This table outlines the LS means, standard errors, and ranges for all of the groups in their values for facial height.
34
Figure 9: LSMeans for Facial Height 90
85
80
75
70
65 FacialHeight 60
55
50 CM EM N WM Group
Figure 9: This figure graphically represents the means of the four included groups for facial height; this figure shows that Neandertals have the highest values for facial height and, like projection, are vastly different from the other included groups.
Pearson Correlations
The next four tables (Tables 9-12) show the results of the Pearson correlation analysis of the data. To reiterate, correlations are considered lacking or weak at 0 to +/-
0.30, moderate at +/- 0.30 to +/- 0.50, and strong at +/- 0.50 and above. Strong correlations are bolded.
Table 9: Neandertal Cranial Correlations Basicranial Cranial Facial Cranial Upper Facial
Length Height Projection Breadth Height Basicranial Length 1 0.789786 0.710831 0.67309 -0.3663212 Cranial Height 1 0.408353 0.497322 0.4537805 Facial Projection 1 0.230825 -0.4485345 Cranial Breadth 1 -0.0732241 Upper Facial Height 1
Table 9: Neandertal cranial correlation analysis finds that the strongest correlations are between cranial base length and cranial height, cranial base length and facial projection, and cranial base length and cranial breadth.
35
Table 10: Early Modern Human Cranial Correlations Basicranial Cranial Facial Cranial Upper Facial
Length Height Projection Breadth Height Basicranial Length 1 0.58947 0.647876 -0.07915 0.283577 Cranial Height 1 0.137934 0.056643 0.0316046 Facial Projection 1 0.475773 0.5400653 Cranial Breadth 1 0.2962059 Upper Facial 1 Height
Table 10: Early modern human cranial correlation analysis finds that the strongest correlations are between cranial base length and cranial height, cranial base length and facial projection, and upper facial length and upper facial height.
Table 11: Cold-Adapted Modern Human Cranial Correlations Basicranial Cranial Facial Cranial Upper Facial
Length Height Projection Breadth Height Basicranial Length 1 0.687503 0.747666 -0.02875 0.31476 Cranial Height - 1 0.469431 -0.03814 0.27351 Facial Projection - - 1 -0.06733 0.25315 Cranial Breadth - - - 1 0.39543 Upper Facial - - - - 1 Height
Table 11: Cold-adapted modern human cranial correlation analysis finds that the strongest correlations are between cranial base length and cranial height, and cranial base length and facial projection. The other measurements are all moderate or weak/lacking.
Table 12: Warm-Adapted Modern Human Cranial Correlations Basicranial Cranial Facial Cranial Upper Facial
Length Height Projection Breadth Height Basicranial Length 1 0.628629 0.667105 0.295785 0.64795 Cranial Height - 1 0.34605 0.432513 0.53299 Facial Projection - - 1 0.007915 0.39815 Cranial Breadth - - - 1 0.35334 Upper Facial - - - - 1 Height
Table 12: Warm-adapted modern human cranial correlation analysis finds that the strongest correlations are cranial base length and cranial height, cranial base length and upper facial length, cranial base length and upper facial height, and cranial height and upper facial height.
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Canonical Output for Cold Group vs. Warm Group
Table 13 outlines the result of the test of Wilks’ Lambda. The null hypothesis here is that there is no difference in variables between the cold group and the warm group. The p value for this is statistically significant, meaning that the null hypothesis will be rejected. This leads to the conclusion that the cold group and warm group are statistically significantly different from one another.
Table 13: MANOVA Test Criteria: Cold-Adapted MH vs. Warm-Adapted MH Statistic Value F Value Num DF Den DF Pr > F Wilks' Lambda 0.76299281 47.90 5 771 <.0001
Table 13: MANOVA output for cold-adapted modern humans versus warm-adapted modern humans reveal a statistically significant result; this indicates that there is a significant difference between the cold-adapted group and the warm-adapted group.
Table 9 outlines the results of the examination of canonical coefficients for cold modern human group versus warm modern human group. In the case of the cold adapted modern group versus the warm adapted modern group, cranial base length is the variable that attributes the most to the differences between the two groups, with cranial breadth coming in second.
37
Table 14: Canonical Coefficients for Cold-Adapted MH vs. Warm-Adapted MH Standardized Can. Coeff.
logCranial Base Length 0.87797092 logCranial Height -0.31415501 logFacial Projection -0.31169587 logCranial Breadth 0.56011785 logFacial Height 0.44237535
Table 14: The canonical coefficients show that the two most influential variables to the difference between cold-adapted modern humans and warm-adapted modern humans are cranial base length and cranial breadth.
Figure 10: Influential Variables – Cold- Adapted MH vs. Warm-Adapted MH 142
141
140 139 138 CM 137 WM
136 CranialBreadth 135 134 133 96 98 100 102 104 Cranial Base Length
Figure 10: This figure reveals the relationship between the two most influential variables, cranial base length and cranial breadth, and their relationship to the two compared groups, cold-adapted modern humans and warm-adapted modern humans.
Canonical Output for Cold Group vs. Neandertals
Table 15 outlines the result of the test of Wilks’ Lambda; this tests the null that is that there is no difference between cold modern humans and Neandertals. This result is found to be statistically significant, which means that the null hypothesis is rejected,
38 leading to the conclusion that there is a difference between the cold and Neandertal group.
Table 15: MANOVA Test Criteria: Cold-Adapted MH vs. Neandertals Statistic Value F Value Num DF Den DF Pr > F Wilks' Lambda 0.87942864 21.14 5 771 <.0001
Table 15: MANOVA output for cold-adapted modern humans versus Neandertals reveal a statistically significant result; this indicates that there is a significant difference between the cold-adapted group and Neandertals.
The two variables that contribute the most to the differences between Neandertals and cold modern humans are facial projection and facial height (Table 16). Cranial height also plays a slight role, with cranial base length and cranial breadth playing little role in differentiating these two groups from one another. Figure 11 is a graphical representation of the relationship between these two variables within each of the groups.
Table 16: Canonical Coefficients for Cold-Adapted MH vs. Neandertals Standardized Can. Coeff.
logCranial Base Length 0.20607761 logCranial Height -0.71500014 logFacial Projection 0.62967678 logCranial Breadth 0.26414950 logFacial Height 0.6197660
Table 16: In the comparison between the cold-adapted group of modern humans and Neandertals shows that the two most influential variables are facial projection and facial height.
39
Figure 11: Influential Variables - Cold- Adapted MH vs. Neandertals 134
133
132 CM 131 N CranialHeight 130
129
128 90 100 110 120 130 Facial Projection
Figure 11: This figure reveals the relationship between the two most influential variables, facial height and facial projection, and their relationship to the two compared groups, cold-adapted modern humans and Neandertals.
Canonical Output for Warm Group vs. Neandertals
Table 17 shows the result of the test of the null that there is no difference between the overall warm modern human group and the Neandertal group. This result is found to be statistically significant, meaning that there is a significant difference between the warm modern human group and Neandertals.
Table 17: MANOVA Test Criteria: Warm-Adapted MH vs. Neandertals Statistic Value F Num DF Den DF Pr > F Wilks’ Lambda 0.84163899 29.01 5 771 <.0001
Table 17: MANOVA output for warm-adapted modern humans versus Neandertals reveals a statistically significant result; this indicates that there is a significant difference between the warm-adapted group and Neandertals.
40
For the case of the warm group versus the Neandertals, the variables that contribute the most to the difference between these two groups are facial height and facial projection (Table 18). Figure 12 reveals these relationships graphically.
Table 18: Canonical Coefficients for Warm-Adapted MH vs. Neandertals Standardized Can. Coeff.
logCranial Base Length 0.35806232 logCranial Height -0.67490775 logFacial Projection 0.47217202 logCranial Breadth 0.34241645 logFacial Height 0.62033479
Table 18: The two most influential variables in separating the warm-adapted modern human group and Neandertals are facial height and facial projection.
Figure 12: Influential Variables - Warm- Adapted MH vs. Neandertals 100
90
80 WM 70 N
FacialHeight 60
50
40 128 129 130 131 132 Cranial Height
Figure 12: This figure reveals the relationship between the two most influential variables, facial height and facial projection, and their relationship to the two compared groups, warm-adapted modern humans and Neandertals.
41
Canonical Output for Neandertals vs. Early Modern Humans
The p value here is well below the comparison-wise alpha, leading to the null hypothesis being rejected and the conclusion that there is a significant difference between
Neandertals and early modern humans.
Table 19: MANOVA Test Criteria: Neandertals vs. Early MH Statistic Value F Num DF Den DF Pr > F Wilks' Lambda 0.89025697 19.01 5 771 <.0001
Table 19: MANOVA output for Neandertals and Early Modern humans reveal a statistically significant result; this indicates that there is a significant difference between Neandertals and Early Modern humans.
In Table 20, it is shown that the two variables that contribute the most to the differences between the Neandertal and early modern humans are facial projection and facial height. Figure 13 below shows the graphical representation of these two variables.
Table 20: Canonical Coefficients for Neandertals vs. Early MH Standardized Can. Coeff.
logCranial Base Length 0.27869901 logCranial Height -0.70931389 logFacial Projection 0.56046200 logCranial Breadth 0.26919392 logFacial Height 0.63692482
Table 20: This table reveals that the two most influential variables when separating Neandertals and Early Modern humans are facial height and facial projection.
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Figure 13: Influential Variables – Early MH vs. Neandertals 90
85
80 N 75 EM FacialHeight 70
65
60 128 129 130 131 132 133 Cranial Height
Figure 13: This figure reveals the relationship between the two most influential variables, facial height and facial projection, and their relationship to the two compared groups, early modern humans and Neandertals.
Canonical Output for Cold Modern vs. Early Modern Humans
The p value for the comparison between cold modern humans and early modern humans is above the comparison-wise alpha, leading to failing to reject the hypothesis. It is concluded then that there is no significant difference between cold modern humans and early modern humans (Table 21).
Table 21: MANOVA Test Criteria: Cold-Adapted MH vs. Early MH Statistic Value F Num DF Den DF Pr > F Wilks' Lambda 0.99492445 0.79 5 771 0.5549
Table 21: MANOVA output for cold-adapted modern humans versus early modern humans reveal a statistically significant result; this indicates that there is not a significant difference between the cold-adapted group and early modern human group.
43
Canonical Output for Warm Modern vs. Early Modern Humans
Table 22 reveals the results of Wilks’ Lambda; p value reveals that it is significant, meaning that there is a detectable difference between the variables in the modern human warm group, and the early modern human group.
Table 22: MANOVA Test Criteria: Warm-Adapted MH vs. Early MH Statistic Value F Num DF Den DF Pr > F Wilks' Lambda 0.76299281 47.90 5 771 <.0001
Table 22: MANOVA output for warm-adapted modern humans versus early modern humans reveal a statistically significant result; this indicates that there is a significant difference between the warm-adapted group and the early modern human group.
Table 23 shows that the two variables that contribute the most to the difference between these two groups are cranial base length and cranial breadth. Figure 14 below shows the linear relationship between these two variables in the two groups being compared.
Table 23: Canonical Coefficients for Warm-Adapted MH vs. Early MH Standardized Can. Coeff.
logCranial Base Length 0.87797092 logCranial Height -0.31415501 logFacial Projection -0.31169587 logCranial Breadth 0.56011785 logFacial Height 0.44237535
Table 23: This table reveals that the two most influential variables are cranial base length and cranial breadth when it comes to determining the difference between warm-adapted humans and early modern humans.
44
Figure 14: Influential Variables – Early MH vs. Warm-Adapted MH 141
140
139
138 EM 137 WM
136 CranialBreadth 135 134 133 96 97 98 99 100 101 Cranial Base Length
Figure 14: This figure reveals the relationship between the two most influential variables, facial height and facial projection, and their relationship to the two compared groups, cold-adapted modern humans and warm-adapted modern humans.
Canonical Output for All Modern Humans vs. Archaic Humans
The null hypothesis here says that there is no overall difference between the cranial dimensions of the pooled modern human group and the pooled archaic human group. The p value here is significant; this indicates that we would have to reject the null and conclude that there is some difference between the group of pooled modern humans and the group of pooled archaic humans (Table 24).
Table 24: MANOVA Test Criteria: Modern Humans vs. Archaic Humans Statistic Value F Num DF Den DF Pr > F Wilks' Lambda 0.89706846 17.69 5 771 <.0001
Table 24: MANOVA output for all modern humans together versus archaic humans reveal a statistically significant result; this indicates that there is a significant difference between all modern humans and archaic humans.
45
Table 25 reveals that the two variables that contribute the most to the difference between these two groups are facial projection and facial height.
Table 25: Canonical Coefficients for Modern Humans vs. Archaic Humans Standardized Can. Coeff.
logCranial Base Length 0.29916522 logCranial Height -0.68032419 logFacial Projection 0.53106761 logCranial Breadth 0.34699425 logFacial Height 0.60576314
Table 25: Canonical coefficients reveal that facial projection and facial height are the two most important differences between all modern humans and archaic humans.
Canonical Output for All Humans vs. Neandertals
The null hypothesis tested is that there is no overall difference between the cranial dimensions of the pooled human group and the Neandertals. The p value here is significant, indicating that the null hypothesis will be rejected, which leads to the conclusion that there is some difference between the pooled human group and
Neandertals (Table 26).
Table 26: MANOVA Test Criteria: Humans vs. Neandertals Statistic Value F Num DF Den DF Pr > F Wilks' Lambda 0.86393494 24.29 5 771 <.0001
Table 26: MANOVA output for all humans (cold-adapted + warm-adapted + early modern) versus Neandertals reveal a statistically significant result; this indicates that there is a significant difference between all humans and Neandertals.
46
Table 27: Canonical Coefficients for Humans vs. Neandertals Standardized Can. Coeff.
logCranial Base Length 0.28559274 logCranial Height -0.70028496 logFacial Projection 0.55120123 logCranial Breadth 0.29487313 logFacial Height 0.62713576
Table 27: Cranial base length and facial height are the two most influential variables when distinguishing between all modern humans and Neandertals.
Contrasts
Contrasts were performed to examine the differences between groups. For these, log transformations were used before the contrasts were performed and all statistically significant results are bolded.
Table 28: Contrasts with Dependent Variable – log Cranial Base Length Contrast DF Contrast SS MS F P Cold Group vs Warm Group 1 0.04879058 0.04879058 96.45 <.0001 Cold Group vs Neandertal 1 0.01010155 0.01010155 19.97 <.0001 Warm Group vs Neandertal 1 0.01852332 0.01852332 36.62 <.0001 Neandertals vs Early Modern 1 0.01046936 0.01046936 20.70 <.0001 Cold Modern vs Early Modern 1 0.00088565 0.00088565 1.75 0.1862 Warm Modern vs Early Modern 1 0.04879058 0.04879058 96.45 <.0001 Modern Humans vs Archaic Humans 1 0.01023285 0.01023285 20.23 <.0001 Neandertals vs Humans 1 0.01361159 0.01361159 26.91 <.0001
Table 28: This table outlines results of contrasts for cranial base length between groups. Only one result was found to be insignificant, and that is the contrast between cold- adapted modern humans and early modern humans.
Table 28 examines the difference in the log transformation of cranial base lengths between different groups. All of the tests are significant except the difference between cold modern humans and early modern humans. The null hypothesis (no difference in
47 mean cranial base length between groups) will be rejected for all tests except between cold modern humans and early modern humans.
Table 29: Contrasts with Dependent Variable – log Cranial Height Contrast DF Contrast SS MS F P Cold Group vs Warm Group 1 0.00947015 0.00947015 23.22 <.0001 Cold Group vs Neandertal 1 0.00044834 0.00044834 1.10 0.2948 Warm Group vs Neandertal 1 0.00002938 0.00002938 0.07 0.7885 Neandertals vs Early Modern 1 0.00020597 0.00020597 0.51 0.4775 Cold Modern vs Early Modern 1 0.00005688 0.00005688 0.14 0.7089 Warm Modern vs Early Modern 1 0.00947015 0.00947015 23.22 <.0001 Modern Humans vs Archaic Humans 1 0.00007288 0.00007288 0.18 0.6726 Neandertals vs Humans 1 0.00020147 0.00020147 0.49 0.4824
Table 29: This table outlines the results of the contrasts for cranial height. Only two results were significant; those between the cold-adapted group and the warm-adapted group, and the warm-adapted modern human and early modern humans.
There were two contrasts found to be significant in the case of cranial height
(Table 29). Warm modern humans and early modern humans, and cold modern humans and warm modern humans were found to be significantly different from one another. This is the only case in which the null hypothesis will be rejected; the conclusion here is that there is a significant difference between cranial heights between these two groups. For all of the other contrasts, the results are non-significant. In these cases, the null hypotheses cannot be rejected, leading to the conclusion that there is not a significant difference in cranial height between groups.
48
Table 30: Contrasts with Dependent Variable – log Cranial Breadth Contrast DF Contrast SS MS F P Cold Group vs Warm Group 1 0.06440664 0.06440664 119.24 <.0001 Cold Group vs Neandertal 1 0.00754785 0.00754785 13.97 0.0002 Warm Group vs Neandertal 1 0.01633415 0.01633415 30.24 <.0001 Neandertals vs Early Modern 1 0.00746615 0.00746615 13.82 0.0002 Cold Modern vs Early Modern 1 0.00047592 0.00047592 0.88 0.3482 Warm Modern vs Early Modern 1 0.06440664 0.06440664 119.24 <.0001 Modern Humans vs Archaic Humans 1 0.00963519 0.00963519 17.84 <.0001 Neandertals vs Humans 1 0.01069442 0.01069442 19.80 <.0001
Table 30: This table reveals results for contrasts for the log transformation of cranial breadth. The only result that revealed any insignificance was between cold modern humans and early modern humans.
For cranial breadth (Table 30), the significant contrasts were those between the cold group and the warm group, the warm group and Neandertals, the warm group and early modern humans, and modern humans versus archaic humans. For these, the null hypotheses are rejected and the conclusion is that they differ significantly in cranial breadth. For the cold group and Neandertals, Neandertals and early modern humans, cold modern humans versus early modern humans, and Neandertals versus all humans, they are non-significant. For these, the null hypothesis would not be rejected; the conclusion would be that there is no difference between these groups and cranial breadth.
49
Table 31: Contrasts with Dependent Variable – log Facial Projection Contrast DF Contrast SS MS F P Cold Group vs Warm Group 1 0.01179671 0.01179671 16.93 <.0001 Cold Group vs Neandertal 1 0.02967572 0.02967572 42.59 <.0001 Warm Group vs Neandertal 1 0.03596076 0.03596076 51.61 <.0001 Neandertals vs Early Modern 1 0.02567724 0.02567724 36.85 <.0001 Cold Modern vs Early Modern 1 0.00048384 0.00048384 0.69 0.4049 Warm Modern vs Early Modern 1 0.01179671 0.01179671 16.96 <.0001 Modern Humans vs Archaic Humans 1 0.02280224 0.02280224 32.73 <.0001 Neandertals vs Humans 1 0.03235128 0.03235128 46.43 <.0001
Table 31: This table outlines results for the contrasts of log-transformed facial projection values. The only result that was statistically insignificant was between cold-adapted modern humans and early modern humans.
For facial projection (Table 31), the only groups that were not significantly different from one another were the cold modern human group and the early modern human group. The null hypothesis for this set of contrasts is that there is no difference in facial projection between the compared groups. The null hypothesis would be rejected leading to the conclusion that there is no difference in facial projection between cold- adapted modern humans and early modern humans. For all other groups, the null hypothesis would be rejected. There is some difference in facial projection between all other groups.
50
Table 32: Contrasts with Dependent Variable – log Facial Height Contrast DF Contrast SS MS F P Cold Group vs Warm Group 1 0.14563264 0.14563264 133.74 <.0001 Cold Group vs Neandertal 1 0.05210656 0.05210656 47.85 <.0001 Warm Group vs Neandertal 1 0.08392791 0.08392791 77.07 <.0001 Neandertals vs Early Modern 1 0.05083049 0.05083049 48.68 <.0001 Cold Modern vs Early Modern 1 0.00294880 0.00294880 2.71 0.1003 Warm Modern vs Early Modern 1 0.14563264 0.14563264 133.74 <.0001 Modern Humans vs Archaic Humans 1 0.04839823 0.04839823 44.45 <.0001 Neandertals vs Humans 1 0.06551542 0.06551542 60.17 <.0001
Table 32: The last table reveals the results of log-transforming facial height values and performing contrasts. The only contrast that was not statistically significant was between cold-adapted modern humans and early modern humans.
As far as facial height is concerned (Table 32), all groups show significant differences in these contrasts except cold modern humans versus early modern humans.
The null hypothesis for these contrasts is that there is no difference in facial height between the two compared groups. For these cases, the null hypothesis is rejected and the conclusion is that there is a significant difference between these groups. For cold modern humans versus early modern humans, the result is non-significant, concluding that there is no difference in facial height between these two groups.
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CHAPTER VI
SUMMARY
The results of the statistics highlight many interesting points. Firstly, for the measurements, Neandertals consistently maintained the highest means, with cold adapted humans following second, early modern humans next, and warm-adapted humans last
(Figures 5-9). This order is the case for every value except for cranial height, where
Neandertals possess the lowest values and cold-adapted modern humans were the highest.
Early modern humans are potentially between cold-adapted modern humans and warm- adapted modern humans in most measurements because they are intermediate in some way. By this point, modern humans had lost much of their archaic cranial form and assumed a fundamentally modern morphology. This sample of early modern humans is composed of groups from a wide span of time and geographic range. This distribution of specimens could be skewing the results to more intermediate values.
Secondly, the data reveal that the correlations between cranial dimensions are usually very high (Tables 4-7), especially those between cranial base length and facial projection, and cranial base length and cranial height. Some variables within the
Neandertal group were found to be negatively correlated, although this is could be due to
52 the much smaller sample sizes and missing values that are found within these groups.
Small sample sizes may not be completely representative of the population from which they are drawn. If there is some sort of bias in the data, it is amplified when the sample sizes are small. This does not negate the usefulness of using small sample sizes, but it does require a more critical eye when interpreting results. Otherwise, these values are mostly highly positively correlated amongst all groups.
Third, the canonical analysis reveals which measurements contribute the most to the difference between groups, and how significant this difference is. For every comparison except for the one between cold modern humans and early modern humans, the results indicate a statistically significant difference between groups. MANOVA output also reveals which variables contribute the most between different groups. The most influential variable in separating groups is cranial height, followed closely by upper facial height, with cranial base length, cranial breadth, and upper facial length trailing behind.
Lastly, the contrasts reveal that in almost every case, the groups are statistically significantly different from one another. The only measurement that reveals a majority of non-significant comparisons is cranial height. This overwhelming non-significance is especially interesting because of its influence in separating different groups that is revealed in the canonical analysis. The only two contrasts that are significant are warm- adapted modern human versus early modern humans and warm-adapted modern humans versus cold-adapted modern humans.
53
CHAPTER VII
DISCUSSION
Neurocranial Dimensions
A number of studies have addressed the impact of geographic location and climate on cranial morphology. Cranial proportions, especially within the neurocranium, have been found to correlate highly with geographic distance from Africa independent of climatic factors (Hubbe et al., 2009). The neurocranium is thought to be a perfect candidate for detecting geographic patterns because brain size is under strong genetic control, and it seems that at least a portion of this genetic control is due to population history (Hubbe et al., 2009). However, brain and neurocranial shape are largely determined by the basicranium that they grow and rest upon (Lieberman and McCarthy,
1999; Rightmire, 2012), which may be under pressure from other influential factors.
Basicranial breadth was not a factor included in this examination, but it can have profound effects on the neurocranium. Basicranial breadth constrains the breadth of the neurocranium (Lieberman et al., 2000) and has been found to be under the influence of climatic factors (Nowaczewska et al., 2011). The control of basicranial breadth on neurocranial breadth and its susceptibility to environmental influences could explain the quantity of studies that associate neurocranial dimensions with cold adaptation.
54
Brachycephalization is thought to be a response to cold adaptation in modern humans.
The explanation behind this is that crania with a rounder and broader shape have less surface area by which to lose heat (Beals et al., 1983). Beals et al. (1983; 1984) examined the relationship between climate variability, cranial morphology, and thermoregulation.
Their study indicated that a potentially thermoregulatory adaptation in head shape can be seen in the fossil record of anatomically modern humans that make the transition to living in colder and colder environments.
The data in this investigation reveal the same pattern found by previous authors when applied to modern humans; that cold-adapted modern humans and warm-adapted modern have statistically significantly different values for cranial breadth (Table 25), with cold-adapted modern humans possessing a much wider neurocranial breadth (Figure
6). In fact, cranial breadth is also one of the two major contributors to the statistically significant difference between warm-adapted modern humans and cold-adapted modern humans (Table 9 & Figure 10). This suggests support for the pattern of more brachycephalic crania found in populations from cold environments and a more dolichocephalic cranium found in modern humans who have adapted to a warmer environment.
Neandertals, however, defy the pattern of brachycephalization despite traditionally being thought to be cold-adapted. They have the widest cranial breadth of all of the groups (Figure 6), but possess the absolute lowest cranial height (Figure 7). As previously stated, basicranial breadth is under some influence from the environment
(Nowaczewska et al., 2011). Neandertals have been found to possess relatively wider cranial bases than modern humans (Lieberman et al., 2000), indicating perhaps some
55 influence of the climate on development of basicranial breadth. This increased basicranal breadth could also be an explanation for the relatively lower cranial vault Neandertals possess despite their significantly wider neurocranial breadth.
Interestingly enough, correlations between cranial breadth and cranial height were only moderately correlated for warm-adapted modern humans (Table 7) and Neandertals
(Table 4), and were lacking or weak between early modern humans (Table 5) and cold- adapted modern humans (Table 6). The lack of significant correlations (over 0.5) for these variables within all of these groups indicates that forces acting on changes in cranial breadth and cranial height may be largely independent of one another. Lieberman et al.
(2000) found in their investigation that cranial base breadth constrains neurocranial breadth, but other basicranial dimensions are mutually independent of one another. So if basicranial dimensions are mutually independent, and cranial breadth and cranial height are largely independent, then it must be some other force than basicranial breadth that causes changes in cranial height.
Cranial height contrasts between warm-modern humans and cold-modern humans with Neandertals finds significant differences in both cases (Table 24), but because F is a ratio of two sources of variance, some conclusions can be drawn using this statistic. The
F statistic for Neandertals versus cold-modern humans is larger than that between warm- modern humans and Neandertals indicating that the cold-adapted group and Neandertals are closer to one another. However, these differences in cranial height are still statistically significant and should be treated as such. This could reveal the same conclusions that other investigators have reached before this; that cranial shape has some sort of adaptive purpose in a cold environment, and perhaps this is due to
56 thermoregulation. Like in modern humans, this broadness could be a function of the breadth of the cranial base while the decreased height of the neurocranium could partially be a function of a broader cranial base. Cranial base length was also found to be longer in
Neandertals (Figure 5), which lends support to this hypothesis. In Neandertals, a longer cranial base that is less flexed and wider could provide a wider platform for the brain to spread out upon. This would partially explain differences in cranial form of Neandertals, such as those emphasized by Gunz and colleagues (2012). However, what is it that causes the cranial base to lengthen so much in Neandertals?
Splanchnocranial Developments
Facial projection and cranial base length examined together present the most interesting results. The means for each of the samples reveal that in almost every case, the cold group possesses higher values for both facial projection and cranial base length over all other humans, while the Neandertal sample is the largest of all of the four groups
(Figure 5 & Figure 8). This may be an indication of some occurrence in the splanchnocranium, such as developments in the nasal passages and pharynx that other authors have found (Franciscus and Trinkaus, 1988; Hernandez et al., 1997; Roseman and Weaver, 2004; Harvati and Weaver, 2006; Rae et al., 2006; Yokley, 2009; Bastir and
Rosas, 2013) or some other cause for increases in mid-facial prognathism.
Some of this increased length in facial projection for Neandertals can be explained by increased alveolar prognathism (Smith, 1983). Neandertals possessed much larger anterior teeth than modern humans, and the increased size of these teeth and their roots may in part be responsible for the increased total facial prognathism that
Neandertals exhibited. There are quite a few hypotheses to explain the size of Neandertal
57 anterior teeth. The first of these view large anterior teeth as a retention from ancestral forms with similarly large teeth compared to the decreased modern human range (Smith,
2013). A second explanation, which is surely related to the former, could be the unusual ways in which Neandertals seem to be using their anterior teeth. The incisors, and even canines in some cases, show high signs of wear. Microwear analysis shows that the striation patterns on these teeth are consistent with scraping on materials such as hide and, in some cases, stone tools (Smith, 1983; Trinkaus, 1983). Whatever the reason, the projection in the alveolus does allow some explanation of the increase in mid-facial prognathism, but not entirely (Rak, 1986; Trinkaus, 1986) that Neandertals exhibit.
Although the different portions of the face are hard to parse out, the mid-face is considered to be composed of the portion that surrounds the nasal cavity (Lieberman,
2011). It is important to note that as well as alveolar prognathism, Neandertals exhibit expansion in the mid-facial region. There are many internal structures associated with this portion of the face that have been considered to be at least moderately associated with climate; these include overall facial shape (Bernal et al., 2006; Rae et al., 2006;
Hubbe et al., 2009; Sardi and Rozzi, 2012), paranasal sinuses (Koertvelyessy, 1972; Rae et al., 2003; Rae et al., 2006), and nasal opening and passages (Franciscus and Trinkaus,
1988; Hernandez et al., 1997; Roseman and Weaver, 2004; Harvati and Weaver, 2006;
Rae et al., 2006; Yokley, 2009; Bastir and Rosas, 2013).
The splanchnocranium is a very popular subject of research with regards to climatic studies. Rae et al. (2003) found that maxillary sinus size is negatively correlated with low ambient temperature in Japanese macaques; the lower the temperature, the smaller the maxillary sinuses. These findings were later corroborated by Rae et al.
58
(2006), who found the same pattern in a collection of rat crania, some of which belonged to rats who had been reared in very deep cold. Rae et al. (2003) found that it seems to be the deepest cold that has the most profound effects on morphology; the selective pressures for low ambient temperatures are more extreme than those associated with even extremely hot environments. This suggests that adaptations to these colder climates are likely to persist even in the event of colonization and extended habitation of warmer climates.
Rae et al. (2011)’s assertions about paranasal sinus size in Neandertals may cause some problems to a climatic study on the Neandertal face. Although maxillary sinus size is not the focus of this investigation, it is considered an important factor in cold adaptation and can affect the morphology in the mid-face. To review, they claim that
Neandertals do not actually possess large sinuses; the sinuses may be larger simply because Neandertals possessed larger faces. However, this is counter to the finding by
Steegman and Platner (1968), who find that in rat crania maxillary sinus and nasal cavity size is independent of cranial size.
Paranasal sinus size in Neandertals has not been extensively examined in the literature before Rae et al. (2011) aside from noting that they exist and they look large. If one takes a figurative leap, one could hypothesize that Neandertals may have also shown variation in sinus size with climatic factors, like what is seen in Japanese macaques, rats, and modern Homo sapiens sapiens (Koertvelyssey, 1972; Shae, 1977). If the tendency towards smaller sinuses is also found in Neandertals that spent more time in colder environments, our small sample size could be unrepresentative of the amount of variation that could be seen in a group that is of late found to actually be highly spread over the
59 landscape in Eurasia (Krause et al., 2007), and inhabited many different climates. Perhaps our Neandertal samples are all from individuals that are adapted to cold; although Rae et al. (2011) argue against this point, one must not forget that it was found that the deepest cold had the most profound effects on morphology (Rae et al., 2003). Perhaps a warmer temperature was not enough to change a morphology that had already adapted to a harsh, cold environment. Despite all of this, the idea that paranasal sinus size in Neandertals is a function of splanchnocranial size cannot be discounted, and may actually be the most likely explanation behind the size of Neandertal sinuses. Regardless of whether they are independent of facial size or not, it can be reasonably asserted that sinus size is not what drives the system.
The mid-facial structures that form the upper respiratory tract are the most relevant in this context. The upper respiratory tract is composed primarily of the external nose and nasal aperture as well as two internal structures; the nasal passages and the pharynx (Figure 15). This complex, the nasopharynx, has important functions, including conditioning inspired air during respiration (Naftali et al., 2005). As previously discussed, the splanchnocranium is highly integrated with the structures included in its margins. This investigation reveals that some aspects of splanchnocranial dimensions are also highly integrated with other portions of the cranium, including the cranial base
(Tables 4-7), which makes up the roof of the nasopharynx.
External nose shape in cold-adapted modern humans is characterized by a high, narrow aperture (Thomson and Buxton, 1923; Davies, 1932; Weiner, 1954; Franciscus and Long, 1991; Franciscus, 1995; Yokley, 2006), and individuals who have evolved in warmer groups have been found to have wider nasal apertures. This portion of the upper
60 respiratory tract is transitory between the outside air and the lower respiratory tract, and it aids in determining direction and turbulence of the air stream (Kasperbauer and Kern,
1987; Adamson, 1987; Scherer et al., 1989; Franciscus and Long, 1991).
Figure 15: Nasopharyngeal Anatomy - This figure shows the structures of the upper respiratory tract, as well as associated structures; the region of the nasopharynx, comprised of the nasal passage and the pharynx, is highlighted in grey.
Nasopharyngeal anatomy is plastic to the environment (Yokley, 2009; Noback et al., 2011; Yokley and Holton, 2013; Yokley, 2014). Changes in ambient temperature trigger alterations in this structure when developing in cold environments versus warm environments. Noback et al. (2011) found in ten modern human samples that groups taken from cold environments tended to have longer, narrower nasal cavities. While the entire complex was found to be associated with temperatures, it was found that nasal cavity shape was more highly influenced by ambient temperature while the pharynx was more closely related to relative humidity. As ambient temperature and relative humidity
61 dropped, the length of the nasopharynx increased relative to other populations from warmer, wetter environments.
Neandertal Upper Respiratory Tract
Neandertals do not possess a narrow nasal aperture. Their nasal bones project forward and the aperture is wide, indicating that they would have had a particularly large external nose (Cartmill and Smith, 2009) and a much wider nasopharynx than what is expected in cold-adapted modern humans (Yokley, 2013). This is counter to what is seen in modern Europeans, who tend to exhibit a pattern of narrow, high noses and nasopharynxes (Holton and Franciscus, 2008; Weaver, 2009). Some authors have claimed that this discrepancy indicates that Neandertals actually did not possess cold- adapted faces (Rae et al., 2011).
However, this may not be entirely the case. While Neandertals and modern humans have similarly tall nasal apertures, our archaic relatives did possess a much wider nose. This may serve to allow more room for air to turbinate and warm before moving into the nasal passages, pharynx, and ultimately the lungs (Cole, 1953; Adamson, 1987;
Toftum et al., 1998). The same differences that are seen in anatomically modern human groups between warm and cold environments are seen between archaic humans from various places. Both African archaic groups and Neandertals possessed very wide noses but Neandertals exhibit a higher degree of nasal projection and an increase in height; this is the pattern seen between modern cold-adapted humans and modern warm-adapted humans (Yokley, 2013).
While the nasopharynx in modern humans from cold environments exhibits narrowing, the Neandertal nasopharynx is much wider (Yokley and Holton, 2013). This
62 is counter to what is expected when considering the nasal passages and cold adaptation if anatomically modern humans are the model. However, width is not everything; length must also be taken into consideration. Neandertal nasopharyngeal width is more in line with what is seen in anatomically modern warm-adapted populations, but they also possess a much longer nasal passage. This is reflected by the larger value for anterior cranial base length documented in this study (Figure 5). This effectively would have given them close to, if not the same, air conditioning capabilities of modern European groups (Yokley and Holton, 2013) despite having a much wider nose and nasal cavity.
Instead of narrowing, the Neandertal adaptation may have simply lengthened the nasopharynx to create more space and mucosal surface.
As the nasopharynx elongates, it forces the structures that make up its boundaries to elongate in tandem. Because the cranium is so highly integrated, it is difficult to parse out exactly which portions have the strongest ontogenetic effects on each other; however, as Enlow (1982) notes, the basicranium continues remodeling throughout life. This opens up discussion of facial effects on cranial base anatomy. With a longer, narrower nasal cavity, one could posit that the anterior cranial base would be affected by this development because of its close proximity and integral relationship with facial development. Through this relationship, a more elongated nasopharynx would lead to a more elongated anterior cranial base and more mid-facial prognathism.
So if a narrow nasal aperture with a narrow nasal passage is the modern human method for evolving to a cold environment, why is there a different evolutionary trajectory to fulfill the same need in Neandertals? This change could be due simply to a difference in population history. Modern humans in Europe come from more or less
63 modern looking groups that arose in Africa, while Neandertals came from relatively archaic groups that had already existed in Europe (Cartmill and Smith, 2009) for hundreds of thousands of years. There was a need for an ecological adaptation for facial structures in both groups, so morphology that is equally adaptive in cold environments
(Yokley, 2013) is achieved via different pathways and resulted in different morphological results. Because pressures drove African Heidelbergs and European Heidelbergs in two different directions, it would make sense that they would fill evolutionary needs through different pathways. However, this does not necessarily mean that these two groups are different enough to be classified as separate species, but there is no consensus at this time of where that line should be drawn.
Neandertal Growth
A discussion of Neandertal growth rates is another line of reasoning to consider for this examination. Cranial and dental remains seem to suggest that Neandertals underwent precocious growth when compared with modern humans (Wolpoff, 1979;
Dean et al., 1986; Smith et al., 2007; Ponce de Leon et al., 2008), both prenatally and for a short time after birth. Minugh-Purvis (1988) corroborates these findings, and concludes that Neandertal craniofacial features are already larger than modern humans at birth, as well as subsequent comparable developmental periods later in life. For Neandertal mothers, there is no evidence that gestational periods would have been any longer than they are in modern humans. Like was previously mentioned, modern humans who are adapted to cold exhibit more rapid growth prenatally than those who are born to warm- adapted parents, while Neandertals possessed more rapid prenatal growth than both of these groups.
64
The cause for this is not entirely clear, although some authors have suggested that perhaps it is due to selective pressures in the form of cold stress (Trinkaus, 1995; Pettitt,
2000). The stresses associated with living in a cold climate would have made it imperative that Neandertals achieved reproductive age as rapidly as possible. This would have allowed them to leave the more vulnerable subadult years more quickly behind in exchange for increased chance of maturation and reproduction in adulthood (Stearns,
1982; Stearns and Koella, 1986; Green, 1990). This would be most effective early in postnatal life when different parts of the body are still growing closely in concert with one another. This condition has already been found in a number of animals (Barnett and
Dickson, 1987; Lilja and Olsson, 1987).
Splanchnocranial Growth
Sardi and Rozzi (2012) note that a more rapid growth rate with a prolonged growth time leads to larger facial development in Europeans compared to recent South
Africans. These results were also found by Green (1990); Europeans were also shown to possess rapid growth rates that were intermediate between modern Africans and
Neandertals, with Neandertals possessing the fastest growth rates. Neandertal faces develop through different ontogenetic pathways, but it is clear that (Dean et al., 1986;
Smith et al., 2007; Ponce de Leon et al., 2008) rapid growth in any group is an important adaption in some way to adaptation to a colder environment.
Increased growth rate in the face could greatly affect Neandertal facial dimensions. Downward palatal growth is facilitated by resorption of bone on the nasal surface of the maxilla and deposition on the oral side (Enlow, 1982). This drives the growth of the entire facial structure in an anterio-inferior direction. In conjunction with
65 the other factors listed above, such as unusual anterior tooth use, this more rapid growth would result in a longer nasopharyngeal cavity and an overall taller face, while subsequently increasing prognathism. This is especially plausible because this pattern of growth in the oro-maxillary region is tied to differences in facial height in adult anatomically modern humans (Enlow, 1990; McCollum, 1999).
This growth pattern does not necessarily explain what we find when facial height is finally examined. Correlations between facial height and facial projection are generally unimpressive except in the case of early modern humans where the correlation surpasses
0.50 (Table 5). In Neandertals, facial height is negatively correlated with every variable except for cranial height (Table 4). In warm-adapted modern humans, facial height is strongly correlated with both cranial base length and cranial height. The inferior and anterior growth of the face to more extremes should increase facial height and facial projection in conjunction with one another. However, early modern humans are the only group that exhibits this pattern.
An investigation into relationships between nasal passages and facial dimensions in Neandertals under covers a relationship between facial height and a depression found in the nasal floor of Pleistocene Homo (Franciscus, 2003), including Middle Pleistocene
African specimens. This relationship between facial height and the presence of “bilevel,” or depressed, nasal floors is explained in part by the continued presence of this trait and the shortening of faces in Homo during the Pleistocene; to accommodate the seemingly tenacious bilevel nasal floor in Neandertals, the face adjusted by increasing in height
(Stewart, 1977). The nasal depression and other nasal features appear early in ontogeny
(by the second trimester) (Mooney and Siegel, 1991; Mooney et al., 1992), making them
66 yet another suite of Neandertal features that appear in infancy. While this feature is not necessarily tied to an adaptation to cold because it appears in virtually all Old World
Homo before anatomically modern Homo sapiens (Demeter et al., 2012), in these Middle to Late Pleistocene archaic specimens it is considered a feature highly related to the development of upper facial height (Franciscus, 2003).
Neurocranial Growth
A recent article tracing neonatal brain growth in Neandertals and modern humans suggest that anatomically modern humans underwent a ‘globularization’ phase, where various portions of the brain expand and humans reach the characteristic cranial shape that defines us today (Neubauer et al., 2010; Gunz et al., 2012). These authors seem to find that Neandertals do not undergo this globularization and other investigations have found that these two groups undergo vastly different growth trajectories postnatally
(Zollikofer and Ponce de Leon, 2004; Bastir et al., 2007; Gunz et al., 2012). Advocates of this model suggest that it is the brain that drives growth of cranial structures. While this study seems to suggest some fundamental differences in the pattern of brain growth, one must consider the profound effects of cranial base development on brain shape.
The brain undoubtedly creates enough pressure to affect basicranial morphology
(Enlow, 1982; Lieberman, 2011). However, the pressure the brain creates on the basicranial fossae surface is not necessarily sufficient enough to explain the differing morphology of Neandertal basicranial morphology to an extent that it completely explains Neandertal cranial form. Neandertal cranial bases are longer and broader than those in modern humans, allowing more room for a growing brain to spread out upon.
Thus perhaps it is the shape of the cranial base, and not exclusively different patterns of
67 brain growth that drive cranial shape. While this does not necessarily explain away all questions brought up by Gunz et al.’s study (2012), it may explain why two very closely related groups with identically-sized brains seem to undergo such dramatic differences in brain development. The Neandertal brain may appear less globular because the brain is spread over a larger surface area, giving the appearance of a brain that developed differently from that of moderns. The key may very well be factors that affect the growth and development of the cranial base.
Green (1990) outlined several patterns found in an analysis of modern human and
Neandertal growth. The first is that the posterior portion of the cranial base showed a stronger relationship with growth in the cerebellum, while the anterior portion of the basicranium was more related to facial developments. The second major conclusion reached regarding growth is that Neandertals possess more rapid prenatal growth velocities which could be a major contributor to the differing morphology of Neandertal and modern human crania. A higher brain growth rate would effectively cause a general flattening of the cranial base due to increasing the load at the mid-sphenoidal region at an earlier time. This pressure causes the mid-sphenoidal to be pushed inferiorly, flattening the cranial base and making the cranial base appear longer (see also Cartmill and Smith,
2009).
68
CHAPTER VIII
CONCLUSIONS
To review, firstly it is found in this investigation that anterior cranial base length is more correlated with facial projection than any other measurement (Tables 4-7). Facial projection is found to be consistently one of the most influential variables when comparing two groups, or independent variables; for the cold-adapted group versus
Neandertals, the warm-adapted group versus Neandertals, early modern humans versus
Neandertals, and all humans together versus Neandertals. In fact, for the comparison of all archaic humans (including early modern humans and Neandertals) versus all anatomically modern humans, facial length is the second most influential variable (the first is always facial height; Figures 11-13 and Tables 20 & 22).
For all of these, alveolar prognathism is a likely explanation for at least some of the difference. As was mentioned before, Neandertals possessed extreme projection at the alveolus for whatever reason (Figure 8), and it is statistically significantly different from all anatomically modern humans (Table 25). This is almost certainly related, at least in large part, to the retention of large anterior teeth and large anterior teeth roots in
Neandertals. Providing a large enough alveolar process to house these teeth would require the face in Neandertals to elongate. However, facial elongation in mammals also requires increased prognathism as the face grows forwards as it lengthens (Enlow, 1982).
Thus, Neandertals would have had more alveolar prognathism, reflected in their larger
69 values for upper facial height and facial length. However, this is likely not all of the explanation. Expansion at the mid-face is also a strong contender for explaining the longer facial length and cranial base length of Neandertals and anatomically modern cold-adapted humans (Figures 5 and 8) due to climatic pressures on adaptive processes; specifically increasing room for air turbination and warming, as well as moisture absorption, in cold climates. Thus selection for both the large anterior teeth and elongation of the nasopharynx in Neandertals likely combine for their unique pattern of facial prognathism.
Nasopharyngeal expansion has been noted in other contexts, including modern human studies. Although the development is slightly different than what is seen in modern humans, Neandertals developed a longer nasopharynx than cold-adapted modern human groups. This allowed them equal modern humans in achieving maximum adaptive benefits from changes in the nasopharynx in colder environments despite having a wider nasopharynx. An increase in nasopharyngeal length would have allowed more room for air to turbinate and be generally conditioned, thus protecting the lungs from extremely cold temperatures in a harsh environment. Lengthening the nasopharynx also must lengthen its roof, which is comprised of the anterior cranial base. This could, in part, be the explanation for increased cranial base length in Neandertals.
Another aspect of the growth process may also be at work in Neandertal cranial base development. An increase in the growth rate at the posterior portion of the cranial base would cause subsequent loading at the mid-sphenoid synchondrosis. The mid- sphenoidal synchondrosis would be moved inferiorly by the pressure of more rapid growth at this point, subsequently flattening the cranial base. This flatter cranial base, in
70 conjunction with the wider cranial base that Neandertals possess would allow for a larger platform for the brain to lie upon, giving it a less globular appearance.
This different cranial form could have been a side effect of overall changes in growth rate. Neandertals, and other groups from cold environments, have been found to undergo more rapid growth both prenatally and shortly after birth. This rapid prenatal growth spurt could be the cause of the different cranial shape of Neandertals, and the differences in growth postnatally that are seen between modern Europeans and South
Africans could be the same cause of changes in Neandertal facial morphology. Facial growth continues for many years after birth no matter what environment an individual exists in, giving outside influences ample time to exert evolutionary forces on morphology to force adaptive changes. This is especially relevant when considering parts of the body that are particularly plastic to environmental forces, such as the splanchnocranium and limbs.
It is important to consider the implications of this valuable combination of attributes. The climate that European Neandertals evolved in was harsh and required a suite of traits that would have aided in adaptation and combating the problems associated with living in extremely cold environments. Probably just one feature in a suite of adaptations Neandertals undoubtedly possessed, a more rapid growth period would have allowed Neandertal infants and children to quickly clear childhood. More rapid growth would produce much larger babies at the time of birth, which is a pattern that has already been detected in Neandertals. A larger baby would be more capable in harsher environments than that of a smaller infant, thus explaining why even anatomically
71 modern humans in colder environments tend to carry their babies long enough for them to come fully to term and produce larger babies that display more rapid growth postnatally.
Thus, the selective processes that shape Neandertal cranial form likely stem from several factors crucial to Neandertal adaptation. The key focuses on why the Neandertal face is so large and projecting. As discussed previously, a portion of this lies in the primitive retention of large anterior teeth and roots that require a large alveolar process, which would in turn require the face to grow both inferiorly and anteriorly. As the data here demonstrate, this is not the only factor selecting for the larger, more prognathic
Neandertal face. Selection for nasopharyngeal elongation as an adaptation to cold in
Neandertals would also contribute to the quintessential Neandertal craniofacial form.
Finally, the selection for increased prenatal growth in Neandertals is likely another aspect of cold adaptation in these people, as larger infants would be more able to withstand the impacts of extreme cold. One aspect of prenatal growth likely influenced the growth patterns on cranial base synchondroses, resulting in a flatter cranial base. The combined impact of these factors provides a compelling explanation for the uniqueness of
Neandertal anterior cranial form. Additionally, the flattening and elongation of the cranial base (along with increased breadth not investigated here) provides a logical explanation for the lower cranial vault exhibited by Neandertals compared with modern humans.
Thus, contra Gunz and colleagues (2012), Neandertal cranial vault for likely reflects aspects of their environment al adaptation rather than a different pattern of brain growth or cognitive ability.
72
REFERENCES
Abi-Rached L, Jobin MJ, Kulkarni S, McWhinnie A, Dalva K, Gragert L, Babrzadeh F, Gharizadeh B, Luo M, Plummer FA, Kimani J, Carrington M, Middleton D, Rajalingam R, Beksac M, Marsh SGE, Maiers M, Guethlein LA, Tavoularis S, Little AM, Green RE, Norman PJ, Parham P. 2011. The Shaping of Modern Human Immune Systems by Multiregional Admixture with Archaic Humans. Science 334:89-94.
Adamson PA. 1987. Open rhinoplasty. Otolaryngologic Clinics of North America 20:837-852.
Ahern J, Lee S, Hawks J. 2002. The late Neandertal supraorbital fossils from Vindija Cave, Croatia: A biased sample? Journal of Human Evolution 43:419-432.
Ahern J, Karavanić I, Paunović M, Janković I, Smith FH. 2004. New discoveries and interpretations of hominid fossils and artifacts from Vindija Cave, Croatia. Journal of Human Evolution 46:24-67.
Ahern J, Janković I, Voisin JL, Smith FH. 2013. Modern Human Origins in Central Europe. In: Smith FH, Ahern JCM, editors. The Origins of Modern Humans: Biology Reconsidered, 2nd edition. New Jersey: John Wiley & Sons, Inc.
Aherne W, Hull D. 1966. Brown adipose tissue and heat production in the newborn infant. The Journal of Pathology and Bacteriology 91:223-234.
Baharati S, Som S, Baharati P, Vasulu TS. 2001. Climate and head form in India. Human Biology 13:626-634.
Barnett SA, Dickson RG. 1987. Hybrids show parental influence in the adaptation of wild mice to cold. Genetics Research, Cambridge 50:199-204.
Barton N. 2000. Mousterian hearths and shellfish: Late Neanderthal activities on Gibraltar. In: Stringer CB, Barton RNE, Finlayson JC, editors. Neanderthals on the Edge: Papers from a conference marking the 150th anniversary of the Forbe’s Quarry discovery, Gibraltar. Oxford: Oxbow Books.
Bar-Matthews, Ayalon A, Gilmour M, Matthews A, Hawkesworth CJ. 2003. Sea-land isotopic relationships from planktonic foraminifera and speleothems in the eastern Mediterranean region and their implication for paleorainfall during interglacial intervals. Geochimica et Cosmochimica Acta 57:3181-3199.
73
Bar-Yosef O, Vandermeersch B, Arensberg B, Belfer-Cohen A, Goldberg P, Meignen L, Rak Y, Speth J, Tchernov E, Tillier AM, Swiner S. 1992. The excavations in Kebara Cave, Mt. Carmel. Current Anthropology 33:497-550.
Bastir M. 2008. A systems-model for the morphological analysis of integration and modulatiry in human craniofacial evolution. Journal of Anthropological Sciences 86:37- 58.
Bastir M, Rosas A. 2013. Cranial Airways and the Integration between the Inner and Outer Facial Skeleton In Humans. American Journal of Physical Anthropology 152:287- 293.
Bastir M, Rosas A, O’Higgins P. 2006. Craniofacial levels and the morphological maturation of the human skull. Journal of Anatomy 209: 637-654.
Bastir M, O’Higgins P, Rosas A. 2007. Facial Ontogeny in Neandertals and Modern Humans. Proceedings of the Royal Society B: Biological Sciences 274:1125-1132.
Bastir M, Rosas A, Stringer C, Cuetara JM, Kruszynski R, Weber GW, Ross CF, Ravosa MJ. 2010. Effects of Brain and Facial Size on Basicranial Form in Human and Primate Evolution. Journal of Human Evolution 58:424-431.
Beals KL, Smith CL, Dodd SM. 1983. Climate and the Evolution of Brachycephalization. American Journal of Physical Anthropology 62:1-13.
Beals KL, Smith CL, Dodd SM. 1984. Brain Size, Cranial Morphology, Climate, and Time Machines. Current Anthropology 25:301-330.
Berger T, Trinkaus E. 1995. Patterns of trauma among the Neandertals. Journal of Archaeological Science 22:841-852.
Bernal V, Perez SI, Gonzalez PN. 2006. Variation and causal factors of craniofacial robusticity in Patagonian hunter-gatherers from the alte Holocene. American Journal of Human Biology 18:748-765.
Bicho, NF. The extinction of Neanderthals and the emergence of the Upper Paleolithic in Portugal. Promontoria 3:173-228.
Biegert J. 1957. Der Formwandel des Primatenschädels und seine Beziehungen zur ontogenetischen Entwicklung und den phylogenetischen Spezialisationen der Kopforgane. Gegenbr. Morph. Jahrb. 98:77-199.
Bischoff JL, Williams RW, Rosenbauer RJ, Aramburu A, Arsuaga JL, Garcia N, Cuenca- Bescos G. 2007. High-resolution U-series dates from the Sima de los Huesos hominids yields 600 kyrs: implications for the evolution of the early Neanderthal lineage. Journal of Archaeological Science 34:763-770.
74
Blackwell B, Schwarcz H. 1986. U-series analyses of the lower travertine at Ehringsdorf, DDR. Quaternary Research24:215-222.
Blain HA, Gleed-Owen CP, Lopez-Garcia JM, Carion JS, Jennings R, Finlayson G, Finlayson C, Giles-Pacheco F. 2013. Climatic conditions for the last Neandertals: Herpetofaunal record of Gorham’s Cave, Gibraltar. Journal of Human Evolution 64:289- 299.
Bland JM, Altman DG. 1995. Multiple significance tests: the Bonferroni method. British Medical Journal 310:170.
Bolboaca SD, Jantschi L. 2006. Pearson versus Spearman, Kendall’s Tau Correlation Analysis on Structure-Activity Relationships of Biologic Active Compounds. Leonardo Journal of Sciences 5:179-200.
Brose D, Wolpoff M. 1971. Early upper Paleolithic man and late Middle Paleolithic tools. American Anthropologist 73:1156-1194.
Burdukiewicz JM. 2014. The origin of symbolic behavior of Middle Palaeolithic humans: Recent controversies. Quaternary International 327:398-405.
Carrion JS, Yll EI, Walker MJ, Legaz AJ, Chain C, Lopez A. 2003. Glacial refugia of temperate, Mediterranean and Ibero-North African flora in south-eastern Spain: new evidence from cave pollen at two Neanderthal man sites. Global Ecology & Biogeography 12:119-129.
Carbonell E, Castro-Curel Z. 1992. Paleolithic wooden artifacts from the Abric Romani (Capellades, Barcelona, Spain). Journal of Archaeological Science 19:707-719.
Carbonell E, Bermudez de Castro JM, Pares JM, Perez-Gonzalez A, Cuenca-Bescos G, Olle A, Mosquera M, Huguet R, van der Made J, Rosas A, Sala R, Vallverdu J, Garcia N, Granger DE, Martinon-Torres M, Rodriguez XP, Stock GM, Verges JM, Allue E, Burjachs F, Caceres I, Canals A, Benito A, Diez C, Lozano M, Mateos A, Navazo M, Rodriguez J, Rosell J, Arsuaga JL. 2008. The first hominin of Europe. Letters to Nature 452:465-469.
Cartmill M, Smith F. 2009. The Human Lineage. New Jersey: Wiley-Blackwell.
Cheverud JM, Kohn LAP, Konigsberg, Leigh SR. 1992. Effects of Fronto-Occipital Artifical Cranial Vault Modification on the Cranial Base and Face. 88:323-345.
Caron F, d’Errico F, Del Moral P, Santos F, Zilhão. 2011. The Reality of Neandertal Symbolic Behavior at the Grotte du Rennne, Arcy-sur-Cure, France. PLoS One 6:e21545.
75
Cnattingius S, Bergstrom R, Lipworth L, Kramer MS. 1998. Prepregnancy weight and the risk of adverse pregnancy outcomes. The New England Journal of Medicine 338:147- 152.
Cole P. 1953. Some Aspects of Temperature, Moisture, and Heat Relationships in the Upper Respiratory Tract. The Journal of Laryngology & Otology 67:449-456.
Conard N. 2003. Paleolithic ivory sculptures from south-western German and the origin of art. Nature 426:830-832.
Condemni S. 2001. Les Néandertaliens de La Chaise. Paris: Comité des Travaux Historiques et Scientifiques.
Coon C. 1962. The Origin of Races. New York: A.A. Knopf.
D’Anastasio R, Wroe S, Tuniz Cl, Mancini L, Cesana DT, Dreossi D, Ravichandiran M, Attard M, Parr WCH, Agur A, Capasso L. 2013. Micro-Biomechanics of the Kebara 2 Hyoid and its Implications for Speech in Neandertals. PLoS One 8:e82261.
Davies A. 1932. A resurvey of the nose in relation to climate. Journal of the Royal Anthropological Institute 62:337-359.
Dawkins MJR, Scopes JW. 1965. Non-shivering Thermogenesis and Brown Adipose Tissue in the Human New-born Infant. Letters to Nature 206:201-202.
Dean MC, Stringer CB, Bromage TG. 1986. Age at Death of the Neanderthal Child from Devil’s Tower, Gibraltar and the Implications for Studies of General Growth and Development in Neanderthals. American Journal of Physical Anthropology 70:301-309.
DeFleur A. 1993. Les sepultures moustériennes. Paris: Editions du CNRS.
DeFleur A, White T, Valensi P, Slimak L, Crégut-Bonnoure. 1999. Neanderthal cannibalism at Moula-Guercy, Ardéche, France. Science 286:128-131.
Demeter F, Shackelford LL, Bacon AM, Duringer P, Westaway K, Sayavongkhamdy T, Braga J, Sichanthongtip P, Khamdalavong P, Ponche JL, Wang H, Lunstrom C, Patole- Edoumba E, Karpoff AM. 2012.Anatomically modern human in Southeast Asia (Laos) by 46 kya. Proceedings of the National Academy of Sciences 108:14375-14380.
Dennell RW, Martinon-Torres M, Bermudez de Castro JM. 2011. Hominin variability, climate instability and population demography in Middle Pleistocene Europe. Quaternary Science Reviews 30:1511-1524.
Dibble H, McPherron S. 2006. The missing Mousterian. Current Anthropology 47:777- 803.
76
Duarte C, Maricio J, Pettitt PB, Souto P, Trinkaus E, van der Plicht H, Zilhão J. 1999. The early Upper Paleolithic human skeleton from the Abrigo do Lagar Velho (Portugal) and modern human emergence in Iberia. Proceedings of the National Academy of Sciences 96:7604-7609.
Enlow DH. 1975. Facial Growth. Philadelphia: WB Saunders.
Enlow DH. 1982. The Handbook of Facial Growth. Philadelphia: WB Saunders.
Enlow DH. 1990. Facial Growth. Philadelphia: WB Saunders. d’Errico F, Villa P. 1997. Holes and grooves: The contribution of microscopy to the problem of art origins. Journal of Human Evolution 33:1-31. d’Errico F, Vanhaeren M, Barton N, Bouzouggar A, Mienis H, Richter D, Hublin JJ, McPherron SP, Lozouet P. 2009. Additional evidence on the use of personal ornaments in the Middle Paleolithic of North Africa. Proceedings of the National Academy of Sciences 106:16051-16056.
Falgueres C, Bahain JJ, okoyama Y, Arsuaga JL, Bermudez de Castro JM, Carbonell E, Bischoff JL, Dolo JM. 1999. Earliest humans in Europe: the age of TD6 Gran Dolina, Atapuerca Spain. Journal of Human Evolution 37:343-352.
Finlayson C, Pacheco FG, Rodriguez-Vidal J, Fa DA, Lopez JMG, Perez AS, Finlayson G, Allue E, Preysler JB, Caceres I, Carrion JS, Jalvo YF, Gleed-Owen CP, Espejo FJJ, Lopez P, Saez JAL, Cantal JAR, Marco AS, Guzman FG, Brown K, Fuentes N, Valarino CA, Villalpando A, Stringer CB, Ruiz FM, Sakamoto T. 2006. Late Survival of Neanderthals at the southernmost extreme of Europe. Nature 443:850-853.
Finlayson C, Carrion JS. 2007. Rapid ecological turnover and its impact on Neanderthal and other human populations. Trends in Ecology and Evolution 4:213-222.
Finlayson C, Brown K, Blasco R, Rosell J, Negro JJ, Bortolotti GR, Finlayson G, Marco AS, Pacheco FG, Vidal JR, Carrion JS, Fa DA, Rodriguez Llanes JM. 2011. Birds of a Feather: Neanderthal Exploitation of Raptors and Corvids. PLoS One 7:e45927.
Flouris AD, Spiropouos Y, Sakellariou GJ, Koutedakis Y. 2009. Effect of seasonal programming on fetal development and longevity: Links with environmental temperature. American Journal of Human Biology 21:214-216.
Franciscus RG. 1995. Late Pleistocene nasofacial variation in western Europe and Africa and modern human origins. Ph.D. Dissertation, University of New Mexico.
Franciscus RG. 2003. Internal nasal floor configuration in Homo with special reference to the evolution of Neandertal facial form. Journal of Human Evolution 44:701-729.
77
Franciscus RG, Long JC. 1991. Variation in human nasal height and breadth. American Journal of Physical Anthropology 85:419-427.
Franciscus RG, Trinkaus E. 1988. Nasal morphology and the Emergence of Homo erectus. American Journal of Physical Anthropology 75:517-527.
Frayer DW. 1997. Ofnet: Evidence of a Mesolithic massacre. In EL Martin, DW Frayer, editors . Troubled Times. New Yorks: Gordon & Breach.
Frayer D, Jelinek J, Oliva M, Wolpoff M. 2006. Aurignacian male crania, jaws and teeth from the Mladec caves, Moravia, Czech Republic. In: Early Modern Humans at the Moravian Gate: The Mladec Caves and their Remains. Teschler-Nicola M, editor. Vienna: Springer.
Gilligan I. 2007. Neanderthal extinction and modern human behavior: the role of climate change and clothing. World Archaeology 39:499-514.
Glass L, Silverman WA, Sinclair JC. 1968. Effect of the Thermal Environment on Cold Resistance and Growth of Small Infants after the First Week of Life. Pediatrics 41:1033- 1046.
Gorjanović-Kramberger D. 1906. Der diluviale Mensch von Krapina in Kroatien. Ein Beitrag zur Paläoanthropologie. Wiesbaden: Kreidel.
Gould SJ. 1977. Ontogeny and Phylogeny. Boston: Harvard University Press.
Gray H. 2008 Gray’s Anatomy: The Anatomical and Basis of Clinical Practice, 40th Edition. London: Churchill Livingston.
Grayson D, Delpech F. 2006. Was there increasing dietary specialization cross the Middle-to-Upper Paleolithic transition in France? In: Conard N, editor. When Neanderthals and Modern Humans Met. Tubingen: Springer Verlag.
Green M. 1990. Neandertal craniofacial growth: An ontogenetic model. M.A.thesis. Knoxville: University of Tennessee.
Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kircher M, Patterson N, Li H, Zhai W, Fritz MHY, Hansen NF, Durand EY, Malaspinas AS, Jensen JD, Marques-Bonet T, Alkan C, Prüfer K, Meyer M, Burbano HA, Good JM, Schultz R, Aximu-Petri A, Butthof A, Höber B, Höffner B, Siegemund M, Weihmann A, Nusbaum C, Lander ES, Russ C, Novod N, Affourtit J, Egholm M, Verna C, Rudan P, Brajkovic D, Kucan Ž, Gušic I, Doronichev VB, Golovanova LV, Lalueza-Fox C, Rasilla M, Fortea J, Rosas A, Schmitz RW, Johnson PLF, Eichler EE, Falush D, Birney E, Mullikin JC, Slatkin M, Nielsen R, Kelso J, Lachmann M, Reich D, Pääbo S. 2010. A Draft Sequence of the Neandertal Genome. Science 7:710-722.
78
Grün R, Stringer C. 1991. Electron spin resonance dating and the evolution of modern humans. Archaeometry 33:153-199.
Guipert G, Mafart B, Tuffreau A, de Lumley MA. 2007. 3D reconstruction and study of a new late Middle Pleistocene hominid: Blache-Saint-Vaast 2, Nord, France. American Journal of Physical Anthropology 44:121-122.
Gunz P, Harvati K. 2007. The Neanderthal “chignon”: Variation, integration, and homology. Journal of Human Evolution 52:262-274.
Gunz P, Neubauer S, Golovanova L, Doronichev V, Maureille B, Hublin JJ. 2012. A Uniquely Modern Human Pattern of Endocranial Development. Insights From a New Cranial Reconstruction of the Neandertal Newborn from Mezmaiskaya. Journal of Human Evolution 62:300-313.
Hamilton WJ, Boyd JD, Mossman HW. 1964. Human Embryology. Cambridge: W. Heffer and Sons Ltd.
Hardy B. 2004. Neanderthal behavior and stone tool function at the Middle Paleolithic site of La Quina, France. Antiquity 78:547-565.
Harrold F. 1980. A comparative analysis of Eurasian Paleolithic burials. World Archaeology 12:195-211.
Harvati K, Weaver TD. 2006. Human cranial anatomy and the differential preservation fo population history and climate sinatures. The Anatomical Record 288A:1225-1233.
Hatcher L, Stepanski E. 1994. A step-by-step approach to using the SAS system for univariate and multivariate statistics. Cary: SAS Institute Inc.
Hawks J, Wolpoff MH. Brief communication: paleoanthropology and the population genetics of ancient genes. American Journal of Physical Anthropology 114:269-272.
Hayden B. 1993. The cultural capacities of Neandertals. A review and reevaluations. Journal of Human Evolution 24:113-146.
Heaton JM. 1972. The distribution of brown adipose tissue in the human. Journal of Anatomy 112:35-39.
Heinrich H. 1988. Origin and consequences of cyclic ice rafting in the Northeast Atlantic Ocean during the past 130,000 years. Quaternary Research 29:142-152.
Henry AG, Brooks AS, Piperno DR. 2011. Microfossils in calculus demonstrate consumption of platns and cooked foods in Neanderthal diets (Shanidar III, Iraq; Spy I and II, Belgium). Proceedings of the National Academy of Sciences 108:486-491.
79
Hernandez M, Fox Cl, Garcia-Moro C. 1997. Fueguian Cranial Morphology: The Adaptation to a Cold, Harsh Environment. American Journal of Physical Anthropology 103:103-117.
Heslop D, Dekkers MJ, Langereis CG. 2002. Timing and structure of the mid-Pleistocene transition: records from the loess deposits of northern China. Palaeogeography, Palaeoclimatology, Palaeoecology 185:133-143.
Hill T, Lewicki P. 2007. STATISTICS: Methods and Applications. Tulsa: Statsoft.
Higham T, Ramsey CB, Karavanić, Smith FH, Trinkaus E. 2006. Revised direct radiocarbon dating of the Vindija G1 Upper Paleolithic Neandertals. Proceedings of the National Academy of Sciences 103:553-557.
Hoffecker JF, Cleghorn N. 2000. Mousterian Hunting Patterns in the Northwester Caucasus and the Ecology of the Neanderthals. International Journal of Osteoarchaeology 10:368-378.
Holton NE, Franciscus RG. 2008. The paradox of a wide nasal aperture in cold-adapted Neandertals: a causal assessment. Journal of Human Evolution 55:842-851.
Holloway R. 1981. Volumetric and asymmetry determinations on recent hominid endocasts; Spy I and II, Djebel Ihroud I, and the sale Homo erectus specimens, with some notes on Neandertal brain size. American Journal of Physical Anthropology 55:385-393.
Holloway R. 1983. Human paleontological evidence relevant to language behavior. Human Neurobiology 2:105-114.
Holloway R. 1985. The poor brain of Homo sapiens neanderthalensis: see what you please. In: Delson E, editor. Ancestors: The hard evidence. New York: Alan R. Liss.
Holloway R. 2000. Brain. In: Delson E, TattersalL I, Van Couvering J, Brooks A, editors. Encyclopedia of Human Evolution and Prehistory, 2nd edition. New York: Garland Publishing Inc.
Holloway R, de La Costeo-Lareymondie M. 1982. Brain endocast asymmetry in pongids and hominids: Some preliminary finds on the paleontology of cerebral dominance. American Journal of Physical Anthropology 58:101-110.
Holloway R, Broadfield DC, Yuan MS. 2004. The Human Fossil Record, Brain Endocasts – The Paleoneurological Evidence. New York: Wiley-Liss.
Holton NE, Franciscus RG. 2008. The paradox of a wide nasal aperture in cold-adapted Neandertals: a causal assessment. Journal of Human Evolution 55:942-951.
80
Howell FC. 1952. Pleistocene glacial ecology and the evolution of “Classic Neanderthal” man. Quarterly Review of Biology 32:377-410.
Howells WW. 1989. Skull Shapes and the Map. Craniometric Analyses in the Dispersion of Modern Homo. Papers of the Peabody Museum of Archaeology and Ethnology 79. Massachusetts: Cambridge.
Hu HH, Tovar JP, Pavlova Z, Smith ML, Gilsanz V. 2012. Unequivocal identification of brown adipose tissue in a human infant. Jouranl of Magnetic Resonance Imaging 35:938- 942.
Hubbe M, Hanihara T, Harvati K. 2009. Climate Signatures in the Morphological Differentiation of Worldwide Modern Human Populations. The Anatomical Record 292:1720-1733.
Hublin JJ, Spoor F, Braun M, Zonneveld F, Condemi S. 1996. A late Neanderthal associated with upper Paleolithic artifacts. Nature 381:224-226.
Huxley T. 1863. Evidence as to Man’s Place in Nature. London: Williams & Nortgate. Katzmarzyk PT, Leonard WR. 1998. Climatic influences on human body size and proportions: ecological adaptations and secular trends. American Journal of Physical Anthropology 106:483-503.
Janković I. 2004. Neandertals – 150 Years Later. Collegium Anthropologicum 2004: 379-401.
Joshi AS, Meyers AD. 2013. Skull Base Anatomy. Medscape http://emedicine.medscape.com/article/882627-overview#aw2aab6b3. Accessed 5/20/14.
Kasperbauer JL, Kern EB. 1987. Nasal valve physiology. Implications in Nasal Surgery. Otolaryngologic clinics of North America 20:699-719.
Karavanić I, Smith F. 1998. The Middle/Upper Paleolithic interface and the relationship of Neaderthals and early modern humans in the Hrvatsko Zagorje, Croatia. Journal of Human Evolution 34:223-248.
Katzmarzyk P, Leonard W. 1998. Climatic influences on human body size and proportions: ecological adaptations and secular trends. American Journal of Physical Anthropology 106:483-503.
King W. 1864. The reputed fossil man of Neanderthal. Quarterly Journal of Science 1:88- 97.
Kjaer I. 1990 Ossification of the Fetal Basicranium. Journal of Craniofacial Genetics and Developmental Biology10:29-38.
81
Klein R. 1999. The Human Career. Human Biological and Cultural Origins. Chicago: University of Chicago Press.
Klein R. 2003. Whither the Neanderthals. Science 299:1525-1527. Koertvelyessy T. 1972. Relationships between the Frontal Sinus and Climatic Conditions: A Skeletal Approach to Cold Adaptation. American Journal of Physical Anthropology 37:161-172.
Kohn LAP, Leigh SR, Jacobs SC, Cheverud JM. 1993. Effects of Annular Cranial Vault Modification on the Cranial Base and Face. American Journal of Physical Anthropology 90:147-168.
Krause J, Orlando L, Serre D, Viola B, Prüfer K, Richard MP, Hublin JJ, Hänni C, Derevianko AP, Pääbo S. 2007. Neanderthals in Central Asia and Siberia. Letters to Nature 449:902-904.
Kuhn S. 1995. Mousterian Lithic Technology: An Ecological Perspective. Princeton: Princeton University Press.
Laitman JT, Reidenberg JS, Marquez S, Gannon PJ. 1996. What the nose knows: New understandings of Neandertal upper respiratory tract specializations. Proceedings of the National Academy of Sciences 93:10543-10545.
Lean ME, James WP, Jennings G, Trayhurn P. 1986. Brown adipose tissue uncoupling protein content in human infants, children and adults. Clinical Science London 71:291- 297.
Lev E, Kislev M, Bar-Yosef O. 2005. Mousterian vegetal food In KEBARA Cave, Mt. Carmel. Journal of Archaeological Science 32:475-484.
Li Q, Wang P, Zhao Q, Tian J, Chen X, Jian Z. 2008. Paleoceanography of the mid- Pleistocene South China Sea. Quaternary Science Reviews 27:1217-1233.
Lieberman DE. 2011. The Evolution of the Human Head. Cambridge: The Belkap Press of Harvard University Press.
Lieberman DE, McCarthy RC. 1999. The Ontogeny of Cranial Base Angulation in Humans and Chimpanzees and its Implication for Reconstructing Pharyngeal Dimensions. Journal of Human Evolution. 36:487-517.
Lieberman DE, Ross CF, Ravosa MJ. 2000. The Primate Cranial Base: Ontogeny, Function, and Integration. Yearbook of Physical Anthropology 43:117-169.
Lieberman DE, Hallgrimsson B, Liu W, Parsons TE, Jamniczky HA. 2008. Spatial Packing, Cranial Base Angulation, and Craniofacial Shape Variation in the Mammalian Skull: Testing a New Model Using Mice. Journal of Anatomy 212:720-735.
82
Lieberman MD, Cunningham WA. 2009. Type I and Type II errors concern fMRI research: re-balancing the scale. Social Cognitive and Affective Neuroscience 4:423-428.
Lilja C, Olsson U.1987. Change in embryonic development associated with long-term selection for high growth rate in Japanese Quail. Growth 51:301-308.
Marean C. 1998. A critique of the evidence of scavenging by Neandertals and early modern humans: New data from Kobeh Cave (Zagros Mountains, Iran) and Die Kelders I Layer 10 (South Africa). Journal of Human Evolution 35:111-136.
Marquet J, Lorblachet M. 2003. A Neanderthal face? The proto-figure from La Rochet- Cotard, Langeais (Indreet Loire, France) Antiquity 77:661-670.
Marshack A. 1989. Evolution of the human capacity: The symbolic evidence. Yearbook of Physical Anthropology 32:1-34.
Maureille B, Houët F. 1997. Nouvelles données sur des charactéristiques derives du massif facial supérieur des Néandertaliens. Archaeologie et Préhistoire 108:89-98.
McCollum MA. 1999. The robust australopithecine face: A morphometric perspective. Science 284:301-305.
McDonald JH. 2009. Handbook of Biological Statistics. Baltimore: Sparky House Publishing.
Mellars P. 1996. The Neanderthal Legacy: An Archaeological Perspective from Western Europe. Princeton: Princeton University Press.
Mercier N, Vallads H, Bar-Yosef O, Vandermeersch B, Stringer C, Joron JL. 1993. Thermoluminescence Date for the Mousterian Burial Site of Es-Skhul, Mt. Carmel. Jouranl of Archaeological Science 20:169-174.
Minugh-Purvis N. 1988. Pattern of craniofacial growth and development in Upper Pleistocene hominids. Ph.D. thesis, University of Pennsylvania.
Monet-White A. 1996. Le Paléolithique en ancienne Yougoslavie. Grenoble: Millon.
Mooney MP Siegel MI. 1991. Premaxillary-maxillary suture fusion and anterior nasal tubercle morphology in the chimpanzee. American Journal of Physical Anthropology 85:451-456.
Mooney MP, Siegel MI, Kimes KR, Todhunter J, Janosky J. 1992. Multivariate analysis of second trimester midfacial morphology in normal and cleft lip and palate human fetal specimens. American Journal of Physical Anthropology 88:203-209.
83
Movius H. 1950. A wooden spear of third ingterglacial age from Lowe Saxony. Southwestern Journal of Anthropology 6:139-142.
Münzel S, Conard N. 2004. Change and continuity in subsistence during the Middle and Upper Paleolithic in the Ach Valley of Swabia (South-west Germany). International Journal of Osteoarchaeology 14:225-243.
Murray LJ, O’Reilly DP, Betts N. 2000. Season and outdoor ambient temperature: effects on birth weight. Obstetrics and Gynecology 96:689-695.
Neftali S, Rosenfeld M, Wolf M, Elad D. 2005. The Air-Conditioning Capacity of the Human Nose. Annals of Biomedical Engineering 33:545-553.
Neubauer S, Gunz P, Hublin JJ. 2010. Endocranial Shape Changes During Growth in Chimpanzees and Humans: A Morphometric Analysis of Unique and Shared Aspects. Journal of Human Evolution 59:555-566.
Noback ML, Harvati K, Spoor F. 2011. Climate-Related Variation of the Human Nasal Cavity. American Journal of Physical Anthropology 145:599-614.
Nowaczewska W, Dabrowski P, Kuzminski L. 2011. Morphological Adaptation to Climate in Modern Homo sapiens Crania: The Importance of Basicranial Breadth. Collegium Antropologicum 3:625-636.
OpenStax College. 2013. The Skull. OpenStax-CNX Website. Accessed May 26, 2014 http://cnx.org/content/m46355/1.4/.
Ouellet V, Labbe SM, Blondin DP, Phoenix S, Guerin B, Haman F, Turcotte EE, Richard D, Carpentier AC. 2012. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. Journal of Clinical Investigation 122:545-552.
Ovchinnikov I, Götherström A, Romanova G, Kharitonov V, Lindén K, Goodwin W. 2000. Molecular analysis of Neanderthal DNA from the Northern Caucasus. Nature 404:490-493.
Pares JM, Perez-Gonzalez A. 1995. Paleomagnetic age for hominid fossils at Atapuerca archaeological site in Spain. Sciece 269:830-832.
Pettitt PB. 2000. Neanderthal Lifecycles: Developmental and Social Phases in the Lives of the Last Archaics. World Archaeology 31:351-366.
Plavcan JM. 2012. Body Size, Size Variation, and Sexual Size Dimorphism in Early Homo. Current Anthropology 53:S409-S423.
84
Plavcan JM, Cope D. 2002. Metric Variation and species recognition in the fossil record. Evolutionary Anthropology 10:202-222.
Ponce de Leon MS, Golovanova L, Doronichev V, Romanova G, Akazawa T, Kondo O, Ishida H, Zollikofer CPE. 2008. Neandertal Brain Size at Birth Provides Insights into the Evolution of Human Life History. Proceedings of the National Academy of Sciences 105:13764-13768.
Prüfer Kay, Racimo F, Ptternson N, Jay Fl, Sakararaman S, Sawyer S, Heinze A, Renaud G, Sudmant PH, de Filippo C, Li H, Mallick S, Dannemann M, Fu Q, Kircher M, Kuhlwilm M, Lachmann M, Meyer M, Ongyerth m, Siebauer M, Theunert C, Tandon A, Moorjani P, Pickrell J, Mullikin JC, Vohr SH, Green RE, Hellmann I, Johnson PLF, Blanche H, Cann H, Kitzman JO, Shendure J, Eichler EE, Lein ES, Bakken TE, Golovanova LV, Doronichev VB, Shunkov MV, Derevianko AP, Viola B, Slatkin M, Reich D, Kelso J, Paabo S. 2014. The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505:43-49.
Rae TC, Hill RA, Hamada Y, Koppe T. 2003. Clinal Variation of Maxillary Sinus Volume in Japanese Macaques (Macaca fuscata). American Journal of Primatology 59:153-158.
Rae TC, Vioarsdottir US, Jeffery N, Steegmann AT. 2006. Developmental Response to Cold Stress Cranial Morphology of Rattus: Implications for the Interpretation of Climatic Adaptation in Fossil Hominins. Proceedings of the Royal Society B 273:2605-2610.
Rae TC, Koppe T, Stringer CB. 2011. The Neandertal Face is Not Cold Adapted. Journal of Human Evolution 60:234-239.
Raghaven P, Bulbeck D, Pathmanathan G, Rathee SK. 2013. Indian Craniometric Variability and Affinities. International Journal of Evolutionary Biology 2013.
Rak Y. 1986. The Neandertal: a new look at an old face. Journal of Human Evolution 15:151-164.
Reidenberg JS, Laitman JT. 1991. Effect of Basicranial Flexion on Larynx and Hyoid Position in Rats: An Experimental Study of Skull and Soft Tissue Interactions. Anatomical Record 230:557-569.
Rigaud J, Simek J, Ge T. 1995. Mousterian fires from the Grotte XVI (Dordogne, France). Antiquity 69:902-912.
Rightmire GP. 2012. The evolution of cranial form in mid-Pleistocene Homo. South African Journal of Science 108:68-77.
Rink W, Schwarcz K, Smith F, Radovičić J. 1995. ESR ages for Krapina hominids. Nature 378:24.
85
Roberts DF. 1978. Climate and Human Variability. Menlo Park: Cummings Publishing Company.
Roebroeks W, Gamble C. 1999. The Middle Palaeolithic Occupation of Europe. Leiden: University of Leiden Press.
Roebroeks W, Conard NJ, van Kolfschoten T. 1992. Dense forests, cold steppes, and the Paleolithic settlement of Northern Europe. Current Anthropology 33:551-586.
Rosas A, Bastir M, Martínez-Maza C, García-Tabernero A, Lalueza-Fox C. 2006. Inquiries into Neanderthal Cranio-Facial Development and Evolution: ‘Accretion’ vs ‘Organismic’ Models. In: Harvati K, Harrison T, editors. Neanderthals Revisited. New York: Springer Verlag. p 38-69.
Roseman CC. 2004. Detecting Interregionally Diversifying Natural Selection on Modern Human Cranial Form by Using Matched Molecular and Morphometric Data. Proceedings of the National Academy of Sciences 101:12824-12829.
Roseman CC, Weaver TD. 2004. Multivariate apportionment of gloval human craniometric diversity. American Jouranl of Physical Anthropology 125:257-263.
Ruff C, Trinkaus E, Holliday T. 1997. Body mass and encephalization in Pleistocene Homo. Nature 387:173-176.
Russell M. 1985. The supraorbital torus: “A most remarkable peculiarity.” Current Anthropology 26:337-360.
Sankararaman S, Patterson N, Li H, Pääbo S, Reich D. 2012. The Date of Interbreeding between Neandertals and Modern Humans. PLoS Genetics 8:e1002947.
Sankararaman S, Mallick S, Dannemann M, Prüfer K, Kelso J, Pääbo S, Patterson N, Reich D. 2014. The genomic landscape of Neanderthal ancestry in present-day humans. Letters to Nature 10:12961.
Sardi ML, Rozzi FVR. 2012. Different Cranial Ontogeny in Europeans and Southern Africans. PLoS One 7:e35917.
Schaaffhausen H. 1858. Zur Kenntniβ der ältensen Rassenschädel. Müllers Archiv 5:453- 478.
Schaaffhausen H. 1888. Der Neanderthaler Fund. Bonn: Marcus.
Scherer PW, Hahn I, Mozell MM. 1989. The biophysics of nasal airflow. Otolaryngologic Clinics of North America 22:265-278.
86
Schliegl S, Goldberg P, Pfretschner H, Conard N. 2003. Paleolithic burnt bone horizons from the Swabian Jura: Distinguishing between in situ fireplace and dumping areas. Geoarchaeology 18:541-565.
Schmitz RW, Serre D, Bonani G, Feine S, Hillgruber F, Krainitzki H, Pääbo S, Smith, FH. 2002. The Neandertal type site revisisted: Interdisciplinary investigations of skeletal remains from the Neander Valley, Germany. Proceedings of the National Academy of Sciences 99:13342-13347.
Schwalbe G. 1906. Studien zur Vorgeschichte des Menschen. Stuttgart: Schweizerbart’sche.
Searle SR, Speed FM, Milliken GA. 1980. Population Marginal Means in the Linear Model: An Alternative to Least Squares. The American Statistician 34:216-221.
Schackleton NJ, Fairbanks rg, Tzu-chien Chiu, Parrenin F. 2004. Absolute calibration of the Greenland time scale: implications for Antarctic time scales and for C14. Quaternary Science Reviews 23:1512-1522.
Shae BT. 1977. Eskimo craniofacial morphology, col stress and the maxillary sinus. American Journal of Physical Anthropology 47:289-300.
Siega-Riz AM, Adair LS, Hobel CJ. 1996. Maternal Underweight Status and Inadequate Rate of Weight Gain During the Third Trimester of Pregnancy Increases the Risk of Preterm Delivery. The Journal of Nutrition 126:146-153.
Skinner M, Gordon A, Collard N. 2006. Mandibular size and shape variation in the hominins at Dmanisi, republic of Georgia. Journal of Human Evolution 51:36-49.
Slimak L, Svendsen JI, Mangerud J, Plisson H, Heggen HP, Brugère A, Pavlov PY. 2011. Late Mousterian Persistence near the Arctic Circle. Sciences 332:841-845.
Smith FH. 1982. Upper Pleistocene hominid evolution South Central Europe” a review of the evidence and analysis of trends. Current Anthropology 23:667-703.
Smith FH. 1983. Behavioral interpretations of changes in craniofacial morphology across the archaic/modern Homo sapiens transition. In: Trinkaus E, editor. The Mousterian Legacy: human biocultural change in the Upper Pleistocene. Oxford: British Archaeological Reports.
Smith FH. 1984. Fossil hominids from the Upper Pleistocene of Central Europe and the origin of modern Europeans. In: Smight FH, Spencer F, editors. The Origins of Modern Humans: A world Survey of the Fossil Evidence. New York: Liss. Pp. 137-209.
Smith FH. 1991. The Neandertals: Evolutionary dead ends or ancestors of modern people. Journal of Anthropological Research 47:219-238.
87
Smith FH. 2013. The Fate of the Neandertals. Journal of Anthropological Research 69:167-200.
Smith FH, Raynard G. 1980. Evolution of the supraorbital region in Upper Pleistocene fossil hominids from South Central Europe. American Journal of Physical Anthropology 53:589-609.
Smith FH, Falsetti A, Donnelly S. 1989. Modern human origins. Yearbook of Physical Anthropology 32:35-68.
Smith FH, Trinkaus E, Pettitt PB, Karavanić I, Paunović M. 1999. Direct radiocarbon dates for Vindija G1 and Velika Pećina Late Pleistocene hominid remains. Proceedings of the National Academy of Sciences 96:12281-12286.
Smith F, Smith M, Schmitz R. 2006. Human skeletal remains from the 1997 and 2000 excavations of cave deposits derived from Kleine Feldhofer Grotte in the Neander Valley, Germany. In: Schmitz 2006: 187-246.
Smith TM, Toussaint M, Reid DJ, Olejniczak AJ, Hublin JJ. 2007. Rapid Dental Development in a Middle Paleolithic Neanderthal. Proceedings of the National Academy of Sciences 104:20220-20225.
Soressi M, McPherron SP, Lenoir M, Dogandzic T, Goldberg P, Jacobs Z, Maigrot Y, Martisius NL, Miller CE, Rendu W, Richards M, Skinner MM, Steele TE, Talamo S, Texier JP. 2013. Neandertals made the first specialized bone tools Europe. Proceedings of the National Academy of Sciences 110:14186-14190.
Stearns SC. 1982. The role of development in the evolution of live histories. In: Bonner JT, editor. Evolution and Development. Berlin: Springer-Verlag.
Stearns SC, Koella JC. 1986. The evolution of phenotypic plasticity in life-history traits: predictions of reaction norms for age and size at maturity. Evolution 40:893-913.
Steegmann AT, Platner WS. 1968. Experimental Cold Modification of Cranio-Facial Morphology. American Journal of Physical Anthropology 28:17-31.
Stepanchuk V. 1993. Prolom II, a Middle Paleolithic cave in the eastern Crimea with non-utilitarian bone artifacts. Proceedings of Paleolithic Society 9:17-37.
Stewart TD. 1977. The Neanderthal skeletal remains from Shanidar Cave, Iraq: A summary of findings to date. Proceedings of the American Philosophical Society 121:121-165.
Strand LB, Barnett AG, Tong S. 2012. Maternal exposure to ambient temperature and the risks of preterm birth and stillbirth in Brisbane, Australia. American Jouranl fo Epidemiology 175:99-107.
88
Straus L. 1989. Grave reservations: More on Paleolithic burial evidence. Current Anthropology 30:633-634.
Stringer CB, Grun R, Schwarcz HP, Goldberg P. 1989. ESR dates for the hominid site of Es Skhul in Israel. Letters to Nature 338:756-758.
Suzuki H, Takai F. 1970. The Amud Man and His Cave. Tokyo, Japan: Academic Press.
Svoboda J. 2006. The Danube Gate to Europe: Patterns of chronology, settlement archaeology, and demography of late Neandertals and early modern humans of the Middle Danube. In: Conard N, editor. When Neanderthals and Modern Humans Met. Tubingen: Springer Verlag.
Tattersall I. 1986. Species recognition in human paleontology. Journal of Human Evolution 15:165-175.
Tattersall I. 1992. Species concepts and species identification in human evolution. Journal of Human Evolution 22:341-349.
Tattersall I, Schwartz J. 1999. Hominids and hybrids: the place of Neanderthals in human evolution. Proceedings of the National Academy of Sciences 96:7117-7119.
Thomson A, Buxton LHD. 1923. Man’s nasal index in relation to certain climatic conditions. Journal of the Royal Anthropological Institute 37:193-222.
Tobias P. 1971. The Brain in Human Evolution. New York: Columbia University Press.
Toftum J, Jorgensen AS, Fanger PO. 1998. Upper limits of air humidity for preventing warm respiratory discomfort. Energy and Buildings 28:15-23.
Trinkaus E. 1983. The Neanderthal face: evolutionary and functional perspectives on a recent hominid face. Journal of Human Evolution 16:429-443.
Trinkaus E. 1986. The Neandertals and modern human origins. Annual Review of Anthropology 15:193-218.
Trinkaus E. 1987. The Neandertal face: evolutionary and functional perspectives on a recent hominid face. Journal of Human Evolution 16:429-443.
Trinkaus E. 1995. Neandertal Mortality Patterns. Journal of Archaeological Sciences 22:121-142.
Trinkaus E. 2003. Neandertal Faces Were Not Long; Modern Human Faces are Short. Proceedings of the National Academy of Sciences 100:8142-8145.
89
Trinkaus E. 2012. Neandertals, early modern humans, and rodeo riders. Journal of Archaeological Science 39:3691-3693.
Trinkaus E, Zilhão J. 2002. Phylogenetic implications. In: Zilhão J, editor. Portrait of the artist as a child. The Gravettian human skeleton from the Abrigo do Lagar Velho and its archaeological context. Trabalhos Arquelogia.
Valladas H, Joron JL, Valladas G, Arensburg B, Bar-Yosef O, Belfer-Cohen A, Goldberg P, Laville H, Meignen L, Rak Y, Tchernov E, Tillier AM, Vandermeersch B. 1987. Thermoluminescence dates for the Neanderthal burial site at Kebara in Israel. Letters and Nature 330:159-160.
Vandermeersch B. 1976. Les sépultures néandertaliennes. In: H. deLumley, editor. La Préhistoire Francais, Volume I. Paris: CNRS. 725-727.
Vlček E. 1973. Postcranial skeleton of a Neandertal child from Kiik-Koba, U.S.S.R. Journal of Human Evolution 2:537-544.
Virchow R. 1872. Untersuchung des Neanderthal-Schädels. ZE 4:157-165.
Wagner GA, Krbetschek M, Degering D, Bahain JJ, Shao Q, Falgueres C, Voinchet P, Dolo JM, Garcia T, Rightmire GP. 2010. Radiometric dating of the type-site for Homo heidelbergensis at Mauer, Germany. Proceedings of the National Academy of Sciences 107:19726-19730.
Weaver TD. 2009. The meaning of Neandertal skeletal morphology. Proceedings of the National Academy of Sciences 106:16028-16033.
Weaver TD, Roseman CC, Stringer CB. 2007. Were Neandertal and modern human cranial differences produced by natural selection or genetic drift? Jouranl of Human Evolution. 53:135-145.
Weiner JS. 1954. Nose shape and climate. American Journal of Physical Anthropology 12:615-618. Weinfurt KP. 1995. Multivariate Analysis of Variance. In: Grimm, LK, Yarnold PR, editors. Reading and Understanding Multivariate Statistics. Washington D.C.: American Psychological Association. P 245-276.
Wells JCK. 2012. Sexual dimorphism in body composition across human populations: associations with climate and proxies for short- and longer-term energy supply. American Journal of Human Biology 24:411-419.
Wen S, Goldenberg RL, Cutter GR, Hoffman HJ, Cliver SP. 1990. Intrauterine growth retardation and preterm delivery: prenatal risk factors in an indigent population. American Journal of Obstetrics and Gynecology 162:213-218.
90
White T. 2003. Early hominids – Diversity or distortion? Science 299:1994-1997.
Wolpoff MH. 1979. The Krapina dental remains. American Journal of Physical Anthropology 50:67-113.
Wolpoff MH. 1999. Paleoanthropology. New York: McGraw Hill.
Wolpoff MH, Smith FH, Malex M, Radovcic J, Rukavina D. 1981. Upper Pleistocene human remains from Vindija cave, Croatia, Yugoslavia. American Jouranl of Physical Anthropology 54:499-545.
Yokley TR. 2006. The functional and adaptive significance of anatomical variation in recent and fossil human nasal passages. Ph.D. Dissertation, Duke University.
Yokley TR. 2009. Ecogeographic Variation in Human Nasal Passages. American Journal of Physical Anthropology 138:11-22.
Yokley TR. 2014. Parallel climatic adaptation in the nasal anatomy of humans and bears. Poster presented at the 84th annual conference of the American Association of Physical Anthropologists in Calgary, Alberta.
Yokley TR, Holton NE. 2013. Re-evaluating the functional and adaptive significance of Neandertal nasofacial anatomy. Poster presented at the 83rd annual conference of the American Association of Physical Anthropologists in Knoxville, Tennessee.
Zilhão J. 1998. The Extinction of Iberian Neandertals and its Implications for the Origins of Modern Humans in Europe. Proceedings of the XIII International Congress of Prehistoric and Protohistoric Sciences (Forli, Italy), 8-14 September 2:299-312.
Zilhão J. 2011. Aliens from Outer Time? Why the “Human Revolution” is Wrong, and Where Do We Go From Here? In: Condemi S, Weniger GC, editors. Continuity and Discontinuity in the Peopling of Europe. New York: Springer.
Zilhão J. 2012. Personal Ornaments and Symbolism Among the Neandertals. In: Elias S, editor. Origins of Human Innovation and Creativity. Amsterdam: Elsevier.
Zilhão J, d’Errico F, Bordes JG, Lenoble A, Texier JP, Rigaud JP. 2006. Analysis of Aurignacian interstratification at the Châtelperronian-type site and implications for the behavioral modernity of Neandertals. Proceedings of the National Academy of Sciences 103:12643-12648.
Zilhão J, Angelucci DE, Badal-Garcia E, d’Errico F, Daniel F, Dayet L, Douka K, Higham TGF, Martinez-Sanchez MJ, Montes-Bernardez R, Murcia-Mascaros S, Perez- Sirvent C, Roldan-Garcia C, Vanhaeren M, Villaverde V, Wood R, Zapata J. 2010. Symbolic use of marine shells and mineral pigments by Iberian Neandertals. Proceedings of the National Academy of Sciences 107:1023:1028.
91
Zollikofer CPE, Ponce De Leon MS. 2004. Kinematics of Cranial Ontogeny: Heterotopy, Heterochrony, and Geometric Morphometric Analysis of Growth Models. Journal of Experimental Zoology Part B: Molecular Developmental Evolution 302B:322-34.
92