UNIVERSITY OF WARSAW FACULTY OF HISTORY
ELŻBIETA JASKULSKA
ADAPTA TION TO COLD CL IMATE
IN THE
NASAL C AVITY SKELET O N
A Comparison of Archaeological Crania from Different Climatic Zones
Ph.D. Dissertation
SUPERVISOR:
Dr hab. prof. UW Arkadiusz Sołtysiak
INSTITUTE OF ARCHAEOLOGY
WARSAW 2014
CONTENTS
Acknowledgements ...7
Introduction ...9
Part I ... 13
Chapter I. Adaptationism in the biological sciences ... 15
Comparison of adaptational research of humans and animals ... 17
Cultural adaptation ... 19
Research strategies in human adaptation studies ... 21
Adaptational terminology... 22
Adaptation ... 24
Acclimatization and acclimation ... 25
Chapter II. Morphology and physiology of the nose ... 27
Morphology ... 27
Physiology ... 34
Chapter III. Review of the current state of research of body adaptation to cold .... 39
Cold adaptations in anatomically modern humans ... 40
Physiological changes ... 40
Morphological changes ... 41
Body anthropometrics ... 42
Craniometry ... 44
Adaptation to cold climate in hominids ... 47
Body anthropometrics ... 48
Homo erectus ... 49
Neanderthal ... 50
Chapter IV. Adaptational value of nasal features — review of current state of
research ... 52
Research into cold adaptation in the nasal features of anatomically modern
humans ... 54
Nasal index – Thomson rule ... 54
Nasal protrusion ... 58
Paranasal sinuses ... 60
Nasal conchae ... 63
Choanae ... 64
Research of the cold adaptation in nasal features of hominids ... 65
Homo erectus ... 65
Neanderthals ... 67
Part II ... 77
Chapter V. New point of view — research hypotheses ... 79
Chapter VI. Material ... 82
Eskimos ... 82
Greenland Norse ... 83
Medieval Danes ... 83
Nubians ... 84
Climatic conditions in researched samples ... 85
Chapter VII. Methods ... 90
Data collection methods ... 90
Photos and SigmaScan® Pro ... 90
Osteometry... 93
Statistical methods ... 93
Chapter VIII. Results ... 96
Homogeneity of the samples ... 96
Eskimos ... 96
Nubians ... 97
Description of variables ... 99
Measurement error ... 104
Sexual dimorphism in researched samples ... 107
Nasal measurements as an unit in cranial morphology ... 114
Ecogeographical correlations of nasal measurements... 119
Shape analysis ... 125
Chapter IX. Discussion ... 132
Nasal measurements as an independent unit ... 132
Nasal measurements as a part of cranial morphology ... 135
NAsal index ... 137
understanding Neanderthal nasal morphology ... 139
Chapter X. Conclusions ... 143
Literature Cited ... 145
ACKNOWLEDGEMENTS
The present dissertation would not have been possible without the Danish Rectors’
Conference Scholarship which allowed me to do research in the Laboratory of Bio-
logical Anthropology, Panum Institute, University of Copenhagen. Therefore I
would like to express my special appreciation and thanks to Professor Niels
Lynnerup, who not only had allowed me to study the skeletal collection of this la-
boratory, but also introduced me to research methods of modern biological anthro-
pology, encouraged my research and has given priceless advice during whole five
month stay in Copenhagen. He had not only granted me access to the material to
work with, but also taught me enough to give me some sense of the anthropologi-
cal science. I would also like to thank my colleague Dr. Arkadiusz Sołtysiak, who
was brave enough to take my never ending research and half-written text under
his supervision, and put a lot of hard work to point out what needed to be done to
produce acceptable dissertation. Dr. Wiesław Więckowski was kind to discuss with
me my theories on the paleoanthropological aspect of research topic and to consult
the chapters where they were presented. Last but not least I would like to thank
Professor Wojciech Nowakowski, without whose final push the dissertation could
still be long coming.
INTRODUCTION
Relations between humans and the environment they occupy has been one of the main research areas since the beginnings of anthropology, both in its cultural and biological aspects, though it is worth mentioning that the intraspecies diversity of Homo sapiens, easily observed by the “naked eye”, has been a fascinating problem acknowledged since antiquity, as proven by works assigned to Hippocrates (Air, Waters and Places, transl. F. Adams, 1891). In the nascence of modern biological science, the rapid spread of our species, spanning the globe and conquering even the harshest and least comfortable environments, seemed the perfect example of Darwinian evolutionary theory, which in that aspect seemed to follow previous notions of human species as the pinnacle of the animal kingdom. Even as late as in the seventies of the last century, human adaptation research was described as one of the main topics of anthropology (Beals 1972, 85).
Early descriptions of possible adaptational traits in humans were directly derived from ideas about the origins of races, and as such were used as arguments for bet- ter or worse adaptation of different populations. The results of such scientific re- search were to prove the higher or lower evolutionary position of said populations (considered races). These theories underlie some of the political movements of the 20
thcentury (Ruff 1994, 65–66) and this unwanted heritage of research on inter- species diversity, including study of adaptation to environment, has strongly in- fluenced the decline in popularity of the subject in anthropological research. This trend continues, though other aspects influence it and the morphological research of adaptation in Homo sapiens has been rather abandoned in contemporary sci- ence, though the situation seems to have changed in the last decade. This trend can be explained by changes in the concept of adaptation within the biological sci- ences (Rose and Lauder 1996, 2). The history of research into human adaptation is further discussed in Chapter III. Review of the current state of research of body ad- aptation, p. 39.
Putting the whole political and historical influences aside, the problem of adapta-
tion in humans is still very much an uncharted part of human biology. Therefore it
is improbable that such research will be completely abandoned by evolutionary
biologists and anthropologists. Evolutionary theory assumes that species adapt to the environment they live in, or become extinct, and climate is one of the most im- portant, and also most variable elements of environment. It then has to be ex- pected that its role in natural selection cannot be ignored. Knowing that this fac- tor was influencing life on Earth from very beginning, it has to be assumed that it also played a major role in shaping the Homo sapiens species and in forming ob- served intraspecies variations (Beall and Steegmann 2000, 163). In this way the study of adaptational traits can also shed light on the evolutionary history of mankind (see: Adaptation to cold climate in hominids p. 47).
Adaptation in modern humans can be considered a real challenge for evolutionary researchers. Several studies underline that many traits from the earliest era of humanity have remain mostly unchanged today, allowing for the accurate descrip- tion encapsulated in the phrase “man is a tropical animal”. Clark and Edholm summarized in their book “Man and his thermal environment” that humans are well adapted to climate in sub-Saharan Africa, where they evolved (Clark and Edholm 1985, 134). The features that are unaltered allowed for a more comforta- ble life in the hot, rather dry climate of grassy savanna, i.e. the great number of eccrine sweat glands, the highest in mammals, or the pronounced lack of hair (Clark and Edholm 1985, 134). Therefore it is justified to assume that at the out- set of Homo evolution the earliest populations were exposed to such environments.
And during the later scattering of the species to nearly all existing environments and conditions of the globe there occurred selection, due to the different surround- ings encountered by migration or changing climatic patterns, which helped devel- op different responses observed as part of intraspecies variation today. Of course, the adaptation was never solely of a biological nature, as the unique cultural ad- justment obviously played a major role in inhabiting new areas. And the results of both mechanisms can be described by the popular citation by Ferdinand Wrangel from his “Narrative of an Expedition to the Polar Sea in the Years 1820-23”: “Man is a creature fit for any climate, and necessity and determination soon reconcile him to anything.” (1840, after: Proctor, Andersen, and Lundqvist 1977, 16).
The coexistence of both biological and cultural factors in human adaptation, in
connection with the inability to study the human biological response in the same
ways as other species provokes the question of the validity of such research. But even the role of cultural changes cannot be denied; in my opinion there is at least one important body function which is poorly influenced by cultural inventions:
breathing. Breathing is essential for living even more than any other life support-
ing activities (Laitman et al. 1996, 10543), and there is no cultural protection
against inhaling the frigid arctic air (Shea 1977, 297). The role of the nose and
mouth in the proper conditioning of the inspired air can be quite intense, and
some analyses shows that the increased calorie intake in populations of cold cli-
matic zones can be traced not to general body response to cold temperature, but
rather the energy spent on conditioning inspired air (Shea 1977, 297). The amount
of air inspired by an adult during normal daily activities equals 17 kilograms, or
about 14,000 liters of air over 24 hours (Franciscus and Trinkaus 1988, 524; Cole
1982a, 353–354). The proper warming and humidifying of such an amount of air
can take significant energy. Optimally the air reaching the lungs should match
internal body conditions, with a temperature of 37°C (body core temperature) and
about 40 grams of water per kilogram of air for proper humidity (Franciscus and
Trinkaus 1988, 524). Failure to comply with those requirements can result in seri-
ous health problems, such as chronic bronchitis, constricted pulmonary vessels
and even pulmonary edema (Beall and Steegmann 2000, 166). The energy re-
quired to achieve proper conditioning of air are greatly influenced by climatic cir-
cumstances, and for example an individual breathing dry air at 17°C requires a
daily amount of 400 Cal to moisten the air and 80 Cal to warm it (Cole 1982a,
353–354). Research shows that this amount can be approximately multiplied ten-
fold when the temperature falls below -30°C, taking about 25% of total heat pro-
duction (Shea 1977, 297). Environmental stress plays a major role in the physiolo-
gy and morphology of the upper airways, and especially the nasal features, as the
actual exchange of heat and moisture takes place when the inspired air passes the
nasal septum and conchae (Shea 1977, 297). The selection process is probably even
more active in neonates, who are preferential nose breathers because of the mor-
phology of the mouth and tongue, as well as neurological and behavioral factors
(Djupesland and Lødrup Carlsen 1998, 99). But though some of the morphological
traits, like proportions of pyriform aperture, or nasal projection have a long histo-
ry of research attempting to correlate them with environmental factors
(Franciscus and Trinkaus 1988, 523–524), it has been emphasized that the actual workings of the nose and its parts remain largely unexplored (Rouadi et al. 1999, 400).
These observations show that there is still potential for adaptational research of
the nasal area, even considering the long history of research, which prompted my
own research and this dissertation. The actual presentation of its aims and pro-
posed hypotheses indicated in Chapter V. New point of view — research hypothe-
ses, p. 79, requires a review of the current state of research and the most im-
portant problems indicated by previous works, which form Part I of the disserta-
tion. The analysis of the researched traits and their probable adaptational mean-
ing constitute Part II.
PART I
CHAPTER I
ADAPTATIONISM IN THE BIOLOGICAL SCIENCES
In the Introduction on p. 9 I mentioned that one of the reasons for the unpopulari- ty of adaptational research in contemporary biological science, and specifically in anthropology, was the rather dramatic change in scientific approach to the sub- ject, which took place over the last 30 years. Some scientists simply divide evolu- tionary biology, and, more importantly, adaptational research into periods ‘before’
and ‘after’ publication of the groundbreaking paper of Gould and Lewontin titled
“The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptationist programme” (Gould and Lewontin 1979). As Rose and Lauder ex- plained in the the introduction to the “Adaptation”, the impact of their article, fur- ther deepened by later papers by other authors, has turned the very term
‘adaptationism’, or even ‘adaptation’ into an unwanted and pejorative one (Rose and Lauder 1996, 2). They argued that Gould and Lewontin, by focusing on the errors of contemporary adaptational research, which often stood in opposition to the original Darwinian concept of evolution, have made this whole branch of evo- lutionary research obsolete and unwanted.
The problems of studying adaptational traits were of course recognized much ear- lier, considering how long this kind of research was popular. The effects of the en- vironmental conditions on different populations, especially human populations, were the source of wonder and philosophical reflection since antiquity. These con- siderations have usually incorporated not only biological, but also cultural differ- ences between various peoples, which, according to authors, were determined by some climatic characteristics (Ruff 1994, 65; see also: Part 14 – Part 24 of Air, Wa- ters and Places, transl. F. Adams, 1891).
Many of the early studies were more concerned with describing how the popula-
tions differ in morphology and physiology, and later also genetics, than with ex-
plaining how such a change can be attributed to climatic, or more generally, envi-
ronmental influence (Baker 1976, 230). Comments as early as in the beginning of
the second part of the 20th century have stressed the popular opinion that genetic
variation in human populations is an effect of natural selection caused exclusively
by environmental factors, and has not taken into account knowledge of other fac- tors (e.g. nutrition, infectious diseases, or effects of genetic drift), which obviously can influence the results (Baker 1976, 231). Furthermore the inherent problem with the traditional approach to research of adaptation was the inability to con- trol all of the variables potentially influencing a studied trait. It is not only impos- sible to negate their impact, but they can also obscure observed trends (R. W.
Newman 1975, 90). This problem generally results from the obvious limitations of the research done on humans, where the experimental method must be severely modified, as they cannot be subjected to long term control. This effectively re- stricts not only research methods, but also influences possible outcomes (Baker 1976, 232). The importance of proper experimental techniques was stressed by Brown (1954, 343–344) who described initial problems with experimental research of the acclimatization to the cold, where laboratory results contradicted field ob- servations of the studied phenomenon. Some researchers also stressed the faulty selection of test subjects. Newman in 1975 has criticized the tendency to restrict the research of human adaptation and acclimatization to climate nearly exclu- sively to adult males, whereas the selective pressure is strongest in the subadult population (R. W. Newman 1975, 83).
Problems have also arisen from the misconceptions concerning the actual mecha-
nisms of the adaptational process. As stated by Schreider (1975, 530) and Rose
and Lauder (1996, 2–3), adaptation is more of a statistical than a purely biological
phenomenon, which means that even in the classical model of working natural
selection it will lead to maximization of mean fitness, not actually to maximal fit-
ness of the individual, and even less to optimally adapted traits. It has been ob-
served that climatic data were also often misinterpreted, as some of the papers
stressed that adaptation should be compared to extreme conditions and not to the
average estimates, which are usually presented (Hiernaux and Froment 1976,
766–767). Some authors have remarked that problems in recognizing traits of
probable adaptation to climatic variables begin with their description as evolu-
tionary adaptations, when it was not demonstrated how natural selection influ-
enced development of said traits (Franciscus and Long 1991, 424). This character-
istic of adaptation had started to be more widely recognized in the contemporary
research of biological adaptation since 1980s.
COMPARISON OF ADAPTATIONAL RESEARCH OF HUMANS AND ANIMALS
These problems are generally acknowledged and responsible for the dramatic changes in adaptational research over the last 30 years. Even without the modern changes in perception of adaptation and ways of studying it, the concept of human adaptation has been subjected to intense discussion between biologists. The
unique characteristics of the species Homo sapiens were and often still are a source of arguments about whether the adaptation of humans itself can be re- searched, and if it can and should be studied by similar methods as research done on animals.
One of the most frequently mentioned aspects, which can be considered an ad- vantage in climatic adaptation research, is the widespread range of the human species spanning the globe and nearly all of its climatic variations (Steegmann 1975, 132; Beall and Steegmann 2000, 176). Nonetheless, Steegmann regards it as a problem, because there is a limitation in possible adaptational response in hu- mans, due to the universal characteristics of the species (Steegmann 1975, 132).
Even in arctic conditions, the form and function of the body does not change dra- matically, which stands in contradiction to other animal groups. It is clear then that a majority of the response is of cultural origin (Steegmann 1975, 132). But as Beall and Steegmann (2000, 176) stated, the problem is not systematically stud- ied, as usually only the natives of the Arctic were tested for cold adaptation and acclimatization, only sporadically were the tests conducted on humans of Europe- an origin (often North Americans), who represent temperate climate populations.
Beall and Steegmann stressed the need for researching the adaptability to cold on the hot climate dwellers: South Asian, Australian and of course African peoples (Beall and Steegmann 2000, 177).
Human adaptation research has also to consider many other factors influencing results. Besides the cultural buffer, the other problematic issue related to
adaptational research is recognizing the change resulting from natural selection
preferring the advantageous trait. Even before the famous Gould and Lewontin
(1979), researchers expressed some well-grounded concerns about the complexity
of the interpretations of cold associated morphological traits. The general agree-
ment about ascribing the differences between populations from different climatic zones to the singular influence of environmental stressors, ignoring the possibility of the broader process of evolution (changes due to effects of genetic drift, genetic hitchhiking, dietary patterns or sexual selection) was no longer accepted
(Steegmann 1975, 131–132). For example, correspondence between body size and climate, which has been the base for acknowledging the occurrence of Allen- Bergmann’s rules in humans, is less evident in more recent populations than it has been suggested by previous analyses, signifying that at least some of the size differences were not as much a result of the climatic adaptations, they were rather more a result of undernutrition (Beall and Steegmann 2000, 179). The strong im- pression of adequate diet on the height and size of the body is a well acknowledged ontogenetic fact, but these secular trends can be mistaken for adaptational chang- es (Baker 1976, 231). Steegmann (1975, 131) also pointed out that the simple presentation of correlation between traits and climate does not imply direct cau- sality, arguing that the shortening of limbs in animals raised in cold conditions can be traced to slowing the growth of the extremities due to direct inhibition of circulation, and is not a result of adaptational changes for heat conservation, though in the end the result can be advantageous. It is then not only possible but rather probable to imply climatic adaptational changes where a causative factor is not climate itself, but another factor which follows clinal distribution of climatic conditions.
Another aspect is related to the high mobility of human population, which is not always taken into consideration and which can strongly influence the results of biological research. There are examples of strong interpopulational differences between neighboring peoples, which make sense only in the context of historical migration, like Y-chromosome diversity between both sides of the German-Polish border (Kayser et al. 2005). Such recognition of the historical facts that can influ- ence biological data is sometimes not taken into account or misinterpreted by re- searchers
*, though there are some works which present positive cooperation of his- torians and biologists in that area (Owens and King 1999). There is also the ques-
*See for example the discussion with Evteev et al. (2013) in Research of the cold adaptation in na- sal features of hominids p. 62
tion of the time needed for selection to work on the human population to develop adaptational trait, as some papers express uncertainty, about whether the time span of human occupancy in Scandinavia (8 to 10 kya) was long enough for natu- ral selection to change populational characteristics compared to Australia (35 to 10 kya, modern data suggest even 60 kya) (Guglielmino-Matessi, Gluckman, and Cavalli-Sforza 1979, 553).
CULTURAL ADAPTATION
One of the main problems considered during research on possible human adapta- tion is the unique buffering from environmental conditions due to cultural ad- justment, both as complex behavioral changes and as material innovations allow the human species to adapt to even more uninhabitable environments such as outer space. The importance of the cultural and behavioral changes in populations of different climatic zones is not a new idea in adaptational research, and has been widely acknowledged in biological science for a long time. Unfortunately the term
‘adaptation’ itself has a different meaning in biological sciences and in social sci- ences, where the main research on human culture differentiation and changes is conducted (Baker 1984, 1). The whole concept of evolutionary changes has only recently been embraced by the social sciences and the results, in the form of socio- biology, remain highly controversial (Fracchia and Lewontin 1999). I will not dis- cuss this problem further here, as it was and still is a very burning debate within the scientific community, but not one that is relevant to the problems discussed in the present dissertation. Here I will focus only on the aspects recognized and de- scribed in biological research, as detailed discussion describing cultural adapta- tions is beyond the scope of the present research.
The essential role of cultural adjustment in the successful inhabitation of new ter-
ritories and climatic zones is not a new idea in human biology. There exists a gen-
eral agreement that it must be considered when studying the problem of adapta-
tion in humans; the most comprehensive presentation of the problem can be found
in Baker (1984). The above-mentioned cultural adjustments are mainly adapta-
tions to a colder environment, as over the last 30 years the concept of the African
plains as the place of origin of the human genus, and then Homo sapiens itself,
has become the leading theory in human evolution. It can therefore be assumed
that the organism of the ‘original’ Homo was biologically adapted to such an envi- ronment, and indeed there is a number of analyses supporting this theory (see for example: Clark and Edholm 1985, 134–135; Baker 1984, 2–4). Most scientists agree that cultural acquisitions in the form of material inventions or behavioral changes were and are essential for conquering territories of different environmen- tal characteristics, and this feature is critical in the case of extremely cold condi- tions (Koertvelyessy 1972, 161; Beall and Steegmann 2000, 180). Some studies show that this cultural buffer can be considered quite effective not only in the case of developed modern industrial civilization, but was probably almost as good in the case of highly specialized indigenous cultures, like the Eskimo
*. Early explor- ers like Stefansson stressed the unique isolational properties of Eskimo houses and clothes, stating that the temperatures inside them were close to that of tropi- cal conditions, namely about 80-90°F (26-32°C) (Stefansson 1921, 76–77). Theoret- ical models confirm that the difference between the outside temperature and that inside of the snow igloo (which was not actually the predominant type of Eskimo housing, contrary to popular belief) with only one inhabitant should achieve 49°F (~9.5°C), allowing even with very cold conditions outside to achieve an indoor temperature of above freezing level (Jinks, Hopton, and Glossop 2011). Moran gives an estimate for the temperature inside the more common subterranean dwelling as ranging between 15 and 21°C (Moran 1981, 7). Many scientists have expressed opinions about the excellent insulating properties of traditional Eskimo clothing, stating that skin temperature in such attire remains optimal (Scholander 1955, 23; Moran 1981, 6; Clark and Edholm 1985, 134–135). Such observations have led to opinions of lesser then expected real exposure to cold of the indigenous people of the American Arctic. Shea (1977, 297) argued that Eskimos are largely not even exposed to the cold apart from the unprotected area of their faces. There-
*In this dissertation the previously more popular term ‘Eskimo’ will be used for describing the indigenous inhabitants of the Western Hemisphere Arctic, as the recently popularized term ‘Inuit’, although it does not carry any pejorative meaning, should be used only in the case of the people of the Canadian High North, sometimes including also the inhabitants of Greenland and northern parts of Alaska state, whereas western parts (the rest of Alaska state and the Chukotka Peninsula together with the Bering Strait isles) are home to the Yupik people. Eskimo is a name traditionally enveloping all of these mentioned peoples.
fore the Wolpoff opinion of the necessity for cultural buffering for living in such harsh conditions and the secondary role of any physiological or biological adapta- tions seems well founded (Wolpoff 1968, 406). Actual research shows that without this cultural buffer an individual could survive only for less than an hour in typi- cal conditions of the Bering Straits region in winter, whereas solely Eskimo cloth- ing without additional shelter can prolong that time to at least five hours (Mather 1993, 564).
This characteristic of cold climate cultures strongly contrasts with the inhabitants of hot environments, who prior to modern inventions allowing for cooling of indoor air had relied solely on the biological responses, and many of them still do, as they do not have access to modern technology facilitating living in such conditions (Crognier 1981, 105). This led some researchers to negate the occurrence of biolog- ical adaptation to cold (Clark and Edholm 1985, 136), though as Baker (1976, 233) has observed, with the exception of modern culture the material and nonmaterial cultural adaptations usually do not create a completely non-stressful environment, but rather reduce stress to biologically tolerable levels. Even today it is simply im- possible for a person living in extreme cold to completely avoid critical periods which can endanger one’s health and life, and in the situation of more primitive conditions, when survival hung in the balance, this occured more frequently (Beals 1972, 90). Therefore beside the material culture also behavioral changes that help with this threat had to be developed and propagated in societies living in cold con- ditions. Most of these are included in contemporary advice on cold climate survival (Beall and Steegmann 2000, 181; Foutch and Mills Jr 1988, 286–287).
RESEARCH STRATEGIES IN HUMAN ADAPTATION STUDIES
The adaptations of Homo sapiens are a rather unique research problem from the
point of view of evolutionary biology, because of the specific limitations of analyz-
ing humans. This was summarized by Baker, who stressed that no animal exper-
imentalist would allow for generalizing how cold influences mice, when the only
controlled variable would be the temperature, without unification of other factors
like genetics or remaining environmental conditions (Baker 1976, 244–245). Cul-
ture is also another uncontrollable variable in human societies, which can differ-
entiate people, even those closely related genetically and environmentally. As a
result most of the research of human adaptation to environment follows the re- search correlation: the null hypothesis states that unselected traits will vary inde- pendently of environmental variables, whereas geographically varying selection will result in correlation between traits and their selective factors. But as it has been stated in theoretical studies of adaptational research methodologies, this method has a main disadvantage: correlation between a morphological trait and a climatic variable may suggest a causal relationship, but is not sufficient to demon- strate it (Endler 1986, 58). Observation of a strong correlation, when it is uniform over a very large area can make evidence stronger, but there is always the ques- tion of whether the actual relationship is a result of the direct influence of one var- iable on the other (Endler 1986, 56–58) or just an effect of their correlation with an unknown (not studied) trait following distribution of climatic data. The prob- lem can be well illustrated by the changing relationship between climate and BMI, body mass, surface area/body mass ratio and sitting height (all those variables are consistent with the ecological Allen-Bergmann rules) in the last 30 years as pre- sented in the paper by Katzmarzyk and Leonard (1998). According to them the shift in trends previously recognized as a result of climatic influence happened because of change in nutrition and health care, which have influenced ontogenesis and adult body mass (Katzmarzyk and Leonard 1998, 494; Cowgill et al. 2012, 567).
The answer to the methodological challenge of researching human adaptational changes was presented by Baker, who suggested several models of analysis (Baker 1976). The proposed solutions are unfortunately hard to meet in present research (e.g. the postulate to restrict research to one stress factor in multiple genetically similar populations is not possible when studying archeologically derived human remains).
ADAPTATIONAL TERMINOLOGY
The problem of adaptational research is also visible through the different termi-
nology used to describe changes in organisms due to environmental stresses. Some
problems were mentioned in Chapter I. Cultural Adaptation p. 19, and here I will
solely focus on biological terminology. The term ‘adaptation’ is used not only for
describing any advantageous adjustment to the environment and the process of
developing it, but in a narrower sense it also is often used as a synonym for ‘genet- ic adaptation’ (resulting from genetic/inheritable response), which restricts the meaning of adaptation to a strictly Darwinian way of natural selection. In opposi- tion to this stands ‘acclimatization’ which describes adjustments to the environ- ment limited to the lifetime of the individuals (Steegmann 1975, 130–131). Alt- hough this solution seems attractive in its simplicity, there are additional prob- lems that should be addressed when choosing appropriate terminology. One of the main aspects in the present paper is its multidisciplinary character, which influ- ences used terminology, e.g. the problem of ‘cultural adaptation’ and its definition in the social sciences, which does not follow the biological sense of adaptation. The other is the much more complicated characteristics of advantageous adjustment to the environment than implied by Steegmann in the aforementioned paper. Even in the chapter “Human Biology” there is a note that mechanisms underlying
adaptational morphological changes may be caused by different immediate factors, not all of them of a genetic or hereditary nature (Beall and Steegmann 2000, 179).
Therefore the idea to understand and use the term ‘adaptation’ in its broadest, most generic sense (Mazess 1975, 9) is in the scope of this work the most appro- priate.
Mazess in his paper describing terminology of adaptation mentions a number of terms used in describing adaptational changes (Mazess 1975, 9). There is ‘acclima- tization’, ‘acclimation’, ‘adaptation’, ‘habituation’, ‘physiological adaptation’, ‘ge- netic adaptation’, ‘adaptedness’, ‘fitness’, ‘persistence’ and ‘aptitudes’. All those terms are used in describing changes in organism due to environmental stresses, though the definitions are usually not precise and are often interchangeable, or at least not mutually exclusive. The intensity of the terminological problem can for example be observed in the work of the Polish physiologist Stanisław Kozłowski who wrote that ‘adaptation’ when constricted to influence of one variable e.g. low atmospheric pressure, low or high temperature, usually can be replaced with ‘ac- climatization’ (Kozłowski 1986, 17–18)
*. Although there is a consensus allowing the division of responses to environmental stressors in the main categories, the
*More common practice would use the word ‘acclimation’ for such changes.
categorization often depends on the point of view specific to each scientific special- ization, and thus for example medical anthropologists tend to consider
adaptational traits in four classes (McElroy 1990, 249):
genetic change,
physiological and developmental adjustments,
cultural responses, and
individual coping.
This point of view seems to encompass most of the aspects of adaptation, but it is still far from the ideal, as for example physiological changes differ in their charac- ter from the developmental ones, as they are much more pliable and can change multiple times during the individual life, whereas developmental adjustments are practically stable after the development stage, and differ from genetic changes mainly in their restriction to life period, without the possibility of genetic inher- itance. Therefore the presentation of the main terminology used in adaptational research cannot be omitted from the present dissertation.
Adaptation
Adaptation is usually defined as the ability to survive, function, and reproduce
(see: Mazess 1975, 10) though adaptational change usually means a change which
is advantageous in one or all of these areas, not necessarily just allowing for these
functions. Even with the critique of the term presented by many papers following
Gould and Lewontin (1979), expressing lack of precision and predestination for
using teleological and functionalist terminology (Depew 2010), some researchers
point out that the adaptational paradigm is a heuristic and conceptual tool that
allows the organizing of different aspects of human response to environmental
stressors (McElroy 1990, 249). The term functions on different levels of biological
organization, beginning with the physicochemical and cellular, through organs
and individuals, up to populations and ecosystems (Mazess 1975, 10). Therefore in
the present work the broadest definition of ‘adaptation’ is the most advantageous,
namely any advantageous adjustment to the environment, which favors its
survival and/or functioning
*in a specific environment, which was in the past used by many recognized researchers (e.g. Baker 1984, 2; Cooper 1976, 37;
Steegmann 1975, 130–131). The precise terminology will be used according to the broad sense of that definition, as ‘genetic adaptation’ in the case of inherited advantageous traits or ‘developmental adaptation’ for changes occurring dur- ing the development, which are constricted to the life of the individual and then
‘physiological adaptation’ describing changes in physiology in response to changes in the environment. For the main hypotheses of the present dissertation the term ‘morphological adaptation’ is the most correct, and it will describe observed changes in the shape and size, thus morphology, of the skeleton, in par- ticular the nasal area. As the wording ‘cultural adaptation’ is widely recognized in both biological and social sciences, the changes of cultural character will be de- scribed as such, though the restrictions discussed previously will apply.
Acclimatization and acclimation
Both terms describe physiological changes induced by environmental factors, but
‘acclimatization’ is usually used for modifications due to complex factors, such as seasonal or climatic variations, whereas ‘acclimation’ is constricted to the influ- ence of singular factor change, commonly temperature, usually in a controlled, experimental environment (Hart 1961; Cooper 1976, 37). The problem commonly raised in terminological discussion, and strongly supported by experimental data, is that significant change in one of climatic conditions correlated will force other factors to change (e.g. humidity levels naturally drop in cold conditions), therefore the control of the conditions cannot be absolute even in an experimental setting (Cooper 1976, 38). As both types of adaptative reactions consider short-term re- versible changes and therefore have a limited input in the present research, both names will be used seldom and with the aforementioned meaning.
*Natural selection usually considers not only differential survival but also differential reproductiv- ity, but review of the literature on the adaptations in humans shows that papers on this subject do not present cases of presumed differential reproductivity, hence the present definition does not focus on this aspect.
Therefore for the purpose of this dissertation I will employ the most commonly
used terminology, namely adaptation as a general term; cultural, genetic, physio-
logical and morphological adaptation for describing adjustments in different sys-
tems, and then acclimatization to describe reversible physiological reaction.
CHAPTER II
MORPHOLOGY AND PHYSIOLOGY OF THE NOSE
MORPHOLOGY
The nose is a morphologically complex structure, whose morphology reflects its various physiological functions: the main airway, with apparatus for cleaning and conditioning inspired air, and the olfactory airway, which is the main olfactory organ in the body. The shape of the upper airways greatly influences the respira- tory airflows (Proctor 1982a, 23) and it can be further changed by unique physio- logical reactions (see next chapter). In normal conditions the main nasal airway passages are narrow, only about 1–3 mm wide, but the dimensions can be dramat- ically contracted by expansion of the nasal lining (see Fig. 1).
Fig. 1. CT scan of human nasal airways. Airways indicated by arrows. Right airway partially blocked due to nasal cycle (illustration source Wikipedia).
The skeletal structures of the nose visible in frontal projection are presented in
Fig. 2. The borders of the anterior nasal aperture, called the pyriform aperture,
is formed by two pairs of bones: the pair of nasal bones which form the upper edge
of the aperture, and the pair of maxillary bones forming the lateral and lower edg-
es of the aperture. The parts of the maxillae lying directly below the pyriform ap-
erture to the incisor root sockets are called the nasoalveolar clivus. The airways
are divided by internal structures, mainly the nasal septum, which separates left
and right airways, which consists of two structures: the perpendicular plate of
vomer and the perpendicular plate of ethmoid bone, fusing usually in early adult life (20-30 y.) (Scheuer and Black 2004, 116).
Fig. 2. Frontal view of the nasal skeleton: 1 – nasal bone; 2 – nasal process of the maxilla bone; 3 – nasal septum: perpendicular plate of ethmoid bone; 4 – pyriform aperture; 5 – nasal septum: per- pendicular plate of vomer; 6 – lower turbinate: inferior nasal concha; 7 – middle turbinate: middle
nasal concha; 8 – nasoalveolar clivus.
The rest of the bony structures visible through the pyriform aperture are the two
main pairs of conchae, which form the internal skeletal structures for pairs of
lower and middle turbinates: accordingly called the inferior and middle nasal con-
chae. The superior turbinates and accordingly the superior nasal conchae are not
visible outside of the nasal cavity and are small rudimentary structure. The infe-
rior conchae are the largest ones, medical sources inform that their size is 50-60
mm long, 7.5 mm in height, and 3.8 mm wide, and form the dominant structure
inside the nasal cavity (Anon). The middle conchae are a little smaller, their
length equals 40 mm and their mean height is 14.5 mm anteriorly and 7 mm pos-
teriorly, and they cover the important openings to the maxillary and sphenoidal
sinuses (Anon.). The smallest superior conchae provide drainage for the posterior
ethmoid air cells (Anon.). Fig. 3 shows the lateral wall of the nasal cavity. It de-
picts the frontal bone with an exposed frontal sinus, nasal bone, maxillary bone
with frontal, alveolar and palatine processes, palatine bone, sphenoid bone with
exposed sphenoid sinus, ethmoid bone and inferior nasal concha. The middle and
superior conchae are part of the ethmoid bone. The exit of the maxillary sinus, the
ostium of the maxillary sinus, is visible on the lateral wall of the nasal cavity,
between the inferior and middle nasal conchae.
Fig. 3. Lateral wall of the nasal cavity skeleton. 1– frontal bone; 2 – nasal bone; 3 – nasal process of maxillary bone; 4 – ostium of maxillary sinus; 5 – alveolar process of maxilla; 6 – palatine bone; 7 – inferior nasal concha; 8 – middle nasal concha; 9– sphenoid sinus; 10 – superior nasal concha; 11 –
frontal sinus (illustration source Gray (1918) with changes).
Fig. 4 presents the location of the internal, or posterior, nasal apertures – the choanae, where the nasal cavity connects to the nasopharynx. The choanae are separated by the posterior part of the nasal septum, consisting entirely of the vo- mer. The upper and lateral edges of the apertures consist of the sphenoid bone, and the lower edge is formed by the palatine bones.
Fig. 4. Skull base. 1 – choana; 2 – nasal septum: vomer; 3 – palatine bone; 4 – sphenoid bone (illus- tration source Gray (1918) with changes).
The rest of the nasal structures are formed from five larger cartilages: the carti-
lage of the septum, the two lateral and the two greater alar cartilages, and
several smaller pieces, the lesser alar cartilages presented in Fig. 5. In the case of archeologically derived human remains these structures of course are preserved only in mummified remains, so their morphology lies outside the scope of the pre- sent dissertation.
Fig. 5. Nasal cartilages. 1 – the cartilage of the septum; 2 – the lateral alar cartilage; 3 – greater alar cartilage; 4 – lesser alar cartilage (illustration source Gray (1918) with changes).
Beside the nasal cavity morphology important parts of nasal structures are formed by the paranasal sinuses. There are a total of 5 pairs of sinuses, with the most commonly known pairs of maxillary and frontal sinuses in the anterior part of the face, and two pairs of ethmoid sinuses (also called ethmoidal air cells) and a pair of sphenoidal sinuses located in the upper and posterior parts of nasal cavity (see Fig. 6)
Fig. 6. Localisation of paranasal sinuses: 1 – maxillary sinuses; 2 – frontal sinuses; 3 – sphenoidal sinuses; 4 – ethmoidal sinuses.
Of these, the maxillary sinuses are the largest, with a volume approximating 10- 15 ml (Proctor 1982a, 36). The frontal sinuses are the most variable in size, and sometimes one or even both of them fail to develop, whereas in other individuals they can achieve considerable size (Proctor 1982a, 36). The sphenoid sinuses, which achieve a size of about 5 ml each (Proctor 1982a, 36), are located between the sella turcica and the nasopharynx. The small ethmoidal sinuses are located along the superior medial walls of the orbits (Proctor 1982a, 36). All of the sinuses open into the nasal cavity by small openings called ostia.
The upper (nasal) airways form several distinct areas, the so-called nasal pas-
sages (Proctor 1982a, 28), which are presented in Fig. 7. The most anterior part
beginning with the nostrils and lined with skin, including a layer of crisscrossing
hairs, forms the nasal vestibule. After that area the nasal passages are lined
with a squamous epithelium. This part of the nasal passages is named the nasal
valve area (not to be mistaken with the nasal valve which is the narrowest por-
tion of the anterior nasal passage) and have special significance to nasal physiolo-
gy which will be discussed further in the next chapter (Physiology, p. 34). The
space between the end of the nasal valve area at the posterior margin of the upper
lateral cartilage and its fibro-adipose attachment to the pyriform aperture and the
internal nasal apertures or choanae is regarded as the main nasal passage,
though the complicated morphology of that area cause further divisions of the pas-
sages in this section. Fig. 8 presents their distribution. In the uppermost area
near the cribriform plate of ethmoid bone is the place where the density of the ol-
factory receptors is the greatest hence the name olfactory airway. The spaces
provided by the middle and inferior turbinate, located laterally are called accord-
ingly the middle and inferior meatuses. The rest of the airways are referred to
as the main nasal airway.
Fig. 7. Areas of the nasal passages. 1 – nasal vestibule; 2 – nasal valve area; 3 – main nasal pas- sage; 4 – nasopharynx (illustration source Gray (1918) with changes).
Fig. 8. Areas of the main nasal passage. 1 – olfactory airway (red area); 2 – main nasal airway (white area); 3 – middle meatus (orange area); 4 – inferior meatus (yellow area).
All of these bones form the skeleton of the nose, which of course in a living indi-
vidual is hidden within soft tissue structures. It is an interesting fact that from
the beginning of research, especially in the context of adaptational changes in the
nasal area, there were raised objections that the traits observed in the nasal skel-
eton were not directly influenced by natural selection and thus climatic stimulus,
and furthermore their relation to the nasal structures of a living person is not eas-
ily recognized (Schultz 1918, 329; Wolpoff 1968, 410). This reasoning is not easy to
understand when related to the external structures of the nose, which have been
the ones most intensely analyzed in the case of adaptational research. It is espe- cially true, considering the long history of facial reconstruction, which from the beginning concentrated heavily on the reconstruction of nasal structures, as the shape of the nose is one of the most important facial features when recognizing an individual (Wilkinson 2004). The intense research done for the purposes of foren- sic facial reconstruction purposes since early 20
thcentury (e.g. Birkner 1907;
Tandler 1909; Virchow 1912) showed that the correlation between the nasal skele- ton and the soft tissue nasal features is a fact, though Gerasimov, in his compre- hensive work on reconstructing faces, has pointed out the importance of examin- ing other parts of the facial skeleton, besides that of the direct nasal structures, in correct reconstruction of the visage (Gerasimov 1955). The scope of the research on the nasal area in facial reconstruction has been comprehensively presented by Wilkinson (2004, 103–110). The main conclusions derived from skeletal morpholo- gy are as follows (all literature after: Wilkinson 2004, 106):
the bony structure of the nose is half the complete nasal length (Broad- bent and Mathews 1957);
the form of the nasal bones must determine the nasal shape (Wilkinson 2004; Angel 1978);
the slope of the anterior nasal spine reflects the slope of the nasal base (Angel 1978)
the form of the anterior nasal spine determines the shape of the nasal tip (Angel 1978)
the lateral spread of the pyriform aperture sets the nostril width and the nostrils bulge 2-3 mm beyond the lateral pyriform edge (Angel 1978);
the nasal width is equal to the nasal aperture width plus 10 mm in Whites, and plus 16 mm in Blacks (Gatliff and Snow 1979);
the nasal projection is three times the length of the anterior nasal spine (Gatliff and Snow 1979);
the bony nasal aperture at its widest point is approximately three-fifths of the overall width of the soft nose (Gerasimov 1955)
This discrepancy between the results of research on the reconstruction of the nose
of a living individual on the basis of the morphology of the nasal skeleton, and the
dominating opinion of poor levels of reconstruction accuracy of that feature are therefore surprising. As Wilkinson (2010, 242) has pointed out, the high level of accuracy in predicting nasal shape on the basis of skull measurements was proven in the CT-scans of living people, which has been proven by further research
(Vermeulen 2012, 188–189).
PHYSIOLOGY
The previous section was dedicated to the presentation of nasal skeleton morphol- ogy, but it has to be stressed that the morphological features constitute only part of the living organism, and many, if not most, of the responses of the individual to environmental stress are purely of a physiological nature. They are often de- scribed in the acclimatization studies, and many responses are common for all representatives of a species or even higher taxa (Steegmann, Cerny, and Holliday 2002, 572), though the differences between the reactions of individuals from sepa- rate populations are the source of conclusions about physiological adaptations of said populations. However the problem of one-way analysis, focusing mainly on the differences between cold climate and temperate climate inhabitants has been raised by Beall and Steegmann (2000, 176). The imbalance of the research, dis- counting the population of warm and hot climates, is somewhat explained by the practical application of the results, as new inhabitants of the cold climates usually come from temperate zones, but as these authors point out, it severely diminishes the adequacy of the acquired knowledge to species-wide conclusions.
This dissertation will be restricted to physiological reactions to inspiring cold air, as these reactions are essential for the present analysis. The actual morphological studies often rely on additional physiological information which can strengthen the argument for the importance of the researched region in the functioning of the living organism and this practice is also employed here.
The physiological reactions of the upper airways, due to inspiring frigid air have
been a rather neglected research field. As Fontanari et al. (1996, 1739) suggest,
respiratory physiologists have often focused on pulmonary reflexes and have
mainly studied the results of the stimulation of the lower airways. Neglecting the
changes in the nose induced by exposure to harsh climatic conditions seems un-
warranted, considering the key role of the area in thorough conditioning of the inspired air. Most of the early studies concentrated on the fact that the principal functions of the nose are warming and humidifying the inspired air (Weiner 1954, 615–617; Shea 1977, 295) and regulating loss of heat during the respiration (Da- vies 1932, 349; Shea 1977, 297). In normal conditions nasal structures are ex- tremely efficient at achieving these goals: inspired cold air of -35°C gets heated to room temperature and is fully humidified by the time it reaches the laryngophar- ynx (Negus 1961, 725). The key role of the nose in the conditioning of the inspired air can be observed in the physiological changes of the breathing pattern
(bronchoconstrictor response) due to inhalation of cold air, which are triggered on- ly when air passes the nasal airways and is not present during mouth breathing.
This reflex is recognized as an attempt to reduce airflow rate in the upper airways and cervical trachea, which can be vital, if the frigid temperature of the environ- ment does not allow for full air conditioning in the nasal airways (Fontanari et al.
1996, 1743).
The physiological reactions of the nose are strongly related to a characteristic of
the nasal mucosa. As the cold air is inspired, the mucosa cools due to evaporation
and in result heats the air. If the respiratory rate increases or the air is colder and
drier the rate of the cooling also will increase, and in result the more distal muco-
sa is cooled to lower temperature. Cool air penetrates deeper into the nose, with
increased number of thermal receptors exposed to low temperature. As the cooling
of mucosa causes evaporation of water, the tissue can become desiccated in in-
creased cooling (Burgess and Whitelaw 1988, 373). The cooling can also cause na-
sal obstruction due to vascular engorgement of the nasal mucosa, which mainly
occurs during the nose inhaling – mouth exhaling process (Strohl et al. 1992,
1245–1246). Research shows that the nasal reaction is not limited to the stimulus
from inside the nasal cavity and therefore is not only the result of the reaction of
nasal thermal receptors, or even perinasal skin or neighboring nasopharynx cool-
ing, as the response of nasal lining can be provoked by cold water immersion of the
hand and forearm, and it exhibits laterality with congestion on the side of the
stimulus (Wilde 1999, 412–413). On the other hand, inhalation of the pre-warmed
air allows the experimental subject to maintain a significantly higher mean skin
and body temperature during prolonged cold exposure (Romet et al. 1986, 275).
Both reactions suggest complexity of neurological responses in connection to the nasal area.
The thermal receptors are thus mainly located in the nasal vestibule area (3.5 cold receptors/cm
2and 3.2 warm receptors/cm
2) and partially in malar skin (2.7 cold receptors/cm
2and 2.6 warm receptors/cm
2) with no thermal receptors in the nasal cavum (area lined by respiratory mucosa; consists of nasal valve area, main nasal passage to nasopharynx) (Jones, Wight, and Durham 1989, 237). Such localization is to be expected, as the nose plays a key role in conditioning the inspired air – the sampling of the inspired air should proceed as close to the entrance as possible.
What is interesting is the importance of the next area, the nasal valve area, in the heating of the air, which under room conditions is mainly warmed in the anterior segment of the nose (Keck et al. 2000, 653). The research shows that in this rela- tively open region, where the velocity of the inspired air is quite high, parts of the airstreams close to the mucosa lined walls have relatively low speed passing the area, for a sufficiently long time to heat inspired air (Keck et al. 2000, 653). What is more interesting, the analysis of the temperature distribution in anterior part of the upper airways clearly shows the importance of the nasal valve area, especially within the short distance between the nasal valve and head of the middle turbi- nate, where along an approximately 1 cm long section the temperature increase is greater than along the whole length of the middle turbinate (about 4 cm long) (Keck et al. 2000, 653).
The physiology and morphology of that area are therefore closely intertwined,
even the importance of the pure geometry is not clear as stated by Proctor (1982b,
460). It was suggested, however that not only the blood distribution along the air-
way wall, but also the cross-sectional area and the perimeter of the nasal cavity
are essential parameters of the physiological air conditioning response (Rouadi et
al. 1999, 404). The size of the upper airways constricts in two main areas; first is
the nasal valve area, where the cross section is at the narrowest point, forming the
smallest passage for total respiratory airflow (about 30–40 mm
2per side) (Proctor
1982a, 29). Then at the junction of the nasal valve area and the main nasal pas-
sage the airway expands to a cross section of about 130 mm
2per side, which is as-
sociated with an abrupt bending of nearly 90°(Proctor 1982a, 29). These dimen-
sions undergo another constriction at the boundary between the main nasal pas- sage and the nasopharynx (from 260 mm
2on both sides to 200 mm
2) (Proctor 1982a, 29). These two areas of narrowing correspond with both nasal skeletal ap- ertures: the pyriform aperture, which lies in the end of the nasal valve area, and the choanae, which form the borderline between the main nasal passage and nasopharynx (see Fig. 9).
Fig. 9. Correspondence between areas of upper airways and nasal skeletal apertures. 1 – nasal valve area; 2 – main nasal passage; 3 – nasopharynx; a – pyriform aperture; b – choanae (illustration
source Gray (1918) with changes).
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