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Human diversity, environmental adaptation and neural crest
Medical Hypotheses (1997) 48, 407-410 © Pearson ProfessionalLtd 1997
Human diversity, environmental adaptation and neural crest M. K. IRMAK, O. OZCAN Department of Histology and Embryology, School of Medicine, GOlhane Military Medical Academy, Etlik, Ankara, Turkey. Correspondence to: M. Kemal Irmak, GA TA Histoloji ABD, Etlik-Ankara, Turkey (Tel: 90 312 3251211/2396; Fax: 90 312 3234923)
A b s t r a c t - The relationship between anatomical/physiological traits, environmental adaptability and neural crest is described, and possible mechanisms leading to human diversity are suggested. It is concluded that environmental adaptation seems to be limited to those structures of neural crest origin.
Introduction Skin color, craniofacial morphology, hair distribution, stature and body proportions are variations in human morphology that have enabled humans to adapt to a broad spectrum of diverse environmental conditions (1). The neural crest is a population of migratory cells arising from the ectoderm, that migrates along defined pathways throughout the embryo and differentiates
Table
into a variety of diverse cell types (2). Pigment cells, most cells of the peripheral nervous system, facial mesenchyme, adrenal medullary cells, parafollicular cells, leptomeninges and aorticopulmonary septum are derived from neural crest (3). Neural crest might be the embryonic origin of human diversity. Possible interactions between environmental stressors and neural crest derivatives which result in human diversity are discussed below and summarized in the Table.
Possible mechanisms underlying human diversity
Anatomical/physiologicalvariable
Related neural crest derivatives
Environmental stressors
Pigmentation Craniofacial characteristics Body proportions Stature, hair distribution Cranial volume Autonomicand sensoryfunctions Blood pressure
Melanocytes Head mesenchyme Parafollicular cells (via thyroid hormones) Adrenal medulla (via cortical androgens) Leptomeninges Peripheral nervous system Aorticopulmonaryseptum
UV rays Climate, chewing Climate Climate Climate Climate, altitude, nutrition ?
Date received 6 May 1996 Date accepted 16 May 1996 407
408
MEDICAL HYPOTHESES
Anatomical/physiological traits and environmental adaptability
Pigmentation Melanin absorbs the harmful ultraviolet rays of the sun and protects the skin. There is a decline in the production and concentration of skin melanin from the southern African countries to the northern Scandinavian countries. The maximum amount of pigmentation (black skin) is found in hot, humid climates, and minimum (white skin) is observed in cooler climates. The low melanin concentration of fair skin promotes maximal cutaneous production of vitamin D. Melanin is produced by melanocytes which are derived from neural crest cells. The skin of all races contains the same spatial density of melanocytes, but the activity of melanocytes differs from one racial group to another (4).
Craniofacial characteristics
aperture is strongly affected by climate. In hot, moist climates, it is generally broad; in cold, dry climates it is narrow. In hot climates, a broad aperture permits maximum exhalation of heated air from the lungs, while a restricted air intake under cold conditions would seem to be essential to lessen the danger of freezing the lungs (6). Individuals from hot climates have thick, everted lips, and those from cooler climates, have thin inverted lips. Thick, everted lips tend to radiate more body heat and thus cool the body. Conversely, thin lips tend to conserve body heat and prevent their freezing in severely cold weather (4). Type of food is another environmental stressor leading to craniofacial diversity. For example, hard diet, which requires more chewing force and time, was observed to promote vertical growth of the mandibular ramus and anterior translocation of the maxilla (7,8).
Stature and body proportions
It seems that craniofacial diversity results from the tissues of neural crest origin. The skeletal and connective tissues of the face, anterior neck and much of the skull are derived from neural crest (5). One can easily notice the regional similarity between the facial mesenchyme of neural crest origin and craniofacial regions subjected to environmental adaptation (Figure). For example, differences in nasal aperture and lip size are anatomical variations that are related to environmental adaptation. The size of the nasal
j
Figure Contributions of neural crest cells to the craniofacial skeleton and connective tissues (dark area.) Modified from (5).
Environmental pressures have produced other noticeable differences among peoples, particularly in body shapes. Among the tallest and most longlimbed peoples in the world are the Nilotic peoples, such as the Dinkas, who live in the hot, dry areas of East Africa. At the opposite extreme in body shape are the Inuit, or Eskimo, who have compact bodies and relatively short arms and legs. The reasons have to do with heat loss. The greater the surface area of a warm body, the more body heat is lost, since heat loss is directly proportional to surface area. For people of a given weight, a long-limbed, tall shape maximizes surface area, while a compact, short-limbed shape minimizes it. Dinkas and Inuit have opposite problems of heat balance: the former usually need desperately to get rid of body heat, while the latter need desperately to conserve it. Thus adaptation molded their body shapes oppositely, based on their contrasting climates (1). Thyroid hormones and adrenal androgens seem to be involved in body proportion and stature differences between populations, respectively: In humans, there are two periods of rapid growth: the first in infancy and the second in late puberty just before growth stops. The first period of accelerated growth is partly a continuation of the fetal growth under the effect of thyroid hormones, and the second growth spurt occurs at the time of puberty under the anabolic effect of androgens (9). Growth velocities in these periods are different between populations (10,II), but the differences do not seem to correlate with either thyrotropin or corticotropin levels (12-15). Furthermore, the source of the ontogenetic control
HUMAN DIVERSITY, ENVIRONMENTAL ADAPTATION AND NEURAL CREST
of the hormone secretion is not yet clear. Here we suggest that control comes from parafollicular cells for the thyroid hormones, and from adrenal medullary cells for the androgens. Both cell types are of neural crest origin and they were reported to stimulate the follicular and adrenocortical cells, respectively, in a paracrine way (16-18). Therefore, it is reasonable to accept that these cells may be involved in stature and body proportion differences between populations. In addition, calcitonin of parafollicular cells may be responsible for the population differences in bone metabolism (19-22).
409
system, which is a part o f the peripheral nervous system (32).
Blood pressure Blacks in the U S A are almost twice as likely as whites to suffer from hypertension (33,34). The aorticopulmonary septum, another crest derivative, may be involved in the population differences in blood pressure.
Conclusion Hair form and distribution Humans who reside in cold climates tend to have straight hair; inhabitants of more moderate climates have wavy hair, and those from hot humid climates have tightly coiled, spiraled, wool-like hair. Tightly coiled, spiraled hair tends to facilitate the removal of body heat and cooling of the head and scalp while straight hair promotes conservation of heat and warming of the body (4). In general, individuals from cooler climates have more body hair than individuals from warmer environments. Lack of hair is obviously advantageous for effective heat loss during sweating in hot climates (6). The adrenal androgens, androstenedione and dehydroepiandrosterone, are known to determine the hair form and body hair distribution (9,23,24), and the secretion of these hormones may be controlled by adrenal medullary cells which are of neural crest origin as mentioned above.
Cranial volume Population differences are present in cranial volume (6). Leptomeninges known to be affected by temperature changes (25-27) may control the cranial size. Leptomeninges are also derived from neural crest cells.
Autonomic and sensory functions Sensory ganglia, sympathetic and parasympathetic ganglia and related supportive cells are components of the peripheral nervous system, and this system also forms from neural crest. The peripheral nervous system seems to be involved in adaptive changes and consequently in anatomical and physiological variations (28-31). For example, the high-altitude populations of the world appear well adapted to their environment (6). Population differences in lactose intolerance may also be attributable to the differences in the functions of the enteric nervous
The above-mentioned considerations make it appear likely that neural crest derivatives might be the structures upon which environment operates to produce permanent anatomical and physiological changes. In other words, environmental adaptation seems to be limited to those structures of neural crest origin.
References 1. Levontin R. Human Variety. New York, San Francisco: W H Freeman, 1982: 128-129. 2. Bronner F M. Neural crest cell formation and migration in the developing embryo. FASEB J 1994; 8: 699-706. 3. Morris K G, Ruberte E, Fukiishi Y. Mammalian neural crest and neural crest derivatives. Anat Anz 1993; 175: 501-507. 4. Johnson E F, McClure J, Herron P, Baskerville K A. Anatomical variation, human diversity, and environmental adaptation [editorial].J Natl Med Assoc 1993; 85: 337-338. 5. Johnston M C. Embryology of the Head and Neck. In: McCarthy J G, Bell L D, eds. Plastic Surgery. Philadelphia: W B Saunders, 1990: 2451-2495. 6. Harrison G A, Tanner J M, Pilbeam D R, Baker P T. Human Biology. Oxford: Oxford University Press, 1988: 305-507. 7. Hylander W L. The adaptive significance of Eskimo craniofacial morphology. In: Dahlberg A A, Graber T M, eds. World Anthropology, Orofacial Growth and Development. Paris: Mouton, 1974: 129-167. 8. Miller A J, Chierici G. Concepts related to adaptation of neuromuscular function and craniofacial morphology. Birth Defects 1982; 18: 21-43. 9. Ganong W F. Review of Medical Physiology. Lebanon: Typopress, 1989: 233-351. 10. Kumanyika S K, Huffman S L, Bradshaw ME et al. Stature and weight status of children in an urban kindergarten population. Pediatrics 1990; 85: 783-790. 11. Liang S F, Dai W Z. A growth velocity standard for Chinese children in Hong Kong. Chin Med J Engl 1989; 102: 233-235. 12. Same D H, Refetoff S, Murata Y, Dick M, Watson F. Variant thyroxine-binding globulin in serum of Australian aborigines: a comparison with familial TBG deficiency in Caucasians and American blacks. J Endocrinol Invest 1985; 8: 217-224. 13. Schectman J M, Kallenberg G A, Hirsch R P, Shumacher R J. Report of an association between race and thyroid stimulating hormone level. Am J Public Health 1991; 81: 505-506. 14. Hesslink R L, D'Alesandro M M, Armstrong D W, Reed H L.
410
15.
16.
17.
18.
19.
20.
21.
22.
MEDICAL HYPOTHESES
Human cold air habituation is independent of thyroxine and thyrotropin. J Appl Physiol 1992; 72: 2134-2139. Pasquali R, Baraldi G, Casimirri F et al. Seasonal variations of total and free thyroid hormones in healthy men: a chronobiological study. Acta Endocrinol Copenh 1984; 107: 42--48. Kalisnik M, Pajer Z, Trobina M. The interdependence of the follicular, parafollicular, and mast cells in the mammalian thyroid gland: A review and a synthesis. Am J Anat 1988; 183: 148-157. Nunez E A, Gershon M D. Parafollicular cell activation of endocytosis in follicular cells: Possible mediation by serotonin. Anat Rec i982; 202: 138A-139A. Bomstein S R, Bornstein M E, Scherbaum W A, Pfeiffer E F, Holst J J. Effects of splanchnic nerve stimulation on the adrenal cortex may be mediated by chromaffin cells in a paracrine manner. Endocrinology 1990; 127: 900-906. Reid I R, Cullen S, Schooler B A, Livingstone N E, Evans M C. Calcitropic hormone levels in polynesians: evidence against their role in interracial differences in bone mass. J Clin Endocrinol Metab 1990; 70: 1452-1456. Specker B L, Lichtenstein P, Mimouni F, Gormley C, Tsang R C. Calcium-regulating hormones and minerals from birth to 18 months of age: a cross-sectional study. II. Effects of sex, race, age, season, and diet on serum minerals, parathyroid hormone, and calcitonin. Pediatrics 1986; 77: 891-896. Stevenson J C, Myers C H, Ajdukiewicz A B. Racial differences in calcitonin and katacalcin. Calcif Tissue Int 1984; 36: 725-728. Dawson H B, H a m s S, Kramich C, Dallal G, Rasmussen H M. Calcium retention and hormone levels in black and white women on high and low calcium diets. J Bone Miner Res 1993; 8: 779-787.
23. Starka T. Epitestosterone, a hormone or not. Endocr Regul 1993; 27: 4 3 4 8 . 24. Winkler E M, Christiansen K. Sex hormone levels and body hair growth in Kung San and Kavango men from Namibia. Am J Phys Anthropol 1993; 92: 155-164. 25. E1-Sabban F, Fahim M A. Local cerebral hyperthermia induces spontaneous thrombosis and arteriolar constriction in the pia mater of the mouse. Int J Biometeorol 1995; 38: 92-97. 26. Eckhardt R R. Hominid brain evolution: two conceptions of science. Anthropol Anz 1991; 49: 289-302. 27. Shipman P. Hotheads. Discover 1991; 12: 18-19. 28. Cerny F J. Breathing pattern during exercise in young black and Caucasian subjects. J Appl Physiol 1987; 62: 2220--2223. 29. Stinson S. Nutritional adaptation. Annu Rev Anthropol 1992; 21 : 143-170. 30. Even P C, Nicolaidis S. Adaptive changes in energy expenditure during mild and severe feed restriction in the rat. Br J Nutr 1993; 70: 421-431. 31. Sand M F, Alger S A, Zurlo F, Young J B, Bogardus C, Ravussin E. Ethnic differences in sympathetic nervous systemmediated energy expenditure. Am J Physiol 1991; 261(6Ptl): E789-E794. 32. Gershon M D, Chalanozitis A, Rothman T P. From neural crest to bowel: development of the enteric nervous system. J Neurobiol 1993; 24: 199-214. 33. Anderson N B, Lane J D, Muranaka M Jr, Williams R B, Houseworth S J. Racial differences in blood pressure and forearm vascular responses to the cold face stimulus. Psychosom Med 1988; 50: 57--63. 34. Daniels D E, Rene A A, Daniels V R. Race: An explanation of patient compliance - Fact or fiction? J Natl Med Assoc 1994; 86: 20-25.
Human diversity, environmental adaptation and neural crest M. K. IRMAK, O. OZCAN Department of Histology and Embryology, School of Medicine, GOlhane Military Medical Academy, Etlik, Ankara, Turkey. Correspondence to: M. Kemal Irmak, GA TA Histoloji ABD, Etlik-Ankara, Turkey (Tel: 90 312 3251211/2396; Fax: 90 312 3234923)
A b s t r a c t - The relationship between anatomical/physiological traits, environmental adaptability and neural crest is described, and possible mechanisms leading to human diversity are suggested. It is concluded that environmental adaptation seems to be limited to those structures of neural crest origin.
Introduction Skin color, craniofacial morphology, hair distribution, stature and body proportions are variations in human morphology that have enabled humans to adapt to a broad spectrum of diverse environmental conditions (1). The neural crest is a population of migratory cells arising from the ectoderm, that migrates along defined pathways throughout the embryo and differentiates
Table
into a variety of diverse cell types (2). Pigment cells, most cells of the peripheral nervous system, facial mesenchyme, adrenal medullary cells, parafollicular cells, leptomeninges and aorticopulmonary septum are derived from neural crest (3). Neural crest might be the embryonic origin of human diversity. Possible interactions between environmental stressors and neural crest derivatives which result in human diversity are discussed below and summarized in the Table.
Possible mechanisms underlying human diversity
Anatomical/physiologicalvariable
Related neural crest derivatives
Environmental stressors
Pigmentation Craniofacial characteristics Body proportions Stature, hair distribution Cranial volume Autonomicand sensoryfunctions Blood pressure
Melanocytes Head mesenchyme Parafollicular cells (via thyroid hormones) Adrenal medulla (via cortical androgens) Leptomeninges Peripheral nervous system Aorticopulmonaryseptum
UV rays Climate, chewing Climate Climate Climate Climate, altitude, nutrition ?
Date received 6 May 1996 Date accepted 16 May 1996 407
408
MEDICAL HYPOTHESES
Anatomical/physiological traits and environmental adaptability
Pigmentation Melanin absorbs the harmful ultraviolet rays of the sun and protects the skin. There is a decline in the production and concentration of skin melanin from the southern African countries to the northern Scandinavian countries. The maximum amount of pigmentation (black skin) is found in hot, humid climates, and minimum (white skin) is observed in cooler climates. The low melanin concentration of fair skin promotes maximal cutaneous production of vitamin D. Melanin is produced by melanocytes which are derived from neural crest cells. The skin of all races contains the same spatial density of melanocytes, but the activity of melanocytes differs from one racial group to another (4).
Craniofacial characteristics
aperture is strongly affected by climate. In hot, moist climates, it is generally broad; in cold, dry climates it is narrow. In hot climates, a broad aperture permits maximum exhalation of heated air from the lungs, while a restricted air intake under cold conditions would seem to be essential to lessen the danger of freezing the lungs (6). Individuals from hot climates have thick, everted lips, and those from cooler climates, have thin inverted lips. Thick, everted lips tend to radiate more body heat and thus cool the body. Conversely, thin lips tend to conserve body heat and prevent their freezing in severely cold weather (4). Type of food is another environmental stressor leading to craniofacial diversity. For example, hard diet, which requires more chewing force and time, was observed to promote vertical growth of the mandibular ramus and anterior translocation of the maxilla (7,8).
Stature and body proportions
It seems that craniofacial diversity results from the tissues of neural crest origin. The skeletal and connective tissues of the face, anterior neck and much of the skull are derived from neural crest (5). One can easily notice the regional similarity between the facial mesenchyme of neural crest origin and craniofacial regions subjected to environmental adaptation (Figure). For example, differences in nasal aperture and lip size are anatomical variations that are related to environmental adaptation. The size of the nasal
j
Figure Contributions of neural crest cells to the craniofacial skeleton and connective tissues (dark area.) Modified from (5).
Environmental pressures have produced other noticeable differences among peoples, particularly in body shapes. Among the tallest and most longlimbed peoples in the world are the Nilotic peoples, such as the Dinkas, who live in the hot, dry areas of East Africa. At the opposite extreme in body shape are the Inuit, or Eskimo, who have compact bodies and relatively short arms and legs. The reasons have to do with heat loss. The greater the surface area of a warm body, the more body heat is lost, since heat loss is directly proportional to surface area. For people of a given weight, a long-limbed, tall shape maximizes surface area, while a compact, short-limbed shape minimizes it. Dinkas and Inuit have opposite problems of heat balance: the former usually need desperately to get rid of body heat, while the latter need desperately to conserve it. Thus adaptation molded their body shapes oppositely, based on their contrasting climates (1). Thyroid hormones and adrenal androgens seem to be involved in body proportion and stature differences between populations, respectively: In humans, there are two periods of rapid growth: the first in infancy and the second in late puberty just before growth stops. The first period of accelerated growth is partly a continuation of the fetal growth under the effect of thyroid hormones, and the second growth spurt occurs at the time of puberty under the anabolic effect of androgens (9). Growth velocities in these periods are different between populations (10,II), but the differences do not seem to correlate with either thyrotropin or corticotropin levels (12-15). Furthermore, the source of the ontogenetic control
HUMAN DIVERSITY, ENVIRONMENTAL ADAPTATION AND NEURAL CREST
of the hormone secretion is not yet clear. Here we suggest that control comes from parafollicular cells for the thyroid hormones, and from adrenal medullary cells for the androgens. Both cell types are of neural crest origin and they were reported to stimulate the follicular and adrenocortical cells, respectively, in a paracrine way (16-18). Therefore, it is reasonable to accept that these cells may be involved in stature and body proportion differences between populations. In addition, calcitonin of parafollicular cells may be responsible for the population differences in bone metabolism (19-22).
409
system, which is a part o f the peripheral nervous system (32).
Blood pressure Blacks in the U S A are almost twice as likely as whites to suffer from hypertension (33,34). The aorticopulmonary septum, another crest derivative, may be involved in the population differences in blood pressure.
Conclusion Hair form and distribution Humans who reside in cold climates tend to have straight hair; inhabitants of more moderate climates have wavy hair, and those from hot humid climates have tightly coiled, spiraled, wool-like hair. Tightly coiled, spiraled hair tends to facilitate the removal of body heat and cooling of the head and scalp while straight hair promotes conservation of heat and warming of the body (4). In general, individuals from cooler climates have more body hair than individuals from warmer environments. Lack of hair is obviously advantageous for effective heat loss during sweating in hot climates (6). The adrenal androgens, androstenedione and dehydroepiandrosterone, are known to determine the hair form and body hair distribution (9,23,24), and the secretion of these hormones may be controlled by adrenal medullary cells which are of neural crest origin as mentioned above.
Cranial volume Population differences are present in cranial volume (6). Leptomeninges known to be affected by temperature changes (25-27) may control the cranial size. Leptomeninges are also derived from neural crest cells.
Autonomic and sensory functions Sensory ganglia, sympathetic and parasympathetic ganglia and related supportive cells are components of the peripheral nervous system, and this system also forms from neural crest. The peripheral nervous system seems to be involved in adaptive changes and consequently in anatomical and physiological variations (28-31). For example, the high-altitude populations of the world appear well adapted to their environment (6). Population differences in lactose intolerance may also be attributable to the differences in the functions of the enteric nervous
The above-mentioned considerations make it appear likely that neural crest derivatives might be the structures upon which environment operates to produce permanent anatomical and physiological changes. In other words, environmental adaptation seems to be limited to those structures of neural crest origin.
References 1. Levontin R. Human Variety. New York, San Francisco: W H Freeman, 1982: 128-129. 2. Bronner F M. Neural crest cell formation and migration in the developing embryo. FASEB J 1994; 8: 699-706. 3. Morris K G, Ruberte E, Fukiishi Y. Mammalian neural crest and neural crest derivatives. Anat Anz 1993; 175: 501-507. 4. Johnson E F, McClure J, Herron P, Baskerville K A. Anatomical variation, human diversity, and environmental adaptation [editorial].J Natl Med Assoc 1993; 85: 337-338. 5. Johnston M C. Embryology of the Head and Neck. In: McCarthy J G, Bell L D, eds. Plastic Surgery. Philadelphia: W B Saunders, 1990: 2451-2495. 6. Harrison G A, Tanner J M, Pilbeam D R, Baker P T. Human Biology. Oxford: Oxford University Press, 1988: 305-507. 7. Hylander W L. The adaptive significance of Eskimo craniofacial morphology. In: Dahlberg A A, Graber T M, eds. World Anthropology, Orofacial Growth and Development. Paris: Mouton, 1974: 129-167. 8. Miller A J, Chierici G. Concepts related to adaptation of neuromuscular function and craniofacial morphology. Birth Defects 1982; 18: 21-43. 9. Ganong W F. Review of Medical Physiology. Lebanon: Typopress, 1989: 233-351. 10. Kumanyika S K, Huffman S L, Bradshaw ME et al. Stature and weight status of children in an urban kindergarten population. Pediatrics 1990; 85: 783-790. 11. Liang S F, Dai W Z. A growth velocity standard for Chinese children in Hong Kong. Chin Med J Engl 1989; 102: 233-235. 12. Same D H, Refetoff S, Murata Y, Dick M, Watson F. Variant thyroxine-binding globulin in serum of Australian aborigines: a comparison with familial TBG deficiency in Caucasians and American blacks. J Endocrinol Invest 1985; 8: 217-224. 13. Schectman J M, Kallenberg G A, Hirsch R P, Shumacher R J. Report of an association between race and thyroid stimulating hormone level. Am J Public Health 1991; 81: 505-506. 14. Hesslink R L, D'Alesandro M M, Armstrong D W, Reed H L.
410
15.
16.
17.
18.
19.
20.
21.
22.
MEDICAL HYPOTHESES
Human cold air habituation is independent of thyroxine and thyrotropin. J Appl Physiol 1992; 72: 2134-2139. Pasquali R, Baraldi G, Casimirri F et al. Seasonal variations of total and free thyroid hormones in healthy men: a chronobiological study. Acta Endocrinol Copenh 1984; 107: 42--48. Kalisnik M, Pajer Z, Trobina M. The interdependence of the follicular, parafollicular, and mast cells in the mammalian thyroid gland: A review and a synthesis. Am J Anat 1988; 183: 148-157. Nunez E A, Gershon M D. Parafollicular cell activation of endocytosis in follicular cells: Possible mediation by serotonin. Anat Rec i982; 202: 138A-139A. Bomstein S R, Bornstein M E, Scherbaum W A, Pfeiffer E F, Holst J J. Effects of splanchnic nerve stimulation on the adrenal cortex may be mediated by chromaffin cells in a paracrine manner. Endocrinology 1990; 127: 900-906. Reid I R, Cullen S, Schooler B A, Livingstone N E, Evans M C. Calcitropic hormone levels in polynesians: evidence against their role in interracial differences in bone mass. J Clin Endocrinol Metab 1990; 70: 1452-1456. Specker B L, Lichtenstein P, Mimouni F, Gormley C, Tsang R C. Calcium-regulating hormones and minerals from birth to 18 months of age: a cross-sectional study. II. Effects of sex, race, age, season, and diet on serum minerals, parathyroid hormone, and calcitonin. Pediatrics 1986; 77: 891-896. Stevenson J C, Myers C H, Ajdukiewicz A B. Racial differences in calcitonin and katacalcin. Calcif Tissue Int 1984; 36: 725-728. Dawson H B, H a m s S, Kramich C, Dallal G, Rasmussen H M. Calcium retention and hormone levels in black and white women on high and low calcium diets. J Bone Miner Res 1993; 8: 779-787.
23. Starka T. Epitestosterone, a hormone or not. Endocr Regul 1993; 27: 4 3 4 8 . 24. Winkler E M, Christiansen K. Sex hormone levels and body hair growth in Kung San and Kavango men from Namibia. Am J Phys Anthropol 1993; 92: 155-164. 25. E1-Sabban F, Fahim M A. Local cerebral hyperthermia induces spontaneous thrombosis and arteriolar constriction in the pia mater of the mouse. Int J Biometeorol 1995; 38: 92-97. 26. Eckhardt R R. Hominid brain evolution: two conceptions of science. Anthropol Anz 1991; 49: 289-302. 27. Shipman P. Hotheads. Discover 1991; 12: 18-19. 28. Cerny F J. Breathing pattern during exercise in young black and Caucasian subjects. J Appl Physiol 1987; 62: 2220--2223. 29. Stinson S. Nutritional adaptation. Annu Rev Anthropol 1992; 21 : 143-170. 30. Even P C, Nicolaidis S. Adaptive changes in energy expenditure during mild and severe feed restriction in the rat. Br J Nutr 1993; 70: 421-431. 31. Sand M F, Alger S A, Zurlo F, Young J B, Bogardus C, Ravussin E. Ethnic differences in sympathetic nervous systemmediated energy expenditure. Am J Physiol 1991; 261(6Ptl): E789-E794. 32. Gershon M D, Chalanozitis A, Rothman T P. From neural crest to bowel: development of the enteric nervous system. J Neurobiol 1993; 24: 199-214. 33. Anderson N B, Lane J D, Muranaka M Jr, Williams R B, Houseworth S J. Racial differences in blood pressure and forearm vascular responses to the cold face stimulus. Psychosom Med 1988; 50: 57--63. 34. Daniels D E, Rene A A, Daniels V R. Race: An explanation of patient compliance - Fact or fiction? J Natl Med Assoc 1994; 86: 20-25.