THE ANATOMICAL RECORD 298:1710–1721 (2015)
Differential Scaling Patterns in Maxillary Sinus Volume and Nasal Cavity Breadth Among Modern Humans LAUREN N. BUTARIC1,2,3* Department of Anthropology, Texas A&M University, College Station, Texas 2 Department of Pathology and Anatomical Sciences, University of Missouri, Columbia, Missouri 3 Department of Anatomy, Des Moines University, Des Moines, Iowa 1
ABSTRACT Among modern humans, nasal cavity size and shape reflect its vital role in air conditioning processes. The ability for the nasal cavity to augment its shape, particularly in inferior breadth, likely relates to the surrounding maxillary sinuses acting as zones of accommodation. However, much is still unknown regarding how nasal and sinus morphology relate to each other and to overall craniofacial form, particularly across diverse populations with varying respiratory demands. As such, this study uses computed tomographic (CT) scans of modern human crania (N 5 171) from nine different localities to investigate ecogeographic differences in (1) the interaction between maxillary sinus volume (MSV) and nasal cavity breadth (NCB) and (2) scaling patterns of MSV and NCB in relation to craniofacial size. Reduced major axis (RMA) regression reveals that all samples exhibit an inverse relationship between MSV and NCB, but statistical significance and the strength of that relationship is sample dependent. Individuals from cold–dry climates have larger MSVs with narrower NCBs, while smaller MSVs are associated with wider NCBs in hot–humid climates. MSV and NCB each scale with positive allometry relative to overall craniofacial size. However, sample differences are evident in the both the interaction between MSV and NCB, as well as their correlation with craniofacial size. While these results provide further support that the maxillary sinus and nasal cavity are integrated among populations from opposite ends of the climatic spectrum, additional epigenetic factors are needed to explain variation of these structures among populations from more intermediate climates. Anat Rec, 298:1710–1721, 2015. C 2015 Wiley Periodicals, Inc. V
Key words: human variation; climate; computed tomography; allometry; paranasal sinuses
Abbreviations used: AMNH 5 American Museum of Natural History; CT 5 computed tomography; MSV 5 maxillary sinus volume; NCB 5 nasal cavity breadth; NMNH 5 National Museum of Natural History; ORSA 5 Open Research Scan Archive; RMA 5 reduced major axis regression; UPMAA 5 University of Pennsylvania Museum of Archaeology and Anthropology Grant sponsor: Richard Gilder Graduate School, Texas Academy of Science, College of Liberal Arts, Texas A&M University. C 2015 WILEY PERIODICALS, INC. V
*Correspondence to: Lauren N. Butaric, Department of Anatomy, Des Moines University, 3200 Grand Avenue, Des Moines, IA 50312-4198. E-mail: [email protected] Received 16 September 2014; Revised 10 February 2015; Accepted 24 April 2015. DOI 10.1002/ar.23182 Published online 8 June 2015 in Wiley Online Library (wileyonlinelibrary.com).
MAXILLARY SINUS AND NASAL CAVITY SCALING
The nasal cavity has been described as the gateway to the respiratory system (Enlow, 1990) and maintains several important respiratory functions, including air conditioning processes in cold–dry environments. The effectiveness of the nose to warm and humidify cold inspired air, as well as to retain heat and moisture from expired air, relates to its overall gross morphology. Several studies indicate that ecogeographic variation in the nasal cavity of modern humans is such that taller, narrower, and longer nasal cavities are found in populations from cold–dry climates, with lower, wider, and shorter nasal cavities in those from hot–humid climates (Yokley, 2009; Maddux et al., 2011; Noback et al., 2011; Evteev et al., 2014). Tall and narrow nasal cavities increase the surface area of respiratory mucosa and enhance airflow turbulence, both of which play an important role in those air-conditioning processes needed in cold–dry climates (Walker et al., 1961; Morgan et al., 1995; Keck et al., 2000; Churchill et al., 2004; Doorly et al., 2008; Yokley, 2009). In equatorial areas where conditioning cold–dry air is not necessary, populations tend to exhibit lower and wider nasal cavities, which is less energetically demanding to maintain (Yokley, 2009; Holton et al., 2013). One way in which the nasal cavity is able to alter its overall shape, particularly in its inferior breadth, is thought to relate to its developmental integration with the maxillary sinuses. These air-filled chambers that surround and communicate with the nasal cavity could accommodate lateral expansion of the inferior nasal cavity where such expansion would not be feasible if the surrounding area were occupied with bone (see Keith, 1902; Enlow, 1968; Shea, 1977; Rae et al., 2003; Holton et al., 2013). If the maxillary sinus acts as a zone of accommodation for adaptive changes in nasal cavity size and shape, one might expect an inverse relationship between the size of these structures. According to this idea, within a given craniofacial size, wider internal nasal cavity breadths (NCBs) should be associated with smaller maxillary sinus volumes (MSVs), and vice versa. Studies on macaques (Rae et al., 1997, 2003; M arquez and Laitman, 2008; Ito et al., 2015) and rats (Rae et al., 2006) provide some evidence for this inverse relationship; however, the architectural relationships and patterns of morphological integration in the faces of macaques and rats may not be directly applicable to modern humans (see, Butaric et al., 2010; Holton et al., 2013). Studies on modern humans (e.g., Shea, 1977; Butaric et al., 2010; Holton et al., 2011, 2013) present conflicting results and raise additional questions. Recently, Holton et al. (2013) revealed a significant inverse relationship between MSV and NCB. Specifically, they found that a mixed sample of European-Americans exhibit narrow NCBs with large MSVs, while a mixed sample of African-Americans and native South Africans exhibit wide NCBs with small MSVs. This finding of larger sinuses among cold-adapted Europeans, compared to smaller sinuses of heat-adapted Africans, supports several previous studies (Wolfowitz, 1990; Fernandes, 2004a,b; Holton et al., 2011). The evidence that this pattern still exists among European- and African-American individuals, who may no longer be living in harsh climates, also indicates that there is a strong genetic component to this adaptive pattern. While Shea (1977) also found an inverse relationship between MSV and NCB in
1711
Arctic Inuits, among his samples, individuals from higher-latitudes actually had smaller, not larger, sinuses. The reason for this discrepancy between Shea’s (1977) and Holton et al.’s (2013) studies has yet to be fully investigated, but may relate to global- versus regional-level differences in the interaction of these structures among populations living in diverse environments. Along these lines, Butaric et al. (2010) failed to find a significant correlation between the volumes of the maxillary sinus and nasal cavity in a pooled global sample of modern humans. These authors suggested that an inverse relationship between these structures is likely only evident in populations residing in extreme environments, that is, at opposite ends of the climate spectrum (also see, Rae et al., 2011; Holton et al., 2013). Similar results have been obtained in other studies of craniofacial variation (Roseman, 2004; Harvati and Weaver, 2006; Hubbe et al., 2009), where the exclusion of samples from extreme climates leads to the loss of climatic signal. Further, explanations of the specific evolutionary and ontogenetic processes related to these adaptive nasal morphologies are still being developed. Several studies show that the components of the nasofacial skeleton related to respiration are relatively modular within the craniofacial skeleton (Enlow, 1990; Hall, 2005; Bastir et al., 2011; Bastir and Rosas, 2013; Holton et al., 2013, 2014). Much is still unknown, however, in how nasal and sinus morphology relate to the craniofacial skeleton, particularly across and within diverse populations. Since understanding how the nasal cavity and maxillary sinus not only relate to each other but also how they relate to overall craniofacial size is an important first step for understanding the mechanisms of their adaptive function (see Holton et al., 2013), the aims of the current study are twofold. First, this study analyzes the direct interaction between MSV and NCB to determine whetehr the inverse relationship is maintained across and within samples from more varied climatic zones. If the maxillary sinus acts as a zone of accommodation for the nasal cavity, then larger MSVs and narrower NCBs are expected in cold–dry climates, with smaller MSVs and wider NCBs in samples from hot–humid climates. However, this inverse relationship may not be found in samples from more intermediate climates, where nasal and sinus structures could be freer to vary with relaxed selection pressures. Second, this study investigates whether modern human samples from diverse climates exhibit differences in how MSV and NCB scale with overall craniofacial size. The importance of investigating scaling patterns of allometry versus isometry is well known in morphological studies as changes in overall size have concomitant changes in shape—often leading to functional implications (Gould, 1966; Emerson and Bramble, 1993). Thus, if the nasal cavity and maxillary sinus are influenced by climatic pressures, then differential scaling patterns among populations experiencing varying levels of respiratory demand should be expected (see, Holton et al., 2011, 2013). Further, if nasal cavity morphology is related to climatic conditions, then NCB should not strongly correlate with overall craniofacial size. This pattern should be particularly evident among samples
1712
BUTARIC
Fig. 1. Map illustrating relative geographic locations and climate zones of samples used in this study. Also see Table 1.
living at opposite ends of the climate spectrum (i.e., cold–dry and hot–humid) in comparison to samples from intermediate climate regions with relaxed respiratory pressures. In considering the two goals investigated here, the overall expectations of the current study are that individuals living in extreme climates will show (1) strong inverse correlations between MSV and NCB and (2) weak correlations of NCB, but not MSV, in relation to overall craniofacial size.
MATERIALS AND METHODS Sample The current study uses computed tomographic (CT) scans of nine modern human samples (total N 5 171). Each cranial sample belongs to one of the following ecogeographic zones (see Fig. 1): Rainforest (Malays), Equatorial (West Africans), Hot Steppe (South Africans), Hot Desert (Egyptian), Temperate (Croatians), Cold Steppe (Iranians; Mongolians), Snow (Buriats), and Arctic (Alaskan Inuits). These eight zones derive from an updated version of the K€oppen-Geiger climate classification system (Kottek et al., 2006) and were collapsed from the original 31 zones based on similarities of temperature and precipitation values. These eight zones represent, in varying degrees, the four major climatic conditions identified by Beals (1972) (also see, Gugleilmino-Matessi et al., 1979) thought to affect human biology: hot–dry, hot–humid, cold–dry, and cold–humid. [However, note that due to the correlation between temperature and absolute humidity (see, Walker et al., 1961), the notion
of a cold–humid or cold–wet environment may be a misnomer.] Table 1 provides a brief description of each sample including sample sizes, geographic provenience, and the specific museum collections and/or CT archives the samples originate.
Data Collection Scans of crania were obtained from several institutions and CT archives. The Alaskan Inuits (housed at the American Museum of Natural History, AMNH, New York, NY) and cranial samples housed at the Smithsonian National Museum of Natural History (NMNH, Washington DC) were scanned at the NMNH using a Siemens Somatom Emotion scanner, and obtained via B Frohlich. The remaining crania housed at the AMNH were scanned at Mt. Sinai Hospital Department of Radiology using a GE Discovery CT 750 HD system. Crania housed at the University of Pennsylvania’s Museum of Archaeology and Anthropology (UPMAA, Philadelphia, PA) were scanned at the Hospital of the University of Pennsylvania using a Siemens Somatom Sensation 64 CT scanner; these particular scans were obtained through the Open Research Scan Archive (ORSA). For all scans, slice thickness ranged from 0.50 to 1.0mm. Inquiries into the use of these scans can be directed to the author or to ORSA. The main variables used for the current study are MSV, internal NCB, and craniofacial size, which is based on several internal and external craniofacial measurements (see Table 2). All internal craniofacial variables were taken from the CT scans while the external
MAXILLARY SINUS AND NASAL CAVITY SCALING
TABLE 1. Samples Used in This Study With Housing Institutions and CT Archives Sample
N
Latitude
Description
South Africans
17
233.600
West Africans
20
20.720
Malays
19
3.620
Egyptians
19
30.057
Iranians
17
36.155
Croatians
20
42.640
Mongolians
19
47.921
Buriats
20
52.276
Inuits
20
68.348
19th century primarily of Khoi-San origin (AMNH; NMNH; ORSA) 19th century from Ghana, Gabon, Liberia, & Cameroon (NMNH; ORSA) Recent from Malaysian Islands (AMNH; ORSA)
Differential Scaling Patterns in Maxillary Sinus Volume and Nasal Cavity Breadth Among Modern Humans LAUREN N. BUTARIC1,2,3* Department of Anthropology, Texas A&M University, College Station, Texas 2 Department of Pathology and Anatomical Sciences, University of Missouri, Columbia, Missouri 3 Department of Anatomy, Des Moines University, Des Moines, Iowa 1
ABSTRACT Among modern humans, nasal cavity size and shape reflect its vital role in air conditioning processes. The ability for the nasal cavity to augment its shape, particularly in inferior breadth, likely relates to the surrounding maxillary sinuses acting as zones of accommodation. However, much is still unknown regarding how nasal and sinus morphology relate to each other and to overall craniofacial form, particularly across diverse populations with varying respiratory demands. As such, this study uses computed tomographic (CT) scans of modern human crania (N 5 171) from nine different localities to investigate ecogeographic differences in (1) the interaction between maxillary sinus volume (MSV) and nasal cavity breadth (NCB) and (2) scaling patterns of MSV and NCB in relation to craniofacial size. Reduced major axis (RMA) regression reveals that all samples exhibit an inverse relationship between MSV and NCB, but statistical significance and the strength of that relationship is sample dependent. Individuals from cold–dry climates have larger MSVs with narrower NCBs, while smaller MSVs are associated with wider NCBs in hot–humid climates. MSV and NCB each scale with positive allometry relative to overall craniofacial size. However, sample differences are evident in the both the interaction between MSV and NCB, as well as their correlation with craniofacial size. While these results provide further support that the maxillary sinus and nasal cavity are integrated among populations from opposite ends of the climatic spectrum, additional epigenetic factors are needed to explain variation of these structures among populations from more intermediate climates. Anat Rec, 298:1710–1721, 2015. C 2015 Wiley Periodicals, Inc. V
Key words: human variation; climate; computed tomography; allometry; paranasal sinuses
Abbreviations used: AMNH 5 American Museum of Natural History; CT 5 computed tomography; MSV 5 maxillary sinus volume; NCB 5 nasal cavity breadth; NMNH 5 National Museum of Natural History; ORSA 5 Open Research Scan Archive; RMA 5 reduced major axis regression; UPMAA 5 University of Pennsylvania Museum of Archaeology and Anthropology Grant sponsor: Richard Gilder Graduate School, Texas Academy of Science, College of Liberal Arts, Texas A&M University. C 2015 WILEY PERIODICALS, INC. V
*Correspondence to: Lauren N. Butaric, Department of Anatomy, Des Moines University, 3200 Grand Avenue, Des Moines, IA 50312-4198. E-mail: [email protected] Received 16 September 2014; Revised 10 February 2015; Accepted 24 April 2015. DOI 10.1002/ar.23182 Published online 8 June 2015 in Wiley Online Library (wileyonlinelibrary.com).
MAXILLARY SINUS AND NASAL CAVITY SCALING
The nasal cavity has been described as the gateway to the respiratory system (Enlow, 1990) and maintains several important respiratory functions, including air conditioning processes in cold–dry environments. The effectiveness of the nose to warm and humidify cold inspired air, as well as to retain heat and moisture from expired air, relates to its overall gross morphology. Several studies indicate that ecogeographic variation in the nasal cavity of modern humans is such that taller, narrower, and longer nasal cavities are found in populations from cold–dry climates, with lower, wider, and shorter nasal cavities in those from hot–humid climates (Yokley, 2009; Maddux et al., 2011; Noback et al., 2011; Evteev et al., 2014). Tall and narrow nasal cavities increase the surface area of respiratory mucosa and enhance airflow turbulence, both of which play an important role in those air-conditioning processes needed in cold–dry climates (Walker et al., 1961; Morgan et al., 1995; Keck et al., 2000; Churchill et al., 2004; Doorly et al., 2008; Yokley, 2009). In equatorial areas where conditioning cold–dry air is not necessary, populations tend to exhibit lower and wider nasal cavities, which is less energetically demanding to maintain (Yokley, 2009; Holton et al., 2013). One way in which the nasal cavity is able to alter its overall shape, particularly in its inferior breadth, is thought to relate to its developmental integration with the maxillary sinuses. These air-filled chambers that surround and communicate with the nasal cavity could accommodate lateral expansion of the inferior nasal cavity where such expansion would not be feasible if the surrounding area were occupied with bone (see Keith, 1902; Enlow, 1968; Shea, 1977; Rae et al., 2003; Holton et al., 2013). If the maxillary sinus acts as a zone of accommodation for adaptive changes in nasal cavity size and shape, one might expect an inverse relationship between the size of these structures. According to this idea, within a given craniofacial size, wider internal nasal cavity breadths (NCBs) should be associated with smaller maxillary sinus volumes (MSVs), and vice versa. Studies on macaques (Rae et al., 1997, 2003; M arquez and Laitman, 2008; Ito et al., 2015) and rats (Rae et al., 2006) provide some evidence for this inverse relationship; however, the architectural relationships and patterns of morphological integration in the faces of macaques and rats may not be directly applicable to modern humans (see, Butaric et al., 2010; Holton et al., 2013). Studies on modern humans (e.g., Shea, 1977; Butaric et al., 2010; Holton et al., 2011, 2013) present conflicting results and raise additional questions. Recently, Holton et al. (2013) revealed a significant inverse relationship between MSV and NCB. Specifically, they found that a mixed sample of European-Americans exhibit narrow NCBs with large MSVs, while a mixed sample of African-Americans and native South Africans exhibit wide NCBs with small MSVs. This finding of larger sinuses among cold-adapted Europeans, compared to smaller sinuses of heat-adapted Africans, supports several previous studies (Wolfowitz, 1990; Fernandes, 2004a,b; Holton et al., 2011). The evidence that this pattern still exists among European- and African-American individuals, who may no longer be living in harsh climates, also indicates that there is a strong genetic component to this adaptive pattern. While Shea (1977) also found an inverse relationship between MSV and NCB in
1711
Arctic Inuits, among his samples, individuals from higher-latitudes actually had smaller, not larger, sinuses. The reason for this discrepancy between Shea’s (1977) and Holton et al.’s (2013) studies has yet to be fully investigated, but may relate to global- versus regional-level differences in the interaction of these structures among populations living in diverse environments. Along these lines, Butaric et al. (2010) failed to find a significant correlation between the volumes of the maxillary sinus and nasal cavity in a pooled global sample of modern humans. These authors suggested that an inverse relationship between these structures is likely only evident in populations residing in extreme environments, that is, at opposite ends of the climate spectrum (also see, Rae et al., 2011; Holton et al., 2013). Similar results have been obtained in other studies of craniofacial variation (Roseman, 2004; Harvati and Weaver, 2006; Hubbe et al., 2009), where the exclusion of samples from extreme climates leads to the loss of climatic signal. Further, explanations of the specific evolutionary and ontogenetic processes related to these adaptive nasal morphologies are still being developed. Several studies show that the components of the nasofacial skeleton related to respiration are relatively modular within the craniofacial skeleton (Enlow, 1990; Hall, 2005; Bastir et al., 2011; Bastir and Rosas, 2013; Holton et al., 2013, 2014). Much is still unknown, however, in how nasal and sinus morphology relate to the craniofacial skeleton, particularly across and within diverse populations. Since understanding how the nasal cavity and maxillary sinus not only relate to each other but also how they relate to overall craniofacial size is an important first step for understanding the mechanisms of their adaptive function (see Holton et al., 2013), the aims of the current study are twofold. First, this study analyzes the direct interaction between MSV and NCB to determine whetehr the inverse relationship is maintained across and within samples from more varied climatic zones. If the maxillary sinus acts as a zone of accommodation for the nasal cavity, then larger MSVs and narrower NCBs are expected in cold–dry climates, with smaller MSVs and wider NCBs in samples from hot–humid climates. However, this inverse relationship may not be found in samples from more intermediate climates, where nasal and sinus structures could be freer to vary with relaxed selection pressures. Second, this study investigates whether modern human samples from diverse climates exhibit differences in how MSV and NCB scale with overall craniofacial size. The importance of investigating scaling patterns of allometry versus isometry is well known in morphological studies as changes in overall size have concomitant changes in shape—often leading to functional implications (Gould, 1966; Emerson and Bramble, 1993). Thus, if the nasal cavity and maxillary sinus are influenced by climatic pressures, then differential scaling patterns among populations experiencing varying levels of respiratory demand should be expected (see, Holton et al., 2011, 2013). Further, if nasal cavity morphology is related to climatic conditions, then NCB should not strongly correlate with overall craniofacial size. This pattern should be particularly evident among samples
1712
BUTARIC
Fig. 1. Map illustrating relative geographic locations and climate zones of samples used in this study. Also see Table 1.
living at opposite ends of the climate spectrum (i.e., cold–dry and hot–humid) in comparison to samples from intermediate climate regions with relaxed respiratory pressures. In considering the two goals investigated here, the overall expectations of the current study are that individuals living in extreme climates will show (1) strong inverse correlations between MSV and NCB and (2) weak correlations of NCB, but not MSV, in relation to overall craniofacial size.
MATERIALS AND METHODS Sample The current study uses computed tomographic (CT) scans of nine modern human samples (total N 5 171). Each cranial sample belongs to one of the following ecogeographic zones (see Fig. 1): Rainforest (Malays), Equatorial (West Africans), Hot Steppe (South Africans), Hot Desert (Egyptian), Temperate (Croatians), Cold Steppe (Iranians; Mongolians), Snow (Buriats), and Arctic (Alaskan Inuits). These eight zones derive from an updated version of the K€oppen-Geiger climate classification system (Kottek et al., 2006) and were collapsed from the original 31 zones based on similarities of temperature and precipitation values. These eight zones represent, in varying degrees, the four major climatic conditions identified by Beals (1972) (also see, Gugleilmino-Matessi et al., 1979) thought to affect human biology: hot–dry, hot–humid, cold–dry, and cold–humid. [However, note that due to the correlation between temperature and absolute humidity (see, Walker et al., 1961), the notion
of a cold–humid or cold–wet environment may be a misnomer.] Table 1 provides a brief description of each sample including sample sizes, geographic provenience, and the specific museum collections and/or CT archives the samples originate.
Data Collection Scans of crania were obtained from several institutions and CT archives. The Alaskan Inuits (housed at the American Museum of Natural History, AMNH, New York, NY) and cranial samples housed at the Smithsonian National Museum of Natural History (NMNH, Washington DC) were scanned at the NMNH using a Siemens Somatom Emotion scanner, and obtained via B Frohlich. The remaining crania housed at the AMNH were scanned at Mt. Sinai Hospital Department of Radiology using a GE Discovery CT 750 HD system. Crania housed at the University of Pennsylvania’s Museum of Archaeology and Anthropology (UPMAA, Philadelphia, PA) were scanned at the Hospital of the University of Pennsylvania using a Siemens Somatom Sensation 64 CT scanner; these particular scans were obtained through the Open Research Scan Archive (ORSA). For all scans, slice thickness ranged from 0.50 to 1.0mm. Inquiries into the use of these scans can be directed to the author or to ORSA. The main variables used for the current study are MSV, internal NCB, and craniofacial size, which is based on several internal and external craniofacial measurements (see Table 2). All internal craniofacial variables were taken from the CT scans while the external
MAXILLARY SINUS AND NASAL CAVITY SCALING
TABLE 1. Samples Used in This Study With Housing Institutions and CT Archives Sample
N
Latitude
Description
South Africans
17
233.600
West Africans
20
20.720
Malays
19
3.620
Egyptians
19
30.057
Iranians
17
36.155
Croatians
20
42.640
Mongolians
19
47.921
Buriats
20
52.276
Inuits
20
68.348
19th century primarily of Khoi-San origin (AMNH; NMNH; ORSA) 19th century from Ghana, Gabon, Liberia, & Cameroon (NMNH; ORSA) Recent from Malaysian Islands (AMNH; ORSA)
