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. 2021 Nov 18;240(5):959–971. doi: 10.1111/joa.13594

Sexual dimorphism in the first rib of Homo sapiens

Mikel Arlegi 1,2,✉, Andrea García‐Sagastibelza 3,4, Christine Veschambre‐Couture 4, Asier Gómez‐Olivencia 3,5,6,✉
PMCID: PMC9005670  PMID: 34796481

Abstract

This work aimed to study sexual dimorphism in the first rib of modern humans, with a special focus on whether differences in shape are due to divergent allometric growth in males and females. Also, we compare the accuracy of sex classification using different approaches based on two methodologies, traditional morphometry based on linear measurements and geometric morphometric analysis based on 2D landmark coordinates. The sample studied here comprised 121 right and left first ribs from 65 female and male adult recent Euro‐American Homo sapiens individuals. For traditional morphometrics, 12 metric variables were collected from each rib using a digital caliper, and for geometric morphometrics, six landmarks and 31 semilandmarks were captured from photographs using digital software. Both geometric morphometric and metric data were analyzed to calculate the index of sexual dimorphism, variation related to lateral asymmetry, variation in size and shape, and allometric trends between males and females. Finally, a linear discriminant analysis (LDA) was performed comparing both methodologies to test the best approach for sex classification. Results indicated that there are significant sex differences in the size and shape of the first ribs of recent Euro‐American Homo sapiens. Regression analysis revealed different allometric patterns for males and females, and this could partially explain shape differences between sexes. Additionally, traditional morphometrics showed that all characteristics analyzed are significantly dimorphic, with the midshaft minimum craniocaudal diameter, the sternal end minimum diameter, and the neck minimum craniocaudal diameter displaying the most dimorphic scores. Similarly, geometric morphometrics results indicated that males have more curved and interno‐exteriorly wider first ribs. Finally, analysis of sex classification using LDA yielded slightly better accuracy for traditional morphometry (83.8%) than the geometric morphometrics approach (81.3%) based on form Procrustes coordinates. This study demonstrates the usefulness of applying two different morphometric approaches to obtain more comprehensive results.

Keywords: allometry, discriminant analysis, double approach, geometric morphometrics, traditional morphometrics

Our study revealed different allometric patterns for males and females, and this could partially explain shape differences between sexes. Also, traditional morphometrics and geometric morphometrics analyses showed that the first rib of Homo sapiens is sexually significantly dimorphic. Finally, analysis of sex classification yielded slightly better accuracy for traditional morphometry than the geometric morphometrics approach based on form Procrustes coordinates.

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1. INTRODUCTION

The study of sexual dimorphism in the human skeleton is important in both human evolution and forensic sciences. In human evolution, the degree of sexual dimorphism of extinct hominin species has attracted considerable interest and debate (e.g., Arsuaga et al., 1997; Lockwood et al., 1996; Lorenzo et al., 1998; Reno & Lovejoy, 2015; Trinkaus, 1980) due to its relationship with sexual and/or ecological selection (Plavcan, 2012). On the other hand, the assessment of sexual dimorphism in various populations to refine sex determination using different procedures is commonly featured in the forensic literature. Most of these studies have focused on the characteristics of the cranium and pelvis, as they are the most dimorphic elements (e.g., Arsuaga & Carretero, 1994; Bruzek & Murail, 2006; Frayer & Wolpoff, 1985). However, other studies have found significant differences in the traits of many other anatomical elements. Among them, long bones from the limbs, especially the humerus (France, 1983; İşcan et al., 1998; İşcan & Miller‐Shaivitz, 1984; Robinson & Bidmos, 2009), femur (Curate et al., 2017; King et al., 1998), and tibia (Holland, 1991; Kranioti, 2015; Steyn & İşcan, 1997), have perhaps been the most studied; however, other anatomical parts have also been featured (Spradley & Jantz, 2011; Steele, 1976). In the postcranial axial skeleton, some researchers have focused on sex determination using the atlas and axis (e.g., Marino, 1995; Wescott, 2000), while others have studied the degree of lumbar lordosis (Bailey et al., 2016; Cheng et al., 1998). More recently, differences in the thorax shape have also been assessed.

Most works have studied different anatomical elements separately to assess sexual dimorphism in the thorax, focusing on the sternum (Singh et al., 2012; Bedalov, 2019; Peleg et al., 2020), the thoracic vertebrae (Bastir et al., 2014), and isolated ribs. Following the work of Isçan (1985), most studies focused on a single rib, using the fourth rib for sex determination (Chand et al., 2015; Macaluso et al., 2012; Ramadan et al., 2010) as it was proposed to be a reliable proxy for this purpose (but see Muñoz et al., 2018). However, several more recent works in the same vein have analyzed differences in the morphology of the first rib between males and females (Elrod, 2012; Kubicka & Piontek, 2016; Kurki, 2005; Lynch et al., 2017; Shathviha & Mohanraj, 2019). Broadly, these studies found that the modern human male first rib is dorsoventrally longer, with a smaller external curvature and more pronounced internal curvature compared to that of females. Additionally, they found significant differences in the overall size of the first rib between the sexes.

Compared to studies based on isolated ribs, fewer works have assessed sexual dimorphism by including the entire ribcage (Bellemare et al., 2001, 2003; García‐Martínez et al., 2016a, 2019; Shi et al., 2014; Tsubaki et al., 2017; Weaver et al., 2014). Broadly, they agree that modern human males and females differ in both thorax shape and size. More specifically, they found that males have about a 10% larger rib cage than females having the same stature, as well as a less craniocaudal orientation of the ribs. However, they also reported that females have longer ribs relative to body length than males, suggesting that the ribs grow longer relative to the axial skeleton in females than in males (Bellemare et al., 2006). Although this sexually dimorphic allometric growth in human ribs was also suggested by another study (García‐Martínez et al., 2016a), this trend has not been directly tested thus far.

Therefore, this work aims to analyze sexual dimorphism in the first rib of Homo sapiens and directly test for the first time, whether differences in shape are due to divergent allometric growth in males and females. We also intend to introduce geometric morphometrics in the context of forensic anthropology as a tool for sex classification. Bearing these purposes in mind, we state three hypotheses to be tested: (1) the first rib of Homo sapiens is sexually dimorphic, (2) males and females show different allometric patterns, and (3) sex classification using geometric morphometrics analysis results in higher accuracy of sex classification than the use of traditional morphometrics.

2. MATERIALS AND METHODS

2.1. Data

The sample studied here comprised 121 right and left first ribs from 33 female and 32 male adult Euro‐American individuals (n = 65) from the Hamann‐Todd osteological collection (Cleveland Museum of Natural History, USA; 33 females and 26 males) and the osteological collection of the Department of Anthropology (University of Iowa, USA; 6 males). For traditional morphometrics, the 121 ribs were measured using digital sliding calipers (Mitutoyo Inc.) to the nearest 0.1 mm. Twelve metric variables from each rib were taken following Gómez‐Olivencia et al. (2010, 2019; Table 1). For geometric morphometrics, ribs that presented slight damage along the shafts were not included to avoid disruptions in sliding the semilandmarks. Thus, the sample for geometric morphometric analyses comprised 112 right and left first ribs from 29 female and 27 male adult individuals (n = 56). The dataset was compiled from directly taken photographs of the original specimens. The camera was located perpendicular to the plane in which the first rib was laid. Ribs were centered, and we ensured that the photograph was larger than the rib to avoid parallax effects from the borders of the photograph. A total of six landmarks and 31 semilandmarks (Table 2, Figure 1) were positioned in the contour of the rib using the software tpsDig2 v. 2.31 (Rohlf, 2017) to capture representative bidimensional coordinates of the first rib shape. The morphological terms used in this work follow White and Folkens (2005). Additionally, we define the internal arc as the arc of the rib located closer to the mid‐sagittal plane (i.e., more medially) while the external arc is that located more laterally.

TABLE 1.

Linear measurement definitions

Variable Description
1a TVC Tubercle‐ventral chord a Straight line distance between the dorsal‐most margin of the articular tubercle to the ventral‐most point of the sternal end of the rib.
2a TVA Tubercle‐ventral arc a Arc length measured along the greater curvature of the rib from the lateral end of the articular surface of the tubercle to the sternal end of the rib.
2c IA Internal arc Arc length measured along the internal curvature of the rib.
4a HCCD Head cranio‐caudal diameter Maximum diameter in approximate craniocaudal direction of the articular surface of the head.
5a TNL Total neck length Straight line distance between the lateral (sternal)‐most margin of the articular tubercle to the medial (vertebral)‐most point of the head.
6 NMnCCD Neck minimum cranio‐caudal diameter Minimum reading of the craniocaudal dimension of the neck, measured perpendicular to the long axis of the neck.
7 NTh Neck thickness Measured at the mid part of the neck. Minimum diameter from internal to external surface of the rib.
14 THD Tubercle horizontal diameter Maximum diameter from the internal surface of the rib to the further extent of the articular tubercle.
19 MMxD Mid‐shaft maximum diameter b Measured at the mid‐shaft, maximum diameter, in this rib (from internal to external surface. In Rib 1, it is measured at the groove for the subclavian artery.
20 MMnD Mid‐shaft minimum diameter b Measured at the mid‐shaft, craniocaudal minimum diameter is measured at the groove for the subclavian artery.
23 SEMxD Sternal end maximum diameterc Measured at the sternal end. Maximum diameter. In this, rib is approximately horizontal.
24 SEMnD Sternal end minimum diameterc Measured at the sternal end. Minimum diameter. In this, rib is approximately vertical.
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Numbering of the variables follows Gómez‐Olivencia (2009).

TNL and NMnCCD variables are equivalent to HAFL and SCTCH from Owers and Pastor (2005).

a

McCown and Keith (1939).

b

Franciscus and Churchill (2002).

TABLE 2.

Landmark definitions

Landmark Anatomical region Number of landmarks Definition
1 Head 1 Ventral‐most point of the head
2 Head 1 Medial‐most point of the head
3 Head 1 Dorsal‐most point of the head
4 Non‐articular tubercle 1 Point of maximum curvature of the non‐articular tubercle
5 Sternal end 1 External end of the sternal end
6 Sternal end 1 Internal end of the sternal end
7–21 Shaft (internal) 15 Semilandmarks
22–41 Shaft (external) 20 Semilandmarks
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FIGURE 1.

FIGURE 1

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Morphological characters, orientation, linear variables, landmarks, and semilandmarks of the first rib of Homo sapiens used in this study. Note that not all the linear variables are represented in this figure (see Table 1 for all variables definition). The right‐most figure shows the two dimensional (2D) Landmarks in green (1–6) and semilandmarks in gray (7–37). Landmark definition in Table 2

2.2. Traditional morphometrics

2.2.1. Sexual dimorphism

To test for potential asymmetry, we first calculated the percentage asymmetry as the absolute difference between right and left sides divided by the smaller side and multiplied by 100 (Franciscus & Churchill, 2002; Trinkaus et al., 1994). Paired t‐tests were used to test for significant differences across all variables except neck thickness (NTh), for which a Wilcoxon test was used due to an absence of normality in this variable. Second, differences in size between males and females were assessed using the index of sexual dimorphism (ISD), i.e., the female mean divided by the male mean times 100 for each of the variables used (Arceredillo et al., 2011). Significance for each variable and to each side of the rib was tested using Student's t‐tests. These statistical analyses were performed using Past v. 4.05 (Hammer & Ryan, 2001).

Additionally, we performed two principal component analysis (PCA) to explore differences between sexes in a multivariate space both including the effect of size and after being removed. The first PCA (hereafter raw PCA) was performed using the 12 linear variables’ values, and the second PCA (hereafter size‐adjusted PCA) was computed by dividing these values by the geometric mean of each rib to remove the influence of size (Darroch & Mosimann, 1985; Jungers et al., 1995).

2.2.2. Sex classification

Finally, we performed a nonparametric flexible discriminant analysis (FDA) for sex classification testing two approaches, first including all the metric variables (n = 12) and then selecting the four variables that best discriminated males and females after the ISD results. Flexible discriminant analysis is an extension of linear discriminant analysis (LDA), which uses optimal scores from more flexible/smoothing nonparametric regression methods to transform the response variable so that the data are in a better form (Hastie et al., 1994). We selected the FDA over other discriminant analyses because it results in a higher percentage of correct classifications than other methods (Stull et al., 2017). In addition to FDA, we also analyzed the sex classification accuracy using a traditional LDA in order to parallel the method employed using geometric morphometric data (see below).

2.3. Geometric morphometrics

2.3.1. Sexual dimorphism

All information related to size, position, and orientation was removed using a generalized Procrustes superimposition (Rohlf & Slice, 1990). To assess and visualize shape and form (i.e., shape + size) differences between sexes, we first performed two PCA using the function “gm.prcomp” of geomorph package v. 3.3.2. (Adams et al., 2021). Statistical differences between males and females mean shape were conducted by Goodall's F statistic test (Goodall, 1991), using shapes package v. 1.2.6 (Dryden, 2021). This test compares the difference in mean shape between two samples relative to the shape variation found within the samples. We then analyzed the relative amount of shape variation in the first rib attributable to sex, size, and side factors (and their interactions) by performing a Procrustes analysis of variance (ANOVA) using the function “procD.lm” of geomorph. This function quantifies the amount of shape variation explained by one or multiple factors in a linear model and evaluates its significance using a residual randomization permutation within the package RRPP v. 0.6.2. (Collyer & Adams, 2018, 2021). As the interaction of size:sex produced a significant variation in shape, suggesting different allometric trends between males and females, from that linear model we next calculated the angle between the male and female samples and its significance from that linear model using the function “pairwise” of RRPP.

2.3.2. Sex classification

Finally, to test for the accuracy of sex classification using geometric morphometrics data, we performed a linear discriminant analysis (LDA) using the function “lda” from the MASS package v. 7.3–53 (Venables & Ripley, 2002). We chose LDA for this test because it has been reported to result in higher accuracy with geometric morphometric data than other discriminant analyses such as quadratic discriminant analysis (QDA), Kernel Fisher discriminant analysis (KLFDA), or mixture discriminant analysis (MDA; Sonnenschein et al., 2015). The data analyzed included the first 13 principal components (PCs) of shape generated from the landmark and semilandmark coordinates. These 13 PCs are those with eigenvalues ≥1 and account for more than 92% of the total variance. In addition, and because sexual dimorphism can be influenced by differences in size, we performed LDA using form (size‐and‐shape; Dryden & Mardia, 1998), i.e., adding centroid size to the Procrustes coordinates. Similarly, we used the PCs whose eigenvalues accounted for ≥1 (n = 13), which sum up to 92.7% of the total variance.

3. RESULTS

3.1. Traditional morphometrics

The results of the analyses of lateral asymmetry and sexual dimorphism in the first rib are presented in Table 3. These results indicate that lateral asymmetry is not present between left and right first ribs in either males or females. All the variables analyzed yielded non‐significant values in the percentage of asymmetry. In contrast, there were significant differences between sexes in both rib shape and size. The comparison between the male and female mean values showed significant differences for all variables except for the internal arc (IA) of the right ribs. ISD ranged between 78.8 (higher dimorphism) and 97.1 (lower dimorphism, this value corresponding to the IA of the right ribs). Broadly, the most dimorphic characters were craniocaudal diameters of the rib, comprising the minimum diameters of the mid‐shaft and sternal end, and the neck. On the other hand, the less dimorphic traits were the internal arch, the tubercle–ventral chord, the tubercle–ventral arc, and total neck length. The differences in the ISD values between variables suggest shape differences between sexes.

TABLE 3.

Raw dimensions (in mm) of the first ribs and results of within‐sex asymmetry (percentage asymmetry and paired t‐test) and sexual dimorphism (Student's t‐test and index of sexual dimorphism [ISD])

Variable a Side Females Males Student's t‐test ISD c
Mean SD Min Max n % asymmetry b (t‐test) Mean SD Min Max n % asymmetry b (t‐test)
1a Tubercle‐ventral chord (TVC) R 79.9 6.6 65.7 99.6 31 0.49 (NS) 84.7 5.4 74.8 94.5 30 0.97 (NS) ** 94.4
L 79.6 7.0 62.3 102.1 33 83.9 4.5 73.9 91.4 30 ** 94.9
2a Tubercle‐ventral arc (TVA) R 97.8 8.4 79.0 121.0 31 0.81 (NS) 104.2 9.4 85.0 126.0 30 0.13 (NS) ** 93.8
L 98.6 8.9 77.0 127.0 33 104.4 8.3 86.0 120.0 30 * 94.4
2c Internal arc (IA) R 86.5 7.0 70.0 105.0 30 1.15 (NS) 89.1 6.3 78.0 104.0 30 0.19 (NS) NS 97.1
L 85.5 7.5 68.0 105.0 33 88.9 5.0 78.0 100.0 29 * 96.2
4a Head cranio caudal diameter (HCCD) R 8.5 1.2 6.5 11.8 32 3.41 (NS) 9.4 1.1 7.3 12.1 32 1.96 (NS) ** 90.8
L 8.2 1.1 6.1 10.5 33 9.2 1.6 6.4 12.9 31 ** 89.5
5a Total neck length (TNL) R 31.1 3.3 25.0 37.8 32 1.45 (NS) 34.1 2.3 28.7 37.5 33 2.65 (NS) ** 91.1
L 31.6 3.0 24.7 38.2 33 33.3 2.4 25.7 36.4 31 * 94.9
6 Neck minimum cranio‐caudal diameter (NMnCCD) R 4.1 0.6 2.8 5.4 32 0.74 (NS) 5.0 0.6 3.9 6.1 33 2.05 (NS) ** 81.5
L 4.0 0.5 3.2 5.1 33 4.9 0.6 3.8 6.1 32 ** 82.6
7 Neck thickness (NTh) R 7.7 1.4 4.5 10.3 32 1.83 (NS) 9.0 1.4 7.0 12.7 32 2.11 (NS (M‐W)) ** 84.9
L 7.8 1.0 5.2 9.3 32 9.2 1.4 7.7 12.5 32 ** (M‐W) 84.7
14 Tubercle horizontal diameter (THD) R 15.4 1.8 11.8 18.7 32 1.56 (NS) 17.1 1.6 12.9 19.8 33 0.41 (NS) ** 89.9
L 15.6 1.9 11.7 19.3 33 17.0 1.6 13.9 19.6 32 ** 91.7
19 Mid‐shaft maximum diameter (MMxD) R 16.8 2.0 12.8 20.9 32 1.55 (NS) 19.6 2.7 14.4 23.9 32 1.66 (NS) ** 85.7
L 17.0 1.7 13.7 21.4 33 19.2 2.8 14.2 24.3 32 ** 88.5
20 Mid‐shaft minimum diameter (MMnD) R 3.3 0.5 2.2 4.8 32 2.47 (NS) 4.2 0.7 2.9 5.3 32 3.69 (NS) ** 78.9
L 3.2 0.5 2.1 4.5 33 4.1 0.6 2.9 5.4 32 ** 79.8
23 Sternal end maximum diameter (SEMxD) R 15.9 2.8 7.2 23.1 31 1.32 (NS) 18.3 2.6 14.0 24.1 30 1.16 (NS) ** 87.1
L 16.1 2.4 11.9 24.1 32 18.1 2.6 13.2 22.8 30 ** 89.3
24 Sternal end minimum diameter (SEMnD) R 7.6 1.1 5.5 9.6 30 0.66 (NS) 9.4 1.5 7.3 12.7 30 0.32 (NS) ** 80.8
L 7.7 1.0 5.6 10.0 33 9.5 0.9 7.9 10.9 30 ** 81.1
Geometric mean R 21.7 1.5 18.1 24.8 31 0 (NS) 24.4 1.5 21.2 27.5 29 1.20 (NS) ** 88.6
L 21.7 1.5 17.7 25.2 33 24.1 1.4 21.2 26.2 28 ** 89.7
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R, right; L, left.

a

Variable description can be found in Gómez‐Olivencia et al. (2010).

b

Percentage asymmetry was calculated as the absolute difference between right and left sides, divided by the smaller side, and multiplied by 100 (Trinkaus et al., 1994).

c

ISD, index of sexual dimorphism: female mean/male mean × 100.

*

p‐value < 0.05.

**

p‐value < 0.01.

The results from the raw PCA showed differences between males and females along with the first principal component (PC1), but with some overlap between groups (Figure 2). In general, males occupied the positive values of the morphospace, and females the negative ones. The loadings of all the variables went in the positive direction of the PC1, with some variables also pointing in the direction of the second principal component (PC2). The length of the vectors indicated that the internal arc and the tubercle‐ventral arc variables had the largest influence in the total shape variation, and the head cranio‐caudal diameter the lowest. The size‐adjusted PCA indicated that once the effect of size was removed, there were still differences between groups. The PC1 discriminated males and females with an overlap in the central part of the morphospace. In this case, the loadings were distributed in all directions of the morphospace, with those with larger influence in the total variation pointing in the direction of the negative values of the PC1 and PC2, and those showing a lower influence in the direction of the positive values of the PC1 and PC2. Finally, the eigenvectors indicated that the tubercle‐ventral chord, the tubercle‐ventral arc, and the internal arc variables had the largest influence in the morphospace occupied by females (negative values of the PC1), and the sternal end minimum diameter, the neck minimum cranio‐caudal diameter, and the mid‐shaft minimum diameter in the morphospace occupied by males (positive values of the PC1; Figure 2). Finally, the results from the FDA and LDA yielded a slightly better sex classification accuracy of pooled variables (FDA: 83.8%, LDA: 83.3%) than the selected four variables (FDA; 81.0%, LDA: 79.2%).

FIGURE 2.

FIGURE 2

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Scatterplots representing two PCA performed using linear variables, both from raw (left) and size‐corrected values (right). The grey arrows indicate the direction of the loadings for each variable. Confidence ellipses at the 95% of variation

3.2. Geometric morphometrics

The PCA results to examine sexual dimorphism in the shape of the first rib revealed that the second principal component (PC2), which accounted for more than 16% of the total variance, discriminated the best between sexes (Figure 3). Male individuals mainly occupied the positive values of PC2 in the morphospace, characterized by interno‐externally wider ventral halves of the rib shaft and by a more curved shape (closer angle) compared to those plotted in the negative values. Statistical comparison of males’ and females’ mean shapes (Figure 3) using Goodall's F statistic yielded significant differences between groups (F = 3.114; p‐value: 0.01). The male first rib was characterized by a wider shaft in relative terms (but also in absolute terms, Table 3), closer internal curvature, and slightly wider external curvature. On the other hand, females had less curved first ribs with narrower shafts. The PCA results to examine differences in the form space (Figure 4) also showed that the PC1, which accounted for more than 41% of the total variation, partially separated males and females. Also, it is worth noting that both sexes showed different trends in the direction of their variation ellipses within the form space,

FIGURE 3.

FIGURE 3

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Scatterplot representing the first two principal components (PCs) of shape variation from Procustes coordinates data. The grids show shape differences at the extremes of the morphospace. The first rib landmark representations at the right‐bottom reflect the mean shape of males (red) and females (black) in the shape space of the PCA. Confidence ellipses at the 95% of variation

FIGURE 4.

FIGURE 4

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Scatterplot representing the first two principal components (PCs) of form variation from Procustes coordinates data. Confidence ellipses at the 95% of variation

The ANOVA revealed that side and their interactions (side:sex and side:size) did not show any significant results, indicating the absence of lateral asymmetry. On the contrary, size and sex factors and their interaction (size:sex) had a significant influence on the relative amount of first rib shape variation (Table 4 and Figure 5), indicating potentially different allometric patterns between sexes. However, the effect sizes (Z scores) indicate that the effects of these factors on shape are relatively small. Thus, we tested for differences in the allometric trends between sexes, and the regression analysis revealed that males and females follow different allometric patterns (Table 4, Figure 6). Male and female regression vectors were significantly divergent, forming an angle of 82.8º. The female vector displayed a clear isomorphic trend, showing no shape variation irrespective of differences in size. Conversely, the male vector showed an allometric growth trend in which larger ribs were characterized by an increase in their curvature and a relatively higher interno‐external width of the rib shaft. Additionally, the pairwise analysis of shape vector (without the influence of size) yielded significant differences between males and females (Table 5), meaning that sex differences are not exclusively due to differences in the allometric pattern. Finally, sex classification using LDA for 2D geometric morphometrics data yielded an accuracy of 74.1% for shape and 81.3% for form (shape + size).

TABLE 4.

ANOVA of size, sex, side, and the combination of them in the first rib of Euro‐American Homo sapiens using Procrustes coordinates

Df MS Rsq F Z Pr (>F)
Size 1 0.01135 0.02466 2.9356 2.0643 0.023 *
Sex 1 0.0164111 0.03564 4.2434 2.5644 0.004 **
Side 1 0.0080317 0.01744 2.5644 1.5484 0.069
Size:Sex 1 0.0177716 0.03860 4.5952 2.8029 0.003 **
Size:Side 1 0.0013355 0.00290 0.3453 −1.7909 0.963
Size:Sex:Side 1 0.0017798 0.00387 0.4602 −1.1117 0.864
Residuals 114 0.0015160 0.00329 0.3920 −1.5695 0.946
Total 111 0.003874 0.87359
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Significant values in bold.

*

p‐value < 0.05

**

p‐value < 0.01.

FIGURE 5.

FIGURE 5

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Size variation in the left and right first rib of Euro‐American Homo sapiens using centroid size (CS) as a proxy. Male first ribs are larger than female ribs

FIGURE 6.

FIGURE 6

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Plots from the regression analysis of size on shape in males and females using Procrustes coordinates. The plots represent the fitted values of the linear model obtained from the regression analysis. The upper scatterplot shows the PC1 for those fitted values against centroid size. The vectors represent different allometric patterns (the angle between vectors is 82.8 at 95% confidence). Females show an isometric trend and males an allometric growth pattern. The grids represent how rib shape varies with increasing size in males (upper grids) and females (bottom grids). The bottom scatterplot represents the standardized shape scores from the regression versus size

TABLE 5.

Pairwise statistics of the fit linear models. First, the statistical analysis of the allometric model comparing males and females vectors, and second, the statistics of shape model (without the influence of size)

Allometric vectors d UCL (95%) Z Pr > d
Distance between vectors 0.00213 0.00150 2.86289 0.002 **
Difference in vector lengths 0.00128 0.00078 2.57215 0.003 **
Angle UCL (95%) Z Pr > d
Vector correlation −0.00846 82.80 1.96839 0.023 *
Shape vectors UCL (95%) Z Pr > d
Distance between vectors 0.02334 0.01805 2.51577 0.007 **
Difference in vector lengths 0.00001 0.00001 1.76641 0.038 *
Angle UCL (95%) Z Pr > d
Vector correlation 0.99973 1.34 2.51576 0.007 **
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Significant values in bold.

*

p‐value < 0.05

**

p‐value < 0.01.

4. DISCUSSION

For this study, we have included a single population, Euro‐Americans. Therefore, the results here obtained are limited to this group. Sex differences in size and shape were found in the first rib of adult recent Euro‐American Homo sapiens. Traditional morphometrics and geometric morphometrics produced complementary and consistent results. Nearly all the variables analyzed using traditional morphometrics were significantly dimorphic, displaying the highest ISD values in the midshaft minimum craniocaudal diameter, the sternal end minimum diameter, and the neck minimum craniocaudal diameter. These results are in concordance with those observed in the PCA based on linear measurements, where these variables had the largest influence in the PC1 variation, which discriminates the best males and females. Results from geometric morphometrics also revealed that broadly, males have more curved and interno‐exteriorly wider first ribs. These differences between sexes are due to, in part, different allometric patterns. Females displayed an isomorphic growth, whereas males yielded a different allometric trend in which an increase in size produced more curved and interno‐exteriorly wider ribs. These differences in the allometric trend are also observable in the Form space (Figure 4), where males and females describe divergent variation ellipses tendencies. Finally, sex classification revealed an accuracy of 83.8%–83.3% (pooled variables, FDA and LDA respectively) and 81.0%–79.2% (selected four variables, FDA and LDA) for traditional morphometrics, and 74.1% and 81.3% for the geometric morphometrics data‐based analysis using shape and form, respectively.

Our results are concordant with previous studies that found significant differences in the shape of the first rib between modern human males and females (Kubicka & Piontek, 2016; Lynch et al., 2017), but with subtle differences mainly due to the variables analyzed and the methods used. Broadly, we agree with previous research in that the midshaft diameter and sternal diameter together with the curvature of the arc are the most dimorphic characters. Other studies have also found sexually dimorphic differences in other ribs (Chand et al., 2015; Macaluso et al., 2012; Peleg et al., 2020; Tsubaki et al., 2017; Ramadan et al., 2010) that result in different thorax shapes as well as different degrees of invagination of the spine within the thorax that result in varying orientations of the transverse process of the thoracic vertebrae (Bastir et al., 2014). Females show a greater anterior–posterior inclination of the ribs (Bellemare et al., 2003), which also results in rib cages that are about 10% smaller than in males of the same height (Bellemare et al., 2006). Differences between males and females in the first (and other) ribs have been proposed to be mainly related to factors linked with respiration (Bellemare et al., 2006; Bellemare & Jeanneret, 2007; De Troyer et al., 2005). Following this, males would have wider mediolateral first ribs to serve the insertion of larger muscles that lift the rib and act as accessory muscles of respiration (i.e., scalenus anticus and medius, and serratus magnus), and of those that are directly implicated in respiration (i.e., intercostal muscles; Gandevia et al., 1996; Raper et al., 1966; De Troyer et al., 2005). These results parallel those found regarding the cranium, wherein males present a relatively larger size of the nasopharyngeal space than females when adjusted for centroid size (Rosas & Bastir, 2002), and are also consistent with generally heavier bodies relative to stature in males (Plavcan, 2001).

Apart from differences in the morphology of the first rib, we found significant differences in rib size. Males had larger ribs than females, which is consistent with general body size differences between the sexes (Ruff, 2017 and references therein). Previous studies also found significant differences in first rib size between the sexes (Kubicka & Piontek, 2016; Lynch et al., 2017), revealing larger ribs in males than in females. However, other studies analyzing the size of the ribs while accounting for body size concluded that female ribs are longer than those of males relative to the axial skeleton (Bellamare et al., 2006). This suggests differences in allometric growth of ribs between the sexes, resulting in a different rib cage shape (i.e., male rib cages are relatively wider, particularly caudally, and shorter; García‐Martínez et al., 2016a). Indeed, our results support this suggestion of different allometric patterns for males and females, revealing a nearly isomorphic growth of the first rib in females and an allometric trend for males. These trends represent an elongated and narrow first rib in females and more curved and mediolaterally wider ribs in males as size increases. This different allometric pattern in males and females could explain some of the morphological differences in the first rib, and by extension, in the entire rib cage, due to the tight link with the rest of the ribs (Bastir et al., 2015; García‐Martínez et al., 2016b). However, specific analyses testing the possible allometric patterns in the entire rib cage are necessary and could be very useful in shedding light on the morphological sexual dimorphism in this region.

Finally, the use of both geometric and traditional morphometric methodologies has resulted in a useful complementary picture of sexual dimorphism in this anatomical element. The combination of these methods has provided us with a better overview of metric and morphological variation. While linear measurements contributed to a better understanding of the sexual dimorphism in specific traits, geometric morphometrics allowed us to examine the morphological differences more holistically and visually. The sex classification analyses resulted in slightly higher accuracy for traditional (83.8%, FDA) than for geometric morphometrics (81.3%, LDA based on form). Additionally, we found differences between the two tests performed for each methodology. Traditional morphometrics yielded slightly higher accuracy (83.8 and 83.1%) for the analysis based on all the linear measurements (n = 12) than the one using only the four more discriminant variables (81 and 79.2%) using FDA and LDA, respectively. As expected, geometric morphometrics produced higher accuracy using form (81.3%) than shape exclusively (74.1%). Previous studies in this vein also reached similar conclusions, reporting that more variables result in higher accuracy than fewer variables (Bruzek & Murail, 2006; Kubicka & Piontek, 2016). The sex determination accuracy obtained here for the first rib lies among the averages obtained in previous studies, with percentages ranging between 60 and 70% (Elrod, 2012) and 91.5% (Kubicka & Piontek, 2016) using traditional morphometric variables, and 84.3–88.1% based on the combination of both traditional and geometric morphometrics (Lynch et al., 2017). Additionally, other studies analyzing sex discrimination in more caudal ribs (i.e., 5–9th) also obtained very high accuracies in the 6th, 8th, and 9th ribs (Peleg et al., 2020). However, sex assessment percentages in different ribs from various studies are not comparable, as each work used different samples, variables, and methods. Further studies including all the ribs and subjecting them to the same variables and methods are necessary to determine the reliability of each anatomical element as a proxy for sex assessment. Finally, and contrary to our expectations, the geometric morphometric analysis yielded slightly fewer correct classification results in the discriminant analysis. It should be noted that the geometric morphometric analysis was performed in 2D and thus did not capture the most dimorphic features in the traditional analysis, i.e., the craniocaudal dimensions. Thus, future analyses should evaluate sexual dimorphism using 3D landmarks to test whether better classification results are obtained.

5. CONCLUSIONS

We hereby highlight three main findings from this study that can contribute to a better comprehension of the sexual differences in the first rib, and by extension, in the entire rib cage to a lesser degree. First, that the first rib of recent Euro‐American Homo sapiens is sexually dimorphic, both in general size and specifically in the curvature of the arc (more curved in males), in the interno‐external width of the shaft (wider in males), and the craniocaudal height of the neck and shaft (thicker in males). Second, that this dimorphism is partially due to the different allometric patterns displayed by the sexes, showing an isomorphic growth in females and a trend in which ribs are more curved and dorsoventrally wider as size increases in males. Finally, that traditional morphometry based on linear measurements yielded slightly higher accuracy for sex discrimination (especially in the test including all variables) than 2D geometric morphometric analysis. These differences in accuracy are reduced when the 2D geometric morphometric analysis is based on form (instead of shape) data. In this regard, a combination of both size and shape assessment using either traditional or geometric morphometrics yields better results for the sex classification of the human first rib. Additionally, we demonstrate that the combination of different quantitative methods to study sex differences in the human skeleton provides complementary results and therefore a more comprehensive understanding of these differences.

AUTHORS CONTRIBUTIONS

M.A. and A.G.‐O. designed the study; A.G.‐O. acquired data; M.A. and A.G.‐S. analyzed data; M.A., A.G.‐S., C.V‐C., and A.G.‐O. drafted and critically revised the manuscript. All the authors approved the final version of the manuscript.

OPEN RESEARCH BADGES

This article has earned an Open Materials badge for making publicly available the components of the research methodology needed to reproduce the reported procedure and analysis. All materials are available at: 10.5281/zenodo.5644920.

ACKNOWLEDGMENTS

We would like to express our gratitude for access and technical help with the collections to Y. Haile‐Selassie and L. Jellema (Cleveland Museum of Natural History, Cleveland, USA) and R.G. Franciscus (University of Iowa, USA). Also we would like to thank L. Urtubia for his insights and inspiration. This research has also received support from the Spanish Ministry of Science and Innovation through the “María de Maeztu” excellence accreditation (CEX2019‐000945‐M), FEDER/Ministerio de Ciencia e Innovación‐Agencia Estatal de Investigación (project PGC2018‐093925‐B‐C33), Research Group IT1418‐19 from the Eusko Jaurlaritza‐Gobierno Vasco and AGAUR (Ref. 2017SGR1040), URV (Ref. 2019PFR‐URV‐91). AGO was supported by the Ramón y Cajal fellowship (RYC‐2017‐22558). The authors have no conflict of interest to declare regarding the material presented in this manuscript.

Arlegi, M. , García‐Sagastibelza, A. , Veschambre‐Couture, C. & Gómez‐Olivencia, A. (2022) Sexual dimorphism in the first rib of Homo sapiens . Journal of Anatomy, 240, 959–971. Available from: 10.1111/joa.13594

Contributor Information

Mikel Arlegi, Email: marlegui@iphes.cat, Email: asier.gomezo@ehu.eus.

Asier Gómez‐Olivencia, Email: asier.gomezo@ehu.eus.

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available in the zenodo open access repository, https://doi.org/10.5281/zenodo.5644920.

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Data Availability Statement

The data that support the findings of this study are available in the zenodo open access repository, https://doi.org/10.5281/zenodo.5644920.

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