Evolution and Human Behavior 24 (2003) 199 – 207
Facial attractiveness in men provides clues to semen quality C. Soler a,*, M. Nu´n˜ez a, R. Gutie´rrez a,b, J. Nu´n˜ez a, P. Medina a, ´ lvarez c,d, A. Nu´n˜ez a,1 M. Sancho a, J. A a
Department of Functional Biology and Physical Anthropology, Universitat de Vale`ncia, 46100 Burjassot, Spain b Department of Chemistry and Biology, Universidad del Norte, Km. 5 Vı´a Puerto Colombia, Barranquilla, Colombia c Unidad de la Mujer, La Corun˜a, Spain d Harvard Medical School, Boston, MA, USA Received 18 November 2002; received in revised form 7 March 2003
Abstract Facial attractiveness has been related to health in both men and women. Certain psychological, physiological, and secondary sex characteristics have been used as accurate markers of hormonal and developmental health. The main objective of this study was to investigate the capacity of women to select males of high reproductive quality based on their facial attractiveness. A total of 66 males were included in the study. Each of them provides a semen sample, and frontal and lateral photographs were taken. Semen analysis was made according to standard WHO (1999) guidelines for morphology, motility, and concentration. Moreover, a Sperm Index (SI) was calculated as the principal component of these parameters. In Study 1, 66 women rated the attractiveness, as a possible permanent couple, of pictures of all 66 men. In Study 2, the pictures of a subset of 12 males were randomly selected from three semen quality subgroups (terciles named good, normal, and bad, according to the value of the SI). These 12 pictures were rated on attractiveness by two independent sets of women (N = 88 and N = 76). Facial attractiveness ratings were significantly (P < .05) and positively correlated with sperm morphology, motility, and SI, but not with concentration, for all the women sets. D 2003 Elsevier Science Inc. All rights reserved. Keywords: Semen quality; Attractiveness; Human evolution; Mate choice
* Corresponding author. Tel.: +34-9635-44387; fax: +34-9635-44387. E-mail address:
[email protected] (C. Soler). 1 In memoriam. 1090-5138/03/$ – see front matter D 2003 Elsevier Science Inc. All rights reserved. doi:10.1016/S1090-5138(03)00013-8
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1. Introduction Judgments of facial attractiveness appear to be reliably associated with mate choice (Chen, German, & Zaidel, 1997; Rhodes, Proffitt, Grady, & Sumich, 1998; Thornhill & Gangestad, 1996, 1999a), but what such judgments reveal about the phenotypic quality of the person is not fully elucidated. Certain aspects of facial attractiveness, such as symmetry and proportions (Magro, 1999; Perrett et al., 1998; Perret, May, & Yoshikawa, 1994), may be reliably correlated with health (Cunningham, 1986; Kalick, Zebrowitz, Langlois, & Johnson, 1998; Shackelford & Larsen, 1997, 1999). If what is deemed attractive about a male’s face is an honest signal of phenotypic quality, one might anticipate that facial attractiveness judgments would be correlated with semen quality (Barber, 1995; Gangestad, 1993; Grammer & Thornhill, 1994; Pawlowski, Dunbar, & Lipowicz, 2000). The aim of the present study was to investigate whether women’s judgements of the attractiveness of men, based on photographs of faces, would be correlated with the quality of the men’s semen, according to standard quality indices of morphology, motility, and concentration.
2. Methods 2.1. Male participants A total of 102 male students from the Universitat de Vale`ncia, Spain, were recruited for this study. The data for 36 men were excluded due to the use of medication, infantile or recent diseases, facial surgery or ornaments (beard, moustache, piercing, etc.), or technical problems during the sampling procedure. The final sample of 66 men ranged in age from 19 to 36 years (mean = 23.4, S.D. = 2.7), with a period of reported sexual abstinence ranging from 1 to 10 days (mean = 4.1, S.D. = 1.5) prior to semen collection. 2.2. Female participants In order to evaluate the attractiveness of men’s images, 75 female students of the Universitat de Vale`ncia were recruited for Study 1. The data from nine women were excluded because they recognized some of the men or because they were using oral contraception. The women ranged in age from 20 to 27 years (mean = 21.8, S.D. = 1.5). For Study 2, another 88 women were recruited (age range = 18–28; mean = 18.6, S.D. = 1.3) without any information about their menstrual cycle, and still another 76 women were recruited (age range = 18–27; mean = 18.8, S.D. = 1.4) with regular cycles, all of them from the Universidad de Zaragoza (320 km from Vale`ncia). The 75 women in Study 1 and the 76 women from Zaragoza were asked about the first day of their last menstrual period and the length in days of the menstrual cycle. The fertility risk in these women (probability of conception following sex) was estimated on the basis of the values reported by Jo¨chle (1973) (Table 1).
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Table 1 Fertility risk index of female raters of men’s attractiveness according to the classification of Jo¨chle (1973) Whole population High-fertlity-risk group Low-fertility-risk group
Study 1 (Vale`ncia)
Study 2 (Zaragoza)
0.09 (52; 0.02 – 0.40) 0.29 (8; 0.18 – 0.40) 0.04 (44; 0.02 – 0.11)
0.17 (76; 0.02 – 0.41) 0.27 (30; 0.18 – 0.41) 0.04 (46; 0.02 – 0.11)
Data are expressed as mean (number; range).
2.3. Semen analysis Following the WHO guidelines on semen analysis (World Health Organization, 1999), three main semen parameters (motility, morphology, and concentration) were assayed. Percent motility was obtained by placing a 5-Al aliquot of semen on a Makler chamber and by counting a minimum of 200 cells under a 400 magnification. To evaluate the percentage of normal forms, a smear of each sample was prepared from a drop of 5 Al, air-dried, fixed, stained according to the protocol of the Hemacolor kit (Merck, Darmstadt, Germany, Catalog no. 1161), and sealed with a mounting medium (Eukitt, O. Kindler, Freiburg, Germany). A minimum of 200 cells were evaluated per sample under a 1000 magnification (using a 100 immersion oil objective). Finally, sperm concentration was obtained following fixation of a semen aliquot with formalin. After 10 min, the diluted sperm suspension was transferred to both chambers of a Neubauer haemocytometer, and the spermatozoa present in an area of 1 mm2 were counted and used for the final calculation of concentration.
Fig. 1. Photographs (frontal and lateral views) were scanned and an oval mask was placed over the image to minimize the effect of hair style.
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Table 2 Description (mean and S.D.) of semen parameter values for the total sample of 66 men (Study 1) and the three subsets of four randomly selected men representing high-quality, normal, and low-quality semen (Study 2) Motility Morphology Concentration SI
High (N = 4)
Normal (N = 4)
73.25 F 5.56 33.13 F 5.71 141.25 F 21.69 1.29 F 0.55
67.75 F 4.19 26.75 F 11.70 53.50 F 34.67 0.19 F 0.52
Low (N = 4) 33.75 F 5.06 5.00 F 3.16 14.5 F 14.89 2.08 F 0.12
Total (N = 66) 60.32 F 15.77 22.35 F 10.26 85.43 F 61.61 0.007 F 0.980
Data adjusted to a normal distribution. WHO (1999) criteria were used to perform the semen analysis for percentage of progressive motile sperm, percentage of normal sperm morphology, and sperm concentration (number of spermatozoa per milliliter). The SI was calculated from the other three by principal component analysis.
A principal component analysis (SPSS version 8.0) was used to combine the three parameters into one index, named Sperm Index (SI).
2.4. Attractiveness ratings 2.4.1. Study 1 Frontal and right-profile head and shoulder photographs of each of the 66 males were taken. Each color photograph was scanned, and an oval mask was placed over the image to minimize the effect of hairstyle, both in frontal and lateral views (Fig. 1). The resulting images were transferred to a Microsoft PowerPoint file. Plates of each individual were shown to the 66 women for 20-s exposures, followed by a neutral sound and exposure to a black image for 3 s. The women rated these computer-displayed images for attractiveness (measured as the desirability of each individual as a permanent partner {pareja estable}) on a 10-point scale (10 = top rating, 0 = lowest rating). The resulting scores from 66 women were averaged, and the median values correlated with the men’s semen parameter values using Pearson’s biponderate statistic (SPSS version 8.0).
2.4.2. Study 2 A replication of Study 1 used printed material and 12 randomly selected images of the men according to three levels of semen quality: poor, normal, and good, based on the value of the SI parameter (Table 2). (The selection of individuals was based on a division of the total sample of men into terciles according the SI parameter and randomly selecting four from each tercile.) The selected sample ranged in age from 21 to 29 years (mean = 23.9, S.D. = 2.3), with a period of reported sexual abstinence of 2–5 days (mean = 3.8, S.D. = 0.8). As in Study 1, a frontal and a right-profile head view (each 5 7 cm) were presented simultaneously in random order to be rated for attractiveness by two independent sets of women (N = 88 and N = 76, respectively), both from the Universidad de Zaragoza. The same 10-point scale as in Study 1 was used to indicate the desirability of each man as a permanent partner.
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3. Results 3.1. Study 1 There was a statistically significant correlation between the median attractiveness ratings by the 66 women and three of the semen quality parameters of the 66 men. Judgments of facial attractiveness of the men as a permanent partner were correlated with sperm morphology ( P < .01), sperm motility, and SI ( P < .05), but not with concentration (Table 3). The same pattern (for morphology, P < .05) was found for women with regular menstrual cycles and for the women who were at low fertility risk. The ratings of the eight women at high fertility risk were only correlated with sperm motility ( P < .05) (Table 3). 3.2. Study 2 In the first set of women, the median ratings of the 12 men on attractiveness as a permanent partner were significantly correlated ( P < .05) with the percentage of normal sperm morphology (Table 3). In the second set of women from the Universidad de Zaragoza,
Table 3 Correlations of semen quality parameters with the median values of male attractiveness ratings as a potential permanent partner Study 1 Regular cycles Number of women Motility Morphology Concentration SI
All women
Low fertility risk
66 .275* .325** .026 .298*
44 .287* .308* .013 .277*
High fertility risk 8 .257* .121 .040 .157
Total 52 .259* .308* .011 .275*
Study 2 Set 2 Number of women Motility Morphology Concentration SI
Set 1
Low fertility risk
High fertility risk
Total
88 .513 .578* .236 .507
46 .605* .630* .232 .562*
30
76 .592* .654* .278 .581*
.533 .573* .235 .512
Ratings in Study 1 were based on 66 facial pictures portrayed on a computer monitor, and ratings in Study 2 were from 12 printed pictures given by two sets of women (Set 1 without information about their menstrual cycle; Set 2 with information on cycle day for women with regular cycles). WHO (1999) criteria were used for the estimation of semen variables (see Table 1). * P < .05. ** P < .01.
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the median ratings of the 12 men on attractiveness were correlated ( P < .05) with the men’s percentage of sperm motility, the percentage of normal sperm morphology, and SI, but not with concentration (Table 3). Moreover, the analysis of the two fertility risk subgroups revealed a significant correlation ( P < .05) with sperm motility, morphology, and SI in the low-fertility-risk group, as was seen in Study 1, but the high-fertility-risk group had a significant correlation ( P < .05) only for sperm morphology; the correlation for motility was close to significance ( P = .07; see Table 3).
4. Discussion Our results show that the attractiveness of men’s faces was highly positively correlated with basic semen parameters. Obviously, the final choice of mate is influenced by a number of other elements, such as social and economic position, body appearance, the capacity to communicate by words and gestures, and social and parental behaviour (Pollard, 1994). Our study has shown that women are able to recognize reproductively fit males on the basis of their facial appearance alone. Previous studies have pointed out a high correlation between hand fluctuating asymmetry (expressed as the digit length ratio (2D/4D) of the right hand) and semen concentration (Manning, Scutt, & Lewis-Jones, 1998, Manning, Scutt, Wilson, & Lewis-Jones, 1998). This correlation was attributed to a possible relationship between general developmental stability and male fertility, but not to any apparent advantage for sexual selection. Moreover, it has been reported (Rolda´n & Gomendio, 1999) that numerous genes in the Y chromosome are functionally related to semen production and dimorphic traits (e.g., body size, tooth development). Among mammals, these traits influence a male’s competitive ability in male–male contests and in sperm competition (Rolda´n & Gomendio, 1999). Our results show that highly attractive faces correspond with high-quality semen samples. This is the first direct evidence of a relationship between the attractiveness of man and his physiological reproductive quality. Similar results have been observed in other animals (Birkhead & Fletcher, 1995; Rolda´n, Cassinello, Abaigar, & Gomendio, 1998), supporting our findings. This would suggest that there might be a link between genes that determine facial phenotype and those that regulate spermatogenesis. It has been argued that sexually selected traits are indicators of pathogen resistance (Kalick et al., 1998) and general health (Grammer & Thornhill, 1994; Perret et al., 1999), but the evidence has been based on indirect indices of pathogen resistance and general health (Pawlowski et al., 2000). For example, it has been shown that men whose faces were horizontally asymmetrical were more depressed and more emotionally labile, while those whose faces were vertically asymmetrical were more impulsive (Shackelford & Larsen, 1997). Moreover, facial asymmetry may be a more reliable sign of poor health in men than in women (Shackelford & Larsen, 1997). In most human populations, only the face and hands are directly observable, and these characteristics are the first on which male attractiveness must be expressed. In a preliminary study, we found that 71% of 246 women from the
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Universitat de Vale`ncia professed that the first characteristic they look at in a man is the face when evaluating his attractiveness (unpublished data). While females are considered the limiting resource for male reproduction (Trivers, 1971), nevertheless, access to a limited set of men underlies female–female competition (polygyny threshold model; Galiana, 1999). Polygynous human societies tend to be characterized by high pathogen loads (Gangestad & Buss, 1993; Low, 2000), and polygynous men in hunter– gatherer societies have more wives and more children (e.g., Kaplan & Hill, 1985). Our results suggest that women may be able to detect the quality of men’s semen from facial attractiveness, and this may, in part, affect the variance in male reproductive success. In the case of extrapair partnerships, one might expect that women would be particularly sensitive to the phenotypic quality of men, especially at midcycle when the risk of ovulating is greatest. The observation that attractiveness ratings by high risk of conception women in our study did not exhibit a significant correlation with semen quality, except for motility in Study 1 and morphology in Study 2, is discordant with the idea and with results previously presented by other authors, indicating that women are capable of selecting more symmetric partners when they are ovulating (Penton-Voak & Perret, 2000; Rikowski & Grammer, 1999; Tarı´n & Go´mez-Piquer, 2002; Thornhill & Gangestad, 1999b). Further research is required to address this question as there were several differences in our two studies and a lack of objective data on ovulation. In addition, future studies should be focused on (i) the analysis of those facial features that are most important in the establishment of facial attractiveness, and (ii) replication of our findings in other cultural environments. A preliminary study in which the same 12 men used in Study 2 were rated by women from Barranquilla (Colombia), where most of the population have Negroid traits, gave results that were completely concordant with the results of the present study (Soler et al., 2000).
Acknowledgements We thank J. Cebria´n and T. Muin˜o for handling the tests in Universidad de Zaragoza, F. Pe´rez, P. Buendı´a, and C. Gago for technical advice, I. Costello for linguistic assistance, and A. Galiana and V. Martı´nez for a careful reading of the manuscript and comments offered to C.S.
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