An Experimental Test of the Westermarck Effect: Sex Differences in Inbreeding Avoidance

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Behavioral The official journal of the ISBE Ecology International Society for Behavioral Ecology

doi:10.1093/beheco/art028 Advance Access publication 18 April 2013 Original Article An experimental test of the Westermarck effect: sex differences in inbreeding avoidance

Urszula M. Marcinkowska,a Fhionna R. Moore,b and Markus J. Rantalaa Downloaded from aUniversity of Turku, Department of Biology, Sect Ecol, Turku 20014, Finland and bUniversity of Dundee, School of Psychology, Dundee DD1 4HN, Scotland UK

In order to avoid inbreeding, humans and other animals develop a strong sexual aversion to individuals with whom they have lived closely in http://beheco.oxfordjournals.org/ infancy and early childhood (usually biological siblings), a phenomenon called the “Westermarck effect” or negative sexual imprinting. The mechanisms underlying this phenomenon, however, remain unclear. For example, it is not known whether negative imprinting is based only on actual sexual aversion to brothers and sisters or also on generalizing the traits of their siblings to nonkin. If imprinting is more general, one could predict that people would avoid mating with all individuals that resemble their other-sex siblings. In our study, women rated morphed other-sex faces that resemble their siblings as significantly lower in sexual attractiveness than morphed faces on average, and the opposite effect was found in men—similarity to sibling increased perceived attractiveness. Interestingly, self-similarity did not influence the preferences of either men or women. These sex differences are consistent with parental investment theory, as females bear greater costs associated with inbreeding depression, perhaps explaining their deeper aversion toward engagement in sexual activities with male individuals who bear cues to relatedness. Furthermore, they indicate that faces resembling siblings are valid stimuli for investigating facial similarity preference. at University of Turku on September 5, 2013 Key words: facial preferences, inbreeding avoidance, incest avoidance, sexual imprinting, Westermarck hypothesis. [Behav Ecol]

Introduction is critical for sibling sexual aversion (the “Westermarck effect”). Inbreeding depression (the accumulation of recessive deleterious The most commonly cited example of the Westermarck effect in alleles and loss of heterosis) is strongly positively correlated with humans comes from data acquired from Israeli kibbutzim, in which degree of kinship of sexual partners (Lynch and Walsh 1998), and participants were found to be unlikely to marry, or to feel sexual the negative consequences of inbreeding for fitness are well docu- desire for, individuals from the communal peer group in which they mented across species (Keller and Waller 2002), including humans were raised (Shepher 1971, 1983). These findings, however, have (Postma et al. 2010). Hence, negative sexual imprinting (i.e., avoid- recently been questioned by Shor and Simchai (2009) who report ance of mating with individuals who resemble kin, based on a visual in-depth interviews with adults who grew up in the kibbutzim template created during development) should be an important adap- communal education system revealing virtually no sexual aversion tation (see Schmitt and Pilcher 2004; Rantala and Marcinkowska toward peers (reviewed in Rantala and Marcinkowska 2011). Results 2011). A number of studies show a tendency for individuals to avoid more consistent with the Westermarck effect are derived from mating with others raised in the same peer or family group: prairie studies of the success of arranged marriages, in which cosocialized dogs (Cynomys ludovicianus) avoid copulations with resident close kin individuals show mutual sexual aversion, higher divorce rates, and (Hoogland 1992), female lions (Panthera leo, Hanby and Bygott 1987), have fewer children (e.g., sim-pua marriages [“little daughter-in- marmosets (Callithrix jacchus), and tamarin monkeys (Saguinas ursula) law”] from southern China and Taiwan, where preadolescent girls postpone sexual maturation if their father or male siblings are pres- are adopted by the family of her future husband (Wolf 1970, 1985); ent during maturation (Abbott 1993), baboons (Simia hamadryas) show patrilateral parallel cousins marriages in the Middle East, where a dispersal from their native group (Livingstone 1980), and female pilot boy is marrying his father’s brother’s daughter (McCabe 1983); or whales (Globicephala melas) reproduce only with males from outside the Karo Batak matrilateral cross-cousins of Sumatra, where a boy is to natal pod (Amos et al. 1993, reviewed in Pusey and Wolf 1996). marry his mother’s brother’s daughter (Fessler 2007)). In Morocco, Westermarck (1921) hypothesized that proximity to others during it was found that sleeping in the same room and having daily social development serves as a cue to biological relatedness and hence contact between other-sex cousins during childhood produced an aversion to marrying a cousin as an adult (Walter 1997; Walter and Buyske 2003). In another study conducted in the United States, siblings’ separation for more than a year during the first 6 years of Address correspondence to U.M. Marcinkowska. E-mail: [email protected]. life increased the likelihood of incestuous, potentially procreative, Received 23 August 2012; revised 7 March 2013; accepted 16 March 2013. sexual behaviors (Bevc and Silverman 1993, 2000). Furthermore,

© The Author 2013. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: [email protected] Marcinkowska et al. • Sex differences in inbreeding avoidance 843 empirical tests for moral (Lieberman et al. 2003, 2007) and daily basis during the first 15 years of their lives, were heterosexual third-party (Fessler and Navarrete 2004) attitudes toward sibling (1–3 on the Kinsey scale question included within the sociodemo- incest show that coresidence while growing up with an other-sex graphic part of the survey), white Caucasian, and of Polish nation- individual is correlated with the expression of negative attitudes ality. All women in the study reported no pregnancy and no use of toward sibling incest. hormonal contraceptives. In humans, cognitive kin-recognition mechanisms have been proposed to govern incest avoidance (Lieberman et al. 2003). Such Stimuli neural circuitry (e.g., a kinship estimator that computes the estimated Male and female “base” faces were constructed by averaging together genetic relatedness between self and a potential sexual partner) is the shape and color of the faces of 5 individuals of matched eth- suggested to trigger sexual aversion to kin. Beside environmental nicity, nationality, and age group using the PsychoMorph Program cues, assessment of kinship can also be facilitated through compari- (Tiddeman et al. 2001). Each picture was delineated based on points son of physical cues of an individual (e.g., the face) to a family tem- located on visual landmarks of the face, following previous research plate (phenotype matching) (DeBruine et al. 2008). Generally, facial (among others DeBruine 2005). “Self-morph” and “sibling-morph” judgment plays an important role in third-party relatedness esti- stimuli were constructed for each participant. Self-morphs were cre- mation of faces (Maloney and Dal Martello 2006). Self-similarity ated by calculating the shape difference between participant’s face increases perceptions of trustworthiness and willingness to coop- Downloaded from and the same-sex base face and applying 50% of this difference to erate (DeBruine 2002, 2005) and preferences for children’s faces the other-sex base face (Penton-Voak et al. 1999; Figure 1). This (Platek et al. 2002, 2003; Bressan et al. 2009), but reduces prefer- was repeated to create the sibling morph, replacing the participant’s ences for adult faces in a mating context (Debruine 2005; DeBruine face in the transform with that of their sibling. By adding the differ- et al. 2011). Recently, it has also been reported that having other- ence between participant and same-sex base face (not directly add- sex siblings is correlated with sexual attitudes toward a phenotypic ing the difference between participant and the other-sex base face), http://beheco.oxfordjournals.org/ cue of kinship in unfamiliar faces achieved by computer-generated we ensured that transformation did not unnecessarily masculinize or facial resemblance (DeBruine et al. 2011). feminize the stimuli (see Debruine 2004). This resulted in a set of There is also, however, evidence for plasticity in human inbreed- 128 images (64 self-morphs and 64 sibling morphs). ing avoidance strategies, including birth order effects such that later born children experience stronger sexual aversion to siblings than earlier born children due to a longer period of cosocialization Procedure with the siblings. Also observing one’s own mother breastfeeding Participants judged the attractiveness of a subset of the facial stimuli and nurturing another infant is a strong cue to kinship detection on a scale of 1–7 (1 = not at all attractive, 7 = very attractive) and and later incest repulsion, which is available only to older off- completed a short sociodemographic survey consisting of questions spring (Lieberman 2009). Also, each additional cosocialized sibling about their age, education, sexual orientation, number of siblings, and at University of Turku on September 5, 2013 increases the strength of disgust response toward incest, although years spent with the family, as well as questions about hormonal sta- this tendency was statistically significant only for men (Fessler and tus for women (e.g., whether or not they were pregnant or using hor- Navarrete 2004). monal contraceptives). Participants were randomly allocated to 1 of 8 The aim of our study is to test the existence of sexual imprinting groups, each consisting of 8 participants. Each group rated a subset (negative or positive) by examining preferences for stimulus faces cre- of 16 facial images, comprised of each of the 8 members’ self- and ated to differ in resemblance to self and to sibling. Based on nega- sibling morphs. Stimuli were displayed in random order. In this way, tive sexual imprinting and the Westermarck effect, we predict that each morph of each participant received 8 ratings. Three scores were self-resemblance and sibling resemblance will reduce the attractive- computed for each participant: self-preference, sibling preference, and ness of faces. Furthermore, parental investment theory posits that nonkin preference. the minimum costs of producing offspring are higher for women than for men, meaning that the costs of a child suffering the negative consequences of inbreeding depression will be higher for women Results (Fessler and Navarrete 2004). Therefore, we also predict that nega- In a mixed-model analysis of variance (1 within-subjects factor: tive imprinting will be stronger for female participants than for male stimulus type [3 levels: self-morph, sibling morph, and nonkin]; participants. Facial resemblance in previous research has been based 1 between-subjects factor: sex [2 levels: male and female]), there on morphing a picture of the participant himself/herself with that of were no significant main effects of either stimulus type or sex an unrelated individual. Although self-morphs undoubtedly contain (P > 0.3). However, there was a significant interaction between cues to kinship (as siblings and other kin are likely to share many facial stimulus type and sex (F(1,62) = 5.73, P = 0.004). Figure 2 shows characteristics), it is more ecologically valid to create morphs based on images of the participants’ real siblings. Therefore, in the current study, we created both self- and sibling morphs to manipulate kinship perception.

Methods Participants

Thirty-two sibling pairs (i.e., 43 women, mean age = 26 [standard Figure 1 deviation, SD = 3.95] and 21 men, mean age = 25.7 [SD = 3.35]) The example of other-sex transforms: (a) participant; (b) transform of the took part in the study. There were 20 same-sex and 12 other-sex participant and an average male; (c) average male; (d) transform of sibling sibling couples. All participants had cohabited with a sibling on a of the participant and average male; (e) sibling of the participant. 844 Behavioral Ecology that attractiveness ratings by men were highest for sibling morphs that shows that men prefer the faces of women who resemble their and for women for nonkin. For women, post hoc t-tests showed a mother (Marcinkowska and Rantala 2012). This finding has been significant difference between the rating of sibling morph and interpreted as sexual imprinting-like mechanism—preference toward nonkin (t43 = −2.66, P = 0.011), a nonsignificant tendency in putative partners that bear facial similarity to one’s parent—that is difference between self-morph and nonkin rating (t43 = −1.71, P not modulated by the relationship with the parent during childhood = 0.095), and no difference between self-morph and sibling-morph and in women is suppressed by inbreeding avoidance. Therefore, rating (t43 = 1.07, P = 0.291). In men, sibling morphs were ranked our results could be interpreted as a positive sexual imprinting-like significantly more attractive than self-morphs (t19 = 2.21, P = 0.039) mechanism that is extended to siblings. It is interesting, then, that and tended to be more highly ranked than nonkin (t19 = 1.64, the same effect was not found for self-morphs for men. P = 0.118), but there was no significant difference between the The observed difference between preferences for self- and sib- ranks of self-morphs and nonkin (t19 = 0.10, P = 0.92). ling-morphed stimuli sheds light on the exposure effect proposed to account for kin attraction (proposed among others by Freud 1953). Also in later studies, it has been showed that increased familiarity with Discussion a presented stimulus can enhance rated attractiveness of the stimu- In this study, we tested for negative sexual imprinting and the lus (Zajonc 1968). Sibling morphs were rated as significantly higher

Westermarck effect in humans. We predicted that, if humans in attractiveness than self-morphs by men, meaning that self-refer- Downloaded from are adapted to avoid inbreeding, preferences for self- and sibling- ent phenotype matching could not be responsible for the attraction resembling faces would be lower than those for nonkin faces. We toward close kin, as it was visible significantly only in sib, but not self- did not find general support for this prediction, but we found a sex- morphs in men. Women’s aversion to kin suppresses the attraction to specific effect such that women preferred nonkin faces significantly similarity and as a result it enhances aversion toward sibling but not more than those morphed with their sibling and men preferred self-similar faces. As the genetic and phenotypic similarity between http://beheco.oxfordjournals.org/ sibling-resembling faces more than nonkin and self-similar faces. siblings can differ, using the real sibling for stimuli pictures can have This sex-specific asymmetry in sexual aversion to kin is consistent variable outcomes (when expecting inbreeding avoidance based on with a parental investment theory of inbreeding avoidance. Females phenotype matching). However, as it constitutes 50% on average, we are proposed to bear higher minimum proximate costs associated expected that even if variable, the amount of shared genes and there- with inbreeding depression, causing them to develop deeper aversion fore facial similarity will be always higher than expected by chance. toward engagement in sexual activities with male individuals who Broadly speaking, mating strategies are an adaptive behavior func- bear cues of relatedness (Trivers 1972; Tooby 1977; Hang 1999). Our tioning in present but shaped in the past—when phenotype match- finding is consistent with those of previous studies, albeit using differ- ing could not be based solely on self, as mirrors were not accessible ent methods, which show that aversion toward siblings is stronger for (pointed out also in Debruine et al. 2008). Hence, a definite advantage women than for men (Walter and Buyske 2003). Therefore, women of using this method to test negative imprinting is that it projects the at University of Turku on September 5, 2013 should be better equipped for detecting similarity, as the putative costs real-life situation (cohabitation with a sibling and a sibling being the of inbreeding depression are stronger for them than for men. direct stimulus for creation of inbreeding avoidance) better than com- Interestingly, men showed stronger preferences for faces that posite faces based on self-picture. resembled their sibling. Because female siblings are likely to resem- Our results showed no significant change of preference when ble the participant’s mother, the result is consistent with research judging picture of self-similar faces (comparing both with that of

Figure 2 Facial preference toward stimulus morphs (self-similar, dark grey; sibling similar, lightgrey; and nonkin similar, white) for male and female participants. Marcinkowska et al. • Sex differences in inbreeding avoidance 845 sib morph and nonkin morph). This would mean that a switch of Hang D. 1999. Asymmetric relations: internal conflicts and the horror of preference is triggered by similarity to kin rather than similarity to incest. Evol Hum Behav. 20:83–98. self. Our results are valuable as they not only confirm the results Hoogland JL. 1992. Levels of inbreeding among prairie dogs. Am Nat. 139:591–602. of the previous studies on positive sexual imprinting (among others Keller LF, Waller DM. 2002. Inbreeding effects in wild populations. Trends Bereczkei et al. 2004; DeBruine 2004; Marcinkowska and Rantala Ecol Evol. 17:230–241. 2012), but more importantly support the outcomes of negative Lieberman D. 2009. Rethinking Taiwanese minor marriage data: evidence sexual imprinting by experimental study—based on real sibling the mind uses multiple kinship cues to regulate inbreeding avoidance. Evol Hum Behav. 30:153–160. faces. Furthermore, we postulate that sibling morphs (and not self- Lieberman D, Tooby J, Cosmides L. 2003. Does morality have a biological morphs) are more sensitive for tests of preference using changes basis? An empirical test of factors governing moral sentiments regarding in similarity and are likely to be more ecologically valid. The incest. Proc R Soc B. 270:819–826. next stage of investigation into this postulated inbreeding avoid- Lieberman D, Tooby J, Cosmides L. 2007. The architecture of human kin ance mechanism should be to analyze the fluctuation of women’s detection. Nature. 445:727–731. Livingstone FB. 1980. Incest and evolutionary theory. Am J Phys Anthropol. preference/avoidance during menstrual cycle and analyzing the 52:249. influence of number and age of siblings on judgments of actual Lynch M, Walsh J. 1998. Genetic analysis of quantitative traits. Sunderland: sibling-similar faces. Sinauer.

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