Sex Differences in Rhesus Monkey Toy Preferences (PDF)

18/01/2022, 05:16 Sex differences in rhesus monkey toy preferences parallel those of children Try out PMC Labs and tell us what you think. Learn More. Horm Behav. Author manuscript; available in PMC 2009 10.1016/j.yhbeh.2008.03.008 Sep 1. Published in final edite...

18/01/2022, 05:16 Sex differences in rhesus monkey toy preferences parallel those of children Try out PMC Labs and tell us what you think. Learn More. Horm Behav. Author manuscript; available in PMC 2009 10.1016/j.yhbeh.2008.03.008 Sep 1. Published in final edited form as: PMCID: PMC2583786 NIHMSID: NIHMS64461 PMID: 18452921 Horm Behav. 2008 Aug; 54(3): 359–364. Published online 2008 Mar 25. doi: Sex differences in rhesus monkey toy preferences parallel those of children 1,3 2 1,3 Janice M. Hassett, Erin R. Siebert, and Kim Wallen Abstract Socialization processes, parents, or peers encouraging play with gender specific toys are thought to be the primary force shaping sex differences in toy preference. A contrast in view is that toy preferences reflect biologically determined preferences for specific activities facilitated by specific toys. Sex differences in juvenile activities, such as rough and tumble play, peer preferences, and infant interest, share similarities in humans and monkeys. Thus if activity preferences shape toy preferences, male and female monkeys may show toy preferences similar to those seen in boys and girls. We compared the interactions of 34 rhesus monkeys, living within a 135 monkey troop, with human wheeled toys and plush toys. Male monkeys, like boys, showed consistent and strong preferences for wheeled toys, while female monkeys, like girls, showed greater variability in preferences. Thus, the magnitude of preference for wheeled over plush toys differed significantly between males and females. The similarities to human findings demonstrate that such preferences can develop without explicit gendered socialization. We offer the hypothesis that toy preferences reflect hormonally influenced behavioral and cognitive biases which are sculpted by social processes into the sex differences seen in monkeys and humans. Keywords: sex differences, toy preference, gender, hormones, rhesus monkey, children, socialization Toy play is one of the most robust human behavioral sex differences, showing moderate to very large effect sizes (Cohen-Bendahan et al., 2005; Collaer and Hines, 1995). As seen in Figure 1a, boys interact more with masculine-type toys than do girls, and girls interact more with feminine-type toys than do boys (Berenbaum and Hines, 1992). Within each sex, boys typically show strong preferences for stereotypically masculine toys, while girls often do not show a statistically greater preference for one toy type over another (Berenbaum and Hines, 1992; Carter and Levy, 1988; Eisenberg and Wolchik, 1985; Frasher et al., 1980; Perry et al., 1984; Sutton-Smith and Rosenberg, 1963; Turner et al., 1993). Thus sex differences in toy preferences are characterized by stronger gender-specific preferences in boys than in girls.  https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2583786/ 1/13 18/01/2022, 05:16 Sex differences in rhesus monkey toy preferences parallel those of children Open in a separate window Figure 1 Figure 1a: Sex difference in play with stereotypical masculine and feminine toys in a choice paradigm. Different superscripts within category or within sex indicate significant differences. (Adapted from Berenbaum and Hines, 1992).  Figure 1b: Sex difference in total frequency of interactions with plush and wheeled toys by rhesus monkeys. Different superscripts within category or within sex indicate significant differences. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2583786/ 2/13 18/01/2022, 05:16 Sex differences in rhesus monkey toy preferences parallel those of children Socialization processes have typically been offered as the primary source of the sex differences in human toy preferences. While there are many hypothesized socialization mechanisms (Bandura and Bussey, 2004; Martin and Halverson, 1981; Martin et al., 2002), one view is that societal endorsement of toys as masculine or feminine drive children’s toy preferences to conform to expected masculine and feminine gender roles (Martin and Little, 1990). Some have suggested that a greater preference for gendered toys in boys reflects a greater rejection of opposite-sex behavior in boys than in girls (Bussey and Perry, 1982). Thus, girls are less rigid than boys in their gender-typed beliefs, behaviors, and preferences, including toy preferences (Ruble et al., 2006). A striking disparity between “masculine” and “feminine” toys is in the kinds of activities with which they are typically associated (Miller, 1987). Possibly, differential attraction to these activities affects children’s toy preferences. In contrast to the socialization perspective this view posits that toy preferences reflect preferences for specific activities, such as active manipulation or cradling, facilitated by specific features of toys and that these activity biases result from the different prenatal hormonal environments of boys and girls. According to this perspective, boys’ and girls’ toy preferences reflect differences in their preference for specific activities and they thus seek out toys that facilitate those preferred activities. The “pink” and “blue” aisles in toy stores thus reflect marked gender preferences for activities and not necessarily societal imposition of gender norms on boys and girls. The socialization and activity bias viewpoints do not resolve the sex differences in the magnitude of the preference for gender specific toys. The more marked preference in boys than girls could reflect either that boys have stronger predispositions to a more limited set of activities, or alternatively that boys’ toy choices are more strongly socially constrained than are girls’ choices (Ruble et al., 2006). One approach to disentangling these potential effects is to look at “toy” preference in a species that shows hormonally biased sexually differentiated juvenile behavior, but where there is no evidence for socialization of specific gendered activities (Wallen, 2005). While demonstration that such nonhuman animals show preferences for toys similar to those seen in children would not eliminate the possibility that children’s toy preferences are primarily socialized, it would lend support to the notion that preferences for specific play objects may reflect underlying preferences for specific activities. Prenatal hormone exposure is known to influence children’s toy preferences as girls with congenital adrenal hyperplasia (CAH), an inherited enzymatic defect preventing glucocorticoid production that results in elevated prenatal adrenal androgen secretion, show more boy-typical toy preferences than do their unaffected sisters or control girls (Berenbaum and Hines, 1992; Meyer-Bahlburg et al., 2004). This preference is evident in CAH girls who look like and are reared as girls (Berenbaum and Hines, 1992; Meyer-Bahlburg et al., 2004) and despite the fact that most of these girls have typical female gender identity (Meyer-Bahlburg et al., 2004). When parental socialization was explicitly studied, one study found that CAH girls are more strongly encouraged to play with female-typical toys than are unaffected female siblings, yet they still show a masculine toy preference (Pasterski et al., 2005). Thus toy preferences appear sensitive to prenatal androgen exposure and seem unlikely to reflect sex of rearing or gender typical socialization. There is evidence suggesting that the activities facilitated by a toy determine gendered toy preferences (Campbell et al., 2000; Eisenberg et al., 1982; Miller, 1987; Servin et al., 1999). For example, children tended to explain their toy preferences in terms of what can be done with a toy, 55% of all explanations, and rarely with reference to the gender appropriateness of the toy, less than 1% of all explanations, (Eisenberg et al., 1982). Such findings support the notion that toy preferences might reflect sex differences in activity preferences.  The CAH evidence for hormonal influences on toy preference is striking; however, as long as the research is conducted only in humans, socialization and biological processes are confounded. An alternative approach is to examine nonhuman animal toy preferences, where socialization for specific toys is unlikely to determine preferences. As with boys, juvenile male monkeys engage in more rough and-tumble play than their female counterparts (Alexander and Hines, 2002; Hines and Kaufman, 1994; Lovejoy and Wallen, 1988; Maccoby, 1998; Wallen, 1996; Wallen, 2005), while girls and https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2583786/ 3/13 18/01/2022, 05:16 Sex differences in rhesus monkey toy preferences parallel those of children juvenile female monkeys show a greater interest in young infants (Herman et al., 2003; Lancaster, 1971; Leveroni and Berenbaum, 1998). These striking behavioral parallels are not reflected in parallel effects of prenatal androgen exposure in monkeys and humans. Although rough and tumble play is strongly influenced by prenatal androgen exposure in monkeys (Goy et al., 1988; Wallen, 1996), it was not increased in CAH girls (Hines & Kaufman, 1994). Similarly, infant interest has been found to be less marked in CAH girls (Leveroni and Berenbaum, 1998), but not in female monkeys treated prenatally with small doses of androgen (Herman, et al., 2003). While these contrasting results from single studies in monkeys and humans may reflect ineffective androgen exposure or inappropriate timing of androgen exposure for the behavioral endpoints, it cannot be ruled out that factors other than androgens influence the development and expression of these behaviors. Nevertheless, if toy preferences stem from activity preferences, behavioral parallels in humans and monkeys predict sex differences in monkey toy preferences. The one previous study of nonhuman primates’ interactions with human toys did not make subjects choose between masculine and feminine toys simultaneously available and thus could not directly measure preference. Instead they compared the relative proportion of interaction times with singly presented toys as a proxy for preference (Alexander and Hines, 2002). Comparisons between sexes found that the proportion of males’ toy interactions directed to masculine toys was greater than the proportion of females’ interactions directed to masculine toys. A similar, but opposite, difference was found for the proportion of interactions directed towards feminine toys, suggesting clear between-sex differences in preference for masculine and feminine toys similar to that seen in humans. When comparisons were made within sex for the magnitude of the preference, however, the results differed significantly from findings in humans. Unlike boys, male vervets spent comparable percentages of time with both masculine and feminine toys, showing no gendered toy preference. Unlike girls, female vervets spent a significantly greater proportion of time with feminine than with masculine toys. Thus, magnitudes of preferences in vervets were opposite to those seen in children. The authors suggested that the lack of a male vervet preference for masculine toys implied that boys’ strong preferences for masculine toys reflected stronger gendered socialization of boys’ toy preference relative to girls’ toy preference (Alexander and Hines, 2002). This explanation seems unlikely as it would imply that their finding of greater female vervet preference for feminine toys means that vervet monkey females are strongly socialized to prefer female toys, whereas girls’ toy preferences are not socialized. A more parsimonious explanation is that since the vervets were never presented with actual toy choices the results do not accurately reflect preferences, but show substantial cross sex willingness to play with any toy. Thus although there are substantial concordances between human and nonhuman primate gendered social behavior, nonhuman primate data leave unresolved the relative concordance between human and nonhuman primate gendered toy preferences. We investigated toy preferences in rhesus monkeys living in a 135 member long-term stable outdoor group by presenting the group with multiple trials of simultaneous access to different two toy combinations of multiple toys: one putatively masculine and one putatively feminine. We present here striking evidence of a sex difference in rhesus monkey preference for human gender-stereotyped toys paralleling that reported in humans, suggesting that gender differences in toy choice may reflect evolved sex differences in activity preferences not primarily resulting from socialization processes. Materials and Methods  Subjects Subjects were rhesus monkey (Macaca mulatta) members of a multi-male, multi-female social group of 135 animals that had lived together for more than 25 years at the Yerkes National Primate Research Center Field Station. This social group had a species-typical multiple matriline social structure with a full age-range of group members from infants to adults. Fourteen animals were not included in analyses because they had been exposed to varying hormonal treatments prenatally, but there were not enough subjects in any one treatment group to systematically analyze preferences. Additionally, the https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2583786/ 4/13 18/01/2022, 05:16 Sex differences in rhesus monkey toy preferences parallel those of children interactions of 39 newborn (0–3 months) infants, while minimal, were not coded due to difficulty in consistent individual identification. This left 61 females and 21 males as potential subjects. Table 1 displays these animals by rank and age. Subjects were housed with their natal group in 25m × 25m outdoor compounds with attached temperature-controlled indoor quarters. Water was continuously available, and the animals were fed monkey chow twice daily, supplemented once per day with fruits and vegetables. research was conducted in accordance with the NIH Guide for the Care and Use of Laboratory Animals and under an environmental enrichment/management protocol of the Yerkes National Primate Research Center approved by Emory’s Institutional Animal Care and Use Committee. Table 1 Males and females by rank and age: totals and participation (non-natal animals do not have matrilineal rank) Non-natal Ranks 1–3 Ranks 4–8 Ranks 9–13 Ranks 14–16 TOTAL Males in group 2 1 4 6 8 21 Males participating 1 (50%) 0 3 (75%) 3 (50%) 4 (50%) 11 (52%) Females in group 0 8 15 17 21 61 6 (75%) 6 (40%) 4 (24%) 7 (33%) 23 (38%) Females participating subadult (5– 7) TOTAL adult (8– 12) juvenile (1– 4) "elderly"(13+) Males in group 12 7 0 2 21 Males participating 8 (67%) 2 (29%) 1 (50%) 11 (52%) Females in group 23 12 14 12 61 10 (43%) 5 (42%) 3 (21%) 5 (42%) 23 (38%) Open in a Females participating separate window Materials Because we hypothesized that some aspects of sexually differentiated toy preferences reflect activity preferences, we categorized our toys not by traditional gender assignment, but by specific object  properties that made our categories comparable, though not exact matches, to stereotypical gender assignments. Thus one set of toys was “wheeled,” most comparable to the masculine vehicle toys and the other was “plush,” most comparable to the feminine doll and stuffed animal toys. The seven plush toys were: Winnie-the-Pooh™, Raggedy-Ann™, a koala bear hand puppet, an armadillo, a teddy bear, Scooby-Doo™, and a turtle. The sizes ranged in length from about 14 cm to 73 cm. The six wheeled toys were: a wagon, a truck, a car, a construction vehicle, a shopping cart, and a dump truck. These ranged in length from 16 to 46 cm. Plush and wheeled toys varied considerably in shape and color as well. Data Collection https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2583786/ 5/13 18/01/2022, 05:16 Sex differences in rhesus monkey toy preferences parallel those of children Seven 25min trials were conducted within the large indoor/outdoor enclosure that housed the social group. Prior to each trial, subjects and other social group members were sequestered indoors while one wheeled and one plush toy separated by 10m were placed in the outdoor living area, with left or right placement location counterbalanced across trials. Monkeys were then released into the outdoor area and each toy and any animal interacting with it was videotaped using separate cameras for each toy. In one case, a plush toy was torn into multiple pieces, ending the trial 7min early. After each trial, toys were removed from the outdoor area. The identity of every animal interacting with the toys and specific behaviors (Table 2) directed towards the toys were coded from the videotapes by two observers working together to achieve consensus on both identity and behaviors. Data were entered on Palm Pilots (IIIXE, Palm Inc., Santa Clara, CA) equipped with Handobs (Center for Behavioral Neuroscience, Atlanta, Georgia), a program designed for entering time-stamped behavioral information. Individuals’ social rank and age were included as variables in the analyses. Rank had been assessed for all individuals in the group through extensive behavioral observations documenting the directionality of grooming, dominance, and submission behavior. Table 2 Interactions with plush and wheeled objects coded from videotaped trials Behavior Description Extended touch Placing a hand or foot on toy Hold Stationary support w/one or more limbs Sit on Seated on the toy or a part of the toy Carry in hand Moving w/toy in hand and off the ground Carry in arm Moving w/ toy in arm and off the ground Carry in mouth Moving w/toy in mouth and off the ground Drag Moving the toy along the ground behind the animal Manipulate part Moving, twisting, or turning a part Turn entire toy Shifting 3-D orientation of toy Touch Brief contact using hands or fingers Sniff Coming very close to the toy with the nose Mouth Brief oral contact – no biting or pulling Destroy Using mouth or hands to bite or tear toy Jump away Approach, then back away from toy with a jumping motion Throw Project into air with hands  Open in a separate window Data analysis All instances of any specific behavior were counted to provide frequencies of occurrence. For behaviors that were continuous, onsets and offsets were also recorded to derive durations of those behaviors. Subjects participated in different numbers of trials so raw frequencies and durations for each subject were divided by the number of trials that subject participated in to provide an average frequency or duration of each behavior.. Subjects with fewer than 5 total behaviors (3 males and 14 females) were excluded from analyses, producing a final n of 23 females and 11 males. Males and 2 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2583786/ 6/13 18/01/2022, 05:16 Sex differences in rhesus monkey toy preferences parallel those of children 2 females did not differ in the proportion of subjects excluded (X (1)=1.23). Total frequencies and total durations were calculated for each animal by summing the calculated averages for each individual behavior.. Analyses were completed using SPSS for Windows (Version 13, SPSS Inc.) and a Microsoft Excel (Microsoft Corp, Redmond, WA) macro for Heterogeneity G-tests (Sokol and Rohlf, 1995). Cohen’s d, a measure of effect size that compares pairs of means and standard deviations (Cohen, 1992), was calculated separately for contrasts of interest. P , a measure of probability of replication rep based on sample size and effect size (Killeen, 2005), is also reported. An examination of the distribution of the behavioral variables using the Kolmogorov-Smirnov test revealed positive skew due to a majority of animals showing relatively low frequencies and durations of behaviors with a few individuals showing very high rates of interaction. Focusing analyses on total frequencies and total durations of interaction rather than on individual behaviors reduced but did not eliminate skew. Square root transformations of total frequency data eliminated skew except for total duration data. To make analyses of both types of data as comparable as possible, we conducted ANOVAs on untransformed total frequency and total duration data to allow us to identify interactions. However, when significant interactions were revealed, follow up comparisons used nonparametric tests on the untransformed data. While we found that skew was no particular threat to the validity of our results when using only parametric tests, we felt the combination of parametric ANOVAs with nonparametric tests for other comparisons to be the most conservative approach to analyzing these data. Results Table 1 identifies the characteristics of the animals included in the analyses, sorted by sex and rank and by sex and age, and the proportion of the total potential males and females in each age and rank group that participated. Total frequency showed a significant interaction between toy type and sex, F = 4.49, p=.04, and (1,32) transformed total frequency was also significant. Nonparametric within-sex comparisons revealed that males preferred wheeled over plush toys (Figure 1b; Z=−2.09, p=.04, d=1.14, p =.95), and that rep females exhibited no significant preference for plush toys over wheeled toys (Figure 1b; Z=−.55, p=.58, d=.12, p =.61). For between-sex comparisons, males and females did not differ in their total rep interactions with wheeled toys (Figure 1b; Z=−.65, p=.52, d=.39, p =.87), but males interacted rep significantly less with the plush toys than did females (Z=−2.23, p=.03, d=.76, p =.98). rep Total duration also showed an interaction between toy type and sex, F =4.65, p=.04. This (1, 32) significant interaction is noted with caution, given the violation of the assumption of normality. As a  follow up, nonparametric Mann-Whitney U comparisons, reflecting the non-normal distributions, revealed a pattern of within-sex effects similar to that seen for the frequency data: males interacted for a greater total time with wheeled (mean ± SEM: 4.76min ± 2.29) than with plush objects (.53min ±.43; Z=−2.22, p=.03, d=.77, p =.88), while females did not differ in the duration of interactions with the rep toy types (wheeled: 1.27 ±.46; plush: 1.49 ±.79; Z=−.82, p=.41, d=.07, p =.56). Overall rep comparisons between males and females revealed that they did not differ significantly in the total time spent with wheeled (Z=−1.20, p=.23, d=.33, p =.87) or with plush (Z=−1.27, p=.21, d=.62, p =.73) rep rep objects. We compared males and females on the magnitude of preference for sex-typical toys. Difference scores were calculated for males and females in the following way: for males, total frequency wheeled - total frequency plush; for females, total frequency plush - total frequency wheeled. The same calculations of difference scores were also completed for total duration. The duration difference scores were significantly skewed and the skew remained for transformed data. Thus, to provide comparable statistical power, nonparametric Mann-Whitney U tests were used for both the frequency and duration data, even though only the duration data were skewed. A significant sex difference in magnitude of preference was revealed for frequency (Males: 7.71 ± 3.11; Females: 1.00 ± 2.42; Z = −2.45, p =.01, d https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2583786/ 7/13 18/01/2022, 05:16 Sex differences in rhesus monkey toy preferences parallel those of children =.61, p =.96) and duration (Males: 4.23 ± 2.42; females:.22 ±.85; Z = −2.23, p =.03, d =.63, rep p =.96). Thus males exhibited a significantly higher preference for the “masculine” (wheeled) toys rep than did females for the “feminine” (plush) toys. 2 As seen in Table 1, participating males and females were comparably distributed across ranks (X = 3.36, p =.18). In addition, a comparison of mean rank between males (9.3) and females (8.7) revealed no significant differences, t =−.77, p=.45. When dominance rank was included as a covariate in 32 frequency data analyses, the interaction between toy type and sex was not significant, F =3.90, (1,31) p=.06, and the interaction between toy type and rank was also not significant F =.78, p=.39. When (1,31) the frequency data were transformed, however, then the interaction between toy type and sex remained significant even with rank as a covariate. For the untransformed duration data, the sex by toy interaction remained significant with rank as a covariate (F =4.56, p=.04) and the toy by rank (1,31) interaction was not significant (F =.05, p=.82). We also conducted Spearman’s correlations to (1,31) determine the relationship between rank and frequency or duration with each toy type. With both sexes combined, rank and total frequency were positively correlated for both the plush toy (r =.43, p=.01, s 2 s2 r =.18) and the wheeled toy (r =.38, p=.03, r =.14), accounting for 18% and 14% of the variance, 2 s s2 respectively. For males, plush toy (r =−.36, p=.27, r =.18) and wheeled toy (r =.21, p=.53, r =.04) total s2 frequencies did not correlate significantly nor did total durations (plush: (r =−.31, p=.35, r =.10; s2 wheeled: r =.005, p=.99, r