X-chromosome dosage affects male sexual behavior - PubMed (original) (raw)

X-chromosome dosage affects male sexual behavior

Paul J Bonthuis et al. Horm Behav. 2012 Apr.

Abstract

Sex differences in the brain and behavior are primarily attributed to dichotomous androgen exposure between males and females during neonatal development, as well as adult responses to gonadal hormones. Here we tested an alternative hypothesis and asked if sex chromosome complement influences male copulatory behavior, a standard behavior for studies of sexual differentiation. We used two mouse models with non-canonical associations between chromosomal and gonadal sex. In both models, we found evidence for sex chromosome complement as an important factor regulating sex differences in the expression of masculine sexual behavior. Counter intuitively, males with two X-chromosomes were faster to ejaculate and display more ejaculations than males with a single X. Moreover, mice of both sexes with two X-chromosomes displayed increased frequencies of mounts and thrusts. We speculate that expression levels of a yet to be discovered gene(s) on the X-chromosome may affect sexual behavior in mice and perhaps in other mammals.

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Figures

Fig. 1

Male mice with two X-chromosomes have enhanced ejaculation capacities compared to males with a single X-chromosome. All mice were castrated and treated with testosterone as adults (Cast+T). (a & c) Kaplan-Meyer curves for the percent accumulation of males reaching their first ejaculation over time in minutes (defined as the interval between the 1st thrust and the first ejaculation) during all four, one-hour trials. (b & d) Histograms of the number of mice ejaculating during 0 (white bars), 1 (lined bars), or 2+ (two or more; black bars) trials. (a) Males in the Four Core Genotypes (FCG) with two X-chromosomes (XXM; solid line) were significantly faster to ejaculate than males with a single X-chromosome (XYM, dashed line; **, P<0.01). (b) XXM ejaculated in more trials than XYM, but this difference was not significant. (c) Latencies to the first ejaculation were not different between Y* males with two copies of X (2XM, solid line) or one copy of X (1XM, dashed line). (d) 2XM ejaculated in more trials than 1XM (**, P<0.01). XXM n=12. XYM n=12. 2XM n=16. 1XM n=18

Fig. 2

Y* mice with two X-chromosomes mount and thrust more frequently during individual trials than mice with one X-chromosome. Mean ± SEM for mounting and thrusting behaviors in adult testosterone treated ovariectomized females (OVX+T) and castrated males (Cast+T) tested with receptive females; only mice that displayed the behaviors at least once were included in the calculations. (a–c) Histograms of Four Core Genotypes (FCG) behaviors. XX, XX genotype (black bars). XY, XY genotype (white bars). (d–f) Histograms of Y* behaviors. 2X, two X-chromosomes genotype (black bars). 1X, one X-chromosome genotype (white bars). FCG females have higher numbers of (a) mounts, (b) thrusts, and (c) thrusts per mount per trial than males. Y* females with two X-chromosome (2XF) have higher numbers of (d) mounts, and (e) thrusts per trial than all other groups. (f) 2X Y* mice have a higher number of thrusts per mount per trial than 1X. *Significantly different than all other groups (P<0.05). **Significant difference between mice with two X-chromosomes versus one (P<0.05). #Significant gonadal sex difference (P<0.05). Panels a–c: XX females (XXF) n=11, XX males (XXM) n=11, XYM n=9. Panel a: XYF n=11. Panels b & c: XYF n=10. Panels d–f: 2XF n=12, 2XM n=16. Panel c: 1XF n=7, 1XM n=17. Panels e & f: 1XF n=6, and 1XM n=13.

Fig. 3

Y* mice with two copies of the X-chromosome mount and thrust at a faster rate during individual trials than mice with one copy of X. Mean ± SEM for mounting and thrusting rates in adult testosterone treated ovariectomized females (OVX+T) and castrated males (Cast+T) tested with receptive females; mounting and thrusting rates were calculated after the first mount and thrust, respectively, only in individual trials in which the behaviors occurred. (a–b) Histograms of Four Core Genotypes (FCG) behaviors. XX, XX genotype (black bars). XY, XY genotype (white bars). (c–d) Histograms of Y* behaviors. 2X, two X-chromosomes genotype (black bars). 1X, one X-chromosome genotype (white bars). (a) FCG mice did not differ in mounts per minute. (b) FCG males had a faster rate of thrusts per minute than females. (c) 2X Y* mice had a faster rate of mounts per minute. (d) 2X Y* mice, and males, had faster rates of thrusts per minute than 1X mice, and females, respectively. **Significant difference between mice with two X-chromosomes versus one (P<0.01). #Significant gonadal sex difference (P<0.05). Panels a & b: XX females (XXF) n=11, XX males (XXM) n=11, and XYM n=9. Panel a: XYF n=11. Panel b: XYF n=10. Panels c & d: 2XF n=12, and 2XM n=16. Panel c: 1XF n=7, and 1XM n=17. Panel d: 1XF n=6, and 1XM n=12.

Fig. 4

Male Y* mice with two X-chromosomes show trends for increased aggression toward an intruder than males with a single X-chromosome. (a) Kaplan-Meyer curves for the percent accumulation of latency to attack an intruder-male over three, ten-minute trials. (b) Histograms of the number of mice attacking in 0 (white bars), 1 (lined bars), or 3 (black bars) trials. (a) Males with two copies of X (2XM, solid line), showed a trend for attacking an intruder faster than males with one X (1XM, dashed line; _P_=0.07). (b) 2XM showed a trend for attacking in more trials than 1XM (_P_=0.1). Cast+T, adult testosterone treated castrates. 2XM, n=20. 1XM, n=20.

Fig. 5

Y* male mice have a larger density of vasopressin immunoreactive area in the lateral septum than females. Mean ± SEM μm2 immunoreactive area. 2X, two X-chromosomes genotype (black bars). 1X, one X-chromosome genotype (white bars). OVX+T, testosterone treated ovariectomized females. Cast+T, adult testosterone treated castrated males. #Significant gonadal sex difference (P<0.05). In all groups n=9.

Fig. 6

Y* mice show no differences in gene expression of the androgen receptor (Ar), aromatase (Cyp19a1), or estrogen receptor-α (Esr1) in the preoptic area of the hypothalamus (POA). Mean ± SEM relative quantification (RQ) of: (a) Ar, (b) Cyp19a1, and (c) Esr1. RQ values were calculated using the ΔΔCt method with cyclophilin B (Ppib) as the endogenous control and normalized to the mean of 1X males. 2X, two X-chromosomes genotype (black bars). 1X, one X-chromosome genotype (white bars). OVX+T, adult testosterone treated ovariectomized females. Cast+T, adult testosterone treated castrated males. In all groups n=6.

References

1. Abel JM, Witt DM, Rissman EF. Sex differences in the cerebellum and frontal cortex: roles of estrogen receptor alpha and sex chromosome genes. Neuroendocrinology. 2011;93:230–240. - PMC - PubMed
1. Abramov U, Puussaar T, Raud S, Kurrikoff K, Vasar E. Behavioural differences between C57BL/6 and 129S6/SvEv strains are reinforced by environmental enrichment. Neurosci Lett. 2008;443:223–227. - PubMed
1. Albers HE. The regulation of social recognition, social communication and aggression: Vasopressin in the social behavior neural network. Horm Behav 2011 - PubMed
1. Arnold AP. Sex chromosomes and brain gender. Nat Rev Neurosci. 2004;5:701–708. - PubMed
1. Arnold AP. Mouse models for evaluating sex chromosome effects that cause sex differences in non-gonadal tissues. J Neuroendocrinol. 2009;21:377–386. - PMC - PubMed

X-chromosome dosage affects male sexual behavior - PubMed (original) (raw)