1. Mate Selection, Sexual Orientation, and Pair Bonding
Chapter 48
Mate Selection, Sexual Orientation, and Pair Bonding
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2. FIGURE 48.1 Percentages of mating choices made by male goats (left panel) and sheep (right panel) that had been cross-fostered at birth and raised by females of the other species. At 1 year of age, males were given a mating choice between tethered ewes and tethered nanny goats. Sheep and goats raised by females of their genetic species mated exclusively with members of their own species (data not shown). In contrast, cross-fostered males in both species mated with their maternal species. This reversed-mating choice was observed if young lambs and goats were raised alone or with a twin of their maternal species (dark column) as well as if they were raised with a twin of their genetic species (variable shaded column). Reversed choices expressed by 1-year-old males were maintained up till 4 years of age despite the fact that animals lived exclusively with members of their genetic species after year one. Source: Redrawn from Ref. 19.
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3. FIGURE 48.2 Perinatal inhibition of aromatase reverses the adult sex-partner preference of male rat expressed as time (seconds) spent in the female compartment minus time in the male compartment when subjects were tested with sexual odors only (A) or with tethered live subjects as stimuli (B). Experimental subjects were control males and females and males exposed to the aromatase inhibitor 1,4,6-androstatriene- 3,17-dione (ATD) pre- and postnatally.56
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4. FIGURE 48.3 Effect of treatment with estradiol benzoate (EB), at high or low dose, during the first 3 weeks of life on the sexual preferences of female rats. The preference scores represent the time spent by the animal in the test chamber containing a female minus the time spent in the chamber containing a male during tests performed in adult ovariectomized subjects treated with estradiol benzoate (EB; left) or with EB plus progesterone (EB + P; right). A negative score indicates a preference for males (usually observed in control females). A positive score indicating a reversal of this choice (preference for females) was observed following treatment with EB at both doses used. Source: Redrawn according to data in Ref. 58.
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5. FIGURE 48.4 Effect of lesions of the medial preoptic area on sexual preferences in male ferrets. Control males (Ctrl) spend the majority of their time in the compartment containing a female and vice versa. Male preferences are reversed following a bilateral lesion of the preoptic area but not by unilateral lesions or lesions of a different, usually adjacent, brain site (missed). Source: Redrawn from data in Ref. 65.
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6. FIGURE 48.5 Theoretical model illustrating how fluctuations around the average concentration or action of testosterone in male and female embryos in humans or other mammalian species could affect sexual orientation and partner preference. Male embryos at the low end of the male distribution and female embryos at the high end of the female distribution are, in this model, beyond a critical threshold of testosterone action and thus exposed to a testosterone concentration or action able to produce a phenotype characteristic of the opposite sex. In this condition they would develop a homosexual orientation.
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7. FIGURE 48.6 Percentages of bi- or homosexual subjects expressed as the ratio of the numbers of subjects rating between K2 (largely heterosexual but also distinctly homosexual) and K6 (completely homosexual) on the Kinsey scale to the total number of subjects (K0 to K6) in girls exposed to prenatal androgenization linked to the syndrome of congenital adrenal hyperplasia (CAH). This percentage increases with the severity of the CAH phenotype from the nonclassical (NC) to the simple virilizing (SV) to the salt-wasting (SW) type. The number of subjects in each category of CAH is indicated below the graph. Source: Drawn from data in Ref. 93.
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8. FIGURE 48.7 Ratio of lengths of the index (2D) and ring finger (4D) as a function of sex and sexual orientation. This figure is reproduced in color in the color plate section. The 2D:4D ratio is greater in women than in men, probably due to in utero exposure to testosterone of male embryos. It is close to the male level in homosexual women, suggesting that they have been exposed to abnormally high levels of testosterone during a part of their embryonic life. For unknown reasons, these differences are more pronounced in the right hand. * = p < 0.05, *** = p < Source: Redrawn from Ref. 117.
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9. FIGURE 48.8 Relationship between sex and sexual orientation and the ratio of width to length of the hand. This figure is reproduced in color in the color plate section. Source: Redrawn from data in Ref. 123.
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10. FIGURE 48.9 Frequency of oto-acoustic emissions (OAE) evoked by click sounds measured in the right ear in men and women as a function of sexual orientation. This figure is reproduced in color in the color plate section. OAE are sexually differentiated and significantly masculinized in homosexual females. Source: Redrawn from data in Refs 124,127.
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11. FIGURE Changes in blood concentrations of luteinizing hormone (LH) in response to injection of a single dose of the estrogenic compound Premarin in heterosexual men and women and in homosexual men. Source: Redrawn from Ref. 135.
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12. FIGURE Average size of the anterior commissure as estimated by its surface in the mid-sagittal plane (left) and volume of the 3rd interstitial nucleus of the anterior hypothalamus (INA-3) (right) in men, gay men, and women. This figure is reproduced in color in the color plate section. Data for the anterior commissure are presented as means ± SEM, whereas for INAH-3 the average value in each group, as well as all individual data points, are shown to clearly illustrate the partial overlap between groups despite the significant differences between men and women and between men and gay men. Individual data points are filled in subjects who died from AIDS and open in subjects who died from other causes. The smaller average size of INAH-3 in gay men cannot be accounted for by the fact that all subjects included in the study had died from AIDS since in the control group, the INAH-3 of men who died from AIDS is not smaller than in men who died from other causes. Source: Redrawn from data in Refs 140,141.
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13. FIGURE Mean percentage of time spent by adult male or female Japanese quail near subjects of the opposite sex that were either familiar siblings (birds were raised together) or unfamiliar subjects with varying degrees of relationship (siblings, 1st or 3rd cousins, unrelated). Source: Redrawn from Ref. 230.
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14. FIGURE 48. 13 Photograph of prairie vole family
FIGURE Photograph of prairie vole family. Pair-bonded male and female prairie voles share a nest and territory and both parents provide parental care to the offspring. Source: Photo by Todd H. Ahern.
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15. FIGURE (A) Illustration of the Partner Preference Test initially developed by Carter and colleagues266 as a proxy for pair bond formation in prairie voles. Prairie voles are cohabited with an opposite-sex partner for a set amount of time. Mating can be controlled by inducing receptivity in the female with estrogen or preventing receptivity by ovariectomy. Drugs may be infused just prior to or during the cohabitation. The partner preference test takes place in a three-chamber testing arena in which the partner is tethered in one chamber, a novel opposite-sex “stranger” is tethered in the opposite chamber, and the experimental subject is placed in the center and is free to interact with either stimulus animal for 3 h. Time in each cage or time huddling with the partner is quantified. An animal is said to have developed a partner preference if it spends more than twice as much time with the partner than with the stranger. The partner preference test can be easily automated using video-based behavioral analysis software.270 (B) Typical results following a 24-h cohabitation with mating. Source: Adapted from Ref. 271.
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16. FIGURE Receptor autoradiography showing the distribution of oxytocin receptor (OTR) binding in the prairie vole and nonmonogamous montane vole brain. Prairie voles have higher densities of OTR in the nucleus accumbens (NAcc) than do nonmonogamous species. The bar graph illustrates the effect of infusing artificial cerebrospinal fluid (CSF, control) or an OTR antagonist into the NAcc, prefrontal cortex (PFC), or the caudate putamen (CP) on mating-induced partner preference formation in female prairie voles after a 24-h cohabitation with a male. Note the OTR antagonist infused into the NAcc and PFC blocked the partner preference. Asterisks indicate statistically significant differences (p < 0.05) in the time spent with partner versus stranger. Source: Adapted from Refs 277,278.
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17. FIGURE Receptor autoradiography showing the distribution of vasopressin V1a receptors (V1aR) in the prairie vole and montane vole forebrain. Prairie voles have higher densities of V1aR in the ventral pallidum (VP) than meadow voles. The bar graph illustrates the effect of infusing a V1aR antagonist into the VP, medial amygdala (MeA), and mediodorsal thalamus (MDthal) on mating-induced partner preferences in male prairie voles. Note that the V1aR antagonist only blocked partner preferences when infused into the VP. Other studies have also shown that blocking V1aR in the lateral septum (LS) also blocks partner preference formation. Asterisks indicate statistically significant differences (p < 0.05) in the time spent with partner verses stranger. Source: Adapted from Refs 277,296.
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18. FIGURE Schematic of the vasopressin V1a receptor gene (Avpr1a) in monogamous prairie voles and nonmonogamous meadow voles. The boxes indicate exons, and the black bars in the exon represent the transmembrane domains of the receptor. The sequences are highly homologous except for a complex repetitive element, referred to as a microsatellite, in the 5′ flanking region of gene (hatched box upstream of the transcription start site, +1). The prairie vole microsatellite is larger than that of the meadow or montane vole. The microsatellite length is polymorphic in prairie voles, and the length has been associated with variation in V1aR binding in the brain as well as behavior in the laboratory, but not in field studies. The brains illustrate the differences in V1aR binding in the lateral septum (LS) between prairie voles with long versus short microsatellites. Source: Adapted from Refs 305,306.
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19. FIGURE Viral vector-mediated shRNA knockdown of the prairie vole V1aR in the ventral pallidum (VP) prevents matinginduced partner preference formation in males. Receptor autoradiography reveals an average reduction in V1aR binding in the VP of 30%, consistent with natural variation in V1aR binding, in shRNA-treated males (upper right brain) compared to males injected with a virus expressing a scrambled sequence (upper left brain). This reduction in V1aR binding impaired partner preference formation is illustrated in the bar graphs below. Asterisks indicate statistically significant differences (p < 0.05) in the time spent with partner versus stranger. These data support the hypothesis that natural variation in Avpr1a gene expression contributes to variation in pair bonding behaviors. Source: Adapted from Ref. 315.
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20. FIGURE 48. 19 The role of dopamine in partner preference formation
FIGURE The role of dopamine in partner preference formation. (A) Female prairie voles were injected intraperitoneally with saline, a dopamine D1 receptor antagonist (D1-ant) or a D2 receptor antagonist (D2-ant) prior to a 24-h cohabitation with mating. The saline and D1-ant groups displayed a robust partner preference, however, the D2 antagonist prevented partner preference formation. It was subsequently shown that D2 antagonist infused into the nucleus accumbens shell blocks partner preference.319 (B) Female prairie voles that spend 6 h with a partner, without mating, do not form a partner preference under control conditions (cerebrospinal fluid (CSF) infused into the NAcc shell). However, microinjection of a D2 agonist (D2-ago) induces the formation of a pair bond during this 6-h cohabitation, an effect that is blocked by coinfusion of a D2 antagonist (D2-antag). An OT antagonist (OTA) also blocks D2 agonist-induced partner preference, suggesting that concurrent activation of D2R and OTR is necessary for pair bonding. Asterisks indicate statistically significant differences (p < 0.05) in the time spent with partner versus stranger. Source: Adapted from Ref. 277.
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21. FIGURE Mu-opioid receptor (muOR) regulation of partner preference formation. Receptor autoradiography showing muOR ligand binding in the prairie vole striatum. muOR density in the nucleus accumbens shell (NAcc) is moderate, but much lower, than muOR density in the caudate putamen (CP). The bar graph illustrates the effects of infusion of a muOR antagonist (CTAP) or vehicle into the NAcc or CP of female prairie voles prior to 24-h cohabitation with a male partner with mating. Females receiving vehicle to the NAC shell or CP formed pair bonds as normal. muOR antagonist injected into the NAcc shell did not affect pair bonding, while muOR antagonist in the CP prevented the formation of a pair bond. These data show that muOR in the CP is necessary for pair bond formation in female prairie voles. Similar experiments have not been performed in males. Asterisks indicate statistically significant differences (p < 0.05) in the time spent with partner versus stranger. Source: Adapted from Ref. 329.
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22. FIGURE A schematic of the proposed neural circuitry of pair bond formation in prairie voles. This figure is reproduced in color in the color plate section. Mating stimulates the release of oxytocin from neurons in the paraventricular nucleus of the hypothalamus (PVN) into the nucleus accumbens (NAcc) and prefrontal cortex (PFC) in females, and the release of vasopressin from neurons in the medial amygdala (MeA) into the ventral pallidum (VP) and lateral septum (LS) in males. Mating also stimulates the release of dopamine from neurons in the ventral tegmental area (VTA) into the NAcc and PFC. The MeA receives olfactory input from the partner and conveys the neural encoding of the olfactory signature of the partner to the striatum and LS. Mu-opioid receptors in the CP stimulate the rewarding aspects of mating. OT and AVP facilitate the processing of the olfactory signatures of the mate, and dopamine facilitates an association between the neural encoding of the social cues of the partner and the opioid-based reward and reinforcement. The actions of these neurochemicals in these circuits lead to a conditioned partner preference. Source: Adapted from Refs 271,334.
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23. FIGURE Loss of a partner leads to an increase in passive coping strategy in male prairie voles. (A) Following 4 days of separation from the bonded partner, males display more time floating (e.g., not actively swimming to escape) in the forced swim test than males who remained paired with their partner, or who were not pair bonded, cohabitated with a same sex sibling, and then separated from their sibling. fp = female partner, sp = sibling partner (B) Males also display an increased plasma concentration of corticosterone when separated from their bonded partner. (C) CRF mRNA expression in the bed nucleus of the stria terminalis is elevated in pair bonded animals compared to nonbonded males. (D) ICV infusion of either a CRF-R1 or CRF-R2 receptor antagonist during the separation period blocks the passive coping strategy in the forced swim test. Source: Adapted from Ref. 344.
© 2015, Elsevier, Inc., Plant and Zeleznik, Knobil and Neill's Physiology of Reproduction, Fourth Edition