Rapid steroid influences on visually guided sexual behavior in male goldfish

The ability of steroid hormones to rapidly influence cell physiology through nongenomic mechanisms raises the possibility that these molecules may play a role in the dynamic regulation of social behavior, particularly in species in which social stimuli can rapidly influence circulating steroid levels. We therefore tested if testosterone (T), which increases in male goldfish in response to sexual stimuli, can rapidly influence approach responses towards females. Injections of T stimulated approach responses towards the visual cues of females 30–45 min after the injection but did not stimulate approach responses towards stimulus males or affect general activity, indicating that the effect is stimulus-specific and not a secondary consequence of increased arousal. Estradiol produced the same effect 30–45 min and even 10–25 min after administration, and treatment with the aromatase inhibitor fadrozole blocked exogenous T's behavioral effect, indicating that T's rapid stimulation of visual approach responses depends on aromatization. We suggest that T surges induced by sexual stimuli, including preovulatory pheromones, rapidly prime males to mate by increasing sensitivity within visual pathways that guide approach responses towards females and/or by increasing the motivation to approach potential mates through actions within traditional limbic circuits.     

Visual sex discrimination in goldfish: seasonal, sexual, and androgenic influences

The olfactory signals used by goldfish for sexual and aggressive communication have been studied extensively, but little work has addressed the role of other sensory modalities in social communication in this species. We therefore investigated the role that visual stimuli play in sex discrimination and the ability of androgens, which masculinize courtship behavior, to affect behavioral responses toward female visual stimuli. We found that males selectively orient toward female visual stimuli during the breeding season but not outside it, whereas prostaglandin F2-alpha (PGF2alpha)-injected females do not differentially approach male and female visual stimuli, even during the breeding season. Implanting adult females with testosterone (T) and 11-ketotestosterone (KT), however, induced orientation responses toward female visual stimuli similar to those observed in males. These results indicate that visual sexual stimuli are likely important for reproductive signaling in goldfish, potentially helping males identify ovulating females from a distance in a shoal of fish, and that androgens can influence mechanisms associated with orientation responses toward such stimuli.     

The effects of sex steroids and vasotocin on behavioral responses to visual and olfactory sexual stimuli in ovariectomized female roughskin newts

Previous studies have found that vasotocin (AVT) administration to male roughskin newts (Taricha granulosa) enhances courtship clasping as well as appetitive responses to specific sexual stimuli and that treating female newts with androgens plus AVT induces the expression of male-typical courtship clasping (the selective clasping of females). However, the unique and/or interactive effects of sex steroids and AVT on appetitive responses to specific sexual stimuli have not yet been determined. To first identify male-typical, sexually dimorphic appetitive responses to female sexual stimuli, we tested intact newts during the breeding season and found that males, but not females, are attracted to female visual and pheromonal sexual stimuli. We then used ovariectomized (ovx) females implanted with empty silastic capsules (Blk) or with capsules containing testosterone (T), dihydrotestosterone (DHT), or estradiol (E2) and then injected with either saline or AVT to determine the effects of steroids and AVT, alone or in combination with each other, on male-typical behavioral responses to those stimuli. E2 treatment depressed responses toward female visual stimuli independently of AVT. On the other hand, only T-implanted, AVT-injected females displayed male-typical behavioral responses toward female olfactory stimuli, preferring to spend more time in proximity to female-scented than unscented newt models and selectively clasping the female-scented models. Together, these results support the conclusion that sex steroids and AVT influence behavioral responses to sexual stimuli via sensory-specific mechanisms. Furthermore, they suggest that T and AVT interact within the brain to influence sensorimotor processing in the pathways that integrate olfactory sexual stimuli into male-typical courtship behaviors.     

Effects of social experience on subsequent sexual performance in naïve male Japanese quail (Coturnix japonica)

On their first sexual encounter, naïve male Japanese quail will attend to and approach a female; they sometimes mount but they do not always copulate. During the second encounter, most males successfully copulate. Although sexual experience facilitates subsequent sexual interactions, sensory cues provided by females, independent of any sexual encounter, may also enhance sexual performance. To investigate whether previous exposure to a conspecific affects subsequent sexual behavior, we allowed inexperienced males to observe an empty box, or a conspecific consisting of either an experienced female or male for 2.5 min/day on 7 days. Measures of appetitive sexual behavior were recorded during these tests. On day 8, subjects were allowed to copulate with a novel female for 5 min. On the following days, all subjects were repeatedly provided with visual access to a female and allowed to mate. In the pre-copulatory trials males initially exhibited a high frequency of appetitive responses that dissipated with repetition. Pre-copulatory experience also significantly affected motivation to mate with subjects exposed to females copulating more quickly than other subjects. Post-copulatory appetitive behavior also differed between groups: control subjects showed the highest behavioral frequency followed by males exposed to females and finally males exposed to males. These data indicate that pre-copulatory social experience profoundly influences subsequent sexual behavior and probably reproductive success. This experience effect is independent of any hormonal effect (such as one resulting from changes in secretion following different social interactions) given that the subjects were castrates chronically treated with testosterone.     

Relationship between testosterone and interest in sexual stimuli: the effect of experience

Testosterone is commonly thought to drive male sexual interest, but little experimental evidence demonstrates a direct relationship between natural variation in testosterone and sexual interest in healthy young men. This study measured young men's testosterone levels and their interest in visual sexual stimuli across three test sessions within 1 month. Fifteen men aged 23–28 viewed pictures of couples engaged in sexually explicit activity. Each session included a unique set of 72 pictures depicting heterosexual oral sex or intercourse presented in randomized order. Participants controlled how long they viewed each picture, with viewing time indicating sexual interest. Men's testosterone (T) levels were assayed from blood spots obtained prior to viewing the pictures. Overall, T and viewing time were positively correlated; however, the strength of this relationship varied by test session. T was marginally correlated with viewing time during the first session (r = 0.43) and not significantly correlated with viewing time on the second session (r = 0.16). During the final test session, when habituation might influence male interest in the stimuli, T was strongly correlated with viewing time (r = 0.80). Thus, the current study demonstrates a direct but context dependent relationship between testosterone and sexual interest in healthy young males.     

Fecal estradiol-17β and testosterone in prepubertal domestic cats

The aim of this article was to describe the time course of prepubertal sexual steroids in domestic cats. Fourteen newborn kittens were followed up until puberty (physical, behavioral, and hormonal changes). Fecal testosterone [T; males] and E estradiol 17-β [E2; females] concentrations were analyzed by repeated measures ANOVA and two consecutive time windows (TWs) were used to compare changes in both male (postnatal weeks 1–4 vs. 5–14) and females (postnatal weeks 1–5 vs. 6–13). Puberty was achieved 14.3 ± 0.3 and 13.3 ± 0.4 weeks after birth in male and female cats, respectively. In both genders, during TW-1 fecal steroids concentrations were similar (males) or even higher (females) to that previously described for mature cats. Fecal T (P < 0.01) and E2 (P < 0.01) varied throughout the weeks. Differences were found when hormonal concentrations of TW-1 were compared with those of TW-2 both for male (61.4 ± 7.9 vs. 16.9 ± 2.2 ng/g; P < 0.01) and female (78.2 ± 12.5 vs. 11.2 ± 4.0 ng/g; P < 0.01) cats. It is concluded that in domestic cats there is a sexual steroid surge during the first 4 and 5 postnatal weeks in male and female animals, respectively.     

The effect of female presence on spermiation, and of male sexual activity on ‘ready’ sperm in the male guppy

This study examines the effect of female presence on the amount of ‘strippable’ sperm, and the relationship between male sexual activity and the amount of ‘ready’ sperm in the male guppy Poecilia reticulata. The amount of strippable sperm was greater in males paired for one week with females than in isolated males. We separated these ‘paired’ males from females by a clear partition and thus exposed males to visual and possibly olfactory stimuli. In the second experiment, control males spent more time attending females and performed more sexual acts during a 15-min test period than males previously stripped of spermatophores. These results indicate that females play an important role in stimulating sperm availability in males and that the amount of ready sperm influences male sexual behaviour. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Tribolium confusum responses to blends of cereal kernels and plant volatiles

In this study, we report on the behavioural responses of the Tribolium confusum to 6 blends of cereal volatiles. There were tested four doses (1 ng/min, 10 ng/min, 100 ng/min and 1000 ng/min in 50 μl of hexane applied on filter paper). A Y‐tube experiment revealed that T. confusum females and males were attracted to the blend 1, 4 and 5 at the concentrations between 1 and 10 ng/min. Confused T. confusum females and males were not attracted to any concentration of blend 2 and 3. Yet the beetle females and males were repelled by the highest concentrations (1000 ng/min) for all the blends tested and also by the concentration 100 ng/min of all the blends tested, except for blend 1 and 4. Females and males were also repelled by the three blend 6 concentrations tested (10, 100 and 1000 ng/min).     

Male mice ultrasonic vocalizations enhance female sexual approach and hypothalamic kisspeptin neuron activity

Vocal communication in animals is important for ensuring reproductive success. Male mice emit song-like “ultrasonic vocalizations (USVs)” when they encounter female mice, and females show approach to the USVs. However, it is unclear whether USVs of male mice trigger female behavioral and endocrine responses in reproduction. In this study, we first investigated the relationship between the number of deliveries in breeding pairs for 4 months and USVs syllables emitted from those paired males during 3 min of sexual encounter with unfamiliar female mice. There was a positive correlation between these two indices, which suggests that breeding pairs in which males could emit USVs more frequently had more offspring. Further, we examined the effect of USVs of male mice on female sexual behavior. Female mice showed more approach behavior towards vocalizing males than devocalized males. Finally, to determine whether USVs of male mice could activate the neural system governing reproductive function in female mice, the activation of kisspeptin neurons, key neurons to drive gonadotropin-releasing hormone neurons in the hypothalamus, was examined using dual-label immunocytochemistry with cAMP response element-binding protein phosphorylation (pCREB). In the arcuate nucleus (Arc), the number of kisspeptin neurons expressing pCREB significantly increased after exposure to USVs of male as compared with noise exposure group. In conclusion, our results suggest that USVs of male mice promote fertility in female mice by activating both their approaching behavior and central kisspeptin neurons.     

Responses to computer-generated visual stimuli by the male praying mantis, Sphodromantis lineola (Burmeister)

We tested male mantis' responses to square, computer-generated visual stimuli of various sizes to determine the stimulus parameters that affect their striking behaviour. Males in a high-hunger group displayed a sharp preference for solid black 12×12-degree squares moving linearly against a white background, especially when the squares moved downward (versus horizontally). Males in a low-hunger group visually tracked but, with rare exception, did not strike at any linearly moving squares. In contrast, when solid black squares moved erratically around visual field centre, males struck regularly at them irrespective of hunger level, even when the squares were as large as 47×47 degrees. Males also recognized black-and-white Julesz-patterned square stimuli moving against a similarly patterned background, indicating that they recognized the synchronous movement of a group of stimulus elements as a single moving object. Finally, we compared allometric and life history data between male and females S. lineola to elucidate the possible reasons for the differences between male response patterns and previously published data on females. These comparisons suggest that males employ a different behavioural strategy than do females when faced with large, erratically moving visual stimuli.     

Physical provocation of pubertal anabolic androgenic steroid exposed male rats elicits aggression towards females

Human studies suggest that anabolic androgenic steroid (AAS) users are aggressive towards women. This study used a rat model to evaluate whether AAS potentiated aggression towards females and the conditions under which this occurs. Gonadally intact pubertal male rats received one of the following AAS treatments (5 mg/kg s.c. 5 days/week for nine weeks): testosterone (T), stanozolol (S), testosterone + stanozolol (T + S), or vehicle control. Each rat was tested with 3 conspecific stimuli: ovariectomized females (OVX), estrogen only females (E), and estrogen + progesterone females (E + P). The response to physical provocation was tested under three conditions: without physical provocation, provocation of the experimental male, and provocation of the conspecific female. Provocation was a mild tail pinch. Both aggressive and sexual behaviors were measured during each test. In the absence of physical provocation, AAS males were not aggressive towards females. However, provocation significantly increased aggression in males treated with testosterone but only towards OVX females. In the presence of E or E + P females, all animals displayed sex behavior, not aggression. Thus, factors such as the nature of the AAS and the hormonal status of the females are important in determining whether male rats will be aggressive towards females. However, the most salient factor determining aggression towards females is the presence of provocation in combination with high levels of testosterone.     

Male Calling Behavior and Female Choice in the Neotropical Treefrog Hyla microcephala

The effect of stimulus call complexity and calling rate on the vocal responses of males and female mate choice was studied in Hyla microcephala in Panama. Males increased the number of notes in their calls in response to increases in stimulus call complexity during both playback of 1 to 8-note advertisement calls and during natural interactions. However, precise matching of the number of notes in stimuli and responses did not occur consistently. Males also increased calling rates if stimuli were presented above prestimulus rates. Two-stimulus choice experiments demonstrated that females prefer both higher calling rates and greater call complexity, indicating that the ways males change their vocal behavior during interactions increases their attractiveness to potential mates. Tests in which the relative intensity of a high and low rate stimulus was varied indicated that females prefer stimuli with higher total sound energy. In a natural chorus, it is likely that females simply approach males giving the most conspicuous calls.     

Hormone–behavior associations in early infancy

The physiological significance of hormonal changes in early postnatal life is emerging, but the behavioral significance in humans is unknown. As a first test of the relationship between hormones and behavior in early infancy we measured digit ratios and salivary hormone levels in forty-one male and female infants (3–4 months of age) who watched a video depicting stimuli differentially preferred by older males and females (toys, groups). An eye-tracker measured visual fixations and looking times. In female infants, hormones were unrelated to visual preferences. In male infants, higher androgen levels predicted stronger preferences for male-typical stimuli. These data provide the first evidence for a role for hormones in emerging sex-linked behavior in early development.     

Attenuation of the neuronal stress responsiveness and corticotrophin releasing hormone synthesis after sexual activity in male rats

Beneficial effects of sexual activity and mating on the responsiveness to environmental stress can be observed in humans and other mammalian species alike, but the underlying neurobiological mechanisms are largely unknown. Sexual activity and mating with a receptive female has recently been shown to reduce the subsequent emotional stress response via activation of the brain oxytocin system. Therefore, we investigated the neuronal and hormonal responses to an acute stressor (forced swimming) after mating in male rats.Attenuation of the stress-induced increase of c-fos and CRH mRNA expression within the hypothalamic paraventricular nucleus 4 h after mating revealed that sexual activity reduced neuronal reactivity in this region. However, this effect was independent of oxytocin as oxytocin receptor blockade, by central administration of an oxytocin receptor antagonist, after mating did not prevent the reduced expression of c-fos mRNA in response to stressor exposure. Mating itself stimulated corticotrophin (ACTH) and corticosterone secretion, which was absent in males after contact with an unreceptive female (non-mated group). However, ACTH and corticosterone responses to forced swimming applied either 45 min or 4 h after female contact were similar between mated and non-mated males. These findings provide evidence for a stress-protective effect of sexual activity and mating in male rats and for dissociation between neuronal and neuroendocrine stress responses.     

Adult female hamsters require long and sustained exposures to heterospecific males to avoid interspecific mating

Interspecific mating normally decreases female fitness. In many species, females avoid heterospecific males innately or by imprinting on their parents. Alternatively, adult females could learn to discriminate against heterospecific males after exposure to such males. For example, Syrian hamster (Mesocricetus auratus) females learn to discriminate between conspecific males and Turkish hamster (M. brandti) males during adulthood by exposure to males of both species. Adult females not previously exposed to Turkish hamster males will mate similarly with conspecific and heterospecific males. However, in a previous study we showed that exposure to a heterospecific male and a conspecific male for 8 days led to mating avoidance and aggression towards the heterospecific male. Here we conducted two experiments to investigate how much exposure to the heterospecific male was required for females to avoid mating with the heterospecific male (Experiment 1) and how long that avoidance lasted in the absence of continuous exposure to heterospecific stimuli (Experiment 2). Fast and durable learning would indicate the evolution of an efficient avoidance response. In Experiment 1, females were exposed to a heterospecific male for 1, 4 h, 4 or 8 days and then paired with that male. We found more avoidance of interspecific mating after 4 or 8 days of exposure than after 1 or 4 h of exposure. In Experiment 2, females were exposed to a heterospecific male for 8 days and then paired with that male either 10 min later or 8 days later. We found that after an 8-day delay females were highly sexually receptive to the heterospecific male. Additionally, a comparison between the current experiments and a previous study indicates that female Syrian hamsters do not require concurrent exposure to a conspecific male and a heterospecific male to learn to avoid interspecific mating; exposure to a heterospecific male is sufficient.     

Non-ovarian aromatization is required to activate female sexual motivation in testosterone-treated ovariectomized quail

Although aromatase is expressed in both male and female brains, its functional significance in females remains poorly understood. In female quail, sexual receptivity is activated by estrogens. However it is not known whether sexual motivation is similarly estrogen-dependent and whether estrogens locally produced in the brain contribute to these behavioral responses. Four main experiments were designed to address these questions. In Experiment 1 chronic treatment of females with the anti-estrogen tamoxifen decreased their receptivity, confirming that this response is under the control of estrogens. In Experiment 2 chronic treatment with tamoxifen significantly decreased sexual motivation as treated females no longer approached a sexual partner. In Experiment 3 (a) ovariectomy (OVX) induced a significant decrease of time spent near the male and a significantly decreased receptivity compared to gonadally intact females, (b) treatment with testosterone (OVX + T) partially restored these responses and (c) this effect of T was prevented when estradiol synthesis was inhibited by the potent aromatase inhibitor Vorozole (OVX + T + VOR). Serum estradiol concentration was significantly higher in OVX + T than in OVX or OVX + T + VOR females. Together these data demonstrate that treatment of OVX females with T increases sexual motivation and that these effects are mediated at least in part by non-gonadal aromatization of the androgen. Finally, assays of aromatase activity on brain and peripheral tissues (Experiment 4) strongly suggest that brain aromatization contributes to behavioral effects observed here following T treatment but alternative sources of estrogens (e.g. liver) should also be considered.     

Women's genital sexual arousal to oral versus penetrative heterosexual sex varies with menstrual cycle phase at first exposure

Reproductive-aged women show increased interest in sexual activity during the fertile phase of the menstrual cycle that can motivate sexual behavior and thereby increase the likelihood of conception. We examined whether women demonstrated greater sexual responses (subjective and genital sexual arousal) to penetrative versus oral sexual activities during the fertile versus non-fertile phases of their cycles, and whether women's arousal responses were influenced by the phase during which they were first exposed to these sexual stimuli (e.g., Slob et al., 1991; Wallen and Rupp, 2010). Twenty-two androphilic women completed two identical sexual arousal assessments in which genital responses were measured with a vaginal photoplethysmograph and their feelings of sexual arousal were recorded. Women viewed an array of 90 s films varying by couple type (female–female, male–male, female–male) and sexual activity type (oral or penetrative), during the fertile (follicular) and non-fertile (luteal) phases of their menstrual cycle, with the order of cycle phase at the first testing session counter-balanced. Women tested first in the fertile phase showed significantly greater genital arousal to female–male penetrative versus oral sex in both testing sessions, whereas self-reports of sexual arousal were not affected by cycle phase or testing order. These results contribute to a growing body of research suggesting that fertility status at first exposure to sexual stimuli has a significant effect on subsequent sexual responses to sexual stimuli, and that this effect may differ for subjective versus genital sexual arousal.     

The sexual preference of female rats is influenced by males' adolescent social stress history and social status

Ongoing development of brain systems for social behaviour renders these systems susceptible to the influence of stressors in adolescence. We previously found that adult male rats that underwent social instability stress (SS) in mid-adolescence had decreased sexual performance compared with control males (CTL). Here, we test the hypotheses that SS in adolescence decreases the “attractiveness” of male rats as sexual partners compared with CTL rats and that dominance status is a protective factor against the effects of SS. The main prediction was that females would spend more time with CTL males than SS males, and that this bias would be greater for submissive than for dominant rats. Among dominant pairs (n = 16), females preferred SS males, spending more time with and visiting more often SS than CTL males (each pair tested 5 ×), and SS males had shorter latencies to ejaculation, shorter inter-ejaculation intervals, and made more ejaculations compared with CTL males. Among submissive pairs (n = 16), females spent more time with, visited more often, and displayed more paracopulatory behaviour with CTL than with SS males, and differences in sexual performance between SS and CTL males were modest and in the opposite direction from that in dominant pairs. The heightened motivation of SS males relative to CTL males for natural rewards may have attenuated differences in sexual performance in a paced mating context. In sum, the experience of stress in adolescence leads to long-lasting changes in males that are perceptible to females, are moderated by social status, and influence sexual behaviour.     

Does Female Personality Determine Mate Choice Through Sexual Cannibalism?

Animal personalities (e.g. consistent across‐context behavioural differences between individuals) can lead to differences in mate choice. However, evidence for this link remains limited. Pre‐mating sexual cannibalism can be a behavioural syndrome (i.e. a suboptimal personality) in which adaptive female aggression towards heterospecific prey spills over on non‐adaptive aggression towards courting males, independently of the female mating or feeding status (i.e. the ‘aggressive spillover hypothesis’, ASH). On the other hand, sexual cannibalism can also be a form of mate choice by which females selectively kill or mate with males depending on the male phenotype. We introduce the hypothesis that the most aggressive females in the population will not only attack males more frequently, but will be less likely to impose sexual selection on males through sexual cannibalism. Assuming that in a field common garden experiment in which females were fed ad libitum the rate of weight gain by a female may reflect her voracity or aggressiveness, we show that in the cannibalistic burrowing wolf spider Lycosa hispanica (formerly L. tarantula), voracity towards heterospecific prey predicts a female's tendency towards sexual cannibalism. Unmated females with higher weight gains were more cannibalistic and attacked males regardless of the male phenotype. On the other hand, females that were less voracious tended to be less cannibalistic, and when they did kill a male, they were selective, killing males in poorer condition and mating with those in better condition. Our results demonstrate that females with different phenotypes (growth rates) differently imposed selection on male condition, tentatively supporting the hypothesis that female aggression levels can spill over on sexual selection through sexual cannibalism.     

Factors influencing aggression toward females by male rats exposed to anabolic androgenic steroids during puberty

Previous results showed that male rats pubertally exposed to anabolic androgenic steroids (AAS) displayed aggression towards females in response to physical provocation. This experiment examined two factors that may modulate AAS-induced behavior towards females: olfactory cues and frustration. Gonadally intact males began one of three AAS treatments at puberty (D40): testosterone propionate (T), stanozolol (S), T+S, or vehicle control. To test for the relevance of olfactory cues in the elicitation of behavior toward females, a hidden neighbor paradigm was used. The proximal stimulus was an ovariectomized (OVX) female, estrogen plus progesterone (E+P) female, or an E+P female with tape-obstructed vagina (OBS). Distal olfactory cues from a hidden neighbor were delivered from a separate cage connected to the testing arena. The vaginally obstructed, sexually receptive female (OBS) was used to determine the effects of frustration on behavior by AAS males. Both sexual and aggressive behaviors were measured. The presence of distal olfactory cues had no effect on either sexual or aggressive behavior. In the presence of E+P and OBS females, all males displayed sex behaviors, not aggression. However, AAS males displayed significantly more aggression towards proximal OVX females than controls. AAS males mounted OBS females significantly more than controls, indicating a persistence of once rewarded behavior. These results suggest (1) proximal cues of the conspecific female are more salient than distal olfactory cues in determining behavior and (2) AAS males display frustration-induced persistence in response to vaginally obstructed receptive females.