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A Drosophila protein specific to pheromone-sensing gustatory hairs delays males' copulation attempts.

In insects, increasing evidence suggests that small secreted pheromone binding proteins (PBPs) and odorant binding proteins (OBPs) are important for normal olfactory detection of airborne pheromones and odorants far from their source. In contrast, it is unknown whether extracellular ligand binding proteins participate in perception of less volatile chemicals, including many pheromones, that are detected by direct contact with chemosensory organs. CheB42a, a small Drosophila melanogaster protein unrelated to known PBPs or OBPs, is expressed and likely secreted in only a small subset of gustatory sensilla on males' front legs, the site of gustatory perception of contact pheromones. Here we show that CheB42a is expressed specifically in the sheath cells surrounding the taste neurons expressing Gr68a, a putative gustatory pheromone receptor for female cuticular hydrocarbons that stimulate male courtship. Surprisingly, however, CheB42a mutant males attempt to copulate with females earlier and more frequently than control males. Furthermore, CheB42a mutant males also attempt to copulate more frequently with other males that secrete female-specific cuticular hydrocarbon pheromones, but not with females lacking cuticular hydrocarbons. Together, these data indicate that CheB42a is required for a normal gustatory response to female cuticular hydrocarbon pheromones that modulate male courtship.

Animals↗

Sexual incentive motivation, olfactory preference, and activation of the vomeronasal projection pathway by sexually relevant cues in non-copulating and naive male rats.

There are some apparently healthy male rats that fail to mate after repeated testing with receptive females. We have previously shown that these "non-copulator (NC)" males show no partner preference for a receptive female when given the opportunity to physically interact with a sexually receptive female or a sexually active male. We also demonstrated that although NC males prefer odors from estrous females to odors from anestrous females, this preference is significantly reduced in comparison to the preference displayed by copulating (C) males. The aim of the present study was to evaluate in NC males sexual incentive motivation, that is, the approach behavior of male rats to either a sexually receptive female or a sexually active male in a test where the subjects can smell, hear, and see the stimulus animal but prevents their physical interaction. In addition, we determined whether NC rats have alterations in their ability to detect odors from conspecifics or odors related to food. In the detection of odors from conspecifics, we determined if these NC males are sexually attracted toward odors from receptive females or sexually active males. For food-related odors, we quantified the time it took the subjects to locate a hidden a piece of apple. Finally, using the induction of Fos-immunoreactivity (Fos-IR) as an index of neuronal activation, we compared the response of the vomeronasal projection pathway (VN pathway) of C and NC male rats exposed to estrous bedding. Males without sexual experience (WSE) were included in all experiments to determine the importance of previous heterosexual experience in the different behavioral tests and in the activity of the VN pathway. In the sexual incentive motivation test, we found that C and WSE male rats have a clear preference for estrous females over sexually active males, whereas NC male rats showed no preference. In odor tests, our results showed that C males had a clear preference for odors from estrous females as opposed to odors from sexually active males. Although NC and WSE male rats showed a preference for estrous female odors, this preference was significantly reduced compared to that shown by C males. No differences were found between WSE, C, and NC males in the detection of stimuli associated with food-related odors. A significant increase in Fos-IR was observed in the mitral cell layer of the accessory olfactory bulb in all groups when exposed to estrous bedding. However, only the C male rats exposed to estrous female bedding showed an increase Fos-IR in all structures of the VN pathway. An increase in Fos-IR was observed in the medial preoptic area (MPOA) of WSE males exposed to estrous bedding. No increases in Fos-IR were detected along the VN pathway in NC male rats. We proposed that NC male rats do not display sexual behavior due to a reduced sexual motivation that could be caused by alterations in the neuronal activity of the VN pathway during the processing of estrous odors.

Animals↗

Effects of testosterone metabolites on copulation, medial preoptic dopamine, and NOS-immunoreactivity in castrated male rats.

The medial preoptic area (MPOA) is an important integrative site for male sexual behavior. Dopamine (DA) is released in the MPOA of male rats shortly before and during copulation. In a previous study, we identified 17beta-estradiol (E(2)) as the metabolite of testosterone (T) that maintains MPOA basal extracellular DA levels. However, the presence of dihydrotestosterone (DHT), an androgenic metabolite of T, is required for the female-induced increase in MPOA DA observed during copulation. Recently, we reported that assays of MPOA tissue DA content showed that castrates actually had more stored DA than did gonadally intact males. Therefore, the reduction in extracellular levels in castrates was not due to decreased availability of DA; most likely it was due to decreased release. Furthermore, T upregulates neuronal nitric oxide synthase (nNOS) in the MPOA. NO has been implicated in the regulation of DA release in the MPOA. It is not known, however, which metabolite(s) of T regulate(s) tissue stores of DA and/or nNOS in the MPOA of male rats. The present experiments were designed to test the following: (1) whether E(2), DHT, or the combination of the two influences MPOA DA tissue levels, an indication of stored DA, in male rat castrates; and (2) whether E(2), DHT, or the combination of the two influences NOS-ir in the MPOA of castrated male rats. The results indicate that E(2) up-regulates nNOS-ir in the MPOA and maintains tissue content of DA at levels similar to those in T-treated rats. DHT did not influence nNOS-ir, while attenuating the effect of castration on tissue DA content.

Analysis of Variance↗

40- and 70-kHz vocalizations of mice (Mus musculus) during copulation.

Ultrasonic vocalizations were tape recorded from five pairs of copulating mice and subjected to spectrographic analysis. As expected, the mice emitted numerous 70-kHz vocalizations. At the beginning of the test, before copulation began, 70-kHz calls were emitted almost continuously, while calls with lower spectrographic frequencies were not observed. Subsequently, bursts of 70-kHz calling generally began shortly before mounts and intromissions and persisted until dismount. Intermixed with these 70-kHz calls were additional vocalizations of about 40 kHz. Calling rates were highest just prior to intromission. Once intromissions began, 70-kHz calls continued at a lower rate until dismount; however, 40-kHz calls occurred infrequently. In a second experiment, the male was found to emit the majority of the 70-kHz calls and all of the 40-kHz calls. When the male was devocalized, few calls were detected, regardless of whether the female was able to call. If the male was not devocalized, high rates of calling were detected, even if the female was devocalized.

Animals↗

A comparative study of rodent ultrasonic vocalizations during copulation.

The temporal patterning of ultrasonic vocalizations (USVs) during copulation was recorded for male-female pairs of Djungarian hamsters (Phodopus campbelli), prairie voles (Microtus ochrogaster), and montane voles (Microtus montanus). Each species appears to utilize a single major frequency band for USVs, centered around 31 kHz for the vole species and 71 kHz for hamsters. Djungarian hamsters exhibited low rates of USVs prior to introduction of the female and following ejaculation, but a high USV rate during periods of copulatory activity. Both vole species called at high rates during all stages of the copulatory sequence, although calling rates decreased following ejaculation. Anesthetization trials, where one pair member was awake and the other anesthesized, suggest that it is the male of each species that produces most USVs. The results were compared with six other muroid species for which data on the temporal patterning of USVs during copulation are available. These data extend our knowledge of the patterning of USVs during copulatory behavior and suggest the need for additional comparative investigations.

Animals↗

Hippocampal electrical activity in the female rat: the estrous cycle, copulation, parturition, and pup retrieval.

Hippocampal electrical activity was examined in female rats across the four phases of the estrous cycle, as well as during copulation, parturition, and pup retrieval. Possible hormonal effects on hippocampal activity were examined by recording daily during struggling and immobility throughout five estrous cycles. No differences in the characteristics of rhythmical slow activity (RSA), large-amplitude irregular activity (LIA), or their relation to behavior were found between the phases of the estrous cycle. Behaviors examined during copulation were lordosis, hopping, and ear wiggling. Lordosis and ear wiggling were both accompanied by irregular waves, with some low frequency RSA also present during lordosis. Hopping was accompanied by RSA which was greater in amplitude and frequency than RSA during walking. Parturition behaviors examined included body extensions, genital or pup licking, and 'body flattening'. Body extensions were found to be associated with irregular hippocampal activity, and appeared to be a Type 2 behavior. Interestingly, sudden suppressions of the hippocampal record lasting 1-5 s often preceded body extensions. Irregular hippocampal activity was present at all times during genital and pup licking. Body flattening was typically accompanied by very high amplitude irregular waves which, although the rats were awake, resembled a sleeping hippocampal pattern. Pup retrieval involved walking and was thus always accompanied by RSA.

Animals↗

Copulation-illness associations in male rats: lithium chloride dose and delay manipulations.

Male rats that receive an injection of lithium chloride (LiCl) after each pairing with an estrous female gradually decrease their copulatory behaviors. In the present experiments we demonstrated that a 6.0 mEq/kg (0.3 M, 20 ml/kg) dose of LiCl injected after trials spaced twice weekly at 3-4-day intervals induced more rapid acquisition of copulation-illness associations than a 3.0 mEq/kg (0.15 M, 20 ml/kg) dose. Contingent 0.3 M saline or noncontingent 0.3 M LiCl injections did not affect copulatory behaviors. The location of the male rat (home cage or test chamber) during a portion of the aversive state induced by LiCl did not influence rate of acquisition. Copulation-illness associations, once established, were retained over a 60-day interval. Comparable decrements in copulatory behaviors were evident when LiCl was injected at 1-, 5-, or 15-min intervals after pairings with estrous females when the males were detained in the test chambers during the delay intervals; decrements were not observed when the interval was increased to 30 or 60 min. An electric shock analog to the aversive state induced by LiCl did not induce decrements in copulatory behaviors. It was suggested that odor-illness associations may, in part, account for the decrements in copulatory behaviors in this paradigm.

Animals↗

Can male decorticate rats copulate?

Sexually experienced or naive male rats, subjected to neocortex removal or neocortex plus hippocampus removal, were paired with female rats for up to 180 days and compared with control rats with respect to success and latency to impregnate the female. All of the control rats and half of the brain-damaged rats successfully impregnated female rats at least once. Success was not correlated with lesion type or presurgical experience. The brain-damaged rats took longer to impregnate the females than control rats. Since the ablations were extensive, more than 95% of the neocortex in many rats, the study shows that decorticate rats can copulate. Presumably the intact subcortical structures are sufficient for male copulation, but cortical structures in some way facilitate rapid female impregnation.

Animals↗

Suppression of precocial copulation by progesterone implants in the male chick forebrain.

Precocial copulation in 2-wk.-old male chicks, described behaviorally as free mount, tread, posterior contact, waggle, peek, and seize, was developed through hand-training experience and androgen treatment. Crystalline progesterone was then implanted in various forebrain or midbrain regions. Results indicated that progesterone inhibited copulatory behavior when placed in the periventricular areas of the preoptic-hypothalamic continuum. Progesterone implants in the preoptic lateral forebrain bundle regions also suppressed precocial copulation. Forebrain implants of cholesterol did not result in copulatory inhibition. The suppression of copulatory behavior was not accompanied by loss of weight or deficits in general activity or comb growth. These data indicate that brain regions responsible for progesterone-induced copulatory inhibition are similar in neuroanatomical distribution to those involved in testosterone-induced copulatory activation.

Age Factors↗

The septum: neural systems involved in eating, drinking, irritability, nuricide, copulation, and activity in rats.

Eating, drinking, irritability, muricide, and copulation were measured in 45 male rats before and after one of three coronal knife cuts in the septal region or a control operation; in addition, activity was measured postoperatively. (a) Cuts posteroventral to the septum resulted in slight hypophagia, marked hyperdipsia, irritability, asexuality, and decrease in activity. (b) Cuts of the fornix resulted only in slight decrease in activity. (c) Cuts through the anterior septum resulted in irritability, slight hyposexuality, and slight decrease in activity. No significant correlations between the various behavioral effects were found. It was suggested that the neural pathways mediating eating, drinking, irritability, muricide, copulation, and activity are relatively distinct and that neural activity in the septal region probably does not influence behavior in any unitary fashion.

Aggression↗

Female bluethroats enhance offspring immunocompetence through extra-pair copulations.

Female birds frequently copulate with extra-pair males, but the adaptive value of this behaviour is poorly understood. Some studies have suggested that 'good genes' may be involved, where females seek to have their eggs fertilized by high-quality males without receiving any material benefits from them. Nevertheless, it remains to be shown that a genetic benefit is passed on to offspring. Here we report that nestling bluethroats, Luscinia svecica, sired by extra-pair males had a higher T-cell-mediated immune response than their maternal half-siblings raised in the same nest. The difference could not be attributed to nestling body mass, sex or hatching order, but may be an effect of paternal genotype. Extra-pair young were also more immunocompetent than their paternal half-sibs raised in the genetic father's own nest, which indicates an additional effect of maternal genotype. Our results are consistent with the idea that females engage in extra-pair copulations to obtain compatible viability genes, rather than 'good genes' per se.

Animals↗

Morphine injected into the paraventricular nucleus of the hypothalamus prevents noncontact penile erections and impairs copulation: involvement of nitric oxide.

Male rats show four to six penile erection episodes when put in the presence of an inaccessible receptive female for 80 min. These noncontact erections occur concomitantly with an increase in nitric oxide production in the paraventricular nucleus of the hypothalamus. This is shown by the increases in the NO2- and NO3- concentrations in the paraventricular dialysate obtained from these males by in vivo microdialysis. The NO2- concentration increased from 0.75 +/- 0. 10 microm to 2.89 +/- 0.39 microm and that of NO3- from 4.13 +/- 0. 58 microm to 9.5 +/- 1.2 microm. Morphine (0.5, 1 and 5 microg), given unilaterally into the paraventricular nucleus 15 min before the introduction of the receptive female, prevented the NO2- and NO3- increases, and noncontact erections, dose-dependently. In contrast, the kappa opioid receptor agonist U-69 593 (5 microg) was ineffective. The effects of morphine on NO2- and NO3-, and on noncontact erections, were prevented by the opiate receptor antagonist naloxone (10 microg) injected into the paraventricular nucleus 15 min before morphine. The NO2- and NO3- concentrations were also increased in the paraventricular dialysate of male rats during copulation, i.e. when in copula penile erections occurred. As found with noncontact erections, morphine, but not U-69 593, injected into the paraventricular nucleus prevented the NO2- and NO3- increases and impaired copulatory behaviour, and naloxone prevented these responses when given before morphine. Although some diffusion of the opiate to surrounding brain areas cannot be completely ruled out, the present results suggest that morphine acts through mu receptors in the paraventricular nucleus to impair noncontact erections and copulation. These effects of morphine are apparently mediated by a prevention of the increased nitric oxide production that occurs in the paraventricular nucleus of the hypothalamus of male rats during sexual activity.

Animals↗

Dynamic increases in dopamine during paced copulation in the female rat.

The role of dopamine in the rewarding aspects of sexual behaviour in female rats was investigated. This is a unique model because sexual behaviour is only rewarding when copulatory stimuli are experienced at the preferred rate of copulation for a female rat. In addition, increases in dopamine in the nucleus accumbens occur during sexual behaviour only when the female achieves this preferred rate of copulation. In this study, minute-by-minute changes in nucleus accumbens dopamine were monitored using in vivo microdialysis. We report here that extracellular dopamine in the nucleus accumbens increases before coital stimulation only when sexual behaviour is occurring under conditions that are rewarding to the female rat. We conclude that increases in dopamine in the nucleus accumbens are involved in anticipation, not consummation, of sexual behaviour in the female rat.

Animals↗

The evolution of infidelity in socially monogamous passerines: the strength of direct and indirect selection on extrapair copulation behavior in females.

Many studies have been aimed at understanding the maintenance of female infidelity in socially monogamous birds. Because engaging in extrapair copulations (EPCs) is believed to be costly for females, it has been argued that EPC behavior must bring indirect benefits to females by elevating offspring fitness. We use empirical data from the literature to assess the relative strength of indirect and direct selection on female EPC behavior, using quantitative genetic approximations of selection. This analysis confirmed that there is generally negative direct selection on EPC behavior caused by depressed paternal investment by social males. In contrast, there was no significant positive indirect selection on EPC behavior in females. A comparison between the two types of selection suggests that the force of direct negative selection is generally much stronger than that of indirect positive selection. Indirect selection is thus unlikely to maintain EPC behavior in the face of direct selection against it. We suggest that EPCs may instead be the result of antagonistic selection on loci influencing the outcome of male-female encounters and that EPC behavior per se may not be adaptive for females but may reflect sexual conflict due to strong selection in males to achieve extrapair copulations.

Animals↗

Dissociation of copulation from ovulation in pregnant rabbits.

Experiments were designed to determine why copulation in the pregnant rabbit does not terminate pregnancy while treatment with ovulatory doses of luteinizing hormone (LH) human chorionic gonadotropin (hCG) or luteinizing hormone-releasing hormone (LHRH) is known to do so. Pregnant rabbits (Day 8) were mated or were injected with hCG (25 IU/doe) or LHRH (1, 10 micrograms/kg). Serial blood samples were collected over the next 72 h and analyzed for content of LH, follicle-stimulating hormone (FSH) and progesterone. At sacrifice, uteri and ovaries from these animals were examined for viability of the embryos and for signs of recent ovulation. Injection of hCG or LHRH into pregnant animals led to ovulation and to patterns of LH, FSH and progesterone secretion like those which precede ovulation in estrous rabbits. However, mating the pregnant does did not lead to ovulation or to any changes in the circulating hormones. To investigate whether the elevated levels of progesterone during pregnancy were responsible for the dissociation of coitus from ovulation, nonpregnant rabbits were injected with progesterone (2 mg/kg) and then mated or injected with hCG or LHRH. In virtually every respect, the numbers of ovulations and the patterns of hormone secretion in the progesterone-treated, nonpregnant rabbits mimicked those observed in the 8-day pregnant animals; injection of hCG or LHRH caused ovulation and hormonal surges while hCG caused ovulation only. Mating did not lead to ovulation or any change in blood levels of LH, FSH or progesterone. Taken together, the results show that the elevated circulating levels of progesterone, characteristic of pregnancy, are probably responsible for the dissociation of copulation from gonadotropin release in pregnant rabbits.

Animals↗

Spontaneous male death during copulation in an orb-weaving spider.

Males of some cannibalistic species of spiders and insects appear to sacrifice themselves by allowing the female to eat them, and the adaptive significance of such drastic terminal reproductive investment has recently been demonstrated for a spider. Typically, the female has to kill the male, but it has been suggested that males of some species in the cannibalistic orb-weaving spider genus Argiope may die in copula without female 'collaboration'. Here, we provide the first experimental evidence to our knowledge of programmed sudden death after onset of copulation in males of the spider Argiope aurantia. Our observations reveal that males invariably die during the insertion of their second pedipalp, regardless of whether they mate with newly moulted, defenceless females or with older mature females that often attack them. We determined experimentally that the death of males is triggered immediately upon insertion of the second palp, when males become unresponsive, and heartbeat ceases within minutes of insertion. We discuss the possible adaptive significance of programmed death during copulation, and argue that male death has evolved in a context other than sexual cannibalism.

Animals↗

Pregnancy in cactus mice: effects of prolonged copulation.

The postejaculatory copulations of cactus mice are demonstrated to function in facilitating neuroendocrine responses necessary for pregnancy. Whereas estrous cycles were altered after just 10 percent of the tests terminated after one ejaculatory series, females became either pregnant or pseudopregnant after 80 percent of tests continued at least to sexual satiety (30 minutes with no copulations).

Animals↗

"Copulation-reward site" in the posterior hypothalamus.

Posterior hypothalamic selfstimulation of male rats, in which monopolar,platinum electrodes had been belaterally implanted, increased after systdmic injection of testosterone. constant stimulation to the same site elicited immediate copulation with estrous female rats. During constant stimulation males would press a bar to open a door for access to females. Even after ejaculation, males continued to open the door and to display sexual activity until stimulation terminated. Posterior hypothalamic stimulation is like normal sexual stimulation; it is rewarding, the reward varies with the amount of the sex hormone, and it elicits motivated copulation.

Animals↗