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Temporal manipulation of ejaculate components by newly fertilized Drosophila melanogaster females.

Observations of newly mated Drosophila melanogaster females suggest that females control the times at which components of the ejaculate cause behavioural and physiological changes characteristic of fertilized females. Females that were assayed immediately after they mated elicited as much courtship as they did when they were virgins, but were unreceptive to copulation. Within a few minutes of when they disengaged from copulation, most females performed ovipositor extrusion, which has been classified as a rejection behaviour, in response to courting males or males that had previously performed courtship. Most females that were assayed immediately after mating had already ovulated. The females, however, do not begin to lay eggs until 4-6 h after mating, at which time they elicit very little courtship (Scott & Richmond 1985, Anim. Behav., 33, 817-824). Our observations suggest that neither ovipositor extrusion nor male-synthesized pheromones that are transferred to females' cuticles during copulation inhibit males' courtship of newly fertilized females. Thus, males cannot determine that newly fertilized females are unreceptive to copulation. These observations also indicate that the failure of newly fertilized females to mate with males is not a consequence of the females' inability to elicit vigorous courtship. Copyright 1998 The Association for the Study of Animal Behaviour. Copyright 1998 The Association for the Study of Animal Behaviour.

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Multiple mating and cooperative breeding in polygynandrous alpine accentors. I. Competition among females

The reproductive strategy of female alpine accentors, Prunella collaris, was studied on the summit of Mt Norikura in Japan. Alpine accentors formed polygynandrous groups consisting of three to six males and three to five females; however, each female laid eggs in her own nest. Within each group, females were organized in stable, linear hierarchies based on age. All females were sexually active but high-ranking females copulated more frequently with several males from the group. In contrast, the degree of multiple mating and frequency of copulations of low-ranking females was lower because their sexual activity was interrupted by more dominant females. All copulations were preceded by female solicitation. When the young hatched, males helped to feed the chicks of several females with whom they had copulated. The main factor influencing reproductive success was the amount of parental care that was available for feeding the chicks. High-ranking females had paternal help from two or more males and secured a high provisioning rate for the brood, which increased fledging success and nestling weight. The reproductive success of low-ranking females was lower because the brood did not receive sufficient paternal investment and so often starved to death early in the nestling period. These results suggest that the greatest potential benefit females might obtain from multiple mating is the subsequent assistance of several males in caring for the offspring. I discuss the implications of these observations with the idea that competition among females for males brings about multiple mating as a female reproductive strategy. Copyright 1998 The Association for the Study of Animal Behaviour.

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Mating tactics of male Cape ground squirrels, Xerus inauris: consequences of year-round breeding.

The Cape ground squirrel is a highly social, tropical ground squirrel that does not hibernate, suggesting that female receptivity could be scattered throughout the year. Males in this species are very social, living in all-male bands. I studied the mating tactics of male Cape ground squirrels to examine the effects of year-round female receptivity and male grouping on these tactics and on the degree of intrasexual competition. Female breeding was highly irregular and unpredictable, and the average operational sex ratio during oestrus was 10:1 (males to females). However, the predicted high rates of aggression were not observed. Instead, competition among males was manifested by competitive searching, repeated copulations and disruptions of copulations. Dominant males had more copulations with more females, first access to females and were more likely to copulate below-ground where disruptions were unlikely to occur. I conclude that the mating patterns of males in this species are a product of the asynchrony of female oestrus, year-round breeding and the survival benefits of grouping. Copyright 1998 The Association for the Study of Animal Behaviour

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A mating plug and male mate choice in Drosophila hibisci Bock.

The functional significance of mating plugs and their relation to male mating behaviour in insects are obscure. In Drosophila hibisci, we describe a firm, gelatinous, mating plug that fills the entire uterus at copulation, and evaluate two nonmutually exclusive hypotheses for the plug's function: (1) retention of sperm near the openings of the sperm storage organs and (2) inhibition of further matings. Unlike full-sized plugs, smaller plugs produced by previously mated males failed to retain sperm at the anterior end of the uterus, indicating that full-sized plugs prevent sperm backflow away from female storage organs. Sexually mature males failed to copulate with previously mated, young females, suggesting that the plug may also deter rival matings. In newly emerged females, the plug remains within the uterus for up to 4 days after copulation, but in mature females, the plug and ejaculate are expelled whenever the next mature oocyte descends into the uterus from the common oviduct, which may be soon after copulation. Males remained in copula significantly longer with mature females, perhaps to compensate for this greater likelihood of ejaculate expulsion. Males showed a mating preference for young virgins over older virgin and nonvirgin females. This unusual mating preference may confer fertility benefits made available through the effectiveness of the plug in reducing sperm competition. Copyright 1998 The Association for the Study of Animal Behaviour.

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Genetic variation in paternal investment in a seed beetle.

Males of many species invest resources in their offspring. For paternal investment to evolve, it must exhibit heritable variation. Using a standard half-sibling quantitative genetic design, we investigated whether genetic variation in male ejaculate size, a trait that affects female fecundity and copulation duration, are present in the seed beetle Callosobruchus maculatus. Ejaculate size was estimated as the amount of weight lost by males during mating. Dams, but not sires, had significant effects on their sons' absolute ejaculate size (both replicates) and relative ejaculate size (proportion of body weight; one replicate only), explaining 21-25% of the variance in absolute ejaculate size and 8-16% of the variance in relative ejaculate size. These results suggest either a large maternal effect on ejaculate size or sex-linkage of loci that affect the variation in ejaculate size. The proportion of phenotypic variance explained by sex- linkage (assuming no maternal effects) was 42 and 49% (ejaculate size) and 17 and 31% (relative ejaculate size) in the two replicates. These results indicate that male paternal investment can respond to selection, and that it may be able to do so especially rapidly because sex-linked traits have the potential to evolve much more quickly than autosomal traits. There were only weak negative correlations between ejaculate size and mating duration, contrary to what we predicted. There was additive genetic variation in female copulation duration, but not in male copulation duration, suggesting that copulation duration is under female control. Copyright 1998 The Association for the Study of Animal Behaviour.

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Female orgasm rate increases with male dominance in Japanese macaques.

Under specific circumstances, nonhuman primate females may experience orgasm. The occurrence of female copulatory orgasm appears to be highly variable, however, and its proximate causation is poorly understood. We investigated the proximate mechanisms that control orgasmic response in female macaques. During 238 h of observation of sexual behaviour in a large captive group of Japanese macaques, Macaca fuscata, 240 copulations were recorded involving 68 different heterosexual pairs formed by 16 males and 26 females. Female orgasmic responses were observed in 80 of 240 copulations (33%). The frequency of orgasms was not correlated with female age or dominance rank, but it was higher for copulations lasting longer and involving a higher number of mounts and pelvic thrusts. When the level of physical stimulation experienced by females during copulation was statistically controlled, the highest frequency of female orgasms was found among pairs formed by high-ranking males and low-ranking females and the lowest frequency among pairs formed by low-ranking males and high-ranking females. These findings suggest that the proximate mechanisms that control orgasmic threshold in female macaques are more responsive to social stimuli and less constrained by physiological limitations than previously thought. Copyright 1998 The Association for the Study of Animal Behaviour.

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Sex roles and sexual selection.

Sexual selection has been portrayed as acting predominantly on males who compete with each other over copulatory access to females; selection was considered to be driven by females choosing between males at the pre- or postcopulatory level. However, a broader view of sexual selection is now emerging. Examining male discrimination between females and female-female competition has been beneficial in identifying factors influencing the direction and strength of sexual selection. Furthermore, consideration of processes such as sexual coercion or genetic incompatibility, which indirectly influence an individual's set of copulation partners, gamete set or their offspring success, has helped to clarify the ways in which sexual selection may operate. Moreover, there is increasing evidence that not all copulations translate directly to paternity and that paternity does not necessarily translate into successful offspring. Postcopulatory and postfertilization mechanisms that influence not only paternity share but offspring recruitment now require further consideration. The benefits to each sex of copulating with particular partners or with more than one partner remains an area of debate. More carefully designed studies which eliminate alternative possibilities or quantify the relative importance of different selective pressures will also benefit from considering that not all copulations function solely to inseminate or receive sperm. It is also now clear that not all individuals of one sex follow the same strategy. Examining the variation between individuals in reproductive behaviour, fertilization success and offspring success will be important in establishing the selective pressures and mechanisms underlying the operation of sexual selection. (c) 1998 The Association for the Study of Animal Behaviour.

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Operational sex ratio influences female preference and male-male competition in guppies.

Manipulation of the operational sex ratio (OSR) in guppies, Poecilia reticulata, causes changes in male-male competition and female mate choice. In this study OSR is defined as the number of sexually active males divided by the total number of sexually active adults of both sexes. The rate of male courtship displays decreased, and interference behaviours between males increased, at male-biased OSRs. The OSR influenced both copulatory tactics and postcopulatory guarding. All copulations followed sigmoid displays, except at an OSR of five males to one female where 60% of copulations occurred during sneak attempts. Compared with copulations that followed sigmoid displays, successful sneak copulations were followed by a shorter period of postcopulatory mate guarding and a shorter refractory period before males resumed courtship activities. Females preferred males with more orange colour whenever they had a choice, and the preference for orange colour was stronger with more male-biased OSRs. The OSR thus influences the presence, absence or relative importance of both female mate choice and male-male competition which, in turn, should affect the evolution of secondary sexual traits. Copyright 1999 The Association for the Study of Animal Behaviour.

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Female preference for multiple partners: sperm competition in the hide beetle, Dermestes maculatus (DeGeer).

Explanations for the evolution of polyandry emphasize either direct benefits or indirect genetic benefits. The former class of explanation predicts that females may seek multiple copulations but not necessarily multiple partners, while the latter predicts that females will seek multiple copulations with different partners. We investigated these predictions experimentally in the hide beetle, in which females mate more than once during their reproductive cycle. Female hide beetles remated more readily with novel males than with their previous partners, suggesting they mate multiply in order to obtain indirect, genetic benefits. In double-mating experiments with sterile males, the proportion of eggs fertilized by the second male was highly variable; this could not be explained by variation in male body size, duration of copulation or mating order. Male hide beetles form postinsemination associations by riding on the backs of females. This behaviour was more prevalent in the presence of rival males and less prevalent in the presence of additional females, suggesting that the behaviour serves to increase paternity, perhaps by obtaining additional copulations. Copyright 1999 The Association for the Study of Animal Behaviour.

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Differences in potential reproductive rates of male and female seahorses related to courtship roles.

Dwarf seahorses, Hippocampus zosterae (Syngnathidae), are distinguished by extreme morphological specialization for paternal care, the formation of monogamous pair bonds and mating repeatedly over the course of a breeding season. To determine the potential reproductive rates of male and female dwarf seahorses, we measured (1) the maximum number of offspring produced per breeding cycle when sexually receptive mates were unlimited, and (2) the relative time each sex was unavailable for mating ('time out'). We paired sexually isolated males and females with sexually receptive partners and observed them from the day of introduction through to copulation, to determine the length of time it takes each sex to prepare to mate. We conducted additional experiments to determine the length of gestation, which when added to the time needed to prepare to mate and copulate gives an estimate of total reproductive cycle duration, T. We estimated potential reproductive rate by dividing the mean number of offspring produced per breeding cycle by the duration of the breeding cycle (T). We estimated reproductive 'time out' by identifying the period of time males and females were physiologically capable of mating ('time in', S) and subtracting time S from time T. When provided with sexually receptive partners, females took 2 days longer than males to complete courtship and copulation, but neither males nor females remated during gestation. Therefore, males could potentially produce 17% more offspring than females over the course of one breeding season. Females had reproductive 'times out' 1.2 times longer than did males, as they were only capable of mating during the 4 h directly preceding copulation. Thus, H. zosterae males have higher potential reproductive rates and shorter reproductive 'times out' compared with H. zosterae females. These results and previous work indicating that seahorses display traditional courtship roles support the prediction that the sex having the higher potential reproductive rate, or equivalently, the shorter 'time out', will compete more intensely for access to the opposite sex. Copyright 2000 The Association for the Study of Animal Behaviour.

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Differential effects of dopamine receptor antagonists on the sexual behavior of male rats.

In the present experiments, the dose-response effects of the dopamine (DA) receptor antagonists haloperidol, pimozide, clozapine, sulpiride, and metoclopramide, were assessed on patterns of copulatory behavior in intact, sexually active male rats with a high level of sexual experience and performance. The typical neuroleptics haloperidol (0.01-0.5 mg/kg) and pimozide (0.1-5.0 mg/kg) dose-dependently delayed the initiation of copulation and reduced the number of intromissions that preceded ejaculation. The atypical neuroleptics clozapine (0.1-5.0 mg/kg), and sulpiride (0.1-5.0 mg/kg) dose-dependently delayed the initiation of copulation but had no effect on copulatory behavior once it was initiated. In contrast, metoclopramide dose-dependently reduced ejaculation but had no effect on the ability of rats to initiate copulation. These experiments suggest that aspects of copulatory behavior in male rats are affected differently by DA antagonists depending upon their site of action in the brain. Blockade of mesolimbic DA receptors by typical and atypical neuroleptics may delay the initiation of copulation, whereas blockade of mesostriatal DA receptors by typical neuroleptics and metoclopramide may decrease the ejaculation threshold.

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Chronic gonadotropin-releasing hormone agonist treatment suppresses ovulation and sexual behavior in group-living female rhesus monkeys.

The sexual behavior of six adult rhesus females was observed with each of four males prior to, during, and following a 90 day treatment with 20 micrograms/day of a gonadotropin releasing-hormone (GnRH) agonist (WY-40972). All females ovulated, approached males and copulated during an untreated cycle. No ovulations occurred during agonist treatment and all females showed reduced sexual interest during the last 25 treatment days. Three females showed elevated estradiol and copulated during the first 10 days of agonist treatment, but never showed similar levels of estradiol or copulation during the rest of treatment. Within 34 days after agonist treatment, all females initiated proximity to males, copulated, and ovulated. All females became pregnant on their second ovulation after agonist treatment. This demonstration that inhibition of ovulation with a GnRH agonist decreased rhesus female sexual initiation, demonstrates the importance of ovarian hormones to female sexual motivation and suggests that the changes in human female sexual interest should be evaluated during the development of agonist-based contraceptives.

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Regional brainstem expression of Fos associated with sexual behavior in male rats.

This study utilized Fos expression to map the distribution of activated cells in brainstem areas following masculine sexual behavior. Males displaying both appetitive and consumatory sexual behaviors (Cop) were compared to animals prevented from copulation (NC) and to socially isolated (SI) animals. Following copulation, Fos was preferentially augmented in the caudal ventral medulla (CVM), a region mediating descending inhibition of penile reflexes, and which may be regulated by a forebrain circuit that includes the medial preoptic area (MPOA). Copulation-induced Fos was observed in the medial divisions of both the dorsal cochlear nucleus (DC) and trapezoid bodies (Tz), areas which are part of a circuit processing auditory information. In addition, the medullary linear nucleus (Li) displayed comparable amounts of Fos in Cop and NC as compared to the SI animals. Other regions of the pontomedullary reticular system, which may mediate sleep and arousal, did not exhibit Fos expression associated with consumatory sexual behavior. We suggest that Fos is associated with the inhibition of sexual behavior following ejaculation in the CVM, and that auditory information arising from the DC and Tz is combined with copulation-related sensory information in the subparafasicular nucleus and projected to the hypothalamus. In addition, equal amounts of Fos expression observed in the Li in both the Cop and NC animals suggests that this region is involved in sexual arousal. Overall, the data suggest that processing by brainstem nuclei directly contributes to the regulation of mating behavior in male rats.

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Cholinergic control of synchronized seminal emissions in Drosophila.

In many animal species, copulation involves the coordinated release of both sperm and seminal fluid, including substances that change female fertility and postmating behavior. In Drosophila melanogaster, these substances increase female fertility and prevent mating with a second male. By using a PGal4 strain, we targeted together with other cells a dozen cholinergic neurons found only in the male abdominal ganglion (Abg-MAch). Genetic feminization apparently deleted these neurons in males and significantly increased their copulation duration, blocked their fertility in 60% of cases, and only weakly repressed remating in females. Genetic repression of Gal4 activity in all cholinergic neurons completely rescued copulation duration and fertility, and totally prevented remating, indicating that Abg-MAch neurons were functional. The conditional blocking of the synaptic activity of these neurons during copulation induced separate effects on the transfer of the seminal substances involved in fertilization and those involved in remating. These effects were dissociated only when Abg-MAch neurons were feminized, indicating that their presence is required to synchronize the emission of the male substance(s) that changes reproductive behaviors.

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An invasion of cheats; the evolution of worthless nuptial gifts.

Nuptial gifts are food items or inedible tokens that are transferred to females during courtship or copulation . Tokens are of no direct value to females, and it is unknown why females require such worthless gifts as a precondition of mating. One hypothesis is that token giving arose in species that gave nutritious gifts and males exploited female preferences for nutritional gifts by substituting more easily obtainable but worthless items. An invasion of such behavior would require that females accept the substitute gift and copulate for a period of time similar to that with genuine gifts. We show that both these prerequisites are met in the dance fly Rhamphomyia sulcata, in which females normally accept a nutritious gift. We removed the gift from copulating pairs and replaced it with either a large or small prey item or inedible token. We found that although pairs copulated longest with a large genuine gift, the tokens resulted in copula durations equivalent to those with a small genuine gift. We also observed that males that returned to the lek with tokens re-paired successfully. These findings suggest that female behavior in genuine gift-giving species is susceptible to the invasion of male cheating on reproductive investment.

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Male mounting alone reduces female promiscuity in the fowl.

The fertilization success of an insemination is at risk when a female has the possibility to copulate with multiple males, generating sperm competition and sexual conflict over remating. Female propensity to remate is often reduced after copulation, and a staggering diversity of highly derived male traits that discourage female promiscuity have been investigated. However, it is difficult to separate the effect of such specialized traits and insemination products from the more basic effect that the act of mounting per se may have on female remating. Here, we use a novel approach that separates the influence of mounting from that of insemination on female remating in the promiscuous feral fowl. Mounting alone caused a transient but drastic reduction in female propensity to remate, and-crucially-the number of sperm that a female obtained from a new male. Therefore, like other taxa, female fowl show a reduction in promiscuity after copulation, but this is entirely due to mounting alone. This effect of mounting, independent of insemination and fertilization, indicates that even copulations that deliver little or no semen, a puzzling behavior common in many species including the fowl, may play a crucial role in sperm competition.

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Dopamine and serotonin: influences on male sexual behavior.

Steroid hormones regulate sexual behavior primarily by slow, genomically mediated effects. These effects are realized, in part, by enhancing the processing of relevant sensory stimuli, altering the synthesis, release, and/or receptors for neurotransmitters in integrative areas, and increasing the responsiveness of appropriate motor outputs. Dopamine has facilitative effects on sexual motivation, copulatory proficiency, and genital reflexes. Dopamine in the nigrostriatal tract influences motor activity; in the mesolimbic tract it activates numerous motivated behaviors, including copulation; in the medial preoptic area (MPOA) it controls genital reflexes, copulatory patterns, and specifically sexual motivation. Testosterone increases nitric oxide synthase in the MPOA; nitric oxide increases basal and female-stimulated dopamine release, which in turn facilitates copulation and genital reflexes. Serotonin (5-HT) is primarily inhibitory, although stimulation of 5-HT(2C) receptors increases erections and inhibits ejaculation, whereas stimulation of 5-HT(1A) receptors has the opposite effects: facilitation of ejaculation and, in some circumstances, inhibition of erection. 5-HT is released in the anterior lateral hypothalamus at the time of ejaculation. Microinjections of selective serotonin reuptake inhibitors there delay the onset of copulation and delay ejaculation after copulation begins. One means for this inhibition is a decrease in dopamine release in the mesolimbic tract.

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Dose-dependent effects of acute kainic acid treatment on sexual behavior of male rats.

Male rats of the Wistar strain were selected as good copulators (displaying at least 1 ejaculation in each of three consecutive tests for male sexual behavior) and sexually sluggish animals (displaying no ejaculations in each of three consecutive tests). The administration of low doses (1 and 2.5 mg/kg, i.p.) of kainic acid in sexually sluggish rats induced an enhancement of some parameters of copulatory behavior. In particular, significant reductions in latency to the first mount and intromission and increases in frequency of mounts and intromissions were observed. In contrast, the drug failed to exert any effect in good copulators. At the dose of 5 mg/kg (i.p.) kainic acid exerted an inhibitory effect on sexual behavior parameters both in good copulators and in sluggish rats. A persistent increase in latency to the first mount, intromission and ejaculation, and reduction in frequency of mounts, intromissions and ejaculation both in good copulators and in sluggish rats were observed 20 days after kainic acid treatment at the higher dose. No persistent effect of kainic acid 1 and 2.5 mg/kg was observed 20 days after treatment. These results suggest that kainic acid may affect in a dose-dependent manner several copulatory parameters of male sexual behavior repertoire. The bimodal effects could be explained considering a possible interaction of kainic acid with different neurotransmissions or receptor subtypes.

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