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Male mating preference for female survivorship in the seaweed fly Gluma musgravei (Diptera: Coelopidae).

The seaweed fly mating system is characterized by pre-mating struggles during which females exhibit a mate rejection response involving kicking, shaking and abdominal curling. Males must resist rejection until females become passive and allow copulation to take place. However, despite the vigorous nature of the struggle males frequently dismount passive females without attempting copulation. Here we show that rejected females suffered higher post-encounter mortality rates than those accepted by males in the seaweed fly Gluma musgravei. Furthermore, we show that males also preferentially mounted females with higher future longevity. We propose that this male mate choice for female survivorship has evolved as a result of females often having to survive for long periods after mating until suitable oviposition sites become available. Such male preferences for female survivorship may be common in species in which oviposition must sometimes be substantially delayed after mating.

Animals↗

Copulatory courtship signals male genetic quality in cucumber beetles.

In the spotted cucumber beetle, Diabrotica undecimpunctata howardi (Coleoptera: Chrysomelidae), males court females during copulation by stroking them with their antennae. Stroking occurs exclusively during the first stages of copulation, after a male has penetrated a female's vaginal duct but before he is allowed access to her bursa copulatrix. Females accept the spermatophore of fast-stroking males and reject those of slow-stroking males by relaxing or constricting muscles distorting the vaginal duct. Here, we measure the repeatability of stroking behaviour within males, examine the effect of losing one antenna on male attractiveness and test whether such female control results in direct phenotypic benefits for the discriminating female or indirect genetic benefits that appear in her offspring. We also use a half-sibling design to quantify the variance and heritability of stroking speed and endurance. Female beetles were paired with a male that was known to stroke either quickly or slowly. No difference was found in the resulting fecundity or egg-hatching rate of the females, or in the survivorship, development rate, size, age at first reproduction or fecundity of their offspring indicating that no direct benefits are gained by discriminating among males on the basis of stroking speed. There were, however, good-genes benefits for the mates of fast-stroking males. Offspring of fast-stroking fathers were also fast strokers and were more likely to be accepted as mates than offspring of slow-stroking fathers. There was substantial variance among sires in stroking speed and endurance and the heritability of each trait was high. The antennal stroking rate was highly repeatable in successive mating attempts and males with only one antenna were not accepted as mates. The repeatability within males, variability between males and heritability between generations of copulatory stroking combine to provide females with a reliable and honest signal of the genetic quality of courting males.

Animals↗

Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success.

Male contests for access to receptive females are thought to have selected for the larger male body size and conspicuous weaponry frequently observed in mammalian species. However, when females copulate with multiple males within an oestrus, male reproductive success is a function of both pre- and postcopulatory strategies. The relative importance of these overt and covert forms of sexual competition has rarely been assessed in wild populations. The Soay sheep mating system is characterized by male contests for mating opportunities and high female promiscuity. We find that greater horn length, body size and good condition each independently influence a male's ability to monopolize receptive females. For males with large horns at least, this behavioural success translates into greater siring success. Consistent with sperm-competition theory, we also find that larger testes are independently associated with both higher copulation rates and increased siring success. This advantage of larger testes emerges, and strengthens, as the number of oestrous females increases, as dominant males can no longer control access to them all. Our results thus provide direct quantitative evidence that male reproductive success in wild populations of mammals is dependent upon the relative magnitude of both overt contest competition and covert sperm competition.

Animals↗

Extracellular excitatory amino acids increase in the paraventricular nucleus of male rats during sexual activity: main role of N-methyl-d-aspartic acid receptors in erectile function.

The concentrations of glutamic and aspartic acids were measured in the dialysate obtained with vertical microdialysis probes implanted into the paraventricular nucleus of the hypothalamus of sexually potent male rats during sexual activity. Animals showed noncontact erections when put in the presence of, and copulated with, a receptive (ovarietomized oestrogen- and progesterone-primed) female rat. The concentrations of glutamic and aspartic acids in the paraventricular dialysate increased by 37 and 80%, respectively, above baseline values during exposure to the receptive female rat and by 55 and 127%, respectively, during copulation. No changes in the concentrations of glutamic and aspartic acids were detected in the paraventricular dialysate when sexually potent male rats were exposed to nonreceptive (ovariectomized not oestrogen- and progesterone-primed) female rats or when impotent male rats were used. The injection into the paraventricular nucleus of the excitatory amino acid receptor antagonist dizocilpine (5 micro g), a noncompetitive N-methyl-d-aspartic acid receptor antagonist, reduced noncontact erections and significantly impaired copulatory activity. The alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor antagonist 6-cyano-7-nitro-quinoxaline-2,3-dione (5 micro g) was also able to impair copulatory activity, but to a much lower extent than dizocilpine. In contrast, (+/-)-2-amino-4-phosphono-butanoic acid, a metabotropic receptor antagonist (5 micro g), was found to be ineffective. These results confirm the involvement of the paraventricular nucleus in the control of erectile function and copulatory behaviour and show that excitatory amino acid concentration increases in the paraventricular nucleus when penile erection occurs in physiological contexts.

6-Cyano-7-nitroquinoxaline-2,3-dione↗

Sperm competition and diversity in rodent copulatory behaviour.

The copulatory behaviour of male mammals is characterized by striking diversity in patterns of copulatory stimulation and ejaculation frequency. We conducted comparative analyses of rodents to investigate the potential influence of sperm competition in the evolution of copulatory behaviour. We found that increasing sperm competition is associated with faster rates of stimulation and earlier ejaculation among species in which males perform multiple intromissions prior to ejaculation, but with no overall change in the number of intromissions per ejaculation. Increasing sperm competition is also associated with a higher frequency of repeated ejaculations with the same female, and with shorter refractory periods between repeated copulations. Increasing sperm competition level thus appears to select for male ability to ejaculate more rapidly and more frequently with each female mated. As prolonged copulations are known to reduce female remating rates, these findings indicate that males may experience opposing selection pressures on copulatory behaviour with respect to offensive and defensive aspects of sperm competition. We conclude that sperm competition is likely to be an important selection pressure explaining diversity in mammalian copulatory behaviour.

Animals↗

Periodic, short-term heat exposure and reproductive function in male and female rats.

Reproductive function of male and female rats was examined in relation to periodic, short-term heat treatment. Daily exposure to an environmental temperature of 38.2 degrees C for 55 min elevated rectal temperatures to 39.9 and 41.2 degrees C in male and female rats, respectively. Heat exposure tended to decrease copulation in males cohabitated with unheated females. The rate of conception was affected similarly, and fetal survival tended to be reduced by paternal heat treatment. Estrous cycles were disrupted initially in heat-exposed females, but the rate of copulation and conception of females cohabitated with unheated males was unaltered by heat treatment. However, maternal heat exposure impaired prenatal survival and growth. During lactation, a high incidence of maternal and pup deaths was observed at approximately 14 days postpartum. Maternal deaths were coincident with a decrease in thermoregulatory ability and rectal temperatures exceeding 42 degrees C.

Animals↗

Copulatory behavior and the initiation of pregnancy in California voles (Microtus californicus).

The copulatory behavior of Microtus californicus and its effect on pregnancy initiation were examined in two experiments. In experiment 1 18 males and 18 females which had received exogenous hormones participated in 54 tests of copulatory behavior, each continued to a satiety criterion of 30 min with no copulations. The basic pattern involved no lock, intravaginal thrusting, ejaculation possible on a single insertion and multiple ejaculation. Ejaculation frequency ranged from 1 to 5, with a mean of 2.2. In experiment 2, it was found that all females receiving satiety tests of copulatory behavior while in male-induced estrus ovulated and became pregnant. Whereas all 10 females receiving one ejaculation ovulated, only 60% became pregnant. Thus, it appears that copulation beyond one ejaculation functions in increasing the likelihood of pregnancy. By comparing different species of Microtus it is proposed that copulatory patterns in which males persist for many thrusts and ejaculations may have evolved in conjunction with ornate penile morphology, large litter sizes, and high stimulus requirements for the initiation of ovulation and a funtional luteal phase.

Animals↗

Evidence for the modulation of sexual behavior by alpha-adrenoceptors in male rats.

Clonidine, a commonly used antihypertensive agent believed to act by stimulation of central alpha-adrenoceptors, produced a dose-related suppression of ejaculatory behavior in sexually vigorous male rats throughout the range of treatment (0.0125-0.5 mg/kg). Treatment with 0.25 mg/kg virtually eliminated ejaculatory behavior, without altering the number of animals mounting and intromitting. These effects were maintained for at least 4 h after treatment. Prazosin, another antihypertensive (but acting by blockade of alpha 1-adrenoceptors), increased latencies to initiation of copulation, to ejaculation, and to reinstatement of copulation following ejaculation. Additionally, prazosin (1 mg/kg) pretreatment failed to attenuate or prevent the clonidine-induced suppression of ejaculation. In contrast, yohimbine, a drug which preferentially blocks alpha 2-adrenoceptors (2 mg/kg, 20 min prior to mating tests), caused a facilitation of copulatory behavior as evidenced by drastic decreases in ejaculation latency and intercopulatory and postejaculatory intervals. Pretreatment with yohimbine completely prevented the clonidine-induced suppression of ejaculation, while clonidine attenuated the facilitatory effects of yohimbine, suggesting a competitive interaction. These data lead to the suggestion that increased excitatory adrenergic activity results in increased sexual arousal either by blockade of alpha 2-or stimulation of alpha 1-adrenoceptors. Alternatively, stimulation of alpha 2-or blockade of alpha 1-adrenoceptors results in diminished sexual motivation. While the precise implications of this animal research for the clinic are as yet unclear, further research could lead to important developments in the pharmacological treatment of sexual dysfunctions.

Animals↗

Continual sexual receptivity in the female chimpanzee (Pan troglodytes).

Daily observations during a 5-year period showed that the mean frequencies of copulation per day during various sexual states of the female chimpanzee were almost identical, except for during maximum tumescence and lactation. The mean frequency of observed copulation peaked during maximum tumescence and was lowest during lactation.

Animals↗

A method for the routine observation of sexual behaviour in rats.

In seeking a method for the routine observation of copulatory behaviour in rats we compared the use of a standard rectangular Makrolon cage, commonly used in toxicology studies, with a Plexiglas cylinder that provided 2.5 times more floor area. The cylinder resulted in a much higher incidence of copulation, either once or for multiple series, within 30 min. This was not affected by whether oestrus was natural or induced. Using the cylinder and 4 h observation periods, we found that the dark phase of a 12-12 h inverse light cycle resulted in many more copulations than occurred during the light phase of a natural cycle. The incidence increased from the first to the second to the last 4 h of the dark phase. We found that placing a virgin receptive female and a naive male together in a Plexiglas cylinder for 1 h towards the end of the dark phase is a useful tool in reproductive toxicology studies in which it is important to know the precise time of insemination.

Animals↗

Effect of copulatory stimuli on incidence of ovulation and on serum luteinizing hormone in the cat.

The relationship among the number of copulatory stimuli, the incidence of ovulation, and the pituitary release of LH was studied in the female cat (queen), an induced or reflex-ovulating species. Estrual queens were mated with a male either once during estrus (on day 1, 2, 3, or 4) or three times at 4-h intervals in a single day of estrus (on day 1, 2, or 3). Laparoscopy was used to examine the ovaries, initially to determine the numbers of preovulatory follicles and later to count corpora lutea. Blood samples were obtained serially from cats in each mating group, and sera were analyzed for LH. The day of estrus on which mating occurred, estrus duration, and follicle numbers had no effect on the proportion of animals ovulating. A single mating resulted in fewer queens ovulating per group (10 of 48 animals) than three matings on a single day (30 of 36). After copulation, LH was elevated only in animals later confirmed to ovulate. LH response in ovulating queens varied among individuals but, when averaged, appeared to be greater and more prolonged in multiple mated vs. single mated animals. These data indicate that the reflex-ovulating cate does not always ovulate after a single copulatory stimulus because of a failure of LH release. The frequency of coital stimulation apparently plays a major role in influencing the proportion of animals ovulating, with multiple copulation apparently enhancing the pituitary release of LH.

Animals↗

Improving sneaky-sex in a low oxygen environment: reproductive and physiological responses of male mosquito fish to chronic hypoxia.

Few studies have examined the adaptive significance of reversible acclimation responses. The aerobic performance and mating behaviour of the sexually coercive male eastern mosquito fish (Gambusia holbrooki) offers an excellent model system for testing the benefits of reversible acclimation responses to mating success. We exposed male mosquito fish to normoxic or hypoxic conditions for 4 weeks and tested their maximum sustained swimming performance and their ability to obtain coercive matings under both normoxic and hypoxic conditions. We predicted that hypoxia-acclimated males would possess greater swimming and mating performance in hypoxic conditions than normoxic-acclimated males, and vice versa when tested in normoxia. Supporting our predictions, we found the sustained swimming performance of male mosquito fish was greater in a hypoxic environment following long-term exposure to low partial pressures of oxygen. However, the benefits of acclimation responses to mating performance were dependent on whether they were tested in the presence or absence of male-male competition. In a non-competitive environment, male mosquito fish acclimated to hypoxic conditions spent a greater amount of time following females and obtained more copulations than normoxic-acclimated males when tested in low partial pressures of oxygen. When males were competed against each other for copulations, we found no influence of long-term exposure to different partial pressures of oxygen on mating behaviour. Thus, despite improvements in the aerobic capacity of male mosquito fish following long-term acclimation to hypoxic conditions, these benefits did not always manifest themselves in improved mating performance. This study represents one of the first experimental tests of the benefits of reversible acclimation responses, and indicates that the ecological significance of physiological plasticity may be more complicated than previously imagined.

Acclimatization↗

Reproductive behaviour in the male cricket Gryllus bimaculatus DeGeer. II. Neural control of the genitalia.

To understand the neural mechanisms of reproductive behaviour in the male cricket, we identified motor neurones innervating the muscles in each genital organ by backfilling with cobalt/nickel and recording their extracellular spike activity from nerve bundles of the terminal abdominal ganglion during tethered copulation and spermatophore formation. During tethered copulation, at least two motor neurones innervating two ipsilateral muscles were activated during projection of the guiding rod of the phallic dorsal pouch. Only one motor neurone, innervating four ipsilateral muscles of the dorsal pouch, was responsible for spermatophore extrusion by deforming the dorsal pouch. For spermatophore transfer, three motor neurones, singly innervating three epiphallus muscles, played a major role in opening passages for haemolymph to enter the ventral lobes and median pouch by bending the epiphallus. Two ventral lobe and 3-5 median pouch motor neurones seemed to play a role in expanding or folding the two membranous structures by relaxing or contracting their muscle fibres. After spermatophore transfer, most of the genital motor neurones exhibited a rhythmic burst of action potentials causing movement of the phallic complex coupled with strong abdominal contractions. For spermatophore formation, the genital motor neurones began to accelerate their rhythmic bursts approximately 30 s prior to subgenital plate opening and then changed their activity to tonic bursting or silence. The results have allowed us to describe the timing of the onset and termination of genital muscle contraction more precisely than before, to examine the neural mechanisms of copulatory motor control and to speculate on the neural organization of the reproductive centre for spermatophore extrusion and protrusion.

Action Potentials↗

Production of rats in synchronised batches.

Successful synchronisation of copulations and births for the 1st parity permit continued synchrony of parturitions in subsequent parities. Foetal implantation after post-partum copulation was delayed by multiples of the oestrous cycle; both season and number of sucking neonates influenced the time of implantation. Post-weaning matings gave a high conception rate with a parturition spread of 36 hours for 94% of the original group.

Animals↗

Characterization of the oestrous cycle and mating season of squirrel monkeys from copulatory behaviour.

Observations of the behaviour of squirrel monkeys, including 8 opposite-sex pairs during daily 30-min social encounters and 2 mixed-sex permanent groups during daily 30-min observation sessions, over a 14-month period were used to determine the periodicity of the oestrous cycle and annual mating season. The median and modal length of the oestrous cycle was 8 days, within which copulations were limited to a 1--2 day period. In a cyclic female, plasma progesterone levels over a 24-day period dropped from 85--151 ng/ml to 25 ng/ml 2 days before oestrus. In non-cyclic females plasma progesterone values were less than 15-4 ng/ml. Males exhibited a 6-8--19-7 week 'season' of copulation and ejaculation. The onset of this 'mating season' in August coincided with the annual peak in male body weight (the 'fatted male' phenomenon).

Animals↗

Effects of an isolated or enriched environment after handling on sexual maturation and behaviour in male and female rats.

Male and female rats that were handled from birth to 30 days had increased adrenal weight at weaning. The animals were then rehoused in (a) groups of 10 in a large cage with an enriched environment, (b) a small cage in pairs, or (c) a small cage alone. Isolation advanced and enrichment retarded vaginal opening (in comparison with paired animals) in handled and unhandled females. Puberty was accelerated by handling irrespective of housing conditions. Isolation improved sexual performance in male rats: almost all ejaculated within 4 daily testing sessions with a receptive female, whereas only half the pair-housed males and even fewer group-housed animals copulated. The group-housed copulators were sexually the most active in a hierarchy observed when a single receptive female was placed in the enriched cage for 15 min. The rank order in which these males initiated and consummated sexual activity was consistent over several tests.

Adrenal Glands↗

Detection of activity similar to that of early pregnancy factor after mating sows with a vasectomized boar.

Incubation of normal pig lymphocytes in serum samples collected from 10 sows immediately before, and at daily intervals after mating with a vasectomized boar significantly elevated the rosette inhibition titre (RIT) of a standard antilymphocyte serum in 6 animals on the first but not on the 2nd and 3rd day after copulation. Infusion of seminal plasma without mating into 5 sows induced an obvious, but not statistically significant, transient rise of titres in 3 pigs. Neither sodium chloride infusion (N = 5), nor sham copulation with diverted penis (N = 5) influenced serum RITs. Porcine seminal plasma showed an inherent rosette-inhibiting property. A depression of rosette formation was evident in a concentration-dependent fashion up to a dilution of 1 in 320. Similarly, preincubation of lymphocytes in serial dilutions of seminal plasma in a non-pregnancy serum sample led to an amplification of the rosette inhibiting capacity of the antilymphocyte serum. Non-specific activation of the eggs to release a signal which induces the production of early pregnancy factor (EPF) or the resorption of seminal plasma components into the blood circulation are considered as possible explanations for the EPF-like activity after mating with a vasectomized boar.

Animals↗

Reproductive inhibition in the Cape porcupine, Hystrix africaeaustralis.

Sexually mature female Cape porcupines kept under natural conditions of illumination and temperature did not conceive while housed within their natal groups. Before removal from their natal groups the sexually mature offspring copulated and experienced cyclic ovarian activity, but conception occurred only 70-120 days after dispersal. Mean oestrous cycle length of these females (36.9 +/- 11.5 days; n = 34) was similar to that of breeding females (33.0 +/- 11.64 days; n = 16), but mean peak plasma progesterone concentration (6.45 +/- 6.03 ng/ml; n = 34) was significantly (P less than 0.01) lower than that of cyclic breeding females (13.58 +/- 6.98 ng/ml; n = 16). Mean progesterone concentration at oestrus in non-breeding females (0.72 +/- 0.45 ng/ml; n = 34) was also significantly (P less than 0.01) lower than that of non-pregnant breeding females (4.21 +/- 2.44 ng/ml; n = 16). Reproductive inhibition within natal groups, in which only one female reproduces, therefore cannot be ascribed to a failure to copulate, but may be due to some factor inhibiting full expression of luteal activity or affecting ovulation.

Animals↗