Sociosexual behavior, male mating tactics, and the reproductive cycle of giraffe Giraffa camelopardalis

Female distribution exerts a major impact on male mating tactics. Giraffe cows have a reproductive cycle, and a social system, that should favor a male roaming reproductive tactic. We conducted a 2-year study of female Rothschild's giraffe (G. c. rothschildi) reproductive endocrinology in order to characterize attributes of the reproductive cycle and investigate how female endocrine and behavioral cues influence mating activity. We used non-invasive fecal steroid methods to determine reproductive state among females residing in a herd in a large outdoor enclosure. We found that females had an estrous cycle of 14.7 days and that they regularly had multiple ovarian cycles prior to conception. Adult males were more likely to associate with, and sexually investigate, females when they were cycling than when they were either pregnant or acyclic. During the estrous cycle, male-female proximity and sociosexual behavior were more pronounced during the probable fertile phase than the rest of the cycle. Sexual activity between giraffe coincided with the periovulatory period, with male interest in females peaking during the fertile window in the absence of proceptive behavior by females. We conclude that males detect reliable cues revealing female reproductive status and partition their reproductive effort in response to such cues. We propose that male giraffe adopt a roaming reproductive strategy with their large size, enabling them to search for and mate guard fertile females while minimizing metabolic costs.     

Differential impact of cocaine on meal patterns in female and male rats

Female rats, relative to males, exhibit greater behavioral activation to cocaine and other psychostimulants, but the effect of sex and the estrous cycle in modulating the hypophagic action of cocaine has not been evaluated. Meal patterns were recorded in automated food hoppers during the first 3 h of the dark phase in adult female and male rats after administration of ascending cocaine doses (0, 7.5, and 15 mg/kg cocaine, i.p.) on successive trials. Cocaine produced a greater suppression of feeding as well as a reduction in meal number over a 3 h test period in female rats during estrus, relative to that noted during diestrus. In contrast, during the 180 min test period, male rats showed minimal hypophagic responses to 7.5 or 15 mg/kg cocaine. These results extend the range of behavioral perturbations induced by cocaine that are modulated by sex and by the estrous cycle and are consistent with the notion that estradiol may modulate the neurochemical actions of cocaine.     

Protocol for Studying Extinction of Conditioned Fear in Naturally Cycling Female Rats

Extinction of conditioned fear has been extensively studied in male rodents. Recently, there have been an increasing number of studies indicating that neural mechanisms for certain behavioral tasks and response behaviors are different in females and males. Using females in research studies can represent a challenge because of the variation of gonadal hormones during their estrous cycle. This protocol describes well-established procedures that are useful in investigating the role of estrogen in fear extinction memory consolidation in female rats. Phase of the estrous cycle and exogenous estrogen administration prior to extinction training can influence extinction recall 24 hr later. The vaginal swabbing technique for estrous phase identification described here aids the examination and manipulation of naturally cycling gonadal hormones. The use of this basic rodent model may further delineate the mechanisms by which estrogen can modulate fear extinction memory in females.     

Measuring male-female relationships during the mating season in wild Japanese macaques (Macaca fuscata yakui)

Heterosexual relationships during one mating season were examined in a wild troop of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. Validation tests of putative mate choice behaviors demonstrated that female initiation and maintenance of proximity, female lookback at the male, and sexual presents to the male, were associated with increased mating. Male grooming the female was also associated with increased mating. Ten dyadic social behaviors were subject to principal components analysis to empirically define behavioral dimensions of male-female relationships. The analysis yielded four relationship dimensions: ‘Mutual Choice and Male Coercion,’ ‘Female Choice’ (two types), and ‘Mutual Choice’ Dyads tended to be characterized by more than one dimension. The results suggested that females sought matings with multiple males of various dominance ranks. Female relationships with high ranking males contained elements of male coercion and mate guarding, however, because these males attempted to inhibit females from mating with lower ranking males. The correlation between each relationship dimension and mating success depended, in part, on the dominance rank of males. Relationships involving high ranking males, which were most likely to contain elements of male coercion and mate guarding, were associated with mating success. Relationships involving low ranking males, which usually lacked such coercive elements. were less strongly correlated with mating success. These results, obtained from a wild troop, are compared to those previously obtained in captive and provisioned groups of Japanese macaques.     

Female presence affects male behavior and testosterone levels in the European starling (Sturnus vulgaris)

In this study, we confronted individually housed male European starlings (Sturnus vulgaris) with a female conspecific for 60 min to study the consequences on behavior and plasma testosterone (T) concentrations. Control males experienced a similar procedure, the only difference being that they were tested in the absence of a female. Female presence significantly affected both behavior and plasma T levels of male starlings. Experimental males spent significantly more time singing in the nest box and flew significantly more into the nest box with green nesting material during female presentations than during control periods. Control males never showed these mate attraction behaviors. In total 5 of the 16 experimental males did not respond behaviorally to the female stimulus bird (NR males). In contrast to T levels of control males, plasma T concentrations of both experimental males that did respond to the female (R males) and of NR males (which only perceived the female stimulus) were positively influenced by female presentation. The time spent singing in the nest box by experimental males (R and NR males combined) during female presence tended to be positively correlated with changes in plasma T levels. Finally, before introduction of a female, plasma T levels of R males were significantly higher than those of NR males indicating that individually housed males respond to the presence of a female conspecific by increasing their mate attraction behaviors only when a threshold plasma T concentration has been reached.     

Estrous asynchrony causes low birth rates in wild female chimpanzees

Estrous cycle asynchrony likely functions to elevate individual females' sexual attractiveness during female mate choice. Female chimpanzees show physiological estrus as anogenital swelling. Copulations are concentrated during the period of maximal tumescence, which is called the estrous period. A group of female chimpanzees in Mahale Mountains National Park, Tanzania, was shown to display asynchrony in both maximal tumescence and periovulatory periods. We tested the hypothesis that females establish asynchronous maximal tumescence or periovulatory periods with respect to other females to increase copulation frequency and birth opportunities (Hypothesis 1). We analyzed differences in birth rates between four asynchronous years and five nonasynchronous years. Counter to Hypothesis 1, females in periovulatory periods during asynchronous years showed significantly lower birth rates than those in nonasynchronous years. In addition, periovulatory females copulated more frequently on days on which no other female in a periovulatory period was present. These results suggest that birth rates tend to decrease when females experience nonoverlapping ovulation cycles, although copulation frequency is high. Such a decrease in the birth rate may have resulted from the cost associated with multiple copulations. We tested two other hypotheses: paternity confusion (Hypothesis 2) and sperm competition (Hypothesis 3). Both of these hypotheses were partially supported. The highest‐ranking male most effectively monopolized access to receptive females when relatively few other males and receptive females from the party (or subgroup) were present. The viability of Hypotheses 2 and 3 requires that dominant males are able to hinder a female from mating with other males. Given that the male‐biased operational sex ratio created by female asynchrony is likely to reduce the efficiency of mate guarding by dominant males, an asynchronous female may gain a fitness benefit by increasing the probability of mating with at least one male who produces superior sperm. Am. J. Primatol. 73:180–188, 2011. © 2010 Wiley‐Liss, Inc.     

The bed nucleus of the stria terminalis is critical for sexual solicitation,but not for opposite-sex odor preference,in female Syrian hamsters

Successful reproduction in vertebrates depends critically upon a suite of precopulatory behaviors that occur prior to mating. In Syrian hamsters (Mesocricetus auratus), these behaviors include vaginal scent marking and preferential investigation of male odors. The neural regulation of vaginal marking and opposite-sex odor preference likely involves an interconnected set of steroid-sensitive nuclei that includes the medial amygdala (MA), the bed nucleus of the stria terminalis (BNST), and the medial preoptic area (MPOA). For example, lesions of MA eliminate opposite-sex odor preference and reduce overall levels of vaginal marking, whereas lesions of MPOA decrease vaginal marking in response to male odors. Although BNST is densely interconnected with both MA and MPOA, little is known about the role of BNST in female precopulatory behaviors. To address this question, females received either bilateral, excitotoxic lesions of BNST (BNST-X) or sham lesions (SHAM), and were tested for scent marking and for investigatory responses to male and female odors. Whereas SHAM females vaginal marked more to male odors than female odors on two days of the estrous cycle, BNST-X females marked at equivalent levels to both odors. This deficit is not due to alterations in social odor investigation, as both BNST-X and SHAM females investigated male odors more than female odors. Finally, BNST lesions did not generally disrupt the cyclic changes in reproductive behaviors that occur across the estrous cycle. Taken together, these results demonstrate that BNST is critical for the normal expression of solicitational behaviors by females in response to male odor stimuli.     

The bed nucleus of the stria terminalis is critical for sexual solicitation, but not for opposite-sex odor preference, in female Syrian hamsters

Successful reproduction in vertebrates depends critically upon a suite of precopulatory behaviors that occur prior to mating. In Syrian hamsters (Mesocricetus auratus), these behaviors include vaginal scent marking and preferential investigation of male odors. The neural regulation of vaginal marking and opposite-sex odor preference likely involves an interconnected set of steroid-sensitive nuclei that includes the medial amygdala (MA), the bed nucleus of the stria terminalis (BNST), and the medial preoptic area (MPOA). For example, lesions of MA eliminate opposite-sex odor preference and reduce overall levels of vaginal marking, whereas lesions of MPOA decrease vaginal marking in response to male odors. Although BNST is densely interconnected with both MA and MPOA, little is known about the role of BNST in female precopulatory behaviors. To address this question, females received either bilateral, excitotoxic lesions of BNST (BNST-X) or sham lesions (SHAM), and were tested for scent marking and for investigatory responses to male and female odors. Whereas SHAM females vaginal marked more to male odors than female odors on two days of the estrous cycle, BNST-X females marked at equivalent levels to both odors. This deficit is not due to alterations in social odor investigation, as both BNST-X and SHAM females investigated male odors more than female odors. Finally, BNST lesions did not generally disrupt the cyclic changes in reproductive behaviors that occur across the estrous cycle. Taken together, these results demonstrate that BNST is critical for the normal expression of solicitational behaviors by females in response to male odor stimuli.     

Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve,Madagascar

Observations of reproductive behavior in free-ranging Lemur catta were carried out during one annual cycle. Variability in the behavior of female ringtailed lemurs during parturition appears to be mainly a function of the female's parity and thus her experience. Females within a troop show estrous asynchrony and characteristically mate with more than one male. Females also exhibit proceptive behavior toward and mate with some males from other troops and with transferring males. The potential for a male to monopolize mating opportunities during a female's short estrous period is therefore limited. Male mating strategies in ringtailed lemurs can be seen as adaptations to female mate choice during a highly restricted breeding season. In this species the dominance hierarchy does not break down with regard to the order of mating. The highest ranking male (central male) mates first and shows precopulatory guarding and longer postejaculatory guarding, which may increase his chances of siring the offspring. Subsequent mating partners have developed various counterstrategies to mitigate mating order effects.     

A novel postcopulatory block of reproduction in white-footed mice

Female white-footed mice (Peromyscus leucopus) fail to produce offspring when paired with a male from weaning until 150 days of age if an adult female or her odor is also present. The present study delineates more clearly which stage of the young female's reproductive cycle is inhibited by the chemosignal of the older female. Age at vaginal opening and first estrus are delayed by the presence of the older female, but only for about 10 days. The presence of a male counteracts this delay. Thus, the basis for the block is not a delay in puberty. The older female's presence does not influence the number of estrous cycles experienced during the 30 days following first estrus, nor does it influence the number of corpora lutea found at autopsy. The presence of sperm in the vaginae of young females indicates that they were copulating. Likewise, examination of embryos 2 and 3 days after copulation reveals normal developmental progress. However, implantation does not occur in young females that have been exposed to an adult female. Thus, the block occurs either during the final stages of embryo transport or in relation to the implantation process itself.     

Estrous cycle effects on behavior of C57BL/6J and BALB/cByJ female mice: implications for phenotyping strategies

Systematic behavioral phenotyping of genetically modified mice is a powerful method with which to identify the molecular factors implicated in control of animal behavior, with potential relevance for research into neuropsychiatric disorders. A number of such disorders display sex differences, yet the use of female mice in phenotyping strategies has been a rare practice because of the potential variability related to the estrous cycle. We have now investigated the behavioral effects of the estrous cycle in a battery of behavioral tests in C57BL/6J and BALB/cByJ inbred strains of mice. Whereas the performance of BALB/cByJ female mice varied significantly depending on the phase of the estrous cycle in the open field, tail flick and tail suspension tests, the behavior of C57BL/6J females, with the exception of the tail suspension performance, remained stable across all four phases of the estrous cycle in all of the tests including open field, rotarod, startle reflex and pre-pulse inhibition, tail flick and hot plate. We also found that irrespective of the estrous cycle, the behavior of C57BL/6J females was different from that of BALB/cByJ groups in all of the behavioral paradigms. Such strain differences were previously reported in male comparisons, suggesting that the same inter-group differences can be revealed by studying female or male mice. In addition, strain differences were evident even for behaviors that were susceptible to estrous cycle modulations, although their detection might necessitate the constitution of large experimental groups.     

Orienting behavior of female white rats in estrus cycle and its dependence on handling

Characteristics of orienting behavior of intact and handled female white rats were studied in the "open field" test. Experimental group of animals were formed according to stages of estrous cycle: (1) diestrus, (2) proestrus, (3) estrus, and (4) metestrus. The stage of the cycle was determined by vaginal smears. Over the period of 10 days rats were handled daily for 5 minutes. No behavioral changes over the course of estrous cycle were found in intact rats. Handling revealed some behavioral features related to the levels of steroid hormones in reproductive cycle. Most prominent changes in orienting behavior were observed at transition from estrous to metestrous. At the stage of estrous motor activity was maximal and grooming was minimal. The maximal contrast in the structure of orienting behavior was observed between estrous and diestrous stages.     

圈养小熊猫繁殖行为变化及繁殖行为对策

In order to investigate the change of reproductive behaviors and understand reproductive strategies of both male and female red pandas, one-year behavioral observation was conducted through the focal sampling method in the Chengdu Research Base of Giant Panda Breeding from December 1999 to November 2000. Our results indicated that reproductive behaviors showed significant differences between the estrous and non-estrous seasons. Frequencies of the rubbing anogenital, sniffing and licking marking were much higher in estrus than in non-estrus. Bleating only appeared in the estrus and can be regarded as an estrous indicator.The result also demonstrated that both male and females applied different reproductive behavioral strategies. Frequencies of activity, rubbing anogenital, licking and sniffing marking, and bleat were much higher in the male than in the female. However, those of resting and investigating were much lower in the male than in the female. This indicated that the male was more active than the female during the estrus and might imply that the male acts mainly as an estrous message sender, and the female as a message receiver in the estrous season.     

Effect of a 20 kHz sawtooth magnetic field exposure on the estrous cycle in mice

Female mice post weaning were exposed to 20 kHz sawtooth electric and magnetic fields (EMF) with 6.25 microT peak intensity for 6 weeks. Estrous cycles were checked using vaginal smears over the last 10 days of the experimental period. The vaginal smears from EMF-exposed mice revealed an increase in the frequency of one or two phases persisting. The number of estrous cycles less than 1 was more in the EMF-exposed group than in the sham control group. Furthermore, in the EMF-exposed group, the duration of proestrous and metestrous stages of the estrous cycle was significantly increased compared with the control group. In conclusion, our results suggest that exposure to 20 kHz sawtooth EMF may affect normal cycling of the estrous cycle by disrupting the female reproductive endocrine physiology. We should not disregard the possible adverse reproductive effect of the 20 kHz sawtooth EMF generated under the occupational exposure situation in females.     

Olfactory bulb cells generated in adult male golden hamsters are specifically activated by exposure to estrous females

Two experiments were carried out to test whether cells which are born in adulthood and migrate to the olfactory bulb of adult male golden hamsters are activated during sexual behaviors, to determine the time course over which such responsiveness appears, and to ask whether activation is specific to sexual cues. In the first experiment, adult male hamsters were injected with 5'-bromodeoxyuridine (BrdU, 50mg/kg b.w.) 3 times over the course of one week in order to mark dividing cells. Ten days, three weeks, or seven weeks after the first BrdU injection, the animals were allowed to mate with an estrous female for half an hour before being sacrificed. Confocal analysis of fluorescent immunostaining of BrdU and c-Fos first revealed dual labeled cells in the olfactory bulb 3 weeks after injection of the thymidine analog. In order to determine whether the activation of these newly generated cells is specific to sexual cues, we next compared the incidence of c-Fos expression in newborn (BrdU positive) cells among male hamsters exposed to an estrous female, an aggressive male, a cotton swab containing vaginal secretion from an estrous female hamster (FHVS), a cotton swab containing peppermint, or a cotton swab containing distilled water. In the mitral and glomerular layers of the accessory olfactory bulb, animals exposed to an estrous female had significantly more double labeled cells than did those given other treatments (p < 0.01). In the mitral layer of the main bulb, animals exposed to an estrous female had a significantly higher percentage of double labeled cells than those of other groups, except those exposed to an aggressive male (p < 0.05). No double labeled cells were seen in medial preoptic area (MPOA), medial nucleus of the amygdala (Me), the bed nucleus of the stria terminalis (BNST), or the hypothalamus. Our results indicate that cells born in adulthood are more responsive to cues arising from estrous females than other stimuli, and thus may participate in sociosexual behaviors.     

Fitness effects of female mate choice: preferred males are detrimental for Drosophila melanogaster females

The evolution of female mate choice, broadly defined to include any female behaviour or morphology which biases matings towards certain male phenotypes, is traditionally thought to result from direct or indirect benefits which females acquire when mating with preferred males. In contrast, new models have shown that female mate choice can be generated by sexual conflict, where preferred males may cause a fitness depression in females. Several studies have shown that female Drosophila melanogaster bias matings towards large males. Here, we use male size as a proxy for male attractiveness and test how female fitness is affected by reproducing with large or small males, under two different male densities. Females housed with large males had reduced lifespan and aged at an accelerated rate compared with females housed with small males, and increased male density depressed female fitness further. These fitness differences were due to effects on several different fitness components. Female fitness covaried negatively with male courtship rate, which suggests a cost of courtship. Mating rate increased with male size, whereas female fitness peaked at an intermediate mating rate. Our results suggest that female mate choice in D. melanogaster is, at least in part, a by-product of sexual conflict over the mating rate.     

Fertile women evaluate male bodies as more attractive,regardless of masculinity

Ovulatory cycle shifts in women's mate preferences have been documented for several physical and behavioral traits. Research suggests that, at peak fertility, women tend to prefer men with characteristics that reflect good genes for short-term sexual relationships. However, existing findings have been criticized for methodological flexibility and failing attempts to replicate core results. In a large (N = 157), pre-registered, within-subject study spanning two ovulatory cycles, we investigated cycle shifts in women's mate preferences for masculine bodies. Using a large set of natural stimuli, we found that when fertile, women's ratings of male bodies increased for sexual as well as for long-term attractiveness. Both effects were partially mediated by the estradiol-to-progesterone-ratio. Furthermore, moderation analyses revealed that both shifts were only evident in women in relationships, but not in singles. Contrary to previous findings, male masculine traits did not interact with cycle phase to predict attraction, indicating that women's preferential priorities do not shift. Taken together, our results do not support women's mate preference shifts, as assumed by the good genes ovulatory shift hypothesis, but are consistent with shifting motivational priorities throughout the cycle. Implications of these results for female estrus theories and methodological recommendations for future research are discussed.     

Hormonal regulation of chemosignal-stimulated precopulatory behaviors in male housemice (Mus musculus)

Five experiments examined the hormonal regulation of the precopulatory reproductive behavior of male housemice of two genotypes (DBA/2J inbreds and C57BL/6J X AKR/J hybrids). The two precopulatory behaviors examined were preferences for female urinary odors and ultrasonic courtship vocalizations to anesthetized females. The preferences were then used to make inferences about odor attractiveness. Gonadally intact hybrid males were highly attracted to the airborne urinary odors of female mice but were either indifferent to, or exhibited less attraction to, male urinary odors. Castration decreased male attraction to female odor such that castrated males were equally attracted to male and female odors. Normal levels of attraction could be maintained in castrated hybrid males by Silastic implants of either testosterone or estradiol. While Silastic implants of dihydrotestosterone (DHT) were also effective in maintaining attraction in hybrids, this hormone was ineffective in inbreds. The effectiveness of estradiol, DHT, and testosterone in maintaining attraction following castration was paralleled in castrated hybrids by the effects of these hormones in maintaining courtship vocalizations to females. In contrast to the genotype-specific effects of DHT upon behavior, DHT was effective in both genotypes in maintaining seminal vesicle weight. Estradiol, on the other hand, which was quite effective in maintaining both precopulatory behaviors in hybrids, had little effect upon seminal vesicle weight. Thus these experiments dissociate the behavioral effects of steroids from their effects upon peripheral morphology. We suggest that testosterone can activate precopulatory behaviors following either aromatization or 5-alpha reduction but that genetic variability somehow gives rise to strain differences in DHT responsiveness.     

Puberty onset in the female offspring of rats submitted to protein or energy restricted diet during lactation

This study aims to determine the effects of maternal protein and energy malnutrition during lactation on the linear growth, body weight and onset of puberty of the female offspring. At parturition, dams were randomly assigned to the following groups: (C) control group, with free access to a standard laboratory diet containing 23% protein; (PR) protein-restricted group, with free access to an isoenergy and protein-restricted diet containing 8% protein; and (ER) energy-restricted group, receiving standard laboratory diet in restricted quantities. After weaning, the female pups had free access to standard laboratory diet. From day 30 onwards, the pups were inspected daily for vaginal opening. Cyclic stages of the ovaries were studied by daily vaginal smears after vaginal opening until day 40 when all animals were sacrificed with pentobarbital. From day 4 after birth until day 40, body weight and linear growth in the PR and ER rats were significantly lower than in controls (p < 0.001). In spite of the significant (p<0.05) delayed in the vaginal opening in PR and ER rats, the first estrous cycle occurred at the same time of vaginal opening in all groups. The PR and ER rats exhibited a lower uterine (PR = 42%, ER = 40%, p < 0.001) and ovarian (PR = 26%, ER=19%, p < 0.05) absolute weight and uterus relative weight (PR = 27%, ER = 22%, p < 0.05). Our data showed that maternal protein and energy malnutrition during lactation leads to growth retardation and delayed on the onset of puberty in female pups, with vaginal opening and estrous cycle occurring at the same time.     

Effects of neonatal treatment with phytoestrogens, genistein and daidzein, on sex difference in female rat brain function: estrous cycle and lordosis

It is well known that neonatal exposure to estrogen induces masculinization or defeminization of the brain. In this study, the effects of neonatal treatment with two kinds of soybean isoflavone aglycone, genistein (GS) and daidzein (DZ), on the estrous cycle and lordosis behavior were investigated. Female rats were injected subcutaneously with 1 mg GS, 1 mg DZ, 100 microg estradiol (E2), or oil daily for 5 days from birth. As a result, vaginal opening was advanced in GS- or E2-treated females. A vaginal smear check indicated that oil- or DZ-treated females showed a constant 4- or 5-day estrous cycle, whereas GS- or E2-treated rats showed a persistent or prolonged estrus. Ovariectomy was performed in all females at 60 days of age. The ovaries in the GS- or E2-treated groups were smaller than those in the oil- and DZ-treated groups and contained no corpora lutea. In the DZ group, although corpora lutea were seen, ovaries were smaller than that of control females. Behavioral tests were carried out after implantation of E2-tubes. All of the oil- or DZ-treated females showed lordosis with a high lordosis quotient (LQ). On the other hand, as male rats, LQs were extremely low in the E2-treated group, when compared to the oil-treated group. In the GS-treated group, the mean LQ was lower than that in the oil-treated group, but higher than those in the E2-treated female or male groups. These results suggest that genistein acts as an estrogen in the sexual differentiation of the brain and causes defeminization of the brain in regulating lordosis and the estrous cycle in rats. In addition, neonatal daidzein also has some influence on ovarian function.