Endocrine changes in male stumptailed macaques (Macaca arctoides) as a response to odor stimulation with vaginal secretions

In mammalian species, social chemosignals are important in modulating endocrine reproductive functions. In nonhuman primates, previous studies have described a high frequency of mounting behavior by females in the follicular and periovulatory phases of the menstrual cycle. Stumptailed macaque females do not signal receptivity by means of sexual swellings, as do others macaques, therefore providing a good model in which to study chemical signaling of reproductive status. We exposed anesthetized stumptailed males to vaginal secretions of either late follicular or menses phase or to saline solution to determine the endocrine changes promoting male sexual behavior. In males exposed to follicular secretions, plasma testosterone concentrations were sustained up to 120 min after exposure. Such an effect was not observed in animals exposed to menses or saline odor sources. A luteinizing hormone surge, occurring 30 minutes after exposure to late follicular phase secretion swabs, preceded this sustained testosterone effect. The fact that late follicular scents induce sustained testosterone concentrations provides support to the idea that stumptailed males draw information concerning female reproductive status from the female's vaginal odor.     

Chemical communication of reproductive status in female cotton-top tamarins (Saguinus oedipusoedipus)

Among Callitrichids, scent secretions have been identified as carrying information regarding species, subspecies, gender, social status, individuality, hormonal status, and timing of ovulation. We propose that information regarding familiarity and reproductive status is also communicated. Seven male–female pairs of cotton-top tamarins (Saguinus oedipus oedipus) were presented with several drops of distilled water, a scent secretion from the female of that pair, scent secretions from unfamiliar, reproductively mature but noncycling females, and scent secretions from unfamiliar, reproductively cycling females. Behavioral responses from both males and females were recorded over a 10 min period. Differences in behavioral response for both males and females were significant across all four conditions. This indicates that cotton-top tamarins are capable of discriminating a familiar scent from an unfamiliar scent as well as the reproductive status of an unfamiliar female. The communication of this information may play an important role in regulating mate selection, reducing reproductive competition, and stabilizing transfers in and out of groups in the wild. Am. J. Primatol. 45:337–349, 1998. © 1998 Wiley-Liss, Inc.     

Assessment of female reproductive status by male longtailed macaques, Macaca fascicularis, under natural conditions

Recent theories on primate sexual selection have paid increasing attention to the importance of reproductive strategies of females living in multimale groups. However, the extent to which females are able effectively to conceal or advertise the time of ovulation as part of these strategies remains unclear. Few studies have investigated the ability of males to discern female reproductive status under natural conditions, and none has taken into account differences in male rank, and thus ability to gain access to females or cues. We tested male assessment of a female's fertile phase under natural conditions in longtailed macaques. We used timing of mate guarding by dominant males and the response of subordinate males towards the repeated playback of a female copulation call to measure male interest in females throughout the ovarian cycle. Relating the degree of male interest to female reproductive status, as determined noninvasively by faecal hormone analysis, we found that interest in females shown by both dominant and subordinate males was strongest during and around the fertile phase. Our results also indicate that males were better able to recognize the fertile period in conception than in nonconception cycles. Furthermore, our finding of a strong positive relation between male interest and female oestrogen levels in all cycles indicates that at least some of the cues used by males to assess female reproductive status are oestrogen related.     

The effects of oestrous condition and familiarity on the sexual behaviour of polecats (Mustela putorius and M. fur × M. putorius hybrids)

The effects of two factors on the sexual behaviour of polecats ( Mustela furo and M. putorius × M. furo hybrids) were investigated, in an indoor arena of 16 m², firstly the oestrous condition of the female and secondly the familiarity of the two individuals.
The initial approaches of a male polecat are similar irrespective of the oestrous condition of the female but his subsequent behaviour is dependent upon the female's response. Whereas males copulated with oestrous females they showed a wider repertoire of social acts and a greater number of changes of behaviour towards females which were not in oestrous. Unreceptive females elicited both sexual and aggressive behaviour from males.
Unfamiliar females provide a more powerful eliciting stimulus for the male's copulatory behaviour than do familiar females.     

Male chimpanzees' grooming rates vary by female age, parity, and fertility status

Copulation preferences in our closest living relative, the chimpanzee, suggest that males prefer older females who have had previous offspring. However, this finding is counter to some behavioral models, which predict that chimpanzee males, as promiscuous breeders with minimal costs to mating, should show little or no preference when choosing mating partners (e.g. should mate indiscriminately). To determine if the preferences indicated by copulations appear in other contexts as well as how they interact, we examined how male chimpanzees' grooming patterns varied amongst females. We found that males' preferences were based on interactions among females' fertility status, age, and parity. First, grooming increased with increasing female parity. We further found an effect of the estrous cycle on grooming; when females were at the lowest point of their cycle, males preferentially groomed parous females at peak reproductive age, but during maximal tumescence, males preferred the oldest multiparous females. Nulliparous females received relatively little grooming regardless of age or fertility. Thus, male chimpanzees apparently chose grooming partners based on both female's experience and fertility, possibly indicating a two-pronged social investment strategy. Male selectivity seems to have evolved to effectively distribute costly social resources in a pattern which may increase their overall reproductive success.     

Social regulation of plasma estradiol concentration in a female anuran

The behavior of an individual within a social aggregation profoundly influences behavior and physiology of other animals within the aggregation in such a way that these social interactions can enhance reproductive success, survival and fitness. This phenomenon is particularly important during the breeding season when males and female must synchronize their reproductive efforts. We examined whether exposure to conspecific social cues can elevate sex steroid levels, specifically estradiol and androgens, in female túngara frogs (Physalaemus pustulosus). We compared plasma estradiol and androgen concentrations in wild-caught females before and after exposure to either natural mate choruses or random tones. After exposure to mate choruses for 10 consecutive nights, estradiol concentrations were significantly elevated whereas there was no significant elevation in estradiol concentrations in the group of females exposed to random tones for 10 nights. Plasma androgen concentrations were not significantly changed after exposure to either natural mate choruses or random tones for 10 consecutive nights. Social modulation of estradiol concentrations may be important in maintaining a female's reproductive state while males are chorusing. To our knowledge, this is the first study to demonstrate social regulation of estradiol concentration in female anurans.     

Contextual determinants of female-female mounting in laboratory rats

Female-female mounting is widespread among mammalian species, but little is known about the proximal function of this behaviour. While such mounting is often regarded as a 'masculine' trait, its widespread occurrence may indicate that it serves specific functions within the context of female-female social behaviour. We valuated female mounting behaviour in Long-Evans rats in standard observation chambers and in a seminatural enclosure. Under these conditions, we examined a number of potential factors that might influence mounting, including the oestrous cycle, social hierarchy, familiarity and male presence. The female's mounting was not influenced by her own oestrous cycle, but did vary with the oestrous cycle of the stimulus female. Socially dominant females mounted significantly more than subordinate females, and mounting by the dominant female was most frequent when the subordinate female was sexually receptive. Females mounted (and fought with) unfamiliar females significantly more than they did with familiar cagemates. Female-female mounting was dramatically reduced when males were present. Further testing showed that female mounting did not affect the induction of the progestational state of pregnancy, suggesting that female mounting does not function as a pseudomale behaviour that can substitute for genital stimulation provided by the male. Based on these data, female mounting does not appear to function as a sexual behaviour per se, but may serve as a form of female social behaviour related to maintenance of the female's social status within female groups. In this regard, the results of this study suggest that female mounting is part of the normal female's complex behavioural repertoire and does not necessarily reflect masculinization of some underlying neural substrate. Copyright 1999 The Association for the Study of Animal Behaviour.     

Smelling wrong: hormonal contraception in lemurs alters critical female odour cues

Animals, including humans, use olfaction to assess potential social and sexual partners. Although hormones modulate olfactory cues, we know little about whether contraception affects semiochemical signals and, ultimately, mate choice. We examined the effects of a common contraceptive, medroxyprogesterone acetate (MPA), on the olfactory cues of female ring-tailed lemurs (Lemur catta), and the behavioural response these cues generated in male conspecifics. The genital odorants of contracepted females were dramatically altered, falling well outside the range of normal female variation: MPA decreased the richness and modified the relative abundances of volatile chemicals expressed in labial secretions. Comparisons between treatment groups revealed several indicator compounds that could reliably signal female reproductive status to conspecifics. MPA also changed a female''s individual chemical ‘signature’, while minimizing her chemical distinctiveness relative to other contracepted females. Most remarkably, MPA degraded the chemical patterns that encode honest information about genetic constitution, including individual diversity (heterozygosity) and pairwise relatedness to conspecifics. Lastly, males preferentially investigated the odorants of intact over contracepted females, clearly distinguishing those with immediate reproductive potential. By altering the olfactory cues that signal fertility, individuality, genetic quality and relatedness, contraceptives may disrupt intraspecific interactions in primates, including those relevant to kin recognition and mate choice.     

Chemosensory cues allow male Tenebrio molitor beetles to assess the reproductive status of potential mates

Males of many insect species, including beetles, choose their mates according to their reproductive status. However, the ways in which male beetles evaluate female reproductive status have received little attention. We tested the existence of male mate choice in the mealworm beetle, Tenebrio molitor, by observing mating and courtship behaviour of males given simultaneous access to pairs of females differing in their reproductive status: (1) mature versus immature; (2) virgin versus previously mated; (3) familiar (mated with the experimental male) versus unfamiliar (mated with a different male). Males courted and mated preferentially with mature and virgin females. To determine whether chemical cues played a role in these discriminations, we exposed males to filter paper squares bearing chemical cues from different types of females: (1) virgin versus mated; (2) mature versus immature. Males were significantly more attracted to those squares bearing chemical cues from virgin and mature females, suggesting that males can assess female reproductive status on the basis of chemical cues alone.     

Familiarity adds to attractiveness in matters of siskin mate choice

There is currently considerable controversy in evolutionary ecology revolving around whether social familiarity brings attraction when a female chooses a mate. The topic of familiarity is significant because by avoiding or preferring familiar individuals as mates, the potential for local adaptation may be reduced or favoured. The topic becomes even more interesting if we simultaneously analyse preferences for familiarity and sexual ornaments, because when familiarity influences female mating preferences, this could very significantly affect the strength of sexual selection on male ornamentation. Here, we have used mate-choice experiments in siskins Carduelis spinus to analyse how familiarity and patterns of ornamentation (i.e. the size of wing patches) interact to influence mating success. Our results show that females clearly prefer familiar individuals when choosing between familiar and unfamiliar males with similar-sized wing patches. Furthermore, when females were given the choice between a highly ornamented unfamiliar male and a less ornamented familiar male, half of the females still preferred the socially familiar birds as mates. Our finding suggests that male familiarity may be as important as sexual ornaments in affecting female behaviour in mate choice. Given that the potential for local adaptation may be favoured by preferring familiar individuals as mates, social familiarity as a mate-choice criterion may become a potential area of fruitful research on sympatric speciation processes.     

Oestrous state dynamics in chemical communication by captive female Asian elephants

In many mammals, reproductive status is revealed through chemical cues in urine. The reproductive status of receivers may influence their interest in such signals. For social mammals that live in matrilineal groups, females may benefit by detecting the reproductive condition of herdmates. Responses to urine during oestrous cycles of senders and receivers are potential indicators of signal functions. We examined the chemosensory responses, first by four captive female Asian elephants,Elephas maximus , over their oestrous cycles to familiar follicular and luteal phase urine and second by 14 different female Asian elephants to unfamiliar conspecific follicular and luteal phase urine. We asked whether females could distinguish the reproductive state of another female as measured by their differential response to luteal- and follicular-phase urine. We further examined the influence of the receiver's reproductive status on response levels. Females responded more with specific tactolfactory trunk behaviours to follicular- than to luteal-phase urine, but only when the receiving female was in her follicular phase. Like their male conspecifics, Asian elephant females can detect changes in the reproductive state of conspecifics. The functional significance of this ability has yet to be determined but may be related more to the resource holding power of females in follicular phase than to a means for females to synchronize oestrous cycles. Such female-female communication may have important effects on social group dynamics. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

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

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

Males adjust their signalling behaviour according to experience of male signals and male–female signal duets

Sexual signals are conspicuous sources of information about neighbouring competitors, and species in which males and females signal during pair formation provide various sources of public information to which individuals can adjust their behaviour. We performed two experiments with a duetting vibrational insect, Enchenopa binotata treehoppers (Hemiptera: Membracidae), to ask whether males adjust their signalling behaviour according to (1a) their own experience of competitors' signals, (1b) how females adjust their mate preferences on the basis of their experience of male signals (described in prior work), and/or (2) their own experience of female response signals to competitors' signals. We presented males with synthetic male signals of different frequencies and combinations thereof for 2 weeks. We recorded males a day after their last signal exposure, finding that (1a) male signal rate increased in response to experience of attractive competitors, but that (1b) male signal frequency did not shift in a manner consistent with how females adjust their mate preferences in those experience treatments. Second, we presented males with different male–female duets for 2 weeks, finding that (2) male signal length increased from experience of female duets with attractive competitors. Males thus make two types of adjustment according to two sources of public information: one provided by experience of male signals and another by experience of female responses to male signals. Signalling plasticity can generate feedback loops between the adjustments that males and females make, and we discuss the potential consequences of such feedback loops for the evolution of communication systems.     

Honesty of a dynamic female aggressive status signal: baseline testosterone relates to bill color in female American goldfinches

Status signals are linked to fighting ability and enable competitors to gain access to resources without risking injury in aggressive combat. The relationship between testosterone (T), a hormone that mediates aggression, and signals of status is well studied in males, but little is known about the relationship between T and female signals of status. Female and male American goldfinches Spinus tristis express a dynamic carotenoid‐based orange bill color during the breeding season and previous work has demonstrated that females use orange bill color to communicate competitive ability during intrasexual competition. We test the hypothesis that female bill color reflects baseline T, which would allow receivers to directly assess a competitor's aggressive potential. We found a positive relationship between T and bill coloration in females, indicating that bill color has the ability to signal female competitive status. This finding is consistent with the hypothesis that female bill color is a reliable signal of fighting ability, and indicates that females, like males, may use coloration to signal their hormonally mediated aggressive potential.     

Influence of male gonadal hormones and familiarity on pregnancy interruption in prairie voles

Pregnancy interruption (PI) was examined in female prairie voles, Microtus ochrogaster, exposed to stimuli from males 7 to 12 days after pairing. Urine from unfamiliar males interrupted pregnancy when placed directly on the external nares of newly mated females, but urine from familiar stud males was without effect. Castration of males did not reduce the efficacy of unfamiliar male urine in interrupting pregnancy. The neuroendocrine system of female prairie voles responded selectively to male urine as a function of its familiarity; the efficacy of male stimuli leading to PI was not dependent on gonadal hormones.     

Independent effects of song quality and experience with photostimulation on expression of the immediate,early gene ZENK (EGR‐1) in the auditory telencephalon of female European starlings

Age influences behavioral decisions such as reproductive timing and effort. In photoperiodic species, such age effects may be mediated, in part, by the individual's age‐accrued experience with photostimulation. In female European starlings (Sturnus vulgaris) that do not differ in age, experimental manipulation of photostimulation experience (photoexperience) affects hypothalamic, pituitary, and gonadal activity associated with reproductive development. Does photoexperience also affect activity in forebrain regions involved in processing a social cue, the song of males, which can influence mate choice and reproductive timing in females? Female starlings prefer long songs over short songs in a mate‐choice context, and, like that in other songbird species, their auditory telencephalon plays a major role in processing these signals. We manipulated the photoexperience of female starlings, photostimulated them, briefly exposed them to either long or short songs, and quantified the expression of the immediate‐early gene ZENK (EGR‐1) in the caudomedial nidopallium as a measure of activity in the auditory telencephalon. Using an information theoretic approach, we found higher ZENK immunoreactivity in females with prior photostimulation experience than in females experiencing photostimulation for the first time. We also found that long songs elicited greater ZENK immunoreactivity than short songs did. We did not find an effect of the interaction between photoexperience and song length, suggesting that photoexperience does not affect forebrain ZENK‐responsiveness to song quality. Thus, photoexperience affects activity in an area of the forebrain that processes social signals, an effect that we hypothesize mediates, in part, the effects of age on reproductive decisions in photoperiodic songbirds. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 2009     

Female reproductive decisions and parasite burden in a calopterygid damselfly (Insecta: Odonata)

There is currently a gap in sexual selection theory about how much the environment drives female mating decisions. We present field data that suggest that female sexual behaviour in the damselfly Calopteryx haemorrhoidalis is influenced by parasite burden. Male wing pigmentation in Calopteryx is a sexually selected trait that signals a male's ability to cope with eugregarine parasites (an intestinal parasite that feeds on the adult's ingested food). Because adult C. haemorrhoidalis females also show wing pigmentation, we examined whether this trait is similarly influenced by parasite burden and whether it may signal the female's reproductive value. MaleC. haemorrhoidalis defend riverine substrates that females use for oviposition. After copulation and during oviposition, females are guarded by the copulating male against intruder males. Alternatively, females may avoid mating and ‘steal’ an oviposition site within a male's territory. In the present study, we found that the amount of female wing pigmentation was negatively correlated with the number of eugregarines present. Females with more parasites produced fewer eggs, survived fewer days, spent less time during courtship, ‘inspected’ fewer males before mating, had a lower mating success, were guarded for less time during oviposition and engaged in fewer ‘stealing’ events during oviposition. The reduced egg production and survival of heavily infected females may result from eugregarine depletion of the females' consumed food reserves. Thus, to offset reduced longevity, heavily infected females may accept a mating more rapidly and mate with fewer males. ‘Stealing’ behaviour may be related to the female's differential use of sperm from some males, particularly high-quality males. Interestingly, males that mated with low-pigmented females showed greater variance in wing pigmentation than did males that mated with high-pigmented females. Possibly, female wing pigmentation may signal a female's reproductive value, which provides females with longer mate-guarding episodes and reduced interference from intruder males. This study points out one possible constraint, intestine parasites, that females may face during mating decisions. Because females in bad condition mate with males in both good and bad condition, this constraint may be pervasive enough to weaken the intensity of selection for a male sexually selected trait, wing pigmentation, and help to maintain its variation in phenotypic expression. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Importance of pause between spider courtship vibrations and general problems using synthetic stimuli in behavioural studies

Effectiveness of natural stimuli (recorded and replayed male vibratory courtship signals) in eliciting a female's vibratory response was compared with that of synthetic stimuli in a plant-dwelling spider (Cupiennius salei). Specifically, the role of interseries (pauses between consecutive male series) was evaluated. Effectiveness was assessed by the number of responding females and the number of responses per female per stimulus. In case of both synthetic and natural stimuli, effectiveness increases with increasing duration of interseries in both measures. Interseries are thus represented in the female's innate releasing mechanism. However, synthetic stimuli are less effective (about 55%) than natural stimuli (set 100%). With decreasing interseries, the number of female responses per unit time sharply increases in case of playback of natural stimuli, but only slightly in case of synthetic stimuli. Since males courting on plants decrease interseries as soon as a female responds, thus facilitating their orientation, the data obtained with natural stimuli much better fit natural male courtship behaviour. This finding brings into question the validity of the synthetic stimulus. In the bioacoustics literature there is neither consensus on the effectiveness of a synthetic stimulus necessary to qualify it for behavioural analysis nor on how to measure effectiveness. We propose three measures : the percentage of responding animals, the action pattern of the response and the number of responses. It may be crucial, particularly when addressing evolutionary questions, to use either natural stimuli or synthetic stimuli (nearly) as effective as natural stimuli to avoid biased sampling of experimental animals and results difficult to interpret in biological terms.     

Testing for links between face color and age,dominance status,parity, weight,and intestinal nematode infection in a sample of female Japanese macaques

Studies of the role of secondary sexual ornaments in mate choice tend to focus on colorful traits in males, but females of many animal species express colorful ornamentation too. Among non-human primates, investigations into the role of female secondary sexual traits as indicators of life history characteristics, reproductive success, and health status have mostly focused on sexual swellings, whereas only few studies have been conducted on the role of facial color. Recent studies on rhesus macaques and mandrills suggested that female ornamentation might provide information about female life history characteristics, but not on disease resistance factors and parasite infection, which have been shown to affect male ornamentation in some non-primate species. In Japanese macaques (Macaca fuscata), females have brightly colored faces that are indicative of their reproductive status. Here, we aimed to determine whether female facial color might also convey information about age, dominance rank, parity, weight, and intestinal nematode infection in free-ranging individuals. We analyzed whether female facial parameters (luminance and redness) were linked to these individual characteristics, using digital photography and data on intestinal parasite infection collected systematically during 1 month for each of seven free-ranging females. We found no evidence to suggest that female facial color is an indicator of any of these measures in Japanese macaques. Considering our small data set, it is still preliminary to draft any clear conclusions. Future studies combining digital, hormonal, parasitological and behavioral data are needed to assess the possible role of female face color on male preferences and mating choice in Japanese macaques.     

Fishy Aroma of Social Status: Urinary Chemo-Signalling of Territoriality in Male Fathead Minnows (Pimephales promelas)

Chemical structures of several urinary reproductive pheromones in fish have been identified, and their role in the chemical communication of reproductive condition is well characterized. On the contrary, the role of chemical communication in signalling of social/territorial status in fish is poorly understood. Fathead minnows are an example of a fish species whose life history traits appear conducive to evolution of chemical communication systems that confer information about social/territorial status. Male reproduction in this species is dependent upon their ability to acquire and defend a high quality nesting territory, and to attract a female to the nest. We hypothesized that fathead minnow males use visual and urine-derived chemical cues to signal territorial status. To test this hypothesis, effects of territorial acquisition on male-specific secondary sex characteristics (SSCs) and urine volumes were first assessed. Second, frequencies of male urination in varying social contexts were examined. Finally, nuclear magnetic resonance-based metabolomics was used to identify urinary metabolites that were differentially excreted in the urine of territorial versus non-territorial males. The expression of SSCs, sperm, and urine volumes increased with territory acquisition, and either remained unchanged or decreased in non-territorial males. Frequency of male urination increased significantly in the presence of females (but not males), suggesting that females are the main target of the urinary signals. Territorial and non-territorial males had distinct urinary metabolomic profiles. An unforeseen finding was that one could discern future territorial status of males, based on their initial metabolomic profiles. Bile acids and volatile amines were identified as potential chemical signals of social status in the fathead minnow. The finding that trimethylamine (a fishy smelling volatile amine) may be a social cue is particularly interesting, because it is known to bind trace amine-associated receptors, indicating that these receptors may play role in chemical signalling of social status in fish.