Female Odors Research Articles

A GnRH neuronal population in the olfactory bulb translates socially relevant odors into reproductive behavior in male mice.

Hypothalamic gonadotropin-releasing hormone (GnRH) neurons regulate fertility and integrate hormonal status with environmental cues to ensure reproductive success. Here we show that GnRH neurons in the olfactory bulb (GnRHOB) of adult mice can mediate social recognition. Specifically, we show that GnRHOB neurons extend neurites into the vomeronasal organ and olfactory epithelium and project to the median eminence. GnRHOB neurons in males express vomeronasal and olfactory receptors, are activated by female odors and mediate gonadotropin release in response to female urine. Male preference for female odors required the presence and activation of GnRHOB neurons, was impaired after genetic inhibition or ablation of these cells and relied on GnRH signaling in the posterodorsal medial amygdala. GnRH receptor expression in amygdala kisspeptin neurons appear to be required for GnRHOB neurons' actions on male mounting behavior. Taken together, these results establish GnRHOB neurons as regulating fertility, sex recognition and mating in male mice.

Effect of dietary phospholipid on the behavior in C57BL/6J mice

Nowadays phospholipids are widely used as hepatoprotective, neuroprotective and anti-stress drugs, as well as the dietary supplements. Besides, lecithin consisting up to 70% of the phospholipids mixture: phosphatidylcholine, phosphatidylethanolamine, phosphatidylinositol and phosphatidic acid, is the often component of food production as an emulsifier. Dose of these biologically active substances in the modern human diet could be quite high. Previously we have shown that chronic intestinal inflammation in Muc2-knockout mice induces behavioral changes along with the significant increase in the content of phospholipids in intestinal epithelial cells, particularly, phosphatidylcholine, phosphatidylserine and phosphatidic acid. Here we investigate the effects of long-term administration of a mixture of these phospholipids, as well as the effects of long-term administration of soy lecithin on the behavioral patterns in laboratory mice. Animals long-term taken a phospholipid mixture shows no normally observed preference towards females in the two intruders test (with female and male). In the social odor preference test, they also did not distinguish female and male odors, while non-social odors discrimination preserved. In addition, we identified a decrease in anxiety, obsessive traits, and schizophrenia-like behavior traits in these animals. Soy lecithin supplementation had similar effects on social behavior and compulsive traits, and increased aggression in males. Thus, long-term perinatal administration of either mixture of phospholipids (phosphatidylcholine, phosphatidylserine and phosphatidic acid) or soy lecithin can influence various aspects of behavior in mice.

Chemical Characterization of Human Body Odor Headspace Components

This study focused on evaluating human body odor volatiles using a chamber approach. Ten participants were asked to sit inside the chamber for 1 h, while using SPME as the extraction technique for vapor sampling. A total of 105 compounds were detected across participants, with nonanal having the highest frequency. PCA statistical analysis depicted tighter clustering in female whole-body odor profiles when compared to males, thus corroborating gender odor differences. Concurrently, various biospecimens (hand, axillary, breath) from the same participants allowed for a comparison between whole-body and individual biospecimen odor signatures. When comparing whole-body sampling and distinctive biospecimens, nonanal and decanal were the only odor volatiles shared. Statistical clustering depicted higher similarity within the odor profiles of individual biospecimens compared to odor profiles of the whole body, indicating distinctiveness of the odor chemical landscape as a function of sampling region. Overall, this study demonstrated that SPME-GC/MS methodology was successful in the extraction, detection, and identification of previously reported human scent volatiles when employing the human chamber for whole-body sampling. Our presented testing paradigm allows for a direct comparison of odor volatiles across the full body and specific body locations that allows odor markers to be furthered exploited for diagnostic and biological detection contexts.

Exposure to female olfactory cues hastens reproductive ageing and increases mortality when mating in male mice.

Theories of ageing predict that investment in reproduction will trade-off against survival and later-life reproduction. Recent evidence from invertebrates suggests that just perceiving cues of a potential mate's presence can reduce lifespan, particularly in males, and that activation of neuroendocrine reward pathways associated with mating can alleviate these effects. Whether similar effects occur in vertebrates remains untested. We tested whether exposure to olfactory cues from the opposite sex would influence mortality and reproductive senescence in male mice. We observed that males exposed to female olfactory cues from middle- to old age (from 10 to 24 months of age) showed reduced late-life fertility, irrespective of whether they had also been allowed to mate with females earlier in life. Males that were exposed to female odours in conjunction with mating also showed an increased mortality rate across the exposure period, indicating that olfactory cues from females can increase male mortality in some environments. Our results show that exposure to female odours can influence reproductive ageing and mortality in male mice, highlighting that sensory perception of mates may be an important driver of life-history trade-offs in mammals.

Evolution remodels olfactory and mating-receptive behaviors in the transition from female to hermaphrodite reproduction

Male/hermaphrodite species have arisen multiple times from a male/female ancestral state in nematodes, providing a model to study behavioral adaptations to different reproductive strategies. Here, we examined the mating behaviors of male/female (gonochoristic) Caenorhabditis species in comparison with male/hermaphrodite (androdiecious) close relatives. We find that females from two species in the Elegans group chemotax to volatile odor from males, but hermaphrodites do not. Females, but not hermaphrodites, also display known mating-receptive behaviors such as sedation when male reproductive structures contact the vulva. Focusing on the male/female species C.nigoni, we show that female chemotaxis to males is limited to adult females approaching adult or near-adult males and relies upon the AWA neuron-specific transcription factor ODR-7, as does male chemotaxis to female odor as previously shown in C.elegans. However, female receptivity during mating contact is odr-7 independent. All C.nigoni female behaviors are suppressed by mating and all are absent in young hermaphrodites from the sister species C.briggsae. However, latent receptivity during mating contact can be uncovered in mutant or aged C.briggsae hermaphrodites that lack self-sperm. These results reveal two mechanistically distinct components of the shift from female to hermaphrodite behavior: the loss of female-specific odr-7-dependent chemotaxis and a sperm-dependent state of reduced receptivity to mating contact. Hermaphrodites from a second androdioecious species, C.tropicalis, recover all female behaviors upon aging, including chemotaxis to males. Regaining mating receptivity after sperm depletion could maximize hermaphrodite fitness across their lifespan.

Phospholipid supplementation inhibits male and female odor discrimination in mice.

Dietary phospholipids (PLs) are promising supplements that are commonly found as natural food ingredients and emulsifier additives. The present study aimed to evaluate the effect of major PLs found in food supplements on social behavior in mice. In this study, the effect of short-term high dietary PL content was studied in terms of social odor discrimination and social interactions with male and female intruders in male mice. We used odor discrimination and habituation tests to demonstrate that PL-fed male mice tend to lose preference toward female odor and fail to discriminate against socially significant scents. At the same time, test animals recognize non-social odors. We also found that PL affected the social behavior of the test males, who tend to behave indiscriminately toward male and female intruders during direct contact. Brain metabolomic profiling revealed no major changes in the intermediary metabolism or neurotransmitter biosynthesis. At the same time, intranasal PL application resembled the effects of dietary supplementation. These data suggest that certain PL might suppress pheromone perception in the olfactory system and affect the sense of socially important odor cues.

Transgenerational exposure to deoxygenation and warming disrupts mate detection in Gammarus locusta

Abstract Ocean deoxygenation and warming have been shown to pose a growing threat to the health of marine organisms and ecosystems. Yet, the potential for acclimation and adaptation remains poorly understood. The aim of this study was to evaluate the effects of transgenerational exposure to reduced oxygen availability and elevated seawater temperature on the chemosensory-dependent mating mechanisms of male amphipods Gammarus locusta. Three subsequent generations were exposed to four experimental treatments for 30 days: 1) present-day scenario, 2) warming; 3) deoxygenation; and 4) warming + deoxygenation. After exposure, the number of individuals that reached adulthood was gauged, and adult males from F0 and F1 were subjected to behavioral trials to assess their capacity of long-distance female cue detection through quantification of response time, the first direction of movement, activity rate, and proportion of time spent in female scent cues. Ocean warming induced mortality, and reduced oxygen availability had adverse effects on each of the investigated behavioral traits, which were amplified when combined with elevated temperature. Still, when compared with F0, the F1 generation demonstrated more adaptability (i.e., higher activity rate and preference for female odors) to the combination of the two stressors, suggesting positive carry-over effects. Nevertheless, full recovery to control levels was not observed. Altogether, this study indicates that future scenarios of ocean deoxygenation and warming have the potential to disrupt chemosensory-dependent mate detection in amphipods, but also suggests possible behavioral adaptations. We call for greater research efforts on long-term impacts of ocean change on the behavioral and physiological processes of benthic coastal communities.

Bile acids as putative social signals in Mozambique tilapia (Oreochromis mossambicus)

Chemical cues provide potential mates with information about reproductive status and resource-holding potential. In the Mozambique tilapia (Oreochromis mossambicus), males can distinguish female reproductive status through chemical cues, and accessibility of males to females depends on their position in the hierarchy, determined in part by chemical cues. Here, we hypothesized that tilapia faecal cues are attractive to conspecifics once released into the water. C18 solid-phase extracts of faeces from dominant males and pre-ovulatory females evoked stronger olfactory epithelium electrical responses (EOG) than, respectively, subordinate males and post-spawning females. Mass spectrometry of the reverse-phase C18 high-performance liquid chromatography fractions of these extracts with highest EOG, identified by amino acids and bile acids. Faeces from pre-ovulatory females contain significantly higher concentrations of cholic acid (CA) and taurocholic acid (TCH) than both post-spawning females and males. A pool of amino acids had no effect on aggression or attraction in males. However, males were attracted to the scent of pre-ovulatory female faeces, as well as CA and TCH, when applied separately. This attraction was accompanied by increased digging behaviour compared to the odour of post-spawning females. CA and TCH exert their action through separate receptor mechanisms. These findings are consistent with a role for faeces – and bile acids therein – in chemical communication in this species, acting as an attractant for males to reproductive females.

Early Postnatal Experience Modifies Activation of the Pituitary Testicular Complex in Male House Mice (Mus Musculus) Exposed to the Odor of Receptive Con- and Heterospecific Females

For the first time, it was shown that activation of the pituitary–testicular complex in male house mice exposed to the odor of receptive females of their own and closely related species was modified under the influence of early postnatal experience and the maternal environment. We have confirmed associated formation of behavioral and physiological mechanisms of precopulatory isolation in early ontogenesis. The serum levels of free testosterone in males of closely related species M. spicilegus and M. m. wagneri differ, it is significantly lower in mound-building mice. In males fostered by a conspecific female, the level of free testosterone was significantly lower when exposed to a heterospecific female odor in comparison with a conspecific odor. The rearing of M. m. wagneri males by females of a closely related species led to a decrease in the testosterone response caused by exposure to female chemosignals (both con- and heterospecific) and to the absence of differences in the serum level of free testosterone when exposed to the odor of a female of their own or closely related species. These results indicate that the rearing conditions had a significant influence on the formation of hormonal mechanisms of reproductive isolation.

EARLY POSTNATAL EXPERIENCE MODIFIES ACTIVATION OF THE PITUITARY-TESTICULAR COMPLEX IN MALE HOUSE MICE (<i>MUS MUSCULUS)</i> EXPOSED TO THE ODOR OF RECEPTIVE CON- AND HETEROSPECIFIC FEMALES

For the first time, data were obtained proving the modification of the activation of the pituitary-testicular complex of male house mice under the influence of early postnatal experience and the maternal environment when exposed to the odor of receptive females of their own and closely related species. We have confirmed the conjugacy of the formation of behavioral and physiological mechanisms of precopulatory isolation in early ontogenesis. The serum level of free testosterone in males of closely related species M. spicilegus and M. m. wagneri differ, it is significantly lower in mound-building mice. The level of free testosterone of males fostered by a conspecific female was significantly lower when they exposed a heterospecific in comparison with a conspecific female odor. The rearing of M. m. wagneri males by females of a closely related species caused a decrease in the testosterone response of males to the exposure of chemosignals from a female (both con-and heterospecific) and led to the absence of differences in the serum level of free testosterone when they exposed to the odor of a female of their own or closely related species. The data obtained indicate a significant influence of the rearing conditions on the formation of hormonal mechanisms of reproductive isolation.

Prostaglandin F2α drives female pheromone signaling in cichlids, revealing a basis for evolutionary divergence in olfactory signaling

Pheromones play essential roles in reproduction in many species. Prostaglandin F2α (PGF2α) acts as a female reproductive hormone and as a sex pheromone in some species. An olfactory receptor (OR) for PGF2α was recently discovered in zebrafish, but this signaling pathway is evolutionarily labile. To understand the evolution of signals that attract males to fertile females, we used the African cichlid Astatotilapia burtoni and found that adult males strongly prefer fertile female odors. Injection of a prostaglandin synthesis inhibitor abolishes this attractivity of fertile females, indicating these hormones are necessary for pheromonal signaling. Unlike zebrafish, A. burtoni males are insensitive to PGF2α, but they do exhibit strong preference for females injected with PGF2α. This attractiveness is independent of the PGF2α hormonal receptor Ptgfr, indicating that this pheromone signaling derives from PGF2α metabolization into a yet-undiscovered pheromone. We further discovered that fish that are insensitive to PGF2α lack an ortholog for the OR Or114 that zebrafish use to detect PGF2α. These results indicate that PGF2α itself does not directly induce male preference in cichlids. Rather, it plays a vital role that primes females to become attractive via an alternative male OR.

Lifespan extension in female mice by early, transient exposure to adult female olfactory cues.

Several previous lines of research have suggested, indirectly, that mouse lifespan is particularly susceptible to endocrine or nutritional signals in the first few weeks of life, as tested by manipulations of litter size, growth hormone levels, or mutations with effects specifically on early-life growth rate. The pace of early development in mice can also be influenced by exposure of nursing and weanling mice to olfactory cues. In particular, odors of same-sex adult mice can in some circumstances delay maturation. We hypothesized that olfactory information might also have a sex-specific effect on lifespan, and we show here that the lifespan of female mice can be increased significantly by odors from adult females administered transiently, that is from 3 days until 60 days of age. Female lifespan was not modified by male odors, nor was male lifespan susceptible to odors from adults of either sex. Conditional deletion of the G protein Gαo in the olfactory system, which leads to impaired accessory olfactory system function and blunted reproductive priming responses to male odors in females, did not modify the effect of female odors on female lifespan. Our data provide support for the idea that very young mice are susceptible to influences that can have long-lasting effects on health maintenance in later life, and provide a potential example of lifespan extension by olfactory cues in mice.

Different armpits under my new nose: Olfactory sex but not gender affects implicit measures of embodiment

Conflicting multisensory signals may alter embodiment to produce self-identification with a foreign body, but the role of olfaction in this process has been overlooked. We studied in healthy participants how sex (male and female sweat odors) and gender (male and female cosmetic scents) olfactory stimuli contribute to embodiment. Participants saw, on a head mounted display, the first-person perspective of a sex mismatching person. Synchronous visuotactile stimulation was applied to enhance illusory embodiment. Simultaneously, they smelled either sex- or gender- congruent or incongruent stimuli. We assessed implicit (skin conductance responses to visual threats) and explicit (questionnaire) measures of embodiment. Stronger responses to threat were found when participants smelled the sex-congruent compared to the sex-incongruent odor, while no such differences were found for the cosmetic scents. According to the questionnaire, embodiment did not differ between conditions. Post-experimental assessment of the presented cues, suggest that while both sweat odors were considered generally male, cosmetic scents were not. The presented scents were generally not associated with the embodied body. Our results suggest that sex-related body odors influence implicit but not explicit aspects of embodiment and are in line with unique characteristics of olfaction in other aspects of cognition.

Electronic Nose Signals for Analysing Similarity of Male and Female Axillary Odour to Food Material Aroma

Electronic Nose Signals for Analysing Similarity of Male and Female Axillary Odour to Food Material Aroma

Mediation of a Mutualistic Conflict for Pollination via Fig Phenology and Odor Recognition between Ficus and Fig Wasp.

The vegetative and reproductive growth of plants provide the basic tempo for an ecosystem, and when species are interdependent, phenology becomes crucial to regulating the quantity and quality of the interactions. In plant–insect interactions, the plants signal the beginning of their reproductive period with visual and chemical cues; however, in the case of Ficus mutualism, the cues are strictly chemical. The volatile organic compounds emitted by a fig species are a unique, specific blend that provides a signal to mutualistic wasps that the figs are receptive for pollination. In this study, we studied both the phenological pattern of Ficus septica in Central Taiwan and its emissions of volatile compounds at receptivity. This dioecious fig species displays a pattern of continuous vegetative and reproductive production all through the year with a decrease in winter. In parallel, the odor blends emitted by male and female trees are similar but with seasonal variations; these are minimal during winter and increase with the size of the wasp population during the favorable season. In addition, the pollinating females cannot distinguish between the male and female summer odor blends. The link between odor similarity, pollinators and intersexual conflict is discussed.

A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females.

Motherhood induces a drastic, sometimes long-lasting, change in internal state and behavior in many female animals. How a change in reproductive state or the discrete event of mating modulates specific female behaviors is still incompletely understood. Using calcium imaging of the whole brain of Drosophila females, we find that mating does not induce a global change in brain activity. Instead, mating modulates the pheromone response of dopaminergic neurons innervating the fly's learning and memory center, the mushroom body (MB). Using the mating-induced increased attraction to the odor of important nutrients, polyamines, we show that disruption of the female fly's ability to smell, for instance the pheromone cVA, during mating leads to a reduction in polyamine preference for days later indicating that the odor environment at mating lastingly influences female perception and choice behavior. Moreover, dopaminergic neurons including innervation of the β'1 compartment are sufficient to induce the lasting behavioral increase in polyamine preference. We further show that MB output neurons (MBON) of the β'1 compartment are activated by pheromone odor and their activity during mating bidirectionally modulates preference behavior in mated and virgin females. Their activity is not required, however, for the expression of polyamine attraction. Instead, inhibition of another type of MBON innervating the β'2 compartment enables expression of high odor attraction. In addition, the response of a lateral horn (LH) neuron, AD1b2, which output is required for the expression of polyamine attraction, shows a modulated polyamine response after mating. Taken together, our data in the fly suggests that mating-related sensory experience regulates female odor perception and expression of choice behavior through a dopamine-gated learning circuit.

Towards an understanding of multimodal traits of female reproduction in chimpanzees

Although primates have long been regarded as microsmatic, recent studies indicate that olfaction is an important sensory mode of primate communication, e.g., in the context of reproduction. However, large gaps remain in our understanding of primate olfactory traits, especially in the great apes. Female chimpanzees (Pan troglodytes) possess an exaggerated sexual swelling, which is an imprecise signal of fertility that is thought to serve to confuse paternity. However, some high-ranking males that copulate most frequently on the days when females are most fertile seem to have more precise information on the timing of ovulation, which suggests the existence of an olfactory fertility trait. In order to examine, and provide evidence for, fertility-related chemical information in female chimpanzees, we used gas chromatography—mass spectrometry to analyze the chemical composition of female body odor collected across the menstrual cycle during various stages of sexual swelling (97 samples of six females). The chemical composition was significantly affected by swelling stage, and eight substances were detected that were strongly related to the latter. The existence of an additional, olfactory, fertility trait may help males to fine-tune their sexual behavior or allow females to strengthen concealment of the exact timing of ovulation, and needs to be further investigated in follow-up studies. The results of our study provide much-needed evidence for the existence of an olfactory cue related to reproduction in chimpanzees, and form a basis for future studies on the interplay between visual and olfactory information on female fertility.

Chemical cues of identity and reproductive status in Japanese macaques.

Olfactory communication plays an important role in the regulation of socio-sexual interactions in mammals. There is growing evidence that both human and nonhuman primates rely on odors to inform their mating decisions. Nevertheless, studies of primate chemical ecology remain scarce due to the difficulty of obtaining and analyzing samples. We analyzed 67 urine samples from five captive female Japanese macaques (Macaca fuscata) and 30 vaginal swabs from three of these females using gas chromatography-mass spectrometry and examined the relationship between odor (compounds identified, richness, intensity, and diversity) and female identity as well as cycle phase. We found a total of 36 urine compounds of which we identified 31, and 68 vaginal compounds of which we identified 37. Our results suggest that urine and vaginal odor varied more between individuals than within cycle phases. However, we found that within a female cycle, urine samples from similar phases may cluster more than samples from different phases. Our results suggest that female odor may encode information about identity (vaginal and urine odor) and reproductive status (urine odor). The question of how conspecifics use female urine and vaginal odor remains open and could be tested using bioassays. Our results and their interpretation are constrained by our limited sample size and our study design. Nonetheless, our study provides insight into the potential signaling role of female odor in sexual communication in Japanese macaques and contributes to our understanding of how odors may influence mating strategies in primates.

Reducing local synthesis of estrogen in the tubular striatum promotes attraction to same-sex odors in female mice

Brain-derived 17β-estradiol (E2) confers rapid effects on neural activity. The tubular striatum (TuS, also called the olfactory tubercle) is both capable of local E2 synthesis due to its abundant expression of aromatase and is a critical locus for odor-guided motivated behavior and odor hedonics. TuS neurons also contain mRNA for estrogen receptors α, β, and the G protein-coupled estrogen receptor. We demonstrate here that mRNA for estrogen receptors appears to be expressed upon TuS dopamine 1 receptor-expressing neurons, suggesting that E2 may play a neuromodulatory role in circuits which are important for motivated behavior. Therefore, we reasoned that E2 in the TuS may influence attraction to urinary odors which are highly attractive. Using whole-body plethysmography, we examined odor-evoked high-frequency sniffing as a measure of odor attaction. Bilateral infusion of the aromatase inhibitor letrozole into the TuS of gonadectomized female adult mice induced a resistance to habituation over successive trials in their investigatory sniffing for female mouse urinary odors, indicative of an enhanced attraction. All males displayed resistance to habituation for female urinary odors, indicative of enhanced attraction that is independent from E2 manipulation. Letrozole's effects were not due to group differences in basal respiration, nor changes in the ability to detect or discriminate between odors (both monomolecular odorants and urinary odors). Therefore, de novo E2 synthesis in the TuS impacts females' but not males' attraction to female urinary odors, suggesting a sex-specific influence of E2 in odor hedonics.

Pheromone communication among sexes of the garden cross spider Araneus diadematus

Chemical communication plays a fundamental role in many aspects of an animal’s life from assessing habitat quality to finding mating partners. Behavioural observations show that chemical communication likewise plays an important role in spiders, but the contexts and the substances involved are little explored. Here, we investigate the chemical communication in the garden cross spider Araneus diadematus (Clerck, 1757) between and within the sexes. Using choice trials, we demonstrate that males are attracted to odours of adult females, but not to those of subadult females. Our data further suggest that adult females avoid odours of conspecific adult females, possibly in order to reduce reproductive competition with other females. Cuticle and silk extracts as well as headspace samples of subadult and adult virgin females were analysed via GC–MS. Available candidate compounds for the female sex pheromone were tested via electroantennography on palps (electropalpography) of adult virgin females and on females in behavioural trials. We propose sulcatone (6-methyl-5-hepten-2-one) as a candidate substance for the female volatile pheromone and several long-chained alkanes and alcohols as candidates for contact pheromones. Apart from demonstrating that attraction of males to females depends on the latter’s developmental stage, our study suggests that pheromones can also play an important role between females, an aspect that requires further attention.