A juvenile mouse pheromone inhibits sexual behaviour through the vomeronasal system

Ferrero, David M.; Moeller, Lisa M.; Osakada, Takuya; Horio, Nao; Li, Qian; Roy, Dheeraj S.; Cichy, Annika; Spehr, Marc; Touhara, Kazushige; Liberles, Stephen D.

doi:10.1038/nature12579

Cited by 159 publications

(151 citation statements)

References 31 publications

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“…This is surprising, because both male odor and male USVs are thought to affect conspecific behavior in mice. Odors of unfamiliar males increase aggressive behavior between males (Archer, 1968;Mackintosh and Grant, 1966), females use male scent marks to assess male fitness (Rich and Hurst, 1998), and body odors have been shown to affect how mice response to other social cues (Asaba et al, 2014;Ferrero et al, 2013). Similarly, female mice approach playbacks of male USVs (Hammerschmidt et al, 2009;Musolf et al, 2010;Shepard and Liu, 2011).…”

Section: Discussionmentioning

confidence: 99%

Evidence for an audience effect in mice: male social partners alter the male vocal response to female cues

Seagraves

Arthur

Egnor

2016

Journal of Experimental Biology

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Mice (Mus musculus) form large and dynamic social groups and emit ultrasonic vocalizations in a variety of social contexts. Surprisingly, these vocalizations have been studied almost exclusively in the context of cues from only one social partner, despite the observation that in many social species the presence of additional listeners changes the structure of communication signals. Here, we show that male vocal behavior elicited by female odor is affected by the presence of a male audience -with changes in vocalization count, acoustic structure and syllable complexity. We further show that single sensory cues are not sufficient to elicit this audience effect, indicating that multiple cues may be necessary for an audience to be apparent. Together, these experiments reveal that some features of mouse vocal behavior are only expressed in more complex social situations, and introduce a powerful new assay for measuring detection of the presence of social partners in mice.

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Section: Discussionmentioning

confidence: 99%

Evidence for an audience effect in mice: male social partners alter the male vocal response to female cues

Seagraves

Arthur

Egnor

2016

Journal of Experimental Biology

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“…At least some of these peptides apparently activate VNO cells (Haga et al, 2010), thus suggesting a role of the ESP peptides in social signalling. For instance, it has recently been described that ESP22 is secreted by lacrimal glands of both male and female mice, in a 50-fold higher concentration in juvenile than adults (Ferrero et al, 2013). ESP22 apparently acts as a juvenile pheromone that inhibits sexual behaviour in adults, in which, like other ESP peptides, is detected by VNO cells, likely expressing V2R receptors.…”

Section: Accepted Manuscriptmentioning

confidence: 99%

From sexual attraction to maternal aggression: When pheromones change their behavioural significance

Martín‐Sánchez

McLean

Beynon

et al. 2015

Hormones and Behavior

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From sexual attraction to maternal aggression: When pheromones change their behavioural significance, Hormones and Behavior (2014), doi: 10.1016/j.yhbeh.2014 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.A C C E P T E D M A N U S C R I P T ACCEPTED MANUSCRIPT A C C E P T E D M A N U S C R I P T ACCEPTED MANUSCRIPT2 AbstractThis paper reviews the role of chemosignals in the socio-sexual interactions of female mice, and reports two experiments testing the role of pup-derived chemosignals and the male sexual pheromone darcin in inducing and promoting maternal aggression. Female mice are attracted to urine-borne male pheromones. Volatile and non-volatile urine fractions have been proposed to contain olfactory and vomeronasal pheromones. In particular, the male-specific major urinary protein (MUP) MUP20, darcin, has been shown to be rewarding and attractive to females. Non-urinary male chemosignals, such as the lacrimal protein ESP1, promote lordosis in female mice, but its attractive properties are still to be tested. There is evidence indicating that ESP1 and MUPs are detected by vomeronasal type 2 receptors (V2R).When a female mouse becomes pregnant, she undergoes dramatic changes in her physiology and behaviour. She builds a nest for her pups and takes care of them. Dams also defend the nest against conspecific intruders, attacking especially gonadally intact males. Maternal behaviour is dependent on a functional olfactory system, thus suggesting a role of chemosignals in the development of maternal behaviour. Our first experiment demonstrates, however, that pup chemosignals are not sufficient to induce maternal aggression in virgin females. In addition, it is known that vomeronasal stimuli are needed for maternal aggression.Since MUPs (and other molecules) are able to promote intermale aggression, in our second experiment we test if the attractive MUP darcin also promotes attacks on castrated male intruders by lactating dams. Our findings demonstrate that the same chemosignal, darcin, promotes attraction or aggression according to female reproductive state.

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“…Pheromones can be the basis for the identification of many features of these potential mates, including species (Billeter et al, 2009;Levesque et al, 2011;Leary et al, 2012), physiological condition related to readiness to mate (Kobayashi et al, 2002;Ferrero et al, 2013), and quality of the mate (Thornhill and Gangestad, 1999). In this context, mate recognition using multicomponent chemicals is one way to establish the specificity of a chemical signal.…”

Section: Introductionmentioning

confidence: 99%

The smell of moulting:N-acetylglucosamino-1,5-lactone is a premoult biomarker and candidate component of the courtship pheromone in the urine of the blue crab,Callinectes sapidus

Kamio

Schmidt

Germann

et al. 2013

Journal of Experimental Biology

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Female blue crabs (Callinectes sapidus) in their pubertal moult stage release unidentified sex pheromone molecules in their urine, causing males to respond with courtship behaviours including a display called courtship stationary paddling and a form of precopulatory guarding called cradle carry. We hypothesized that pheromones are mixtures of molecules and are more concentrated in urine of pubertal premoult females compared with other moulting stages and thus that these molecules are biomarkers (i.e. metabolites that can be used as an indicator of some biological state or condition) of pubertal premoult females. We tested this hypothesis by combining bioassay-guided fractionation and biomarker targeting. To evaluate the molecular mass of the putative pheromone by bioassay-guided fractionation, we separated urine from pubertal premoult females and intermoult males by ultrafiltration into three molecular mass fractions. The <500 Da fraction and the 500-1000 Da fraction but not the >1000 Da fraction of female urine induced male courtship stationary paddling, but none of the fractions of male urine did. Thus, female urine contains molecules of <1000 Da that stimulate courtship behaviours in males. Biomarker targeting using nuclear magnetic resonance (NMR) spectral analysis of the 500-1000 Da fraction of urine from premoult and postmoult males and females revealed a premoult biomarker. Purification, nuclear magnetic resonance, mass spectrometry and high pressure liquid chromatography analysis of this premoult biomarker identified it as N-acetylglucosamino-1,5-lactone (NAGL) and showed that it is more abundant in urine of premoult females and males than in urine of either postmoult or juvenile females and males. NAGL has not been reported before as a natural product or as a molecule of the chitin metabolic pathway. Physiological and behavioural experiments demonstrated that blue crabs can detect NAGL through their olfactory pathway. Thus, we hypothesize that NAGL is a component of the sex pheromone and that it acts in conjunction with other yet unidentified components.

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A juvenile mouse pheromone inhibits sexual behaviour through the vomeronasal system

Cited by 159 publications

References 31 publications

Evidence for an audience effect in mice: male social partners alter the male vocal response to female cues

Evidence for an audience effect in mice: male social partners alter the male vocal response to female cues

From sexual attraction to maternal aggression: When pheromones change their behavioural significance

The smell of moulting:N-acetylglucosamino-1,5-lactone is a premoult biomarker and candidate component of the courtship pheromone in the urine of the blue crab,Callinectes sapidus

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