Female mice ultrasonically interact with males during courtship displays

“This is akin to other species; receptive females slow down permitting the courting male to approach and mate (McGill, 1962; Beach, 1976; Hall, 1994; Kowalski et al., 2004; Szykman et al., 2007).”

“DOI: 10.7554/eLife.06203 1 of 24 between males (Silk, 2007).”

“Second, although mice appear to produce characteristic vocal patterns or songs (Holy and Guo, 2005; Sugimoto et al., 2011; Hoffmann et al., 2012), individual ultrasonic vocalizations are similar across animals, both within and between sexes (Hammerschmidt et al., 2012a).”

“This is akin to other species; receptive females slow down permitting the courting male to approach and mate (McGill, 1962; Beach, 1976; Hall, 1994; Kowalski et al., 2004; Szykman et al., 2007).”

“Other systems capitalized on the power of an array to determine the number of animals hidden in dense terrain (Celis-Murillo et al., 2009; Blumstein et al., 2011) or map the boundaries of an animal’s territory (Kirschel et al.”

“An automated classifier (Janelia Automatic Animal Behavior Annotator; JAABA; Kabra et al. (2013), http://jaaba.sourceforge.net) was used for identifying events when a female mouse was being followed.”

“Transfer of social information occurs over a wide range of timescales, from short-term information about an individual’s current motivational state (Moles and D’Amato F, 2000) to longer-term information about dominance status (Ficken et al., 1987; Grosenick et al., 2007) or fertility (Leong et al.”

“Mice produce ultrasonic vocalizations in many social contexts including establishment of territory, resident–intruder interactions, pup care, juvenile play, social reunion, and mating (Sales and Pye, 1974).”

“Moreover, it is known that female mice possess the neural circuitry necessary to emit USVs during interactions with males because surgical or genetic lesions to the vomeronasal organ unmask this behavior (Kimchi et al., 2007).”

“Most studies have found that vocal behavior is either important for joint territorial defense or maintaining affiliation, particularly between mated pairs (Hall, 2004).”

“These interactions are supported by information exchange through a variety of sensory modalities (Adolphs, 2010).”

“Furthermore, a female’s participation in these vocal interactions may function as a signal that indicates a state of increased receptivity.”

“Female responsiveness modulates male mating behavior throughout the animal kingdom (Coleman et al., 2004; Higham et al., 2009; Akre and Ryan, 2011).”

“A similar interdependence of behavior between partners occurs in the early stages of human courtship, where a female’s non-verbal displays modulate a male’s approach behavior (Moore, 1985).”

“Moreover, mice living in large populations for extended periods exhibit social interactions that are affected by the dynamics of multiple group members (Shemesh et al., 2013) and complex dominance hierarchies (Weissbrod et al., 2013).”

“Interactions between males and females during courtship also occur in the vocal domain (Janson, 1984; Tobias et al., 1998; Garamszegi et al., 2007).”

“, 2010) or whistle-like control sounds (Hammerschmidt et al., 2009).”

“This is akin to other species; receptive females slow down permitting the courting male to approach and mate (McGill, 1962; Beach, 1976; Hall, 1994; Kowalski et al., 2004; Szykman et al., 2007).”

“Moreover, mice living in large populations for extended periods exhibit social interactions that are affected by the dynamics of multiple group members (Shemesh et al., 2013) and complex dominance hierarchies (Weissbrod et al., 2013).”

“DOI: 10.7554/eLife.06203.001”

“This behavior strongly resembles a chase, a fundamental component of mouse courtship (Van Oortmerssen, 1971).”

“, 2010), female mice spend more time near vocalizing males than mute males (Pomerantz et al., 1983), and female mice preferentially approach a speaker playing male vocalizations rather than a speaker playing background noise (Musolf et al.”

“First, there is no obvious visual sign that a mouse is producing a USV (Chabout et al., 2012).”

“Mouse sound source estimation was performed using a procedure similar to that of Zhang et al. (2008).”

“Moreover, it is known that female mice possess the neural circuitry necessary to emit USVs during interactions with males because surgical or genetic lesions to the vomeronasal organ unmask this behavior (Kimchi et al., 2007).”

“courting male, despite evidence that both sexes produce virtually indistinguishable vocalizations.”

“Interactions between males and females during courtship also occur in the vocal domain (Janson, 1984; Tobias et al., 1998; Garamszegi et al., 2007).”

“To address this question, we developed a microphone array system to localize vocalizations from socially interacting, individual adult mice.”

“Furthermore, a female’s participation in these vocal interactions may function as a signal that indicates a state of increased receptivity.”

“However, females have been reported to vocalize at high rates during same sex interactions (Maggio and Whitney, 1985; Moles et al., 2007).”

“For example, inDrosophila melanogaster, males modulate their song patterning in response to variation in sensory cues about the female’s position and motion (Coen et al., 2014).”

“At least one week prior to the start of the recordings, mice were marked with distinctive patterns for identification by applying harmless hair bleach to the fur (Ohayon et al., 2013).”

“Second, although mice appear to produce characteristic vocal patterns or songs (Holy and Guo, 2005; Sugimoto et al., 2011; Hoffmann et al., 2012), individual ultrasonic vocalizations are similar across animals, both within and between sexes (Hammerschmidt et al., 2012a).”

“…use pairs of mice (Bean et al., 1981; Choi et al., 2011; D’Amato and Moles, 2001; Hammerschmidt et al., 2012b; Nunez et al., 1978; Nyby et al., 1976; Ogawa et al., 2000; Pomerantz and Clemens, 1981; Rotschafer et al., 2012; Scattoni et al., 2008; Warburton et al., 1989; White et al., 1998).”

“…during mating (Sewell, 1972; Hanson and Hurley, 2012), urine from females but not males stimulates vocal production in males (Nyby et al., 1979; Musolf et al., 2010), female mice spend more time near vocalizing males than mute males (Pomerantz et al., 1983), and female mice preferentially…”

“Supporting previous work (Sewell, 1972; Nyby, 1983; Chabout et al., 2012), we directly showed that male mice vocalize in the presence of freely moving female mice.”

“…use pairs of mice (Bean et al., 1981; Choi et al., 2011; D’Amato and Moles, 2001; Hammerschmidt et al., 2012b; Nunez et al., 1978; Nyby et al., 1976; Ogawa et al., 2000; Pomerantz and Clemens, 1981; Rotschafer et al., 2012; Scattoni et al., 2008; Warburton et al., 1989; White et al., 1998).”

“…use pairs of mice (Bean et al., 1981; Choi et al., 2011; D’Amato and Moles, 2001; Hammerschmidt et al., 2012b; Nunez et al., 1978; Nyby et al., 1976; Ogawa et al., 2000; Pomerantz and Clemens, 1981; Rotschafer et al., 2012; Scattoni et al., 2008; Warburton et al., 1989; White et al., 1998).”

“DOI: 10.7554/eLife.06203.001”

“…vocal behavior of adult mice, most experimental paradigms use pairs of mice (Bean et al., 1981; Choi et al., 2011; D’Amato and Moles, 2001; Hammerschmidt et al., 2012b; Nunez et al., 1978; Nyby et al., 1976; Ogawa et al., 2000; Pomerantz and Clemens, 1981; Rotschafer et al., 2012;…”

“As for the role of female vocalizations in courtship, many believe a female’s participation may serve as an indication of her receptivity (Janson, 1984) or may encourage competition between males (Montgomerie and Thornhill, 1989).”

“…(Blank et al., 2014), songbirds stimulate reproductive activity in females by singing (Bentley et al., 2000), sac-winged bats produce complex serenades during sexual displays (Behr and von Helversen, 2004), and anurans phonotaxis towards ultrasonic courtship vocalizations (Shen et al., 2008).”

“In the past, microphone arrays have been used to study the acoustic features of many species (Payne et al., 2003;Mennill et al., 2006; Chiu et al., 2010; Collier et al., 2010; Kalcounis-Rueppell et al., 2010).”

“In rodents, reports indicate that USVs are important for female receptivity during estrus (Floody et al., 1977; McIntosh et al., 1978) and, therefore two hours prior to the anticipated start of the experiment, non-invasive lavage and cytological assessment of vaginal cells were performed.”

“In rodents, reports indicate that USVs are important for female receptivity during estrus (Floody et al., 1977; McIntosh et al., 1978) and, therefore two hours prior to the anticipated start of the experiment, non-invasive lavage and cytological assessment of vaginal cells were performed.”

“Interactions between males and females during courtship also occur in the vocal domain (Janson, 1984; Tobias et al., 1998; Garamszegi et al., 2007).”

“, 2014), songbirds stimulate reproductive activity in females by singing (Bentley et al., 2000), sac-winged bats produce complex serenades during sexual displays (Behr and von Helversen, 2004), and anurans phonotaxis towards ultrasonic courtship vocalizations (Shen et al.”

“For example, USVs occur during mating (Sewell, 1972; Hanson and Hurley, 2012), urine from females but not males stimulates vocal production in males (Nyby et al., 1979; Musolf et al., 2010), female mice spend more time near vocalizing males than mute males (Pomerantz et al.”

“When examining the ultrasonic vocal behavior of adult mice, most experimental paradigms use pairs of mice (Bean et al., 1981; Choi et al., 2011; D’Amato and Moles, 2001; Hammerschmidt et al., 2012b; Nunez et al., 1978; Nyby et al., 1976; Ogawa et al., 2000; Pomerantz and Clemens, 1981; Rotschafer et al., 2012; Scatton…”

“Female responsiveness modulates male mating behavior throughout the animal kingdom (Coleman et al., 2004; Higham et al., 2009; Akre and Ryan, 2011).”

“Second, although mice appear to produce characteristic vocal patterns or songs (Holy and Guo, 2005; Sugimoto et al., 2011; Hoffmann et al., 2012), individual ultrasonic vocalizations are similar across animals, both within and between sexes (Hammerschmidt et al., 2012a).”

“In the past, microphone arrays have been used to study the acoustic features of many species (Payne et al., 2003;Mennill et al., 2006; Chiu et al., 2010; Collier et al., 2010; Kalcounis-Rueppell et al., 2010).”

“DOI: 10.7554/eLife.06203.001”

“DOI: 10.7554/eLife.06203.001”

“Moreover, it is known that female mice possess the neural circuitry necessary to emit USVs during interactions with males because surgical or genetic lesions to the vomeronasal organ unmask this behavior (Kimchi et al., 2007).”

“…the number of animals hidden in dense terrain (Celis-Murillo et al., 2009; Blumstein et al., 2011) or map the boundaries of an animal’s territory (Kirschel et al., 2011), whereas our system was specifically designed to link, with high resolution and accuracy, the vocal and social behaviors of…”

“…mice, most experimental paradigms use pairs of mice (Bean et al., 1981; Choi et al., 2011; D’Amato and Moles, 2001; Hammerschmidt et al., 2012b; Nunez et al., 1978; Nyby et al., 1976; Ogawa et al., 2000; Pomerantz and Clemens, 1981; Rotschafer et al., 2012; Scattoni et al., 2008; Warburton et…”

“In the past, microphone arrays have been used to study the acoustic features of many species (Payne et al., 2003;Mennill et al., 2006; Chiu et al., 2010; Collier et al., 2010; Kalcounis-Rueppell et al., 2010).”

“…of social information occurs over a wide range of timescales, from short-term information about an individual’s current motivational state (Moles and D’Amato F, 2000) to longer-term information about dominance status (Ficken et al., 1987; Grosenick et al., 2007) or fertility (Leong et al., 2003).”

“Female responsiveness modulates male mating behavior throughout the animal kingdom (Coleman et al., 2004; Higham et al., 2009; Akre and Ryan, 2011).”

“However, females have been reported to vocalize at high rates during same sex interactions (Maggio and Whitney, 1985; Moles et al., 2007).”

“Group size influences the behavior of individual animals (Fitzsimmons and Bertram, 2013; Shen et al., 2014).”

“…studies have addressed the difficulty in determining the source by assuming a single mouse produced the majority of the observed vocalizations (Barthelemy et al., 2004; Choi et al., 2011; Hanson and Hurley, 2012), or by experimentally preventing one mouse from vocalizing (Whitney et al.,…”

“For example, in a variety of species, the full range of a male’s vocal repertoire only occurs when multiple males are present (Rand and Ryan, 1981; Martinez-Rivera and Gerhardt, 2008; Charlton and Reby, 2011).”

“Group size influences the behavior of individual animals (Fitzsimmons and Bertram, 2013; Shen et al., 2014).”

“Transfer of social information occurs over a wide range of timescales, from short-term information about an individual’s current motivational state (Moles and D’Amato F, 2000) to longer-term information about dominance status (Ficken et al., 1987; Grosenick et al., 2007) or fertility (Leong et al.”

“This is akin to other species; receptive females slow down permitting the courting male to approach and mate (McGill, 1962; Beach, 1976; Hall, 1994; Kowalski et al., 2004; Szykman et al., 2007).”

“DOI: 10.7554/eLife.06203.001”

“We used speed at the time of the male vocalization as a proxy for female receptivity (Kowalski et al., 2004).”

“In the past, microphone arrays have been used to study the acoustic features of many species (Payne et al., 2003;Mennill et al., 2006; Chiu et al., 2010; Collier et al., 2010; Kalcounis-Rueppell et al., 2010).”

“Previous studies have addressed the difficulty in determining the source by assuming a single mouse produced the majority of the observed vocalizations (Barthelemy et al., 2004; Choi et al., 2011; Hanson and Hurley, 2012), or by experimentally preventing one mouse from vocalizing (Whitney et al.”

“Gazelles roar during mating displays (Blank et al., 2014), songbirds stimulate reproductive activity in females by singing (Bentley et al., 2000), sac-winged bats produce complex serenades during sexual displays (Behr and von Helversen, 2004), and anurans phonotaxis towards ultrasonic courtship…”

“…of male courtship songs in mice are correlated with mate choice (Asaba et al., 2014); adult females are known to vocalize in the presence of novel conspecifics and vocally interact with males during courtship and parenting (Hammerschmidt et al., 2012; Liu et al., 2013; Neunuebel et al., 2015).”

“Biologists have deployed a wide array of sensors to capture animal behavior, including infrared sensors (Friedman et al. 1997), microphone arrays (Neunuebel et al. 2015), laser Doppler vibrometry (Elias et al. 2003),…”

“…dynamics to, for example, audio dynamics through asking what behavioral features predict the performance of a particular song or song type using methods such as general linear models (GLMs) [88–90], and improvements in automated methods have increased the throughput of audio data analysis [91–94].”