Final Report Summary - MCM (Neural Mechanisms Underlying Mate Preference and selection in Mice)
Sex is the essential feature of reproduction in most of the animal kingdom. Numerous factors influence mating, including genetic barriers or geographical proximity, but for most species there is an element of behavioral choice that is fundamental.
The process of choosing mates can be divided into three stages: (1) reception of signals broadcast by prospective mates; (2) evaluation of the signals by choosers; (3) translation of the resulting evaluation to either mate or reject. Many of the signals emitted by mates and used by choosers to decide have been identified, including coloration in fish; song patterns in insects, birds and amphibians; and chemical signals in rodents. From the receiver’s side, the sensory pathways that detect and process these signals have been described for several systems, particularly for rodents. In contrast, much less is known about the mechanisms of mate choice beyond the periphery, including how multiple mate signals are evaluated or how prior experience, internal state, comparison set or interactions with prospective mates influence this complex decision-making process.
We focused on assortative mate choice, which is known to contribute to the reproductive isolation of the two European subspecies of house mouse, Mus musculus musculus and Mus musculus domesticus. To understand the decision process, we developed full mating and limited-contact paradigms. We found that receptive musculus females exhibited a robust preference to mate with males of the same subspecies. However, if females were non-receptive they exhibited no preference. Furthermore, if presented with a male individually, this means, in a non-choice condition, females readily mated with domesticus or musculus males. These experiments establish an assortative mate preference assay appropriate for the investigation of its underlying substrates. Our results also highlight the interplay between the chooser´s internal state and the nature of the interaction with prospective mates and suggests that the decision in based on a comparison of the options available, rather than on an absolute preference (Zinck and Lima, 2013).
We then investigated the ontogeny of this preference, by performing adoption experiments where musculus females were raised in a domesticus environment. Our results show that female mouse mate preference has a hierarchical dependence on early postnatal life experience and the order of males encountered as an adult. Whereas females raised in their normal musculus environment display a robust homosubspecific preference, females fostered in a domesticus family prefer the first male encountered, regardless of subspecies. Thus, early life experience of musculus females, when and only when concordant with genetic self-identify, overrides sampling order effects, ensuring robust assortative choice. In the absence of this phylogenetic-ontogenetic match, simple primacy effects dominate mate preference (Zinck, Moreira and Lima, in prep).
To start gaining insights into the brain mechanisms that are underlying this preference and choice we used immediate early genes as read-outs of neuronal activity. We exposed adopted and control musculus females to musculus males and investigated how different brain regions respond to these individuals. We know, from our behavioral experiments, that musculus males are more valuable for control females than for adopted females, so we reasoned that both groups of females would represent these males in a different manner. We focused our efforts into brain regions that are important for rewarding/value coding, including the nucleus accumbens, and areas involved in olfactory processing, like for example the medial amygdala. We found differential activation of neurons in the Islands of Calleja (IC) across the two conditions. The IC have been implicated in the establishment of olfactory memories in rodents and so they are a good candidate brain area to underlie the memory of the correct subspecies.
The process of choosing mates can be divided into three stages: (1) reception of signals broadcast by prospective mates; (2) evaluation of the signals by choosers; (3) translation of the resulting evaluation to either mate or reject. Many of the signals emitted by mates and used by choosers to decide have been identified, including coloration in fish; song patterns in insects, birds and amphibians; and chemical signals in rodents. From the receiver’s side, the sensory pathways that detect and process these signals have been described for several systems, particularly for rodents. In contrast, much less is known about the mechanisms of mate choice beyond the periphery, including how multiple mate signals are evaluated or how prior experience, internal state, comparison set or interactions with prospective mates influence this complex decision-making process.
We focused on assortative mate choice, which is known to contribute to the reproductive isolation of the two European subspecies of house mouse, Mus musculus musculus and Mus musculus domesticus. To understand the decision process, we developed full mating and limited-contact paradigms. We found that receptive musculus females exhibited a robust preference to mate with males of the same subspecies. However, if females were non-receptive they exhibited no preference. Furthermore, if presented with a male individually, this means, in a non-choice condition, females readily mated with domesticus or musculus males. These experiments establish an assortative mate preference assay appropriate for the investigation of its underlying substrates. Our results also highlight the interplay between the chooser´s internal state and the nature of the interaction with prospective mates and suggests that the decision in based on a comparison of the options available, rather than on an absolute preference (Zinck and Lima, 2013).
We then investigated the ontogeny of this preference, by performing adoption experiments where musculus females were raised in a domesticus environment. Our results show that female mouse mate preference has a hierarchical dependence on early postnatal life experience and the order of males encountered as an adult. Whereas females raised in their normal musculus environment display a robust homosubspecific preference, females fostered in a domesticus family prefer the first male encountered, regardless of subspecies. Thus, early life experience of musculus females, when and only when concordant with genetic self-identify, overrides sampling order effects, ensuring robust assortative choice. In the absence of this phylogenetic-ontogenetic match, simple primacy effects dominate mate preference (Zinck, Moreira and Lima, in prep).
To start gaining insights into the brain mechanisms that are underlying this preference and choice we used immediate early genes as read-outs of neuronal activity. We exposed adopted and control musculus females to musculus males and investigated how different brain regions respond to these individuals. We know, from our behavioral experiments, that musculus males are more valuable for control females than for adopted females, so we reasoned that both groups of females would represent these males in a different manner. We focused our efforts into brain regions that are important for rewarding/value coding, including the nucleus accumbens, and areas involved in olfactory processing, like for example the medial amygdala. We found differential activation of neurons in the Islands of Calleja (IC) across the two conditions. The IC have been implicated in the establishment of olfactory memories in rodents and so they are a good candidate brain area to underlie the memory of the correct subspecies.