Auditory experience controls the maturation of song discrimination and sexual response in Drosophila

In birds and higher mammals, auditory experience during development is critical to discriminate sound patterns in adulthood. However, the neural and molecular nature of this acquired ability remains elusive. In fruit flies, acoustic perception has been thought to be innate. Here we report, surprisingly, that auditory experience of a species-specific courtship song in developing Drosophila shapes adult song perception and resultant sexual behavior. Preferences in the song-response behaviors of both males and females were tuned by social acoustic exposure during development. We examined the molecular and cellular determinants of this social acoustic learning and found that GABA signaling acting on the GABAA receptor Rdl in the pC1 neurons, the integration node for courtship stimuli, regulated auditory tuning and sexual behavior. These findings demonstrate that maturation of auditory perception in flies is unexpectedly plastic and is acquired socially, providing a model to investigate how song learning regulates mating preference in insects.
eLife digest Many mammals and birds have a critical period in youth when hearing the vocal cues of their parents helps them to learn the specific features of their communication sounds. Scientists have been studying the brains of humans, birds and other animals to find out what is happening in their brains when the animals hear these sounds. However, the brains of these species are too complex to fully understand how early vocal influences shape the brain networks that control behavior. Therefore, scientists often use ‘simpler’ organisms, such as insects, to study these processes. For example, fruit flies use a series of courtship behaviors – including mating calls – to attract their potential mates. To produce a courtship song, males vibrate their wings, which consists of short pulsed songs and sequences of humming. The time interval between the pulses is specific to a species. Until now it was thought that these mating calls are innate behaviors that cannot be learned or modified. To test this, Li et al. clipped the wings of male fruit flies so they could not produce their own song. First, they placed the females with the males and played one species-specific courtship song, and one from a different species. Both songs resulted in successful copulation and did not affect the female’s choice. To find out if a previous experience of a courtship song can influence the behavior of the fruit flies, Li et al. raised one group hearing their species-specific song and the other with a song from a different species. The results showed that females growing-up with their species-specific song, rejected males when a song of another species was played. However, the females accustomed to the other species’ song did not change their song preference and receptivity towards males. The same was also true for males: male fruit flies raised with their species-specific song later ignored another species’ song, which usually increased their mating drive. Li et al. further identified a specific region in the brain of the fruit flies known to be important for courtship, and a key molecule that regulated this behavior. These findings suggest that far from being innate, the mating preference in fruit flies can be learned and influenced by social experience. A next step will be to find out if fruit flies also have critical period for learning vocal cues and if so, how it is regulated at the molecular and neural levels. A better understanding of how fruit flies learn and discriminate sounds may bridge knowledge gaps in research using humans and other mammals.