Drosophila male courtship is controlled by the male-specific products of the fruitless (fruM) gene and its expressing neuronal circuitry. fruM is considered a master gene that controls all aspects of male courtship. By temporally and spatially manipulating fruM expression, we found that fruM is required during a critical developmental period for innate courtship toward females, while its function during adulthood is involved in inhibiting male-male courtship. By altering or eliminating fruM expression, we generated males that are innately heterosexual, homosexual, bisexual, or without innate courtship but could acquire such behavior in an experience-dependent manner. These findings show that fruM is not absolutely necessary for courtship but is critical during development to build a sex circuitry with reduced flexibility and enhanced efficiency, and provide a new view about how fruM tunes functional flexibility of a sex circuitry instead of switching on its function as conventionally viewed.
Keywords: D. melanogaster; circuit flexibility; courtship; fruitless; innate behavior; neuroscience; sexual orientation.
Innate behaviors are behaviors that do not need to be learned. They include activities such as nest building in birds and web spinning in spiders. Another behavior that has been extensively studied, and which is generally considered to be innate, is courtship in fruit flies. Male fruit flies serenade potential mates by vibrating their wings to create a complex melody. This behavior is under the control of a gene called ‘fruitless’, which gives rise to several distinct proteins, including one that is unique to males. For many years, this protein – called FruM – was thought to be the master switch that activates courtship behavior. But recent findings have challenged this idea. They show that although male flies that lack FruM fail to show courtship behaviors if raised in isolation, they can still learn them if raised in groups. This suggests that the role of FruM is more complex than previously thought. To determine how FruM controls courtship behavior, Chen et al. have used genetic tools to manipulate FruM activity in male flies at different stages of the life cycle and distinct cells of the nervous system. The results revealed that FruM must be present during a critical period of development – but not adulthood – for male flies to court females. However, FruM strongly influences the type of courtship behavior the male flies display. The amount and location of FruM determines whether males show heterosexual, homosexual or bisexual courtship behaviors. Adult flies with lower levels of FruM show an increase in homosexual courtship and a decrease in heterosexual courtship. These findings provide a fresh view on how a master gene can generate complex and flexible behaviors. They show that fruitless, and the FruM protein it encodes, work distinctly at different life cycles to modify the type of courtship behavior shown by male flies, rather than simply switching courtship behavior on and off. Exactly how FruM acts within the fruit fly brain to achieve these complex effects requires further investigation.
© 2021, Chen et al.