Neuronal circuits and behavior

Animals and their nervous systems have evolved to reproduce. Although each species courts and mates differently, common mechanisms of how nervous systems implement sex differences during development, organize action sequences, encode approach and reward and communicate during social interactions are conserved. We use the fruit fly Drosophila melanogaster, where we can manipulate the action of genes and the development and activity of neurons with advanced genetic tools, to address basic questions about the neuronal circuits orchestrating reproductive behavior.
We focus on circuits for motor pattern generation and the architecture of neuro-muscular networks, as well as the mechanisms of higher order coordination of complex motor behaviors and behavioral sequences. Furthermore, we are interested in the communication between nervous system and the rest of the body. We address inter-organ signaling in the context of sexual behavior during copulation and aim at understanding how sensing of seminal fluid impacts female sexual behavior and how female signals affect male seminal fluid allocation.

Main lines of research

• Acoustic communication during Drosophila reproduction

  When a Drosophila male encounters a female, he uses wing vibrations to entice his potential mating partner. Courtship wing song is a highly structured, species specific acoustic signal. It stimulates the receptivity of a virgin female and drives her to accept males for copulation. Although largely innate, male singing behaviour is not a rigid reflex, but is modulated by multiple external and internal factors, such as physiological state, behavioural context and social experience.
  Recently, we discovered that not only males, but also females produce acoustic signals during reproduction. In contrast to males, females do not sing during courtship, but only during copulation (which lasts around 20min). Interestingly, female song depends on the receipt of seminal fluid. The proximate and ultimate causes of this new female behavior are not yet completely understood.
  In the laboratory, we use high throughput audio recording of courtship song as a way to precisely quantify motor behavior at millisecond resolution. From the oscillogram, changes in wing movements can be detected with high temporal and spatial resolution, allowing for both efficient screening of large number of genotypes and sensitive, in depth analysis of a broad variety of phenotypes.

• Mechanisms of sex specific motor pattern generation during acoustic communication

  How do dimorphisms in gene expression shape nervous system anatomy and physiology, explaining dimorphisms in behaviour?
  We have dissected the motor neuron control system for male song and its multifunctional use in flight control (O’Sullivan et al. 2018). Motor neurons are present in both sexes. In contrast, interneurons for motor patterning and action selection develop sex-specific cell fates, morphologies and physiological characteristics under the control of the transcription factors Fruitless and/or Doublesex. So far, the circuits for courtship song have been studied under the assumption that only male flies sing. The discovery of female song redefines the functional interpretation of dimorphic circuit development and provides a starting point for identifying new genetic and neuronal motifs underlying acoustic communication. We aim at investigating to which extent the neuronal substrate for acoustic signalling overlaps in both sexes and how differences in male and female singing behaviour can be explained on the level of gene expression, neuromodulation and circuit architecture.

• Behavioral hierarchy and coordination- state dependent action selection

  How do different behaviors interact and influence each other on a circuit level? During courtship, some behavioral elements are combined and others exclude each other or occur in a preferred sequence. We discovered that dependent on the state of the animal and the behavior it is engaged in, activation of neuronal classes has drastically different motor outcomes. By using optogenetic circuit interrogation, we explore the neuronal and genetic basis of state dependent action selection, aiming at identifying circuits and neuromodulators for behavioral hierarchy and coordination. Our findings highlight inhibition as an important mechanism for structuring behavioral sequences, ensuring appropriate, context dependent response to sensory stimuli.

• Communication between the nervous system and reproductive organs: genes, pathways and circuits for sensing and allocating ejaculate components

  In animals with internal fertilization, seminal fluid strongly influences the physiological requirements for reproduction. Active components and signalling molecules transferred together with sperm and impact sperm storage and viability, ovulation, female immunity, susceptibility to infection, the female nervous system and her behaviour.
  We found that specific components of seminal fluid incite acoustic signalling of female Drosophila during copulation (Kerwin et al. 2020). Our data indicates that female copulation song influences in turn male ejaculate allocation and biases the outcome of paternity shares under reproductive competition. These findings suggest that 1) females can rapidly sense and behaviourally react to seminal fluid and 2) males have evolved mechanisms to adjust seminal fluid quality and transfer in response to acoustic signals from the female.
  Currently, we aim at identifying which seminal fluid protein or metabolite triggers female copulation song. We are also investigating the neuronal control mechanisms of male plastic ejaculate allocation in response to female song.
  By this research, we aim at a general understanding of the female and male neuronal circuits mediating communication between the nervous system and the reproductive organs. We are interested how this signalling axis is modulated by sensory input and physiological conditions known to impact reproductive decisions (aging, nutritional state, infection, mating history and social exposure).