Understanding multi-level impact of male-derived sex peptide on female reproductive behaviours

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Reproductive behaviors and their regulation are most fundamental to all animals. Since they are largely hard-wired into the brain we can learn how behavior is encoded in the brain and shaped by perception and decision-making processes. Understanding how behavior is encoded in the brain is one of the big challenges in biology and requires a behaviorally and genetically tractable model organism. Female reproductive behaviors of the fruit fly Drosophila melanogaster profoundly change after mating leading to refusal to remate and induction of egg laying. Male-derived sex-peptide (SP) is the key molecule inducing these post-mating behaviors, which can last up to one week in the presence of sperm. This very robust behavioral response of Drosophila females to sex-peptide provides the essential prerequisites to map SP responsive neurons and eventually learn how complex behaviors such as mating choice and control of egg laying are encoded in the brain. A key tool to find SP-target neurons is membrane-tethered SP (mSP), that will induce a response when the same neuron that expresses mSP also expresses an SP receptor. Our recent studies showed that there are several distinct neuronal populations that can via exposure to mSP induce refusal to remate and egg laying. Importantly, we could also show that these two post-mating responses can be separated by mSP expression either in the trunk or in the head leading to induction of egg laying or reduction of receptivity, respectively. These exciting findings draw a much more complex picture how SP interferes through multiple sites with female reproductive behaviors to coordinate the post-mating response, yet how this works at a brain systems level remains to be elaborated. We currently have very limited understanding of where SP-target neurons are located in the fly brain. To identify the neuronal circuitry underlying the sex-peptide response, we have used expression of mSP in subsets of neurons of genes involved in the SP-response and the sex-determination pathway. In particular, we subdivided the regulatory region of the broadly expressed SP receptor (SPR) gene into small regulatory fragments expressing only in subsets of neurons. Using this paradigm-shifting approach we have identified small populations of neurons, one that reduces receptivity and induces egg laying, and another one that only induces egg laying upon expression of mSP. Through these experiments we now have worked out, in principle, how to identify all the different populations of SP target neurons. Hence, we now need to identify small regulatory fragments in sex determination genes and SP response pathway genes to identify additional SP target neurons. These experiments will be then be the resource to identify the relevant neurons in the recently become available high-resolution Drosophila brain from the fly connectome project to build the circuitry directing the female post-mating response.With these experiments we will test the hypothesis that SP-target neurons are present at multiple sites in the brain to direct female reproductive behaviors for a coordinated post-mating response. Compared to a previous model arguing for central induction of all PMRs, a modular assembly of individual PMRs holds evolutionary flexibility during speciation and adaptation to diverse habitats, but can maintain basic regulatory principles such as the control of egg laying. We therefore anticipate that the knowledge obtained from our studies will be applicable to a wide range of pest insects pinpointing towards novel strategies for pest management to protect crop and control insect born diseases by interfering with egg laying. In particular, our findings are directly transferable to the close relative Drosophila suzukii, one of the few species able to lay eggs into fruits, which is currently invading Europe including the UK and causing damage in billions to fruit production.