The importance of increasing brain complexity for the evolution of novel social behaviors.
Evolution, Anthropology
Molecular Biology and Physiology of Neurons and Glial Cells
Final Report Abstract
Sexual reproduction does not only enable two individual to mix their genetic material and to create genetically novel offspring but also sets the ground for sexual conflicts between both sexes. Such conflicts can lead to overly complex regulatory systems as each sex tries to gain control over behaviors or physiological responses that influence the fitness of each sex in opposite directions. We have identified such a conflict in the fruit fly Drosophila melanogaster: females evolved the ability to advance the timepoint at which they eject the ejaculate of the last male the mated with to facilitate a faster remating with a subsequent male. This novel behavior is beneficial for the females as it enables them to adjust the paternity ratio of the first and the second male they mate with. In contrast, an advanced ejaculate ejection is particularly costly for the first male as the proportion of offspring sired by this male and thus, his fitness, are reduced. This predicts the emergence of counteradaptations in males that enable them to delay ejaculate ejection and by that, to increase their fitness. Preliminary data indeed indicated that males gained access over the neuronal circuit that controls ejaculate ejection to prevent the female from expelling the ejaculate. This sexual conflict in combination with the powerful tools available in D. melanogaster allow us to dissect the evolution of brain complexity and to understand how a sexual conflict is carried out on a neuronal circuit level. In this project, I aimed at dissecting this neurocircuit that regulates the timing of ejaculate ejection including its additional layers of complexity resulting from the sexual conflict and by identifying the selective driver that led to their evolution. By integrating the neurogenetic toolkit exclusively available in D. melanogaster with behavioral experiments, I (i) revealed the sensory neurons via which females monitor male presence and male attractiveness, (ii) identified a population of neurons that are functionally involved in inducing ejaculate ejection and that might have been highjacked by the male, and (iii) demonstrated that fitness of males and females is influenced by the timepoint of ejaculate ejection which provide ultimate explanations for the rise of this conflict. As such, these data suggest that neuronal circuits can become the target of a sexual conflict and that one sex can get access over the behavior of the other sex by highjacking neurons of that pathway and by manipulating them to their own benefit.
Publications
- Bioassaying the function of pheromones in Drosophila melanogaster’s social behavior. In Behavioral Neurogenetics pp 123 – 156, Springer
Verschut, Kohlmeier, Billeter
(See online at https://doi.org/10.1007/978-1-0716-2321-3_9) - Mating increases Drosophila melanogaster females’ choosiness by reducing olfactory sensitivity to a male pheromone. Nature Ecology and Evolution 5: 1165-73
Kohlmeier, Zhang, Gorter, Su, Billeter
(See online at https://doi.org/10.1038/s41559-021-01482-4) - Genetic mechanisms modulating behaviour through plastic chemosensory responses in insects. Molecular Ecology 32: 45-60
Kohlmeier & Billeter
(See online at https://doi.org/10.1111/mec.16739)