Predation evolved through modifications to canonical aggression circuits
1 Max Planck Research Group Genetics of Behavior, Max Planck Institute for Neurobiology of Behavior u2013 caesar, Ludwig-Erhard-Allee 2, 53175, Bonn, Germany
2 Max Planck Research Group Neural Information Flow, Max Planck Institute for Neurobiology of Behavior u2013 caesar, Ludwig-Erhard-Allee 2, 53175, Bonn, Germany
3 College of Plant Protection, Northwest Agriculture and Forestry University, Yangling, Shaanxi, 712100, China.
4 Graduate School of Integrated Sciences for Life, 10 Hiroshima University, Higashi-Hiroshima, Hiroshima 739-8526, Japan
Aggression is a critical behavior influencing survival, reproduction and evolution. It varies across species and contexts and is dependent on a complex interplay of genetic, environmental and neurobiological factors making the underlying mechanisms challenging to elucidate. While aggression is ubiquitous, few molecular mechanisms have been reported and aggression has not been well characterized in nematodes. Here, we explore the evolution of aggression and its association with the predatory behaviors observed in the nematode Pristionchus pacificus. We developed an automated behavioral tracking method alongside machine learning models and identified persistent and robust states specific to predatory events. These states are disrupted in mutants defective for the biogenic amines octopamine and tyramine which act antagonistically and represent the invertebrate noradrenergic-like aggression pathway. In P. pacificus, octopamine is required to establish aggressive predatory bouts while tyramine induces the non-predatory state. Mechanistically, state changes occur through the octopamine receptors Ppa-ser-3 and Ppa-ser-6 and the tyramine gated ion channel Ppa-lgc-55. Strikingly, we find that while the neurons associated with the biosynthesis of octopamine and tyramine are conserved across nematode evolution, receptor localization has diversified and IL2 head sensory neurons have acquired novel functions associated with predatory state regulation. Thus, noradrenergic-like circuits balance aggressive internal states and are adaptively associated with the evolution of predatory behavioral traits.