Neuromodulatory roles of dopamine and acetylcholine in mediating agonistic behaviors of boxer shrimps (Stenopus species)

Background Agonistic behaviors are crucial and common among animals due to their importance in securing an individual’s fitness, and neuroendocrine regulators are known to mediate the behaviors. Stenopus , a genus of shrimp-like decapod crustaceans characterized by a pair of enlarged pereiopods, exhibits prominent agonistic behaviors when encountering conspecifics of the same sex owing to its monogamous social structure. These shrimps are potentially excellent non-insect model organisms for investigating the neuroendocrine regulation of agonistic behaviors in arthropods, but the underpinning molecular basis has never been studied. Using S. hispidus and S. cyanoscelis as representatives, the present study is the first to systematically examine the genetics of agonistic behaviors of Stenopus . Three organs, including (1) antennae + antennules, (2) central nervous system, and (3) eyestalks, were RNA-sequenced to find out the differentially expressed genes (DEGs) and pathways conserved in winners and losers of Stenopus after fighting interactions. Results Our results demonstrated that Stenopus agonistic interactions likely involved the simultaneous modulation and interplay of multiple signaling cascades, organismal systems, and metabolic pathways. DEGs in both winners and losers typically enriched for gene ontologies involved in neuroendocrine signaling, and sensory and behavioral processes. Regarding enriched pathways, while those related to glycan biosynthesis and metabolism were enriched in winners, cholesterol metabolism and one-carbon pool by folate were enriched in losers. These different sets of pathways suggested that while fighting interactions in Stenopus were injurious to both combatants, the damage in losers appeared to be more traumatic. Four neuroendocrine regulators, including dopamine, acetylcholine, octopamine, and glutamate were identified as the major ones in modulating agonistic behaviors and fighting interactions in both Stenopus species, with the first two believed to play relatively more important roles. A comparison of the neuroendocrine regulators involved in mediating aggression among pan-crustaceans showed that Stenopus shrimps appeared to stand out by its seemingly major reliance on dopamine and acetylcholine, as opposed to the primarily serotonin-based regulation of aggression in most examined pan-crustaceans. Conclusions This study presents a valuable opportunity for studying behavioral genetics and aggression regulation in crustaceans aside from traditional crayfish and lobster models.