Transcriptomic investigation of agonistic behaviors of boxer shrimps (Stenopus species): insights into the potential neural signaling roles of dopamine and acetylcholine.

backgroundAgonistic behaviors are crucial and common among animals due to their importance in securing an individual's fitness, and neural signaling molecules are known to mediate these 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 represent another potentially excellent model organism for investigating the neural signaling basis of agonistic behaviors in crustaceans aside from traditional models. Yet, their underpinning molecular aspects have never been studied. Using S. hispidus and S. cyanoscelis as representatives, the present study is the first that systematically examines the genetics of agonistic behaviors in Stenopus. Three organs, including (1) antennae + antennules, (2) central nervous system, and (3) eyestalk ganglia, were RNA-sequenced to identify the differentially expressed genes (DEGs) and pathways potentially conserved in winners and losers of Stenopus after fighting interactions.

resultsOur results suggested that Stenopus agonistic interactions might be systemic activities involving the simultaneous modulation and interplay of multiple signaling cascades, organismal systems, and metabolic pathways. In particular, winners and losers typically exhibited enriched gene ontologies involved in neural 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. Furthermore, four neural signaling systems, including dopamine, acetylcholine, octopamine, and glutamate, were identified as potentially major mediators of agonistic behaviors and fighting interactions in both Stenopus species, with the first two appearing to be relatively more important. A comparison of the neural signaling systems involved in mediating aggression among pan-crustaceans suggested that Stenopus appeared to stand out by its seemingly major reliance on dopamine and acetylcholine, as opposed to the primarily serotonin-based regulation of aggression observed in most examined pan-crustaceans.

conclusionsThe different metabolic responses between winners and losers in Stenopus highlight the profound, asymmetric physiological costs of social conflict at the molecular level. Furthermore, their unique reliance on dopamine and acetylcholine reveals diverse evolutionary trajectories in the neuroendocrine regulation of aggression, providing new insights into the current paradigms of invertebrate social behavior.