A unique neurogenomic state emerges after aggressive confrontations in males of the fish Betta splendens.

Abstract

Territorial defense involves frequent aggressive confrontations with competitors, but little is known about how brain-transcriptomic profiles change between individuals competing for territory establishment. Our previous study elucidated that when two fish Betta splendens males interact, transcriptomes across their brains synchronize in a way that reflects a mutual assessment process between them at the gene expression level. Here we aim to evaluate how the brain-transcriptomic profiles of opponents change immediately after shifting their social status (i.e., the winner/loser has emerged) and 30min after this shift. We showed that changes in the expression of certain genes are unique to different fighting stages and the expression patterns of certain genes are transiently or persistently changed across all fighting stages. These brain transcriptomic responses are in accordance with behavioral changes across the fight. Strikingly, the specificity of the brain-transcriptomic synchronization of a pair during fighting was gradually lost after fighting ceased, leading to the emergence of a basal neurogenomic state in which the changes in gene expression were reduced to minimum and consistent across all individuals. This state shares common characteristics with the hibernation state that animals adopt to minimize their metabolic rates to save energy. Interestingly, expression changes for genes related to metabolism, autism spectrum disorder, and long-term memory still differentiated losers from winners. Together, the fighting system using male B. splendens provides a promising platform for investigating neurogenomic states of aggression in vertebrates.