Behavioral and brain- transcriptomic synchronization between the two opponents of a fighting pair of the fish Betta splendens
Autor: | Hao Ven Wang, Kenshiro Oshima, Y. W. Lin, Takashi Gojobori, H. Sunny Sun, Akiko Maruko, Satoshi Tamaki, Wen-Hsiung Li, Chih-Kuan Chen, Shun Fen Tzeng, Takashi Abe, Mei Yeh Lu, Erica Iioka, Yuki Iwasaki, Masaru Hojo, Shuji Shigenobu, Chao Li Huang, Hao Jen Huang, Norihiro Okada, Tzen Yuh Chiang, Akio Kanai, Trieu Duc Vu |
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Jazyk: | angličtina |
Rok vydání: | 2020 |
Předmět: |
Male
Cell signaling Cancer Research Video Recording Gene Expression Social Sciences Signal transduction QH426-470 Transcriptome Sequencing techniques Learning and Memory 0302 clinical medicine Synchronization (computer science) Psychology RNA-Seq Cooperative Behavior Mating Zebrafish Genetics (clinical) 0303 health sciences Behavior Animal Animal Behavior Fishes Brain Eukaryota Signaling cascades RNA sequencing Genomics Animal Models Aggression Experimental Organism Systems Osteichthyes Vertebrates Fish medicine.symptom Betta splendens Behavior Observation Techniques Transcriptome Analysis Research Article Cell biology MAPK signaling cascades Fish Biology Biology 03 medical and health sciences Model Organisms Memory Fish Physiology medicine Genetics Animals Learning Animal Physiology Interpersonal Relations Molecular Biology Ecology Evolution Behavior and Systematics 030304 developmental biology Behavior Ion Transport Organisms Biology and Life Sciences Computational Biology Behavioral pattern Genome Analysis biology.organism_classification Vertebrate Physiology Research and analysis methods Molecular biology techniques Fish Biting Gene Expression Regulation Evolutionary biology Animal Studies Zoology 030217 neurology & neurosurgery Neuroscience |
Zdroj: | PLoS Genetics, Vol 16, Iss 6, p e1008831 (2020) PLoS Genetics |
ISSN: | 1553-7404 1553-7390 |
Popis: | Conspecific male animals fight for resources such as food and mating opportunities but typically stop fighting after assessing their relative fighting abilities to avoid serious injuries. Physiologically, how the fighting behavior is controlled remains unknown. Using the fighting fish Betta splendens, we studied behavioral and brain-transcriptomic changes during the fight between the two opponents. At the behavioral level, surface-breathing, and biting/striking occurred only during intervals between mouth-locking. Eventually, the behaviors of the two opponents became synchronized, with each pair showing a unique behavioral pattern. At the physiological level, we examined the expression patterns of 23,306 brain transcripts using RNA-sequencing data from brains of fighting pairs after a 20-min (D20) and a 60-min (D60) fight. The two opponents in each D60 fighting pair showed a strong gene expression correlation, whereas those in D20 fighting pairs showed a weak correlation. Moreover, each fighting pair in the D60 group showed pair-specific gene expression patterns in a grade of membership analysis (GoM) and were grouped as a pair in the heatmap clustering. The observed pair-specific individualization in brain-transcriptomic synchronization (PIBS) suggested that this synchronization provides a physiological basis for the behavioral synchronization. An analysis using the synchronized genes in fighting pairs of the D60 group found genes enriched for ion transport, synaptic function, and learning and memory. Brain-transcriptomic synchronization could be a general phenomenon and may provide a new cornerstone with which to investigate coordinating and sustaining social interactions between two interacting partners of vertebrates. Author summary Agonistic encounters induce changes in the brain and behavior, but their underlying molecular mechanisms remain poorly understood. The fighting fish Betta splendens are small freshwater fish that are well known for their aggressiveness and are widely used to study aggression. Here, by measuring aggressive behavior displays (bite/strike/surface-breathing) between two opponents during fighting, we demonstrate that the two opponents in each fighting pair showed similar fighting configurations by influencing each other. In addition, we compared brain gene expression between opponents and showed synchronization of gene expression within a fighting pair, leading to pair-specific synchronization in genes associated with ion transport, synapse function, and learning and memory. This study presents the possibility that similar behaviors in pairs of animals under similar conditions may trigger synchronizing waves of transcription between the individuals, providing a hint to support the idea that fighting behaviors contain cooperative aspects at the molecular level. |
Databáze: | OpenAIRE |
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