Winning and losing experiences differentially alter learning performance and forebrain protein expression in mangrove rivulus killifish, Kryptolebias marmoratus

Contest outcomes alter future social behavior, but whether and how a single win or loss influences non-social learning-task performance and triggers rapid forebrain molecular responses remains unclear. The self-fertilizing mangrove rivulus killifish, Kryptolebias marmoratus, offers a useful system because contest outcomes can be standardized while reducing genetic background variation. We predicted that winning and losing would produce distinct post-contest behavioral profiles rather than equivalent or opposite shifts across tasks.

We tested whether standardized winning, losing, or control experiences altered aggression, landmark-guided spatial task performance, and risk-avoidance task performance 1 h, 3 h, or 48 h after experience. In a separate experiment, we quantified whole-forebrain protein abundance 1 h after the same manipulation to identify outcome-associated molecular responses. Winners showed increased aggression and improved landmark-guided spatial task performance, whereas losers showed reduced aggression and improved risk-avoidance task performance.

Proteomic analysis identified 23 outcome-associated proteins, including candidates linked to synaptic plasticity, cytoskeletal regulation, and neural energetics. Because behavioral and proteomic measurements used independent animals, these data do not establish within-individual or causal relationships between protein abundance and behavior performance. Instead, the proteomic results identify outcome-associated candidate molecules that may contribute to experience-dependent behavioral plasticity and should be tested directly in future studies.

We thank Caitlin Curtis for assisting with scoring behavior videos. We also thank all members of the Earley laboratory, Kültz laboratory, and Li laboratory for their comments on the manuscript and their support on this project. This research was supported by Sigma Xi Scientific Research Honors Society (Grants-in-Aid: G201703158955-1084 to C.Y.L.), Animal Behavior Society Student Research Grant (C.Y.L.), Society for Integrative and Comparative Biology Fellowship of Graduate Student Travel (C.Y.L.) and College Academy for Research, Scholarship and Creative Activity (CARSCA) grant at the University of Alabama (R.L.E. and C.Y.L.).

C.Y.L is supported by the National Cancer Institute and the Office of the Director of the National Institutes of Health under Award Number U54CA272205. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Department of Biological Sciences, University of Maryland, Baltimore County, Baltimore, MD, 21250, USA Department of Neurobiology, School of Medicine, University of Maryland, Baltimore, MD, 21201, USA Department of Animal Sciences, University of California, Davis, CA, 95616, USA Department of Bioinformatics and Genomics, University of North Carolina at Charlotte, Charlotte, NC, 28223, USA Department of Biological Sciences, University of Alabama, Tuscaloosa, AL, 35487, USA The authors declare no competing interests.

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