Evolution of schooling drives changes in neuroanatomy and motion characteristics across predation contexts in guppies

Alberto Corral-Lopez (), Alexander Kotrschal, Alexander Szorkovszky, Maddi Garate-Olaizola, James Herbert-Read, Wouter Bijl, Maksym Romenskyy, Hong-Li Zeng, Severine Denise Buechel, Ada Fontrodona-Eslava, Kristiaan Pelckmans, Judith E. Mank and Niclas Kolm
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Alberto Corral-Lopez: University of British Columbia
Alexander Kotrschal: Stockholm University
Alexander Szorkovszky: University of Oslo
Maddi Garate-Olaizola: Stockholm University
James Herbert-Read: University of Cambridge
Wouter Bijl: University of British Columbia
Maksym Romenskyy: Stockholm University
Hong-Li Zeng: Nanjing University of Posts and Telecommunications
Severine Denise Buechel: Stockholm University
Ada Fontrodona-Eslava: Stockholm University
Kristiaan Pelckmans: Uppsala University
Judith E. Mank: University of British Columbia
Niclas Kolm: Stockholm University

Nature Communications, 2023, vol. 14, issue 1, 1-15

Abstract: Abstract One of the most spectacular displays of social behavior is the synchronized movements that many animal groups perform to travel, forage and escape from predators. However, elucidating the neural mechanisms underlying the evolution of collective behaviors, as well as their fitness effects, remains challenging. Here, we study collective motion patterns with and without predation threat and predator inspection behavior in guppies experimentally selected for divergence in polarization, an important ecological driver of coordinated movement in fish. We find that groups from artificially selected lines remain more polarized than control groups in the presence of a threat. Neuroanatomical measurements of polarization-selected individuals indicate changes in brain regions previously suggested to be important regulators of perception, fear and attention, and motor response. Additional visual acuity and temporal resolution tests performed in polarization-selected and control individuals indicate that observed differences in predator inspection and schooling behavior should not be attributable to changes in visual perception, but rather are more likely the result of the more efficient relay of sensory input in the brain of polarization-selected fish. Our findings highlight that brain morphology may play a fundamental role in the evolution of coordinated movement and anti-predator behavior.

Date: 2023
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DOI: 10.1038/s41467-023-41635-6

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