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

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.

Relative telencephalon size does not affect collective motion in the guppy (Poecilia reticulata)

“…We interpret these results such that divergence should be substantial enough to demonstrate differences in collective motion should they have existed. This further corroborates the hypothesis that collective motion is generated by basic cognitive functions, such as perception and attention ( Corral-López et al 2023 ). Whereas changes in telencephalon size change the processing of cognitive functions such as learning, memory, and decision-making ( Triki et al 2022 , 2023 ).…”

“…Microcomputed tomography on the polarization guppy selection lines revealed an enlargement of the thalamus and of the optic tectum but a reduction in the size of the medulla oblongata. No discernible differences were observed in 8 additional brain regions, including the telencephalon, compared to the control lines ( Corral-López et al 2023 ). This suggests that telencephalon size does not influence collective motion in female guppies, and our results support this finding.…”

“…We conclude that other brain regions may be more essential components of the neural circuity involved in the evolution of collective motion in fish. These could include the thalamus and optic tectum that regulates perception, attention, and motor responses, as recently proposed by Corral-Lôpez et al (2023) . Lesion studies have been highly important to reveal specific functions of distinct brain regions (e.g.…”

“…The Trinidadian guppy ( Poecilia reticulata ) is a commonly used evolutionary model system to test hypotheses on various aspects of brain evolution and collective motion (e.g. Herbert-Read et al 2015 , 2017 ; Kotrschal et al 2018 , 2020 ; Sumpter et al 2018 ; Corral-López et al 2023 ). In this study, we use guppies artificially selected for small and large relative telencephalon size to answer the question: how do independent changes in relative telencephalon size affect collective motion?…”

Brain anatomy of a clonal fish, the Amazon molly (Poecilia formosa): Effects of early-life environment

“…As a result, abiotic factors such as environmental enrichment may require more investment in the telencephalon as foraging and sheltering becomes more varied and conditional, whereas biotic factors such as social presence drive this region to develop more intricate social cognitive skills (Gonda et al, 2009). The optic tectum is relevant for perception and subsequently behavioural predator avoidance (Huber et al, 1997;Kotrschal et al, 2017, Corral-Lopez et al 2023). Both skills would require more investment as the environment becomes more complex, but predator avoidance may decrease as social presence increases, because vigilance may be distributed across multiple individuals.…”