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

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.

On the role of body size, brain size, and eye size in visual acuity.

ABSTRACT: The visual system is highly variable across species, and such variability is a key factor influencing animal behavior. Variation in the visual system, for instance, can influence the outcome of learning tasks when visual stimuli are used. We illustrate this issue in guppies (Poecilia reticulata) artificially selected for large and small relative brain size with pronounced behavioral differences in learning experiments and mate choice tests. We performed a study of the visual system by quantifying eye size and optomotor response of large-brained and small-brained guppies. This represents the first experimental test of the link between brain size evolution and visual acuity. We found that female guppies have larger eyes than male guppies, both in absolute terms and in relation to their body size. Likewise, individuals selected for larger brains had slightly larger eyes but not better visual acuity than small-brained guppies. However, body size was positively associated with visual acuity. We discuss our findings in relation to previous macroevolutionary studies on the evolution of brain morphology, eye morphology, visual acuity, and ecological variables, while stressing the importance of accounting for sensory abilities in behavioral studies. SIGNIFICANCE STATEMENT: Pre-existing perceptual biases can be keys for the development of specific behavioral patterns. Hence, potential differences in sensory systems need to be taken into account in the study of animal behavior. We highlight this necessity concentrating on the visual domain and using experimental data on brain size-selected guppies in which we assessed eye size and visual acuity. Behavioral differences between large-brained and small-brained guppies in learning and mate choice predominantly relied on tests using visual cues. Analyses of visual capabilities in this system are therefore necessary. Furthermore, this system offers the unprecedented opportunity to experimentally test the relationship between brain size, eye morphology, and visual capabilities. Our results show similar visual acuities between large-brained and small-brained guppies. However, the differences observed in eye area between the sexes, together with the observed positive relationship between body size and visual acuity, highlight the need to incorporate perceptive differences in the study of animal behavior.