Heatwaves negatively impact behaviour with associated cognitive impairment in humans. A growing body of literature also reports negative effects of heatwaves on cognition in other animals. A larger brain is known to generate enhanced cognitive abilities that may buffer against environmental changes and thereby potentially increase fitness in large-brained individuals. How a larger brain buffers against adverse effects on cognitive abilities induced by thermal stress, such as that experienced during heatwaves, remains unknown. We examined detour problem solving and working memory during an experimental heatwave in guppies artificially selected on brain size with matching differences in neuron number. Overall, detour problem-solving was impaired among guppies during the heatwave, while working memory was unaffected. Large-brained guppies outperformed small-brained guppies in detour problem-solving and working memory in both the heatwave and control temperature treatments. During the heatwave, large-brained guppies exhibited cognitive performance levels comparable to those of small-brained guppies under normal temperature conditions in the detour task. Our study thus suggests that small-brained individuals might have lower fitness also during heatwaves if increased temperature impair cognitive abilities required for survival and reproduction. Furthermore, our results open up the possibility that cognition-driven brain size evolution may have been influenced by abiotic factors.

Avoiding predation is essential for most animals. For group-living species, effective predator avoidance relies on making fast and accurate collective decisions. However, the mechanisms underlying the ability to make adaptive collective decisions and to coordinate movements under predation threat remains unclear. Here, we used guppies artificially selected for divergence in the size of the telencephalon, the main brain region for advanced decision-making in vertebrates, to test the influence of telencephalon size on collective decision-making under predation threat. We measured the latency and accuracy of collective decision-making to avoid a model predator in guppy shoals. In addition, we used high-resolution tracking analysis to assess shoaling dynamics under predator threat between the telencephalon size selection lines. We found that collective decision-making latency was shorter in large telencephalon guppy shoals, indicating that variation in telencephalon size can cause variation in the ability to avoid predation. This result is unlikely to be driven by differences in boldness, as several standard tests suggest that there is no difference in boldness between the telencephalon size selection lines. General aspects of shoaling dynamics did not differ between the telencephalon size selected lines. Our study highlights that rapid mosaic changes in brain region size may be an important mechanism behind social behavioural variation with strong fitness implications.

Animals can employ various spatial learning strategies to navigate through their environment, and the proficiency in specific strategies varies greatly both intraspecifically and interspecifically. Currently, the neural basis of this variation is poorly understood. Here, we tested whether variation in performance in egocentric and allocentric spatial learning strategies is related to differential investment in distinct brain regions. To do so, we used guppies (Poecilia reticulata) from artificial selection lines expressing differences in relative telencephalon size, and tested their ability to learn a spatial task, based on either egocentric (left–right) or allocentric (environmental) cues. Surprisingly, fish with larger telencephalons showed enhanced performance in both tasks, regardless of cue type, suggesting a more complicated role of the fish telencephalon in spatial learning than previously thought. Our study provides the first direct evidence that evolutionary changes in relative telencephalon size lead to corresponding shifts in spatial cognition at the within-species level. Furthermore, our results offer critical and novel insights regarding the function of the telencephalon and its role in the evolution of spatial cognition.

Domestication is a well-known example of the relaxation of environmentally based cognitive selection that leads to reductions in brain size. However, little is known about how brain size evolves after domestication and whether subsequent directional/artificial selection can compensate for domestication effects. The first animal to be domesticated was the dog, and recent directional breeding generated the extensive phenotypic variation among breeds we observe today. Here we use a novel endocranial dataset based on high-resolution CT scans to estimate brain size in 159 dog breeds and analyze how relative brain size varies across breeds in relation to functional selection, longevity, and litter size. In our analyses, we controlled for potential confounding factors such as common descent, gene flow, body size, and skull shape. We found that dogs have consistently smaller relative brain size than wolves supporting the domestication effect, but breeds that are more distantly related to wolves have relatively larger brains than breeds that are more closely related to wolves. Neither functional category, skull shape, longevity, nor litter size was associated with relative brain size, which implies that selection for performing specific tasks, morphology, and life history does not necessarily influence brain size evolution in domesticated species. 

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.