Despite the common assumption that the brain is malleable to surrounding conditions mainly during ontogeny, plastic neural changes can occur also in adulthood. One of the driving forces responsible for alterations in brain morphology is increasing environmental complexity that may demand enhanced cognitive abilities (e.g. attention, memory and learning). However, studies looking at the relationship between brain morphology and learning are scarce. Here, we tested the effects of both learning and environmental enrichment on neural plasticity in guppies (Poecilia reticulata), by means of either a reversal-learning test or a spatial-learning test. Given considerable evidence supporting environmentally induced plastic alterations, two separate control groups that were not subjected to any cognitive test were included to account for potential changes induced by the experimental setup alone. We did not find any effect of learning on any of our brain measurements. However, we found strong evidence for an environmental effect, where fish given access to the spatial-learning environment had larger relative brain size and optic tectum size in relation to those exposed to the reversal-learning environment. Our results demonstrate the plasticity of the adult brain to respond adaptively mainly to environmental conditions, providing support for the environmental enhancement theory.

The vertebrate brain displays enormous morphological variation and the quest to understand the evolutionary causes and consequences of this variation has spurred much research. The mosaic brain evolution hypothesis, stating that brain regions can evolve relatively independently, is an important idea in this research field. Here we provide experimental support for this hypothesis through an artificial selection experiment in the guppy (Poecilia reticulata). After four generations of selection on relative telencephalon volume (relative to brain size) in replicated up-selected, down-selected and control-lines, we found substantial changes in telencephalon size, but no changes in other regions. Comparisons revealed that up-selected lines had larger telencephalon while down-selected lines had smaller telencephalon than wild Trinidadian populations. No cost of increasing telencephalon size was detected in offspring production. Our results support that independent evolutionary changes in specific brain regions through mosaic brain evolution can be important facilitators of cognitive evolution.

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Mosaic brain evolution, the change in the size of separate brain regions in response to selection on cognitive performance, is an important idea in the field of cognitive evolution. However, untill now, most of the data on how separate brain regions respond to selection and their cognitive consequences stem from comparative studies. To experimentally investigate the influence of mosaic brain evolution on cognitive ability, we used male guppies artificially selected for large and small telencephalons relative to the rest of the brain. Here, we tested an important aspect of executive cognitive ability using a detour task. We found that males with larger telencephalons outperformed males with smaller telencephalons. Fish with larger telencephalons showed faster improvement in performance during detour training and were more successful in reaching the food reward without touching the transparent barrier (i.e., through correct detouring) during the test phase. Together, our findings provide the first experimental evidence showing that evolutionary enlargement of relative telencephalon size confers cognitive benefits, supporting an important role for mosaic brain evolution during cognitive evolution.

Experimental evidence shows that mosaic evolution can drive brain morphology variation and potentially cognitive evolution.