Brain morphology and behaviour in the guppy (Poecilia reticulata) : Effects of plasticity and mosaic brain evolution

Abstract: Understanding how brains have evolved and subsequently culminated in the huge variation in brain morphology among contemporary vertebrate species has fascinated researchers for many decades. It has been recognized that brain morphology is both genetically and environmentally determined. Adaptations to ecological challenges, for one, has been proposed to be a major force in brain diversification processes. Considering the large energetic costs of neural tissue, it is believed that brain evolution is a highly complex process, involving a delicate balance between the corresponding costs and benefits. Using the guppy (Poecilia reticulata) as the model organism, I first examined the conditions under which diversity in brain morphology is generated. This was done by investigating factors known to exert an influence on brain plasticity, namely environmental and cognitive effects (Paper I). Existing studies generally indicate that the provision of environmental enrichment lead to the enlargement of specific brain structures. While plastic alterations in brain morphology was found to respond to environmental complexity in my study, successful performance in two cognitive tasks did not produce any significant changes. I next assessed the feasibility of the mosaic brain evolution hypothesis by artificially selecting for an increase and decrease in the relative size of the telencephalon (Paper II). Telencephalon size was shown to respond rapidly to divergent selection pressures, with no substantial changes in any of the other brain regions. A comparison with wild fish revealed that fish from the unselected control treatment had telencephalon sizes most similar to that of wild populations, whereas both up-selected and down-selected fish had considerably larger and smaller telencephalon, respectively. I tested fish from the artificial selection lines in a test battery to determine if known differences in telencephalon size affects boldness (Paper III). Individuals were subjected to an emergence test, an open field test and a novel object test. I found no differences in boldness levels across selection treatments, but distinct sex differences were noted whereby males were more active and bolder. The cognitive benefits associated with a larger telencephalon were examined in males in a test of self-control (Paper IV). Guppies from the up-selected lines attained a steeper learning curve and made more correct detours compared to their down-selected conspecifics. In conclusion, I provide experimental evidence for the mosaic brain evolution hypothesis by showing that a specific brain region (telencephalon) can evolve rapidly and independently under directed selection. Future tests on other cognitive benefits as well as implicated costs, together with underlying neuronal changes would help to further unravel the factors governing brain evolution.