Genetic architecture of brain evolution during ecological divergence

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How do nervous systems produce such a diversity of animal behaviours? Distinct environments contain different information, and present problems that require tailored solutions. The resulting behavioural adaptations are mediated by the evolution of brain function, but like any trait or characteristic, brains and sensory organs are the product of two processes: evolution and development. How these processes interact to determine how brains vary in form and function has been debated for decades, with no clear resolution. Analyses of how the volumes of different brain regions vary both in relation to each other, and with overall brain size, have been central to this debate. In vertebrates, brain structure is characterised by both relative consistency in scaling between components, but also by many examples where one brain region expands or contracts independently of the rest of the brain, often viewed as a hallmark of behavioural specialisation or innovation. Alternative hypotheses about how brains evolve explain these two patterns by emphasising either i) external processes, such as correlated selection pressures, which can explain why brain regions vary in size together, and more targeted selection pressures that could produce region specific change (so-called mosaic evolution); or ii) internal processes, like developmental links among brain regions that could explain the general conservation of brain structure (so-called concerted evolution) by tracing variation in the size of brain regions to common sources. Although these hypotheses are not mutually exclusive, there is little agreement over their relative importance, or how that importance may vary across environmental or ecological contexts.Recently, to resolve this debate, increased attention has fallen on the predictions these hypotheses make about the number and effects of genes underpinning brain evolution. Mosaic and concerted hypotheses make directly opposing predictions. Mosaic brain evolution requires a greater degree of independence between the genes shaping variation in different brain structures, while concerted brain evolution predicts that the majority of variation in the volumes of brain regions will be explained by genes controlling the development of overall brain size. To date, only a handful of studies have tested these predictions, but the importance of this work has been emphasised by theoretical modelling of brain evolution that reveals how patterns of volumetric variation among extant species are potentially uninformative for inferring what developmental mechanisms shape brain structure. Here, we aim to reveal the nature of genetic variation facilitating brain evolution between ecologically divergent cichlid fishes to test the extent, nature and conservation of genetic associations among brain components. Our system is unique, in that it encapsulates three pairs of lineages that are increasingly divergent from one another, allowing us to compare how the genes involved in brain evolution vary over time. This, together with available genomic data, will enable us to investigate the evolutionary and phylogenetic history of genes governing brain evolution. At the same time, we will identify key developmental periods where trajectories of brain structure divide, providing a foundation to confirm the causative effects of genes implicated in brain evolution, and to examine how changes in the development of one structure impact another. At the end of this grant we will have uncovered rich information about how freely brain regions are to evolve independently, how flexible brain development is to facilitate this kind of adaptation, and the kinds of genetic change that alter brain development. This information is vital for interpreting why brain structure is generally conserved across species, what it means when it is not, and the role adaptive restructuring of the brain plays in enabling species to take advantage of new ecological opportunities.