Genetic architecture of brain evolution during ecological divergence

神经系统是如何产生如此多样化的动物行为的？不同的环境包含不同的信息，并提出需要量身定做的解决方案的问题。由此产生的行为适应是通过大脑功能的进化来调节的，但就像任何特征或特征一样，大脑和感官是两个过程的产物：进化和发展。这些过程如何相互作用来决定大脑在形式和功能上的变化，几十年来一直在争论，没有明确的解决方案。分析不同大脑区域的体积如何彼此相关，以及与整体大脑大小的关系，一直是这场辩论的核心。在脊椎动物中，大脑结构的特点是各组成部分之间的比例相对一致，但也有许多例子表明，一个大脑区域独立于大脑其他部分扩张或收缩，这通常被视为行为专业化或创新的标志。关于大脑如何进化的另一种假说强调以下两种模式：i)外部过程，例如相关的选择压力，可以解释为什么大脑区域的大小一起变化；或者ii)内部过程，比如大脑区域之间的发育联系，可以通过追踪大脑区域大小的变化来解释共同来源，从而解释大脑结构的一般保守(所谓的协同进化)。尽管这些假设并不是相互排斥的，但对于它们的相对重要性，或者这种重要性如何在环境或生态环境中变化，几乎没有达成一致。最近，为了解决这场争论，越来越多的注意力落在了这些假设对支撑大脑进化的基因的数量和影响的预测上。马赛克和一致的假设做出了截然相反的预测。马赛克脑进化需要在不同大脑结构中形成变异的基因之间有更大程度的独立性，而协调的脑进化预测，大脑区域体积的大部分变异将由控制大脑整体大小发育的基因来解释。到目前为止，只有少数几项研究验证了这些预测，但这项工作的重要性被大脑进化的理论模型所强调，该模型揭示了现存物种之间的体积差异模式对于推断什么发育机制塑造大脑结构可能没有任何信息。在这里，我们旨在揭示促进生态差异的慈鱼之间大脑进化的遗传变异的本质，以测试大脑组成部分之间遗传关联的程度、性质和保守性。我们的系统是独一无二的，因为它包含了三对彼此越来越不同的谱系，使我们能够比较参与大脑进化的基因如何随着时间的推移而变化。这与现有的基因组数据一起，将使我们能够研究控制大脑进化的基因的进化和系统发育历史。同时，我们将确定大脑结构轨迹分裂的关键发育时期，为证实与大脑进化有关的基因的因果效应提供基础，并研究一种结构的发育变化如何影响另一种结构。在这笔赠款结束时，我们将发现丰富的信息，关于大脑区域如何自由地独立进化，大脑发育如何灵活地促进这种适应，以及改变大脑发育的基因变化的种类。这些信息对于解释为什么大脑结构在物种之间通常是保守的，当它不是这样的时候意味着什么，以及大脑的适应性重组在使物种能够利用新的生态机会方面所起的作用是至关重要的。

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.