Genetic architecture of brain evolution during ecological divergence

神经系统是如何产生如此多样的动物行为的？不同的环境包含不同的信息，并提出需要定制解决方案的问题。由此产生的行为适应是由大脑功能的进化介导的，但就像任何性状或特征一样，大脑和感觉器官是两个过程的产物：进化和发展。这些过程如何相互作用，以确定大脑在形式和功能上如何变化，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在彼此之间以及与整体大脑大小之间变化，一直是这场辩论的核心。在脊椎动物中，大脑结构的特点是组件之间的比例相对一致，但也有许多例子，其中一个大脑区域独立于大脑的其他部分扩展或收缩，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其他假说通过强调外部过程来解释这两种模式，例如相关的选择压力，这可以解释为什么大脑区域的大小在一起变化，以及更有针对性的选择压力，可以产生区域特异性变化（所谓的马赛克进化）;或ii）内部过程，比如大脑区域之间的发育联系，可以解释大脑结构的一般保守性，（所谓的协同进化）通过追踪大脑区域大小的变化到共同的来源。虽然这些假说并不相互排斥，但对于它们的相对重要性，以及这种重要性如何在环境或生态背景下变化，人们几乎没有达成共识。最近，为了解决这一争论，越来越多的注意力落在这些假说对支撑大脑进化的基因数量和影响的预测上。马赛克假说和协调假说做出了直接相反的预测。镶嵌式大脑进化要求不同大脑结构中形成变异的基因之间具有更大程度的独立性，而协调式大脑进化则预测，大脑区域体积的大部分变异将由控制整个大脑大小发育的基因来解释。到目前为止，只有少数研究已经测试了这些预测，但这项工作的重要性已经通过大脑进化的理论建模得到了强调，该模型揭示了现存物种之间的体积变化模式对于推断什么样的发育机制塑造大脑结构可能是没有信息的。在这里，我们的目标是揭示自然的遗传变异，促进大脑进化之间的生态分歧慈鲷鱼测试的程度，性质和保护的大脑组件之间的遗传协会。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时间变化。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史。与此同时，我们将确定大脑结构轨迹划分的关键发育时期，为确认与大脑进化有关的基因的因果作用提供基础，并研究一种结构的发展变化如何影响另一种结构。在这项资助的最后，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遗传变化。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，当它不是时意味着什么，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至关重要。

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.