A conserved teleost motor asymmetry requires evolutionary retention of vision

Behavioral laterality is a prominent feature in Bilateria, where a motor function is performed with a leftward or rightward preference. Underlying these lateralized or asymmetric behaviors is thought to be hemispheric specializations that improve behavioral performance. Despite the prevalence of behavioral lateralization, our understanding of the neural and molecular substrates instructing its underlying neural mechanisms are limited. Moreover, how functional lateralization is selected for or modulated throughout evolution is poorly understood. Comparative approaches are a powerful strategy for addressing fundamental biological questions at individual, population, and evolutionary scales. Yet, a major obstacle for employing comparative analysis to address laterality has been the lack of a conserved lateralized behavior in lab assessable species. Previously, we described a robust visuomotor asymmetry in larval zebrafish that is a motor element of search pattern behavior. In this study, we compare search pattern behavior and motor asymmetry across a range of lab-accessible larval teleost species. We show that motor patterns underlying search behavior are variable throughout teleost evolution while behavioral asymmetry is conserved across four phylogenetic Orders of sighted larval teleost, yet not naturally blind cavefish. Our data demonstrates that motor asymmetry in larval teleosts is a conserved and tractable lateralized behavior that can be modulated by natural selection in a vision dependent manner. Our findings reveal that motor asymmetry is a deeply conserved and tractable behavioral phenotype in larval teleosts, and one that can be shaped by natural selection. This establishes larval teleosts as a powerful system for dissecting the neural architecture and evolutionary forces that govern behavioral lateralization, bridging the gap between mechanism and adaptation行为偏侧性（Behavioral laterality）是两侧对称动物（Bilateria）的典型特征，指运动功能呈现左侧或右侧偏好。驱动此类偏侧化或不对称行为的核心机制，被认为是大脑半球功能特化（hemispheric specializations），该特化可提升行为表现的效能。尽管行为偏侧现象广泛存在，但目前学界对调控其背后神经机制的神经与分子底物的认知仍较为有限。此外，功能性偏侧化如何在演化进程中被选择或调控，目前仍缺乏深入了解。比较研究方法是在个体、种群及演化尺度上解答基础生物学问题的有力策略。然而，采用比较分析探究偏侧化现象的主要阻碍，在于实验室可研究物种中缺乏保守的偏侧化行为模型。此前本团队报道了斑马鱼幼体（larval zebrafish）中存在显著的视觉运动不对称性（visuomotor asymmetry），该不对称性属于搜索模式行为（search pattern behavior）的运动组成部分。本研究中，我们对多种实验室可培养的硬骨鱼（teleost）幼体的搜索模式行为与运动不对称性开展了比较分析。研究结果显示，搜索行为背后的运动模式在硬骨鱼演化过程中存在显著变异，但行为不对称性在四个系统发育目的有视觉硬骨鱼幼体中均保守存在，而天然盲眼的洞穴鱼（blind cavefish）则未表现出该保守特性。本研究数据表明，硬骨鱼幼体的运动不对称性是一种保守且易于研究的偏侧化行为，其可通过视觉依赖的方式受自然选择（natural selection）调控。本研究结果进一步揭示，硬骨鱼幼体的运动不对称性是一种高度保守且易于开展研究的行为表型（behavioral phenotype），且可被自然选择塑造。该研究确立了硬骨鱼幼体作为研究模型，可用于解析调控行为偏侧化的神经结构与演化动力，填补了行为机制与适应性演化之间的研究空白。