Consistent Individual Differences Drive Collective Behavior and Group Functioning of Schooling Fish

Consistent Individual Differences Drive Collective Behavior and Group Functioning of Schooling Fish
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DOI:
10.1016/j.cub.2017.08.004
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发表时间:
2017-09-25
期刊:
影响因子:
9.2
通讯作者:
Manica, Andrea
Manica, Andrea
中科院分区:
生物学1区
文献类型:
--
作者:
Jolles, Jolle W.;Boogert, Neeltje J.;Manica, Andrea

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一致的个体间行为差异的普遍存在(“动物个性”)[1,2]表明,它们可能在推动动物群体的运动和功能方面发挥重要作用[3,4],包括它们的集体决策、觅食行为和躲避捕食者。尽管越来越多的证据突显了它们的重要性[5-16],但我们仍然缺乏一个统一的机制框架来解释和预测一致的个人差异如何驱动集体行为。在这里,我们通过对自由游泳的刺鱼(Gasterbone Aculeatus)浅滩的已知行为类型进行高分辨率跟踪,研究群体的结构、领导力、运动动力学和觅食能力如何从个体间的差异中显现出来。我们发现,通过经典的“社交能力”测试,个体与他人呆在一起的倾向与一系列环境中的游泳速度呈负相关,并预测了群体内的空间位置和领导力,以及群体之间结构和运动动力学的差异。反过来,这一特征与个人的探索倾向一起,通过经典的“大胆”分析来衡量,解释了个人和群体的觅食表现。这些一致的个体差异对群体水平状态的影响自然而然地出现在一个由不同速度和目标导向的个体组成的自组织群体的通用模型中。我们的研究为一种简单的机制提供了实验和理论证据,该机制可以解释集体行为从一致的个体差异中出现的原因,包括跨社会和生态尺度的群体结构、领导力、运动动力学和功能能力的差异。此外,我们还论证了个体表现取决于群体构成,表明社会选择如何驱动个体之间的行为差异。
The ubiquity of consistent inter-individual differences in behavior ("animal personalities'') [1, 2] suggests that they might play a fundamental role in driving the movements and functioning of animal groups [3, 4], including their collective decision-making, foraging performance, and predator avoidance. Despite increasing evidence that highlights their importance [5-16], we still lack a unified mechanistic framework to explain and to predict how consistent inter-individual differences may drive collective behavior. Here we investigate how the structure, leadership, movement dynamics, and foraging performance of groups can emerge from inter-individual differences by high-resolution tracking of known behavioral types in free-swimming stickleback (Gasterosteus aculeatus) shoals. We show that individual's propensity to stay near others, measured by a classic "sociability'' assay, was negatively linked to swim speed across a range of contexts, and predicted spatial positioning and leadership within groups as well as differences in structure and movement dynamics between groups. In turn, this trait, together with individual's exploratory tendency, measured by a classic "boldness'' assay, explained individual and group foraging performance. These effects of consistent individual differences on group-level states emerged naturally from a generic model of self-organizing groups composed of individuals differing in speed and goal-orientedness. Our study provides experimental and theoretical evidence for a simple mechanism to explain the emergence of collective behavior from consistent individual differences, including variation in the structure, leadership, movement dynamics, and functional capabilities of groups, across social and ecological scales. In addition, we demonstrate individual performance is conditional on group composition, indicating how social selection may drive behavioral differentiation between individuals.