Artificial selection for schooling behaviour and its effects on individual learning abilities

The evolution of collective behaviour has been proposed to have important effects on individual cognitive abilities. Yet, in what way they are related remains enigmatic. In this context, the ‘distributed cognition’ hypothesis suggests that reliance on other group members relaxes selection for individual cognitive abilities. Here, we test how cognitive processes respond to evolutionary changes in collective motion using replicate lines of guppies (Poecilia reticulata) artificially selected for the degree of schooling behaviour (group polarization) with 15% difference in schooling propensity. We assessed associative learning in females of these selection lines in a series of cognitive assays: colour associative learning, reversal-learning, social associative learning, and individual and collective spatial associative learning. We found that control females were faster than polarization selected females at fulfilling a learning criterion only in the colour associative learning assay, but they were also less likely to reach a learning criterion in the individual spatial associative learning assay. Hence, although testing several cognitive domains, we found weak support for the distributed cognition hypothesis. We propose that any cognitive implications of selection for collective behaviour lie outside of the cognitive abilities included in food-motivated associative learning for visual and spatial cues.

集体行为的演化被提出对个体认知能力具有重要影响。然而，它们之间如何关联仍是个谜。在此背景下，‘分布式认知’假说提出，依赖于其他群体成员可以缓解对个体认知能力的筛选。在本研究中，我们通过模拟金鱼（Poecilia reticulata）的群体行为演化，测试了认知过程如何响应集体运动中的进化变化。这些金鱼是经过人工选择，以学校行为（群体极化）程度为标准，群体行为倾向存在15%的差异。我们对这些选择系中的雌性进行了系列认知实验评估：颜色联想学习、逆转学习、社会联想学习以及个体和集体空间联想学习。我们发现，在颜色联想学习实验中，对照组雌性在满足学习标准方面比极化选择组雌性更快，但在个体空间联想学习实验中，她们达到学习标准的可能性也更低。因此，尽管测试了多个认知领域，我们对于分布式认知假说的支持仅限于较弱的程度。我们提出，对于集体行为的筛选可能对认知能力产生的影响，并不包含在食物动机驱动的视觉和空间线索的联想学习之中。