Evolutionary dynamics of recent selection on cognitive abilities

Evolutionary dynamics of recent selection on cognitive abilities
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DOI:
10.1073/pnas.1918592117
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发表时间:
2020-01
期刊:
Proceedings of the National Academy of Sciences
影响因子:
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通讯作者:
Sara E. Miller;A. Legan;M. Henshaw;Katherine L. Ostevik;K. Samuk;F. M. Uy;M. J. Sheehan
Sara E. Miller;A. Legan;M. Henshaw;Katherine L. Ostevik;K. Samuk;F. M. Uy;M. J. Sheehan
中科院分区:
其他
文献类型:
--
作者:
Sara E. Miller;A. Legan;M. Henshaw;Katherine L. Ostevik;K. Samuk;F. M. Uy;M. J. Sheehan

文献摘要

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人类长期以来一直对动物认知着迷,但很少有研究涉及认知特征进化的动态。认知进化是否涉及对新突变的强选择或对先前存在的遗传变异的选择?选择性事件是同时发生的还是多个独立的回合?我们研究了种群基因组特征的认知适应在Polistes fuscatus纸黄蜂,最近已经发展出个人的面部识别。我们发现了与学习、记忆、大脑发育和视觉处理相关的基因的多重硬选择性扫描的证据。可以说,认知选择是物种近代史上最强的选择压力之一。这些数据提供了对新认知特征进化过程的深入了解。不同物种的认知能力差异很大。社会和生态挑战在塑造认知进化方面的相对重要性一直是长期争论和最近重新争论的主题,但很少有工作试图了解认知能力进化背后的选择性动态。在这里,我们调查最近的选择有关的纸黄蜂Polistes fuscatus的认知,黄蜂,具有独特的进化视觉个人识别能力。我们产生高质量的从头基因组组件和人口基因组资源的多个物种的纸黄蜂,并使用人口基因组框架来询问可能的模式和克里思的认知进化。最近,在P. fuscatus强,硬选择性扫描包含基因座注释功能的长期记忆的形成,蘑菇体的发展,和视觉处理,最近演变的特征与个人识别。在缺乏个体识别的密切相关的黄蜂中,同源途径不受选择。事实上,在最强的选择性扫描中候选认知位点的流行表明,认知能力的进化在P.fuscatus最近的进化史中是最强的选择压力之一。对包含候选认知基因座的选择性扫描的详细分析揭示了过去几千年来对从头突变进行硬选择性扫描的多个案例,主要发生在非编码区。这些数据为认知进化的某些过程提供了前所未有的洞察力。
Significance Humans have long been fascinated by animal cognition, but little research has addressed the dynamics of the evolution of cognitive traits. Does cognitive evolution involve strong selection on novel mutations or selection on preexisting genetic variation? Do selective events happen in concert or in multiple independent bouts? We examined population genomic signatures of cognitive adaptation in Polistes fuscatus paper wasps, which have recently evolved individual facial recognition. We find evidence for multiple hard selective sweeps of novel mutations associated with genes involved in learning, memory, brain development, and visual processing. Arguably, selection on cognition has been among the strongest selective pressures in the species’ recent history. These data provide insight into the evolutionary processes by which new cognitive traits evolve. Cognitive abilities can vary dramatically among species. The relative importance of social and ecological challenges in shaping cognitive evolution has been the subject of a long-running and recently renewed debate, but little work has sought to understand the selective dynamics underlying the evolution of cognitive abilities. Here, we investigate recent selection related to cognition in the paper wasp Polistes fuscatus—a wasp that has uniquely evolved visual individual recognition abilities. We generate high quality de novo genome assemblies and population genomic resources for multiple species of paper wasps and use a population genomic framework to interrogate the probable mode and tempo of cognitive evolution. Recent, strong, hard selective sweeps in P. fuscatus contain loci annotated with functions in long-term memory formation, mushroom body development, and visual processing, traits which have recently evolved in association with individual recognition. The homologous pathways are not under selection in closely related wasps that lack individual recognition. Indeed, the prevalence of candidate cognition loci within the strongest selective sweeps suggests that the evolution of cognitive abilities has been among the strongest selection pressures in P. fuscatus’ recent evolutionary history. Detailed analyses of selective sweeps containing candidate cognition loci reveal multiple cases of hard selective sweeps within the last few thousand years on de novo mutations, mainly in noncoding regions. These data provide unprecedented insight into some of the processes by which cognition evolves.