Comparative genomics of adaptation to nocturnal lifestyle in owls

Though the majority of birds is diurnal, nocturnality has evolved independently in parrots, kiwis, oilbirds, nightjars and owls. Owls share traits with other raptors and nocturnal birds, such as cryptic plumage patterns, reversed sexual size dimorphism and acute vision and hearing. Additionally, some traits are owl specific, such as their asymmetrical ears, dish-shaped faces, and silent flying due to their feather’s structure. The genetic basis of some of these adaptations to a nocturnal predatory lifestyle has been studied by candidate gene approaches, but rarely with genome-wide scans. Here, we used a genome-wide comparative analysis to test for selection in the early history of the Strigiformes. We estimated the substitution rates in the coding regions of twenty bird genomes, including eleven owl species of which five were newly sequenced. Then, we tested for functional overrepresentation across the genes with selection signals. In the ancestral branch of the owls, we found that positive selection has led the evolution of genes functionally related to visual perception, especially to phototransduction, and chromosome packaging. Other genes with selection signals were functionally related to acoustic perception, circadian rhythm and feathers. We discuss whether these results support previous findings and how selection could affect the early adaptative history of the Strigiformes as nocturnal birds of prey.

尽管多数鸟类为昼行性动物，但夜行性（nocturnality）在鹦鹉、几维鸟、油鸱、夜鹰与猫头鹰类中均独立演化而来。猫头鹰兼具猛禽与夜行鸟类的共同特征，例如隐蔽性羽色模式、反向性体型二态性，以及敏锐的视觉与听觉。此外，部分特征为猫头鹰所独有：不对称的耳部结构、盘状面盘，以及因羽毛结构特化而实现的静默飞行。此前已有研究通过候选基因法（candidate gene approaches）探究了部分适应夜行掠食性生活方式的遗传基础，但鲜有全基因组扫描（genome-wide scans）层面的相关研究。
本研究采用全基因组比较分析方法，对鸮形目（Strigiformes）早期演化历程中的选择信号进行检测。我们对20份鸟类基因组的编码区替换速率进行了估算，其中包含11种猫头鹰的基因组，另有5种为本次研究新测序所得。随后，我们对携带选择信号的基因开展了功能富集性检测。在猫头鹰的祖先支系中，我们发现正选择驱动了与视觉感知（尤其光转导（phototransduction）通路）及染色体包装相关基因的演化。其余携带选择信号的基因则与听觉感知、昼夜节律及羽毛发育相关。本研究最后讨论了上述结果是否支持既往研究结论，以及自然选择如何作用于鸮形目作为夜行性猛禽的早期适应性演化历程。