Tsai Fu-Yu, Lin Che-Yi, Su Yi-Hsien, Yu Jr-Kai, Kuo Dian-Han
Department of Life Science, National Taiwan University, Taipei, Taiwan.
Institute of Cellular and Organismic Biology, Academia Sinica, Taipei, Taiwan.
Mol Biol Evol. 2025 Apr 1;42(4). doi: 10.1093/molbev/msaf072.
Human and fly FoxP homologs are well-known for their roles in the development of cognitive abilities. These findings have led to the hypothesis that the ancestral function of FoxP was in the development of cognitive neural circuits. However, complex brains in human and fly evolved independently, and the similar cognitive function of FoxP in human and fly may thus be interpreted as a result of convergent evolution. In addition, the 4 gnathostome FoxP paralogs also possess diverse developmental functions unrelated to neurodevelopment, which might have been overlooked in comparative studies of invertebrate FoxP homologs. To resolve these uncertainties, we set out to improve the phylogenetic reconstruction of vertebrate FoxP homologs and broaden the taxonomic sampling of gene expression profiling to include an invertebrate chordate, ambulacrarian deuterostomes, and a spiralian protostome. Using phylogenetic analysis combined with synteny mapping, we elaborated the hypothesis that the 4 FoxP paralogs arose through the 2R-WGD events shared by all gnathostome species. Based on this evolutionary scenario, we examined the FoxP expression pattern in amphioxus development and concluded that FoxP already had complex developmental functions across all germ layers in the chordate ancestor. Moreover, in sea urchin, hemichordate, and catenulid flatworm, FoxP was expressed in the gut prominently, in addition to the anterior neurogenic ectoderm. This surprising similarity shared among these distantly related species implies that FoxP may have a significant function in gut development in addition to the neural development function in the last common ancestor of bilaterians.
人类和果蝇的FoxP同源物因其在认知能力发展中的作用而广为人知。这些发现引发了一种假说，即FoxP的原始功能是在认知神经回路的发育中。然而，人类和果蝇的复杂大脑是独立进化的，因此FoxP在人类和果蝇中相似的认知功能可能被解释为趋同进化的结果。此外，4种颌口动物的FoxP旁系同源物还具有与神经发育无关的多种发育功能，这在无脊椎动物FoxP同源物的比较研究中可能被忽视了。为了解决这些不确定性，我们着手改进脊椎动物FoxP同源物的系统发育重建，并扩大基因表达谱的分类取样范围，纳入一种无脊椎脊索动物、步带类后口动物和一种螺旋类原口动物。通过系统发育分析结合共线性图谱，我们阐述了这样一种假说，即4种FoxP旁系同源物是通过所有颌口动物物种共有的2R-WGD事件产生的。基于这一进化情景，我们研究了文昌鱼发育过程中的FoxP表达模式，并得出结论，FoxP在脊索动物祖先的所有胚层中已经具有复杂的发育功能。此外，在海胆、半索动物和链状扁形虫中，FoxP除了在前神经外胚层表达外，在肠道中也有显著表达。这些远缘物种之间惊人的相似性意味着，除了两侧对称动物的最后一个共同祖先中的神经发育功能外，FoxP在肠道发育中可能也具有重要功能。
